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Oh SC, Jeon BC, Jang IH, Song MR, Hwang H, An D, Yue L, Jung Y, Lee Y, Jo S, Park SK, Kim TD. Genetic manipulation of OGT enhances NK cell-mediated cytotoxicity in tumor immunity. Journal of advanced research 2025 40914422
Abstract:
Natural killer (NK) cells are essential effectors in immune surveillance and cancer immunotherapy, but their function is often compromised by metabolic stress and environmental factors within the tumor microenvironment (TME). O-GlcNAcylation, a post-translational modification, regulates immune responses, yet its impact on NK cell function and therapeutic potential in immune cell-based therapies remains underexplored.
O-GlcNAc proteins:
UBA6, PIPSL, KIF2A, DX39A, MYO1F, HAX1, AIP, GTPB1, STXB3, AP3B1, PSD11, PSD12, SPT5H, CLIC1, EIF3F, PK3CD, IPO5, DNM1L, RTCA, IFRD1, PSDE, BIN1, IMA4, STK25, PESC, MPP10, NOP56, IMA3, PPP6, TXND9, COPE, AP3D1, TOR1A, TOR1B, ANM5, CHK1, TCRG1, NDC80, TNPO2, PSA7, SCAM3, IFIT3, IKKB, HAT1, MYPT1, HNRDL, XPO1, SR140, PUR4, ANR28, FYB1, SCAM2, ARPC2, RPAC1, PLS1, SPTC1, SPTC2, OGT1, PPM1G, EIF3D, EIF3H, HDAC3, NVL, PDPK1, TPSN, TTI1, PRP4, DC1L2, ZW10, SNUT1, HNRPR, TXNL1, IF4G3, PPIP1, TIM44, PRC1, ZN207, GET3, BUB3, ACTN4, HTSF1, AP1G1, SGTA, MCAT, CPSF5, STRN, U3IP2, AKAP8, NRDC, ORC5, ORC4, RAD21, KPRB, SMCA5, OPA1, KDM1A, TBCD4, OGA, HNRPQ, NEMF, BUB1B, IF4E2, DIAP1, ANM3, IMA7, LPXN, SNX2, DPM1, CCD22, DKC1, IF2P, DNJA2, WDR1, CLAP2, ZC11A, ANR17, NDUS2, ZPR1, HMMR, VPS4B, H2AY, PEX14, CISY, PR40A, TACC1, VP26A, MPPB, MED24, PSIP1, NDUS3, EED, SF3B1, CSDE1, STX11, KS6A5, U520, TIPRL, NU155, S2512, RNH2A, CD123, EIF3G, EIF3J, IDHC, SASH3, GLRX3, RL1D1, CLPX, CIAO1, SRP72, B3GA3, ST17B, MTA2, STK10, TOM70, UBXN7, PLPHP, GLSK, UBP19, AP2A2, SC31A, UBR5, SCAF4, LETM1, LC7L3, KIF4A, NDUAA, 6PGL, SMC2, IPO7, ARI2, CD2B2, AHSA1, PARN, FMNL1, SC24A, AGRL2, OXSR1, HS74L, PTBP3, AP2A1, RIGI, STAU1, TTC4, AIFM1, BPNT1, ECD, EOMES, MBD3, TOM40, ACL6A, LDHA, DHE3, GSHR, PNPH, AATM, PGK1, HLAB, HLAH, TFR1, ALDOA, G3P, HLAA, CPNS1, RPN1, GNAI2, ITB2, ADT2, IF2A, ICAM1, RLA0, LA, ITB1, LCK, FYN, CDK1, ATPB, CD2, IF4E, ENOA, NPM, HEXA, LDHB, PDIA1, ANXA2, CAN1, TBB5, HEXB, SYEP, HS90A, HNRPC, TPM2, ANXA6, 