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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, CC168, 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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Hung YW, Ouyang C, Ping X, Qi Y, Wang YC, Kung HJ, Ann DK. Extracellular arginine availability modulates eIF2α O-GlcNAcylation and heme oxygenase 1 translation for cellular homeostasis. Journal of biomedical science 2023 30(1) 37217939
Abstract:
Nutrient limitations often lead to metabolic stress during cancer initiation and progression. To combat this stress, the enzyme heme oxygenase 1 (HMOX1, commonly known as HO-1) is thought to play a key role as an antioxidant. However, there is a discrepancy between the level of HO-1 mRNA and its protein, particularly in cells under stress. O-linked β-N-acetylglucosamine (O-GlcNAc) modification of proteins (O-GlcNAcylation) is a recently discovered cellular signaling mechanism that rivals phosphorylation in many proteins, including eukaryote translation initiation factors (eIFs). The mechanism by which eIF2α O-GlcNAcylation regulates translation of HO-1 during extracellular arginine shortage (ArgS) remains unclear.
O-GlcNAc proteins:
TVBY1, TX13D, CC195, SPEM3, TVB42, FR1L5, HFM1, CCD66, SBNO1, Z804B, LRRD1, XIRP2, POTEF, PSD1, BDP1, NKX26, SWAHB, F181B, SMCO2, MGT4D, CAN8, EPOP, SMHD1, AKD1B, T200C, AQP73, AXA2L, NTM2B, ZAR1L, AN36A, NEU1B, GG6L6, B2R853, KDM4E, HNRC2, ERVV1, HNRC3, TEX22, TM232, MEIOS, CK098, SO1B7, TEX46, KIF2A, BACH, MYO1C, AP3B1, IKBE, HIP1, TULP1, WASL, PDE2A, SAP18, DNM1L, IFRD1, ZN593, FAAH1, PESC, SDCB1, MPP10, NOP56, DDX3X, CCN1, PLPP3, NCKP5, AGRB1, AP3D1, IDLC, CHD1, CHD2, PDCD5, ANM5, H17B6, FPGT, TCRG1, KIF3C, GEMI2, ML12B, CLGN, MYPT1, S27A2, XPO1, AT2A1, PLXB2, SR140, PER2, GRRE1, MCF2L, NACAD, ATS3, ANR28, VILL, LAMA5, MATN3, ATX7, INP4B, TRI18, GPR37, RPA34, MAGB3, PER1, KDM6A, DHX15, TTI1, PRP4, SERA, ADA12, IRAK2, ZW10, SNUT1, SPIT2, SRGP3, VIP2, PRPF3, GRID2, TGON2, LAT, SYT7, PLRG1, BUB3, PLPP2, PI15, ACTN4, SCO2, IDH3B, CALU, AGRB3, MED14, FGF17, PRKN, JIP4, KIF5C, ZC3H1, KATIP, OPA1, KIF1B, NMD3B, PEPL, PLXC1, ADCY9, HNRPQ, TPST1, RNBP6, CCNT1, FAIM3, ANM3, HCN1, RT14, HNRC1, H2B1K, PQBP1, PRAF2, DKC1, IF2P, TRI13, DNJA2, BRD4, NBN, IGSF3, DEN4B, ADA23, MFA3L, CLAP2, OBSL1, BRE1B, RFIP3, KDM4A, DJC13, ANR17, ZPR1, NIPS2, HMMR, ZN217, SC22B, PR40A, DPOLQ, ZN254, PSIP1, ERLN1, ECI2, KHDR3, TADA3, SF3B1, MED6, FOXH1, SPB7, U520, UTP20, TCEA3, SPI2, KLF7, MMP23, RASF9, CCNK, PRAF3, DYSF, SPF27, ATP5H, TRIO, RL1D1, NEBL, OCTN2, PDE9A, SRP72, B3GA3, UBP1, SLIT2, TOM70, MICA2, NFASC, FARP2, ERLN2, PRP6, GLSK, RNF37, WDR47, AP2A2, CE152, HEXI1, UBE4B, CSPG5, LETM1, LC7L3, KIF4A, GOSR1, KAT7, MRP6, TNKS1, KCNK5, VAPB, IPO7, M3K6, UTS2, CD2B2, FMNL1, SGPL1, G6PE, SC24A, ACSL3, DUS4L, ZBT11, CPSF4, K2C75, HERC2, SNP29, AP2A1, WIZ, STAU1, BAG2, ONEC2, TOP3B, APCL, PX11B, PAK4, LDHA, NB5R3, F13A, MOS, PGK1, TRYP, OVAL, IGHG1, IGHG2, IGHG3, IGHG4, HLAH, HBE, LMNA, ALBU, VTDB, TRFE, FRIH, MIS, VTNC, TDT, ALDOA, ANXA1, APOB, OAT, K2C1, SEMG1, TBB4A, G3P, NTRK1, P53, HSPB1, RPN1, RPN