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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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Li S, Zhu H, Wang J, Wang X, Li X, Ma C, Wen L, Yu B, Wang Y, Li J, Wang PG. Comparative analysis of Cu (I)-catalyzed alkyne-azide cycloaddition (CuAAC) and strain-promoted alkyne-azide cycloaddition (SPAAC) in O-GlcNAc proteomics. Electrophoresis 2016 37(11) 26853435
Abstract:
O-linked β-N-acetylglucosamine (O-GlcNAc) is emerging as an essential protein post-translational modification in a range of organisms. It is involved in various cellular processes such as nutrient sensing, protein degradation, gene expression, and is associated with many human diseases. Despite its importance, identifying O-GlcNAcylated proteins is a major challenge in proteomics. Here, using peracetylated N-azidoacetylglucosamine (Ac4 GlcNAz) as a bioorthogonal chemical handle, we described a gel-based mass spectrometry method for the identification of proteins with O-GlcNAc modification in A549 cells. In addition, we made a labeling efficiency comparison between two modes of azide-alkyne bioorthogonal reactions in click chemistry: copper-catalyzed azide-alkyne cycloaddition (CuAAC) with Biotin-Diazo-Alkyne and stain-promoted azide-alkyne cycloaddition (SPAAC) with Biotin-DIBO-Alkyne. After conjugation with click chemistry in vitro and enrichment via streptavidin resin, proteins with O-GlcNAc modification were separated by SDS-PAGE and identified with mass spectrometry. Proteomics data analysis revealed that 229 putative O-GlcNAc modified proteins were identified with Biotin-Diazo-Alkyne conjugated sample and 188 proteins with Biotin-DIBO-Alkyne conjugated sample, among which 114 proteins were overlapping. Interestingly, 74 proteins identified from Biotin-Diazo-Alkyne conjugates and 46 verified proteins from Biotin-DIBO-Alkyne conjugates could be found in the O-GlcNAc modified proteins database dbOGAP (http://cbsb.lombardi.georgetown.edu/hulab/OGAP.html). These results suggested that CuAAC with Biotin-Diazo-Alkyne represented a more powerful method in proteomics with higher protein identification and better accuracy compared to SPAAC. The proteomics credibility was also confirmed by the molecular function and cell component gene ontology (GO). Together, the method we reported here combining metabolic labeling, click chemistry, affinity-based enrichment, SDS-PAGE separation, and mass spectrometry, would be adaptable for other post-translationally modified proteins in proteomics.
O-GlcNAc proteins:
AXA2L, EIFCL, MYO1C, P2Y10, IPO5, PLOD2, DDX3X, ZN197, XPO1, PPM1G, HNRPR, ACTN4, SNG2, OGA, UGDH, BRD4, FLNB, U520, IDHC, TOM70, K2C75, LDHA, AL1A1, DHE3, PGK1, PIGR, IGHA1, K1C14, K2C6A, LMNA, ALBU, TRFL, K2C6B, K2C1, AT1A1, ALDH2, S10A8, ITB1, K1C18, K2C8, ENOA, G6PI, HYEP, PDIA1, TBB5, SYEP, HS90A, 4F2, HS90B, VIME, K2C7, K1C16, RSSA, DLDH, PARP1, LIGO3, UBB, HS71A, CH60, BIP, HSP7C, PYGB, G6PD, C1TC, K2C3, ACTN1, PEPD, XRCC5, RINI, EF2, K1C10, K1C13, K2C5, PDIA4, P4HA1, GLU2B, KPYM, ENPL, HNRPL, PLAK, DESP, NCPR, AT2A2, NAGAB, HSP76, CAN2, NUCL, IF2B, ANXA7, FLNA, TGM2, PUR6, UBA1, SAHH, RPB1, ATPA, MOES, EF1G, CALR, MAP4, CALX, ITPI2, TKT, PDIA3, 2AAA, AL3A1, CPSM, QCR1, HNRH1, STIP1, HSP74, K1C9, MYH9, MYH10, K22E, PRS7, SRBP1, HSPA9, IF4A3, IF2G, LPPRC, MATR3, AL3B1, NAMPT, UBP5, KI67, MAP1B, UTRN, IQGA1, TCPE, K2C6C, AL9A1, NASP, FAS, TCPG, EFTU, SYAC, F10A1, TCPQ, TCPD, 6PGD, HNRPM, ACLY, SYRC, UBP14, S12A2, TERA, ECHB, NP1L1, EIF3B, SYMC, EIF3E, ACTB, UB2D3, ARP3, HNRPK, PRS4, ACTC, EF1A1, TBA1B, TBB4B, KRT85, PRKDC, DCD, S25A3, CLH1, HNRPU, SPTB2, PFKAP, FKBP4, AKA12, IF4G1, K1C17, CKAP4, DHX9, RBBP4, TP53B, TRAP1, PSMD2, SQSTM, TBB3, SPTN1, HNRPD, EIF3A, GANAB, GOGB1, IMB1, NUMA1, PDIA6, PLEC, PCM1, K1H1, KCC4, DREB, TRXR1, HKDC1, LRRF1, FILA2, BIG3, CROCC, BROX, K2C79, K2C80, PRP8, CCD81, SPT6H, SND1, MYH14, CC190, HORN, UNC80, GHDC, CDRT4, TXND5, NDRG1, GCN1, TNPO1, SIPA1, ERO1A, ODAD4, VPS35, ERP44, EHD4, SLK, RTN4, DDX21, SYFB, MYOF, RRBP1, SRP68, ACINU, SRRM2, PA2G4, MA2B2, RTCB, TLN1
Species: Homo sapiens
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