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Zhang N, Meng Y, Mao S, Ni H, Huang C, Shen L, Fu K, Lv L, Yu C, Meekrathok P, Kuang C, Chen F, Zhang Y, Yuan K. FBXO31-mediated ubiquitination of OGT maintains O-GlcNAcylation homeostasis to restrain endometrial malignancy. Nature communications 2025 16(1) 39894887
Abstract:
Protein O-GlcNAcylation is a post-translational modification coupled to cellular metabolic plasticity. Aberrant O-GlcNAcylation has been observed in many cancers including endometrial cancer (EC), a common malignancy in women. However, clinical characterization of dysregulated O-GlcNAcylation homeostasis in EC and interrogating its molecular mechanism remain incomplete. Here we report that O-GlcNAcylation level is positively correlated with EC histologic grade in a Chinese cohort containing 219 tumors, validated in The Cancer Genome Atlas dataset. Increasing O-GlcNAcylation in patient-derived endometrial epithelial organoids promotes proliferation and stem-like cell properties, whereas decreasing O-GlcNAcylation limits the growth of endometrial cancer organoids. CRISPR screen and biochemical characterization reveal that tumor suppressor F-box only protein 31 (FBXO31) regulates O-GlcNAcylation homeostasis in EC by ubiquitinating the O-GlcNAc transferase OGT. Downregulation of O-GlcNAcylation impedes EC tumor formation in mouse models. Collectively, our study highlights O-GlcNAcylation as a useful stratification marker and a therapeutic vulnerability for the advanced, poorly differentiated EC cases.
O-GlcNAc proteins:
FR1L5, ERIC2, PKHG3, CCD78, ZN320, WDR27, MBPHL, CFA69, CDHR4, PINLY, VWA3A, NPB15, AKD1B, CC154, AGAP5, MET15, SAC31, CB081, TTL13, ENO4, CFA96, ZSWM8, OCAT2, NPIB5, LYRM9, ZBBX, CMI2B, NOTO, ARG33, CMA1B, DCD2C, IQCF6, ZN487, SHSA9, ADM5, PROB1, PTG3L, TM262, CK098, CS084, DCDC1, BACH, S28A1, SYT5, VMA5A, PITM1, MPP10, CCL22, EST2, P3C2B, UBE2C, TOR1A, P5I11, RPC1, PSA7, TR13B, RGS12, HAT1, CE290, NPFF, PGRC2, NPHP1, SIVA, TRI18, HMGB3, MRP3, INSI1, SRGP3, ADCY6, FGF16, IF4G3, ADA20, HTSF1, RAD21, NPA1P, L37A3, EREP2, NMD3B, TSN1, DPM1, TOM1, NSMA, HUS1, CTNS, AOC2, NPHP4, SNN, PROP1, PEX14, MED24, Z324A, UBP2, ZMY10, SPI2, IDHC, RBBP9, SOAT2, SPF27, DNJC8, FGF18, UBP1, BAIP3, FARP2, ZN432, KDM4B, HEXI1, UPP2, REC8, NDUB4, MRP6, RASL1, TACC2, RPGF3, BAG4, ATS2, ACSL3, RAB36, FRITZ, DRC4, CCNE2, ANF, PROC, PDGFA, LCAT, B3A2, CFAI, CO5A2, PGK2, RU2B, FGF4, PKHD1, SPRC, INHBB, F163B, OST4, PRR35, PAL4G, CGB3, VSIG8, COX8A, MYBB, RALA, CD79A, PCNA, ECP, PPA5, PRG2, OXDA, ZNF44, RFA2, UD2B7, STMN1, YBOX3, ZNF19, ZNF23, INAR1, SAP3, PRS6A, GBRB1, TNR1A, AOC1, AMY2B, PSB1, LMNB1, CAN3, CP3A5, HNF1A, CP2A7, ENDOU, ZNF10, DRD4, CCNO, CP7A1, CRYGS, EST1, RIR1, PAR1, MCM3, PSA2, PSA3, HMGB2, KAD4, PSB6, MZF1, RBL1, PTPRM, 3MG, PBLD, STX2, ERD22, MCM5, GALNS, SDC2, BMP8B, SPB6, RFA3, DEK, PRS7, GGT2, TNR3, TALDO, IF4A3, FEN1, HNF4A, M3K8, LAP2A, LAP2B, STAT6, MTHR, AL3B1, S15A1, MSS4, RFX2, INAR2, PRC2A, HSP13, GCST, PAXI, MAPK2, RPIA, CENPA, CENPF, PRI1, ACADV, NUMB, 5NTC, GUAA, DNLI4, ZNF83, IRAK1, CCR8, CLCN7, VAV2, ZN140, BIEA, MK10, OAZ1, AT1B3, DRG2, RAD, FGF8, UCN1, FOXA1, ALR, CTBP2, BCAR1, WDR4, CORO7, FBXW4, CABP4, RAB15, DJB13, SC61G, PTEN, SRP54, CKS1, PFD3, SUMO2, PP1A, PRS4, RUXG, LSM3, TYB4, TRA2B, 3BP2, RBM6, RPP38, HEPC, GPSM2, BAT1, RT35, CBX1, METK1, TF2B, CDK3, E2F1, MLRA, MYL5, ID2, P, HGFA, LGUL, RAD51, MCL1, PDE4C, SG11B, F27E3, DMPK, R51A2, INCA1, CF210, MGAT2, SFSWA, BIRC1, PAFA, IFT88, KLF10, SEM3B, PHLP, PPIG, PEX6, RB33A, DPOA2, SRC8, FLOT2, GALE, SLBP, HABP2, MCM6, TTLL4, RRP5, 2A5D, CND2, SPCS2, AR6P1, K0040, PEA15, CDK10, PON2, 2A5A, IRF4, TAF5, TAF1C, TRBP2, TRIP6, ZNF79, E2F4, ZN239, SNAT, NFE2, STX1A, MEA1, MK06, CDKN3, THTR, PCKGM, ZN827, MOONR, CL16A, MTHSD, FA83E, CF184, TECT1, PRSR3, TXIP1, CCD57, HKDC1, FHOD3, BTBDG, GFOD2, TKFC, TTLL9, DRC12, CDNF, HYDIN, SRCRM, PCDP1, CCD40, IQCC, PLCH1, VAS1L, PDCD4, LRC23, ZC21C, T4S20, FBLN7, CC157, M3K19, PAN3, TRI61, HERC4, MDH1B, ZN311, CC038, DYLT4, MEIG1, RRP12, WDR38, EFHC1, COL12, PA2GC, MANEA, PKHS1, SNPC4, F201A, F120S, MORN1, CFA70, UBX11, AXDN1, MRP7, ZFY27, AGRF1, CFA58, KIF24, SYT6, IER5L, ARM12, KAD9, DAAF9, CF163, RHG40, TMCO4, STPG1, EFCB6, CROCC, MEX3C, CBPC2, MCAF2, GP157, AXA81, CCD30, AGAP6, SLX4I, NXNL2, ARMC3, TTC23, FBX31, FBXW9, AL2CL, KFA, ATG9B, FTM, SLN13, FRPD2, Z518A, DMKN, TTLL5, ABLM2, ELP2, IQCE, CCSAP, ACD10, LCN12, OGFD2, NANP8, SAPL1, PWP2B, SWAP1, EFC12, NXRD1, ANR54, RM14, LTMD1, WDR93, EDC4, CP046, WDR73, PRS54, CP087, HAGHL, DCR1A, ATAD2, SPG17, ATRAP, ZN474, PLPR3, NHS, CC171, MAP12, GLB1L, BI2L2, RBP10, NSMF, CSC2A, DNMBP, DJC14, THADA, ZN497, LRC69, TMM91, DG2L6, PKHG7, MMS22, RHG27, FA47E, TM1L2, TTL10, KCP, UBP43, SMIM5, MED25, ZN765, CENPQ, MCM10, STRAA, MICA3, ZN367, APTX, TMC4, MUC19, DPOLN, SAXO4, CEA19, ADAT2, CATIP, ZN605, MYPN, YRDC, NHRF4, NLRX1, CAPS2, ST32C, THOC4, SESD1, WDR5B, TMM17, DAA11, NUD13, CNDG2, CTSR3, TXND6, DZIP3, PTH, TDRP, MYLK4, CASC2, RN135, CF337, ZN584, FMNL3, MSTN1, T151B, TRI59, CD302, CMA1C, DRC2, PGKA1, DRC7, CKP2L, DI3L2, SUV3, CCD13, SYTL1, REM2, CC170, KATL2, CFA46, RN168, DZI1L, AGRF2, CDK20, ASPM, TENS4, CENPL, ATOH7, F177A, ORML3, AHI1, CF107, ARG28, PYRD2, ABD12, LRC43, OR2LD, BBS5, PHTF2, TXND3, SVOPL, MINK1, ARL14, SPA6L, CCD24, LRC71, ARRD1, CC022, CCD33, TM148, CN178, BEND7, ADGB, CL076, ENDOV, S2529, CB069, IGS22, MUT7, CI163, SR1IP, ANR53, DAAF3, NLS1, NETO2, ZN485, MACA2, ADAD2, MORN4, CFA43, ZN248, TT21A, NSUN7, CS018, TTC16, DEN6B, ARMC2, DAAF1, TRPV1, WDR19, ANKK1, BHE22, BBS1, CC148, BEST4, NLGNY, CADM4, NEK11, OR1K1, O13C5, SVIP, DNJB8, CLHC1, GA2L2, ZSC18, PMFBP, ADA32, MIEAP, FANK1, SPP2B, SACA4, DLG5, NSUN6, TBCK, ZDHC1, NEUFC, S38A5, BLNK, OSCP1, SNR27, SKA2, TFB1M, STAG1, CQ050, TEKT4, DYDC1, SPIR2, S13A3, MB3L1, SREK1, MT21A, ASB13, ATS14, DYH7, PPM1E, TM234, CV015, TCPW, GBF1, LAR4B, NPIB3, PXDN, RSLAA, N42L2, DNSL2, OSTF1, HPS1, CLP1, WNT8B, SCAM4, TF3C6, LSM10, PMEPA, AKTS1, LENG9, ELMO3, ARL8A, ZN669, TIFA, EAF2, RB39B, DYH11, DRC10, RRFM, NGBR, OMA1, ZN837, CHFR, ADAT3, NEIL1, KIF12, IFT43, LRC46, HMCES, MED8, FAH2A, MSD3, CCD34, ZN845, RSRC1, TXD15, MRP9, MRP8, CHAP1, LRIQ1, BT3L4, DNJC1, RPGR1, ALPK3, IFT74, CCD17, CC74B, LRGUK, CFA53, KAD8, STAC3, HEXI2, PPM1M, CFA57, NOL4L, F218A, SPT33, CFA54, ZN396, SPT13, ODAD4, PCFT, AGAP4, FCRL4, ERMAP, ALS2, PRAM, ALPK1, 1A1L1, FCRL5, S26A8, MED15, IF140, CEP89, MBOA4, MMS19, INSM2, TBX5, TEAD3, CDCA3, SPSB2, RAD9A, ZN184, MGLL, ATX2, BARD1, FOXB1, SPAG8, RNZ2, TCF25, MEP50, LBHD1, PSD2, NEUL2, PIGQ, CPPED, HDHD3, GCP2, FEM1A, PHAF1, FUZZY, CHCH7, DERL1, DHRS6, RSRP1, KTNB1, KIFC3, DPCD, SMIM2, IFT27, THIC, NADAP, TM2D2, BBS2, TEKT3, IDI2, NUSAP, CAYP2, STK33, TRI55, BCDO2, DB126, FRMD8, PITM2, OSBL7, ULBP1, CHIA, B2L14, TSG10, SPEF2, ZFHX2, CFA74, ZN436, DYH6, LRC27, BSSP4, DNAI2, CHST5, CLPB, DRC9, ENKD1, TKTL2, MMP28, MIXL1, ZN106, VCX1, ABHGB, TOR3A, FA83D, COE3, MROH8, CSTP1, TM231, TASP1, CS044, CJ095, TBA4B, WDR76, CN093, COG4, MLXIP, KIF9, S28A3, SIAE, CLSPN, CYBP, NMUR1, IF122, PARVG, SPC25, LST2, ARGAL, NCK5L, LRC4C, SPCS, NRX3B, EMC7, UBE2T, SLAF7, TMM9B, TF7L2, IFT46, XPP3, ANM8, AAAS, STK36, SOSSC, GLRX2, CLTR2, KIF15, SEM4G, CT096, MITOS, KLH11, HAUS2, MED9