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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, GRP75, IF4A3, COIA1, STAT3, MDHM, ECHA, IF2G, PERI, ELK3, LAP2A, LAP2B, STAT1, 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, HCFC1, 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, TLE3, 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, CA131, 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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Huo B, Zhang W, Zhao X, Dong H, Yu Y, Wang J, Qian X, Qin W. A triarylphosphine-trimethylpiperidine reagent for the one-step derivatization and enrichment of protein post-translational modifications and identification by mass spectrometry. Chemical communications (Cambridge, England) 2018 54(98) 30379171
Abstract:
We report a new reagent that is capable of both chemical derivatization and selective enrichment of azide-labeled PTM peptides for sensitive identification by mass spectrometry (MS). Facile sample recovery, enhanced ionization and fragmentation in MS of the enriched PTM peptides are achieved, which leads to the identification of 3293 O-GlcNAc peptides and the location of 1706 sites in HeLa cells and efficiently expands the current mapping scale.
O-GlcNAc proteins:
MEIKN, BLT3B, SHOT1, TTC24, PIPSL, HFM1, ZN320, NBAS, CQ102, VWA8, SBNO1, Z804B, CC14C, SH321, EFCB5, XIRP2, ODAD3, CNOT1, BDP1, ANR62, CC88B, AN33B, NKX26, PGP, F186A, ARRD5, FBP12, ANKUB, CI092, CE052, FA47D, SMHD1, LRIQ4, GLOD5, ZN233, SH2D7, MARHB, TTLL8, ABTB3, A30BL, ZSWM8, P121C, ERI2, PP2D1, CEA18, R212B, YV023, ZN727, VGLL3, YD021, RUXGL, IQAK1, MAGBH, FOXO6, FHAD1, SRRM5, ZN879, S14L6, CJ142, KRBX1, MCRI1, FONG, CE067, F227A, CRCC2, KIF2A, MYO1C, EYA2, AP3B1, SPT5H, TAF4, HIP1, CDC7, ST1C2, WASL, IPO5, EMAL1, P3C2A, EXOC5, PSDE, USP9Y, BCL9, CAC1A, PITM1, MPP10, TRI38, NDKM, ARI1A, NCKP5, FCHO1, SOCS3, TRAD1, RHG33, TYB4Y, UTY, ENC1, ZN197, APAF, TERT, CHK1, GNB5, TCRG1, UN13B, RASM, PPE1, IFIT3, IKKB, TIM23, HGS, AURKA, MYPT1, XPO1, IPP2C, ZN646, PDZD2, SPTN2, SET1A, TRNK1, PER2, SYNJ2, ZN536, IKKA, TBX3, ARPC2, TBXT, VILL, NKRF, ZN185, CASC3, CLIC2, ACOX3, NPHP1, OGT1, PPM1D, RA51B, SHIP2, EIF3D, IPO8, MSH4, MAGB4, ARPC5, PER1, ZSC9, ZZEF1, TET3, SI1L1, PRP4, SERA, IRAK2, PSMD3, TEX33, AP5Z1, MTSS1, PAX4, WDR62, PRPF3, SYNJ1, IF4G3, KCAB3, E41L2, FOXO3, TGM5, SYT7, PPIP1, CHM2A, PLRG1, LDB2, BUB1, HTSF1, STX6, ENSA, CPSF5, CREB3, AK1BA, KALRN, MYPT2, MED14, SOX15, KLK8, PRKN, SMCA5, ZC3H1, TYW4, LZTS3, GANP, KIF1B, PHLP1, ZN861, BRNP1, MPZL2, OGA, VINEX, HNRPQ, RNBP6, GMDS, REV3L, JAK2, MAFK, MUSC, CTND1, HPGDS, Z354A, RT14, PQBP1, BRD4, ABCB7, PLCH2, SRGP2, DEN4B, N4BP1, ROCK2, COBL, CPNE3, ZBED4, LIPA3, OBSL1, BRE1B, PHF2, ZC11A, CLU, DJC13, ANR17, SIN3B, LIPA2, LIPA4, ZN253, ZN217, FLNB, NCOR1, NDUS6, RM33, DPOLQ, CDC45, MPPB, USH2A, SRS10, GEMI, ECI2, TAF5L, ZN821, DAB1, MYCB2, U520, OFD1, UTP20, NU155, S2512, PALM, ZN189, CCNK, SERF1, PIAS1, DNJC8, RAD17, ANXA9, CLPX, SEGN, CDKL5, NEBL, S14L2, RECQ4, RECQ5, RMP, AL1A2, TOM70, TOX4, MICA2, K0754, FCSD2, SRBS2, SASH1, CSCL1, LRIG2, SUN1, PRP6, PCF11, KDM4B, CE152, SOX30, UBR5, REC8, DUS14, NDUB8, KLHL2, LETM1, MBD4, KAT7, KCNH1, SMC2, IPO7, SLU7, SVIL, NPT2B, LCA5L, FMNL1, PCNT, CNOT4, CPSF4, NFAC1, EYA4, BRD1, HERC2, HS74L, RIGI, ZMYM6, BAG3, DCMC, DDAH2, TGM3L, TBX18, TBX6, BCL10, APBA3, NSD2, GSHR, CRYAB, LMNA, SPTA1, ESR1, ANGI, TDT, CYTB, GCR, SODM, MYCN, G3P, P53, HSPB1, ARGI1, PCCB, RLA2, RLA0, RPC4, K1C18, FYN, NFL, NFM, PERT, CRGC, SYEP, ANXA6, RHOC, GLI1, PFKAM, CATG, INHBA, VIME, ANXA5, SNRPA, VILI, CN37, HMOX1, DLDH, HXB7, DPOLA, IFIT2, WEE2, FBSP1, BNIP5, AN34C, ACSM4, PRR29, F90AO, YT014, R10B1, GRL1A, F200B, DERPC, CTF8, ZN888, RGPD2, GIMD1, ZN728, CH088, AT8OS, MYBA, ARAF, ODP2, KAP0, HEM4, HSP7C, SPTB1, TOP2A, VDR, DMD, ADHX, NFH, TPR, ANXA3, SKIL, NR2C1, HXD8, ENOB, T2FB, MTDC, 3BHS1, GFAP, KPYM, HXB1, PO2F1, ERF3A, EZRI, PHKG2, DESP, ANK1, NCPR, CBPE, PLCG2, ZFX, ZNF14, ZN708, ZNF17, ZNF19, ZNF20, ZKSC1, ZNF28, ZNF30, ZSC20, ZNF7, KPCA, UBF1, ATF7, DDX5, LOX12, EGR1, ARY1, SON, ATF1, ATF6A, NUCL, HXK1, TNNI3, HME2, SL9A1, RAB3B, LMNB1, GRAH, NEBU, AOFA, ZNF10, TGM2, MUTA, PERL, ROA2, CBL, KAPCB, HEMH, XPA, CRCM, SAHH, IF4B, PAX7, GATA2, CPT2, RIR1, EF1B, CCNC, DNJB2, PSA1, MOES, DDX6, RAE2, PTBP1, SYVC, 1433T, ARNT, RFA1, MAP4, PSB9, TMOD1, ITPI2, HXD9, ERCC5, EPHB2, PTN6, SHC1, KDM5A, LMOD1, TYK2, PRDX6, CDC27, WEE1, MPIP1, MPIP2, NKTR, CLIP1, RPB2, KAP1, CPSM, ZEP2, CASPE, 1433B, STIP1, FOXN2, TF2H1, C2TA, LSP1, DUT, GCYA2, MCM7, HYES, MPI, CTNA1, NOS2, SPB6, MERL, RFC4, RFC1, ADML, RORA, CBS, GDE, ACTN2, ADDB, NU214, DEK, CYLC1, ATP7B, SOX5, SOX11, ZNF93, VATE1, 8ODP, LONM, PGM1, GNL1, PEDF, ODO2, SRP14, IF4A3, SMBP2, CUX1, TYRP2, MLH1, STAT3, UBP8, PEX19, ECHA, ETV6, STAT6, AF9, HELZ, LPPRC, HD, ECE1, MUC18, BTD, MAGB1, KSYK, UBP5, KI67, KPB2, KPB1, RECQ1, IF2M, BRCC3, RL28, MAP1B, NEDD4, UTRN, CAPZB, CDX1, RL29, UCRI, PPCE, RFX5, PI42A, RXRG, NRIP1, PRC2A, CCN3, AL9A1, NASP, RM19, CENPF, MCM2, YLPM1, VPS41, NUMB, CLK1, NU153, RBP2, RGS3, RGS7, TSC2, TAF6, DNLI3, ETV1, DYN2, TUB, TCPD, PAPOA, PLCD1, ZNF80, ZNF81, ZNF84, BRCA2, RENBP, MECP2, HCFC1, SSDH, AFF2, AFF3, MYOM1, HNRPM, NCBP2, MP2K6, GDIR2, AGFG1, ZN135, ZN142, ZN143, RBM5, SPSY, HXK2, DGKQ, THOP1, TXTP, PPP5, LIMK2, SMTN, DPOG1, ICLN, BLM, PDE1A, GALC, KAD2, IF5, NR1H2, AFAD, AF17, ADK, DSRAD, UCP3, DLX1, SYMC, ATP5I, HDAC4, PEX3, PER3, RP1, SIK1, PRD15, UBS3A, NAC3, NU107, SNX16, RGS8, FBXW4, SESN2, TIRAP, H2B1D, CU082, MCCD1, EIF3E, PTEN, IF4A1, SNP25, DEST, ARP2, ISL1, REC21, STXB1, 