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Li G, Meng F, Zhong X, Yu K, Zhang N, Zhang K, Huang H, Li W, Zhang J, Wang W, Ren Y, Liu Y. DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions. Scientific reports 2025 15(1) 40596516
Abstract:
O-linked β-N-acetylglucosamine (O-GlcNAc), a critical post-translational modification predominantly found in the nucleus, plays a substantial role in regulating gene expression by modulating transcription factors (TFs) activity. However, quantitative analysis investigating the influence of O-GlcNAcylation on protein-DNA interactions at a proteome scale remains undone. Herein, a pulldown screening approach using a consensus TF response element (catTFRE) was employed to unravel the impact of fluctuating levels of O-GlcNAcylation on the DNA binding efficiency of endogenous TFs/co-factors. Utilizing quantitative proteomics, we identified a substantial enhancement in the binding capacity of 241 nuclear proteins (NPs) to DNA sequences due to elevated levels of O-GlcNAcylation, whereas a decrease in DNA binding was observed for 2 NPs concurrently. Intriguingly, the O-GlcNAcylation elevation significantly enhanced the binding of 146 TFs/co-factors to specific DNA sequences. We further established that the O-GlcNAcylation of several Forkhead family TFs, including FOXA1 and FOXC1, notably enhances their binding to specific DNA sequences in living cells. Our research presents an efficacious approach to assessing the impact of O-GlcNAcylation on the interactions between proteins and DNA. This significantly enhances our understanding of the role O-GlcNAcylation plays in the regulation of transcription.
O-GlcNAc proteins:
RBM47, ESYT2, HACL2, VWA8, CNOT1, PGP, SMHD1, U119B, MET15, MYO1G, ADAS, PDLI1, BACH, HAX1, SPT5H, TAF4, CLIC1, BMAL1, SAP18, DNM1L, PLOD2, PSDE, BIN1, NOP56, DDX3X, TRI38, NFIB, PPP6, CDKA1, ABLM1, ADA10, CHK1, PSA7, TX1B3, TIM23, MYPT1, S27A2, XPO1, SYN3, ZN609, SR140, SET1A, ZN185, ATX7, OGT1, EIF3D, EIF3H, TNC18, MOT4, P4HA2, NUP42, ARPC5, CLOCK, MAFG, KDM6A, DHX15, RRP8, PRP4, SERA, PHF1, DC1L2, PSMD3, SNUT1, MCA3, HNRPR, PRPF3, TPD54, EMC8, MGA, KLF4, TIM44, PLRG1, ZN207, BUB3, ACTN4, BUD23, ENSA, SPOP, LANC1, AKAP8, CALU, ORC5, ZNRD2, MED14, NPA1P, ZC3H1, AQR, GANP, KDM1A, ACSL4, VINEX, CCNT1, PLOD3, TSN3, PLIN3, MAFK, UGDH, PQBP1, TBL1X, NBN, MITF, CPNE3, ZC11A, ANR17, H2AY, FLNB, NCOR1, SPAG7, RM33, SC22B, PR40A, MPPB, KTNA1, PSIP1, ERLN1, NDUS3, SRS10, SF3B1, CSDE1, U520, NU155, CRTAP, S2512, EIF3G, SOAT2, CCNK, SPF27, SPF30, RL1D1, CLPX, SYUG, DFFB, SRP72, RECQ5, ATG12, TOX4, K0754, SRBS2, SUN1, ERLN2, PRP6, SC31A, UBR5, AGFG2, SCAF4, DUS14, SPN1, NDUB8, RTN3, EPN2, LC7L3, MBD4, VAPB, 6PGL, ZBT7A, IPO7, SLU7, CD2B2, PSMG1, SC24B, ZBT11, SNP29, OXSR1, HS74L, LSM8, AP2A1, WIZ, BAG2, AIFM1, BPNT1, SNAI1, DDAH2, TXD12, MBD3, TOM40, NAPSA, ACL6A, CCNE2, LDHA, NB5R3, PGK1, A1AT, FOS, RASH, LDLR, LMNA, ALBU, TFR1, TRFL, FRIH, NU3M, MIS, VTNC, CATA, GBA1, FUCO, ALDOA, CYTB, GCR, SODM, KITH, K2C1, G3P, HLAA, CPNS1, HSPB1, TYSY, RPN1, RPN2, GNAI2, AT1A1, AT1B1, A4, APOD, ALDH2, PERM, PPBT, IF2A, RLA2, RLA0, JUN, ITB1, K1C18, K2C8, GELS, ATPB, IF4E, ENOA, NPM, ITAV, GDN, ACBP, LDHB, CATD, ANXA2, TBB5, SAP, CATL1, SYEP, CATB, HNRPC, FUMH, TSP1, SP1, ANXA6, HS90B, SRPRA, ODPA, RU2B, RU17, ITA5, NFIC, VIME, K2C7, GNAI3, ANXA5, SNRPA, HMGB1, DLDH, ROA1, RU2A, LKHA4, CTF8, MNS60, RO60, MYBB, LYAG, HLAC, KAP0, CH60, CLUS, BIP, HSP7C, GTR1, ODPB, LAMP1, ACADM, TOP1, TOP2A, G6PD, MPRI, PRPS2, PABP1, PCNA, ADT3, FA5, IMDH2, TPR, KCRU, SKI, ACTN1, XRCC6, NR2C1, LAMP2, EF2, K1C10, K1C13, PDIA4, PLST, T2FB, MIF, FPPS, KPYM, ENPL, MYL6B, RSMB, PO2F1, PLAK, ALDR, RAC2, ERF3A, EZRI, ATF2, FOSL2, MCP, NDKA, GNS, RS2, DESP, MUC1, CREB1, MGMT, CD36, STMN1, YBOX3, ZFX, JUNB, UBF1, JUND, ATF7, PTN2, DDX5, ARF4, PTPRA, SON, NELFE, RCC1, ATF1, ATF6A, XRCC1, LFA3, NUCL, ELK1, TFE3, CSK22, NFKB1, TYPH, TBP, RAB6A, PSB1, LMNB1, HXA5, CSRP1, FLNA, VDAC1, SDHB, CD9, PIMT, FBRL, UBA1, NDKB, ROA2, RFX1, KAPCB, QCR2, ITA6, SFPQ, PPIB, MAOM, SP100, NFYA, SAHH, COF1, IF4B, GATA2, THIL, MCM3, RS12, BRD2, TYY1, ATPA, PSA1, PSA4, ITA3, DDX6, PTBP1, SYVC, KAD4, 1433T, VATL, ARNT, RFA1, APEX1, PYR1, CALR, MAP4, CALX, PSA5, PSB4, PEX2, NDUS1, TEAD1, GRN, T2EB, 3MG, TKT, SPB3, ECHM, KCY, PEBP1, PDIA3, 2AAA, CDC27, HMOX2, PURA2, AMRP, RPB2, SDHA, METK2, HXA11, HXC9, CPSM, 3HIDH, PUR9, HNRH3, HNRH1, 1433S, STIP1, L1CAM, PRDX2, P5CR1, ELF1, CGL, RL9, CSTF2, MCM4, MCM7, HSP74, TRY3, GPC1, CTNA1, BMI1, PCGF2, PHB1, RADI, RFC4, RFC1, MYH9, MYH10, COPB2, SOAT1, ADDB, BASI, FUS, NU214, DEK, GLRX1, K22E, MP2K2, VATE1, RL4, PGM1, SPB5, ODO2, SRP14, NUP62, TAGL2, SYUA, ETFB, RBMX, VATA, HSPA9, IF4A3, TXLNA, TCPZ, PBX2, MLH1, STAT3, MDHM, ECHA, IF2G, S19A1, ELK3, ACTY, LAP2A, LAP2B, LPPRC, THIM, ECE1, MUC18, MATR3, GPDM, SSRA, RANG, PRS6B, VDAC2, MP2K4, KI67, RAGP1, RECQ1, NOP2, CRKL, NEDD4, IQGA1, STT3A, CAPZB, RL29, UCRI, RFX5, COPD, PSMD8, PRC2A, HSP13, AGRE5, DPOD2, NR2C2, RPIA, LMAN1, FAS, CDK8, RM19, AL7A1, CENPF, SYAC, SYCC, SYSC, MCM2, ACADV, YLPM1, RBM25, CLK1, NU153, RBP2, GSK3A, GSK3B, TAF6, GUAA, DNLI3, MRE11, IDH3A, EMD, CPT1A, SERPH, F10A1, MXI1, MAP2, PPT1, TCPQ, TCPD, FXR1, FXR2, RAB5C, RAB7A, SMCA4, IDH3G, GALK1, MECP2, DHB4, SPHM, HDGF, ROA3, 6PGD, IMA1, GDS1, MP2K6, AGFG1, HNRPF, TF2AA, MSH6, CAZA1, CRIP2, NUP98, PLK1, ACLY, SUCA, COPA, PTTG, SC24C, TCP4, ICLN, HIRA, SYYC, UBP14, HSP72, AT1B3, RD23A, RD23B, KAD2, SNAA, IF5, RAD, TERA, DSRAD, TPD52, SEC13, PSA, HNRH2, EIF3B, SYMC, DPOE2, ATP5I, IF6, NU107, SESN2, FOXL2, EPIPL, TPIS, SC61B, ACTB, IF4A1, PRPS1, SRP54, RAB2A, ARP2, ACTZ, CSN2, ARF3, CH10, STXB1, B2MG, WDR5, HNRPK, RS16, SMD2, ERF1, RS4X, ACTA, RL23A, RS6, H4, GBB1, RL32, RL8, PPIA, RS27A, RL40, AP2B1, 1433Z, IF5A1, RACK1, ACTG, YBOX1, TPM4, EF1A1, ACTS, TBA1B, TBA4A, TBB4B, CSK21, HBB, HBA, CXAR, NOP14, RBM6, PITX1, IF4G2, GTF2I, GSTO1, PO6F2, PRKDC, BASP1, RT22, RT05, RT11, RT34, RT09, HMGN5, SARNP, LACTB, TXN4A, RL19, FOXK1, RBM10, EM55, TFAM, VIGLN, CDK5, CLH1, HNRPU, SPTB2, TIAR, SET, FOXK2, RUNX1, CAP1, TFAP4, EXOSX, XPC, EWS, MEF2A, SP2, ODO1, KIF23, DSG1, SP3, RL18A, FKBP4, PLOD1, TOP2B, M2OM, DYST, CREM, KMT2A, CENPC, LMNB2, UPAR, KIME, TAP1, IF4G1, K1C17, SSBP, SRS11, EF1A2, CALD1, KDSR, SUH, GABPA, GABP1, PRDX1, RL18, C1QBP, CKAP4, ZO1, KHDR1, SRSF4, PP2BA, DHX9, LG3BP, MFGM, CD47, SSRP1, SLFN5, RBBP4, NCBP1, EP300, AHNK, MGAT2, GALT2, BST2, MPPA, SIA4C, NU160, TBL3, TF3C1, ASPH, SNF5, BPTF, NFIA, CHD3, TP53B, IFRD2, AIMP1, ILF3, LMAN2, FOXC1, PP1R8, ECH1, PRDM2, CSN1, KLF10, NR1H3, TADBP, ROA0, PAK2, PSMD2, DDX10, GPS2, SRSF5, SRSF6, TIF1B, G3BP1, STF1, NMI, KCAB2, SKP2, PABP4, GRB10, MTA1, DC1I2, ORC2, SNTB2, PPIG, TCOF, ADAM9, TUSC3, SMAD4, PICAL, TBB3, ASAH1, HDAC1, SNW1, STIM1, CUL4A, CUL4B, FHL1, RUNX3, THOC5, SPTN1, NOG2, KLF5, RUNX2, PEBB, NFYC, CKAP5, SCRB2, DAG1, VEZF1, DSG2, KEAP1, MORC3, SAFB2, EIF3A, UBP2L, MLEC, ZMYM3, DCTN1, DYHC1, EI2BA, ELOA1, MAP7, SRC8, FLNC, CAPR1, NF2L1, HABP2, DHX8, ITPR3, PLSI, TRIPC, PUM1, MDC1, EPN4, SMC1A, RRP1B, RRP5, BMS1, GANAB, MBTP1, 2A5D, LBR, CBX2, KIF22, MEF2D, CHD4, LASP1, ARI5B, NFIX, ZN638, NOLC1, NUMA1, GAPD1, SPCS2, EMC2, MO4L2, ABRX2, CND1, SUZ12, U5S1, SYK, RRS1, IF4H, BRD3, WDR43, ACOX1, EBP, PLEC, PON2, NONO, PTPA, PWP2, RNPS1, RCN1, PCBP1, MTFR1, SF3B3, PUM3, DLGP5, KS6A1, SF3A2, SC23A, SF3A1, SURF1, MED22, TAF5, TAF7, MARE2, TSN, SF01, PCH2, MED1, JHD2C, TRIP6, MARE1, ELF2, NAB2, AAAT, USF2, VAS1, RB11B, EZH2, ZYX, SEPT7, ADRM1, TAF12, DDB1, SNPC1, CDC37, DPYL2, SYPL1, TAF9, SRSF7, DREB, NRF1, PCKGM, DDR2, LY6K, HNRL2, PDS5A, ZN800, P3H1, RA1L2, MA7D1, TBRG1, LARP7, ACSF3, TPRN, EPC2, DHB12, UBP39, SETMR, YIF1B, ZN326, NOM1, SH319, RRP12, TOIP1, TDIF2, NU188, HP1B3, ZN362, SYRM, ZC3HD, LRIF1, RM02, UBAP2, RBM26, RIF1, MRCKA, RPRD2, BRE1A, TASO2, KHDR2, AR6P4, ARID2, GL8D1, NR3L1, MSL1, ABLM2, GLYAT, TWF2, K0930, SN12L, SDE2, LIN54, ALKB2, PPR18, CAVN1, CDC73, PRP8, SCYL2, GOLM2, RHGBA, NFRKB, RSBNL, KCD18, NCEH1, MDEAS, ZC3HE, SAMD1, C1TM, FIP1, CSPG4, PLGT2, SBSN, CF089, LCN15, CREL2, LRIG3, BCOR, MPRIP, CD109, SRCAP, UBN2, IKIP, CENPU, LARP4, HAKAI, NOL8, ASXL2, SND1, DDX46, TM10C, EIF3M, MCM10, NDUF7, CXXC5, APTX, ZCCHV, KANL1, NUP54, POGZ, NUFP2, SZRD1, CLAP1, HEAT3, HDGR2, BRAP, EMSY, I2BP2, RBBP6, YTHD3, TAF8, TMED4, CENPV, PHLB2, MYPN, ACOT1, PABP2, LDB1, PB1, YRDC, LYRIC, KTN1, LUZP1, CAND1, THOC6, DDX42, SPAS2, CACL1, P66A, RIOX2, CRLF3, VRK3, NAV2, CCD50, MISP, CTL2, MGAP, SFPA2, SFTA1, PHF6, CHERP, SUGP1, SUGP2, CCAR1, BAP18, RM41, KLHL7, MILK2, DHX37, YAF2, SRRM1, ZZZ3, K2013, ELMD2, CORA1, PELP1, TTC5, MIER1, NDUF2, NUP93, ZN687, CMTR1, LRC47, INT1, ABD12, CARME, FBXL6, SRBD1, NKAP, RP25L, ATPF2, RM50, CPSF7, ARFG2, EFNMT, ARFG1, PAF1, ENAH, DAND5, KRI1, MLKL, XXLT1, GOLM1, SUMF2, SUMF1, PGLT1, DHB11, TXND5, SERB1, CHSTE, LS14A, FSAF1, RB15B, PHC3, DIK2A, POPD1, SRFB1, SP20H, VP37A, PCAT1, BD1L1, NUP35, KNL1, PLBL2, DDX55, THOC2, WDR36, KI18A, GABP2, NPL4, STT3B, SPP2B, BRX1, STK35, NEK7, GPX8, PO210, GEMI5, FBF1, ZN384, WIPF2, SETD7, SMAP2, TM263, NU133, PDC6I, CO040, NUDC2, TWST2, SCFD1, PCNP, SPRY4, TRUB1, LMO7, CTL1, CKAP2, ATX2L, PHIP, RT4I1, NELFB, PALLD, PYDC1, PSPC1, P66B, BBX, CTBL1, ELYS, S39A7, H1X, RT27, NR4A3, PHF3, NDRG1, HS105, ZN592, LAR4B, NU205, PRCC, TFG, TAF4B, RREB1, HDAC2, SC65, SYMPK, GGH, DDX17, RAD50, CELF1, GSLG1, GPKOW, SMRC1, SMRD2, RAB8B, FUBP2, TNPO1, ARHG2, GLMN, KAT5, UBP7, POP5, LSM10, LMBL2, NCLN, FUBP1, SOSB2, PBIP1, SH3K1, PF21A, PINX1, P5CR2, INT12, FWCH2, FAF2, RMD1, MSI2H, RRFM, MTEF3, THA11, SGF29, DTBP1, PTCD3, MMAB, MCRS1, CERS2, SMRD1, TOE1, DDX27, SYMM, P121A, PDLI5, ERO1A, INT4, FUBP3, SYNM, VSIG2, HPDL, PAWR, RBM41, RSRC1, THOC3, CHAP1, S35E1, CLP1L, Z512B, ZFR, EP400, CNO6L, PRRC1, ZN512, YTDC1, SPT33, ZN830, RPR1A, RBM14, NED4L, QKI, LENG8, TRNT1, PP1RA, DEPD7, ATAD5, TEFM, MED15, EFGM, PIGS, TM209, IWS1, SIN3A, RBM15, MINT, NIBA2, YMEL1, HTF4, CNN2, SEC62, CDC5L, PSMD1, RING2, PARK7, EYA3, LGMN, PLIN2, POP1, SCAFB, TEAD3, TTC1, PHB2, CSN8, HCD2, SMAD5, ROAA, S29A1, CPNE1, MYD88, PKP2, SH3G1, GDF15, ARP5L, ZFY21, CMS1, DPH2, TBA1C, BCL7B, MBB1A, COR1B, TIRR, FSP1, PELO, ERP44, TACO1, ESYT1, CCM2, CNPY3, DIDO1, NDC1, ZSA5A, PAXX, HNRL1, RPP25, RCAF1, TBB2B, TM109, NUP58, GNL3, RIOK2, TIM21, THIC, RBM4, MND1, NADAP, SSBP3, RFIP5, ORNT2, NAA15, SRRT, AP1M1, NUSAP, HDHD5, RTF2, PECR, PDIP3, CEP41, RM37, GTPB4, UACA, UCK2, TB182, LNP, CEP44, WDR33, CTDS1, MFF, RB33B, NAT10, SP130, BRD8, RGAP1, CSTFT, LMA2L, CK054, F234A, RBM38, TDIF1, ALX4, SIL1, APC1, TMX4, WDR13, TARA, EPC1, ADNP, IPYR2, RM46, PININ, TM245, FOXP1, CPVL, GHITM, NELFA, BORG4, UN45A, SMOC2, AMPB, ZHX3, EMRE, REEP4, TM231, SH24A, DOCK5, CH033, SDS3, ACAD9, CQ10B, GORS2, JUPI2, SFXN1, SPE39, UBP42, RPF1, RPA2, GBB4, BRF2, RISC, CYBP, TENS1, TAF9B, TM165, MRM3, NCOA5, TRI39, SDF2L, AT131, RM47, APMAP, ARFG3, VTA1, PLPL8, SYSM, OSGEP, DMAP1, UBN1, RTN4, KMT5A, INCE, PRD10, ANLN, PDLI7, DDX21, MBNL1, SIR7, AAAS, ABCBA, PNO1, MBIP1, RAD18, SLX9, BMP2K, PDS5B, ECHD1, MDN1, DECR2, STAU2, DDX28, T106B, SPS2L, TYDP1, SEP11, DJC11, HAUS2, RBM22, MED9, ARGL1, SLTM, RMND1, AKIP, OXSM, THG1, HPF1, NDUBB, OCAD1, MARH5, MIC19, SIR5, CWC25, TEX10, THUM1, ING3, CARF, NSE4A, AATF, DDX56, TE2IP, ABI2, HXC10, BCLF1, TMOD3, MTCH1, HPBP1, MAT2B, ITSN2, CHMP5, THYN1, VAPA, RCC2, SLAI2, BCCIP, FPRP, RRBP1, CPSF2, RBM27, KANL3, GRHPR, NXF1, DAXX, TRM7, VTI1B, ABCF2, SYWM, SEC63, NDRG3, SUN2, LIMA1, SEPT9, TRPS1, DPP2, BAP29, NB5R1, S30BP, MED13, KAD3, HACL1, S2513, DBNL, CDC23, GMEB2, RCOR1, ACINU, NUP50, ZHX1, CDV3, CNO11, INT6, MCTS1, ZBT21, YETS2, ZMYD8, TMCO1, EPDR1, MYO6, KMT2B, PRP19, G3BP2, PACN2, MAGD2, PPIE, DIM1, MINP1, MACF1, PHF8, LIMC1, XCT, SRRM2, PA2G4, SMC3, SCML2, ZN148, RUVB2, VDAC3, RT33, PLAK2, ICE1, DDX52, MAN1, TR150, WBP11, MED16, NOP58, ZN281, SYYM, COQ6, LSM2, PHOCN, ORN, RT23, HDGR3, STRAP, RTCB, NOC2L, CHTOP, VPP2, TLN1, TRRAP, CRBG1, HYOU1, LAS1L, SAM50, PRC2C, RBM7, INSL6, YTHD2, PAXB1, SP16H, UTP18, CD2AP, SRPRB, TSSC4, SNX5, NUBP2, HCFC2, LRRF2, NPTN, 5MP1, DC1L1, CABIN, COX11, SCC4, ZHX2, MORC2
Species: Homo sapiens
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Vang S, Helton ES, Guo Y, Burpee B, Rose E, Easter M, Bollenbecker S, Hirsch MJ, Matthews EL, Jones LI, Howze PH 4th, Rajasekaran V, Denson R, Cochran P, Attah IK, Olson H, Clair G, Melkani G, Krick S, Barnes JW. O-GlcNAc transferase regulates collagen deposition and fibrosis resolution in idiopathic pulmonary fibrosis. Frontiers in immunology 2024 15 38665916
Abstract:
Idiopathic pulmonary fibrosis (IPF) is a chronic pulmonary disease that is characterized by an excessive accumulation of extracellular matrix (ECM) proteins (e.g. collagens) in the parenchyma, which ultimately leads to respiratory failure and death. While current therapies exist to slow the progression, no therapies are available to resolve fibrosis.