, CB042, SIR5, MKS1, P4HTM, ARH38, PP4R2, BTG4, APC11, WSB2, MYOF, C1RL, CC167, KCMF1, RN181, SPAT7, CAC1I, DYH1, KIF17, C2D2A, MYEF2, ANKY1, SAE1, IF172, DPOLL, NAT8, RPGFL, NDUAC, SCNBA, DNAI1, TEKT2, PS1C1, KAD3, APC5, GGA1, DJC12, FBXL2, NXT1, RALY, TSN16, FBX5, INTU, TPC1, ABT1, AKP8L, GUC1B, PCDGG, PCDA6, RHG26, RBL2B, B9D1, ANR26, CE164, MOK, SPG7, LAMP3, COLQ, DLEC1, PSF2, KCNK6, INVS, ASF1A, FBW1A, VP9D1, SL9A8, WDR37, GSTK1, RT28, RPC10, UB2J1, COQ4, EXOS1, CBY1, DYR1B, AAKB1, NRX3A, C170B, SPEF1, IFT25, SHAN1, ASB4, CEP83, PCDGM, TM14A, CABIN, USH1C, TNR11, SCIN
Species: Homo sapiens
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Levine ZG, Fan C, Melicher MS, Orman M, Benjamin T, Walker S. O-GlcNAc Transferase Recognizes Protein Substrates Using an Asparagine Ladder in the Tetratricopeptide Repeat (TPR) Superhelix. Journal of the American Chemical Society 2018 140(10) 29485866
Abstract:
The essential mammalian enzyme O-GlcNAc Transferase (OGT) is uniquely responsible for transferring N-acetylglucosamine to over a thousand nuclear and cytoplasmic proteins, yet there is no known consensus sequence and it remains unclear how OGT recognizes its substrates. To address this question, we developed a protein microarray assay that chemoenzymatically labels de novo sites of glycosylation with biotin, allowing us to simultaneously assess OGT activity across >6000 human proteins. With this assay we examined the contribution to substrate selection of a conserved asparagine ladder within the lumen of OGT's superhelical tetratricopeptide repeat (TPR) domain. When five asparagines were mutated, OGT retained significant activity against short peptides, but showed limited limited glycosylation of protein substrates on the microarray. O-GlcNAcylation of protein substrates in cell extracts was also greatly attenuated. We conclude that OGT recognizes the majority of its substrates by binding them to the asparagine ladder in the TPR lumen proximal to the catalytic domain.
O-GlcNAc proteins:
E2F8, PRXD1, TSPY2, CGB1, ZN839, CENPX, PDLI1, WWP2, FOXN3, IMA4, DPYL4, ABLM1, MEIS2, HGS, GAK, PLS1, MAGB4, ARPC5, DC1L2, FGF16, WIPF1, FRS3, RNF13, ZN207, ENSA, SMCA5, CE104, OGA, AP180, PQBP1, E2F6, ADAP1, DNJC8, FLOT1, TPPP, SCEL, CELF2, RPGF3, CLD14, KLF8, BAG3, PAK4, IGHG3, MBP, NFIC, SNRPA, CEL3A, RU1C, IGLC1, MTAP2, ERG, DMD, IRF2, ENPL, FOSL2, F261, SDC1, ATF1, ATF3, ELK1, TFEB, RXRA, COMT, USF1, FGFR3, NR4A1, THAS, MARK3, ARNT, PSB4, RBMS1, FCERG, MPIP1, CSTF2, CD68, BMI1, COPB2, SOX5, RS19, ARL4A, ETV5, IPP2, STAT6, ABL2, KSYK, TFPI2, RFX5, RXRG, CDK8, GSK3B, TAF6, SPS1, DNLI3, DYN2, GALK1, AGFG1, SC24C, DLX1, HDAC4, CTBP2, KLF3, TIRAP, PPIA, CSK21, 