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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, GRP75, 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, HCFC1, 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, HBS1L, 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, HCFC1, 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, TLE3, 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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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, TPM3, 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, GRP75, 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, OD3L1, 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, HBS1L, 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: Gallus gallus, Homo sapiens, Sus scrofa, Bos taurus, Streptomyces avidinii
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Liu J, Hao Y, Wang C, Jin Y, Yang Y, Gu J, Chen X. An Optimized Isotopic Photocleavable Tagging Strategy for Site-Specific and Quantitative Profiling of Protein O-GlcNAcylation in Colorectal Cancer Metastasis. ACS chemical biology 2022 17(3) 35254053
Abstract:
O-linked-β-N-acetylglucosamine (O-GlcNAc) glycosylation is a ubiquitous protein post-translational modification of the emerging importance in metazoans. Of the thousands of O-GlcNAcylated proteins identified, many carry multiple modification sites with varied stoichiometry. To better match the scale of O-GlcNAc sites and their dynamic nature, we herein report an optimized strategy, termed isotopic photocleavable tagging for O-GlcNAc profiling (isoPTOP), which enables quantitative and site-specific profiling of O-GlcNAcylation with excellent specificity and sensitivity. In HeLa cells, ∼1500 O-GlcNAcylation sites were identified with the optimized procedures, which led to quantification of ∼1000 O-GlcNAcylation sites with isoPTOP. Furthermore, we apply isoPTOP to probe the O-GlcNAcylation dynamics in a pair of colorectal cancer (CRC) cell lines, SW480 and SW620 cells, which represent primary carcinoma and metastatic cells, representatively. The stoichiometric differences of 625 O-GlcNAcylation sites are quantified. Of these quantified sites, many occur on important regulators involved in tumor progression and metastasis. Our results provide a valuable database for understanding the functional role of O-GlcNAc in CRC. IsoPTOP should be applicable for investigating O-GlcNAcylation dynamics in various pathophysiological processes.
O-GlcNAc proteins:
A0A0B4J203, A0A0C4DFX4, RBM47, E2F8, WDR27, SBNO1, CNOT1, P121B, P121C, H0YAE9, H0YHG0, H7C469, K7ELQ4, M0QZ24, PDLI1, HAX1, TAF4, BCL9, CAC1A, DDX3X, NFIB, PPP6, MA2B1, ARI1A, SOCS7, ABLM1, KMT2D, GBRD, RGRF2, TX1B3, HGS, MYPT1, SYN3, ZN609, TRI66, PDZD2, MAST4, SC16A, SET1A, CASC3, FOXP2, MOT4, P4HA2, ARPC5, CLOCK, MAFG, PER1, KDM6A, TET3, SI1L1, TGFI1, M3K7, MCA3, PRPF3, TPD54, SYNJ1, IF4G3, E41L2, WIPF1, FOXO3, TGM5, RNF13, SPY2, PLRG1, ZN207, AKAP8, CALU, ORC5, MYPT2, GANP, OGA, CCNT1, BUB1B, PLOD3, PLIN3, MOT2, MAFK, PQBP1, BRD4, TBL1X, PP1RB, NBN, MITF, SRGP2, N4BP1, ROCK2, PP6R2, CNOT3, ANR17, FLNB, NCOR1, SF3B1, REM1, CREG1, CRTAP, SYUG, CYTF, TOX4, TOX, SUN1, PCF11, AGFG2, UBE4B, CAC1H, SVIL, SC24A, SC24B, CNOT4, EYA4, ZMYM6, BAG3, LATS1, DDAH2, TXD12, ONEC2, CLPT1, ABL1, CRYAB, LMNA, TFR1, CATA, GBA1, FUCO, ALDOA, GCR, G3P, CPNS1, HSPB1, RLA2, RLA0, ITB1, K1C18, NPM, CATL1, CATB, MCR, BGLR, ITA5, NFIC, VIME, SNRPA, FGR, ATX1L, DERPC, ZN865, GLI2, MYBB, CLUS, PPAL, MPRI, PABP1, TPR, BMP3, SKIL, ENPL, PO2F1, PLAK, ATF2, ZEP1, RS2, TFE2, F261, ITB4, ZNF23, ZNF25, JUNB, ATF7, TPH1, DDX5, EGR1, SON, NELFE, ATF1, ATF6A, CADH2, ICAL, CSRP1, FLNA, RFX1, CBL, SFPQ, COF1, IF4B, GATA2, APC, DDX6, ARNT, MAP4, LYOX, HXD9, MZF1, CLIP1, 5HT1F, HXA11, ZEP2, ELF1, CTNB1, FBN1, ADDA, BASI, NU214, VGFR2, SRP14, NUP62, SYUA, VATA, CUX1, TXLNA, STAT3, LAP2A, EPS15, HELZ, MATR3, SSRA, SSRB, KI67, ATRX, MAP1B, YAP1, UTRN, STT3A, SC6A8, RFX5, SOX2, PRC2A, HSP13, NR2C2, NASP, CDK8, DHE4, YLPM1, NU153, RBP2, TAF6, MRE11, EMD, MXI1, MAP2, TOB1, PPT1, TCPQ, PAPOA, HCFC1, GDS1, AGFG1, CRIP2, NUP98, SMTN, SC24C, HIRA, ATX1, ATN1, AFAD, AF10, AF17, DSRAD, SEC13, NU107, ZN445, CSN2, RL37, WDR5, TIM10, F193A, RBM6, PITX1, IF4G2, PHC1, ADA17, KGD4, RL19, FOXK1, DAB2, RHG04, RBM10, HNRPU, SPTB2, FOXK2, RUNX1, MEF2A, SP2, SP3, PLOD1, KMT2A, TF65, IF4G1, NOTC2, TLE3, TLE4, PTN12, CALD1, MEF2C, P5F1B, GABPA, ZO1, ACK1, EP300, AHNK, FCHO2, HMGX3, SRBP2, FOXO1, ASPH, TROAP, BPTF, FSTL1, NFIA, DPYD, TP53B, FOXC1, ECH1, ROA0, DDX10, TBX2, GPS2, G3BP1, PABP4, ADAM9, PICAL, NAB1, SERC3, RIPK1, IQGA2, STIM1, CUL4B, ASPP2, CAC1S, RUNX2, NFYC, CDK13, TOB2, VEZF1, UBP2L, GIT2, SRC8, CAPR1, LAGE3, PUM1, MDC1, EPN4, TTLL4, RRP1B, NCOA6, GSE1, MEF2D, LASP1, MYPC3, ZN638, NUMA1, SART3, CND1, R3HD1, KIF14, WDR43, PLCL1, PLEC, NOMO1, NONO, RCN1, RYR3, KS6A1, RBMS2, TAF1C, SF01, MED1, JHD2C, TRIP6, T22D1, ELF2, TAB1, HERC1, NCOA1, VAS1, ZFHX3, ZYX, ADRM1, SYPL1, TAF9, DREB, DGKD, CGT, GEN, LY6K, RFX7, QSER1, AAK1, PRSR3, QRIC1, MA7D1, WDR72, TBRG1, TB10B, TPRN, FIL1L, SVEP1, AMOT, EPC2, CRTC2, PAN3, HS904, YIF1B, AG10A, IGS11, ZN628, BCORL, FIGN, BRD10, SH319, TGO1, PRC2B, TOIP1, CEP78, P4R3B, HP1B3, CE170, ZN362, FKB15, AKND1, ZEP3, LRIF1, SWT1, RHG21, UBAP2, RBM26, DEP1A, OGRL1, AHDC1, F222A, RPRD2, RN220, ZN318, TASO2, ZMYM4, PAPD7, TENS2, KANK2, ARID2, USF3, RHG17, CYTSA, ANR40, BICRL, JADE1, PKHA7, NIPBL, LIN54, TET2, RINT