O-GlcNAc proteins:
NUD4B, GAL3B, UBA6, HACL2, SPD2B, NBAS, SBNO1, VP37C, CNOT1, ZN316, DDTL, ZSWM8, P121C, GNAT3, EIFCL, C2D4D, IGLL5, NACAM, DNS2A, ADAS, PDLI1, BACH, MYO1C, AIP, GTPB1, AP3B1, PSD11, PSD12, PSMD9, ATOX1, CBX4, PGRC1, SPT5H, TAF4, DFFA, CLIC1, TR11B, EIF3F, ODPX, MATN2, QSOX1, WASL, IPO5, EMAL1, IF2B3, DNM1L, MANBA, PLOD2, MEIS1, PSDE, ZN593, IMA4, BCL9, PESC, NOP56, DDX3X, CCN1, IMA3, MA2B1, SCD, PLPP3, ARI1A, TRAD1, HSPB6, COPE, IF1AY, CCS, DVL2, TOR1A, P5I11, ANM5, NHRF1, TPP1, TCRG1, NRP1, PSA7, SCAM3, ML12B, HGS, MYPT1, GAK, HNRDL, XPO1, ZN609, SC16A, PLXB2, SR140, SET1A, SYNJ2, PUR4, NPC1, TBX3, ARC1B, ARPC2, ARPC3, TIF1A, NKRF, CASC3, RER1, SURF4, SPTC1, SPTC2, OGT1, PMM2, PPM1G, SHIP2, EIF3D, EIF3H, IPO8, STX7, MOT4, MRP4, P4HA2, NUP42, ARPC5, CLOCK, TPSN, KDM6A, DHX15, ASAP2, PRP4, SERA, DC1L2, PSMD3, RFOX2, PAPS1, SNUT1, DAPK3, TGFI1, CTIF, M3K7, MCA3, HNRPR, PRPF3, TXNL1, TPD54, EMC8, SYNJ1, IF4G3, ARK72, E41L2, B4GA1, FOXO3, RNF13, DENR, XPOT, PLRG1, ZN207, NDUA2, BUB3, ACTN4, AP1G1, SNG2, SGTA, SYNC, KRT86, MYO1B, CPSF5, LANC1, U3IP2, AKAP8, NRDC, CALU, EDIL3, SAHH2, EXTL3, MED14, SMCA5, TRAK2, GANP, FADS1, PEPL, NRP2, MA1A2, ACSL4, SNX3, OGA, HNRPQ, TPST1, NEMF, GREM1, PLOD3, SEP15, TSN3, PLIN3, MAFK, UGDH, CTND1, DPM1, USO1, RT14, H2B1K, PRAF2, DKC1, IF2P, DNJA2, BRD4, MITF, SRGP2, WDR1, ROCK2, CPNE3, PHF2, T22D2, PP6R2, CREST, ANR17, GGCT, NDUS2, ZPR1, DUS11, NIPS2, SEM7A, LX12B, TBCA, VATG1, H2AY, FLNB, NCOR1, NDUS6, CISY, SPAG7, SC22B, DEAF1, PR40A, MPPB, PSIP1, ERLN1, CLN5, CLD11, SF3B1, CSDE1, WBP4, PRKRA, LYPA1, ERAL1, U520, TIPRL, CRTAP, EIF3G, EIF3J, CBR3, FACE1, IDHC, ATRN, STAM2, PIAS1, PIAS2, DNJC8, SPF30, ATP5H, TRIO, CBPD, KT33A, KRT34, KRT36, RL1D1, WFS1, CLPX, STC2, PDE5A, SRP72, DDAH1, B3GA3, MTA2, AL1A2, TOM70, TOX4, SC24D, PHF14, CSCL1, TOX, SUN1, ERLN2, PRP6, NFAT5, GLSK, SC31A, CSTN1, YIF1A, AGFG2, SCAF4, ZFPL1, ELP1, NDUB8, LETM1, ZRAB2, LC7L3, VAPB, MPZL1, NDUAA, FKBP9, 6PGL, PAPS2, SMC2, IPO7, AGM1, SVIL, AHSA1, PSMG1, NSA2, G6PE, SC24A, SC24B, ETHE1, ACSL3, CNOT4, EYA4, K2C75, OXSR1, AP2A1, WIZ, STAU1, BAG2, BAG3, AIFM1, LATS1, BPNT1, FADS2, DDAH2, ABHGA, TXD12, FBLN4, RECK, NUDT3, NDUBA, CLPT1, TOM40, ACL6A, CYB5, LDHA, DHE3, NB5R3, GSHR, COX2, PNPH, HPRT, AATM, EGFR, PGK1, C1R, PLMN, UROK, TPA, ANT3, A2MG, CO3, CO5, TIMP1, CYTA, RASN, LDLR, TGFB1, IGHG1, IGHA1, HLAB, CO1A1, CO3A1, CRYAB, K1C14, K2C6A, LMNA, APOA1, APOC3, FIBA, FIBB, FINC, AMBP, FETUA, FETA, VTDB, TFR1, TRFE, TRFL, CATA, RAF1, GBA1, FUCO, ALDOA, ANXA1, APOB, GCR, PRIO, SODM, OAT, HRG, THY1, K2C6B, K2C1, G3P, HLAA, CPNS1, AMYP, HSPB1, RPN1, RPN2, GNAI2, AT1A1, A4, ARGI1, APOD, ALDH2, ITB3, S10A8, PAI1, ADT2, IF2A, RLA2, RLA0, JUN, LA, HEP2, ITB1, K1C18, K2C8, CO5A2, DCUP, LCK, GELS, PTMA, CDK1, ATPB, S10A9, S10A6, IF4E, ENOA, G6PI, NPM, ITAV, HEXA, H2B1J, GDN, HYEP, LDHB, PGK2, PDIA1, H10, CATD, ANXA2, CAN1, TBB5, TRY1, PGS2, SAP, HEXB, CATL1, PROF1, APT, SYEP, CATB, HS90A, HNRPC, LAMB1, TPM2, FUMH, TSP1, SP1, CO1A2, ANXA6, 4F2, PFKAM, HS90B, SRPRA, ASNS, ODPA, CY1, RU2B, RU17, ITA5, NFIC, VIME, A2AP, RS17, GNAI3, ANXA5, K1C16, STS, RSSA, CD63, FGF2, GSTP1, RU1C, LEG1, DHPR, HMGB1, SPRC, TPM1, CLCA, ANXA4, CN37, PGFRB, DLDH, ROA1, PARP1, UCHL1, LKHA4, ALDOC, CO4A, H2AZ, UCRIL, ATX1L, POTEI, ZN865, ZN888, INAM2, HS71A, GLI2, LYAG, HLAC, H14, ODP2, THIO, PPGB, MGST1, KAP0, ESTD, CH60, CLUS, BIP, LAMC1, PPAL, HSP7C, UMPS, ODPB, ODB2, PYGB, RALA, LAMP1, ACADM, FGFR1, TOP1, G6PD, PYC, C1TC, MPRI, ADHX, SRF, PABP1, PCNA, HARS1, CO6A1, CO6A2, CO6A3, ADT3, IMDH2, TPR, ACTN1, PEPD, XRCC6, XRCC5, COX41, IFM1, LAMP2, RINI, CSPG2, EF2, K1C13, K2C5, PDIA4, P4HA1, TCTP, HLAE, PLST, ACPH, ETFA, KAP2, ENOB, CD59, MIF, CD99, GLU2B, FPPS, NID1, AK1A1, KPYM, ENPL, RSMB, IDE, PO2F1, HNRPL, SYDC, PLAK, ALDR, AMPN, PVR, ERF3A, B4GT1, EZRI, ATF2, UCHL3, FOSL1, FOSL2, NDKA, GNS, ZEP1, ARSB, RS2, ITF2, TFE2, DESP, RFA2, CD44, CBR1, CREB1, PGFRA, BGAL, H15, H13, H12, NCPR, AT2A2, FAAA, STMN1, NAGAB, AATC, KPCA, JUNB, ITA2, ASM, UBF1, HXB6, ATF7, CAN2, DESM, CEBPB, PYRG1, EGLN, DDX5, LEG3, IBP3, TCPA, PTN1, IBP2, RL35A, ARF4, RL7, EGR1, VINC, SON, RL17, PGAM1, RCC1, ATF1, NUCL, HXK1, E2AK2, SPEE, CSK22, RXRA, ITIH2, ITIH1, NFKB1, FST, IF2B, ANXA7, CD22, RAB3B, RAB5A, PSB1, MPRD, COX5A, LMNB1, HXA5, IMDH1, CO5A1, FILA, GSTM3, VATB2, CSRP1, FLNA, ACOHC, 5NTD, VDAC1, PGS1, SDHB, COMT, TGM2, PIMT, FBRL, PUR2, PUR6, SCP2, UBA1, NDKB, SPR1B, SPR2E, ROA2, RFX1, CBL, IBP4, QCR2, TGM1, FBLN1, PGH1, ITA6, SFPQ, PPIB, MAOM, SYWC, RS3, SAHH, COF1, IF4B, AT2B4, DGKA, GATA2, CPT2, KTHY, RIR1, EF1B, IBP5, PPAC, THIL, TENA, MYL9, RPB1, PAR1, MCM3, NFYB, ZA2G, THTM, RS12, TYY1, DNJB1, DNJB2, ATPA, PSA1, PSA2, PSA3, PSA4, ITA3, MOES, DDX6, DNMT1, U2AF2, RL13, IVD, HMGB2, PTBP1, SYTC, SYVC, EF1G, FKBP2, STOM, 1433T, DPP4, ARNT, RL10, APEX1, PYR1, CALR, MAP4, CALX, PSB8, PSA5, PSB4, PSB6, PSB5, ABCD3, ITPI2, LYOX, ELK4, NDUS1, MK01, GRN, AMPL, TPP2, IMPA1, CCN2, EPHA2, EPHB2, TKT, SPB3, RBMS1, PML, EF1D, MARCS, GNA11, AL4A1, ERP29, PRDX6, BLVRB, PRDX5, PRDX3, ATPD, RL12, ECHM, PEBP1, PDIA3, 2AAA, CDC27, T4S1, NMT1, PURA2, UFO, AMRP, TSPO, PUR8, CLIP1, SORCN, CTR1, AL1B1, RPB2, LCN1, SDHA, GDIA, S10A7, METK2, RIR2, TIA1, ZEP2, DNJA1, AKT1, QCR1, 3HIDH, PUR9, HNRH3, HNRH1, CASPE, 1433B, STIP1, S10AB, PRDX2, P5CR1, GBP1, ELF1, RL9, KINH, DUT, MRP1, MCM4, MCM5, MCM7, CD68, GLYM, HSP74, PROF2, CTNA1, CTNB1, PHB1, RADI, RFA3, RFC2, RL22, CBS, K1C9, FBN1, FBN2, IRS1, MYH9, MYH10, COPB2, ADDA, BASI, TIMP3, FUS, NU214, DEK, SOX5, GLRX1, PRS7, MP2K2, ATPG, RL4, LONM, PGM1, PP1G, PEDF, ODO2, GPX4, SRP14, NUP62, TAGL2, TALDO, ETFB, RBMX, VKGC, VATA, HSPA9, IF4A3, RS19, RL3, COIA1, OST48, AN32A, FEN1, CAPG, IL6RB, TXLNA, TCPZ, NNMT, RL13A, STAT3, MDHC, MDHM, ECHA, IF2G, ETV6, WNT5A, BUD31, NAA10, CSK, GARS, SYIC, KPCI, LAP2A, LAP2B, MTREX, HUTH, CASP3, RS27, HELZ, LPPRC, THIM, RL35, PCP, ECE1, LIS1, MUC18, MATR3, SSRA, RANG, PRS6B, PPIC, VDAC2, CBX5, UBP5, RAGP1, RECQ1, NOP2, CRKL, BAG6, NSF, NOTC1, MP2K3, RL27A, RL5, RL21, RL28, RS9, RS5, RS10, MAP1B, YAP1, UTRN, IQGA1, STT3A, CAZA2, CAPZB, SYQ, RL29, LEG7, TISD, ATPO, LIMS1, PPCE, MAOX, RFX2, RFX5, SOX9, COPD, LSS, PP2BC, CD151, PRC2A, TCPE, NEST, HSP13, KC1D, IDHP, PIPNB, PAXI, NR2C2, AL9A1, RL34, LMAN1, NASP, FAS, CDK8, TCPG, EFTU, AL7A1, SRP09, PCY1A, SYAC, SYCC, SYSC, MA2A2, PSB2, MCM2, COMP, ACADV, YLPM1, TMEDA, RBM25, NUMB, HINT1, NU153, RBP2, GSK3A, TAF6, 5NTC, SEPP1, GUAA, IDH3A, MMP14, GDIB, EMD, CPT1A, SERPH, PDLI4, F10A1, VASP, DYN2, MAP2, TOB1, CDK9, BCAM, PPT1, RL14, TCPQ, TCPD, ANX11, PAPOA, RAB5C, RAB7A, RAB9A, DAP1, RT29, SMCA4, IDH3G, SSRD, BAP31, DHB4, PSMD7, SPHM, CLCN5, KS6A3, HDGF, LUM, CNN1, NDUA8, ROA3, 6PGD, HNRPM, IMA1, NCBP2, GDIR1, AGFG1, HNRPF, STAT2, TF2AA, MSH6, ZN143, RBM5, SPSY, THOP1, CAZA1, CRIP2, NUP98, BIEA, TXTP, PPP5, ACLY, FOSB, MAP11, SUCA, PGTB2, COPB, COPA, CATC, RPAB4, MOT1, SC24C, TCP4, SYRC, ATX1, ATN1, CA2D1, SYYC, UBP14, AAKG1, HSP72, BCAT1, AT1B3, RD23A, RD23B, ANAG, KAD2, P5CS, SNAA, IF5, PSMD4, DRG2, XPO2, TERA, ECHB, MANF, AF10, DSRAD, LAMB2, CAD11, CAD13, SEC13, NH2L1, PSA, HNRH2, SCOT1, EIF3B, BID, SYMC, ITA1, MAZ, ATP5E, ATP5I, HDAC4, IF6, CTBP2, BCAR1, TMM33, PCBP3, NU107, MTPN, ARPC4, TPIS, EIF3E, SC61B, PP4C, GBRL2, MYL6, ACTB, IF4A1, RS20, PRPS1, PSA6, S10AA, CDC42, DEST, SPCS3, SRP54, RAB2A, RAB10, UBC12, UBE2K, UBE2N, RAB14, ARP3, ARP2, ARF3, ABCE1, RAP1B, RS3A, RL26, RL15, MGN, RL27, VA0D1, RL37A, RHOA, CH10, S61A1, LYSC, STXB1, B2MG, DAD1, NPC2, COPZ1, SUMO2, UFM1, NTF2, HNRPK, 1433G, RS7, PP1A, PP1B, PRS4, PRS8, RS8, RS15A, RS16, 1433E, RS14, RS23, RS18, RS29, RS13, RS11, RUXE, RUXF, SMD1, SMD2, PRS10, RL7A, RB11A, ERF1, CNBP, YPEL5, RS4X, PP2AB, ACTA, RL23A, RS6, H4, RAB1A, RAN, RL23, RS15, RS25, RS26, RS28, RS30, GBB1, RBX1, GBB2, RL30, RL31, RL10A, RL32, RL11, RL8, PPIA, FKB1A, RS27A, GRB2, RAC1, AP2B1, VAMP2, GNAS2, 1433Z, SUMO1, RL38, SKP1, RS21, IF5A1, RACK1, ACTG, ACTH, PP2AA, YBOX1, SC11A, CSK2B, TPM4, UB2L3, EF1A1, TBA4A, TBB4B, CSK21, HBB, NOMO3, HBA, F193A, IGBP1, SHPS1, SERB, PITX1, IF4G2, GTF2I, CNTP1, PHC1, TCPB, RAE1L, GSTO1, PRKDC, MAP1A, NUCB2, DCD, SSBP2, SARNP, RL24, RL36A, SMAD3, ERH, RHOG, RL19, SRSF3, FOXK1, DAB2, FBLN2, PGBM, XIAP, RBM10, RBM3, CYC, S25A3, VIGLN, PURA, BORG5, CLH1, FKBP3, REEP5, DHSO, HNRPU, U2AF1, SPTB2, TIAR, SET, SRSF2, FOXK2, RUNX1, AMPD2, FABP5, CAP1, K22O, HMCS1, LAT1, EXOSX, OTUD4, PFKAP, EWS, PLCB3, ROR2, TAGL, MEF2A, ODO1, DSG1, SP3, RL18A, FKBP4, PLOD1, NUCB1, RL6, TOP2B, CREB5, AKA12, M2OM, DYST, CAV1, KMT2A, LMNB2, UPAR, TF65, GLGB, IF4G1, K1C17, NOTC2, TLE4, LGUL, AK1C1, 1433F, PLP2, CSTF1, UBE3A, FAK1, CALD1, COEA1, PUR1, GFPT1, SUH, MEF2C, GABPA, GABP1, PRDX1, RL18, CKAP4, ZO1, KHDR1, BAX, KLC1, ACK1, LRP1, SRSF1, RHG01, TLE5, TGM3, PP2BA, DHX9, QOR, GOGA3, GOGA2, LG3BP, DSC1, CD47, PPID, SSRP1, NSUN2, RBBP4, NCBP1, MGT5A, EP300, AHNK, IFFO1, INCA1, NEXN, MGAT2, GALT2, GALT1, AP1B1, CPSF1, MPPA, SCRN1, NU160, SCAP, SRBP2, TWF1, ASPH, FBLN3, TROP, BPTF, FSTL1, GRSF1, NFIA, SFSWA, SF3A3, SEPR, TP53B, AIMP1, ILF3, LMAN2, EPS8, TRAP1, TAF10, ECH1, STRN3, CDC16, FLII, CSN1, MTAP, AAPK1, EI2BE, TADBP, ROA0, AIMP2, PRDX4, PAK2, CBX3, PSMD2, TBX2, SRSF9, SRSF5, SRSF6, TIF1B, G3BP1, SG2A2, PTK7, PABP4, EIF3I, CTBP1, UB2V1, DC1I2, ILK, NNTM, TCOF, S39A6, SF3B2, ADAM9, TMED1, LSAMP, MYO9B, GAB1, SMAD4, PICAL, MAMD1, SQSTM, TBB3, ASAH1, PRP4K, PIN1, RIPK1, HDAC1, KCC2D, DCTN2, TRA2A, SNX1, CUL1, CUL4A, CUL4B, DYR1A, FCL, FHL1, FHL3, CD166, RUNX3, SPTN1, PKP1, DX39B, BLMH, TBB2A, IDI1, RUNX2, PEBB, NFYC, CDK13, CKAP5, COTL1, HNRPD, SCRB2, NID2, DAG1, VEZF1, EIF3A, UBP2L, SCRIB, GIT2, MLEC, TTL12, FHL2, DPYL3, DCTN1, DYHC1, SRC8, RCN2, TRI25, FLNC, FKBP8, FZD2, GAS6, CAPR1, RBM39, FAT1, SEM3A, MCM6, DSC3, PUM1, EPN4, SMC1A, RRP1B, NCOA6, GSE1, GANAB, 2A5D, LBR, MVP, LTBP1, LTBP2, MEF2D, CHD4, LASP1, ARI5B, PTGR1, NC2A, ZN638, IMB1, NOLC1, NUMA1, K2C72, CND2, PSMD6, SEPT2, SART3, CND1, U5S1, R3HD1, TRAM2, RB3GP, SYK, IF4H, BRD3, POSTN, OXA1L, EEA1, PDIA6, PA1B3, PCOC1, PLEC, IPYR, TEBP, NONO, RBBP5, RCN1, PCBP1, PCBP2, RHEB, DHC24, SF3B3, PUM3, DLGP5, RSU1, CNN3, SF3B4, SF3A2, RBMS2, SC23A, SF3A1, CDSN, SSXT, BGH3, NCOA2, TRAM1, SF01, MED1, JHD2C, TRIP6, MARE1, T22D1, ELAV1, ELF2, NAB2, MYLK, TAB1, AAAT, MLF2, ITSN1, TBCC, VAS1, ZFHX3, ZYX, ETFD, SEPT7, ADRM1, UAP1, IBP7, AINX, LAMA4, EXT1, PSMD5, CSRP2, DDB1, CDC37, DPYL2, KCC4, RBBP7, TAF9, ECM1, SRSF7, CPSF6, DREB, NRF1, FSCN1, IF16, DECR, GLO2, H2A2C, NDUA9, PCKGM, DDR2, HCDH, UGPA, TRXR1, MIC60, CPEB4, HNRL2, INF2, RFX7, QSER1, AAK1, PRSR3, QRIC1, LRRF1, P3H1, MA7D1, AL1L2, K2C71, TIM50, FUT11, TB10B, ANO6, FIL1L, SVEP1, AMOT, EPC2, FND3B, CRTC2, QORX, DHB12, CYBR1, IN80D, PAN3, YIF1B, F133B, ZN326, FILA2, MEST, HERC4, PIGG, BCORL, FA76B, TGO1, PREP, PRC2B, RRP12, TOIP1, PCID2, EOGT, TTC38, TM201, NU188, HP1B3, CE170, ZN362, FBP1L, FKB15, ZEP3, ZC3HD, LRIF1, UBR4, STXB5, RHG21, RM02, UBAP2, KPRP, KPLCE, RBM26, WLS, TUT4, H37, NT5D1, AHDC1, MRCKA, RPRD2, MYOME, ZN318, BROX, TASO2, PEAR1, MBNL2, ZMYM4, FHI2A, CD276, TSH3, TENS2, KANK2, AR6P4, OLM2A, HGNAT, ARID2, TENS3, CRBG3, RHG17, BICRL, AMERL, ATLA3, NXN, IQEC1, VASN, CPIN1, PTRD1, ELP2, LTOR1, TWF2, ADNP2, K2C80, LIN54, SCMC1, TM214, PPR18, CAVN1, CDC73, RM14, TATD1, EDC4, PRP8, SCYL2, GOLM2, NFRKB, RL22L, ALKB5, NCEH1, MDEAS, ZC3HE, OGFD3, LARP1, C1TM, FIP1, CRTC1, CSPG4, ARAID, LRSM1, TMCO3, LCLT1, CREL2, PAMR1, FAT4, MCAF1, CP2R1, PACS1, BCOR, MPRIP, HACD2, GGYF2, HSDL2, KAT3, CERS6, THSD4, MEX3B, ZN574, RN111, BAKOR, SRCAP, RIPR1, YJ005, TSH1, BGIN, UBN2, TMTC3, RAPH1, MOB2, IKIP, H32, LARP4, TBA1A, RS27L, HAKAI, ASXL2, CCD80, SPT6H, SND1, DDX46, 