2, B3A2, AT1A1, CP17A, ITB2, HMGN1, CFAI, PCCA, IF2A, HMGN2, RLA1, RLA2, RLA0, AP2A, INSR, AGAL, RB, CDK1, ATPB, ENOA, NPM, H2B1J, LDHB, H10, CATD, ANXA2, CO8A, TBB5, PROF1, HS90A, HNRPC, TPM2, GLI1, ACM2, CEL2A, HS90B, SRPRA, ODPA, CO4A2, MET, RU17, VIME, RS17, K2C7, ANXA5, K1C16, RSSA, GSTP1, RU1C, VILI, HMGB1, TPM1, WNT2, ROA1, C1S, PARP1, H2BFM, ATX1L, MYZAP, ZCC18, POTEI, POTEJ, SP9, UBB, UBC, MPC1L, ST1A4, HS71B, C1C1L, IGG1, D130B, M14OS, TBA3D, PR20G, TZAP, ACRO, H14, ODP2, THIO, PPGB, CH60, THA, BIP, HSP7C, ODPB, PYGB, PYGM, BCR, SPTB1, TOP1, PYC, DMD, C1TC, PABP1, K2C3, CO6A2, SKI, FETUA, ACTN1, MYH7, XRCC6, XRCC5, EF2, K1C10, K1C13, K2C5, TNNT1, COBA2, SUIS, KPYM, ENPL, CCNB1, HNRPL, MYOD1, EZRI, AREG, NQO1, RS2, CD44, H15, H13, H12, YBOX3, ZNF18, ZN182, ZNF43, HSP76, HMGA1, ZNF8, KPCA, CXA1, UBF1, DESM, NEUM, CR1, IBP3, TCPA, ITB5, RL7, SON, RL17, SDC1, K2C4, NUCL, E2AK2, CSK22, NCF2, FST, IF2B, ANXA7, CD33, BTF3, TNR1B, RAB3B, CAN3, ICAL, CO5A1, PHOS, CD11B, CSRP1, FLNA, PERL, TENX, PUR6, UBA1, H1T, ROA2, SAV, FBLN1, TCEA1, ITA6, SFPQ, PPIB, RS3, PTPRE, H2B1O, COF1, IF4B, CPT2, CCND1, RAE1, KPCL, THIL, RPB1, LAMA1, DNJB1, ATPA, DDX6, CTNA2, DNMT1, U2AF2, RL13, S10A4, HMGB2, PTBP1, HGFL, STOM, PON1, 1433T, RL10, CALR, MAP4, CALX, PSA5, ABCD3, LYOX, HXD10, PTPRM, PTN4, T2EB, EPHA2, EPHA8, TKT, LMOD1, EF1D, RL12, PDIA3, 2AAA, MPIP3, BKRB2, NKTR, KPYR, SDHA, HXA10, HXA9, GBRA5, DNJA1, AKT1, HNRH1, 1433B, S10AB, P5CR1, IFNA8, DSG3, RL9, KINH, CP2CI, H2B1B, EVI2B, HS71L, HSP74, PHB1, MERL, RADI, RL22, T2FA, SCN1A, K1C9, FBN1, FBN2, IRS1, MYH9, MYH10, COPB2, SOAT1, FUS, DEK, CYLC1, MYH11, AHR, K22E, ACHA7, RL4, LONM, ACV1B, SRP14, ZEB1, TAGL2, BRCA1, VATA, HSPA9, RS19, RL3, OST48, FEN1, TXLNA, TCPZ, ARL1, UBP8, RFC3, ECHA, IF2G, PERI, BUD31, NAA10, KDM5C, GARS, SYIC, NBL1, LAP2A, LAP2B, EPS15, RS27, LPPRC, RL35, PF2R, MUC18, MATR3, GPDM, RANG, NAMPT, EFTS, KI67, RAGP1, ATRX, IF2M, BAG6, RL27A, RL5, RL21, RS9, RS5, RS10, MAP1B, IQGA1, IF1AX, OMP, RL29, ATPO, TCPE, K2C6C, KC1A, MASP1, HSP77, TCPG, EFTU, SRP09, SYAC, SYCC, SYSC, YLPM1, TMEDA, RBM25, TSC2, GUAA, ENTP1, MEOX1, ST1A1, ST1A2, GATM, SERPH, KNTC1, CDK9, R144A, RL14, TCPQ, TCPD, FXR1, RAB7A, ZNF83, SSRD, AL3A2, DHB4, PSMD7, CCL11, ZNF41, ROA3, MYOM1, HNRPM, IMA1, IMA5, MP2K6, HNRPF, MSH6, HMGA2, CRIP2, COPB, COPA, CRBB1, SMTN, MOT1, IST1, SC24C, TCP4, SYRC, ATX3, TERF1, SYYC, HSP72, ATNG, EPHA4, GYS2, DRG2, XPO2, MFAP1, PAR2, BRPF1, NP1L1, ANM2, PSA, EIF3B, SYMC, HDAC4, IF6, RP1, NRG3, H2BFS, UBS3A, WDR4, SNX16, SELB, SESN2, H2B1D, NAL11, DJB13, TPIS, MYPR, MYL6, ACTB, IF4A1, RS20, S10AA, CDC42, DEST, SRP54, RAB2A, RAB14, ZC3H6, ACTZ, ARF3, ABCE1, RS3A, RL26, RL15, RL27, RL37A, DCAF7, HNRPK, RRAS2, RS7, RS8, RS15A, RS16, 1433E, RS14, RS18, RS29, RS13, RS11, SMD1, SMD2, ARF6, RL7A, RS4X, ACTA, RL23A, RS6, VISL1, H4, H2B1C, RAB1A, RAN, RL23, RS15, RS24, RS25, RS26, RS30, RL39, RL31, RL10A, RL32, RL11, RL8, PPIA, RS27A, RL40, TRA2B, AP2B1, 1433Z, 