4F2, HS90B, SRPRA, HEM3, ODPA, PLEK, PTPRC, RU2B, RU17, VIME, GNAI3, ANXA5, RSSA, CD48, HMGB1, GNAO, CN37, ROA1, RU2A, FGR, PARP1, GRAB, RO60, HLAC, ODP2, KAP0, CH60, CLUS, BIP, UMPS, ODPB, ODB2, LAMP1, ACADM, TOP1, TOP2A, G6PD, C1TC, MPRI, PRPS2, PABP1, PCNA, HARS1, IMDH2, TPR, GRAA, ODBA, XRCC6, XRCC5, LAMP2, RINI, NCAM1, ITA4, EF2, PDIA4, P4HA1, CEAM1, HLAE, PLSL, ACPH, ETFA, GYS1, KAP2, T2FB, MTDC, GLU2B, HCLS1, FPPS, AK1A1, ENPL, IL2RB, PO2F1, HNRPL, ETS1, ALDR, ERF3A, EZRI, UCHL3, VAV, RS2, RFA2, CD44, H15, H12, NCPR, FER, PLCG2, UBF1, KAPCA, CAN2, PYRG1, DDX5, PRS6A, TCPA, PTN1, RL7, PGAM1, DNLI1, XRCC1, NUCL, HXK1, RPB3, SPEE, CSK22, NFKB1, TYPH, IF2B, ANXA7, PSB1, MPRD, LMNB1, ITAL, GRAH, IMDH1, RASA1, PRPS3, CD11B, VATB2, VATC1, FLNA, VDAC1, ODBB, OSBP1, FBRL, RS4Y1, PUR2, PUR6, UBA1, ROA2, KAPCB, QCR2, ITA6, MAOM, SYWC, RS3, SAHH, H2B1O, COF1, IF4B, EF1B, AT5F1, THIL, MCM3, TYY1, ATPA, PSA1, PSA2, PSA3, PSA4, ITB7, MOES, U2AF2, RL13, IVD, MGAT1, HMGB2, PTBP1, SYTC, SYVC, EF1G, NKG2A, 1433T, MK03, DCK, CALR, CALX, P85A, PSB8, PSB9, PSA5, PSB4, NDUS1, DPOD1, MK01, AMPL, CD38, T2EA, TPP2, TKT, CASP1, PML, EF1D, OAS2, RL12, ECHM, PDIA3, 2AAA, 2AAB, HLAF, HMOX2, PURA2, PUR8, ILEU, AL1B1, SDHA, COR1A, GDIA, DNJA1, AKT1, QCR1, PUR9, HNRH3, HNRH1, 1433B, STIP1, GBP1, GBP2, ELF1, RL9, ACSL1, KINH, LSP1, MCM5, MCM7, GLYM, HSP74, PHB1, PTN7, RADI, RFC4, RFC2, T2FA, MYH9, ADDA, BASI, DEK, PRS7, MP2K2, RL4, LONM, PP1G, GNL1, ODO2, NUP62, FDFT, TALDO, ETFB, RBMX, VATA, RL3, OST48, AN32A, TCPZ, PSB10, RL13A, MLH1, IF2G, NAA10, CSK, GARS, SYIC, ACTY, ECI1, LAP2A, LAP2B, MTREX, RHG25, EPS15, CASP2, CNDD3, LPPRC, THIM, WASP, MATR3, MSH2, SSRA, RANG, NAMPT, PRS6B, EFTS, VDAC2, UBP5, KI67, RAGP1, BAG6, RS9, RS5, IQGA1, GLYG, CAZA2, CAPZB, SYQ, UCRI, ATPO, PPCE, PI42A, COPD, GSH0, PSMD8, TCPE, HSP13, IDHP, PK3CG, AGRE5, DPOD2, AL9A1, LMAN1, NASP, FAS, FNTA, DHYS, TCPG, RM19, INPP, PCY1A, SYAC, SYHM, PRI1, PRI2, CTCF, PSB3, RBM25, NU153, RBP2, RGS3, NDUV1, TAF6, GRAK, 5NTC, GUAA, MRE11, IDH3A, GDIB, EMD, SPB9, VASP, PPT1, RL14, TCPQ, TCPD, ANX11, FXR1, FXR2, GRAM, RB27A, RT29, SMCA2, IDH3G, TPMT, MECP2, PSMD7, UBP11, HDGF, ROA3, 6PGD, IMA1, IMA5, GDS1, JAK3, GDIR1, HNRPF, KIF11, RBM5, SPSY, HXK2, CAZA1, NUP98, ACLY, SUCA, PGTB2, CATC, SC24C, ICLN, SYRC, SYYC, UBP14, AAKG1, RD23A, RD23B, SNAA, IF5, PSMD4, DRG2, XPO2, TERA, ECHB, ELL, NP1L1, DSRAD, SEC13, PSA, SCOT1, EIF3B, SYMC, CATW, IF6, CORO7, NU107, GSDMD, SELB, EIF3E, PP4C, IF4A1, PRPS1, PSA6, SRP54, ARP3, ARP2, ACTZ, CSN2, RS3A, PSME3, VA0D1, HNRPK, 1433G, RS7, PP1A, PP1B, PRS4, PRS8, RS8, RS16, 1433E, RS18, RS11, PRS10, RL7A, ERF1, RS4X, RS6, H4, RAN, GBB1, GBB2, RL8, TRA2B, AP2B1, 1433Z, 2ABA, RSMN, RACK1, YBOX1, TPM4, ACTC, TBA4A, TBB4B, CSK21, H31, NOP14, RPP30, GTF2I, PI42B, TCPB, RAE1L, PRKDC, IN35, RT22, RT35, RT34, COG7, RHG04, RBM10, CDK6, PURA, CLH1, NFKB2, HNRPU, U2AF1, SET, CAP1, HMCS1, EWS, ODO1, KIF23, BDH, MP2K1, FKBP4, RL6, TOP2B, M2OM, LMNB2, CEBPZ, UBXN1, IF4G1, 