5MP2, DHX30, EIF3M, CYFP1, TAOK1, KDM3B, PHF5A, ERMP1, ZCCHV, NUP54, POGZ, MON2, K1C27, NUFP2, MAVS, CLAP1, DHX29, PLGT3, LIMS2, HDGR2, DCXR, EMSY, RAI1, I2BP2, RBBP6, SH3R1, RABEK, HUWE1, YTHD3, K2C1B, KHDC4, TMED4, COXM1, CENPV, GALT5, PHLB2, GLT10, MYPN, SYVN1, ACOT1, PABP2, LDB1, LYRIC, ZN598, KTN1, BCL9L, PHLB1, LUZP1, GP180, CAND1, HOOK3, TSYL5, CARM1, PRSR1, MEX3D, DDX42, P66A, HORN, RB6I2, RELL1, PLD3, FOXP4, P3H2, P3H3, CCD50, SPA12, CTL2, WDFY1, TEX2, NXP20, MGAP, Z3H7A, CHERP, ANKH1, SUGP1, CCAR1, DJC10, MSRB3, PLPL6, MILK2, SPB1, SMAP1, P20D2, PHAR4, ZNF34, ELMD2, DCP1B, XRN1, MAML2, ABI1, SELH, SPART, RPTOR, CCAR2, SIX5, NUP93, K2C78, ZCH24, LTBP4, ASCC3, SYNPO, FNBP4, AFAP1, CERS5, NKAP, CPSF7, ARFG2, ARFG1, LRC17, EMC1, ENAH, RM43, YP023, ANR52, GT251, SUMF2, SUMF1, PGLT1, PCYXL, TXND5, SCPDL, SERB1, LEMD2, NECP1, FA98A, CHSTE, APCDL, RN214, LS14A, TNR6A, PHC3, ABCF1, SP20H, ZNT7, NAV1, VP37A, FBX22, PCAT1, ZMIZ2, ARI1B, NUP35, NEUA, PLBL2, MFSD8, NEDD1, ZNT5, G45IP, SMRC2, NPL4, PUM2, KISHA, RDH11, STT3B, SPP2B, HM13, ALMS1, NEK9, PKHO2, DDX54, DLG5, NEK7, GPX8, GEMI5, IPO4, ZN384, SETD7, F222B, SMAP2, CHUR, CEMIP, PDC6I, FBLI1, PHLA1, NUDC2, SCFD1, POF1B, LMO7, ATX2L, SELM, PALLD, SREK1, PSPC1, P66B, AUTS2, ZCH14, IRGQ, DDB2, ASM3A, DDX1, S39A7, FAM3C, GBF1, SMG7, RTF1, NICA, TM9S4, TM131, RT27, F168A, PHF3, MAML1, HS105, LAR4B, GCN1, ZN516, NU205, PXDN, AN32B, NECT2, TFG, ARC1A, STAM1, REQU, SC65, CBP, GGH, NELL1, DDX17, TANK, CELF1, GSLG1, RENT1, CSN5, GATA6, SMRC1, FUBP2, TNPO1, ARHG2, UBP13, USP9X, UBP7, LPP, RBPMS, SMCE1, CAVN3, MYDGF, YIPF5, PIGT, RL36L, ZN622, WBP2, NCLN, MRTFA, ERGI1, RFT1, FERM2, FUBP1, TTC17, LRC59, PBIP1, FKB10, AKTS1, PF21A, EFHD2, GALM, INT12, CTHR1, KLH29, OPTN, AP2M1, RCN3, REPS1, KBP, DAZP1, RBM33, CK024, ZN503, I17RA, OTUB1, PGM2, CERS2, ZC21A, P121A, PDLI5, CREL1, ERO1A, PGAM5, FUBP3, SUCB2, GMPPA, KIRR1, WNK4, TMX3, CHAP1, ZFP91, PDLI2, ZC3HA, CLP1L, SCYL1, Z512B, CNDP2, ZFR, B3GT6, EP400, VATG3, PRRC1, ZN512, NOL4L, MBOA7, DOCK7, TOX2, SPB12, ARHGH, RBM14, QKI, LENG8, GSDMA, PP1RA, S38A2, VPS35, PHF12, SNX18, CIC, MED15, ERGI2, NUDC1, ERBIN, PIGS, WRIP1, RANB9, CLCC1, UBL7, MYADM, SIN3A, RUFY1, MINT, MMS19, UHRF1, NIBA2, HTF4, TBCB, NELL2, PSB7, CNN2, SEC62, PCY2, K1C12, CDC5L, PSMD1, SDF2, PARK7, EYA3, NEUR1, VAT1, LGMN, PLIN2, NUP88, MNT, SCAFB, DNJC7, PHB2, RGPD5, PITX2, ATX2, HCD2, COCA1, SMAD5, ROAA, LITAF, NP1L4, ACON, TM9S2, TS101, CPNE1, TCPH, EBP2, ANM1, SH3G1, CND3, DDX50, MEP50, VKOR1, TBA1C, SELS, MBB1A, COR1B, TXD17, VPS25, RM45, MXRA8, CAB45, ADPGK, PELO, ERP44, LXN, ESYT1, CNPY3, LIMD2, CSN4, WAC, DIDO1, DCTN5, AASD1, TMM43, TBCD, TBB6, HNRL1, HTAI2, DDX23, DHRS6, CA050, WDR18, THUM3, RN126, TBB2B, TM109, TMED9, NUP58, ELOV1, THIC, REPI1, RBM4, SFXN3, SSBP3, NAA15, KLF16, SRRT, TGT, HDHD5, EIF2A, CADM1, MK67I, YTHD1, WNK3, NEUL, RM37, GTPB4, UACA, RAB34, TBL1R, UBL5, EDEM3, API5, K1C23, UNK, FTO, TB182, AMRA1, TTYH3, ADSSP, PITH1, SKI8, SLIRP, WWTR1, TWSG1, NAA50, MKRN2, PAIP1, LSG1, NAT10, XRN2, SP130, BRD8, DDX47, MAGT1, LMA2L, SIL1, I2BPL, NUCKS, EHD4, VPS16, SH3L3, EPC1, SLK, S38A1, PDCL3, RBGPR, ADNP, DPH5, HIPK2, FOXP1, CK068, BOLA2, TMX1, NELFA, GCP60, PTN23, UN45A, OFUT1, WNK1, AMPB, GAPR1, ZHX3, EHD1, ZN768, SG196, CC134, PEAK1, AAMDC, WDR26, PKHG2, ZN703, ACAD9, GORS2, JUPI2, SYP2L, SFXN1, FKRP, ELP3, KT3K, FBRS, MLXIP, PKHA5, GBB4, XPO5, GRPE1, MYG1, RC3H2, TENS1, TAF9B, EMAL4, GLOD4, ZBT20, NCOA5, TANC2, MOV10, ZN532, ZN160, TNR6C, CHD8, SDF2L, CD248, SEC12, S10AE, AT131, RM47, CHM1A, TM9S3, APMAP, TRXR2, ARFG3, RAB18, VTA1, CD320, UBN1, DCP1A, TF7L2, RTN4, NIT2, NECT3, EXOS3, ANLN, XPP1, GEPH, PDLI7, DDX21, SAR1A, SIAS, SHLB2, MBNL1, 4ET, AAAS, STRN4, UBQL4, HEBP1, ABC3C, PHP14, F1142, TM7S3, KRT84, SYFB, SYIM, BMP2K, ATG3, SMC4, SAC1, OLA1, ZF64B, RBM12, ABHDA, SHFL, T106B, SPS2L, DD19A, TBC23, CC50A, SEP11, MED17, DJC11, INT7, ATD3A, ARL8B, DDX18, RT18A, NLE1, ZN358, RBM22, ARGL1, RM22, CZIB, GEMI8, F120C, OCAD1, IMPA3, MIC19, CKLF6, P4HTM, TOR4A, TRM1, CARF, DPP3, DDX56, BCLF1, TAB2, M3K20, UGGG2, UGGG1, CDK12, TECR, ERAP1, GGA3, F120A, GDE1, IF2B1, MAT2B, MYOF, ITSN2, BICRA, EHD2, CNOT2, CALL5, CRIM1, HACD3, KCMF1, RAI14, RM27, SENP1, SH3B4, PHRF1, RCC2, SLAI2, TEN3, CT2NL, RRBP1, SYLC, RBM27, KANL3, ANFY1, RERE, SUCB1, LRIT1, DPM3, SAE1, COPG2, MRC2, GBG12, DHCR7, DKK3, VPS29, EIF3K, GRHPR, CATZ, SAE2, NXF1, B4GT7, PEF1, FBLN5, CLIP2, ZO2, DNJB4, ADDG, ABCF2, TES, LIMD1, Z3H7B, TCF20, SUN2, LIMA1, SRP68, CHRD1, SEPT9, UBQL2, PCYOX, DDX20, ATS1, DPP2, CEIP2, NB5R1, S30BP, MED13, PUF60, NRBP, VATH, CBPA4, XPO7, BAZ2B, SIX4, GGT7, MSRA, NAGK, DBNL, DCTN4, CDC23, STML2, DBR1, AKA11, GMEB2, CPSF3, PARP4, RALY, ITA11, NUP50, ZHX1, ZN346, DNPEP, MCTS1, S39AA, ASAP1, MRTFB, HEG1, ZMIZ1, PRR12, YETS2, HECD1, ZMYD8, COR1C, NOTC3, SPAT2, PPT2, PRP19, UBQL1, SNX12, SYNRG, G3BP2, CHIP, PACN2, MAGD2, SNX6, PSD13, FAF1, PPIE, CSN3, MINP1, S12A4, MACF1, SCAF8, TRI33, TNR6B, SMAG1, CE164, FOXJ3, SHAN2, COR2B, SRRM2, PA2G4, ZN148, RTRAF, RUVB2, CLC11, EIF3L, PLAP, RUVB1, NUDC, VDAC3, COF2, ERGI3, SYFA, DRG1, NCKP1, PLAK2, ZN652, MA2B2, OFUT2, FND3A, E41L3, R3HD2, RRP44, LRCH1, GSTK1, DDX52, RT07, TMA7, MAN1, CHSP1, TR150, NOP58, ZN281, SGT1, ACOT9, NOSIP, MEMO1, SHLB1, LC7L2, SBDS, TMED7, ORN, UFC1, STRAP, RTCB, ZN330, RL36, SAMH1, TLN1, ARIP4, MTCL1, TCAF1, UBP15, LOXL2, CRBG1, HYOU1, TBL2, KLF12, ARI1, LSM4, RN114, PRC2C, RBM7, YTHD2, SP16H, SRPRB, MRCKB, ZN706, MAGD1, SNX5, HCFC2, FHOD1, SERC, NCOR2, NPTN, CBPQ, SOX21, RT18B, COPG1, FKBP7, GMEB1, CLIC4, EMIL1, MTCH2, 5MP1, DC1L1, EPN1, NEMO, IF2B2, ZNT1, NCOA3, NUMBL, PIAS3, ZHX2, S23IP
Species: Bos taurus, Homo sapiens
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Hou C, Deng J, Wu C, Zhang J, Byers S, Moremen KW, Pei H, Ma J. Ultradeep O-GlcNAc proteomics reveals widespread O-GlcNAcylation on tyrosine residues of proteins. Proceedings of the National Academy of Sciences of the United States of America 2024 121(47) 39531497
Abstract:
As a unique type of glycosylation, O-linked β-N-acetylglucosamine (O-GlcNAc) modification (O-GlcNAcylation) on Ser/Thr residues of proteins was discovered 40 y ago. O-GlcNAcylation is catalyzed by two enzymes: O-GlcNAc transferase (OGT) and O-GlcNAcase (OGA), which add and remove O-GlcNAc, respectively. O-GlcNAcylation is an essential glycosylation that regulates the functions of many proteins in virtually all cellular processes. However, deep and site-specific characterization of O-GlcNAcylated proteins remains a challenge. We developed an ultradeep O-GlcNAc proteomics workflow by integrating digestion with multiple proteases, two mass spectrometric approaches (i.e., electron-transfer/higher-energy collision dissociation [EThcD] and HCD product-dependent electron-transfer/higher-energy collision dissociation [HCD-pd-EThcD]), and two data analysis tools (i.e., MaxQuant and Proteome Discoverer). The performance of this strategy was benchmarked by the analysis of whole lysates from PANC-1 (a pancreatic cancer cell line). In total, 2,831 O-GlcNAc sites were unambiguously identified, representing the largest O-GlcNAc dataset of an individual study reported so far. Unexpectedly, in addition to confirming known sites and identifying many other sites of Ser/Thr modification, O-GlcNAcylation was found on 121 tyrosine (Tyr) residues of 93 proteins. In vitro enzymatic assays showed that OGT catalyzes the transfer of O-GlcNAc onto Tyr residues of peptides and OGA catalyzes its removal. Taken together, our work reveals widespread O-GlcNAcylation on Tyr residues of proteins and that Tyr O-GlcNAcylation is mediated by OGT and OGA. As another form of glycosylation, Tyr O-GlcNAcylation is likely to have important regulatory roles.
O-GlcNAc proteins:
NPIA9, RBM47, E2F8, SBNO1, CNOT1, P121B, HMX3, RHG32, P121C, NACAM, PDLI1, TAF4, DNM1L, PLOD2, CAC1A, ARI1A, CDKA1, NCAN, ABLM1, KMT2D, HGS, MYPT1, ZN609, SC16A, SET1A, TRNK1, OGT1, TNC18, P4HA2, NUP42, KDM6A, ASAP2, SI1L1, RFOX2, PRPF3, SYNJ1, IF4G3, MTG8R, E41L2, PLRG1, ZN207, BUB1, MYPT2, KPRB, ZN292, SI1L3, GANP, TBC12, OGA, KLH41, PLIN3, MAFK, ABCC9, TBL1X, MITF, SRGP2, SLIT3, T22D2, PP6R2, ANR17, LIPA4, ZN217, NCOR1, U520, RASF9, DYSF, TOX4, SC24D, FCSD2, PCF11, NFAT5, SC31A, AGFG2, SCAF4, ELP1, MRP6, SVIL, SC24A, SC24B, CNOT4, ZMYM6, BAG3, LATS1, LMNA, CATA, GCR, CPNS1, HSPB1, RPN1, RLA2, ITB1, K1C18, K2C8, NPM, CATD, GP1BA, SAP, CATB, SP1, PTPRC, NFIC, VIME, K1C19, SNRPA, ATX1L, LAMC1, ARY2, SRF, PABP1, TPR, SKIL, ENPL, PO2F1, B4GT1, ATF2, FOSL1, FOSL2, GNS, ZEP1, RS2, TFE2, CREB1, HXB6, ATF7, EGR1, SON, ATF1, NUCL, ICAL, OSBP1, RFX1, CBL, NFYA, IF4B, GATA2, ARNT, MAP4, GRN, CDC27, CLIP1, HXC9, ZEP2, ELF1, NU214, NUP62, CUX1, STAT3, BUD31, HNF4A, LAP2A, MTOR, PCP, MATR3, GATA4, UTRN, STT3A, RFX5, SOX9, PRC2A, NEST, HSP13, NASP, CDK8, YLPM1, NU153, RBP2, TAF6, EMD, PPT1, PAPOA, FXR2, KCNQ1, MYOM1, AGFG1, HNRPF, NUP98, SMTN, SC24C, ATX1, RD23B, AF17, DSRAD, MAZ, CTBP2, CSK21, F193A, SERB, IF4G2, GTF2I, PHC1, NGAL, KGD4, SARNP, FOXK1, DAB2, PGBM, RHG04, SPTB2, FOXK2, OTUD4, EWS, SP2, NRG1, SP4, SP3, PAX2, KMT2A, IF4G1, NOTC2, PTN12, GABPA, GABP1, CKAP4, ZO1, ACK1, TLE5, EP300, AHNK, ASPH, TROAP, BPTF, NFIA, TP53B, FOXC1, TAF10, PICAL, MAMD1, SQSTM, RIPK1, STIM1, CUL4B, NFYC, CDK13, CKAP5, VEZF1, UBP2L, GIT2, SRC8, CAPR1, PUM1, MDC1, EPN4, TTLL4, RRP1B, NCOA6, GSE1, MEF2D, ZN638, NUMA1, HECAM, R3HD1, DAZP2, KIF14, PDK3, EBP, NONO, LRC41, RBMS2, SSXT, NCOA2, SF01, MED1, JHD2C, T22D1, ELF2, TAB1, NCOA1, TBCC, ZFHX3, ZYX, CCDC6, TAF9, DREB, NRF1, GEN, RFX7, QSER1, AAK1, PRSR3, RGPA2, QRIC1, TB10B, TPRN, FIL1L, CRTC2, IF44L, YIF1B, NOM1, BCORL, DDX6L, BRD10, SH319, TGO1, PRC2B, CE170, ZN362, DCST2, ZEP3, ZC3HD, CSCL2, LRIF1, RHG21, UBAP2, RBM26, CF163, AHDC1, RPRD2, ZN318, TASO2, ZMYM4, PAPD7, TENS2, KANK2, ICE2, ARID2, TENS3, USF3, ANR40, BICRL, SDE2, NIPBL, LIN54, TET2, ZNT6, EDC4, SCYL2, TTC27, NFRKB, RSBNL, TT23L, NCEH1, MDEAS, ZC3HE, FIP1, CRTC3, SAS6, ARSK, MCAF1, BCOR, GGYF2, AEBP2, BNC2, NFXL1, CO039, SRCAP, UBN2, TM1L2, RAPH1, HAKAI, ASXL2, SPT6H, BOP, KDM3B, ZCCHV, NUP54, RGPD4, POGZ, ZFY16, NUFP2, MAVS, EMSY, RAI1, I2BP2, SDK1, SRGP1, RBBP6, SH3R1, YTHD3, CENPV, KAISO, MYPN, LDB1, LYRIC, ABCAC, BCL9L, CASZ1, TSYL5, CARM1, PRSR1, DDX42, CACL1, P66A, HIPK1, RB6I2, AHNK2, NAV2, GID4, ARI3B, TEX2, MGAP, Z3H7A, ANKH1, SUGP1, CCAR1, MILK2, GAR4, TBC21, PHAR4, XRN1, MAML2, SPART, NUP93, DOCK4, SYNPO, FNBP4, AF1L2, TAB3, NOPC1, IGSF1, ARFG1, ENAH, TM102, WDR31, MISSL, TNR6A, PHC3, SP20H, NAV1, VP37A, KMT2C, ARI1B, NUP35, KNL1, O52H1, PLBL2, NEDD1, SMRC2, TBC15, ZN507, ALMS1, DLG5, FNIP1, ZN384, WIPF2, PYRD1, D42E1, PCNP, LMO7, ATX2L, P66B, BBX, ELYS, ZCH14, PIEZ1, GBF1, RTF1, PHF3, MAML1, ZN592, LAR4B, SORL, TFG, TAF4B, RREB1, CBP, DDX17, GPKOW, M4K1, FUBP2, LPP, WNT2B, P33MX, ACD, FKB10, TTC28, PF21A, ZN669, ZN501, REPS1, RBM33, CERS2, GWL, P121A, CC120, PDLI5, SENP5, VCIP1, ZN462, CHAP1, LCOR, Z512B, ZFR, EP400, BMF, PRRC1, NOL4L, RBM14, QKI, PHF12, CIC, MED15, ERBIN, SIN3A, MINT, HTF4, EYA3, DNJC2, ELF4, RGPD5, ATX2, TS101, ARI3A, TEP1, DPH2, GPTC1, WAC, DIDO1, HNRL1, CP250, NUP58, RBM4, UBP26, YTHD1, BCDO2, B2L14, AMRA1, CE295, TANC1, ZC12C, CEP44, SP130, BRD8, I2BPL, RBNS5, EPC1, ADNP, HIPK2, ZN106, PTN23, WNK1, ZHX3, ZN644, HAUS4, SLAP2, YTDC2, PEAK1, PKHG2, ECT2, GORS2, MLXIP, PKHA5, CLSPN, CDHR5, RC3H2, TAF9B, NCOA5, TANC2, ZN532, TNR6C, CHD8, APMAP, UBE2T, DMAP1, UBN1, DCP1A, RTN4, PRD10, PDLI7, EI2BG, MBNL1, RNC, RBM12, INT7, CARF, ABI2, HXC10, TAB2, CDK12, GRHL1, ITSN2, BICRA, CNOT2, FLRT1, KCMF1, DAPLE, CHD7, F135A, RBM27, KANL3, RERE, LIMD1, TCF20, SUN2, UBQL2, TRPS1, S30BP, PUF60, NRBP, BAZ2B, SIX4, HOOK1, GGA2, TASOR, AKA11, GMEB2, PARP4, MYO15, MYH13, NUP50, ZHX1, CDV3, MRTFB, ZBT21, PLXB3, PRR12, YETS2, HECD1, ZMYD8, SPAT2, PRP19, SOX13, SCAF8, TRI33, TNR6B, SET1B, SATB2, SHAN2, HPS5, SRRM2, SCML2, R3HD2, ZN281, KLK5, ARIP4, MTCL1, RPGF2, CRBG1, HYOU1, PRC2C, RBM7, YTHD2, HCFC2, NCOR2, GMEB1, NCOA3, S23IP
Species: Homo sapiens
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He J, Fan Z, Tian Y, Yang W, Zhou Y, Zhu Q, Zhang W, Qin W, Yi W. Spatiotemporal Activation of Protein O-GlcNAcylation in Living Cells. Journal of the American Chemical Society 2022 144(10) 35138101
Abstract:
O-linked N-acetylglucosamine (O-GlcNAc) is a prevalent protein modification that plays fundamental roles in both cell physiology and pathology. O-GlcNAc is catalyzed solely by O-GlcNAc transferase (OGT). The study of protein O-GlcNAc function is limited by the lack of tools to control OGT activity with spatiotemporal resolution in cells. Here, we report light control of OGT activity in cells by replacing a catalytically essential lysine residue with a genetically encoded photocaged lysine. This enables the expression of a transiently inactivated form of OGT, which can be rapidly reactivated by photo-decaging. We demonstrate the activation of OGT activity by monitoring the time-dependent increase of cellular O-GlcNAc and profile glycoproteins using mass-spectrometry-based quantitative proteomics. We further apply this activation strategy to control the morphological contraction of fibroblasts. Furthermore, we achieved spatial activation of OGT activity predominantly in the cytosol. Thus, our approach provides a valuable chemical tool to control cellular O-GlcNAc with much needed spatiotemporal precision, which aids in a better understanding of O-GlcNAc function.