1433G, UBP46, TIM10, PRS4, PRS10, ERF1, GAK8, RS4X, RBX1, TRA2B, ACTG, F193A, NOP14, RBM6, GTF2I, DLG4, IRX6, GSTO1, RELN, PRKDC, ELF3, MAP1A, SIM1, SSBP2, TMF1, RT05, RT11, RT09, HMGN5, SKOR1, FOXK1, PRR5, DAB2, EFNB1, RBM10, RBM3, VIGLN, BORG5, FANCC, CLH1, HSF1, MYPC1, U2AF1, SPTB2, TIAR, SET, FOXK2, RELB, AMPD2, ANK2, TFAP4, XPC, OCRL, AK17A, MEF2B, SP2, CENPE, KIF23, MMSA, ID2, ZNF45, APBA1, HEN1, FKBP4, RL6, TOP2B, DYST, KMT2A, CENPC, ERCC6, TAP1, ZN117, ARI5A, IF4G1, TLE3, TLE4, UBE3A, DYN1, SRS11, CALD1, RN5A, EMAL5, BTK, EXOS9, MTG8, GABPA, CDK18, ZO1, TRHY, PDE4B, SPAG1, KHDR1, DPOE1, SRSF4, GOGA3, PDE4C, DEMA, PDE4D, RBL2, ZN844, ACSM1, DMWD, EP300, AHNK, ZNFS1, FCHO2, PLCX2, DYH14, K2012, CGNL1, CF210, FP100, MESP2, NEXN, CPSF1, MPPA, SCRN1, TF3C1, HYAL1, BPTF, SFSWA, SF3A3, DPYD, TP53B, IFRD2, ILF3, EPS8, FOXC1, ANK3, GNDS, SEC20, NFX1, TIAM1, AF1Q, AKAP6, PRDM2, CAF1A, TRAF3, AIMP2, CBX3, DDX10, TBX2, ERCC8, GPS2, SBP1, NMI, PABP4, CD5R2, PPIL2, MB211, PM2P3, ORC1, ORC2, SNTB2, PPIG, FKBP5, MYO9B, GAB1, BIRC2, PICAL, SQSTM, BFSP2, PRP4K, ATR, SNW1, IQGA2, MTMR1, CUL4B, ASPP2, DYR1A, PTC1, RAB32, FHL1, FHL3, PM2PB, CAC1S, THOC5, NCOA4, SPTN1, KCNC3, CDK13, CKAP5, CYLC2, DAG1, SRTD2, MORC3, SAFB2, UBP2L, SCRIB, DOC2B, DOCK1, BTG3, ZMYM3, DYHC1, EI2BA, SRC8, FAK2, FLNC, FA50A, GRB14, HES1, NF2L1, FAT1, DHX8, MCM6, ITPR3, ZN266, ZN235, ZN460, PLSI, PUM1, KANK1, MELK, SMC1A, RRP1B, NCOA6, GSE1, PSF1, BMS1, LBR, STAT4, CBX2, KIF22, MEF2D, MTF1, MYPC3, NC2A, NFIX, ZN638, NOLC1, NR1D2, PSME4, CUL7, SLMAP, GAPD1, FRPD4, CND2, MO4L2, SUZ12, R3HD1, SNX17, S39AE, LRC14, DPOD3, IF4H, KIF14, EEA1, CD5R1, NCF4, PLCL1, PDK1, PLCB4, PLEC, PTPRR, PWP2, IRF4, ZMY11, L2GL1, UBE3C, PUM3, DLGP5, RBY1F, KS6A1, SAFB1, SYCP1, PP1R7, SP17, MED22, TAF1C, NCOA2, TRIPB, PCH2, MED1, JHD2C, ZN174, DLG2, CEBPE, TAB1, STXB2, ZFHX3, ZBTB6, ZYX, SEPT7, ADRM1, AINX, PSMD5, PKN2, TAF12, CDC37, B2LA1, TAF9, MAPK3, TBR1, CP1B1, DGKD, THTR, PCKGM, ZN827, LONF1, EX3L4, TPRXL, GEN, HNRL2, LONF2, SAMTR, PDS5A, MOONR, QSER1, WASC4, EX3L2, TECT1, ERC6L, RGPA2, D19L1, ZXDC, CCD57, PWP3A, ATG2A, FHOD3, IF2GL, KLH38, HFE, BTBDG, LRRF1, RFX4, LRRK1, F161A, INAVA, MA7D1, PKHG6, CHD9, TBC25, C144B, OD3L2, ZN718, AL1L2, P12L1, PTHB1, GON4L, GRDN, GVQW3, PAR14, CP100, ZN404, CL036, SPAS1, SV2C, YJ016, ZFP69, CE022, C2CD3, KMT5B, LARP7, HYDIN, KCD21, IQCC, PLCH1, FIL1L, ARI4B, GRAP1, Z658B, PAP1L, TIGD2, FNDC1, VWA3B, PAN2, CN177, Z585B, SBK1, SNUT2, TYW2, FAKD1, CTSRT, SGO2, CC178, ODFP2, CAVN4, FSIP2, UROL1, ZN628, TRI61, ESCO1, ZN789, BCORL, ZMAT1, PP6R3, DCA17, FSCB, BRD10, ZC12B, NHSL2, ZN831, AKAP4, MTUS2, FA47A, MEIG1, PRC2B, RRP12, IQEC2, SPIN3, ZN506, DOP1, F209B, GASP1, DGKK, CYTSB, CD158, SPXN4, FBX47, TCHL1, TDIF2, ERIC3, LRRK2, SAPC1, CE170, PR15B, CJ055, SNPC4, CTSRE, NHSL1, F120S, C2D1B, TEX35, FA83B, SYRM, AXDN1, FKB15, AKND1, ZC3HD, MPP7, UBR4, ZN684, SWT1, SKT, CC183, RHG21, BEND3, UBAP2, PHF19, LITD1, F27D1, TSTD2, ER6L2, PPR26, ACBD5, UT14C, TUT4, DEP1A, CE162, FRY, ZBT37, MAGI3, KAD9, DDI2, MEI1, CC181, LIN9, ZN658, CROCC, CBPC2, MCAF2, RIF1, ZN468, SPXN1, OBSCN, NTM2D, CE350, RPRD2, SYDE2, KLD7A, BRE1A, MYOME, P210L, ZN318, A20A3, ZN691, PPRC1, SPO16, MYSM1, NTM1B, TAF3, SNX30, TASO2, KHDR2, ECM29, NAA35, MBNL2, OBI1, USPL1, F219B, RN123, FBX31, FBW10, ZKSC2, RN213, WDR25, CP135, Z385C, AR6P4, ARID2, TENS3, SPT2, FMN1, ANKS6, USF3, MSL1, S31H1, CRBG3, FRPD2, RHG17, DUS29, C19L1, VIR, CYTSA, ZN660, REP15, BLT3A, SP5, CARL2, K0930, JADE1, SNR48, CAPR2, SPOPL, CCSAP, PKHA7, ADNP2, IF5AL, GRHL2, ZN425, ACD10, IFIX, NIPBL, LIN54, R7BP, TET2, TEN4, Z280D, NAA16, RADX, SANBR, ZSC25, SCMC1, ACSM5, JHY, CRCDL, SWAP1, ZN774, ZN544, JMJD6, CAVN1, FXL22, M18BP, CDC73, T2H2L, XRRA1, TTC41, NEK5, NFRKB, LMOD2, RL22L, PKN3, ERIC5, ANR16, FXL19, ZN880, TM10B, KLH35, PSRC1, BORA, IYD1, KCD18, GASP3, FBX38, FOXR1, ARMD1, BRAT1, ZC3HE, LARP1, ATAD2, SPG17, RICTR, BRWD3, TSSK4, F111B, SAMD1, SARM1, KLH17, PADI6, C1TM, ANR12, ANR11, FIP1, SAS6, UD2A3, CWC27, LRIG3, MIC27, BI2L2, MCAF1, BCOR, MPRIP, ZY11A, NSMF, RBMS3, RPTN, DNMBP, GGYF2, CCNI2, ZN782, EMAL6, SYNE3, MASTR, CU136, MEX3B, ZNF66, ZN793, LN28B, CCD81, RN111, ZN704, BICL1, CC141, WDR87, ZN493, CO039, CCD73, SRCAP, ZN662, NBEL1, YD022, SHSA6, YO027, YJ005, TSH1, CBAR2, CG065, MSD1, K0408, CFA65, UBN2, BEND4, F205A, RHG27, FRMD7, FOXNB, RFX8, FGD6, ANKS3, YS043, VP13C, UBP34, UBP31, UBP53, UBP43, ZN365, CEFIP, CENPU, SSH2, CEP68, SPT6H, RUFY3, ERIP6, DHX30, ZN765, MCM10, DOK3, GDPD3, RFIP2, FAKD5, OTU6A, ZN627, KDM3B, STRAA, MICA3, OTOP3, SSX7, U17L1, H2BWT, ZCCHV, GVIN1, TICRR, EFL1, PBIR2, SETX, KANL1, NUP54, PRIC2, ZN572, RGPD4, POGZ, ZFY16, MYCPP, TMC6, NUFP2, MAVS, CLAP1, DHX29, LIMS2, TT21B, HEAT3, CFA91, ZN438, HDGR2, EMSY, AKNA, RAI1, ANKAR, I2BP2, AB12B, SNX20, SPRE1, RBBP6, ANS1B, UBE3D, PTAR1, TCPR1, RABEK, HUWE1, YTHD3, FLIP1, TAF8, KHDC4, VP13B, S1A7A, PHLB2, CROL1, KAISO, ZN605, UBP37, K1328, RN180, PATL1, MYPN, PEG10, ATG4D, TTC7B, ISCA2, PABP2, LDB1, PB1, RIP, MARH3, NFE4, RIMS1, CATAC, NT5D3, CASZ1, VASH2, LUZP1, MORC1, MYPOP, NRAP, IQGA3, ZCH18, PACS2, MON1A, TSYL5, ZSC30, PARG, LIPB1, LONP2, RASF3, NLRC5, CHD1L, SKAP1, AROS, CDR2L, DAA11, EZHIP, CQ082, CIR1, HTR5A, ZFAN4, SNX32, HOGA1, DRC11, ZN761, GOLI, TRI50, Z354C, CD20B, KMT5C, ZN573, PRGC2, P66A, RASL3, MD12L, I2BP1, RB6I2, RIOX2, MY18B, RBM45, SIAH1, RELL1, LACC1, HID1, ANKY2, PSTK, VRK3, CROL2, PKHH2, AHNK2, TIAM2, AN18A, FMNL3, SAM9L, NAV3, NAV2, CCD50, FABD, MISP, HERC6, WDR75, MFN1, CCD60, TEX14, MA7D3, NXP20, CCD83, DNAI3, MGAP, GCC2, RP1L1, BRSK2, Z3H7A, TPH2, UBR2, ANKH1, SUGP1, SUGP2, KIBRA, GOR, CCAR1, SLF2, RM41, GPAM1, KLHL7, ETKMT, DDIAS, RB12B, ZC3H3, SMC5, DHX37, KBTB2, SPB1, NIM1, C144C, CKP2L, IHO1, SUV3, ERF3B, FANCM, ZZZ3, EXOC8, CF206, P20D2, DAAF8, CFA46, SAXO1, SACDR, RTKN2, SAM14, KMT2E, DOCK3, ABI1, ASPM, F185A, CA087, IQCK, SPG16, SPART, SPICE, TTC5, TAGAP, RPTOR, EID3, AHI1, ZN567, ZN687, REXO1, S6OS1, CRBG2, THEM5, ANR35, CLASR, AN36B, RUSC2, CF223, RHG18, PARP8, EH1L1, METL4, CMYA5, VPS8, PALS1, SYNPO, FNBP4, RDHE2, PRS35, PGBD5, NIN, SPA6L, SPEM1, TT30B, LRC71, AF1L2, CERS5, SRBD1, TAB3, MACOI, MINY1, CCD33, TM148, ESX1, PACRL, TRIMM, TM217, ZN676, NANG2, ANR31, CNTD1, TEANC, ZN615, K1958, ENAH, CDYL2, CO056, ZN709, JMY, ZN454, ZN565, YV006, SR1IP, CDRT4, TAC2N, GAR2, FSIP1, ZN383, PNDC1, FA47B, MARHA, KBTB3, CI106, CAST3, ZBT38, CH058, SMYD1, UN13C, KY, CK072, ZN114, SERB1, HJURP, SEN2, GLBL3, MACA2, SMG8, RN214, Z280C, MROH1, PAPD5, CC168, ICA1L, EHBP1, CBPC5, RB15B, SMC1B, PHC3, BEND2, SIMC1, NSUN7, SRFB1, DDHD1, SP20H, CBPC3, ARMC2, PDZD8, ZN555, RTL9, DP13B, NAV1, WDR19, KMT2C, FBX22, SYNE1, BD1L1, FAD1, FLCN, PXT1, DBF4B, IPMK, ABHDB, DMBX1, FBH1, PJA1, KNL1, NEK11, KDM2B, ARK74, CLHC1, CFA61, NEDD1, RLA0L, ZFP28, THOC2, INADL, KI18A, ZNT5, SNIP1, WDR48, UHMK1, NEIL3, FA76A, ZN671, PRR7, PUM2, KLDC4, NANP, AT2L1, RBM46, PMFBP, CC110, ZN502, TBC15, ZN596, GAR3, FANK1, ZN507, PHOP1, ALMS1, DC2L1, CHD6, HUMMR, SP7, ACTT1, HELQ, DMXL2, DLG5, MIPT3, OTU7A, S26A7, ATS17, S3TC1, TBCK, PO210, CE192, GEMI5, FBF1, RPGF6, SMCR8, PARD3, PNISR, ZN483, DI3L1, ZN526, GIPC2, CP078, DUS19, THAP3, ZDHC1, TB22A, PDC6I, CO040, DCAF4, MITD1, TFB1M, TPC14, DC2I1, UBCP1, TRUB1, LMO7, CKAP2, CCNB3, ATX2L, PHIP, RT4I1, PALLD, CRGN, SYNE2, CNKR2, ASB10, ACO11, P66B, ASB17, BBX, CTBL1, ELYS, TITIN, TRIB2, SMG7, RTF1, IP6K1, PHYIP, DCNL4, P55G, NR4A3, PHF3, NDRG1, HS105, ZN592, PRP16, ANS1A, FAN, AKAP1, ZN75C, CENPI, PRCC, RREB1, HDAC2, DPF1, DPF3, REQU, CBP, SYMPK, HYAS2, KAT2A, RPGR, DDX17, KIFA3, NEO1, RAD50, RAB8B, ARHG2, IRF7, TF3B, DVL3, USP9X, CUL5, LPP, TP4A1, HGD, SMCE1, FBXW7, FBX32, TOP1M, TRI63, LMBL2, ZN622, 5NT3B, FBXW5, PSMG2, TEKT1, FAKD4, TET5B, C102A, RM24, SPSB4, ZUP1, CC74A, TTC28, R51A1, DACT3, SH3K1, PF21A, ELMO3, PINX1, CC049, S1PBP, ZN775, DOC10, ATG2B, ZBTB9, ROP1L, COAC, CHM4C, CC124, OPTN, S7A6O, GASP2, RMD1, OTUB2, ATG4C, DRC10, MTBP, RRFM, MTEF3, ELP4, HOOK2, MTMR8, ZN837, RL39L, MITOK, SGF29, RBM33, DTBP1, ZN503, ELMD3, THOC1, HMCES, IMP4, KLD7B, SCMH1, TOE1, MSD3, ZCCHL, TONSL, NTAQ1, PDLI5, PRR11, FMC1, C2AIL, INT4, SYNM, REXO5, GMPPA, GMCL1, ZN496, NGLY1, RBM41, TPD55, ESIP1, MAP6, ZN594, ZN469, ZN462, FEM1C, PGBD1, ZN521, TOPK, PRAC1, COX42, KCNS1, Z512B, ZFR, F167A, P12L2, CD036, NSD1, EP400, IFT74, SGCZ, CX058, CEP19, CH048, CL037, MRFL, Z354B, PRIPO, RMD2, CJ090, IFAS1, TEKT5, TEX55, FEAS2, CCDC7, CFA53, ZN512, CQ10A, NSE2, CE034, RIPR3, TEAN2, ZSWM3, YTDC1, ZNF48, F161B, F218A, TTC14, CK037, ZN578, PWP2A, DOCK7, ZN641, ZN582, ZFP3, LRRC7, BIRC8, INP4A, TSSK2, RBM14, ADCYA, IPP2L, ZN317, PNMA5, K1908, FMNL2, PUS7, F111A, PLIN4, SMG1, ALKB3, KI20B, RHG07, ATAD5, TEFM, RAB3I, GCNA, PRAM, MAGI1, RET7, PANX2, MED15, ERBIN, TRIB1, HMCN1, CRML, PRR25, LYSM1, CCNL2, SMC6, ZN607, ZN587, IWS1, SEBP2, RSF1, RUFY1, IMP2L, MINT, SETB2, ACOX2, AGAP2, EYA3, DNJC2, MPP9, M3K14, S10AD, SCAFB, ELF4, KLF6, PHB2, CHP1, KIF2C, LYST, ATX2, SMAD5, BARD1, NPAS1, EPAS1, TS101, CPNE1, SMO, EBP2, PKP2, AKAP9, ARP5L, SIN1, RNZ2, CMS1, SENP7, SLF1, COE4, ST4A1, ZSWM1, COR1B, LSMD1, SRSF8, PYGO2, FSP1, GPTC1, LLPH, SIKE1, TRI56, ZPBP1, BTBDA, TACO1, PIMRE, S2533, HAUS8, ALKB7, DIDO1, MTA3, DCNL5, RAMAC, FAP24, LRRC1, MED18, RCAF1, SCMC3, THUM3, CP250, KTNB1, PHF20, RUSC1, RIOK2, TIM21, KIFC1, HIRP3, TRAIP, FUND2, CYREN, CDCA7, MND1, CAR10, NADAP, GATA5, SYCP2, FANCJ, SRBS1, CARD6, ZN471, OSB10, RFIP5, SPZ1, CAR14, CAR11, T121B, TGT, TDRD1, TEX15, RNF17, STK31, UBP26, OSBL1, FACD2, AN30A, MAK16, SCAPE, DGC6L, RTF2, PECR, LRRC3, RNF26, SCOT2, RM01, ACE2, MSTRO, HYCCI, YTHD1, LRRC2, NEUL, PBX4, BCDO2, CEP41, SETD2, TBD2A, LDH6B, PANK2, NSD3, NUF2, PUS3, BARH1, OSBL7, UACA, REN3B, NIBA1, UBXN6, TRI15, TRIM4, F117A, SPEF2, LRCC1, ZFHX2, CFA74, AMRA1, CE295, ZY11B, TANC1, XPO4, GRIP2, ASXL3, CEP44, ZN407, SRCN1, CCSE1, WDR33, TGIF2, ROGDI, REXO4, NXF2, MFF, DRC3, CLPB, LSG1, NUAK2, NAT10, IQCN, ILKAP, SP130, UBP44, BRD8, RGAP1, PUS7L, ZCPW1, GZF1, BC11A, I2BPL, ISCU, RSPH9, VPS11, AL8A1, TARA, EPC1, CI037, PDCL3, ADNP, TNMD, RBP17, IPYR2, MIXL1, HIPK2, ZN106, E41LB, UBQL3, YI012, MOD5, GHITM, BOLA2, BORG4, UN45A, DSN1, CA198, RBSK, FN3K, WNK1, PLK3, E41L1, EMRE, PRD12, ZN644, VIAAT, THAP9, BICC1, CCD86, MYH16, CIAO3, ACSS3, BCAS3, ZN552, ASB8, SH24A, SMYD3, MB12B, ZN665, CCSE2, ZN430, NOL11, PAAT, MINY3, ECT2, F204A, CF208, ANKZ1, GHC1, PPIP2, MARH7, CNO10, SPE39, ANRA2, UNKL, RPF1, RPA2, SYCM, NMNA1, MLXIP, RENT2, BRF2, CLSPN, BCDO1, PRD16, PKHA1, AS3MT, TENS1, NMRL1, SPC25, TAF9B, Z286A, TPC, MRM3, GPBL1, CENPJ, ZBT20, HES4, NCOA5, TANC2, ZN532, SYTL2, MAGE1, K1586, ZSWM6, ZDBF2, CHD8, GPAT1, FBSL, ZN304, NDF4, HMX1, S40A1, GCM1, VTA1, EXOS4, UBN1, MKKS, MED4, SCRT2, CK016, PLCB1, A1CF, DDX4, DMRT3, INCE, PRDM9, BIN3, ENTP7, BIRC6, PDLI7, ACSA, DYRK4, ANM8, ASH1L, KLHL1, TSH2, SMYD2, SNRK, TBG2, STRN4, ZN277, LATS2, C42S1, PNO1, TOPRS, MBIP1, RAD18, HOME2, SALL1, ZN275, BRWD1, KLC4, AT8A2, DEPP1, CTSRZ, ZF64B, ECHD1, RBM12, ANKE1, MDN1, UFSP2, MITOS, OTULL, TYDP1, POTE1, DCA13, NUD15, RN19A, TYW1, EXOC1, UQCC1, MED17, TBC13, DJC11, INT7, FANCI, INT13, DZAN1, FAIM1, INT10, KTU, TBCC1, RPC2, RBM28, RBM22, BSDC1, WDR70, SLTM, SMOX, PIHD1, PARI, RMND1, BABA1, THG1, HPF1, IRAK4, TXN4B, NDUBB, MARH5, SYBU, MTMRA, TEX10, CNTLN, TRM1, CARF, NSE4A, DDX43, DPP3, ETAA1, ABI2, DYH9, HXC10, DACT1, FA53C, BCLF1, TAB2, CDK12, SMAL1, SACS, MAT2B, MYOF, ITSN2, ARHGC, CNOT2, VSX1, CWC15, RAI14, H2AW, RM27, VPS54, CAMP3, PHRF1, DAPLE, ZFAT, RELCH, DIP2B, JCAD, SLAI2, BAHC1, PAK5, CHD7, F135A, RRBP1, MAP10, CE126, CPSF2, KLHL9, SYLC, C2D2A, DISP3, TBC14, RBM27, KANL3, HECW2, STAR9, RERE, ANKY1, IMPCT, HNF6, HSFX1, RBX2, MYOTI, PRGC1, ARP21, GULP1, SAE2, POLK, DBF4A, NXF1, ZMYM2, REV1, ZNF70, S14L4, DAXX, ADDG, HYPDH, FXL17, CCD39, ABCF2, S23A2, AAKG2, KDM5B, SYWM, TCF20, SUN2, NDOR1, AFF4, SEPT9, UBQL2, IP6K2, NUFP1, SMPX, S30BP, MED13, PFD2, NRBP, FEZ2, EVL, CTNA3, XPO7, BAZ2B, BAZ2A, BAZ1B, HERC5, SIX4, ZMYM5, HACL1, STAG3, HOOK1, NGAP, ZN391, SALL4, S2513, FBXL7, ZN112, DBNL, ZN229, ZN180, HSPB8, KS6A6, DBR1, FBXL4, FBXL2, GMEB2, PO2F3, GPTC8, C8AP2, FBX4, FBXW2, IKZF3, TRHDE, HDAC9, ACINU, AGO2, NUP50, ZHX1, DSE, SARDH, CFA45, AGO1, ZN236, ZN214, MKLN1, NRX1A, PADI1, ZN777, INTU, ZN608, WWC3, F184B, INO80, KDIS, MRTFB, ZBT21, NEB1, AT7L1, K1210, PKHG1, SHRM4, PKHH1, YETS2, CNOT6, HECD1, ZMYD8, HSF4, PADI4, APC