1433F, UBE3A, PTN11, PUR1, GFPT1, EXOS9, GABPA, TNFC, RL18, C1QBP, KHDR1, KLC1, SRSF1, RHG01, PP2BA, SSRP1, NSUN2, RBBP4, NCBP1, APOBR, AP1B1, MPPA, NU160, TF3C1, AKP13, CAD17, SF3A3, TRI26, AIMP1, ILF2, ILF3, LMAN2, TRAP1, PP1R8, STRN3, CDC16, STK4, FLII, RM28, LCP2, CSN1, CAF1A, CAF1B, AAPK1, EI2BE, TADBP, AIMP2, PRDX4, PAK2, PSMD2, DNJC3, SRSF9, SRSF5, TIF1B, G3BP1, SLAF1, PABP4, MTA1, EIF3I, ITAD, 2A5G, CTBP1, AP3B2, DC1I2, ORC2, IKZF1, XRCC4, TCOF, SF3B2, FKBP5, NFAC2, PICAL, SQSTM, TBB3, RIPK1, HDAC1, KCC2D, DCTN2, ULA1, ITPK1, IQGA2, SNX1, PWP1, CUL1, CUL4A, CUL4B, FCL, AAMP, MOGS, NACA, THOC5, DX39B, BLMH, EXOS2, BYST, NFYC, CKAP5, COTL1, HNRPD, BOP1, UBE4A, KEAP1, EIF3A, ARHG7, UBP2L, MLEC, DPOA2, DCTN1, DYHC1, EI2BA, FLOT2, RCN2, FKBP8, GNA13, GALE, CAPR1, BECN1, CASL, HLTF, MCM6, IRF3, TRIPC, PUM1, MDC1, SMC1A, UBP10, GANAB, RFTN1, 2A5D, PTCA, CASP8, IMB1, CND2, FL2D, ABRX2, SART3, CND1, EXOS7, ACAP1, U5S1, SYLM, SNX17, RB3GP, SYK, RRS1, ARHG6, DPOD3, ACAP2, WDR43, PDIA6, PCM1, IPYR, PTPA, PWP2, RASA2, RBBP5, KS6A2, PCBP1, PCBP2, SF3B3, DLGP5, RSU1, SAFB1, SF3A2, PP1R7, SC23A, SC23B, SF3A1, TERF2, MARE2, TSN, PCH2, TRIP4, MARE1, ELAV1, NSDHL, TAB1, AAAT, TBCE, STXB2, NEDD8, SEPT7, ADRM1, PSMD5, PKN1, 2A5E, MK14, CDC37, DPYL2, RBBP7, SRSF7, CPSF6, SMN, NRF1, NDUA9, PCKGM, HCDH, CP51A, UGPA, MIC60, HNRL2, PDS5A, AAK1, TSR1, LRRF1, P3H1, TRM5, UAP1L, TIM50, PAR14, GLYR1, CE022, ACSF3, GRAP1, FA98B, PDCD4, UBP39, AGK, EIPR1, RHG15, ACTBL, HS904, NOM1, PP6R3, COQ5, TOIP1, SYAM, GNAS1, S27A3, SAMD9, P4R3B, TDIF2, RBG1L, EXOS6, HP1B3, UBR4, UBAP2, QNG1, RBM26, NT5D1, RIF1, VPS53, RSBN1, RN213, F91A1, MAP1S, INT3, RHG17, C19L1, VIR, ATLA3, IQEC1, SMYD5, TWF2, CNDH2, P4R3A, PDE12, TM214, PPR18, ZCHC8, ERAP2, CDC73, EDC4, PRP8, SCYL2, PDXD1, GIMA6, CTR9, AAGAB, ZC3HE, LARP1, ATAD2, CP20A, CWC27, RFIP1, HSDL2, SYNE3, GDPP1, QSOX2, BGIN, BCAP, UN13D, TBA1A, SPT6H, SND1, 5MP2, DHX30, EIF3M, CSN6, KDM3B, NUP54, MYH14, CLAP1, HEAT3, HDGR2, DCXR, WAPL, RHG30, HUWE1, UB2Q1, PATL1, NOP9, PABP2, LYRIC, UBP48, CAND1, HOOK3, ZC3C1, SKAP1, DDX42, LRC33, P66A, HPS6, ZNG1B, CRLF3, ARMC8, DEN1C, ARI3B, CEP97, ANKH1, CCAR1, DJC10, NELFD, MIRO2, SIR2, RAVR1, SPB1, ERF3B, EXOC8, A16A1, PELP1, TTC5, MIER1, CCAR2, NUP93, LRC47, PIAS4, RHG18, STAG2, OGFD1, SH2D3, CPSF7, ARFG2, ARFG1, PAF1, ANR44, DDX51, GBP7, KRI1, MLKL, AFG2A, NHLC2, GT251, RDH13, NF2IP, PDPR, PSD4, ABCF1, SHCBP, PCAT1, DOCK8, FAD1, NUP43, NUP37, TOIP2, ATLA2, GIMA7, SMRC2, NPL4, PUM2, UBA3, TBC15, CIP2A, PNPT1, MO2R1, PKHO2, DTX3L, BRX1, DCA11, IPO4, NOC3L, ZC3HF, HDAC7, NU133, PDC6I, CHMP7, CTF18, LEO1, SCFD1, HNRLL, UBCP1, CKAP2, ATX2L, PRP31, NELFB, PSPC1, MADD, CTBL1, SEPT1, TITIN, DDX1, GBF1, RTF1, NICA, RT27, ELMO1, UBXN4, HS105, CNOT9, GCN1, HMHA1, PRP16, NU205, RT31, AN32B, PGTA, TFG, HDAC2, GGH, SHIP1, SEM4D, RAD50, OSTF1, ARHG1, GSLG1, RENT1, CSN5, SMRC1, SMRD2, FUBP2, TNPO1, GLMN, USP9X, UBP7, SMCE1, RRF2M, NCLN, FAKD4, CCD47, EXOC4, EXOS8, DOC10, DCPS, FAF2, FXRD1, LRC58, HVCN1, SNR40, SLAF6, RM38, SAAL1, DNJA3, PTCD3, CYFP2, GIMA5, CCD97, EDC3, WDR89, THOC1, OTUB1, TRM61, PGM2, LTV1, PLPP, SMRD1, TOE1, DDX27, ERO1A, PGAM5, DDRGK, FUBP3, SPF45, SYNM, SUCB2, ITCH, COG3, CK5P3, ELMO2, TMX3, UBP47, CNDP2, ZFR, PRRC1, RPR1A, IPO9, MIA2, RBM14, GBP5, GBP4, PUS7, VPS35, PURB, XPO6, H2A1A, SPAG5, SNX18, EFGM, ERBIN, FNBP1, PIGS, WRIP1, SRPK1, STRBP, IWS1, SIN3A, INT14, RBM15, RUFY1, RMD3, TBCB, PSB7, CNN2, PSMD1, AGAP2, EYA3, NEUR1, SORT, DNJC2, NUP88, POP1, TSNAX, EIF3C, DNJC7, METH, HCD2, SGMR1, ROAA, NP1L4, CPNE1, TCPH, ARI3A, H2A1J, H2B1L, CND3, DDX50, RNZ2, GRWD1, CMS1, TBL1Y, ECSIT, MEP50, TBA1C, APOL2, MBB1A, RM45, ADPGK, ZNG1A, PELO, TRI56, ERP44, ESYT1, CCM2, CSN4, MTA3, MCMBP, AASD1, AN32E, TMM43, TBCD, HGH1, TBB6, HNRL1, DDX23, MTNA, THUM3, TBB2B, NOC4L, UT14A, NUP58, GNL3, NUP85, HIRP3, THIC, RBM4, NADAP, NAA15, SRRT, HDHD5, MAK16, RTF2, RM04, RM01, MK67I, YTHD1, RM37, GTPB4, OSBL8, TBL1R, NIBA1, UCK2, API5, FTO, UBE2O, XPO4, WDR12, UBA5, CLPB, NAT10, KLC2, ILKAP, XRN2, PAR12, 5NT3A, CYRIA, GBP3, TMX4, ASCC2, PDCL3, RBGPR, DHX36, PININ, TMX1, GCP60, UN45A, OFUT1, TOR3A, GLP3L, GOLP3, DEFI6, TRABD, OSBL3, EHD1, CAPAM, HEAT1, NOL6, LDAH, WDR55, RANB3, RPF2, WDR26, PHAX, UBE2Z, ACAD9, GHC1, ARP8, ARMT1, LRC40, SFXN1, COG4, ARP5, RM44, L2HDH, CSN7B, RPA2, PPCS, NJMU, XPO5, PKHA2, PARVG, ABC3G, MCCB, CWC22, SYTL2, GPN1, GOPC, APMAP, SH22A, RT30, EXOS4, OSGEP, DCP1A, RIC8A, SLAF7, TIGAR, RTN4, RPR1B, EXOS5, EXOS3, XPP1, SAS10, BIRC6, DDX21, SHLB2, EI2BG, FBX6, AAAS, BAZ1A, STRN4, PNO1, F1142, SYFB, KLC4, ATG3, PDS5B, SMC4, OLA1, ECHD1, ZCHC3, ABHDA, ABCF3, CYRIB, GIMA4, DJC11, INT7, FANCI, ATD3A, INT13, DDX18, RPC5, RBM28, RBM22, SLTM, BABA1, HPF1, LYAR, THUM1, BABA2, KCTD5, CARF, PP4R2, DPP3, AATF, TBA8, TE2IP, BCLF1, RM39, UGGG1, ERAP1, HPBP1, OGFR, GMIP, BCCIP, STK26, CPSF2, SYLC, RBM27, SUCB1, ATX10, NCDN, TFP11, ORC3, SAE1, COPG2, ASH2L, EIF3K, GRHPR, DJB11, SAE2, NXF1, SE1L1, BIN2, STK39, TES, SEC63, NDRG3, SUN2, SRP68, SEPT9, DDX20, S30BP, PUF60, NRBP, EI2BD, VATH, IPO11, CYH4, XPO7, VPS51, KAD3, LCAP, CNOT7, NAGK, TRM6, S2513, DBNL, DCTN4, APC7, ANC2, STML2, DBR1, MRT4, CPSF3, DP13A, RCOR1, RALY, TF3C4, IKZF2, IKZF3, ACINU, CNO11, BAG5, PSME2, DNPEP, ACSL5, NOB1, PRP19, VPS4A, G3BP2, PACN2, SNX6, PSD13, FAF1, DIM1, CSN3, NSF1C, MACF1, PP6R1, TRI33, TBD2B, DICER, SRRM2, PA2G4, SMC3, T3JAM, RUVB2, CDYL, RUVB1, NUDC, BCS1, VDAC3, SYFA, DRG1, RRP44, RCL1, GSTK1, PTN22, AP3M1, TR150, WBP11, TDRKH, GIT1, AAR2, SHLB1, LC7L2, DHRS7, RT02, SBDS, RRP15, STRAP, FBX7, 