O-GlcNAc proteins:
SBNO1, CNOT1, BACH, PSD11, PSD12, TAF4, CLIC1, EIF3F, IPO5, IF2B3, ARI1A, KMT2D, ANM5, PSA7, HAT1, HGS, MYPT1, XPO1, SC16A, SR140, SET1A, PUR4, NPC1, OGT1, HMGB3, PPM1G, EIF3D, EIF3H, P4HA2, SERA, PSMD3, PAPS1, MSI1H, IF4G3, E41L2, FOXO3, ZN207, BUB3, ACTN4, SYNC, SAHH2, KPRB, GANP, PEPL, OGA, PLOD3, IMA7, IF2P, DNJA2, MITF, CPNE3, CLU, PP6R2, CREST, ANR17, NCOR1, VP26A, CLN5, CSDE1, IDHC, SRP72, MTA2, TOX4, SC24D, PCF11, NFAT5, SC31A, AGFG2, SCAF4, SMC2, IPO7, PSMG1, SC24A, SC24B, EYA4, HS74L, TOM40, LDHA, PNPH, HPRT, PGK1, CAH2, ALDOA, ANXA1, G3P, IF2A, RLA1, RLA2, RLA0, JUN, LA, AGAL, KCRM, ENOA, PYGL, G6PI, LDHB, H10, ANXA2, TBB5, PROF1, APT, SYEP, HS90A, LAMB1, SP1, ANXA6, DAF, PFKAM, HS90B, ASNS, RS17, ANXA5, RSSA, GSTP1, HMGB1, PARP1, LKHA4, ALDOC, ATX1L, HS71B, RO60, PTPRF, THIO, HSP7C, EPB41, UMPS, G6PD, C1TC, ADHX, SRF, PRPS2, PABP1, PCNA, IMDH2, KCRB, PEPD, XRCC6, XRCC5, RINI, EF2, P4HA1, PLST, ACPH, GYS1, KPYM, PO2F1, SYDC, PLAK, ERF3A, NDKA, RS2, CBR1, CREB1, HSP76, PYRG1, DDX5, PFKAL, TCPA, RL35A, ARF4, RL7, RL17, PGAM1, DNLI1, NUCL, SPEE, CSK22, PSB1, FLNA, PIMT, PUR2, PUR6, UBA1, NDKB, RFX1, CBL, RS3, NFYA, SAHH, COF1, EF1B, MCM3, RS12, BRD2, PSA1, PSA2, PSA3, PSA4, MOES, DDX6, DNMT1, PAX6, U2AF2, RL13, SYTC, SYVC, EF1G, 1433T, ARNT, RL10, RFA1, APEX1, PYR1, MAP4, PSB6, PSB5, AMPL, TKT, RBMS1, EF1D, PRDX6, RL12, PEBP1, 2AAA, CDC27, NMT1, PURA2, PUR8, METK2, DNJA1, PUR9, 1433B, STIP1, PRDX2, ELF1, CGL, RL9, KINH, MCM4, MCM5, MCM7, HSP74, RL22, CBS, MYH9, MYH10, COPB2, FUS, DEK, PRS7, RL4, SRP14, TALDO, RS19, RL3, TCPZ, RL13A, MDHC, IF2G, CSK, GARS, SYIC, RS27, RANG, BAG6, NSF, RL27A, RL5, RL21, RL28, RS9, RS10, SYQ, RL29, ATPO, PPCE, COPD, TCPE, PIPNB, AL9A1, NASP, FAS, TCPG, SYAC, SYSC, PSB3, MCM2, YLPM1, RBM25, HINT1, GSK3A, GUAA, DNLI3, GDIB, SERPH, F10A1, RL14, TCPQ, TCPD, ANX11, PAPOA, SMCA4, SSDH, 6PGD, IMA1, AGFG1, HNRPF, THOP1, PPP5, ACLY, COPB, COPA, SC24C, SYRC, ATN1, SYYC, RD23B, ANAG, XPO2, TERA, NP1L1, PSA, EIF3B, ATPK, SYMC, TPIS, EIF3E, IF4A1, RS20, PRPS1, PSA6, CDC42, UBC12, UBE2N, ARP3, ARP2, ACTZ, CSN2, ABCE1, RS3A, RL26, RL15, RL27, 1433G, RS7, PRS8, RS8, RS15A, RS16, 1433E, RS23, RS18, RS13, RS11, RUXE, PRS10, RL7A, ERF1, RS4X, RL23A, RS6, RAN, RL23, UB2D2, RS24, RS25, RS26, RL30, RL10A, RL32, RL11, RL8, PPIA, RS27A, RAC1, AP2B1, 1433Z, RSMN, SUMO1, RL38, IF5A1, RACK1, YBOX1, EF1A1, TBA1B, CSK21, F193A, IF4G2, PHC1, TCPB, GSTO1, RL24, RL36A, ARF1, RL19, FOXK1, RBM10, CYC, CLH1, SPTB2, SET, FOXK2, CAP1, OTUD4, EWS, SP3, RL18A, FKBP4, RL6, KMT2A, IF4G1, TLE4, 1433F, SRS11, EF1A2, GFPT1, EXOS9, SUH, GABPA, PRDX1, RL18, SRSF1, SSRP1, RBBP4, EP300, AP1B1, SFSWA, FOXC1, ACACA, CSN1, AIMP2, PSMD2, G3BP1, PABP4, EIF3I, SF3B2, PICAL, ULA1, CUL4B, FHL1, NACA, SPTN1, NFYC, CKAP5, EIF3A, UBP2L, TTL12, DYHC1, RCN2, CAPR1, RBM39, PUM1, EPN4, NCOA6, GSE1, MEF2D, ZN638, IMB1, NOLC1, NUMA1, PSMD6, SEPT2, R3HD1, BRD3, PA1B3, IPYR, TEBP, RCN1, PCBP1, PCBP2, SC23A, SF3A1, NCOA2, SF01, MED1, JHD2C, ELF2, TAB1, TBCE, VAS1, ZYX, SEPT7, ADRM1, CCDC6, PKN2, DDB1, CDC37, NRF1, FSCN1, RFX7, QSER1, QRIC1, TBB8, LARP7, TB10B, AMOT, TGO1, PRC2B, UBAP2, QNG1, RBM26, RPRD2, TASO2, TSH3, ARID2, LIN54, EDC4, SCYL2, NFRKB, ZC3HE, FIP1, MCAF1, BCOR, UBN2, LARP4, SPT6H, SND1, DDX46, CYFP1, KDM3B, ZCCHV, NUFP2, PLGT3, RAI1, RBBP6, SH3R1, HUWE1, YTHD3, CENPV, KAISO, KTN1, CAND1, RTTN, CARM1, PRSR1, P66A, SPA12, Z3H7A, ANKH1, SUGP1, CCAR1, PHC2, SMAP1, PHAR4, DCP1B, FNBP4, CPSF7, ARFG1, ENAH, SUMF2, PGLT1, SERB1, LS14A, TNR6A, ABCF1, NEDD1, WDR36, SMRC2, PO210, PDC6I, ATX2L, P66B, DDX1, SMG7, MAML1, HS105, LAR4B, GCN1, AN32B, TFG, CBP, RENT1, SMRC1, FUBP2, TNPO1, USP9X, NCLN, FERM2, FKB10, P5CR2, ISOC1, NMD3, EDC3, OTUB1, PDLI5, FUBP3, ZC3HA, EP400, PRRC1, RBM14, VPS35, CIC, MED15, SEC62, PSMD1, PARK7, EYA3, VAT1, SCAFB, EIF3C, ATX2, TS101, TCPH, ANM1, RNZ2, TBA1C, CNPY3, WAC, DIDO1, AN32E, TBB6, HNRL1, TBB2B, GNL3, THIC, RBM4, NAA15, YTHD1, WNK3, UNK, UBA5, BRD8, LMA2L, FOXP1, NELFA, PTN23, WNK1, AMPB, RPF2, GORS2, LRC40, MLXIP, MYG1, RISC, CYBP, RC3H2, TAF9B, NCOA5, CHD8, CELR2, DCP1A, PDLI7, SAR1A, SHLB2, MBNL1, SALL1, SYFB, PDS5B, OLA1, RBM12, DD19A, FANCI, LYAR, CARF, TAB2, UGGG1, CDK12, IF2B1, ITSN2, BICRA, CNOT2, RCC2, SYLC, RBM27, KANL3, ATX10, SAE1, SAE2, SUN2, SRP68, CHRD1, UBQL2, S30BP, PUF60, DACH1, SIX4, HOOK1, MRT4, NUP50, MRTFB, ZMIZ1, YETS2, HECD1, MYO6, PRP19, UBQL1, G3BP2, MAGD2, CSN3, SCAF8, TRI33, SRRM2, PA2G4, RUVB2, EIF3L, DRG1, OFUT2, E41L3, R3HD2, RRP44, NOP58, ZN281, LC7L2, SBDS, STRAP, RTCB, SALL2, TLN1, ARIP4, HYOU1, KLF12, ARI1, PRC2C, YTHD2, SP16H, SERC, GMEB1, ZHX2, S23IP
Species: Homo sapiens
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Liu J, Hao Y, Wang C, Jin Y, Yang Y, Gu J, Chen X. An Optimized Isotopic Photocleavable Tagging Strategy for Site-Specific and Quantitative Profiling of Protein O-GlcNAcylation in Colorectal Cancer Metastasis. ACS chemical biology 2022 17(3) 35254053
Abstract:
O-linked-β-N-acetylglucosamine (O-GlcNAc) glycosylation is a ubiquitous protein post-translational modification of the emerging importance in metazoans. Of the thousands of O-GlcNAcylated proteins identified, many carry multiple modification sites with varied stoichiometry. To better match the scale of O-GlcNAc sites and their dynamic nature, we herein report an optimized strategy, termed isotopic photocleavable tagging for O-GlcNAc profiling (isoPTOP), which enables quantitative and site-specific profiling of O-GlcNAcylation with excellent specificity and sensitivity. In HeLa cells, ∼1500 O-GlcNAcylation sites were identified with the optimized procedures, which led to quantification of ∼1000 O-GlcNAcylation sites with isoPTOP. Furthermore, we apply isoPTOP to probe the O-GlcNAcylation dynamics in a pair of colorectal cancer (CRC) cell lines, SW480 and SW620 cells, which represent primary carcinoma and metastatic cells, representatively. The stoichiometric differences of 625 O-GlcNAcylation sites are quantified. Of these quantified sites, many occur on important regulators involved in tumor progression and metastasis. Our results provide a valuable database for understanding the functional role of O-GlcNAc in CRC. IsoPTOP should be applicable for investigating O-GlcNAcylation dynamics in various pathophysiological processes.
O-GlcNAc proteins:
A0A0B4J203, A0A0C4DFX4, RBM47, E2F8, WDR27, SBNO1, CNOT1, P121B, P121C, H0YAE9, H0YHG0, H7C469, K7ELQ4, M0QZ24, PDLI1, HAX1, TAF4, BCL9, CAC1A, DDX3X, NFIB, PPP6, MA2B1, ARI1A, SOCS7, ABLM1, KMT2D, GBRD, RGRF2, TX1B3, HGS, MYPT1, SYN3, ZN609, TRI66, PDZD2, MAST4, SC16A, SET1A, CASC3, FOXP2, MOT4, P4HA2, ARPC5, CLOCK, MAFG, PER1, KDM6A, TET3, SI1L1, TGFI1, M3K7, MCA3, PRPF3, TPD54, SYNJ1, IF4G3, E41L2, WIPF1, FOXO3, TGM5, RNF13, SPY2, PLRG1, ZN207, AKAP8, CALU, ORC5, MYPT2, GANP, OGA, CCNT1, BUB1B, PLOD3, PLIN3, MOT2, MAFK, PQBP1, BRD4, TBL1X, PP1RB, NBN, MITF, SRGP2, N4BP1, ROCK2, PP6R2, CNOT3, ANR17, FLNB, NCOR1, SF3B1, REM1, CREG1, CRTAP, SYUG, CYTF, TOX4, TOX, SUN1, PCF11, AGFG2, UBE4B, CAC1H, SVIL, SC24A, SC24B, CNOT4, EYA4, ZMYM6, BAG3, LATS1, DDAH2, TXD12, ONEC2, CLPT1, ABL1, CRYAB, LMNA, TFR1, CATA, GBA1, FUCO, ALDOA, GCR, G3P, CPNS1, HSPB1, RLA2, RLA0, ITB1, K1C18, NPM, CATL1, CATB, MCR, BGLR, ITA5, NFIC, VIME, SNRPA, FGR, ATX1L, DERPC, ZN865, GLI2, MYBB, CLUS, PPAL, MPRI, PABP1, TPR, BMP3, SKIL, ENPL, PO2F1, PLAK, ATF2, ZEP1, RS2, TFE2, F261, ITB4, ZNF23, ZNF25, JUNB, ATF7, TPH1, DDX5, EGR1, SON, NELFE, ATF1, ATF6A, CADH2, ICAL, CSRP1, FLNA, RFX1, CBL, SFPQ, COF1, IF4B, GATA2, APC, DDX6, ARNT, MAP4, LYOX, HXD9, MZF1, CLIP1, 5HT1F, HXA11, ZEP2, ELF1, CTNB1, FBN1, ADDA, BASI, NU214, VGFR2, SRP14, NUP62, SYUA, VATA, CUX1, TXLNA, STAT3, LAP2A, EPS15, HELZ, MATR3, SSRA, SSRB, KI67, ATRX, MAP1B, YAP1, UTRN, STT3A, SC6A8, RFX5, SOX2, PRC2A, HSP13, NR2C2, NASP, CDK8, DHE4, YLPM1, NU153, RBP2, TAF6, MRE11, EMD, MXI1, MAP2, TOB1, PPT1, TCPQ, PAPOA, GDS1, AGFG1, CRIP2, NUP98, SMTN, SC24C, HIRA, ATX1, ATN1, AFAD, AF10, AF17, DSRAD, SEC13, NU107, ZN445, CSN2, RL37, WDR5, TIM10, F193A, RBM6, PITX1, IF4G2, PHC1, ADA17, KGD4, RL19, FOXK1, DAB2, RHG04, RBM10, HNRPU, SPTB2, FOXK2, RUNX1, MEF2A, SP2, SP3, PLOD1, KMT2A, TF65, IF4G1, NOTC2, TLE4, PTN12, CALD1, MEF2C, P5F1B, GABPA, ZO1, ACK1, EP300, AHNK, FCHO2, HMGX3, SRBP2, FOXO1, ASPH, TROAP, BPTF, FSTL1, NFIA, DPYD, TP53B, FOXC1, ECH1, ROA0, DDX10, TBX2, GPS2, G3BP1, PABP4, ADAM9, PICAL, NAB1, SERC3, RIPK1, IQGA2, STIM1, CUL4B, ASPP2, CAC1S, RUNX2, NFYC, CDK13, TOB2, VEZF1, UBP2L, GIT2, SRC8, CAPR1, LAGE3, PUM1, MDC1, EPN4, TTLL4, RRP1B, NCOA6, GSE1, MEF2D, LASP1, MYPC3, ZN638, NUMA1, SART3, CND1, R3HD1, KIF14, WDR43, PLCL1, PLEC, NOMO1, NONO, RCN1, RYR3, KS6A1, RBMS2, TAF1C, SF01, MED1, JHD2C, TRIP6, T22D1, ELF2, TAB1, HERC1, NCOA1, VAS1, ZFHX3, ZYX, ADRM1, SYPL1, TAF9, DREB, DGKD, CGT, GEN, LY6K, RFX7, QSER1, AAK1, PRSR3, QRIC1, MA7D1, WDR72, TBRG1, TB10B, TPRN, FIL1L, SVEP1, AMOT, EPC2, CRTC2, PAN3, HS904, YIF1B, AG10A, IGS11, ZN628, BCORL, FIGN, BRD10, SH319, TGO1, PRC2B, TOIP1, CEP78, P4R3B, HP1B3, CE170, ZN362, FKB15, AKND1, ZEP3, LRIF1, SWT1, RHG21, UBAP2, RBM26, DEP1A, OGRL1, AHDC1, F222A, RPRD2, RN220, ZN318, TASO2, ZMYM4, PAPD7, TENS2, KANK2, ARID2, USF3, RHG17, CYTSA, ANR40, BICRL, JADE1, PKHA7, NIPBL, LIN54, TET2, RINT1, CRCDL, ZNT6, TTC41, RHGBA, NFRKB, RSBNL, KCD18, NCEH1, MDEAS, ZC3HE, LARP1, NHS, CRTC3, SAS6, MCAF1, BCOR, MPRIP, DNMBP, GGYF2, THADA, BNC2, NFXL1, NBEL2, CO039, SRCAP, CBAR2, UBN2, XIRP1, RAPH1, LARP4, HAKAI, ASXL2, SPT6H, KDM3B, ZCCHV, KANL1, RGPD4, POGZ, ZFY16, NUFP2, MAVS, CLAP1, EMSY, I2BP2, SRGP1, RBBP6, SH3R1, HUWE1, YTHD3, NPM2, ILDR1, KAISO, MYPN, LDB1, LYRIC, BCL9L, LUZP1, NRAP, RTTN, PRSR1, DDX42, CEP57, CD20B, CACL1, P66A, HIPK1, KCC1D, RN135, MY18B, AHNK2, FOXP4, NAV3, NAV2, MISP, ARI3B, IPRI, TEX2, MGAP, CC28A, Z3H7A, ANKH1, SUGP1, RPAP2, MILK2, SRRM1, ZZZ3, GAR4, PHAR4, RTKN2, DCP1B, XRN1, PELP1, CKLF8, TENS4, SPART, RPTOR, NUP93, ZN687, DOCK4, RHG24, RUSC2, SYNPO, FNBP4, D2HDH, RP25L, ATPF2, CPSF7, ARFG1, ENAH, SPOT1, SUMF1, KCNH5, SLAI1, TNR6A, PHC3, DRC6, CBPC3, NAV1, VP37A, KMT2C, ZMIZ2, BD1L1, ARI1B, FLCN, NUP35, TOIP2, TNIP2, KNL1, OR2L2, PUM2, CC110, TBC15, STT3B, ZN507, ALMS1, DLG5, KCNV2, BRX1, DOT1L, GEMI5, PARD3, ZN384, SMAP2, IASPP, TM263, ZFN2B, NUDC2, PCNP, TRUB1, LMO7, ATX2L, PALLD, P66B, BBX, ZCH14, GBF1, SMG7, RTF1, NICA, PHF3, MAML1, ZN592, LAR4B, TFG, TAF4B, RREB1, SC65, CBP, SYMPK, DDX17, GPKOW, FUBP2, UBP7, LPP, LSM10, NCLN, MRTFA, FUBP1, TTC17, PBIP1, TTC28, TOM6, PF21A, INT12, REPS1, ESS2, MBD6, ELP4, SGF29, RBM33, ZN503, P121A, TONSL, PDLI5, ERO1A, DOCK6, FUBP3, RSRC1, ZN594, VCIP1, ZN462, LCOR, PDLI2, CLP1L, Z512B, ZFR, EP400, MRFL, H6ST2, TIGD1, NOL4L, DOCK7, RPR1A, RBM14, ADCYA, QKI, LENG8, TRNT1, PP1RA, PHF12, CIC, MED15, ERBIN, HMCN1, LMF1, PIGS, WRIP1, SIN3A, MINT, HTF4, EYA3, POP1, TEAD3, TTC1, CSN8, ATX2, ARI3A, ANM1, PKP2, TEP1, DPH2, WAC, DIDO1, HNRL1, RBM4, SSBP4, PRR14, SSBP3, YTHD1, KPCD2, ZCHC2, TB182, AMRA1, CE295, TANC1, ZC12C, CEP44, STRAB, SP130, BRD8, RGAP1, SMG9, APC1, I2BPL, TMX4, KI13A, WDR13, EPC1, ADNP, ZN106, TM245, FOXP1, PABP3, WNK1, E41L1, ZHX3, BICC1, PEAK1, PPR3E, ZN703, PKHA5, CLSPN, BCDO1, RC3H2, ZFYV1, TAF9B, EMAL4, ZBT20, NCOA5, TANC2, ZN532, NCK5L, TNR6C, CHD8, FBSL, APMAP, DMAP1, UBN1, DCP1A, INCE, ANLN, GEPH, PDLI7, TULP4, HOME2, SLX9, DIAP3, BMP2K, RBM12, STAU2, DDX28, CWC25, CARF, ETAA1, ABI2, HXC10, BCLF1, TAB2, CELR3, CDK12, GRHL1, SACS, ITSN2, BICRA, CNOT2, TMEM9, CAC1I, CAMP3, DAPLE, RCC2, DIP2B, MBD5, CT2NL, F135A, KANL3, RERE, SE1L1, TRM7, YM012, KDM5B, LIMD1, TCF20, SUN2, LIMA1, SEPT9, UBQL2, TRPS1, S30BP, NRBP, BAZ2B, SIX4, HOOK1, CDC23, TASOR, GMEB2, TNIK, PARP4, NUP50, ZHX1, CDV3, MCTS1, KCNH3, LRFN2, MRTFB, ZBT21, PRR12, YETS2, HECD1, ZMYD8, NOTC3, SPAT2, SOX13, G3BP2, MAGD2, MINP1, MACF1, CP131, SCAF8, TRI33, PHF8, LIMC1, TNR6B, SRRM2, SCML2, ZN148, POLH, INVS, ICE1, R3HD2, MAN1, TR150, WBP11, ZN281, STA13, WNK2, ARIP4, MTCL1, DCAF1, RPGF2, IRS2, CRBG1, HYOU1, SAM50, PRC2C, YTHD2, NCOR2, GMEB1, DC1L1, EPN1, NCOA3, ZHX2, S23IP, U3KPZ7, V9GYH0
Species: Homo sapiens
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Chen Y, Tang F, Qin H, Yue X, Nie Y, Huang W, Ye M. Endo-M Mediated Chemoenzymatic Approach Enables Reversible Glycopeptide Labeling for O-GlcNAcylation Analysis. Angewandte Chemie (International ed. in English) 2022 61(23) 35289036
Abstract:
To selectively enrich O-linked β-N-acetylglucosamine (O-GlcNAc) peptides in their original form from complex samples, we report the first reversible chemoenzymatic labeling approach for proteomic analysis. In this strategy, the O-GlcNAc moieties are ligated with long N-glycans using an Endo-M mutant, which enables the enrichment of the labeled glycopeptides by hydrophilic interaction liquid chromatography (HILIC). The attached glycans on the enriched glycopeptides are removed by wild-type Endo-M/S to restore the O-GlcNAc moiety. Compared with classic chemoenzymatic labeling, this approach enables the tag-free identification, and eliminates the interference of bulky tags in glycopeptide detection. This approach presents a unique avenue for the proteome-wide analysis of protein O-GlcNAcylation to promote its mechanism research.
