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Ramirez DH, Aonbangkhen C, Wu HY, Naftaly JA, Tang S, O'Meara TR, Woo CM. Engineering a Proximity-Directed O-GlcNAc Transferase for Selective Protein O-GlcNAcylation in Cells. ACS chemical biology 2020 15(4) 32119511
Abstract:
O-Linked β-N-acetylglucosamine (O-GlcNAc) is a monosaccharide that plays an essential role in cellular signaling throughout the nucleocytoplasmic proteome of eukaryotic cells. Strategies for selectively increasing O-GlcNAc levels on a target protein in cells would accelerate studies of this essential modification. Here, we report a generalizable strategy for introducing O-GlcNAc into selected target proteins in cells using a nanobody as a proximity-directing agent fused to O-GlcNAc transferase (OGT). Fusion of a nanobody that recognizes GFP (nGFP) or a nanobody that recognizes the four-amino acid sequence EPEA (nEPEA) to OGT yielded nanobody-OGT constructs that selectively delivered O-GlcNAc to a series of tagged target proteins (e.g., JunB, cJun, and Nup62). Truncation of the tetratricopeptide repeat domain as in OGT(4) increased selectivity for the target protein through the nanobody by reducing global elevation of O-GlcNAc levels in the cell. Quantitative chemical proteomics confirmed the increase in O-GlcNAc to the target protein by nanobody-OGT(4). Glycoproteomics revealed that nanobody-OGT(4) or full-length OGT produced a similar glycosite profile on the target protein JunB and Nup62. Finally, we demonstrate the ability to selectively target endogenous α-synuclein for O-GlcNAcylation in HEK293T cells. These first proximity-directed OGT constructs provide a flexible strategy for targeting additional proteins and a template for further engineering of OGT and the O-GlcNAc proteome in the future. The use of a nanobody to redirect OGT substrate selection for glycosylation of desired proteins in cells may further constitute a generalizable strategy for controlling a broader array of post-translational modifications in cells.
O-GlcNAc proteins:
SBNO1, CNOT1, P121C, DX39A, GTPB1, AP3B1, PGRC1, TAF4, EIF3F, IPO5, IF2B3, NOP56, DDX3X, ARI1A, IRS4, ANM5, TCRG1, PSA7, HGS, MYPT1, HNRDL, XPO1, SET1A, PUR4, NPC1, TIF1A, NKRF, OGT1, PPM1G, EIF3D, EIF3H, DHX15, SERA, HNRPR, IF4G3, E41L2, ZN207, BUB3, ACTN4, HTSF1, AP1G1, SYNC, AKAP8, CALU, SMCA5, JIP4, OGA, HNRPQ, DIAP1, TSN3, SNX2, DKC1, CLAP2, CPNE3, PHF2, ANR17, H2AY, FLNB, NCOR1, CISY, PR40A, SF3B1, CSDE1, U520, EIF3G, PRAF3, SRP72, MTA2, TOX4, SC24D, SC31A, SCAF4, ZRAB2, LC7L3, VAPB, IPO7, SC24B, ACSL3, AP2A1, AIFM1, LDHA, COX2, HPRT, AATM, PGK1, LMNA, TFR1, ALDOA, OAT, G3P, RPN1, RPN2, AT1A1, ADT2, PCCA, IF2A, RLA0, ITB1, ATPB, ENOA, PYGL, G6PI, NPM, LDHB, PDIA1, H10, TBB5, HEXB, PROF1, SYEP, HS90A, HNRPC, 