3BP1, T22D4, NOC2L, TLN1, DCAF1, RBM19, UBP15, HYOU1, ATG4B, TELO2, AFG32, ARI1, SAM50, PRC2C, PPME1, CTDP1, PAXB1, UCHL5, VATD, TNPO3, SRPRB, CERT, TF3C5, NUBP2, PUS1, NPTN, RT18B, COPG1, AUP1, MTCH2, STK24, 5MP1, DC1L1, WASF2, ENPP4, NS1BP, S23IP
Species: Homo sapiens
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Xu S, Zheng J, Xiao H, Wu R. Simultaneously Identifying and Distinguishing Glycoproteins with O-GlcNAc and O-GalNAc (the Tn Antigen) in Human Cancer Cells. Analytical chemistry 2022 94(7) 35132862
Abstract:
Glycoproteins with diverse glycans are essential to human cells, and subtle differences in glycan structures may result in entirely different functions. One typical example is proteins modified with O-linked β-N-acetylglucosamine (O-GlcNAc) and O-linked α-N-acetylgalactosamine (O-GalNAc) (the Tn antigen), in which the two glycans have very similar structures and identical chemical compositions, making them extraordinarily challenging to be distinguished. Here, we developed an effective method benefiting from selective enrichment and the enzymatic specificity to simultaneously identify and distinguish glycoproteins with O-GlcNAc and O-GalNAc. Metabolic labeling was combined with bioorthogonal chemistry for enriching glycoproteins modified with O-GlcNAc and O-GalNAc. Then, the enzymatic reaction with galactose oxidase was utilized to specifically oxidize O-GalNAc, but not O-GlcNAc, generating the different tags between glycopeptides with O-GlcNAc and O-GalNAc that can be easily distinguishable by mass spectrometry (MS). Among O-GlcNAcylated proteins commonly identified in three types of human cells, those related to transcription and RNA binding are highly enriched. Cell-specific features are also revealed. Among glycoproteins exclusively in Jurkat cells, those involved in human T-lymphotropic virus type 1 (HTLV-1) infection are overrepresented, which is consistent with the cell line source and suggests that protein O-GlcNAcylation participated in the response to the virus infection. Furthermore, glycoproteins with the Tn antigen have different subcellular distributions in different cells, which may be attributed to the distinct mechanisms for the formation of protein O-GalNAcylation.