10, MYO6, SPAT2, KMT2B, CAN11, PHTF1, MAGD2, CSN3, TTF2, BSN, MACF1, SCAF8, TRI33, PHF8, LIMC1, TRI35, TNR6B, PLCL2, EXOC7, SMAG1, CE164, CBPC1, SATB2, UN13A, DICER, SRRM2, PA2G4, CD11A, CTND2, BAIP2, SCML2, RUVB2, CDYL, HIG1A, AKT3, PRLD1, PLAP, T53G5, ADIP, ICE1, EFR3B, PKHA6, MAST1, AMOL2, ZBTB1, KDM2A, FRM4B, FAN1, KLH20, CRYL1, AXIN2, GUAD, MAN1, TR150, MED16, ZBT32, MTO1, SYYM, ZBT12, CAB39, LC7L2, RBMX2, HDGR3, BOLA1, STA13, T22D4, RL36, C2CD2, HBS1L, ZN175, DMXL1, TRRAP, MTCL1, ZN451, WDR7, C170B, RIPR2, TLN2, DTNA, CRBG1, LAS1L, AFG32, PRC2C, PPME1, TRI17, CEP83, PAXB1, SP16H, MAGD1, KLF2, SNX5, LRRF2, FHOD1, IRAK3, NCOR2, GMEB1, BIG2, MD1L1, RM42, ATP23, SNCAP, CABIN, OAS3, NEMO, SQOR, NCOA3, NUMBL, Z780B, CCD61, SCIN, PCLO, SETBP, MORC2, NS1BP
Species: Homo sapiens
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Zhang W, Liu T, Dong H, Bai H, Tian F, Shi Z, Chen M, Wang J, Qin W, Qian X. Synthesis of a Highly Azide-Reactive and Thermosensitive Biofunctional Reagent for Efficient Enrichment and Large-Scale Identification of O-GlcNAc Proteins by Mass Spectrometry. Analytical chemistry 2017 89(11) 28510447
Abstract:
O-linked β-N-acetylglucosamine (O-GlcNAc) is a ubiquitous post-translational modification of proteins in eukaryotic cells. Despite their low abundance, O-GlcNAc-modified proteins play many important roles in regulating gene expression, signal transduction, and cell cycle. Aberrant O-GlcNAc proteins are correlated with many major human diseases, such as Alzheimer's disease, diabetes, and cancer. Because of the extremely low stoichiometry of O-GlcNAc proteins, enrichment is required before mass spectrometry analysis for large-scale identification and in-depth understanding of their cellular function. In this work, we designed and synthesized a novel thermosensitive immobilized triarylphosphine reagent as a convenient tool for efficient enrichment of azide-labeled O-GlcNAc proteins from complex biological samples. Immobilization of triarylphosphine on highly water-soluble thermosensitive polymer largely increases its solubility and reactivity in aqueous solution. As a result, facilitated coupling is achieved between triarylphosphine and azide-labeled O-GlcNAc proteins via Staudinger ligation, due to the increased triarylphosphine concentration, reduced interfacial mass transfer resistance, and steric hindrance in homogeneous reaction. Furthermore, solubility of the polymer from complete dissolution to full precipitation can be easily controlled by simply adjusting the environmental temperature. Therefore, facile sample recovery can be achieved by increasing the temperature to precipitate the polymer-O-GlcNAc protein conjugates from solution. This novel immobilized triarylphosphine reagent enables efficient enrichment and sensitive detection of more than 1700 potential O-GlcNAc proteins from HeLa cell using mass spectrometry, demonstrating its potential as a general strategy for low-abundance target enrichment.