1, CRCDL, ZNT6, TTC41, RHGBA, NFRKB, RSBNL, KCD18, NCEH1, MDEAS, ZC3HE, LARP1, NHS, CRTC3, SAS6, MCAF1, BCOR, MPRIP, DNMBP, GGYF2, THADA, BNC2, NFXL1, NBEL2, CO039, SRCAP, CBAR2, UBN2, XIRP1, RAPH1, LARP4, HAKAI, ASXL2, SPT6H, KDM3B, ZCCHV, KANL1, RGPD4, POGZ, ZFY16, NUFP2, MAVS, CLAP1, EMSY, I2BP2, SRGP1, RBBP6, SH3R1, HUWE1, YTHD3, NPM2, ILDR1, KAISO, MYPN, LDB1, LYRIC, BCL9L, LUZP1, NRAP, RTTN, PRSR1, DDX42, CEP57, CD20B, CACL1, P66A, HIPK1, KCC1D, RN135, MY18B, AHNK2, FOXP4, NAV3, NAV2, MISP, ARI3B, IPRI, TEX2, MGAP, CC28A, Z3H7A, ANKH1, SUGP1, RPAP2, MILK2, SRRM1, ZZZ3, GAR4, PHAR4, RTKN2, DCP1B, XRN1, PELP1, CKLF8, TENS4, SPART, RPTOR, NUP93, ZN687, DOCK4, RHG24, RUSC2, SYNPO, FNBP4, D2HDH, RP25L, ATPF2, CPSF7, ARFG1, ENAH, SPOT1, SUMF1, KCNH5, SLAI1, TNR6A, PHC3, DRC6, CBPC3, NAV1, VP37A, KMT2C, ZMIZ2, BD1L1, ARI1B, FLCN, NUP35, TOIP2, TNIP2, KNL1, OR2L2, PUM2, CC110, TBC15, STT3B, ZN507, ALMS1, DLG5, KCNV2, BRX1, DOT1L, GEMI5, PARD3, ZN384, SMAP2, IASPP, TM263, ZFN2B, NUDC2, PCNP, TRUB1, LMO7, ATX2L, PALLD, P66B, BBX, ZCH14, GBF1, SMG7, RTF1, NICA, PHF3, MAML1, ZN592, LAR4B, TFG, TAF4B, RREB1, SC65, CBP, SYMPK, DDX17, GPKOW, FUBP2, UBP7, LPP, LSM10, NCLN, MRTFA, FUBP1, TTC17, PBIP1, TTC28, TOM6, PF21A, INT12, REPS1, ESS2, MBD6, ELP4, SGF29, RBM33, ZN503, P121A, TONSL, PDLI5, ERO1A, DOCK6, FUBP3, RSRC1, ZN594, VCIP1, ZN462, LCOR, PDLI2, CLP1L, Z512B, ZFR, EP400, MRFL, H6ST2, TIGD1, NOL4L, DOCK7, RPR1A, RBM14, ADCYA, QKI, LENG8, TRNT1, PP1RA, PHF12, CIC, MED15, ERBIN, HMCN1, LMF1, PIGS, WRIP1, SIN3A, MINT, HTF4, EYA3, POP1, TEAD3, TTC1, CSN8, ATX2, ARI3A, ANM1, PKP2, TEP1, DPH2, WAC, DIDO1, HNRL1, RBM4, SSBP4, PRR14, SSBP3, YTHD1, KPCD2, ZCHC2, TB182, AMRA1, CE295, TANC1, ZC12C, CEP44, STRAB, SP130, BRD8, RGAP1, SMG9, APC1, I2BPL, TMX4, KI13A, WDR13, EPC1, ADNP, ZN106, TM245, FOXP1, PABP3, WNK1, E41L1, ZHX3, BICC1, PEAK1, PPR3E, ZN703, PKHA5, CLSPN, BCDO1, RC3H2, ZFYV1, TAF9B, EMAL4, ZBT20, NCOA5, TANC2, ZN532, NCK5L, TNR6C, CHD8, FBSL, APMAP, DMAP1, UBN1, DCP1A, INCE, ANLN, GEPH, PDLI7, TULP4, HOME2, SLX9, DIAP3, BMP2K, RBM12, STAU2, DDX28, CWC25, CARF, ETAA1, ABI2, HXC10, BCLF1, TAB2, CELR3, CDK12, GRHL1, SACS, ITSN2, BICRA, CNOT2, TMEM9, CAC1I, CAMP3, DAPLE, RCC2, DIP2B, MBD5, CT2NL, F135A, KANL3, RERE, SE1L1, TRM7, YM012, KDM5B, LIMD1, TCF20, SUN2, LIMA1, SEPT9, UBQL2, TRPS1, S30BP, NRBP, BAZ2B, SIX4, HOOK1, CDC23, TASOR, GMEB2, TNIK, PARP4, NUP50, ZHX1, CDV3, MCTS1, KCNH3, LRFN2, MRTFB, ZBT21, PRR12, YETS2, HECD1, ZMYD8, NOTC3, SPAT2, SOX13, G3BP2, MAGD2, MINP1, MACF1, CP131, SCAF8, TRI33, PHF8, LIMC1, TNR6B, SRRM2, SCML2, ZN148, POLH, INVS, ICE1, R3HD2, MAN1, TR150, WBP11, ZN281, STA13, WNK2, HBS1L, ARIP4, MTCL1, DCAF1, RPGF2, IRS2, CRBG1, HYOU1, SAM50, PRC2C, YTHD2, NCOR2, GMEB1, DC1L1, EPN1, NCOA3, ZHX2, S23IP, U3KPZ7, V9GYH0