O-GlcNAc proteins:
RBM47, E2F8, SBNO1, CNOT1, HMX3, ABTB3, RHG32, P121C, PDLI1, SNP23, PSMD9, TAF4, ARI1A, ABLM1, STX16, HGS, MYPT1, SC16A, SR140, SET1A, FYB1, TIF1A, PPM1G, SHIP2, EIF3D, NUP42, KDM6A, TET3, SI1L1, DC1L2, HNRPR, PRPF3, TPD54, E41L2, ZN207, BUB3, AKAP8, ZNRD2, MYPT2, GANP, HNRPQ, DIAP1, PLIN3, MAFK, TBL1X, MITF, N4BP1, ZC11A, T22D2, PP6R2, ANR17, BCAS1, NCOR1, SPAG7, TIPRL, SPF30, TOX4, TOX, PCF11, AGFG2, ZFPL1, KIF4A, SC24A, SC24B, CNOT4, ASML, M4K4, BPNT1, PX11B, CHK2, LMNA, GLPA, TFR1, ALDOA, GCR, HSPB1, GNAI2, RLA1, RLA2, RLA0, K1C18, K2C8, RB, CATD, SYEP, PTPRC, VIME, GSTP1, HMGB1, ROA1, ATX1L, DERPC, ZN865, TPR, LAMP2, EF2, PLSL, PLST, GLU2B, HCLS1, PO2F1, RAC2, ATF2, ZEP1, TFE2, MUC1, CREB1, JUNB, ATF7, PTN2, DDX5, SON, ATF1, CSK22, NFKB1, FLNA, PUR2, RFX1, CBL, COF1, PTBP1, ARNT, DCK, PYR1, MAP4, CALX, 3MG, PRDX6, CDC27, AMRP, CLIP1, ZEP2, HNRH1, 1433S, ELF1, LSP1, PTN7, IRS1, ADDA, NU214, CUX1, TXLNA, MLH1, ECHA, IF2G, HNF4A, LAP2B, GPDM, RANG, KI67, CRKL, CAPZB, RFX5, SOX2, CAMLG, NASP, FAS, CDK8, SRP09, YLPM1, NU153, RBP2, TAF6, EMD, LRBA, PAPOA, HDGF, AGFG1, HNRPF, HXK2, NUP98, ATX1, RD23B, AF10, AF17, DSRAD, FOXA1, HNRH2, NU107, TPIS, PSME3, TPM4, F193A, GTF2I, PHC1, PRKDC, MAP1A, SARNP, FOXK1, FBLN2, FAM3A, EM55, NFKB2, HNRPU, SPTB2, FOXK2, RUNX1, FLI1, SATB1, SP2, MP2K1, NUCB1, KMT2A, IF4G1, TLE4, KPCT, PSME1, GABPA, PRDX1, ACK1, AHNK, IFFO1, GALT2, SRBP2, TROAP, BPTF, TP53B, CBX3, NFAC2, PICAL, CUL4B, ASPP2, NFYC, CDK13, VEZF1, UBP2L, SRC8, CAPR1, LAGE3, PUM1, MDC1, EPN4, RRP1B, NCOA6, GSE1, UBP10, 2A5D, MEF2D, LASP1, NUMA1, CND1, TEBP, PCBP1, RBMS2, SF3A1, TSN, SF01, MED1, TRIP6, ELF2, TAB1, ZFHX3, ZYX, ADRM1, DPYL2, TAF9, MAPK3, CSPP1, PDS5A, QSER1, AAK1, LRRF1, VP26B, ACSF3, TPRN, CRTC2, PAN3, YIF1B, PRC2B, CEP78, ZN362, FKB15, LRIF1, CAF17, UBAP2, NT5D1, AHDC1, LYRM7, RPRD2, ZN318, TASO2, TBC9B, ARID2, C19L1, ABLM2, TWF2, GRHL2, CPZIP, NIPBL, LIN54, ZCHC8, C2D1A, SCYL2, NFRKB, RSBNL, MDEAS, ZC3HE, LARP1, SAMD1, FIP1, CRTC3, SAS6, MCAF1, BCOR, GGYF2, NBEL2, CO039, SRCAP, UBN2, TM1L2, ASXL2, SPT6H, MEPCE, BOP, KDM3B, ERMP1, TRM1L, ZCCHV, KANL1, POGZ, ZFY16, NUFP2, MAVS, EMSY, RAI1, I2BP2, SRGP1, RHG30, SH3R1, HUWE1, YTHD3, GALT7, LYRIC, BCL9L, CASZ1, TSYL5, DDX42, CACL1, P66A, I2BP1, VRK3, FOXP4, ARI3B, TEX2, MGAP, ANKH1, SUGP1, MILK2, ERF3B, K2013, PHAR4, XRN1, ZN687, FNBP4, ARFG1, ENAH, NHLC2, AVL9, XXLT1, GOLM1, TXND5, SERB1, CHSTE, SLAI1, TNR6A, PHC3, SP20H, VP37A, KMT2C, ARI1B, KNL1, NEDD1, ALMS1, PREX1, DLG5, GEMI5, PIGO, UBS3B, WIPF2, FRS2, PDC6I, ZFN2B, TPC12, SEN15, PCNP, LMO7, ATX2L, CSKI2, PSPC1, P66B, GBF1, SMG7, RTF1, TOPB1, PHF3, MAML1, TTC9A, PRCC, RREB1, CBP, DDX17, SEM4D, ARHG1, GPKOW, FUBP2, LPP, TTC28, PF21A, FAF2, ESS2, EDC3, A7L3B, P121A, PDLI5, FUBP3, VCIP1, PDLI2, Z512B, ZFR, EP400, PRRC1, NOL4L, RBM14, PURB, NACC1, CIC, MED15, NUDC1, SIN3A, AEDO, MINT, HTF4, CNN2, RGPD5, ATX2, HCD2, S29A1, ARI3A, SH3G1, TRIR, DPH2, MGME1, ERP44, ESYT1, CCM2, CNPY3, WAC, DIDO1, HGH1, MMTA2, PAXX, NTM1A, RBM4, SGPP1, HEMGN, HDHD5, YTHD1, FTO, CEP44, BC11B, PITH1, SP130, BRD8, RGAP1, I2BPL, ADNP, DHX36, FOXP1, CENPH, WNK1, E41L1, ZHX3, YTDC2, RANB3, PHAX, ECT2, CNO10, MLXIP, PKHA5, PKHA1, RC3H2, LY9, RDH14, TAF9B, NCOA5, TANC2, TNR6C, CHD8, SDF2L, ARFG3, UBN1, RTN4, PDLI7, CHSTC, STRN4, PNO1, BMP2K, RBM12, STAU2, TXLNG, PNPO, CARF, TAB2, TMOD3, CDK12, F120A, HPBP1, ITSN2, CNOT2, CHMP5, VAPA, CAMP3, RBM27, KANL3, RERE, ZN219, SE1L1, STAP2, LIMD1, TCF20, SEPT9, UBQL2, TRPS1, S30BP, NRBP, EI2BD, SIX4, APC7, TASOR, GMEB2, PARP4, MA1B1, ACINU, ZHX1, CDV3, MRTFB, ZBT21, YETS2, HECD1, ZMYD8, SCAF8, PP6R1, TRI33, TNR6B, ZC3H4, SHAN2, SRRM2, CTND2, SCML2, ZN148, T3JAM, VDAC3, PLAK2, DDX52, NOP58, GIT1, ZN281, SIT1, SALL2, ARIP4, CRBG1, HYOU1, KLF12, PRC2C, YTHD2, CD2AP, TNPO3, SRPRB, TSSC4, NUBP2, HCFC2, FHOD1, NCOR2, GMEB1, NCOA3, S23IP
Species: Homo sapiens
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Zhu Y, Willems LI, Salas D, Cecioni S, Wu WB, Foster LJ, Vocadlo DJ. Tandem Bioorthogonal Labeling Uncovers Endogenous Cotranslationally O-GlcNAc Modified Nascent Proteins. Journal of the American Chemical Society 2020 142(37) 32870666
Abstract:
Hundreds of nuclear, cytoplasmic, and mitochondrial proteins within multicellular eukaryotes have hydroxyl groups of specific serine and threonine residues modified by the monosaccharide N-acetylglucosamine (GlcNAc). This modification, known as O-GlcNAc, has emerged as a central regulator of both cell physiology and human health. A key emerging function of O-GlcNAc appears to be to regulate cellular protein homeostasis. We previously showed, using overexpressed model proteins, that O-GlcNAc modification can occur cotranslationally and that this process prevents premature degradation of such nascent polypeptide chains. Here, we use tandem metabolic engineering strategies to label endogenously occurring nascent polypeptide chains within cells using