4F2, HS90B, ASNS, ODPA, RU17, RSSA, SNRPA, GSTP1, HMGB1, DLDH, ROA1, PARP1, LKHA4, HS71B, H14, ODP2, THIO, CH60, BIP, HSP7C, EPB41, ODPB, LAMP1, ACADM, TOP1, TOP2A, PYC, C1TC, MPRI, PRPS2, PABP1, PCNA, HARS1, IMDH2, TPR, KCRB, XRCC6, XRCC5, EF2, PDIA4, PLST, GLU2B, KPYM, ENPL, PO2F1, HNRPL, SYDC, PLAK, ALDR, EZRI, GNS, RS2, CREB1, H12, AT2A2, JUNB, PYRG1, DDX5, PRS6A, TCPA, RL35A, RL7, VINC, SON, RCC1, NUCL, HXK1, E2AK2, SPEE, IF2B, ANXA7, LMNB1, FLNA, VDAC1, FBRL, PUR2, PUR6, UBA1, NDKB, ROA2, RFX1, TCEA1, SFPQ, PPIB, RS3, NFYA, SAHH, COF1, IF4B, EF1B, MCM3, BRD2, ATPA, PSA1, PSA3, PSA4, PAX6, U2AF2, RL13, PTBP1, SYTC, SYVC, EF1G, RFA1, APEX1, PYR1, CALR, MAP4, CALX, PSB5, TKT, PRDX6, PRDX5, PRDX3, RL12, PEBP1, PDIA3, 2AAA, CDC27, AMRP, SDHA, QCR1, PUR9, HNRH1, STIP1, PRDX2, RL9, CSTF2, MCM4, MCM5, MCM7, GLYM, HSP74, PHB, MYH9, COPB2, ADDA, BASI, FUS, NU214, DEK, MP2K2, ATPG, RL4, SRP14, NUP62, RBMX, GRP75, IF4A3, RS19, RL3, TXLNA, TCPZ, MDHC, MDHM, ECHA, IF2G, GARS, SYIC, LAP2A, LAP2B, MTREX, RS27, LPPRC, MATR3, RANG, VDAC2, UBP5, KI67, RAGP1, NOP2, CRKL, BAG6, RL27A, RL5, RL21, RL28, RS9, STT3A, COPD, PRC2A, TCPE, AL9A1, RL34, NASP, FAS, TCPG, EFTU, SYAC, SYSC, PSB3, MCM2, YLPM1, TMEDA, RBM25, NU153, RBP2, GSK3A, TAF6, GUAA, MRE11, GDIB, EMD, F10A1, LRBA, RL14, TCPQ, TCPD, ANX11, PAPOA, RAB7A, SMCA4, HCFC1, DHB4, ROA3, 6PGD, HNRPM, IMA1, AGFG1, HNRPF, MSH6, RBM5, NUP98, ACLY, COPB, COPA, MOT1, SC24C, SYRC, SYYC, AT1B3, RD23B, P5CS, IF5, XPO2, TERA, AFAD, DSRAD, PSA, SYMC, CTBP2, NU107, TPIS, ACTB, IF4A1, PSA6, ARF3, ABCE1, RAP1B, RS3A, RL26, RL15, S61A1, HNRPK, RS7, RS8, 1433E, RS14, RS23, RS11, SMD1, RL7A, RS4X, H4, RAN, RL23, GBB2, RL10A, RL11, RL8, PPIA, RL40, TRA2B, AP2B1, IF5A1, RACK1, YBOX1, EF1A1, TBB4B, CSK21, IF4G2, GTF2I, TCPB, PRKDC, RL24, RL19, SRSF3, FOXK1, RBM10, MPCP, CLH1, HNRPU, SPTB2, FOXK2, CAP1, LAT1, EXOSX, EWS, RL18A, FKBP4, RL6, TOP2B, KMT2A, LMNB2, TF65, IF4G1, TLE3, SRS11, PUR1, SUH, GABPA, PRDX1, RL18, C1QBP, KHDR1, SRSF1, DHX9, CD47, SSRP1, RBBP4, AHNK, AP1B1, NU160, BPTF, TP53B, AIMP1, ILF2, ILF3, LMAN2, TRAP1, PP1R8, ACACA, ROA0, PRDX4, CBX3, PSMD2, SRSF6, TIF1B, PTK7, PABP4, EIF3I, TCOF, SF3B2, TMED1, PICAL, RIPK1, HDAC1, CUL4B, CD166, IDI1, NFYC, CKAP5, HNRPD, SCRB2, DSG2, EIF3A, UBP2L, SCRIB, TTL12, DCTN1, DYHC1, SRC8, CAPR1, RBM39, MCM6, MDC1, EPN4, SMC1A, RRP1B, UBP10, GANAB, LBR, ZN638, IMB1, NUMA1, SEPT2, SART3, U5S1, SYK, BRD3, PDIA6, IPYR, TEBP, NONO, PWP2, RCN1, PCBP1, PCBP2, SF3B3, SAFB1, SF3A1, NCOA2, SF01, MARE1, NSDHL, TAB1, AAAT, VAS1, ZYX, CCDC6, PKN2, DDB1, CDC37, SRSF7, CPSF6, NRF1, H31T, QSER1, QRIC1, P3H1, TB10B, AMOT, DHB12, PRC2B, H2B2F, HP1B3, CE170, ZC3HD, RBM26, RIF1, RPRD2, ZN318, ECM29, ZMYM4, MAP1S, LIN54, EDC4, PRP8, SCYL2, NFRKB, ZC3HE, LARP1, FIP1, MCAF1, GGYF2, SPT6H, SND1, DHX30, KDM3B, ZCCHV, NUP54, POGZ, NUFP2, MAVS, I2BP2, RBBP6, HUWE1, YTHD3, CENPV, LYRIC, ZN598, GP180, CAND1, CARM1, DDX42, P66A, ARI3B, MGAP, PHF6, CHERP, ANKH1, SUGP1, CCAR1, SPB1, PHAR4, SPART, CCAR2, NUP93, S11IP, FNBP4, CPSF7, ARFG1, ENAH, AFG2H, TXND5, LS14A, Z280C, TNR6A, SMRC2, TBC15, PNPT1, HM13, PO210, GEMI5, ZN384, SMAP2, NU133, PDC6I, PCNP, CKAP2, ATX2L, P66B, ELYS, DDX1, GBF1, NICA, UBXN4, HS105, LAR4B, NU205, AKAP1, TFG, CBP, DDX17, CELF1, RENT1, SMRC1, FUBP2, TNPO1, UBP7, NCLN, FUBP1, FKB10, KBP, PDLI5, FUBP3, CHAP1, Z512B, ZFR, PRRC1, DOCK7, RBM14, VPS35, CIC, EFGM, SIN3A, MINT, CDC5L, PSMD1, EYA3, ATX2, HCD2, ACON, TS101, TCPH, ANM1, SH3G1, COR1B, DIDO1, HNRL1, DDX23, TMED9, NUP58, RBM4, NAA15, B2L13, YTHD1, UNK, ILKAP, SP130, BRD8, I2BPL, SLK, S6A15, PININ, NELFA, PTN23, WNK1, AMPB, GORS2, CYBP, TAF9B, GLOD4, CBX8, NCOA5, CHD8, APMAP, DCP1A, RTN4, ANLN, GEPH, PDLI7, DDX21, SYFB, SYIM, SMC4, RBM12, DDX18, CARF, UGGG1, CDK12, TECR, IF2B1, HPBP1, ITSN2, CNOT2, HACD3, RCC2, SYLC, SUCB1, UBQL2, PCYOX, S30BP, PUF60, NRBP, DACH1, BAZ2A, BAZ1B, CDC23, TASOR, ACINU, CDV3, MRTFB, YETS2, HECD1, PKCB1, DD19B, PRP19, MAGD2, FAF1, TRI33, SRRM2, PA2G4, RUVB2, RUVB1, VDAC3, E41L3, TR150, NOP58, SHLB1, LC7L2, TMED7, STRAP, RTCB, HBS1L, TLN1, HYOU1, PRC2C, SP16H, COPG1, DC1L1, S23IP
Species: 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, TPM3, 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, PHB, SPB6, RFC4, RL22, K1C9, MYH9, MYH10, COPB2, BASI, FUS, NU214, DEK, K22E, PRS7, ATPG, RL4, PP1G, GNL1, SRP14, NUP62, TAGL2, TALDO, RBMX, VKGC, GRP75, IF4A3, RS19, RL3, OST48, FEN1, CAPG, TXLNA, TCPZ, RL13A, STAT3, MDHC, MDHM, IF2G, GARS, SYIC, LAP2A, LAP2B, STAT1, 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, HCFC1, 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, MPCP, 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, TLE3, 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, PRP4B, 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, BZW1, 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, PAIRB, 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, NOG1, 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, PKCB1, 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, BZW2, IF2B2, 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, TPM3, 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, GRP75, 