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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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Malaker SA, Penny SA, Steadman LG, Myers PT, Loke JC, Raghavan M, Bai DL, Shabanowitz J, Hunt DF, Cobbold M. Identification of Glycopeptides as Posttranslationally Modified Neoantigens in Leukemia. Cancer immunology research 2017 5(5) 28314751
Abstract:
Leukemias are highly immunogenic, but they have a low mutational load, providing few mutated peptide targets. Thus, the identification of alternative neoantigens is a pressing need. Here, we identify 36 MHC class I-associated peptide antigens with O-linked β-N-acetylglucosamine (O-GlcNAc) modifications as candidate neoantigens, using three experimental approaches. Thirteen of these peptides were also detected with disaccharide units on the same residues and two contain either mono- and/or di-methylated arginine residues. A subset were linked with key cancer pathways, and these peptides were shared across all of the leukemia patient samples tested (5/5). Seven of the O-GlcNAc peptides were synthesized and five (71%) were shown to be associated with multifunctional memory T-cell responses in healthy donors. An O-GlcNAc-specific T-cell line specifically killed autologous cells pulsed with the modified peptide, but not the equivalent unmodified peptide. Therefore, these posttranslationally modified neoantigens provide logical targets for cancer immunotherapy. Cancer Immunol Res; 5(5); 376-84. ©2017 AACR.
O-GlcNAc proteins:
SC16A, ASTN2, IGHM, NFYA, NOTC1, SPTB2, MEF2C, PICAL, CDK13, MEF2D, NFE2, PRC2B, UBAP2, TXD11, MCAF1, ZCCHV, POGZ, SYVN1, PRSR1, HIPK1, KAT6B, F168A, EP400, MINT, UBN1, DCP1A, TLR9, CDK12, MRTFB, R3HD2, PRC2C
Species: Homo sapiens
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