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Wong YK, Wang J, Lim TK, Lin Q, Yap CT, Shen HM. O-GlcNAcylation promotes fatty acid synthase activity under nutritional stress as a pro-survival mechanism in cancer cells. Proteomics 2022 22(9) 35083852
Abstract:
Protein O-GlcNAcylation is a specific form of protein glycosylation that targets a wide range of proteins with important functions. O-GlcNAcylation is known to be deregulated in cancer and has been linked to multiple aspects of cancer pathology. Despite its ubiquity and importance, the current understanding of the role of O-GlcNAcylation in the stress response remains limited. In this study, we performed a quantitative chemical proteomics-based open study of the O-GlcNAcome in HeLa cells, and identified 163 differentially-glycosylated proteins under starvation, involving multiple metabolic pathways. Among them, fatty acid metabolism was found to be targeted and subsequent analysis confirmed that fatty acid synthase (FASN) is O-GlcNAcylated. O-GlcNAcylation led to enhanced de novo fatty acid synthesis (FAS) activity, and fatty acids contributed to the cytoprotective effects of O-GlcNAcylation under starvation. Moreover, dual inhibition of O-GlcNAcylation and FASN displayed a strong synergistic effect in vitro in inducing cell death in cancer cells. Together, the results from this study provide novel insights into the role of O-GlcNAcylation in the nutritional stress response and suggest the potential of combining inhibition of O-GlcNAcylation and FAS in cancer therapy.
O-GlcNAc proteins:
RUXGL, ADAS, DX39A, MYO1C, IPO5, PESC, NOP56, DDX3X, SCD, MGST3, HNRDL, XPO1, SURF4, OGT1, PPM1G, MOT4, DHX15, CYB5B, SERA, HNRPR, BUB3, ACTN4, MYO1B, GANP, HNRPQ, NDUS7, MPU1, H2AY, FLNB, SC22B, SF3B1, U520, UTP20, NU155, ATP5H, RL1D1, MTA2, RTN3, VAPB, IPO7, ACSL3, BAG2, TOM40, LDHA, DHE3, AATM, PGK1, ASSY, LMNA, TFR1, ALDOA, K2C1, G3P, HSPB1, RPN1, AT1A1, ADT2, PCCA, RLA1, RLA0, LA, K1C18, K2C8, ATPB, ENOA, NPM, TPM3, LDHB, PDIA1, ANXA2, TBB5, TRY1, PROF1, SYEP, HS90A, HNRPC, DAF, 4F2, HS90B, ODPA, RU17, VIME, RS17, K2C7, GNAI3, RSSA, LEG1, ROA1, PARP1, PRS56, HS71B, ODP2, THIO, MGST1, CH60, BIP, HSP7C, GTR1, TOP2A, PYC, PABP1, PCNA, ADT3, IMDH2, KCRU, XRCC6, XRCC5, EF2, K1C10, K2C5, PDIA4, PLST, ETFA, MIF, KPYM, ENPL, HNRPL, PLAK, EZRI, NDKA, RS2, DESP, H13, NCPR, AT2A2, DDX5, TCPA, PTN1, ARF4, RL7, RL17, NUCL, GSTM3, FLNA, FBRL, PUR6, UBA1, ROA2, QCR2, SFPQ, PPIB, RS3, SAHH, COF1, MCM3, RS12, ATPA, U2AF2, RL13, S10A4, PTBP1, SYVC, EF1G, STOM, RL10, APEX1, PYR1, CALX, TKT, ERP29, PRDX6, PRDX5, PRDX3, RL12, PDIA3, CPSM, HNRH1, STIP1, L1CAM, PRDX2, P5CR1, DUT, MCM7, GLYM, HSP74, PHB1, RL22, MYH9, SOAT1, DEK, K22E, RL4, LONM, NUP62, GRP75, IF4A3, RL3, RL13A, ARL1, STAT3, MDHM, RFC3, ECHA, SYIC, LAP2A, LPPRC, MATR3, MSH2, GPDM, VDAC2, KI67, BAG6, RL27A, RL5, RS9, STT3A, CAPZB, SYQ, RL29, AT5G3, TCPE, RL34, FAS, TCPG, EFTU, ACADV, TMEDA, NU153, RBP2, CPT1A, SERPH, RL14, TCPQ, TCPD, FXR1, RAB5C, RAB7A, HCFC1, ROA3, 6PGD, HNRPM, IMA1, HNRPF, MSH6, TXTP, ACLY, COPA, MOT1, SYRC, KAD2, P5CS, XPO2, TERA, NP1L1, DSRAD, ATPK, TMM33, TPIS, MYL6, IF4A1, RS20, S10AA, RAP1B, RL15, RL37A, HNRPK, RS8, RS16, 1433E, RS14, RS23, RS11, RUXE, RL7A, RS4X, RS6, H4, RAB1A, RAN, RL23, RS25, RS26, RL10A, RL11, RL8, PPIA, RS27A, RSMN, RACK1, ACTG, UBC9, TBA1B, TBB4B, GTF2I, TCPB, PRKDC, RL24, ARF5, RL19, SRSF3, S25A3, CLH1, HNRPU, SPTB2, EXOSX, RL18A, RL6, IF4G1, K1C17, PRDX1, RL18, C1QBP, KHDR1, DHX9, NCBP1, AHNK, NU160, SF3A3, ILF3, ACACA, PRDX4, CBX3, TIF1B, SPTN1, HNRPD, SAFB2, TTL12, CAPR1, ITPR1, RRP1B, GANAB, LBR, GOGB1, IMB1, NUMA1, SUZ12, U5S1, RRS1, PDIA6, PLEC, TEBP, NONO, PCBP1, PCBP2, DHC24, SF3B3, SF3A1, TRAM1, ELAV1, AAAT, RBBP7, H31T, PDS5A, TSR1, IF2GL, RRP12, NU188, HP1B3, EF1A3, PPR18, PRP8, C1TM, DHX30, CAND1, MISP, SPB1, PELP1, RDH10, CCAR2, TXND5, STT3B, BRX1, PO210, GEMI5, RT27, HS105, GCN1, NU205, AKAP1, AN32B, RBP56, DDX17, FUBP2, TNPO1, UBP7, UTP4, LRC59, PGAM5, FUBP3, MBOA7, MCCA, WRIP1, UHRF1, POP1, HCD2, ROAA, TM9S2, TCPH, ANM1, H2B1L, RNZ2, MEP50, MBB1A, ESYT1, H2AJ, GNL3, HDHD5, GTPB4, API5, RPF2, SFXN1, RDH14, ABCB6, DDX21, MDN1, DCA13, ATD3A, DDX18, MIC19, TEX10, TECR, MYOF, THYN1, HACD3, RRBP1, ABC3B, RLP24, ACINU, OGDHL, COR1C, PRP19, SSRG, TRI33, EIF3L, RUVB1, VDAC3, PDIP2, NOP58, SF3B6, RTCB, RL36, LAS1L, SRPRB, COPG1, MTCH2, CEPT1, ZNT1
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, HCFC1, 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, TLE3, 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, QSPP, 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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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, TPM3, 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, GRP75, 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, STAT1, 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, HCFC1, 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, SNUT2, 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: Homo sapiens, Mus musculus, Sus scrofa, Bos taurus
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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, PHB1, 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, 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, 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, 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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