O-GlcNAc proteins:
TM271, HEAT9, SBNO1, P121B, GGT3, TAF4, AGRIN, MEIS1, RNT2, NFIB, MA2B1, CDKA1, ABLM1, ADA10, KMT2D, MYPT1, ZN609, SC16A, PLXB2, SET1A, VA0E1, TNC18, TLR3, TET3, PRPF3, IF4G3, ZN207, AKAP8, CALU, EXTL3, PCDH7, TRAK2, GANP, TSN3, MAFK, KERA, SRGP2, ANR17, NCOR1, U520, CRTAP, ATRN, CBPD, RMP, TOX4, SC24D, SRBS2, SUN1, ERLN2, PCF11, SCAF4, VAPB, SMC2, SC24B, CNOT4, EGFR, HPT, GLHA, LMNA, NU3M, VTNC, GCR, A1BG, K2C1, HSPB1, RPN1, AT1B1, K1C18, K2C8, ITAV, GDN, TRY1, SAP, MET, NFIC, VIME, K2C7, SNRPA, UCRIL, ATX1L, NT2NC, LYAG, LAMC1, PPAL, LAMP1, MPRI, TPR, SKIL, T2FB, GLU2B, NID1, PO2F1, MCP, ZEP1, CD36, ATF7, EGR1, SON, ATF1, ICAL, CO5A1, ASPG, SFPQ, ITA3, NKG2A, ARNT, TEAD1, 3MG, TKT, UFO, HXA11, HXC9, ZEP2, HNRH1, ELF1, CD68, RFC1, FBN1, NU214, RL4, SCNNA, SRP14, NUP62, TAGL2, CUX1, IL6RB, PBX2, STAT3, NBL1, LAP2A, LAP2B, LIFR, PCP, ECE1, MUC18, MATR3, SSRB, VDAC2, ATRX, NOTC1, UTRN, RFX5, HSP13, CCN3, AGRE5, NR2C2, CDK8, CENPF, YLPM1, RBM25, NU153, RBP2, TAF6, EMD, PPT1, SMCA4, AGFG1, NUP98, PTTG, ATX1, AT1B3, AF17, DSRAD, LAMB2, CAD13, ITA1, NU107, TGFB2, ACTG, CXAR, PITX1, CNTP1, ABCA4, PHC1, ADA17, KGD4, SARNP, FOXK1, DAB2, HNRPU, SPTB2, FOXK2, MEF2A, SP3, PLOD1, KMT2A, UPAR, IF4G1, NOTC2, SRS11, SUH, MFGM, AHNK, TMM62, GALT1, BST2, SIA4C, ASPH, BPTF, NFIA, FOXC1, ADAM9, NFAC2, MAMD1, NAB1, TBB3, PKD2, LAMB3, KLF5, NFYC, CDK13, SCRB2, LRP8, VEZF1, UBP2L, LAGE3, MDC1, RRP1B, MEF2D, ARI5B, NUMA1, PON2, RCN1, TAF1C, SF01, MED1, JHD2C, ELF2, TAB1, ZFHX3, ZYX, ADRM1, LAMA4, TAF9, FOXD1, LAMA3, RFX7, QSER1, SVEP1, SYTL3, EPC2, LUZP6, CRTC2, YIF1B, BCORL, BRD10, PRC2B, ZN362, LRIF1, UBAP2, RBM26, VP13D, RPRD2, RN220, ZN318, TASO2, ECM29, ARID2, SE1L3, BICRL, SCAR3, NIPBL, LIN54, FSTL4, TET2, ZNT6, GOLM2, NFRKB, S39A4, ZC3HE, FIP1, CRTC3, PLGT2, SUSD1, MCAF1, BCOR, IGS10, B3GLT, CD109, FRRS1, SRCAP, NBEL1, UBN2, RAPH1, HAKAI, ASXL2, SPT6H, KDM3B, NRK, NUP54, POGZ, MAVS, PK1L3, PLGT3, EMSY, RAI1, YTHD3, LDB1, LYRIC, OSTM1, PRSR1, DDX42, P66A, FOXP4, CTL2, TEX2, MGAP, ANKH1, SUGP1, NUP93, PLD6, FNBP4, ARFG1, PMGT2, GOLM1, PGLT1, TM87A, FSAF1, PHC3, SP20H, ARI1B, NUP35, OR6C4, VA0E2, PLBL2, PUM2, SPP2B, DLG5, GPX8, PO210, ZN384, LMO7, MUC16, P66B, BBX, SMG7, NICA, TM131, PHF3, TAF4B, GGH, GSLG1, FUBP2, LPP, NCLN, TTC17, FKB10, TOM6, PF21A, RBM33, I17RA, P121A, PDLI5, CREL1, FUBP3, TXD15, LOXL4, VCIP1, CHAP1, Z512B, ZFR, EP400, HUTU, RBM14, KI20B, PHF12, PANX1, CIC, MED15, ERBIN, JMJD8, MINT, TEAD3, SEM3C, WAC, DIDO1, HNRL1, TM109, NUP58, M4A8, YTHD1, ULBP3, AMRA1, TANC1, TWSG1, S22A4, SP130, APC1, I2BPL, WNT5B, VP33B, EPC1, ADNP, ZN106, FOXP1, PTN23, WNK1, SIA7D, ZHX3, PIEZ2, SG196, TM231, PEAK1, DOCK5, CF155, CNO10, MLXIP, SIAE, PKHA5, RC3H2, TAF9B, ZBT20, NCOA5, TANC2, ZN532, CELR2, APMAP, ABCB9, CHSTB, UBN1, NECT3, PDLI7, RBM12, OCAD1, CARF, ETAA1, HXC10, TAB2, CELR1, CDK12, CNOT2, CRIM1, TMEM9, RCC2, CHD7, RBM27, KANL3, MRC2, SUCO, TCF20, SUN2, UBQL2, LCAP, GGT7, TASOR, GMEB2, ZHX1, DSE, WWC3, MRTFB, ZBT21, PRR12, YETS2, NOTC3, KMT2B, PRP19, MINP1, SCAF8, ZC3H4, SRRM2, SCML2, UST, ICE1, ZN281, DAAM1, IRS2, PRC2C, NCOR2, NPTN, GMEB1, POMT1, S4A7, S23IP
Species: Homo sapiens
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Xie X, Wu Q, Zhang K, Liu Y, Zhang N, Chen Q, Wang L, Li W, Zhang J, Liu Y. O-GlcNAc modification regulates MTA1 transcriptional activity during breast cancer cell genotoxic adaptation. Biochimica et biophysica acta. General subjects 2021 1865(8) 34019948
Abstract:
Chromatin modifier metastasis-associated protein 1 (MTA1), closely associated with tumor angiogenesis in breast cancer, plays an important role in gene expression and cancer cell behavior. Recently, an association between O-GlcNAc transferase (OGT) and MTA1 was identified by mass spectroscopy. However, the potential relationship between MTA1 and O-GlcNAc modification has not yet explored.
O-GlcNAc proteins:
MED19, SBNO1, PGP, DPRX, SMHD1, RGPD3, ZSWM8, P121C, VGLL3, MCRI1, CK098, KIF2A, DX39A, PDLI1, BACH, MYO1C, MYO1F, AIP, SMAP, AP3B1, PSD11, PSD12, PSMD9, SPT5H, TAF4, DFFA, CLIC1, EIF3F, MATN2, LORF2, IPO5, SAP18, IF2B3, DNM1L, RTCA, AGRIN, PLOD2, HMGN4, IMA4, BCL9, PESC, NOP56, DDX3X, PODXL, CCN1, IMA3, NFIB, MA2B1, PDXK, ARI1A, TXND9, G3PT, CTRO, COPE, AP3D1, PDCD5, NHRF1, TPP1, TCRG1, TNPO2, PSA7, GIPC1, HAT1, HGS, MYPT1, HNRDL, XPO1, ZN609, SPTN2, SC16A, PLXB2, SR140, SET1A, LSM1, NPC1, ARC1B, ARPC2, ARPC3, TIF1A, PGRC2, PFD6, NKRF, LAMA5, ZN185, CASC3, OGT1, PMM2, HMGB3, PPM1G, FANCA, EIF3D, EIF3H, HDAC3, IPO8, STX7, NUP42, CLOCK, KDM6A, DHX15, MCES, FLRT2, PRP4, SERA, DC1L2, PSMD3, RFOX2, PAPS1, ZW10, SNUT1, SPIT2, TGFI1, M3K7, MCA3, HNRPR, PRPF3, TPD54, COCH, IF4G3, PPIH, ARK72, E41L2, TGON2, S26A4, FOXO3, DENR, XPOT, PLRG1, RGS10, ZN207, GET3, BUB3, ACTN4, BUD23, HTSF1, AP1G1, SYNC, KRT86, CPSF5, LANC1, AKAP8, CALU, RAD21, DHX16, MED14, SMCA5, JIP4, ZC3H1, TRAK2, AQR, GANP, KDM1A, GSDME, EVI5, SNX3, OGA, HNRPQ, CCNT1, PLOD3, AP180, PLIN3, MAFK, IMA7, UGDH, CTND1, SNX2, USO1, CCD22, PQBP1, DKC1, IF2P, EDF1, DNJA2, BRD4, PFD1, NBN, MCE1, WDR1, CPNE3, BRE1B, ZC11A, CLU, T22D2, PP6R2, CNOT3, CREST, ANR17, ZPR1, DUS11, PDCD6, TBCA, VATG1, H2AY, FLNB, NCOR1, SPAG7, SC22B, DEAF1, PR40A, VP26A, SAP30, MED24, KTNA1, PSIP1, SRS10, BAF, SF3B1, CSDE1, PRKRA, MED6, NPM3, LYPA1, U520, NU155, WDHD1, CRTAP, EIF3G, STAM2, CCNK, PRAF3, PIAS1, PIAS2, SPF27, DNJC8, SPF30, MPDZ, GLRX3, KRT36, RL1D1, CIAO1, SRP72, DDAH1, RECQ4, MTA2, MYO1D, TOX4, SC24D, PHF14, UBXN7, SUN1, PLPHP, ERLN2, PRP6, PCF11, NFAT5, HAUS5, AP2A2, SC31A, HEXI1, SEM3D, UBR5, AGFG2, SCAF4, ZFPL1, EPN2, ZRAB2, LC7L3, KAT7, MPZL1, FKBP9, CELF2, PAPS2, SMC2, LYPA2, IPO7, AGM1, CD2B2, BAG4, AHSA1, PSMG1, SC24A, SC24B, AGRL2, ACSL3, PCNT, CNOT4, CPSF4, EYA4, K2C75, SNP29, OXSR1, HS74L, PTBP3, AP2A1, STAU1, CAVN2, BAG2, M4K4, BPNT1, MBD3, CLPT1, ACL6A, CYB5, ADH1B, ADH1G, LDHA, DHE3, NB5R3, GSHR, SODC, PNPH, HPRT, AATM, EGFR, PGK1, KAD1, LALBA, FA10, TRYP, ASSY, A2MG, LDLR, HLAH, HBA, CO1A1, K1C14, K2C6A, LMNA, CASA1, CASA2, CASB, CASK, FINC, LACB, ALBU, ALBU, TFR1, GBA1, ALDOA, CYTB, ANXA1, GCR, PRIO, KITH, K2C6B, K2C1, G3P, CPNS1, HSPB1, RPN1, RPN2, GNAI2, AT1B1, ALDOB, A4, ARGI1, S10A8, HMGN1, ISG15, IF2A, HMGN2, ICAM1, RLA1, RLA2, JUN, LA, ITB1, K1C18, K2C8, MYL1, GELS, PTMA, CDK1, ATPB, S10A6, IF4E, ENOA, PYGL, G6PI, DPOLB, NPM, ITAV, LIPL, HEXA, ACBP, FABPL, LDHB, PDIA1, H10, CATD, ANXA2, CAN1, TBB5, TRY1, SAP, HEXB, PROF1, APT, K2C4, SYEP, CATB, HS90A, HNRPC, LAMB1, TPM2, FUMH, TSP1, SP1, ANXA6, DAF, MDR1, 4F2, HS90B, ASNS, ADH4, HEM3, RU2B, MET, RU17, ITA5, NFIC, VIME, RS17, K2C7, K1C13, ANXA5, K1C16, RSSA, CD63, SNRPA, GSTP1, RU1C, LEG1, HMGB1, CLCA, ROA1, RU2A, PARP1, UCHL1, LKHA4, ALDOC, CC175, ATX1L, ZN865, CT45A, HS71B, CALM3, RO60, H14, PTPRF, THIO, PPGB, KAP0, HEM4, ESTD, CH60, BIP, LAMC1, PPAL, HSP7C, GTR1, PYGB, LAMP1, TOP1, TOP2A, G6PD, C1TC, MPRI, ADHX, SRF, PABP1, PCNA, HARS1, IMDH2, TPR, KCRB, ANXA3, ACTN1, XRCC6, XRCC5, LAMP2, RINI, MYH6, ICAM2, AT1A3, EF2, K1C10, K2C5, PDIA4, TCTP, PLST, GYS1, T2FB, CD59, MIF, GLU2B, FPPS, TRI27, AK1A1, KPYM, ENPL, CCNB1, PO2F1, HNRPL, SYDC, ETS1, PLAK, ALDR, AMPN, PVR, ERF3A, EZRI, ATF2, FOSL1, FOSL2, MCP, NQO1, GNS, ZEP1, RS2, TFE2, DESP, RFA2, CD44, ITB4, CBR1, CREB1, BGAL, H15, H13, H12, AT2A2, STMN1, YBOX3, HSP76, HMGA1, JUNB, UBF1, JUND, ATF7, CAN2, PTN2, PYRG1, DDX5, PFKAL, LEG3, PRS6A, TCPA, PTN1, ARF4, RL7, VINC, SON, NELFE, RL17, PGAM1, RCC1, ATF1, XRCC1, CADH2, ML12A, NUCL, HXK1, RO52, SPEE, SL9A1, CSK22, RXRA, NFKB1, IF2B, ANXA7, TBP, BTF3, PSB1, MPRD, LMNB1, ICAL, CD11B, VATC1, CSRP1, FLNA, 5NTD, TAF1, CD9, TGM2, PIMT, FBRL, PUR2, PUR6, UBA1, NDKB, ROA2, RFX1, CBL, EST1, FBLN1, TCEA1, ITA6, SFPQ, PPIB, SYWC, RS3, NFYA, SAHH, COF1, IF4B, KTHY, CCND1, COT2, EF1B, PPAC, RPB1, CDK2, MCM3, NFYB, THTM, LAMA1, RS12, BRD2, TYY1, DNJB1, ATPA, PSA1, PSA3, PSA4, ITA3, MOES, DDX6, CTNA2, DNMT1, PAX6, U2AF2, RL13, HMGB2, PTBP1, SYTC, SYVC, EF1G, 1433T, ARNT, RL10, RFA1, APEX1, PYR1, CALR, MAP4, CALX, PSA5, DPOD1, MK01, RXRB, GRN, PTPRM, T2EA, CCN2, EPHA2, 3MG, KDM5A, TKT, RBMS1, PML, EF1D, ERP29, PRDX6, BLVRB, PRDX5, RL12, KCY, PEBP1, PDIA3, 2AAA, 2AAB, NMT1, HMOX2, PURA2, UFO, PUR8, CLIP1, SORCN, ILEU, RPB2, SDHA, METK2, CPSM, TIA1, ZEP2, DNJA1, AKT1, PUR9, HNRH3, HNRH1, 1433B, 1433S, STIP1, S10AB, L1CAM, PRDX2, OTX1, CDD, ELF1, RL9, KINH, CSTF2, DUT, TTK, MCM4, MCM5, MCM7, HSP74, GPC1, PROF2, CTNA1, CTNB1, PCGF2, SPB6, RADI, RFA3, RFC4, RFC2, RFC1, RL22, T2FA, SPRE, HXD13, CBS, K1C9, FBN2, GDE, MYH9, MYH10, COPB2, BASI, FUS, NU214, DEK, K22E, RL4, PP1G, GNL1, SRBP1, SRP14, NUP62, TAGL2, TALDO, RBMX, COIL, VKGC, HSPA9, IF4A3, RS19, RL3, COIA1, OST48, AN32A, FEN1, CAPG, IL6RB, TXLNA, TCPZ, NNMT, PBX2, RL13A, STAT3, MDHC, MDHM, RFC5, IF2G, CETN2, BUD31, NAA10, CSK, GARS, SYIC, EIF1, KPCI, LAP2A, LAP2B, MTREX, RS27, HELZ, RL35, CDN2A, PCP, ECE1, LIS1, MUC18, MATR3, MSH2, SSRA, RANG, NAMPT, PRS6B, NKX21, VDAC2, CBX5, UBP5, KI67, RAGP1, RECQ1, NOP2, CRK, CRKL, BAG6, NSF, NOTC1, MP2K3, RL27A, RL5, RL21, RL28, RS9, RS5, RS10, MAP1B, GNPI1, YAP1, UTRN, IQGA1, STT3A, CAPZB, IF1AX, SYQ, RL29, LIMS1, PPCE, RFX2, RFX5, SOX9, COPD, GSH0, PSMD8, PRC2A, TCPE, NEST, HSP13, KC1A, PIPNB, AGRE5, DPOD2, PAXI, RL34, NASP, FAS, CDK8, TCPG, EFTU, SRP09, PCY1A, SYAC, SYCC, SYSC, PRI2, CTCF, PSB2, MCM2, TSP3, YLPM1, TMEDA, RBM25, NUMB, HINT1, NU153, RBP2, GSK3A, GSK3B, TAF6, SPS1, GUAA, DNLI3, MRE11, CRIP1, GDIB, EMD, SERPH, F10A1, VASP, DYN2, CDK9, BCAM, PPT1, RL14, TCPQ, TCPD, ANX11, PAPOA, FXR1, FXR2, RAB5C, RAB7A, DUS3, SMCA4, GALK1, SSRD, UBP11, NR0B1, HDGF, ROA3, 6PGD, HNRPM, IMA1, IMA5, GDIR1, AGFG1, HNRPF, TF2AA, MSH6, ZN131, ZN143, RBM5, SPSY, EFNB2, CAZA1, CRIP2, NUP98, PPP5, ACLY, MAP11, COPB, COPA, CATC, AP2S1, PTTG, SMTN, IST1, SC24C, TCP4, ICLN, SYRC, ATX1, ATN1, SYYC, UBP14, HSP72, BCAT1, AT1B3, RD23B, PRRX1, HMCS2, SNAA, IF5, DRG2, XPO2, TERA, MFAP1, AF10, AF17, NP1L1, ADK, DSRAD, LAMB2, FOXG1, TPD52, SEC13, NH2L1, PSA, HNRH2, SUMO3, EIF3B, GFRA1, SYMC, IF6, CTBP2, TMM33, PCBP3, PCBP4, CORO7, NU107, MTPN, H2B1D, DEF3, ARPC4, SC61G, TPIS, EIF3E, SC61B, PP4C, MYL6, ACTB, IF4A1, RS20, PRPS1, PSA6, S10AA, CDC42, DEST, GMFB, RAB8A, SPCS3, RAB2A, RAB5B, RAB10, UBC12, UBE2N, ARP3, ARP2, ACTZ, CSN2, ABCE1, RS3A, RL26, PSME3, RL15, RL27, RL37A, RHOA, S61A1, LYSC, COPZ1, SUMO2, DCAF7, WDR5, NTF2, HNRPK, 1433G, RS7, PP1A, PP1B, PRS4, PRS8, RS8, RS15A, RS16, UB2G1, 1433E, RS14, RS23, RS18, RS29, RS13, RS11, RUXE, RUXF, RUXG, LSM3, LSM6, SMD1, SMD2, SMD3, TYB4, PRS10, RL7A, RB11A, ERF1, CNBP, RS4X, RL23A, RS6, H4, H2B1C, RAB1A, RAN, RL23, RAP1A, UB2D2, RS24, RS25, RS26, RS28, RS30, GBB1, RBX1, GBB2, RL30, RL31, RL10A, RL32, RL11, RL8, PPIA, FKB1A, RS27A, GRB2, TRA2B, RAC1, AP2B1, 1433Z, RSMN, SUMO1, DYL1, RL38, GBG5, RS21, IF5A1, RACK1, ACTG, SPT4H, UBC9, TYB10, PP2AA, YBOX1, CSK2B, TPM4, UB2L3, EF1A1, ACTS, TBA4A, TBB4B, CSK21, PA1B2, HBB, HBA, F193A, IGBP1, RBM6, IF4G2, RPP30, GTF2I, CNTP1, PHC1, TCPB, KRT85, RAE1L, PRKDC, MT1X, NUCB2, DCD, SSBP2, SARNP, RL24, CBX1, ARF1, ERH, RL19, SRSF3, FOXK1, DAB2, FBLN2, PGBM, RHG04, EFNB1, RBM10, RBM3, 