Species: Homo sapiens
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Wang S, Yang F, Petyuk VA, Shukla AK, Monroe ME, Gritsenko MA, Rodland KD, Smith RD, Qian WJ, Gong CX, Liu T. Quantitative proteomics identifies altered O-GlcNAcylation of structural, synaptic and memory-associated proteins in Alzheimer's disease. The Journal of pathology 2017 243(1) 28657654
Abstract:
Protein modification by O-linked β-N-acetylglucosamine (O-GlcNAc) is emerging as an important factor in the pathogenesis of sporadic Alzheimer's disease (AD); however, detailed molecular characterization of this important protein post-translational modification at the proteome level has been highly challenging, owing to its low stoichiometry and labile nature. Herein, we report the most comprehensive, quantitative proteomics analysis for protein O-GlcNAcylation in postmortem human brain tissues with and without AD by the use of isobaric tandem mass tag labelling, chemoenzymatic photocleavage enrichment, and liquid chromatography coupled to mass spectrometry. A total of 1850 O-GlcNAc peptides covering 1094 O-GlcNAcylation sites were identified from 530 proteins in the human brain. One hundred and thirty-one O-GlcNAc peptides covering 81 proteins were altered in AD brains as compared with controls (q < 0.05). Moreover, alteration of O-GlcNAc peptide abundance could be attributed more to O-GlcNAcylation level than to protein level changes. The altered O-GlcNAcylated proteins belong to several structural and functional categories, including synaptic proteins, cytoskeleton proteins, and memory-associated proteins. These findings suggest that dysregulation of O-GlcNAcylation of multiple brain proteins may be involved in the development of sporadic AD. Copyright © 2017 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
O-GlcNAc proteins:
SBNO1, F221A, CNOT1, WIPF3, MYO9A, APBB1, TAF4, P3C2A, DLGP1, C2C2L, DC1I1, CTRO, NCAN, ABLM1, KMT2D, MYPT1, PDZD2, RIMB2, TCPR2, ERC2, ANR28, LAMA5, OGT1, CLOCK, SI1L1, M3K13, HS12A, CP110, MTSS1, M3K7, TPD54, IF4G3, E41L2, FOXO3, KCNQ3, RNF13, MYPT2, AP180, PLIN3, MOT2, MAFK, HCN1, SLIT3, CLAP2, DEPD5, LIPA3, PP6R2, ANR17, LIPA4, NCOR1, GGYF1, HSBP1, ATRN, FLOT1, SYUG, TPPP, TOX4, SRBS2, TOX, ABLM3, AGFG2, RTN3, KCNH1, VAPB, ZFYV9, SC24B, CNOT4, ZMYM6, BAG3, DDAH2, ABL1, CRYAB, LMNA, MBP, FUCO, GCR, G3P, HSPB1, APOD, PERM, IF2A, NFL, NFM, SAP, VIME, CO4A, AN34C, ATX1L, ELFN1, DERPC, CALM1, CALM2, CALM3, LYAG, LAMC1, MTAP2, EPB41, BCR, LAMP1, PABP1, NFH, CO6A2, CO6A3, TPR, SKI, CSPG2, GFAP, KPYM, GNS, ZEP1, ARSB, ITB4, STMN1, ATF7, SYN1, NEUM, EGR1, SON, ELK1, TFE3, CSK22, ICAL, MAG, CSRP1, VDAC1, TENX, CBL, PTPRZ, OMGP, LAMA2, TENA, APC, DNJB2, MAP4, PTPRM, CLIP1, ZEP2, L1CAM, HS71L, CTNB1, ADDA, NU214, NUP62, SYUA, VATA, CUX1, STAT3, PTGDS, GRM5, GRIA1, MATR3, ATRX, NOTC1, MAP1B, SC6A8, PRC2A, UB2R1, NU153, RBP2, GSK3A, TAF6, TOB1, PPT1, FXR2, MECP2, HCFC1, AGFG1, NUP98, ATX1, DSRAD, LAMB2, CAD13, TPD52, STX17, MYPR, CSK21, F193A, SHPS1, IF4G2, PHC1, MAP1A, BASP1, KGD4, FOXK1, PGBM, RHG04, HNRPU, SPTB2, ANK2, NAAA, DYST, NOTC2, TLE2, TLE4, NMDZ1, MEF2C, ZO1, ACK1, LG3BP, DEMA, CAMP2, AHNK, BPTF, CNTN1, ANK3, ROA0, GPS2, MTA1, LSAMP, GAB1, PICAL, ASAH1, RIPK1, KCC2B, BMPR2, VEZF1, UBP2L, GIT2, DPYL1, DCTN1, SRC8, PUM1, EPN4, RRP1B, NCOA6, KCNB1, LASP1, CRYM, NFIX, NUMA1, SHPRH, HECAM, IF4H, PLEC, PTPRR, PTPA, NCOA2, SF01, JHD2C, T22D1, PI5PA, TAB1, NCOA1, ZYX, SYUB, ADRM1, CCDC6, AINX, DPYL2, NTRK2, TBR1, RTN1, RFX7, QSER1, AAK1, QRIC1, MA7D1, TBC25, TB10B, TPRN, FIL1L, SVEP1, GRAP1, AMOT, CCD93, IGS11, ARMX4, NHLC3, PRC2B, SNP47, CE170, ZEP3, SKT, UBAP2, RBM26, AHDC1, VP13D, MRCKA, RPRD2, RN220, F1711, TASO2, MLIP, PAPD7, TENS2, KANK2, CRBG3, ANR40, ABLM2, CAPR2, LIN54, F117B, SCYL2, NFRKB, MDEAS, ZC3HE, LARP1, FIP1, PAMR1, MCAF1, MPRIP, GGYF2, NFXL1, PPR3F, K154L, RAPH1, UB2R2, HAKAI, MTSS2, ASXL2, CEP68, SPT6H, SYT13, MICA3, GRIN1, POGZ, ZFY16, MAVS, EMSY, RBBP6, SH3R1, HUWE1, YTHD3, FLIP1, LYRIC, RIMS1, F124A, LUZP1, PACS2, RLGPB, P66A, KCC1D, AHNK2, NAV3, TEX2, MGAP, CC28A, UBR1, ANKH1, NPAS3, MILK2, ULK2, PHAR4, DCP1B, SPART, CEND, RPTOR, KT222, ZN687, DOCK4, SYNPO, FNBP4, MINK1, OXR1, AVL9, CAMKV, SLAI1, NUP35, REPS2, NBEA, MYRIP, SVIP, PLBL2, NCOA7, TBC15, NEK9, DLG5, GEMI5, WIPF2, F222B, SMAP2, TM263, ZFN2B, LMO7, CTL1, ATX2L, PALLD, CSKI1, MADD, P66B, BAALC, ZCH14, LAR4B, PTPRU, RYR2, TAF4B, SYN2, DDX17, GPKOW, FUBP2, ARHG2, LPP, SNX21, MRTFA, SH3K1, PF21A, ATG2B, PLD4, REPS1, CYFP2, PHIPL, PGCB, PDLI5, MAP6, VCIP1, ZFR, EP400, SPT33, DOCK7, LRRC7, RBM14, NED4L, QKI, SYGP1, LMTK3, PLIN4, ARX, CIC, MED15, KKCC2, MINT, PKP4, ATX2, SH3G3, DPH2, KTNB1, TPPP3, SRBS1, BBS2, YTHD1, WNK3, CFA74, ZCHC2, TB182, AMRA1, ZC12C, SRCN1, SP130, BRD8, WDR13, EPC1, CA198, WNK1, E41L1, ZHX3, VIAAT, Z385D, DOCK5, GORS2, JUPI2, MA6D1, SIAE, PKHA5, RC3H2, TENS1, EMAL4, ZBT20, TANC2, E41LA, APMAP, ARFG3, GEPH, ENTP7, BMP2K, RN146, STAU2, T106B, CARF, TAB2, GGA3, ARHGC, SPN90, DLGP2, CAMP3, PHRF1, PLCE1, STOX2, KANL3, ARP21, S30BP, NRBP, CDC23, GGA2, AKA11, GMEB2, TNIK, PARP4, HCN2, MRTFB, YETS2, EPDR1, NOTC3, SPAT2, SYNRG, G3BP2, BSN, SCAF8, LIMC1, TRAK1, SHAN2, RIMS2, SRRM2, CTND2, JIP1, KCC2A, DLGP4, E41L3, GIT1, WNK2, C2CD2, TLN1, ARIP4, MTCL1, DCAF1, RPGF2, PRC2C, SHAN1, FLVC1, NCOR2, GMEB1, EMIL1, EPN1, NUMBL, M3K4, PCLO, ZHX2, S23IP
Species: Homo sapiens
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