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Luna S, Malard F, Pereckas M, Aoki M, Aoki K, Olivier-Van Stichelen S. Studying the O-GlcNAcome of human placentas using banked tissue samples. Glycobiology 2024 34(4) 38253038
Abstract:
O-GlcNAcylation is a dynamic modulator of signaling pathways, equal in magnitude to the widely studied phosphorylation. With the rapid development of tools for its detection at the single protein level, the O-GlcNAc modification rapidly emerged as a novel diagnostic and therapeutic target in human diseases. Yet, mapping the human O-GlcNAcome in various tissues is essential for generating relevant biomarkers. In this study, we used human banked tissue as a sample source to identify O-GlcNAcylated protein targets relevant to human diseases. Using human term placentas, we propose (1) a method to clean frozen banked tissue of blood proteins; (2) an optimized protocol for the enrichment of O-GlcNAcylated proteins using immunoaffinity purification; and (3) a bioinformatic workflow to identify the most promising O-GlcNAc targets. As a proof-of-concept, we used 45 mg of banked placental samples from two pregnancies to generate intracellular protein extracts depleted of blood protein. Then, antibody-based O-GlcNAc enrichment on denatured samples yielded over 2000 unique HexNAc PSMs and 900 unique sites using 300 μg of protein lysate. Due to efficient sample cleanup, we also captured 82 HexNAc proteins with high placental expression. Finally, we provide a bioinformatic tool (CytOVS) to sort the HexNAc proteins based on their cellular localization and extract the most promising O-GlcNAc targets to explore further. To conclude, we provide a simple 3-step workflow to generate a manageable list of O-GlcNAc proteins from human tissue and improve our understanding of O-GlcNAcylation's role in health and diseases.
O-GlcNAc proteins:
TRGV5, TVBL4, HV320, TM275, MRCOL, EXC1L, TVB74, TVBK3, FEZF1, DEND3, MTMRB, PI4P2, POTEF, ARB2P, U17L3, LIRA5, S22AV, O6C75, SHSA7, TCPQL, SIG16, O4C45, P12LL, D11L8, ARG33, CD15L, YQ037, ZN487, TDR15, ERVV1, NACAM, ADAS, TAF4, CLIC1, MATN2, LORF2, ACACB, ARI1A, NCKP5, IRS4, ADA10, ZN609, SC16A, MCF2L, ERC2, ARHGB, FANCG, TNC18, MRP5, SIA8E, DDX3Y, MEFV, TET3, TTI1, SI1L1, SERA, M3K13, SNUT1, MTSS1, ZN208, HXA3, HNRPR, IF4G3, FOXO3, KCNQ2, LAT, BUD23, MYO1B, NRDC, S28A2, KIF1C, ADCY3, JIP4, SI1L3, TRAK2, L37A3, OPA1, GANP, KDM1A, FZD6, PLIN3, F262, SH21A, MMP20, ROCK2, LRP5, GLRA3, ZN217, USH2A, MYCB2, NU155, P3C2G, NALF2, CABYR, CDKA2, TRIO, C1QRF, CBPD, OR7C1, RECQ4, RECQ5, BAIP3, ATG12, NFASC, SRBS2, PCF11, ABLM3, SC31A, KCNK2, UBR5, AGFG2, SPN1, UBE4B, SCEL, CAC1H, RTN3, EPN2, STBD1, OR6A2, KCNH1, SMC2, TACC2, ZBT7A, CLD9, AGRL2, GLP2R, LGI1, MBD3, ANGT, EGF, IL2RA, LV223, IGHG3, IGHG4, IGHM, CO1A1, CO2A1, CO3A1, CO4A1, FETA, HMDH, A1BG, TBB4A, CP1A1, RPN2, ALDH2, HEP2, CO5A2, INSR, GELS, TY3H, ACBP, LDHB, NFM, CATD, TBB5, CBG, PFKAM, INHBA, CO4A2, IL6RA, PKHD1, HXB5, DLDH, IFI6, DANCR, DU4L4, O13C7, CC192, EFCE2, TZAP, LYAG, TGFB3, HSP7C, PSG1, MPRI, PRPS2, FGF5, COBA1, CO6A3, RLBP1, KCRU, MYH1, HEM1, K1C13, CO6, COBA2, ENPL, ATF2, VAV, IGLL1, PGCA, ZN823, HSP76, JUND, PFKAL, EGR1, XRCC1, K2C4, CADH2, TSN8, LFA3, ITIH1, TYPH, PSB1, CO9A1, C4BPB, NEBU, PRPS3, FLNA, NF1, MUTA, TENX, IDS, PROZ, KS6B1, PTPRZ, MYL9, CO8A2, ITA3, 