2ABB, PIPNA, S25A3, VIGLN, TF2B, CDK5, CLH1, HSF1, FKBP3, DHSO, HNRPU, U2AF1, SPTB2, TIAR, SET, SRSF2, FOXK2, RUNX1, FABP5, CAP1, NC2B, TFAP4, EXOSX, OTUD4, PFKAP, EWS, TAGL, AK17A, MEF2A, KIF23, NRG1, DSG1, SP4, SP3, RL18A, MP2K1, FKBP4, PLOD1, NUCB1, RL6, TOP2B, DYST, CREM, KMT2A, LMNB2, TF65, UBXN1, GLGB, IF4G1, K1C17, NOTC2, TLE2, TLE4, LGUL, AK1C1, 1433F, CSTF1, PTN12, FAK1, SRS11, EF1A2, CALD1, PTN11, GFPT1, EXOS9, PSME1, SUH, GABPA, GABP1, RING1, PAX8, FMR1, PRDX1, RL18, CKAP4, ZO1, KHDR1, BAX, KLC1, LRP1, SRSF1, SRSF4, DHX9, GOGA2, LG3BP, CD47, PPID, SSRP1, NSUN2, RBBP4, EP300, AHNK, APOBR, HSP7E, MGAT2, GALT2, AP1B1, CPSF1, BST2, WASC5, NU160, SCAP, SRBP2, TBL3, ASPH, TROAP, TROP, SNF5, BPTF, CDC20, FSTL1, GRSF1, SFSWA, CHD3, SF3A3, TP53B, AIMP1, ILF2, ILF3, LMAN2, ELAV2, FOXC1, PP1R8, CSTF3, FLII, COASY, ACACA, CSN1, CAF1B, RED, MTAP, TADBP, ROA0, AIMP2, FADD, PRDX4, PAK2, CBX3, STK3, PSMD2, GPS2, SRSF9, SRSF5, SRSF6, TIF1B, G3BP1, CLN3, PTK7, PABP4, IFIT5, MTA1, EIF3I, 2A5G, CTBP1, UB2V1, DC1I2, ILK, MSLN, PPIG, TCOF, SF3B2, HAP28, ADAM9, FKBP5, SMAD4, PICAL, SQSTM, TBB3, ASAH1, PRP4K, PIN1, RIPK1, HDAC1, KCC2G, DCTN2, SNW1, STIM1, TRA2A, PWP1, CUL1, CUL2, CUL3, CUL4B, ASPP2, DYR1A, TPBG, FHL1, PM2PB, MOGS, CD166, NACA, THOC5, SPTN1, PKP1, DX39B, EXOS2, TBB2A, KLF5, BYST, IDI1, RUNX2, PEBB, NFYC, CDK13, CKAP5, CIRBP, COTL1, HNRPD, SCRB2, NID2, DAG1, VEZF1, DSG2, SAFB2, EIF3A, UBP2L, SCRIB, MLEC, TTL12, FHL2, DCTN1, DYHC1, EI2BA, IF4A2, SRC8, TRI25, FLNC, FA50A, MYPC2, GAMT, CAPR1, RBM39, KT33B, HLTF, PDIA5, DHX8, MCM6, ITPR3, MDC1, EPN4, SMC1A, RRP1B, NCOA6, GSE1, PSF1, UBP10, GANAB, 2A5D, LBR, GOGB1, MEF2D, CHD4, LASP1, NC2A, ZN638, IMB1, NOLC1, NUMA1, GAPD1, K2C72, NAA25, FL2D, SEPT2, SART3, U5S1, S39AE, SETB1, IF4H, BRD3, EEA1, PDIA6, PA1B3, PLEC, NOMO1, IPYR, TEBP, NECT1, NONO, PTPA, RBBP5, RCN1, K1H1, PCBP1, PCBP2, ELOC, SF3B3, DLGP5, RSU1, CNN3, SAFB1, SF3B4, SF3A2, RBMS2, SC23A, SC23B, SF3A1, SSXT, TAF5, TEAD4, TGIF1, NCOA2, NHRF2, TRAM1, SF01, TRIPB, PCH2, MED1, HMGN3, JHD2C, TRIP6, MARE1, ELAV1, ELF2, TAB1, AAAT, MLF2, TOM34, TBCE, UB2V2, STXB2, NEDD8, USF2, VAS1, VPS72, ZFHX3, ZYX, SEPT7, ADRM1, CCDC6, UAP1, AINX, PSMD5, CSRP2, DDB1, CDC37, DPYL2, RBBP7, TAF9, SRSF7, CPSF6, SMN, NRF1, FSCN1, IF16, GLO2, H2B2E, CGT, TRXR1, LY6K, HNRL2, Q1RMN8, PDS5A, QSER1, AAK1, WASC4, PRSR3, TSR1, QRIC1, SMU1, P3H1, MA7D1, CHD9, LSM12, GELS, A1AG, TBB8, GLYR1, FIL1L, AMOT, FA98B, EPC2, RHG29, FND3B, CRTC2, DHB12, GLE1, UBP39, LACB2, P5CR3, PKHG4, H90B2, R39L5, ZN326, FILA2, BCORL, FIGN, BRD10, AG10B, CC038, TGO1, PRC2B, RRP12, TOIP1, PCID2, SPXN3, SMAG2, BRM1L, TM201, NU188, HP1B3, CE170, ZN362, EYS, FKB15, DDX59, ZC3HD, LRIF1, UBR4, UBAP2, KPRP, KPLCE, RBM26, NT5D1, AHDC1, RPRD2, PR38B, BRE1A, ZN318, BROX, TASO2, ECM29, MBNL2, ZMYM4, K2C79, ARID2, USF3, C19L1, VIR, K1C40, HEAT6, BICRL, ATLA3, CARL2, CPIN1, TWF2, P4R3A, NIPBL, PDE12, LIN54, TET2, TM214, ARMC6, CAVN1, ERAP2, CDC73, TAF2, MED27, EDC4, PRP8, SCYL2, TTC27, GOLM2, NFRKB, MZT2A, CTR9, NCEH1, TRI65, MDEAS, BRAT1, ZC3HE, LARP1, BRWD3, SMRD3, FIP1, CRTC1, SAS6, CSPG4, CWC27, WDR82, ATL4, MCAF1, PACS1, MPRIP, GGYF2, CD109, CERS6, QSOX2, SRCAP, RIPR1, YJ005, UBN2, FGD6, PAXI1, RAPH1, IKIP, H32, LARP4, MED25, TBA1A, H2AV, HAKAI, ASXL2, CCD80, BT2A1, SPT6H, SND1, DDX46, 5MP2, RSRC2, CYFP1, KDM3B, OLIG3, PHF5A, ZCCHV, KANL1, NUP54, POGZ, MYH14, NUFP2, CLAP1, PLGT3, HEAT3, HDGR2, EMSY, RAI1, I2BP2, RBBP6, SH3R1, HUWE1, YTHD3, KHDC4, TMED4, CENPV, T179B, Q862S4, KAISO, PATL1, MYPN, PEG10, NOP9, PABP2, MTA70, LDB1, PB1, LYRIC, TLK2, ZN598, KTN1, BCL9L, DTX2, LUZP1, THOC4, GP180, PACS2, CAND1, TSYL5, THOC6, MET16, ZC3C1, CARM1, PRSR1, MEX3D, DDX42, DAAF5, P66A, HORN, RB6I2, RIOX2, RBM45, PLD3, NUDC3, AHNK2, FOXP4, TEX2, Z3H7A, PHF6, CHERP, ANKH1, SUGP1, CCAR1, SLF2, PHC2, BAP18, RB12B, RAVR1, SPB1, IHO1, SRRM1, SMAP1, P20D2, KATL2, PHAR4, TRM2A, DCP1B, NALCN, MAML2, PELP1, ABI1, PORIM, CCAR2, NUP93, ZN687, CMTR1, LRC47, K2C78, ABD12, PALS1, STAG2, FNBP4, TAB3, DPP10, CPSF7, ARFG1, EMC1, PAF1, UBR7, ENAH, KRI1, PR38A, F184A, KDM1B, NHLC2, GT251, PGLT1, DHB11, TXND5, SERB1, LEMD2, FA98A, RN214, LS14A, MISSL, TNR6A, PHC3, ABCF1, NGDN, SP20H, VP37A, KMT2C, ZMIZ2, ARI1B, NUP43, NUP37, NUP35, STXB6, KNL1, PLBL2, RLA0L, THOC2, WDR36, SMRC2, NPL4, PUM2, RDH11, STT3B, SPP2A, HM13, ALMS1, C99L2, MK15, BRX1, RBCC1, DOT1L, PO210, GEMI5, PARD3, IPO4, ZN384, K2C79, NOC3L, SCRB1, SMAP2, CCD12, TM263, NU133, PDC6I, GATD1, THEM6, CTF18, NUDC2, SCFD1, HNRLL, UBCP1, PCNP, LMO7, ATX2L, PHIP, PRP31, NELFB, PALLD, SREK1, PSPC1, P66B, DYH7, DNJC9, BBX, CTBL1, KAT6B, ELYS, ZCH14, AP2B, DDX1, H1X, PSMF1, SMG7, RTF1, NICA, TM131, ELMO1, BAP1, PHF3, MAML1, NDRG1, HS105, CNOT9, ZN592, LAR4B, GCN1, PRP16, NU205, AN32B, NECT2, PRCC, TFG, TAF4B, HDAC2, STAM1, REQU, CBP, KAT6A, SYMPK, RBP56, GGH, DDX17, RAD50, CELF1, OSTF1, UFD1, RENT1, CSN5, GPKOW, SMRC1, SMRD2, FUBP2, TNPO1, NEP1, GLMN, USP9X, UBP7, CUL5, STMN2, LPP, MED12, H2A1C, BHMT1, SMCE1, MYDGF, RL36L, PSMG2, NCLN, UTP4, PP14A, MGN2, FERM2, FUBP1, LRC59, FKB10, PF21A, PPWD1, INT12, FWCH2, KLH29, CC124, AP2M1, REPS1, SNR40, MBD6, RMXL1, SEH1, TCAL4, THA11, GNA1, T3HPD, DAZP1, SAAL1, SGF29, RBM33, TMA16, ZN503, DYL2, CPNE2, THOC1, OTUB1, HMCES, MED8, DUS3L, DCNL1, SMRD1, DDX27, GWL, LIN37, ZCCHL, P121A, PDLI5, ERO1A, C2AIL, MED30, INT4, FUBP3, SPF45, ABHEB, PAWR, THOC3, KIRR1, WNK4, COG3, TMX3, CHAP1, LCOR, PDLI2, ANCHR, ZC3HA, TOPK, SCYL1, EHMT2, ZFR, EP400, PRRC1, FXL18, CCD43, NOL4L, DACH2, NSUN5, RPR1A, IPO9, RBM14, QKI, ALS2, PP1RA, S38A2, VPS35, PURB, PHF12, XPO6, NACC1, CIC, MED15, MCCA, NUDC1, ERBIN, WRIP1, RANB9, MYADM, SRPK1, STRBP, TM209, IWS1, SIN3A, RSF1, RBM15, RUFY1, MINT, PNKP, MMS19, UHRF1, NIBA2, HTF4, TBCB, CNN2, CDC5L, PSMD1, PFD5, RING2, PARK7, EYA3, VAT1, LGMN, NUP88, POP1, MNT, SCAFB, EIF3C, TTC1, DNJC7, KIF2C, RGPD5, ATX2, ROAA, NP1L4, SNAG, TS101, CPNE1, TCPH, EBP2, ARI3A, ANM1, H2A1J, PKP2, SEM3C, VRK1, RBM4B, DDX50, RNZ2, MEP50, TBA1C, MBB1A, COR1B, TXD17, CPPED, PDD2L, PYGO2, LLPH, PSF3, ERP44, GCP2, ESYT1, SEN34, CSN4, WAC, DIDO1, RBM42, MCMBP, DCNL5, RAMAC, AN32E, NDC1, MMTA2, TBB6, HNRL1, PHF23, DDX23, MCRI2, WDR18, MTND, NTM1A, TBB2B, ASHWN, TM109, UT14A, TMED9, NUP58, SELO, DPCD, GNL3, KIFC1, NUP85, ELOV1, THIC, RBM4, GATA5, LS14B, RBM24, TRPM6, NAA15, SRRT, AP1M1, MAK16, ITPA, RTF2, EIF2A, PDIP3, TMPSD, MK67I, YTHD1, WNK3, GTPB4, UACA, CRNL1, TBL1R, PP12C, API5, DPY30, TRIM4, GRB1L, UNK, TB182, AMRA1, TANC1, TTYH3, WDR33, TINAL, NDEL1, PIP30, MKRN2, ILKAP, XRN2, TOLIP, SP130, RGAP1, CSTFT, RAB1B, LMA2L, ING2, I2BPL, TMX4, EPN3, MED28, SH3L3, PPIL3, ADNP, DHX36, PININ, PABP3, CPVL, BOLA2, TMX1, NELFA, PTN23, UN45A, CHM4B, OFUT1, WNK1, AMPB, ZHX3, EHD1, HEAT1, SUV92, CCD86, PRR36, BCAS3, RANB3, PEAK1, SMYD3, WDR26, SDS3, SFR19, KAT8, PHAX, UBE2Z, RMD5A, BRD9, GORS2, JUPI2, GHC1, MED20, CNO10, KANL2, FBRS, SP30L, MLXIP, XPO5, MYG1, CYBP, RC3H2, TENS1, SPC25, TAF9B, GLOD4, NCOA5, MOV10, TNR6C, CHD8, SYF1, SRA1, CHM1A, TM9S3, APMAP, ARFG3, HM20A, SSU72, VTA1, ENY2, CD320, DMAP1, UBN1, DCP1A, MED4, RIC8A, LUC7L, TIGAR, RTN4, RPR1B, EXOS3, PRD10, ANLN, PDLI7, DDX21, SAR1A, SIAS, SHLB2, MBNL1, AAAS, BAZ1A, ADPPT, OSTC, UBQL4, RAB6B, ABC3C, PHP14, HELLS, KRT84, KRT82, SYFB, PLPL3, BMP2K, ATG3, SMC4, OLA1, ZF64B, RBM12, MDN1, STAU2, T106B, SPS2L, CYRIB, DD19A, MRGBP, CC50A, SEP11, MED17, INT13, DDX18, NLE1, RBM22, WDR70, SLTM, LYAR, MED29, NSMA3, THUM1, TRM1, CARF, GAR1, FA53C, BCLF1, TAB2, FKB11, TMOD3, UGGG1, CDK12, GGA3, TLS1, IF2B1, HPBP1, MAT2B, MYOF, ITSN2, BICRA, EHD2, CNOT2, SPN90, LMCD1, CHMP5, COMD9, CWC15, THYN1, HACD3, KCMF1, RAI14, VAPA, H2AW, TMEM9, SEP10, CACO1, DAPLE, RCC2, MBD5, SLAI2, BCCIP, RRBP1, CPSF2, SYLC, MYEF2, RBM27, KANL3, ANFY1, RERE, ATX10, EP15R, SAE1, COPG2, MRC2, ASH2L, DKK3, TRMB, GULP1, VPS29, GRHPR, CATZ, SAE2, NXF1, PEF1, DNJB4, STK39, CNOT8, ABCF2, GTR6, Z3H7B, TCF20, HMGX4, SWP70, SUN2, RLP24, LIMA1, SRP68, CHRD1, SEPT9, UBQL2, CEIP2, S30BP, MED13, PFD2, PUF60, NRBP, TR112, XPO7, LCAP, MBD1, SIX4, CNOT7, PLXA1, MAGL2, TRM6, FOXD3, DBNL, DDX41, VPS28, CCNL1, TASOR, JUPI1, GMEB2, MRT4, CPSF3, GPTC8, NXT1, RCOR1, RALY, TF3C4, ACINU, AGO2, NUP50, ZHX1, CDV3, CNO11, ZN236, PSME2, MCTS1, ASAP1, MRTFB, ZMIZ1, MED23, PRR12, YETS2, HECD1, ZMYD8, COR1C, TPX2, AKP8L, MAFF, TMCO1, EPDR1, DD19B, PPT2, PRP19, SYNP2, UBQL1, VPS4A, G3BP2, CHIP, PACN2, MAGD2, SNX6, SSRG, FAF1, EPCR, CSN3, NSF1C, SCAF8, TRI33, TNR6B, ZC3H4, SMAG1, TRAK1, FOXJ3, SRRM2, PA2G4, SPG7, SMC3, SCML2, ZN148, RTRAF, RUVB2, CDYL, EIF3L, PLAP, RUVB1, NUDC, COF2, SYFA, DRG1, NCKP1, OFUT2, PKHA6, WDR37, E41L3, MYH15, R3HD2, KDM2A, RRP44, RCL1, DDX52, TMA7, YBOX2, MAN1, CHSP1, TR150, WBP11, MED16, NOP58, GIT1, ZN281, SGT1, AAR2, NOSIP, MEMO1, LSM2, SHLB1, LC7L2, SBDS, TMED7, SF3B6, ORN, RRP15, NOP16, PPIL1, MED31, KAD6, STRAP, RTCB, FBX7, NOC2L, RL36, CHTOP, SAMH1, PKP3, SALL2, TLN1, TRRAP, ARIP4, MTCL1, MYO5A, CRBG1, HYOU1, ATG4B, TBL2, KLF12, LSM4, RN114, PRC2C, PPME1, RBM7, YTHD2, PAXB1, SP16H, CD2AP, TNPO3, RBM8A, SNX9, NUBP2, HCFC2, PUS1, SERC, NCOR2, SPIN1, COPG1, GMEB1, CLIC4, CFA20, TACC3, MD1L1, 5MP1, EPN1, TEST, IF2B2, S4A7, ROBO1, NCOA3, SCC4, ZHX2, S23IP
Species: Mus musculus, Sus scrofa, Bos taurus, Homo sapiens
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Liu Y, Chen Q, Zhang N, Zhang K, Dou T, Cao Y, Liu Y, Li K, Hao X, Xie X, Li W, Ren Y, Zhang J. Proteomic profiling and genome-wide mapping of O-GlcNAc chromatin-associated proteins reveal an O-GlcNAc-regulated genotoxic stress response. Nature communications 2020 11(1) 33214551
Abstract:
O-GlcNAc modification plays critical roles in regulating the stress response program and cellular homeostasis. However, systematic and multi-omics studies on the O-GlcNAc regulated mechanism have been limited. Here, comprehensive data are obtained by a chemical reporter-based method to survey O-GlcNAc function in human breast cancer cells stimulated with the genotoxic agent adriamycin. We identify 875 genotoxic stress-induced O-GlcNAc chromatin-associated proteins (OCPs), including 88 O-GlcNAc chromatin-associated transcription factors and cofactors (OCTFs), subsequently map their genomic loci, and construct a comprehensive transcriptional reprogramming network. Notably, genotoxicity-induced O-GlcNAc enhances the genome-wide interactions of OCPs with chromatin. The dynamic binding switch of hundreds of OCPs from enhancers to promoters is identified as a crucial feature in the specific transcriptional activation of genes involved in the adaptation of cancer cells to genotoxic stress. The OCTF nuclear factor erythroid 2-related factor-1 (NRF1) is found to be a key response regulator in O-GlcNAc-modulated cellular homeostasis. These results provide a valuable clue suggesting that OCPs act as stress sensors by regulating the expression of various genes to protect cancer cells from genotoxic stress.