3BP2, SSBP2, CDKL1, BORG5, TFAP4, ROR2, CACB1, CREM, MECOM, TLE4, FAK1, COEA1, MTG8, GABPA, GABP1, DERM, TLE5, DEMA, ASPH, PP1R8, LCP2, DUS4, MTAP, EI2BE, G3BP1, GRB10, MTA1, PPIL2, PICAL, DYR1A, FHL3, NCOA4, CAYP1, CIRBP, DGCR6, VGLL4, CAPR1, GRB7, CASL, MEF2D, LASP1, SPCS2, SEPT2, PCM1, SIX1, SF01, TRIP6, RHOH, TAB1, ADRM1, CCDC6, BATF, NFE2, MAR1, NRF1, SMTL2, LETM2, OD3L2, AX2R, AMOT, AKIR2, PRR30, LARGN, RGPS1, PRC2B, TEX30, SNP47, PHYD1, KANK4, EEIG1, CPTP, AHDC1, KHDR2, EF1DL, OLM2B, ANKS6, RHG17, CNDH2, GRHL2, HMBX1, JHY, PP4R4, JMJD6, SCYL2, GOLM2, RSBNL, PSRC1, DRIC1, KCD18, FIP1, SAS6, CLM9, CCBE1, DUSTY, E400N, TM1L2, UBP45, MARK2, KCTD9, MCM10, CC186, POGZ, FLIP1, TAF8, RM55, S1A7A, SYVN1, PHLB1, CASZ1, PIM3, GA2L3, DDX42, CEP57, SPAS2, Z280B, PDPN, KCC1D, TF2LX, LOXH1, ARI3B, APLF, CC28A, RHG12, SKA3, PHC2, HYCC2, CMIP, SMAP1, RUSD2, ABI1, SYCE1, RPTOR, BATF2, S35F6, KLH36, ANS4B, MARHA, ZSCA1, UXS1, NECP1, BBOF1, LIPB2, MISSL, PHC3, TMIE, NUP35, OR4D6, JOS2, WDR48, GABP2, DPTOR, ALAT2, BRSK1, GRP4, HELQ, BL1S5, BCAS4, LMX1A, SSH3, SH3R2, FBF1, DLRB2, HDAC7, STYX, GTSF1, NEUR4, CSRN3, AP2B, SHC3, RORB, STAM1, CELF1, ARHG1, CSN5, RBPMS, ZDH16, PMEPA, UTP4, FERM2, SOSB2, R51A1, CR025, LENG1, BIRC7, PBIR1, CC126, PF21B, NRBF2, EDC3, PDLI5, ANCHR, ZC3HA, PKNX2, EGLN2, MARK4, UB2E2, PRRC1, NOL4L, AP4AT, SCLT1, TOX2, QKI, PNMA5, YPEL2, NUDC1, RB40C, UBL7, CK2N2, OSBL9, PNKP, PLIN2, CDCA3, HCD2, SNAG, ARI3A, DPYL5, CG025, SOSB1, TCF25, COE4, MIC25, UTP23, ALKB7, RBM42, LRRC1, TRMO, MCRI2, RSRP1, BBLN, ASHWN, SARG, NADAP, SSBP3, PLVAP, OSB11, B2L13, STK31, DGC6L, RM01, KLC2, SIK2, REN3A, NELFA, PPDPF, ILRUN, ES8L2, KI3X1, SP14L, B2L12, PKHA3, PKHA1, TAF9B, ARNT2, SYTL2, CIP1, CASS4, HINT3, PRDM5, PAR11, MBNL1, BRWD1, KLC4, TB22B, MBNL3, NFIP2, ZSC32, TMOD3, UGGG2, CWC15, KANL3, RBPJL, DKK4, LIMD1, DPOLL, AFF4, UBQL2, PUF60, BAZ2B, GGA2, ING1, BORG2, AGO2, ZHX1, MUCEN, ANR50, PCDGK, POLI, LIMC1, SMAG1, BAIP2, RPC10, PPIL1, C2CD2, MTL5, TBL2, YTHD2, T10B, SNX14, RT18B, GMEB1, STON1, PCLO, ZHX2, S23IP
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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