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, HCFC1, 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, XP32, 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, CMC2, 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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Li S, Zhu H, Wang J, Wang X, Li X, Ma C, Wen L, Yu B, Wang Y, Li J, Wang PG. Comparative analysis of Cu (I)-catalyzed alkyne-azide cycloaddition (CuAAC) and strain-promoted alkyne-azide cycloaddition (SPAAC) in O-GlcNAc proteomics. Electrophoresis 2016 37(11) 26853435
Abstract:
O-linked β-N-acetylglucosamine (O-GlcNAc) is emerging as an essential protein post-translational modification in a range of organisms. It is involved in various cellular processes such as nutrient sensing, protein degradation, gene expression, and is associated with many human diseases. Despite its importance, identifying O-GlcNAcylated proteins is a major challenge in proteomics. Here, using peracetylated N-azidoacetylglucosamine (Ac4 GlcNAz) as a bioorthogonal chemical handle, we described a gel-based mass spectrometry method for the identification of proteins with O-GlcNAc modification in A549 cells. In addition, we made a labeling efficiency comparison between two modes of azide-alkyne bioorthogonal reactions in click chemistry: copper-catalyzed azide-alkyne cycloaddition (CuAAC) with Biotin-Diazo-Alkyne and stain-promoted azide-alkyne cycloaddition (SPAAC) with Biotin-DIBO-Alkyne. After conjugation with click chemistry in vitro and enrichment via streptavidin resin, proteins with O-GlcNAc modification were separated by SDS-PAGE and identified with mass spectrometry. Proteomics data analysis revealed that 229 putative O-GlcNAc modified proteins were identified with Biotin-Diazo-Alkyne conjugated sample and 188 proteins with Biotin-DIBO-Alkyne conjugated sample, among which 114 proteins were overlapping. Interestingly, 74 proteins identified from Biotin-Diazo-Alkyne conjugates and 46 verified proteins from Biotin-DIBO-Alkyne conjugates could be found in the O-GlcNAc modified proteins database dbOGAP (http://cbsb.lombardi.georgetown.edu/hulab/OGAP.html). These results suggested that CuAAC with Biotin-Diazo-Alkyne represented a more powerful method in proteomics with higher protein identification and better accuracy compared to SPAAC. The proteomics credibility was also confirmed by the molecular function and cell component gene ontology (GO). Together, the method we reported here combining metabolic labeling, click chemistry, affinity-based enrichment, SDS-PAGE separation, and mass spectrometry, would be adaptable for other post-translationally modified proteins in proteomics.