2ABA, RL38, RACK1, ACTG, ACTH, YBOX1, CSK2B, TPM4, ACTC, EF1A1, ACTS, TBA1B, TBA4A, TBB4B, CSK21, HBG1, HBG2, NOP14, RPP30, PHC1, S35A1, PRKDC, M3K9, SSBP2, RT22, RT11, RT09, ATL3, RL24, RL19, SRSF3, MUC5A, TFAM, CLH1, NFKB2, HNRPU, MYPC1, MDM2, U2AF1, AMPD2, DIAC, CAP1, K22O, CAC1D, EXOSX, PFKAP, EWS, CO4A3, AK17A, CENPE, MMSA, BDH, DSG1, H11, GHRHR, M3K10, PLOD1, RL6, PO3F1, CAV1, KMT2A, TAP2, ZN117, IF4G1, SRS11, EF1A2, CALD1, AT5G2, PTN11, GABP1, ZN33A, FMR1, PRDX1, RL18, C1QBP, CKAP4, PDE4B, KHDR1, SLC31, SOS2, SRSF1, ACTN3, TLE5, SRSF4, DHX9, GOGA2, DSC1, SSRP1, CAMP2, NSUN2, AHNK, DIK1C, LR74A, LMOD3, CF210, GALT2, AP1B1, HMGX3, NU160, TBL3, TF3C1, ASPH, TROP, BPTF, CNTN1, SFSWA, CHD3, SF3A3, NMDE1, TP53B, ILF3, TIAM1, AKAP6, FLII, TRDN, ACACA, ZBT17, REST, TADBP, ROA0, CBX3, STK3, CBLB, DNJC3, M3K1, SRSF6, I15RA, G3BP1, ATM, AP3B2, PPIG, TCOF, SF3B2, GOGA4, ROCK1, TOP3A, SQSTM, MED21, MTX1, TBB3, PRP4K, ATR, KCC2D, TDG, SNW1, DGKZ, CUL1, S12A1, MOGS, NACA, THOC5, NOG2, PTK6, TBB2A, CAC1C, CKAP5, CO4A6, LRP8, PDE1C, BOP1, SEPT6, MORC3, EFR3A, UBP2L, SIM2, DYHC1, ELOA1, TRI25, MYPC2, FRG1, CAPR1, RBM39, SCN5A, PDIA5, HS902, ZN266, ZN235, SMC1A, RRP1B, NCOA6, GANAB, 2A5D, MVP, LTBP1, GOGB1, GRM7, CHD4, LASP1, RB39A, IMB1, PSME4, CUL7, NAA25, RTP5, MO4L2, SEPT2, SUZ12, U5S1, BRD3, EEA1, PDIA6, PCOC1, PDK2, PLEC, PCM1, NONO, RASA2, RNPS1, PCBP1, PCBP2, SF3B3, RYR3, CNN3, SF3B4, RBMS2, SF3A1, SIX1, MED22, TRAM1, SF01, TRIPB, OASL, MED1, TRIP6, TWST1, PI5PA, CEBPE, AAAT, TOM34, NCOA1, GRK1, SCN9A, ZYX, SEPT7, UAP1, GBRA6, CSRP2, CDC37, IL17, DPYL2, M3K11, SRSF7, CPSF6, AT2B3, H2A2C, H2B2E, HCDH, FA98C, TIGD6, NKPD1, KNOP1, ESRG, PDS5A, MOONR, BLTP1, KIF7, TSR1, C19L2, CO3, PRTG, GAB4, ZN750, P3H1, RA1L2, MA7D1, CHD9, TKFC, PTHB1, RABL6, TBB8, CRFM7, GLYR1, C2CD3, LARP7, TB10B, A20A4, GRAP1, MIDN, PKDCC, CN177, CEP55, KLH22, PLA1A, SGO2, ACTBL, BRDT, H90B4, H90B3, H90B2, HS905, ODFP2, ESCO1, SH319, AN36C, PPM1J, FGD3, RRP12, CF157, ZN484, GNAS1, GASP1, EOGT, BRM1L, H2B2F, PPM1L, TM201, CA167, TT39A, HP1B3, CE170, FREM2, CE85L, SZT2, AXDN1, EYS, ZC3HD, GPTC4, RBM20, UBR4, GNTK, ER6L2, HENMT, TTC22, FRY, B2L15, KAD9, M3K21, DDI2, MROH9, EFCB6, A20A1, CROCC, CL060, OBSCN, FA78B, EF1A3, PR38B, BRE1A, SMBT2, SPO16, TASO2, MALR1, ECM29, SHE, NAA35, TM268, RES18, K2C79, KFA, WSCD1, F91A1, CP135, AR6P4, MROH7, UTP25, RHG17, Z518A, SCAR3, KDM4D, IQEC1, XAF1, OVOS1, CAPR2, IQCE, ZN770, F166A, NIPBL, LIN54, TET2, TEN4, OGFD2, TM214, CAVN1, CDC73, ARMX5, MED27, ANM9, PRP8, PLBL1, NFRKB, ALKB5, TRI40, TBA3E, PONL1, TTC33, MYO7B, RICTR, BRWD3, POTEE, POTEA, CC171, S4A10, FIP1, PRS55, LRSM1, SBSN, CLM9, LRIG3, RSPO2, TMC5, RFIP1, CD109, HSDL2, B3GN6, CCNI2, M3K15, LN28B, NFXL1, DYH12, RN207, ITPI1, CRACD, YC006, PLPL7, FGD6, PHLP2, ANKS3, YS043, NEK10, KRA55, KRA52, VP13C, UBP34, RAPH1, UBP51, UBP45, UBP50, IKIP, MD13L, TBA1A, B4GN4, ATS13, HECW1, BT2A1, SND1, DDX46, TM10C, RSRC2, DET1, H2A3, FAKD5, NLRC3, SSX6, MOT9, OVCH1, PLPR4, PCLI1, NRK, MON2, K1C28, K1C27, K1C25, CSMD3, NUFP2, SZRD1, NPHP3, TT21B, GDF7, KI21A, CFA91, ZN438, HDGR2, SDK1, SPRE1, SRGP1, RBBP6, NECA2, SH3R1, SEN54, K2C1B, CNTRL, CTU1, RM55, VP13B, AGRE4, GLRX5, ZN605, DAAM2, K1328, PATL1, DDX53, TRPT1, LYRIC, AKA28, KTN1, GTD2A, ABCAD, EST1A, PHLB1, LUZP1, THOC4, IFTAP, LRRT4, ZCH18, ARHGP, MON1A, THOC6, AMGO1, AMGO3, AROS, CHSS1, DDX42, NIBA3, CEP57, DAAF5, LYPD6, STX12, DZIP1, HORN, KLOTB, WFDC8, GLT13, ZDH13, CRLF3, CRERF, ARMC8, K0825, ANKY2, AHNK2, DYH10, P3H2, SPNS2, VSTM4, WDFY1, PHF6, SULF2, CHERP, ANKH1, PHC2, CMA1C, F217A, DDIAS, RB12B, SP8, DDX60, RAVR1, SPB1, DRC7, EFC13, CKP2L, SRRM1, CCD13, ELOA2, CC105, ZN100, SMYD4, MICU2, CFA46, RN168, CHSS2, RTKN2, DOCK3, AGRF3, XRN1, ASPM, DSEL, RBIS, SPICE, TAGAP, NDUF2, VPS52, LRC47, K2C78, MYO1H, KLH34, H2B3B, ANR35, GAPT, UB2J2, AN36B, LAT4, EH1L1, PALS1, FNBP4, GUF1, RIBC1, NIN, ZN276, ZN561, SRBD1, NKAP, MACOI, PAR16, AADAT, IQCF1, EFNMT, KLDC1, PLD5, ANR31, CDYL2, AMER3, NEPR1, YJ012, MUT7, BANP, SR1IP, TOPZ1, CO053, PR38A, UBP38, UN13C, FANCB, GOLM1, GT251, DHB11, TM145, SERB1, DYHC2, CC020, GIMA8, TNR6A, ZN740, DIK2A, ZN738, ABCF1, DUS18, ZN548, EXPH5, KMT2C, ABHDB, MYRIP, KNL1, RDM1, O52E5, DDX55, MAFA, ZFP28, THOC2, KCNG3, TTC8, PI42C, TBC15, MIEAP, CIP2A, ZN507, CERK1, BICD2, CHD6, HELQ, CHD5, KCNG4, BRX1, CLM1, OTU7A, ATS16, DYH5, DQX1, TP4AP, WHAMM, UBS3B, AT8B4, SHRM3, WIPF2, F222B, ZC3HF, PPIL4, CCD12, HDAC7, PDC6I, CATIN, CO040, SFT2A, SNR27, HNRLL, UBCP1, CQ050, CTL1, CKAP2, SPIR2, ATX2L, ABCAA, SREK1, CRGN, SYNE2, MUC16, P66B, DNJC9, TITIN, DDX1, H1X, TM131, IP6K1, AP3S1, HS105, SEPT8, PRP16, AN32B, TFG, AP2C, STAM1, DPF3, REQU, RBP56, EVPL, DDX17, KIFA3, SEM4D, XPF, SMRD2, RAB1C, FUBP2, KCNB2, USP9X, UBP7, CUL5, VPP1, MED12, TATD2, H2B1H, FBXW7, YIPF5, UBE2F, RL36L, GTPB3, H2B1A, CCD47, FERM2, PLPL2, LRC59, PBIP1, TTC28, BORC7, SPSB1, ANKR9, CC127, DOC10, P5CR2, ROP1L, FAF2, ZN689, AP2M1, NTNG2, KCD12, PGBD4, MTBP, RMXL1, HOOK2, RBM33, DTBP1, TMA16, ALG14, CPNE2, KIF12, SIPA1, THOC1, RM48, DDX27, P121A, TONSL, PDLI5, PGAM5, COX14, AJUBA, A26L1, PAWR, VPS50, JPH4, NEUL4, HSH2D, ZN514, AGRG7, RPGR1, ZFR, NAR5, ALPK3, IFT74, PPR36, LRGUK, DNHD1, KLH15, ZN512, RIPR3, RN145, CFA44, ZDH15, PWP2A, DOCK7, ZN830, BROMI, SCLT1, CNT3B, ANR27, GP101, IPO9, LRC3B, PGRP2, INP4A, ADCYA, GBP4, ZN317, NED4L, SLIK1, NEK1, PP1RA, XPO6, H2A1A, MAGI1, SNX18, S26A8, MCCA, CTGE2, HMCN1, S22AC, RANB9, CCNL2, SMC6, ZN347, STRBP, SIN3A, RBM15, PNKP, SETB2, NIBA2, SCN2A, NELL2, PSB7, SEC62, CDC5L, STAC, AGAP2, GA2L1, DNJC2, PHB2, KIF2C, HCD2, CPNE1, EBP2, H2B1N, H2B1M, H2B1L, MYOC, SEM3C, GDF15, AKAP9, MICU1, TRIR, SLX1, MEP50, TBA1C, SELS, MBB1A, SYT3, NRIP2, FYCO1, GPTC1, RIOK1, LLPH, WDR83, S35A5, PIMRE, SOX7, WAC, MTA3, MCMBP, MED10, LRRC1, TBB6, HNRL1, DDX23, TBB2B, TMED9, RIOK2, ELOV1, RFIP5, ASPN, AP1M1, NUSAP, TDRD1, EMIL2, AN30B, SCAPE, RTF2, DUS16, MK67I, HOIL1, RT26, KRA41, SETD2, TBD2A, ACTBM, CNTP3, PC11X, PC11Y, PUS3, UACA, REN3B, CRNL1, EDEM3, UBXN6, API5, ZFHX2, CFA74, CE295, ASXL3, ZN407, LRC27, WDR12, IMUP, SENP6, CHST5, WN10A, EGLN1, PEG3, CHST6, NACA2, PAIP1, LSG1, KLC2, ZN541, INT2, DDX47, F234A, NUCKS, S6A17, ABCG5, EHD4, P2Y12, VPS11, TARA, SLK, TNKS2, RBP17, RM46, PININ, SNX25, MOD5, MTRFR, HRH4, NDST4, PTN23, SEM6B, MFSD1, PIGU, PLK3, FA83D, TRABD, EHD1, MROH8, PDZD7, TFB2M, DHX35, ZN576, BICC1, Z385D, CCD86, PRR36, RANB3, AT133, NRDE2, METL8, ZN430, CAAP1, NOL11, ZFAN3, F204A, VRTN, MARH7, SFXN1, SPE39, VP37B, UBP42, KANL2, LN28A, EAF6, ZN556, LIN7B, RENT2, XPO5, CP343, MKNK2, UBP29, PLRKT, SPC25, GPR35, SPON1, LST2, TANC2, EPG5, K1586, ZBT26, FBSL, ZN334, SPCS, MYO10, APMAP, ZCC17, VTA1, SYSM, SIX2, DCP1A, MED4, GP108, LUC7L, SCUB2, RM40, CASS4, RTN4, IFT46, RPR1B, ANLN, BIRC6, DDX21, SAR1A, ASH1L, ARHG4, ARHG3, MXRA5, SPTN5, SNRK, STRN4, TRYG1, SOSSC, F1142, LTBP3, KRT84, DIAP3, PDS5B, SMC4, MA2C1, RN146, MDN1, LYRM2, SPS2L, ABCF3, MRGBP, SEP11, MED17, FANCI, DDX18, KLH11, RPC5, SDA1, CS073, ARGL1, PK1IP, HPIP, CB042, SDHF2, NHP2, LYAR, MED29, CWC25, THUM1, SCN3A, TBA8, DYH9, HXC10, FKB11, CELR1, CDK12, FMN2, RTEL1, IL36B, SACS, E2AK3, PA2GE, MYOF, BICRA, NOP53, HACD3, KCMF1, RAI14, VAPA, SLAF8, SIRPG, HCN3, DYH2, RCC2, TEN3, RRBP1, CPSF2, SYLC, ANKY1, HOP2, IKBL1, COPG2, MYOTI, P2RX2, SPAST, TRMB, FA8A1, DBF4A, MO4L1, MALT1, DAXX, MARCO, ZBT47, CGBP1, GCP4, KDM5B, SYWM, HMGX4, NOL12, ARMX3, SWP70, SUN2, AFF4, MKRN1, NPCL1, CHRD1, SEPT9, PCS1N, NB5R1, S30BP, PUF60, SCNBA, DNAI1, BAZ2B, PHF11, VAX2, RABX5, TRM6, ZN391, APC7, STML2, VPS28, CCNL1, FBX9, MRT4, PITC1, GPTC8, PARP4, MYO15, TF3C4, ADA28, NUP50, ZN236, ZN346, HCN2, ZN214, NRX1A, ZN608, MRTFB, ATD2B, NEB1, SHRM4, TMCC3, MYO5B, TPX2, NP1L2, MAFF, NOTC3, PRP19, G3BP2, RHG26, CHIP, MAGD2, SSRG, ING4, DIM1, TTF2, L10K, LIMC1, AGAP1, TNR6B, ZC3H4, THS7A, RIMS2, SRRM2, CTND2, BAIP2, SCN8A, PPR3C, LAMP3, RTRAF, RUVB2, LZTS1, TN13B, SYFA, SIGL7, DRG1, NCKP1, TLR6, ATF5, DIP2C, DLGP4, FYV1, KDM2A, TPPC8, KLH20, S27A6, YBOX2, TR150, WBP11, NOP58, NOSIP, LC7L2, SF3B6, ORN, NOP16, TIM16, RT23, RTCB, HCN4, ZN330, RL36, CCDC9, DMXL1, ZAN, KDM3A, MFHA1, PLXD1, HECD4, WDR7, IRS2, HYOU1, OARD1, SP16H, PCDGH, HEY1, SRPRB, O51B2, CORIN, DMRT2, MRCKB, NOX1, RBM8A, ZN706, SNX9, SCNAA, HCFC2, PUS1, MYH4, SPIN1, COPG1, CFA20, EMIL1, PTC2, DC1L1, STYL1, OAS3, TLL2, ZNT1, MYO16, GAK19
Species: Streptomyces avidinii, Gallus gallus, Bos taurus, Sus scrofa, Homo sapiens
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Chen Y, Tang F, Qin H, Yue X, Nie Y, Huang W, Ye M. Endo-M Mediated Chemoenzymatic Approach Enables Reversible Glycopeptide Labeling for O-GlcNAcylation Analysis. Angewandte Chemie (International ed. in English) 2022 61(23) 35289036
Abstract:
To selectively enrich O-linked β-N-acetylglucosamine (O-GlcNAc) peptides in their original form from complex samples, we report the first reversible chemoenzymatic labeling approach for proteomic analysis. In this strategy, the O-GlcNAc moieties are ligated with long N-glycans using an Endo-M mutant, which enables the enrichment of the labeled glycopeptides by hydrophilic interaction liquid chromatography (HILIC). The attached glycans on the enriched glycopeptides are removed by wild-type Endo-M/S to restore the O-GlcNAc moiety. Compared with classic chemoenzymatic labeling, this approach enables the tag-free identification, and eliminates the interference of bulky tags in glycopeptide detection. This approach presents a unique avenue for the proteome-wide analysis of protein O-GlcNAcylation to promote its mechanism research.