3BHS2, SYVC, PON1, VATL, CD82, MAP4, TPP2, EPHA8, CO4A5, MPIP1, V2R, SC6A1, CLIP1, HXD11, 3HIDH, PRDX2, DSG3, C2TA, ACSL1, CSTF2, MRP1, MCM7, BMP8B, HSP74, TRY3, PCGF2, ADML, ADA1A, GGT2, VATA, HSPA9, COFA1, PK3CB, PI4KA, CNDD3, THIM, MAGAC, ABCG1, KI67, NOP2, UTRN, PA24A, OR1D4, TNFL6, SC6A8, IREB2, PK3CG, RPIA, SYCC, RBP2, RGS3, GSK3B, MNX1, F10A1, LRBA, TCPD, SMCA2, GALK1, IRAK1, DHB4, NEK3, ROA3, MYOM1, IMA1, JAK3, ZN142, EFNA4, SMTN, SC24C, ATX3, SYYC, HSP72, RD23A, GYS2, LMIP, SYMC, DPOE2, HDAC4, PER3, BACE1, BCAR1, CORO7, KCNKA, SESN2, FOXL2, ATS20, C1QT8, SIA8F, RS6, VPK21, POK7, HBA, RNF4, IRX4, DEN2B, SSBP2, RT05, EFNB1, AT8B2, EM55, HXC5, PLCB2, PSG9, E2F1, CO4A3, OCRL, NAAA, CO7A1, DSG1, MUC3A, GUC2D, AKA12, DYST, CREM, ROM1, KIME, COAA1, COEA1, KDSR, ZO1, SOS2, PP2BA, DHX9, CACB2, GOGA3, CLM6, SPIR1, EP300, AHNK, KLH30, MN1, SIAT6, WASC5, KCMA1, RB40B, DLG1, NFAC3, ABR, STK4, CSN1, IFT88, KLF10, RFA4, PSMD2, MMRN1, M3K1, IFIT5, PDE3B, ADAM9, BIRC2, OLIG2, CUL4B, DYR1A, PTC1, THOC5, CAYP1, CDK13, CO4A6, NID2, VEZF1, DELE1, BTG3, DYHC1, NPAT, E2F2, FLNC, LRC32, NF2L1, FAT1, HABP2, SCN5A, ITIH4, TRIPC, NCOA6, MBTP1, PTCA, ICAM4, MYPC3, COJA1, NAA25, CND1, ACAP1, SETB1, RRS1, RYR3, KS6A1, SURF1, TAF7, OR7A5, PCH2, MED1, JHD2C, U2AFM, HERC1, CAC1E, B2LA1, MIA, QPCT, RTN1, PPR3A, SIA4B, PTPRN, SYT16, COOA1, DOK7, CSPP1, INF2, MICB, KI26B, BLTP1, MGAL, SC5A9, RPEL1, TMM44, SMTL2, COSA1, KLH38, FR1L6, S4A8, RGL3, WDR72, CCD14, C2CD3, HYDIN, SRCRM, GREB1, SEZ6, DHB12, SETMR, SDK2, DCAF6, ACTMP, ACBG2, ESCO1, FREM1, PWP3B, BRD10, MTX3, AKAP4, PREP, RRP12, FRPD3, DOP1, SNP47, MUC21, SAPC1, SNPC4, EYS, MRP7, RBM20, ZFY27, CAMP1, RM02, ADIPL, LITD1, KANK4, TTBK1, MTCL3, BIG3, STPG1, RAIN, RIF1, OBSCN, MRCKA, EF1A3, AGAP9, TCRGL, RSBN1, C1QL3, DEN4C, RRAGB, USPL1, EST4A, RN123, RN213, EGFLA, TENS2, SAXO2, ICE2, MAP1S, B3GNL, RPGP2, NR3L1, USF3, ZFY26, CR063, S31H1, WWC2, BLT3A, MRCKG, RGPA1, NADE, CPZIP, ALKB2, DHX57, MSD2, ACSM6, BGP11, ZN549, CCD62, S2534, TXD11, XKR2, GP179, TRAF7, CORO6, ARL9, ANR11, CRTC1, CSPG4, CP20A, EST3, PRS57, XKR5, PAMR1, ITIH6, FAT4, NHLC1, BCOR, IGS10, GGYF2, ATL5, EMAL6, NFXL1, ALKMO, NBEL2, DMP46, NBEL1, RFLA, CFA47, TPGS1, UBN2, MROH5, TPRG1, PHLP2, ACD11, UBP54, UBP43, UB2R2, MD13L, KNDC1, SND1, TEDC2, NDUF7, FA2H, VASH1, GRP2, CXXC5, ZCCHV, GLUCM, VP35L, MIER3, CA2D4, ZFY16, CSMD3, LFG1, PK1L2, GDF7, HEAT3, MDGA2, BRAP, MUC19, RBBP6, SH3R1, RAB44, TAF8, TARSH, VP13B, TMED4, UBP37, K1328, ALPK2, ACOT1, CN023, PABP2, MTA70, LYRIC, BCL9L, GGN, CASZ1, VASH2, MOGT3, NAL14, NLRC5, HEAT4, RLGPB, CIR1, MICU3, HOGA1, GA2L3, PRSR1, ZGRF1, THNS2, C2CD5, KR191, TMTC1, AHNK2, MGAP, ANKH1, LMTD2, ZC3H3, SP8, MILK2, REM2, ELMD2, CORA1, MAML2, DSEL, MIER1, INT1, SCML4, LRC43, CIART, CLIP4, CMYA5, PRR18, T151A, PAQR4, FBXL6, SRBD1, NKAP, TBC19, MEIOB, IGSF1, TEX26, ARFG2, ARI2O, SIGL1, DCBD1, AMER3, ABTB2, SYT2, TRIML, DAAF3, LMTD1, LMBL4, FANCB, NHLC2, DRAXI, SIDT2, DHB11, P5I13, CAMKV, MACA2, SMG8, RN214, HMCN2, LRTM3, RB15B, TNR6A, BHE23, DIK2A, CC112, ZSWM2, ZMIZ2, COMA1, MYRIP, NEK11, O4F15, O51S1, OR6T1, OR6K6, O10R2, OR1FC, LIRB1, KI18A, NPL4, MUC7, ALMS1, LKAM1, MO2R1, DSCL1, GTR14, GRP4, ACTT1, CHD5, DMXL2, DLG5, HAVR2, LMX1A, SH3R3, FBF1, FNIP1, ZN526, SETD7, COG1, FRS2, LMO7, TCP11, NELFB, PALLD, ATRIP, STON2, AGRV1, CNKR2, MUC16, ASB15, TITIN, S39A7, NR4A3, MAML1, HS105, AKAP1, RYR2, TENR, RREB1, CBP, PRG4, GLMN, DVL3, TNR25, SBP2L, NKD2, POP5, P33MX, SOSB2, RPE, CR3L1, MSI2H, NXPE2, SGTB, TV23C, DTBP1, MCRS1, MISP3, LRC46, CFA36, FUBP3, BOD1, HPDL, LRIG1, M4A14, DYH8, VPS39, SPTCS, MAML3, ZN333, LCOR, MY15B, S35E1, PHAR3, P12L2, ALPK3, IFT74, PRRC1, CCDC7, DNHD1, HARB1, CFA44, SPT33, TTC14, HUTU, LRRC7, QRFPR, GPR78, NOE3, PGRP2, ARHGH, GBP4, SIG12, PP1RA, DEPD7, PHF12, MAGI1, TAAR9, MED15, GCP5, HMCN1, CRML, WDR24, S22AC, TM209, CP2S1, NIBA2, STAC, AGAP2, PLIN2, PKP4, PI3R4, PMYT1, EPYC, LYST, COCA1, SMAD5, ZNT3, TEP1, TBL1Y, SLF1, SYT15, TIRR, PSF3, ZN649, CRDL1, ZSA5A, TBB2B, TRPM6, C1QT4, PINK1, COPA1, TEX15, AN30A, PECR, K1671, CDHR2, GSDMC, TRI55, PITM3, CPEB1, BARH1, IRX2, CFA74, TANC1, LNP, ASXL3, SRCN1, WDR33, ARP3C, BRD8, RBM38, I2BPL, TRPV6, S6A17, GBA3, CAD23, VPS11, SLK, HIPK2, ATS10, E41LB, UBQL3, KDM4C, SEM6C, RIBC2, PDZD7, AT133, MT21D, CCNP, GORS2, PANK3, SPE39, AGO3, RPA2, S28A3, LY9, TENS1, TM165, NCKX3, MUC5B, CAN10, SPON1, NCOA5, TANC2, PLXA4, TRI39, PDE11, WDR6, MLXPL, OSGEP, UBN1, MEPE, ANO2, BIRC6, ARHG4, KCNQ5, MXRA5, 4ET, SH2B1, SNRK, KCNH7, SIA7A, LRC4B, MDN1, FX4L1, ZBT40, DECR2, SPS2L, HAUS2, AKIP, OXSM, SIR5, ZDHC7, ING3, SNTG2, SO1C1, DACT1, CELR1, CELR3, ERAP1, PDXL2, DTL, PA2GE, MYOF, CNOT2, LRP1B, FOXJ2, AKA7G, YP008, SIRPG, PHRF1, PLCE1, ZSWM5, DYH2, JCAD, FPRP, CT2NL, CHD7, HTR5B, F135A, UNC79, RRBP1, UBP35, KANL3, NYNRI, ZN219, HNF6, MYO1A, DBF4A, KCNN3, AAKG2, RPGFL, MED13, VAX2, ENPP5, DP13A, BORG2, TLK1, PO2F3, MUC12, CDV3, TEN1, TRPC5, PADI1, DEN2A, F184B, INO80, MRTFB, ZBT21, HECD1, ZMYD8, CAPS1, COHA1, KMT2B, BARX2, PCDGK, PACN2, ATS8, BSN, LHX6, MACF1, PHF8, IQEC3, LIMC1, ANR26, UBP24, CBPC1, TUTLB, SRRM2, CNTN6, CHKB, RT33, ZN652, SL9A8, ANKR6, PKHA6, SIK3, YBOX2, COG6, ZBT32, LSM2, PHOCN, RTCB, GRIP1, WNK2, LMBL1, DMXL1, ARIP4, MTCL1, CRBG1, PRC2C, YTHD2, PCDB7, SPO11, CD2AP, ENTP2, CERT, MRCKB, NR2E3, HEBP2, NCOR2, COX11, AP1M2, NCOA3, M3K4
Species: 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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