O-GlcNAc proteins:
AXA2L, EIFCL, MYO1C, P2Y10, IPO5, PLOD2, DDX3X, ZN197, XPO1, PPM1G, HNRPR, ACTN4, SNG2, OGA, UGDH, BRD4, FLNB, U520, IDHC, TOM70, K2C75, LDHA, AL1A1, DHE3, PGK1, PIGR, IGHA1, K1C14, K2C6A, LMNA, ALBU, TRFL, K2C6B, K2C1, AT1A1, ALDH2, S10A8, ITB1, K1C18, K2C8, ENOA, G6PI, HYEP, PDIA1, TBB5, SYEP, HS90A, 4F2, HS90B, VIME, K2C7, K1C16, RSSA, DLDH, PARP1, LIGO3, UBB, HS71A, CH60, BIP, HSP7C, PYGB, G6PD, C1TC, K2C3, ACTN1, PEPD, XRCC5, RINI, EF2, K1C10, K1C13, K2C5, PDIA4, P4HA1, GLU2B, KPYM, ENPL, HNRPL, PLAK, DESP, NCPR, AT2A2, NAGAB, HSP76, CAN2, NUCL, IF2B, ANXA7, FLNA, TGM2, PUR6, UBA1, SAHH, RPB1, ATPA, MOES, EF1G, CALR, MAP4, CALX, ITPI2, TKT, PDIA3, 2AAA, AL3A1, CPSM, QCR1, HNRH1, STIP1, HSP74, K1C9, MYH9, MYH10, K22E, PRS7, SRBP1, GRP75, IF4A3, IF2G, LPPRC, MATR3, AL3B1, NAMPT, UBP5, KI67, MAP1B, UTRO, IQGA1, TCPE, K2C6C, AL9A1, NASP, FAS, TCPG, EFTU, SYAC, F10A1, TCPQ, TCPD, 6PGD, HNRPM, ACLY, SYRC, UBP14, S12A2, TERA, ECHB, NP1L1, EIF3B, SYMC, EIF3E, ACTB, UB2D3, ARP3, HNRPK, PRS4, ACTC, EF1A1, TBA1B, TBB4B, KRT85, PRKDC, DCD, MPCP, CLH1, HNRPU, SPTB2, PFKAP, FKBP4, AKA12, IF4G1, K1C17, CKAP4, DHX9, RBBP4, TP53B, TRAP1, PSMD2, SQSTM, TBB3, SPTN1, HNRPD, EIF3A, GANAB, GOGB1, IMB1, NUMA1, PDIA6, PLEC, PCM1, K1H1, KCC4, DREB, TRXR1, HKDC1, LRRF1, FILA2, BIG3, CROCC, BROX, K2C79, K2C80, PRP8, CCD81, SPT6H, SND1, MYH14, CC190, HORN, UNC80, GHDC, CDRT4, TXND5, NDRG1, GCN1, TNPO1, SIPA1, ERO1A, ODAD4, VPS35, ERP44, EHD4, SLK, RTN4, DDX21, SYFB, MYOF, RRBP1, SRP68, ACINU, SRRM2, PA2G4, MA2B2, RTCB, TLN1
Species: Homo sapiens
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Hahne H, Sobotzki N, Nyberg T, Helm D, Borodkin VS, van Aalten DM, Agnew B, Kuster B. Proteome wide purification and identification of O-GlcNAc-modified proteins using click chemistry and mass spectrometry. Journal of proteome research 2013 12(2) 23301498
Abstract:
The post-translational modification of proteins with N-acetylglucosamine (O-GlcNAc) is involved in the regulation of a wide variety of cellular processes and associated with a number of chronic diseases. Despite its emerging biological significance, the systematic identification of O-GlcNAc proteins is still challenging. In the present study, we demonstrate a significantly improved O-GlcNAc protein enrichment procedure, which exploits metabolic labeling of cells by azide-modified GlcNAc and copper-mediated Click chemistry for purification of modified proteins on an alkyne-resin. On-resin proteolysis using trypsin followed by LC-MS/MS afforded the identification of around 1500 O-GlcNAc proteins from a single cell line. Subsequent elution of covalently resin bound O-GlcNAc peptides using selective β-elimination enabled the identification of 185 O-GlcNAc modification sites on 80 proteins. To demonstrate the practical utility of the developed approach, we studied the global effects of the O-GlcNAcase inhibitor GlcNAcstatin G on the level of O-GlcNAc modification of cellular proteins. About 200 proteins including several key players involved in the hexosamine signaling pathway showed significantly increased O-GlcNAcylation levels in response to the drug, which further strengthens the link of O-GlcNAc protein modification to cellular nutrient sensing and response.