O-propargyl-puromycin (OPP) and target the specific subset of nascent chains that are cotranslationally glycosylated with O-GlcNAc by metabolic saccharide engineering using tetra-O-acetyl-2-N-azidoacetyl-2-deoxy-d-galactopyranose (Ac4GalNAz). Using various combinations of sequential chemoselective ligation strategies, we go on to tag these analytes with a series of labels, allowing us to define conditions that enable their robust labeling. Two-step enrichment of these glycosylated nascent chains, combined with shotgun proteomics, allows us to identify a set of endogenous cotranslationally O-GlcNAc modified proteins. Using alternative targeted methods, we examine three of these identified proteins and further validate their cotranslational O-GlcNAcylation. These findings detail strategies to enable isolation and identification of extremely low abundance endogenous analytes present within complex protein mixtures. Moreover, this work opens the way to studies directed at understanding the roles of O-GlcNAc and other cotranslational protein modifications and should stimulate an improved understanding of the role of O-GlcNAc in cytoplasmic protein quality control and proteostasis.
O-GlcNAc proteins:
P121C, PSD11, PSD12, PGRC1, DDX3X, IRS4, PUR4, ARPC3, PSMD3, IF4G3, ACTN4, CPNE3, NDUS7, SC22B, MPPB, RL1D1, SC31A, 6PGL, GNAS3, HS74L, NB5R3, LMNA, OAT, RPN1, JUN, PDIA1, SYEP, ANXA6, ASNS, PABP1, HARS1, IMDH2, PLSL, ENPL, NDKA, PYRG1, TCPA, GSTM3, PIMT, PUR2, SFPQ, PPIB, RS12, PSA3, PSA4, SYTC, RL10, MAP4, CALX, PRDX6, PRDX3, METK2, HXA10, DNJA1, QCR1, PUR9, HNRH3, HNRH1, 1433B, STIP1, RL9, MCM7, PROF2, RL22, MYH9, COPB2, NU214, PRS7, NUP62, TALDO, TCPZ, RFC3, IF2G, GARS, ECI1, LPPRC, MATR3, RAGP1, RL5, CAPZB, SYQ, SYAC, NU153, TAF6, GUAA, TCPQ, ANX11, HNRPM, NUP98, COPA, SC24C, SYRC, AT1B3, RD23B, P5CS, XPO2, DSRAD, PSA, EIF3E, DEST, UBE2N, ABCE1, 1433G, PRS8, RS18, PRS10, RL23, GNAS2, IF4G2, KRT85, GSTO1, PRKDC, SRSF3, ALEX, EWS, MEF2A, IF4G1, SRSF1, SF3A3, CSN1, AIMP2, CBX3, STF1, CUL4B, DX39B, MCM6, GANAB, PDIA6, IPYR, SF01, ZYX, ADRM1, CDC37, AMOT, GNAS1, HP1B3, UBAP2, RBM26, SND1, POGZ, PTOV1, CCAR1, CISD2, NNRE, PDC6I, ATX2L, NDRG1, HS105, TFG, DDX17, FUBP2, FKB10, PDLI5, ZFR, RBM14, VPS35, PHB2, TS101, TCPH, NUP58, NAA15, PTN23, AMPB, PDLI7, DDX18, IF2B1, HPBP1, VAPA, SYLC, ATX10, SRP68, COR1C, VDAC3, DRG1, RRP44, PRC2C, 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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