O-GlcNAc proteins:
RBM47, SBNO1, CNOT1, RGPD3, P121C, PDLI1, MYO1C, AIP, PSD11, PGRC1, TAF4, CLIC1, IPO5, IF2B3, AGRIN, PLOD2, HMGN4, IMA4, PESC, NOP56, DDX3X, PODXL, IMA3, NFIB, ARI1A, G3PT, PDCD5, TCRG1, PSA7, SCAM3, HGS, MYPT1, HNRDL, XPO1, ZN609, SC16A, SR140, SET1A, NPC1, TBX3, ARC1B, TIF1A, PGRC2, PFD6, NKRF, ZN185, OGT1, HMGB3, PPM1G, EIF3D, IPO8, RPA34, NUP42, DHX15, PRP4, SERA, PSMD3, RFOX2, PAPS1, MCA3, HNRPR, PRPF3, TPD54, IF4G3, KLF4, E41L2, DENR, XPOT, PRC1, ZN207, GET3, BUB3, ACTN4, BUD23, SYNC, KRT86, CPSF5, U3IP2, CALU, SAHH2, MED14, SMCA5, ZN862, GANP, KDM1A, ACSL4, SNX3, OGA, HNRPQ, PLOD3, MAFK, IMA7, UGDH, PQBP1, DKC1, IF2P, EDF1, DNJA2, BRD4, PFD1, WDR1, CPNE3, ZC11A, CLU, T22D2, PP6R2, CREST, ANR17, PDCD6, TBCA, H2AY, FLNB, NCOR1, SC22B, PR40A, PSIP1, SRS10, SF3B1, CSDE1, NPM3, U520, NU155, WDHD1, CRTAP, IDHC, CCNK, PIAS2, SPF27, DNJC8, RL1D1, SRP72, MTA2, TOM70, TOX4, SC24D, SUN1, NFAT5, AP2A2, SC31A, SEM3D, AGFG2, ZRAB2, LC7L3, LYPD3, FKBP9, SMC2, IPO7, AHSA1, PSMG1, SC24A, SC24B, CNOT4, OXSR1, HS74L, AP2A1, BAG3, CLPT1, ACL6A, LDHA, AATM, EGFR, PGK1, ASSY, LDLR, K1C14, LMNA, APOA2, FINC, ALBU, TFR1, PROC, ALDOA, CYTB, ANXA1, GCR, KITH, THY1, K2C1, G3P, HSPB1, RPN1, GNAI2, AT1A1, AT1B1, ADT2, IF2A, HMGN2, ICAM1, RLA2, JUN, LA, ITB1, K1C18, K2C8, CDK1, ATPB, S10A6, ENOA, PYGL, G6PI, NPM, ITAV, ACBP, LDHB, PDIA1, H10, CATD, ANXA2, TBB5, PROF1, SYEP, HS90A, HNRPC, TSP1, SP1, ANXA6, RHOC, DAF, MDR1, 4F2, HS90B, SRPRA, ASNS, CY1, RU17, ITA5, NFIC, VIME, RS17, K2C7, ANXA5, K1C16, RSSA, SNRPA, GSTP1, LEG1, HMGB1, TPM1, ROA1, RU2A, PARP1, PPBI, UCHL1, ALDOC, ATX1L, HS71B, CALM3, RO60, H14, PTPRF, THIO, ESTD, CH60, BIP, HSP7C, LAMP1, TOP1, TOP2A, PYC, C1TC, MPRI, ADHX, PABP1, PCNA, HARS1, IMDH2, TPR, KCRB, ACTN1, XRCC6, XRCC5, RINI, EF2, K1C10, K2C5, PDIA4, P4HA1, PLST, T2FB, CD59, MIF, GLU2B, CBPM, AK1A1, KPYM, ENPL, CCNB1, PO2F1, HNRPL, SYDC, PLAK, ALDR, AMPN, ERF3A, EZRI, FOSL1, FOSL2, MCP, NQO1, GNS, ZEP1, RS2, DESP, MUC1, CD44, CBR1, CREB1, H15, H13, H12, NCPR, AT2A2, CD36, STMN1, HSP76, HMGA1, JUNB, UBF1, JUND, ATF7, CEBPB, PYRG1, DDX5, PFKAL, LEG3, TCPA, PTN1, RL35A, RL7, VINC, SON, RL17, PGAM1, RCC1, ATF1, ML12A, NUCL, SPEE, RXRA, NFKB1, IF2B, ANXA7, BTF3, PSB1, MPRD, LMNB1, CSRP1, FLNA, 5NTD, VDAC1, CD9, TGM2, PIMT, FBRL, PUR2, PUR6, UBA1, NDKB, ROA2, RFX1, CBL, TCEA1, ITA6, SFPQ, PPIB, SYWC, RS3, NFYA, SAHH, COF1, IF4B, KTHY, EF1B, PPAC, CDK2, MCM3, RS12, BRD2, DNJB1, ATPA, PSA1, PSA3, PSA4, S100P, ITA3, MOES, DDX6, DNMT1, PAX6, U2AF2, RL13, S10A4, HMGB2, PTBP1, SYTC, SYVC, EF1G, STOM, 1433T, ARNT, RL10, RFA1, APEX1, PYR1, CALR, MAP4, CALX, TEAD1, GRN, EPHA2, 3MG, TKT, RBMS1, PML, EF1D, ERP29, PRDX6, RL12, KCY, PEBP1, PDIA3, 2AAA, NMT1, PURA2, UFO, SORCN, ILEU, RPB2, METK2, TIA1, ZEP2, DNJA1, PUR9, HNRH3, HNRH1, 1433B, 1433S, STIP1, S10AB, L1CAM, PRDX2, CDD, ELF1, RL9, CD70, KINH, CSTF2, MCM4, MCM5, MCM7, GLYM, HSP74, PROF2, PHB1, SPB6, RFC4, RL22, K1C9, MYH9, MYH10, COPB2, BASI, FUS, NU214, DEK, K22E, PRS7, ATPG, RL4, PP1G, GNL1, SRP14, NUP62, TAGL2, TALDO, RBMX, VKGC, HSPA9, IF4A3, RS19, RL3, OST48, FEN1, CAPG, TXLNA, TCPZ, RL13A, STAT3, MDHC, MDHM, IF2G, GARS, SYIC, LAP2A, LAP2B, MTREX, RS27, LPPRC, RL35, CDN2A, ECE1, LIS1, MUC18, MATR3, MSH2, SSRA, RANG, VDAC2, CBX5, UBP5, KI67, RAGP1, RECQ1, NOP2, BAG6, NOTC1, RL27A, RL5, RL21, RL28, RS9, RS5, RS10, IQGA1, CAPZB, IF1AX, RL29, SOX9, COPD, GSH0, PSMD8, PRC2A, TCPE, PTSS1, K2C6C, AGRE5, PAXI, RL34, LMAN1, NASP, FAS, CDK8, TCPG, EFTU, SYAC, SYSC, MCM2, ACADV, YLPM1, TMEDA, RBM25, HINT1, NU153, RBP2, TAF6, GUAA, CRIP1, GDIB, EMD, SERPH, F10A1, MAP2, RL14, TCPQ, TCPD, ANX11, PAPOA, FXR1, FXR2, RAB7A, SMCA4, SSRD, HDGF, ROA3, 6PGD, HNRPM, IMA1, GDIR1, AGFG1, HNRPF, MSH6, CAZA1, CRIP2, NUP98, ACLY, COPA, SC24C, TCP4, SYRC, ATX1, ATN1, SYYC, UBP14, AT1B3, RD23B, SNAA, IF5, PSMD4, XPO2, TERA, AF10, AF17, NP1L1, ADK, DSRAD, SEC13, NH2L1, PSA, EIF3B, SYMC, IF6, CTBP2, TMM33, NU107, EPIPL, TPIS, EIF3E, SC61B, MYL6, ACTB, IF4A1, RS20, PRPS1, PSA6, S10AA, CDC42, DEST, RAB10, UBC12, UBE2N, ARP3, ABCE1, RS3A, RL26, PSME3, RL15, RL27, RL37A, S61A1, PFD3, B2MG, DAD1, SUMO2, WDR5, NTF2, HNRPK, 1433G, RS7, PP1A, PP1B, RS8, RS15A, RS16, 1433E, RS14, RS23, RS18, RS29, RS13, RS11, RUXE, SMD1, SMD2, SMD3, PRS10, RL7A, ERF1, CNBP, RS4X, RL23A, RS6, H4, RAN, RL23, RAP1A, RS24, RS25, RS26, RS30, GBB2, RL30, RL31, RL10A, RL32, RL11, RL8, PPIA, FKB1A, RS27A, TRA2B, AP2B1, 1433Z, RSMN, SUMO1, DYL1, RL38, RS21, RACK1, UBC9, YBOX1, CSK2B, TPM4, EF1A1, ACTS, TBA1B, TBA4A, TBB4B, CSK21, PA1B2, HBB, HBA, PITX1, GTF2I, PHC1, TCPB, RAE1L, PRKDC, SARNP, RL24, ARF1, ERH, RL19, SRSF3, FOXK1, DAB2, EFNB1, RBM10, RBM3, CYC, S25A3, VIGLN, CLH1, FKBP3, HNRPU, U2AF1, SPTB2, TIAR, SRSF2, FOXK2, RUNX1, FABP5, LAT1, TFAP4, OTUD4, PFKAP, XPC, EWS, MEF2A, SP3, H11, RL18A, FKBP4, PLOD1, RL6, M2OM, DYST, KMT2A, LMNB2, TF65, UBXN1, GLGB, IF4G1, K1C17, REL, 1433F, PLP2, CSTF1, SRS11, EF1A2, SUH, GABPA, PAX8, FMR1, PRDX1, RL18, CKAP4, KHDR1, LRP1, SRSF1, DHX9, LG3BP, PPID, SSRP1, NSUN2, RBBP4, EP300, AHNK, HSP7E, GALT2, BST2, NU160, TBL3, ASPH, TROAP, BPTF, NFIA, SF3A3, AIMP1, ILF2, ILF3, LMAN2, TRAP1, FOXC1, MYO1E, CSTF3, ECH1, ACACA, CAF1B, RED, MTAP, TADBP, ROA0, PRDX4, CBX3, PSMD2, GPS2, SRSF9, SRSF5, SRSF6, TIF1B, G3BP1, PTK7, PABP4, EIF3I, TCOF, SF3B2, HAP28, FKBP5, SMAD4, PICAL, TBB3, PRP4K, PIN1, RIPK1, HDAC1, DCTN2, SNW1, TRA2A, CUL4B, DYR1A, TPBG, FHL1, MOGS, CD166, SPTN1, DX39B, TBB2A, KLF5, BYST, RUNX2, CDK13, CKAP5, CIRBP, HNRPD, SCRB2, DAG1, VEZF1, DSG2, EIF3A, UBP2L, SCRIB, TTL12, FHL2, DPYL3, DYHC1, IF4A2, SRC8, TRI25, FLNC, FA50A, CAPR1, RBM39, MCM6, ITPR1, PUM1, MDC1, EPN4, SMC1A, RRP1B, NCOA6, GSE1, UBP10, GANAB, LBR, MEF2D, CHD4, LASP1, ZN638, IMB1, NOLC1, NUMA1, SEPT2, SART3, CND1, ACAP1, U5S1, SYK, IF4H, PDIA6, PLEC, NOMO1, PON2, IPYR, TEBP, NONO, PWP2, RNPS1, PCBP1, PCBP2, SF3B3, KS6A1, SAFB1, SF3A2, RBMS2, SC23A, SC23B, SF3A1, SSXT, NCOA2, TRAM1, SF01, MED1, HMGN3, JHD2C, TRIP6, MARE1, ELAV1, ELF2, TAB1, AAAT, TOM34, UB2V2, NEDD8, ZYX, SEPT7, ADRM1, UAP1, PSMD5, DDB1, CDC37, DPYL2, RBBP7, TAF9, SRSF7, CPSF6, NRF1, FSCN1, IF16, KYNU, H2A2C, H2B2E, TRXR1, HNRL2, PDS5A, QSER1, TSR1, SMU1, P3H1, LSM12, CRTC2, GLE1, H90B2, ZN326, BCORL, TGO1, PRC2B, RRP12, TOIP1, PCID2, NU188, HP1B3, CE170, ZN362, ZC3HD, LRIF1, UBR4, UBAP2, KPRP, RBM26, AHDC1, CROCC, RPRD2, ECM29, MBNL2, ZMYM4, AR6P4, STEA4, ARID2, BICRL, CPIN1, LIN54, TM214, CAVN1, CDC73, EDC4, PRP8, SCYL2, GOLM2, NFRKB, NCEH1, MDEAS, ZC3HE, LARP1, FIP1, CRTC3, SAS6, CSPG4, WDR82, MCAF1, PACS1, SRCAP, RIPR1, UBN2, FBX50, IKIP, H32, LARP4, H2AV, RS27L, HAKAI, SPT6H, SND1, DDX46, 5MP2, CYFP1, KDM3B, PHF5A, ZCCHV, NUP54, POGZ, NUFP2, HEAT3, EMSY, RAI1, I2BP2, RBBP6, SH3R1, HUWE1, YTHD3, KHDC4, CENPV, KAISO, MYPN, PEG10, PABP2, KTN1, THOC4, GP180, CAND1, CARM1, PRSR1, DDX42, DAAF5, P66A, RB6I2, CHERP, ANKH1, CCAR1, RAVR1, SPB1, SMAP1, PHAR4, MAML2, PORIM, CCAR2, NUP93, LRC47, MT1M, FNBP4, CPSF7, PR38A, GT251, TXND5, SERB1, FA98A, TNR6A, PHC3, ABCF1, VP37A, NUP43, NUP37, NUP35, RLA0L, THOC2, WDR36, SMRC2, PUM2, SPP2A, ALMS1, C99L2, DDX54, DLG5, BRX1, DOT1L, PO210, GEMI5, ZN384, SCRB1, ZC3HF, NU133, PDC6I, NUDC2, GLMP, LMO7, ATX2L, PALLD, PSPC1, P66B, DNJC9, ELYS, DDX1, H1X, NICA, TM131, MAML1, HS105, CNOT9, ZN592, LAR4B, GCN1, NU205, TFG, TAF4B, STAM1, CBP, RBP56, DDX17, CELF1, OSTF1, RENT1, SMRC1, SMRD2, FUBP2, TNPO1, NEP1, UBP7, STMN2, LPP, MED12, H2A1C, SMCE1, RL36L, NCLN, FERM2, FUBP1, LRC59, FKB10, PF21A, INT12, FWCH2, AP2M1, REPS1, CMBL, SNR40, SEH1, DAZP1, RBM33, S10AG, OTUB1, HMCES, DDX27, P121A, PDLI5, FUBP3, WNK4, CHAP1, ZC3HA, CLP1L, CNDP2, ZFR, EP400, PRRC1, NOL4L, RBM14, QKI, PLIN4, S38A2, VPS35, CIC, MED15, MCCA, WRIP1, STRBP, TM209, SIN3A, MINT, UHRF1, HTF4, CDC5L, PFD5, RING2, EYA3, NUP88, POP1, MNT, SCAFB, EIF3C, DNJC7, PHB2, ATX2, ROAA, NP1L4, TS101, CPNE1, TCPH, EBP2, ANM1, H2B1M, RNZ2, TBA1C, MBB1A, TXD17, ERP44, ESYT1, WAC, DIDO1, AN32E, TMM43, TBB6, HNRL1, DDX23, TBB2B, TM109, TMED9, NUP58, GNL3, KIFC1, NUP85, RBM4, NAA15, SRRT, PDIP3, YTHD1, WNK3, GTPB4, UNK, SLIRP, IF5A2, NAT10, ILKAP, XRN2, SP130, RGAP1, DDX47, I2BPL, PININ, BOLA2, PTN23, WNK1, FA83D, ZHX3, STEEP, RPF2, ZN703, GORS2, JUPI2, MLXIP, CYBP, RC3H2, TENS1, EMAL4, NCOA5, TNR6C, CHD8, APMAP, ENY2, CD320, UBN1, DCP1A, LUC7L, RTN4, RPR1B, NIT2, ANLN, PDLI7, DDX21, SIAS, SHLB2, MBNL1, OSTC, RAB6B, PHP14, SYFB, RBM12, DD19A, LYAR, CARF, BCLF1, TAB2, TMOD3, CDK12, IF2B1, MAT2B, MYOF, ITSN2, BICRA, CNOT2, SEP10, RCC2, BCCIP, RRBP1, RBM27, KANL3, ATX10, MRC2, SAE2, NXF1, ABCF2, TES, TCF20, SUN2, LIMA1, CHRD1, SEPT9, UBQL2, S30BP, MED13, PFD2, PUF60, XPO7, SIX4, DDX41, CCNL1, JUPI1, MRT4, GPTC8, NUDT5, RALY, ACINU, AGO2, NUP50, ZHX1, CDV3, TRPC5, MRTFB, ZMIZ1, YETS2, HECD1, ZMYD8, COR1C, TPX2, AKP8L, PRP19, UBQL1, G3BP2, CHIP, PACN2, SSRG, EPCR, SCAF8, TRI33, SRRM2, PA2G4, CD11A, SMC3, RTRAF, RUVB2, EIF3L, RUVB1, NUDC, SYFA, DRG1, E41L3, RRP44, TR150, WBP11, NOP58, ZN281, SGT1, NOSIP, LSM2, LC7L2, SBDS, STRAP, RTCB, NOC2L, RL36, CHTOP, TLN1, ARIP4, HYOU1, PRC2C, PPME1, YTHD2, SP16H, TNPO3, SRPRB, RBM8A, ZN706, NCOR2, NPTN, COPG1, CLIC4, MD1L1, 5MP1, IF2B2, SCC4, ZHX2, S23IP
Species: Homo sapiens
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Woo CM, Lund PJ, Huang AC, Davis MM, Bertozzi CR, Pitteri SJ. Mapping and Quantification of Over 2000 O-linked Glycopeptides in Activated Human T Cells with Isotope-Targeted Glycoproteomics (Isotag). Molecular & cellular proteomics : MCP 2018 17(4) 29351928
Abstract:
Post-translational modifications (PTMs) on proteins often function to regulate signaling cascades, with the activation of T cells during an adaptive immune response being a classic example. Mounting evidence indicates that the modification of proteins by O-linked N-acetylglucosamine (O-GlcNAc), the only mammalian glycan found on nuclear and cytoplasmic proteins, helps regulate T cell activation. Yet, a mechanistic understanding of how O-GlcNAc functions in T cell activation remains elusive, partly because of the difficulties in mapping and quantifying O-GlcNAc sites. Thus, to advance insight into the role of O-GlcNAc in T cell activation, we performed glycosite mapping studies via direct glycopeptide measurement on resting and activated primary human T cells with a technique termed Isotope Targeted Glycoproteomics. This approach led to the identification of 2219 intact O-linked glycopeptides across 1045 glycoproteins. A significant proportion (>45%) of the identified O-GlcNAc sites lie near or coincide with a known phosphorylation site, supporting the potential for PTM crosstalk. Consistent with other studies, we find that O-GlcNAc sites in T cells lack a strict consensus sequence. To validate our results, we employed gel shift assays based on conjugating mass tags to O-GlcNAc groups. Notably, we observed that the transcription factors c-JUN and JUNB show higher levels of O-GlcNAc glycosylation and higher levels of expression in activated T cells. Overall, our findings provide a quantitative characterization of O-GlcNAc glycoproteins and their corresponding modification sites in primary human T cells, which will facilitate mechanistic studies into the function of O-GlcNAc in T cell activation.