O-GlcNAc proteins:
UBA6, SHOT1, MEX3A, TPC13, CNOT1, PGP, CE051, SMHD1, CC85C, I4E1B, ZBBX, B2R8K8, B2RB32, B3KNS4, B3KUR4, B4DF70, B4DIH0, B4DIR9, B4DTN6, B8XCX8, DX39A, BACH, GTPB1, SMAP, AP3B1, PSD12, PSMD9, ATOX1, PGRC1, SPT5H, TAF4, DFFA, CLIC1, EIF3F, WASL, IPO5, EF2K, PLOD2, MEIS1, PSDE, IMA4, BCL9, SDCB1, NOP56, IMA3, ARI1A, UBFD1, CCS, DVL2, KMT2D, ANM5, TNPO2, GEMI2, HAT1, MYPT1, GAK, XPO1, ZN609, SC16A, SR140, PUR4, NKRF, ZN185, CASC3, OGT1, PMM2, HMGB3, PPM1G, SHIP2, NVL, NUP42, R113A, KDM6A, DHX15, MCES, RRP8, SERA, DC1L2, ZW10, M3K7, RIPK2, WDR62, TXNL1, IF4G3, E41L2, FOXO3, DENR, XPOT, BUB3, ACTN4, HTSF1, SGTA, SYNC, LANC1, DHX16, ZNRD2, KPRB, AQR, GANP, HNRPQ, BUB1B, DIAP1, PLIN3, ANM3, CTND1, EIF1B, USO1, IF2P, NBN, SRGP2, N4BP1, ROCK2, CLAP2, CPNE3, BRE1B, ZC11A, CLU, T22D2, ANR17, GGCT, HMMR, VATG1, FLNB, NCOR1, SPAG7, PR40A, GGYF1, PSIP1, NDUS3, SRS10, KHDR3, SF3B1, CSDE1, PRKRA, KS6A5, NPM3, LYPA1, U520, TIPRL, OFD1, WDHD1, CD123, EIF3G, PSD10, SPF27, CIAO1, RMP, TOX4, SC24D, ST65G, UBXN7, PLPHP, NFAT5, SOGA1, UBP19, WDR47, SC31A, HEXI1, UBR5, SCAF4, UBE4B, ELP1, ZRAB2, KIF4A, VAPB, SNAPN, 6PGL, SMC2, ATG7, IPO7, AGM1, ZFYV9, SVIL, BAG4, AHSA1, PARN, PSMG1, SC24A, SC24B, AGRL2, TYDP2, PCNT, YETS4, STABP, ASML, EYA4, CEP43, HS74L, WIZ, STAU1, BAG2, BAG3, BPNT1, ECD, MBD3, BCL10, MOC2B, TOM40, CHK2, GSHR, PNPH, HPRT, ADA, CYTB, OAT, KITH, CPNS1, P53, HSPB1, TYSY, RPN1, RLA1, JUN, LA, NPM, NFL, NFM, ANXA2, SYEP, HS90A, HNRPC, SP1, 4F2, HS90B, ASNS, VIME, GSTP1, LEG1, HMGB1, UCHL1, LKHA4, H2A1, UBC, GLI2, ODP2, LAMP1, G6PD, ADHX, CDK4, SRF, PCNA, HARS1, ADT3, IMDH2, ACTN1, PEPD, XRCC5, LAMP2, RINI, EF2, PLST, ACPH, KAP2, CD99, GLU2B, AK1A1, KPYM, PO2F1, SYDC, ALDR, ERF3A, GNS, ZEP1, DESP, CREB1, GCFC2, UBF1, ATF7, CAN2, PYRG1, TCPA, SON, NELFE, ATF1, NFKB1, ICAL, IMDH1, GSTM3, FLNA, COMT, FBRL, PUR2, PUR6, UBA1, ENPP1, CBL, SP100, NFYA, SAHH, COF1, TENA, THTM, RS12, DNJB1, PSA4, DNMT1, RAE2, PTBP1, SYTC, 