O-GlcNAc proteins:
TM271, HEAT9, SBNO1, P121B, GGT3, TAF4, AGRIN, MEIS1, RNT2, NFIB, MA2B1, CDKA1, ABLM1, ADA10, KMT2D, MYPT1, ZN609, SC16A, PLXB2, SET1A, VA0E1, TNC18, TLR3, TET3, PRPF3, IF4G3, ZN207, AKAP8, CALU, EXTL3, PCDH7, TRAK2, GANP, TSN3, MAFK, KERA, SRGP2, ANR17, NCOR1, U520, CRTAP, ATRN, CBPD, RMP, TOX4, SC24D, SRBS2, SUN1, ERLN2, PCF11, SCAF4, VAPB, SMC2, SC24B, CNOT4, EGFR, HPT, GLHA, LMNA, NU3M, VTNC, GCR, A1BG, K2C1, HSPB1, RPN1, AT1B1, K1C18, K2C8, ITAV, GDN, TRY1, SAP, MET, NFIC, VIME, K2C7, SNRPA, UCRIL, ATX1L, NT2NC, LYAG, LAMC1, PPAL, LAMP1, MPRI, TPR, SKIL, T2FB, GLU2B, NID1, PO2F1, MCP, ZEP1, CD36, ATF7, EGR1, SON, ATF1, ICAL, CO5A1, ASPG, SFPQ, ITA3, NKG2A, ARNT, TEAD1, 3MG, TKT, UFO, HXA11, HXC9, ZEP2, HNRH1, ELF1, CD68, RFC1, FBN1, NU214, RL4, SCNNA, SRP14, NUP62, TAGL2, CUX1, IL6RB, PBX2, STAT3, NBL1, LAP2A, LAP2B, LIFR, PCP, ECE1, MUC18, MATR3, SSRB, VDAC2, ATRX, NOTC1, UTRN, RFX5, HSP13, CCN3, AGRE5, NR2C2, CDK8, CENPF, YLPM1, RBM25, NU153, RBP2, TAF6, EMD, PPT1, SMCA4, AGFG1, NUP98, PTTG, ATX1, AT1B3, AF17, DSRAD, LAMB2, CAD13, ITA1, NU107, TGFB2, ACTG, CXAR, PITX1, CNTP1, ABCA4, PHC1, ADA17, KGD4, SARNP, FOXK1, DAB2, HNRPU, SPTB2, FOXK2, MEF2A, SP3, PLOD1, KMT2A, UPAR, IF4G1, NOTC2, SRS11, SUH, MFGM, AHNK, TMM62, GALT1, BST2, SIA4C, ASPH, BPTF, NFIA, FOXC1, ADAM9, NFAC2, MAMD1, NAB1, TBB3, PKD2, LAMB3, KLF5, NFYC, CDK13, SCRB2, LRP8, VEZF1, UBP2L, LAGE3, MDC1, RRP1B, MEF2D, ARI5B, NUMA1, PON2, RCN1, TAF1C, SF01, MED1, JHD2C, ELF2, TAB1, ZFHX3, ZYX, ADRM1, LAMA4, TAF9, FOXD1, LAMA3, RFX7, QSER1, SVEP1, SYTL3, EPC2, LUZP6, CRTC2, YIF1B, BCORL, BRD10, PRC2B, ZN362, LRIF1, UBAP2, RBM26, VP13D, RPRD2, RN220, ZN318, TASO2, ECM29, ARID2, SE1L3, BICRL, SCAR3, NIPBL, LIN54, FSTL4, TET2, ZNT6, GOLM2, NFRKB, S39A4, ZC3HE, FIP1, CRTC3, PLGT2, SUSD1, MCAF1, BCOR, IGS10, B3GLT, CD109, FRRS1, SRCAP, NBEL1, UBN2, RAPH1, HAKAI, ASXL2, SPT6H, KDM3B, NRK, NUP54, POGZ, MAVS, PK1L3, PLGT3, EMSY, RAI1, YTHD3, LDB1, LYRIC, OSTM1, PRSR1, DDX42, P66A, FOXP4, CTL2, TEX2, MGAP, ANKH1, SUGP1, NUP93, PLD6, FNBP4, ARFG1, PMGT2, GOLM1, PGLT1, TM87A, FSAF1, PHC3, SP20H, ARI1B, NUP35, OR6C4, VA0E2, PLBL2, PUM2, SPP2B, DLG5, GPX8, PO210, ZN384, LMO7, MUC16, P66B, BBX, SMG7, NICA, TM131, PHF3, TAF4B, GGH, GSLG1, FUBP2, LPP, NCLN, TTC17, FKB10, TOM6, PF21A, RBM33, I17RA, P121A, PDLI5, CREL1, FUBP3, TXD15, LOXL4, VCIP1, CHAP1, Z512B, ZFR, EP400, HUTU, RBM14, KI20B, PHF12, PANX1, CIC, MED15, ERBIN, JMJD8, MINT, TEAD3, SEM3C, WAC, DIDO1, HNRL1, TM109, NUP58, M4A8, YTHD1, ULBP3, AMRA1, TANC1, TWSG1, S22A4, SP130, APC1, I2BPL, WNT5B, VP33B, EPC1, ADNP, ZN106, FOXP1, PTN23, WNK1, SIA7D, ZHX3, PIEZ2, SG196, TM231, PEAK1, DOCK5, CF155, CNO10, MLXIP, SIAE, PKHA5, RC3H2, TAF9B, ZBT20, NCOA5, TANC2, ZN532, CELR2, APMAP, ABCB9, CHSTB, UBN1, NECT3, PDLI7, RBM12, OCAD1, CARF, ETAA1, HXC10, TAB2, CELR1, CDK12, CNOT2, CRIM1, TMEM9, RCC2, CHD7, RBM27, KANL3, MRC2, SUCO, TCF20, SUN2, UBQL2, LCAP, GGT7, TASOR, GMEB2, ZHX1, DSE, WWC3, MRTFB, ZBT21, PRR12, YETS2, NOTC3, KMT2B, PRP19, MINP1, SCAF8, ZC3H4, SRRM2, SCML2, UST, ICE1, ZN281, DAAM1, IRS2, PRC2C, NCOR2, NPTN, GMEB1, POMT1, S4A7, S23IP
Species: Homo sapiens
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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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Shen B, Zhang W, Shi Z, Tian F, Deng Y, Sun C, Wang G, Qin W, Qian X. A novel strategy for global mapping of O-GlcNAc proteins and peptides using selective enzymatic deglycosylation, HILIC enrichment and mass spectrometry identification. Talanta 2017 169 28411811
Abstract:
O-GlcNAcylation is a kind of dynamic O-linked glycosylation of nucleocytoplasmic and mitochondrial proteins. It serves as a major nutrient sensor to regulate numerous biological processes including transcriptional regulation, cell metabolism, cellular signaling, and protein degradation. Dysregulation of cellular O-GlcNAcylated levels contributes to the etiologies of many diseases such as diabetes, neurodegenerative disease and cancer. However, deeper insight into the biological mechanism of O-GlcNAcylation is hampered by its extremely low stoichiometry and the lack of efficient enrichment approaches for large-scale identification by mass spectrometry. Herein, we developed a novel strategy for the global identification of O-GlcNAc proteins and peptides using selective enzymatic deglycosylation, HILIC enrichment and mass spectrometry analysis. Standard O-GlcNAc peptides can be efficiently enriched even in the presence of 500-fold more abundant non-O-GlcNAc peptides and identified by mass spectrometry with a low nanogram detection sensitivity. This strategy successfully achieved the first large-scale enrichment and characterization of O-GlcNAc proteins and peptides in human urine. A total of 474 O-GlcNAc peptides corresponding to 457 O-GlcNAc proteins were identified by mass spectrometry analysis, which is at least three times more than that obtained by commonly used enrichment methods. A large number of unreported O-GlcNAc proteins related to cell cycle, biological regulation, metabolic and developmental process were found in our data. The above results demonstrated that this novel strategy is highly efficient in the global enrichment and identification of O-GlcNAc peptides. These data provide new insights into the biological function of O-GlcNAcylation in human urine, which is correlated with the physiological states and pathological changes of human body and therefore indicate the potential of this strategy for biomarker discovery from human urine.
O-GlcNAc proteins:
TX13C, ESYT2, BICL2, ODAM, SRCRL, SYTC2, Z804B, O2A25, XIRP2, NKX26, SMCO2, MFS2B, O51F1, NCF1B, ABTB3, SRRM4, D11L8, YV023, LEUTX, MEIOS, RB27B, CACB4, SOCS6, CHD1, NDC80, KIF3C, MYPT1, IPP2C, MUSK, MRP3, PA2GX, ARPC5, P2RX6, ZW10, ZN749, KCAB3, ACTN4, VEGFD, BNI3L, ZN292, PI51C, MABP1, CCG3, NOBOX, REV3L, TBL1X, NBN, KI21B, PX11A, UBP2, CAN15, ATRN, SPF30, MYO1D, SUN1, ENDD1, M4K4, CFAB, LV151, K1C14, K2C1, HSPB1, CHLE, SAP, SRPRA, GNAI3, IL6RA, VILI, AT8OS, GLI3, RNAS2, LYAG, SPTB1, PSG2, LAMP2, CSPG2, SC5A1, F261, DPEP1, EPB42, ITB6, LMNB1, NEBU, RYR1, TENX, SP100, ANX13, ADH6, GNA11, NMT1, CPSM, GBRA5, AKT2, I5P2, MYH11, HMGCL, PGM1, CDN1A, MLH1, SATT, DCC, MAGAA, MMP13, ABCG1, MP2K3, UTRN, IDHP, PSB3, RBP2, MRE11, ETV1, IRAK1, ARSD, NEK4, SPSY, COPA, SMTN, ATN1, PMS1, PMS2, ATNG, PRRX1, AF17, NXPH1, NAL12, IF4A1, STX1B, KCNJ2, HPCA, PKD1, REEP5, CAC1D, MMSA, SEMG2, ACY1, P, ZNF91, LG3BP, PDE4C, SCAP, PO4F2, NMDE1, OVGP1, ANK3, NFAC3, AKAP6, CENPR, SF3B2, TRA2A, CUL4B, ALKB1, CO9A2, FA53B, WRN, SLBP, GOGB1, ZN169, ODFP1, FRPD4, MELT, SART3, IF4H, KIF14, PLCL1, PLEC, PSG5, DLGP5, MARE2, ENOX2, CNGA2, AINX, HCDH, CSPP1, QSER1, ZN423, SPKAP, PRSR3, ATOSA, K2C71, GON4L, GNPTA, LEGL, PAR14, PCDP1, PLCH1, AARD, RHG29, SPIN4, FA76B, CX066, BRM1L, ODR4, SZT2, SYRM, EEIG2, CE162, CL060, MYOME, ARHGG, CA140, CARL1, ZMYM4, EST4A, F219B, WDR25, F90A2, LAR1B, ATG9B, ARID2, FTM, USF3, KCD16, ZNF57, K1C39, Z518A, BLT3A, CV042, RTL6, CAPR2, ADAM5, ZNT6, CA094, VIP1, AGRD1, CC171, KLH24, ABRX1, PAMR1, TM14E, ITIH6, RFIP1, IGS10, WDR87, SHSA6, FGD6, RGMC, NEK10, UBP31, NOL8, MARK2, BEND5, PCAT2, EPMIP, DPH6, OLIG3, TRPM8, CC186, MYCPP, TMC7, Z804A, TAF8, RALYL, RBM23, CC190, PKHL1, GA2L3, TCAM2, STX12, KI18B, RB6I2, ARMC8, K0825, STH, RP1L1, TPH2, F217A, PLPL6, EFC13, CJ067, PSYR, TBC21, DOCK3, AGRF4, SYCE1, CADM3, CP4Z2, CLASR, ZN786, CLIP4, CBPA6, NKAP, TM156, CPSF7, EFNMT, IGS22, LMBL4, ZFP62, PHC3, DDHD1, EXPH5, NAV1, BD1L1, BPIB6, TET1, MYRIP, FBH1, O10K1, ST3L4, CHD6, DMXL2, MIPT3, ES8L3, DOT1L, NAT14, CKAP2, ARAP3, CSKI1, ATRIP, MUC16, ELYS, TITIN, LZIC, PHF3, TBCD5, K0232, PRCC, TFG, SFRP3, COR2A, ARHG2, TATD2, LENG9, FAM3D, ALKB8, CHM4C, LRC58, REPS1, PGBD4, P3IP1, CDCA5, HMCES, DMAC1, IGS21, PAWR, ITCH, M4A14, CLMN, S41A2, HSH2D, TM87B, ZN514, P12L2, C295L, CQ10A, ROBO3, WWAS2, DB118, KI20B, PHF12, SPAG5, OR2M4, HMCN1, RANB9, CCNL2, IWS1, K1C12, NPY6R, S1PR3, LYST, CDC6, EBP2, NIPS1, DDX50, FA83C, PIMRE, NDC1, MTNA, UT14A, NUP85, TDRD1, MSTRO, SETD2, OSBL8, UACA, TSG10, TB182, EGLN1, CRLD2, CSTFT, NKX24, CT191, ESF1, PIEZ2, RANB3, CSR2B, UCK1, ZN556, MLXIP, TNR6C, HMX1, EQTN, PRDM9, TLR8, HELLS, TOPRS, KIF15, RAD18, HOME2, BRWD1, TEN2, CCM2L, FGOP2, MCUB, MIC19, KCTD5, CARF, FAT2, DTL, SACS, KLHL8, CE126, WDR35, NRX2A, DNM3B, COPG2, GCP4, PARP2, TCF20, ASIC3, RABX5, STAG3, NGAP, FBX5, MKLN1, ZBT21, PKHH1, SOX13, LIMC1, EXOC7, CBPC1, TUTLB, XCT, SHOC2, RUVB2, PDE10, PRLD1, FBW1A, DLGP4, WDR37, ZBTB1, NSG2, LSM2, DOP2, C170B, SAM50, PCDBB, PCDA3, TF3C3, CCG2, BIG1, S4A4, PCLO
Species: Homo sapiens
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Jiang K, Gao Y, Hou W, Tian F, Ying W, Li L, Bai B, Hou G, Wang PG, Zhang L. Proteomic analysis of O-GlcNAcylated proteins in invasive ductal breast carcinomas with and without lymph node metastasis. Amino acids 2016 48(2) 26374642
Abstract:
The potential role of protein O-GlcNAcylation in cancer has been studied extensively, and the spread of cancer cells to regional lymph nodes is the first step in the dissemination of breast cancer. However, the correlation between O-GlcNAcylation and lymphatic metastasis in breast cancer remains elusive. In this study, we demonstrated that the overall O-GlcNAcylation as well as O-GlcNAc transferase (OGT) tends to decrease in response to the augmentation of lymph node metastasis (LNM) in invasive ductal breast carcinomas (IDCs). Although accumulating evidence indicates that individual O-GlcNAcylation may be important in the pathogenesis of breast cancer, O-GlcNAcylated proteins in IDCs are still largely unexplored. Herein, O-GlcNAcylated proteins of IDCs were chemo-enzymatically enriched and identified via liquid chromatography combined with tandem mass spectrometry. In total, 155 O-GlcNAcylated proteins were determined, of which 41 were only observed in LNM tissues, while 40 were unique in non-LNM samples. Gene ontology analysis showed that O-GlcNAc is primarily a nucleocytoplasmic post-translational modification, and most enriched functional terms were related to cancer development in both metastatic and non-metastatic IDCs. Moreover, several O-GlcNAcylated proteins involved in glycolysis and its accessory pathway were identified from LNM and non-LNM groups, respectively. These results indicate that the O-GlcNAcylation statuses of individual proteins were independent of the overall O-GlcNAcylation levels of metastatic and non-metastatic IDCs. Aberrant O-GlcNAc modification of these proteins might be associated with LNM progression.
O-GlcNAc proteins:
IGLL5, NPT3, SURF4, OGT1, GGCT, LX12B, NCOR1, IDHC, AATM, ASSY, CYTA, PIGR, TRFL, CATA, VWF, G3P, HSPB1, ALDOB, ARGI1, ALDH2, S10A8, ATPB, S10A9, ENOA, PGK2, PDIA1, CATD, ANXA2, CAH3, GSTA2, GSTP1, F16P1, S31D3, UBC, THIO, CH60, HSP7C, LAMP1, ETFA, PLAK, DESP, HSP76, TGM1, LORI, ATPA, PSA5, PSB4, PSB6, GSTM2, TKT, SPB3, S10A7, CPSM, CASPE, S10AB, PRDX2, SPR1A, PGM1, TALDO, RL3, HUTH, SSRA, RS5, PSB2, CASP5, HMCS2, EPIPL, TPIS, IF4A1, RS3A, RS14, H4, RS24, 1433Z, ACTG, EF1A1, ACTS, HBB, ARF5, FABP5, DSG1, PRDX1, CKAP4, TGM3, DSC1, BLMH, DYHC1, DSC3, CDSN, SYPL1, HCDH, PTHD3, ACTBL, KPLCE, CNDH2, SBSN, DEN5B, FBX50, H32, H2AV, SPA24, HORN, KLD8B, POF1B, MUC16, TITIN, NAR4, BHMT1, MUCL1, DIRA2, SPB12, GSDMA, PSMD1, TCPH, PGES2, S10AE, ALG13, GNL3L, TBA8, ING1, NINL
Species: Homo sapiens
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