O-GlcNAc proteins:
UBA6, ESYT2, HACL2, DEND3, SBNO1, XIRP2, CNOT1, PINLY, MT21E, SWAHB, P121B, TCAF2, MET15, F177B, P121C, GNAT3, MYO1G, SPT5H, TAF4, PK3CD, DNM1L, P3C2A, BT3A1, PSDE, BIN1, PITM1, DDX3X, RNT2, ARI1A, NCKP5, TRAD1, RHG33, ABLM1, KMT2D, IFIT3, HGS, MYPT1, S27A2, GAK, SC16A, SET1A, KDM6B, ARHGB, FYB1, ATX7, SHIP2, EIF3D, EIF3H, TOX3, NUP42, MEFV, DHX15, ZZEF1, PHF1, ZW10, PRPF3, TPD54, EMC8, SYNJ1, IF4G3, E41L2, WIPF1, LAT, OX1R, PLRG1, ZN207, ST1B1, LANC1, AKAP8, PLIN1, ZN292, AQR, GANP, HBP1, LY75, OGA, DIAP1, MAFK, HCN1, CCD22, BRD4, PP1RB, ABCB7, KI21B, LRP4, N4BP1, CPNE3, OBSL1, BRE1B, CAND2, T22D2, PP6R2, ANR17, H2AY, FLNB, NCOR1, PR40A, LRCH4, MPPB, PSIP1, NDUS3, KS6A5, MYCB2, U520, CCNK, CBPD, CYTF, LTN1, TOX4, PHF14, SUN1, PCF11, FRYL, TRI37, SC31A, CE152, AGFG2, SCAF4, SPN1, RTN3, APOL3, ATE1, CELF2, 6PGL, IPO7, CD2B2, ABCA1, SC24A, SC24B, PCNT, CNOT4, HERC2, HS74L, RIGI, M4K4, AIFM1, TXD12, LDHA, COX1, A1AT, FOS, LDLR, LMNA, ALBU, CYTB, GCR, HG2A, K2C1, G3P, HLAA, CPNS1, RPN1, RPN2, GNAI2, AT1A1, RLA2, JUN, ATPB, CD2, NPM, ANXA2, SYEP, TSP1, SP1, ANXA6, MDR1, HS90B, INHBA, ODPA, PTPRC, RU2B, HCK, VIME, GNAI3, ADA2A, HMGB1, ROA1, LKHA4, DERPC, F231L, GLI2, GRAB, RO60, RARB, HSP7C, EGR2, ODPB, LAMP1, SRF, FA5, IMDH2, TPR, SKI, ACTN1, K1C10, CEAM1, PLSL, GLU2B, HCLS1, PO2F1, RAC2, ATF2, FOSL2, PGCA, LEUK, CREB1, GDC, PECA1, MGMT, ZNF25, JUNB, UBF1, JUND, ATF7, PTN2, DDX5, EGR1, PTPRA, SON, RCC1, ATF1, ML12A, PLCG1, NUCL, NFKB1, LMNB1, CAN3, HNF1A, FLNA, TNAP3, PIMT, UBA1, ROA2, RFX1, CBL, QCR2, MAOM, SP100, NFYA, IF4B, AT2B4, RPB1, BRD2, ATPA, DDX6, PTBP1, ARNT, RFA1, APEX1, PYR1, CALR, MAP4, ERCC5, PTN6, SPB3, PDIA3, 2AAA, HLAF, HMOX2, CLIP1, RPB2, COR1A, ZEP2, HNRH3, HNRH1, STIP1, ELF1, KINH, LSP1, PHB1, PTN7, RFC4, MYH9, MYH10, COPB2, ACTN2, SOAT1, ADDA, FUS, NU214, ATP7B, MYH11, GLRX1, PPM1A, K22E, MP2K2, NUP62, HSPA9, IF4A3, COIA1, STAT3, MDHM, ECHA, IF2G, PERI, ELK3, LAP2A, LAP2B, RHG25, DPP6, HD, MATR3, GPDM, ZAP70, TNR4, VDAC2, MP2K4, NOP2, NOTC1, UTRN, IQGA1, STT3A, NPBW1, COPD, AGRE5, NASP, FAS, EFTU, CENPF, MA2A2, YLPM1, CLK1, NU153, RBP2, TAF6, GUAA, IDH3A, EMD, LRBA, AT1A2, MECP2, CCR3, KS6A3, LUM, ROA3, GDIR2, AGFG1, STAT2, TF2AA, CAZA1, NUP98, FOSB, SUCA, COPA, ITA8, SC24C, ATX1, UBP14, RD23B, EPHB3, AF17, CASP6, DSRAD, PSA, TPIS, SC61B, ACTB, ARF3, HNRPK, RS16, ACTA, GBB1, PPIA, RS27A, AP2B1, 1433Z, IF5A1, RACK1, ACTG, ACTS, TBA1B, TBA4A, PHC1, PRKDC, BTG2, SSBP2, ATL3, TXN4A, FOXK1, RHG04, NFKB2, SPTB2, FOXK2, RUNX1, AMPD2, CAP1, FLI1, OTUD4, PFKAP, SATB1, EWS, MEF2A, SP2, RHAG, SP4, SP3, RL18A, NUCB1, DYST, CREM, KMT2A, TF65, IF4G1, TLE4, REL, UBE3A, GABPA, GABP1, CD69, ZO1, TLE5, DHX9, GOGA3, SLFN5, S38AB, RBBP4, NCBP1, AHNK, MN1, FOXO1, TBL3, TF3C1, AKP13, BPTF, NFIA, CHD3, TP53B, ANK3, PP1R8, AKAP6, ROA0, PAK2, TBX2, M3K1, ATM, DC1I2, IKZF1, TCOF, ROCK1, NFAC2, SMAD4, PICAL, PRP4K, SNW1, IQGA2, MTMR1, MTMR3, CUL4A, CUL4B, RUNX3, NFYC, KGP1, CDK13, IL16, CKAP5, CO4A6, VEZF1, MORC3, UBP2L, SCRIB, GIT2, DYHC1, ELOA1, FLNC, CAPR1, CASL, SCN5A, SEM3A, ITPR2, PLSI, LAGE3, PUM1, EPN4, RRP1B, NCOA6, LBR, STAT4, MEF2D, LASP1, NUMA1, GAPD1, SPCS2, SUZ12, ACAP1, R3HD1, SYK, ARHG6, ACAP2, BRD3, PLEC, L2GL1, EPHA7, SF3B3, RYR3, TAF5, MARE2, TSN, SF01, MED1, JHD2C, T22D1, ELF2, NAB2, TAB1, SPEG, USF2, ZFHX3, ZYX, SEPT7, ADRM1, PKN1, DDB1, TAF9, OBF1, NRF1, PTPRO, ZN827, EX3L4, HNRL2, AAK1, CCD57, QRIC1, PRTG, CEA16, TM249, FR1L6, LRRF1, EMAL3, UAP1L, GON4L, LARP7, EPC2, CRTC2, PAR10, TYW2, RHG15, H90B3, BCORL, ZN831, TGO1, DOC11, PRC2B, TOIP1, CEP78, CD158, TDIF2, KMCP1, ZN362, FKB15, ZEP3, ODAD2, MPP7, LRIF1, UBR4, UBAP2, GNTK, RBM26, CE350, RPRD2, AGAP9, MYOME, TASO2, RN213, GL8D1, PDPK2, BICRL, OTU7B, RGPA1, TWF2, SDE2, NIPBL, LIN54, ZN544, PPR18, ZCHC8, CDC73, ARMX5, SCYL2, NFRKB, LMOD2, LEG1H, TMM81, PDXD1, RSBNL, MDEAS, ZC3HE, LARP1, SCND3, POTEE, ZN322, ANR11, SPIT4, AFTIN, FIP1, CRTC3, MCAF1, PACS1, BCOR, DJC14, DG2L6, LR74B, OTOG, RHG36, YJ005, RHG27, TMTC3, UN13D, HAKAI, NOL8, HECW1, SPT6H, SND1, KDM3B, S26A9, DYM, PRS41, APTX, ZCCHV, SETX, NUP54, GLUCM, POGZ, MYH14, NUFP2, MAVS, HDGR2, EMSY, I2BP2, AB12B, DHB13, CMKMT, SRGP1, RBBP6, RHG30, NRARP, TCPR1, HUWE1, YTHD3, CENPV, ATL2, YRDC, GPAT4, ZFHX4, ABCAD, BCL9L, KIF27, LRRT3, IQGA3, VS10L, CEP57, FRAS1, CACL1, P66A, I2BP1, CRLF3, CRERF, DYH10, GID4, ARI3B, WDR75, MGAP, ANKH1, SUGP1, SUGP2, CCAR1, BAP18, PLPL6, CMIP, TIGD4, YAF2, IHO1, SRRM1, FANCM, CC116, A16A1, DCP1B, PELP1, WDFY3, ABCA7, LGI4, NUP93, LRC47, ABD12, FNBP4, GALT4, RN175, CARME, AF1L2, TAB3, CPSF7, EFNMT, MAGB6, LRTM2, KRI1, TTC29, POC5, LR75A, S43A3, SUMF2, NETO2, NF2IP, LS14A, MISSL, FSAF1, TNR6A, PHC3, SRFB1, SP20H, VP37A, PCAT1, DOCK8, SYNE1, ARI1B, ENASE, TET1, MYRIP, OR6K3, CFA61, THOC2, WDR36, GABP2, MARH1, ALMS1, PREX1, PKHO2, DYH3, DSCL1, DTX3L, NETO1, NEK7, MICA1, ATS18, RN128, SNX29, SMCR8, ZN384, HASP, SMAP2, SCFD1, LMO7, ATX2L, PHIP, RUFY2, CSKI1, MADD, AGRV1, SYNE2, MUC16, P66B, AUTS2, BBX, TITIN, CTTB2, GBF1, SMG7, SNX19, PHF3, HS105, ZN592, HMHA1, TFG, TAF4B, CBP, KAT6A, SYMPK, SHIP1, DDX17, TANK, RAD50, CELF1, SMRD2, RAB8B, FUBP2, DVL3, LPP, TATD2, AT2A3, MRTFA, PLPL2, SH3K1, PF21A, DOC10, INT12, ACSF2, GCP3, SLAF6, RSPRY, MTEF3, SIR1, THA11, GLT14, CERS2, SYMM, PDLI5, FUBP3, PP16A, COG3, VCIP1, CHAP1, PDLI2, ANCHR, UBP47, Z512B, ZFR, EP400, CNO6L, CA074, PRRC1, ZN512, CNT3B, LRRC7, ARAP1, AGRA2, INP4A, RBM14, NED4L, LENG8, TRNT1, MCCA, PCX1, CCNL2, SIN3A, SEBP2, MINT, HTF4, CDC5L, EYA3, LGMN, MNT, SCAFB, TTC1, OSMR, ATX2, METH, ACON, CPNE1, TBA1C, MBB1A, GPTC1, ERP44, ESYT1, CCM2, FUZZY, DIDO1, MCMBP, CABL2, NDC1, PAXX, HNRL1, NUP58, RIOK2, THIC, RBM4, NADAP, SSBP3, NAA15, AP1M1, M10L1, YTHD1, BACH2, PANK2, PC11Y, ASPC1, UCK2, TRI31, UNK, FTO, AMRA1, CE295, DRC3, SP130, BRD8, CSTFT, ZCPW1, LMA2L, CK054, SLIK2, CSRN2, I2BPL, VPS16, EPC1, ADNP, IPYR2, FOXP1, PTN23, WNK1, AMPB, E41L1, GSX1, ELOV6, CH033, VISTA, SFR19, GORS2, LN28A, MLXIP, GBB4, PKHA1, RISC, TAF9B, MRM3, ZBT20, NCOA5, TANC2, TNR6C, CHD8, AT131, VTA1, SYSM, UBN1, DCP1A, KI13B, PRD10, XPP1, PDLI7, DDX21, MBNL1, SIR7, TULP4, ABCBA, LATS2, UBQL4, THSD1, CENPM, PDS5B, RBM12, MED9, SLTM, MIC19, NSMA3, THUM1, CARF, SNTG2, MTMR4, TE2IP, TAB2, CDK12, GGA3, ITSN2, BICRA, CNOT2, TMOD2, THYN1, PDP1, VAPA, TEN3, CHD7, DYH1, SYLC, KLH42, KANL3, RERE, HDC, TRPC4, MALT1, ADDG, TCF20, NDRG3, SUN2, NDOR1, UBQL2, S30BP, RPGFL, AGRE2, NRBP, BAZ2A, HOOK1, S2513, TASOR, AKA11, GMEB2, PARP4, C8AP2, IKZF2, ACINU, CNO11, AT7L1, K1210, YETS2, HECD1, NOTC3, PRP19, UBQL1, FAF1, PPIE, DIM1, MACF1, SCAF8, SET1B, JIP3, ZC3H4, SRRM2, CLCA2, SMC3, ZN148, MTMR6, ENTP4, SAC2, MAST1, FYV1, WDR37, TR150, ZN281, FBX7, 3BP1, OR2W1, NOC2L, SAMH1, DMXL1, ARIP4, MTCL1, RIPR2, PKHM1, RPGF2, CRBG1, PRC2C, YTHD2, SP16H, ANGL3, PCDG3, SNX13, NUBP2, NCOR2, COPG1, GMEB1, DC1L1, ROBO1, NCOA3, M3K4, PCLO, CAN7, SCC4, ZHX2, S23IP
Species: Homo sapiens
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Berthier A, Vinod M, Porez G, Steenackers A, Alexandre J, Yamakawa N, Gheeraert C, Ploton M, Maréchal X, Dubois-Chevalier J, Hovasse A, Schaeffer-Reiss C, Cianférani S, Rolando C, Bray F, Duez H, Eeckhoute J, Lefebvre T, Staels B, Lefebvre P. Combinatorial regulation of hepatic cytoplasmic signaling and nuclear transcriptional events by the OGT/REV-ERBα complex. Proceedings of the National Academy of Sciences of the United States of America 2018 115(47) 30397120
Abstract:
The nuclear receptor REV-ERBα integrates the circadian clock with hepatic glucose and lipid metabolism by nucleating transcriptional comodulators at genomic regulatory regions. An interactomic approach identified O-GlcNAc transferase (OGT) as a REV-ERBα-interacting protein. By shielding cytoplasmic OGT from proteasomal degradation and favoring OGT activity in the nucleus, REV-ERBα cyclically increased O-GlcNAcylation of multiple cytoplasmic and nuclear proteins as a function of its rhythmically regulated expression, while REV-ERBα ligands mostly affected cytoplasmic OGT activity. We illustrate this finding by showing that REV-ERBα controls OGT-dependent activities of the cytoplasmic protein kinase AKT, an essential relay in insulin signaling, and of ten-of-eleven translocation (TET) enzymes in the nucleus. AKT phosphorylation was inversely correlated to REV-ERBα expression. REV-ERBα enhanced TET activity and DNA hydroxymethylated cytosine (5hmC) levels in the vicinity of REV-ERBα genomic binding sites. As an example, we show that the REV-ERBα/OGT complex modulates SREBP-1c gene expression throughout the fasting/feeding periods by first repressing AKT phosphorylation and by epigenomically priming the Srebf1 promoter for a further rapid response to insulin. Conclusion: REV-ERBα regulates cytoplasmic and nuclear OGT-controlled processes that integrate at the hepatic SREBF1 locus to control basal and insulin-induced expression of the temporally and nutritionally regulated lipogenic SREBP-1c transcript.
O-GlcNAc proteins:
A4D111, POTEF, A5GZ75, AXA2L, P121C, A9Z0R7, EIFCL, C3UMV2, F1JVV5, I6TRR8, MYO1C, IF2B3, DDX3X, TCRG1, OPLA, XPO1, SC16A, SET1A, OGT1, EIF3D, DDX3Y, DHX15, PRP4, SERA, PSMD3, HNRPR, ACTN4, MYO1B, AKAP8, HNRPQ, UGDH, USO1, WDR1, ANR17, GGCT, LX12B, FLNB, PR40A, SF3B1, SPB7, NU155, KRT38, SC24D, GLSK, SC31A, ELP1, SMC2, AGM1, UTS2, BAG4, SC24A, SC24B, AP2A1, LDHA, AL1A1, PGK1, A2MG, CO3, CYTA, KV117, IGHG1, IGHA1, APOE, APOC2, FIBG, TFR1, TRFE, CATA, ALDOA, TBB4A, G3P, HSPB1, RPN1, RPN2, AT1A1, ARGI1, ALDH2, S10A8, ADT2, GELS, ATPB, APOA4, ENOA, PYGL, G6PI, PDIA1, CATD, ANXA2, CAN1, TBB5, HS90A, SP1, CO1A2, HS90B, PO2F2, GSTP1, VILI, ANXA4, PARP1, LKHA4, ATX1L, POTEI, UBB, UBC, SAA2, HS71A, HS71B, IGG1, TBA3C, TBA3D, THIO, CH60, BIP, HSP7C, PYGB, PYGM, G6PD, PYC, C1TC, NFH, IMDH2, XRCC6, XRCC5, AT1A3, EF2, PDIA4, P4HA1, ENOB, GFAP, ENPL, IDE, PO2F1, HNRPL, PLAK, DESP, AT2A2, HSP76, DDX5, LEG3, TCPA, RL7, VINC, E2AK2, ITIH2, ANXA7, HNF1A, FILA, CD11B, FLNA, VDAC1, TGM2, PUR2, UBA1, NDKB, TGM1, EST1, SFPQ, SAHH, MCM3, ATPA, PTBP1, SYVC, ABCD3, GRN, TKT, SPB3, AL4A1, PDIA3, KPYR, RPB2, AKT1, PUR9, HNRH1, CASPE, 1433S, S10AB, PRDX2, MCM4, MCM7, HS71L, CTNB1, IRS1, GDE, MYH9, FUS, SPB5, NUP62, TALDO, HSPA9, CAPG, TCPZ, STAT3, MDHC, MDHM, ECHA, GARS, SYIC, HUTH, LPPRC, MATR3, MSH2, VDAC2, SYQ, LEG7, COPD, SPB4, TCPE, AL9A1, LMAN1, FMO5, TCPG, SYAC, RBM25, KLK7, DYN2, TCPQ, TCPD, RAB7A, KS6A3, HNRPM, HXK2, CAZA1, NUP98, ACLY, COPB, COPA, SC24C, SYRC, SYYC, UBP14, HSP72, P5CS, XPO2, TERA, MTP, AF17, PSA, HNRH2, EIF3B, SYMC, NU107, EPIPL, TPIS, ACTB, IF4A1, HNRPK, 1433G, PRS4, ACTA, H4, RS27A, RL40, 1433Z, RACK1, ACTG, ACTH, ACTC, ACTS, TBA1B, TBA4A, TBB4B, PRKDC, DCD, VIGLN, CLH1, HNRPU, FABP5, MSHR, EWS, SEMG2, DSG1, SP3, PLOD1, EF1A2, GFPT1, PRDX1, KHDR1, TGM3, DHX9, LG3BP, DSC1, ILF3, TRAP1, PAK2, PSMD2, PABP4, PICAL, PKP1, BLMH, SNTB1, TBB2A, VEZF1, TRI29, UBP2L, LY6D, SRC8, PDIA5, HS902, EPN4, SMC1A, GANAB, MVP, PLEC, NONO, SC23A, SC23B, CDSN, JHD2C, CYTM, DPYL2, PCKGM, TKFC, Q53G76, Q58FF2, Q59EA0, ZN326, FILA2, UBAP2, KPLCE, RBM26, EF1A3, ARID2, TBA3E, POTEE, SBSN, FBX50, Q70T18, Q71E78, TBA1A, SND1, NUP54, MYH14, PEG10, PRP39, TAXB1, CAND1, CARM1, PRSR1, SPA12, ANKH1, ASXL1, NUP93, RDHE2, Q8N6B4, PDPR, TNR6A, COP1, PDC6I, POF1B, ATX2L, DDX1, BAP1, TFG, RBP56, EVPL, DDX17, RENT1, FUBP2, UBP7, NCLN, H2B1A, WNK4, ZC3HA, SCYL1, SPB12, GSDMA, VPS35, PHF12, CIC, STRBP, VAT1, NUP88, ATX2, CPNE1, TCPH, TBA1C, DIDO1, HNRL1, TBB2B, NUP58, ACTBM, TB182, SP130, WNK1, AGO3, MCCB, MOV10, TNR6C, S10AE, DD19A, ATD3A, TBA8, UGGG1, IF2B1, CALL5, RRBP1, NXF1, S2513, PO2F3, AGO2, AGO1, Q9UL79, ACSL5, DD19B, TNR6B, CD11A, EIF3L, SYFA, KLK5, RTCB, WNK2, PKP3, HYOU1, SNX9, COPG1, IF2B2, S23IP
Species: Homo sapiens
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Ha C, Lim K. O-GlcNAc modification of Sp3 and Sp4 transcription factors negatively regulates their transcriptional activities. Biochemical and biophysical research communications 2015 467(2) 26431879
Abstract:
The addition of O-linked N-acetylglucosamine (O-GlcNAc) on serine or threonine modifies a myriad of proteins and regulates their function, stability and localization. O-GlcNAc modification is common among chromosome-associated proteins, such as transcription factors, suggesting its extensive involvement in gene expression regulation. In this study, we demonstrate the O-GlcNAc status of the Sp family members of transcription factors and the functional impact on their transcriptional activities. We highlight the presence of O-GlcNAc residues in Sp3 and Sp4, but not Sp2, as demonstrated by their enrichment in GlcNAc positive protein fractions and by detection of O-GlcNAc residues on Sp3 and Sp4 co-expressed in Escherichia coli together with O-GlcNAc transferase (OGT) using an O-GlcNAc-specific antibody. Deletion mutants of Sp3 and Sp4 indicate that the majority of O-GlcNAc sites reside in their N-terminal transactivation domain. Overall, using reporter gene assays and co-immunoprecipitations, we demonstrate a functional inhibitory role of O-GlcNAc modifications in Sp3 and Sp4 transcription factors. Thereby, our study strengthens the current notion that O-GlcNAc modification is an important regulator of protein interactome.
O-GlcNAc proteins:
SP4, SP3
Species: Homo sapiens
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