1433T, RFA1, APEX1, PYR1, MAP4, CALX, PSA5, NDUS1, TPP2, SHC1, TKT, PML, MARCS, PRDX6, PRDX5, PRDX3, KCY, 2AAA, 2AAB, CDC27, NMT1, SDHA, GDIA, METK2, DNJA1, AKT1, PUR9, HNRH1, S10AB, ARRB2, DCTD, TF2H1, KINH, CSTF2, DUT, TTK, PROF2, CAH8, RFC4, RFC2, HXD13, MYH9, MYH10, ADDA, BASI, NU214, DEK, MYH11, PPM1A, PRS7, ARL3, MP2K2, RL4, 8ODP, NUP62, ZEB1, TAGL2, COIL, VATA, GRP75, TXLNA, STAT3, PEX19, RFC5, RFC3, IF2G, NAA10, KDM5C, CSK, GARS, SYIC, LAP2A, LAP2B, STAT1, EPS15, CASP3, LPPRC, HD, MSH2, GPDM, RANG, VDAC2, CBX5, UBP5, MK09, KI67, RECQ1, ATRX, CRKL, RL21, MAP1B, IQGA1, GLYG, SYQ, ID4, TISD, PPCE, RFX5, GSH0, PRC2A, NEST, RPIA, NASP, FAS, ARRB1, CENPF, SRP09, PCY1A, SYAC, SYSC, PSB2, ACOT2, RBM25, NUMB, NU153, RBP2, GUAA, MRE11, SERPH, PDLI4, VASP, MAP2, LRBA, TCPD, FXR1, FXR2, RAB5C, DUS3, GALK1, HCFC1, IRAK1, UBP11, HDGF, ROA3, 6PGD, IMA1, GDS1, GDIR1, AGFG1, HNRPF, TF2AA, MSH6, KIF11, ZN143, HXK2, THOP1, NUP98, BIEA, PPP5, ARFP2, NUBP1, ACLY, COPB, CCHL, ICLN, SYRC, SYYC, AAPK2, BCAT1, RD23B, KAD2, P5CS, IF5, XPO2, TERA, AFAD, AF17, ADK, DSRAD, PKNX1, ALR, HNRH2, EIF3B, BID, RRP1, IF6, GEMI4, EPIPL, MTPN, TPIS, EIF3E, MYL6, ACTB, IF4A1, RS20, PRPS1, S10AA, DEST, CSN2, ABCE1, RS3A, PSME3, MGN, PFD3, HNRPK, PP1A, RS15A, RUXF, PPIA, RS27A, AP2B1, 1433Z, DYL1, SKP1, IF5A1, RACK1, UBC9, UB2L3, ACTS, CSK21, PA1B2, IGBP1, IF4G2, GTF2I, PI42B, TCPB, RAE1L, GSTO1, PRKDC, TMF1, RL19, SRSF3, MXRA7, FOXK1, XIAP, TFAM, VIGLN, PURA, BORG5, CLH1, NFKB2, U2AF1, FOXK2, AMPD2, NC2B, TFAP4, OTUD4, EWS, CDR2, TOP2B, AKA12, KMT2A, UBXN1, IF4G1, K1C17, LGUL, REL, 1433F, UBE3A, PTN12, SRS11, CALD1, PTN11, PUR1, GFPT1, PSME1, GABPA, RING1, FMR1, KHDR1, KLC1, SRSF1, DHX9, GOGA2, LG3BP, SSRP1, VAC14, NSUN2, RBBP4, NCBP1, AHNK, HSP7E, SCRN1, NU160, FOXO1, TBL3, TFCP2, GRSF1, SFSWA, TP53B, ILF3, ELAV2, TRAP1, FOXC1, TAF10, NFAC3, CSTF3, UBP4, CAF1A, RED, MTAP, LIPA1, FADD, PRDX4, CBX3, STK3, PSMD2, SBP1, SRSF6, TIF1B, PABP4, IFIT5, PHLP, UB2V1, DC1I2, PPIG, TCOF, GOGA4,