O-GlcNAc proteins:
A0A024R5Q9, A0A0B4J1V8, A0A0B4J203, GAL3B, RBM47, UBA6, ESYT2, SHOT1, NDUF8, VWA8, GTPBA, A5Y5A3, CNOT1, PGP, TBAL3, SMHD1, LR14B, NCF1B, A8K005, B4DLC0, B4DLN1, B4DQP1, B4E259, EIFCL, B7Z2B5, B7Z532, B7Z5W1, DSA2D, D7RF68, E9PL57, E9PLN8, I1VE18, L0R5A1, S35U4, ADAS, KIF2A, PDLI1, AIP, SMAP, NDUS8, PSD12, PSMD9, SPT5H, DFFA, HIP1, EIF3F, IPO5, SAP18, IF2B3, DNM1L, NDUA4, PSDE, BIN1, NOP56, DDX3X, IMA3, TRI38, SCD, DHSD, TXND9, ACPM, UBFD1, AP3D1, DVL2, CHD1, TOR1A, PTGES, ACOT8, NHRF1, TPP1, RPC1, PSA7, MGST3, HAT1, QCR8, HGS, S27A2, HNRDL, BTAF1, SR140, PUR4, NPC1, DEGS1, SCAM2, ARPC2, ARPC3, BET1, RPAC1, PGRC2, NDUA1, RER1, OGT1, PMM2, HMGB3, EIF3H, ARPC5, DHX15, CYB5B, PRP4, SERA, NDUS4, PAPS1, ZW10, SNUT1, RIPK2, PRPF3, PPIH, E41L2, XPOT, DNPH1, PSCA, TSN6, ZN207, NDUB5, BUB1, BUD23, GATC, HTSF1, SGTA, SYNC, PM34, CPSF5, SCO2, ORC5, TIM8A, DHX16, SMCA5, MAST3, OPA1, TBCD4, OGA, HNRPQ, DIAP1, MOT2, IMA7, CTND1, DPM1, Z354A, RT14, PQBP1, TI17B, DKC1, IF2P, EDF1, MCE1, ABCB7, WDR1, BRE1B, ZC11A, CLU, ANR17, COQ9, NDUS7, NIPS2, VPS4B, CISY, PR40A, NDK6, VP26A, MPPB, PSIP1, ECI2, BAF, SF3B1, CSDE1, PRKRA, NPM3, ERAL1, TIPRL, KS6A4, NU155, XRP2, WDHD1, CRTAP, S2512, RNH2A, EIF3G, AP1G2, IDHC, CCNK, SPF27, FLOT1, GLRX3, RL1D1, CLPX, CIAO1, SRP72, LTN1, UFL1, UBXN7, PRP6, PCF11, GLSK, SC31A, RPP14, YIF1A, AGFG2, NDUB6, UBE4B, ELP1, NDUB8, LC7L3, KIF4A, MPZL1, 6PGL, PAPS2, TRI16, ARI2, PSMG1, MPC2, ASML, RPP29, HS74L, AP2A1, TTC4, TM50A, BAG2, EMAL2, BPNT1, NDUBA, ACL6A, COX1, COX2, PNPH, AATM, EGFR, ADA, ATP6, RASN, LDLR, HLAB, LMNA, ALBU, NU1M, NU3M, NU4M, KITH, K2C1, G3P, HLAA, TYSY, RPN2, HMGN1, ISG15, LA, K1C18, DCUP, CDK1, NPM, TPM3, HEXA, HYEP, H10, SAP, SYEP, HNRPC, YES, SP1, DAF, PFKAM, HEM3, CY1, RU17, ITA5, RS17, RSSA, RM03, SRP19, RU1C, HMOX1, RU2A, PARP1, LKHA4, ALDOC, F86B2, GSTT2, ST1A3, HS71B, RPAC2, ECE2, EFMT4, EFCE2, MYBA, HLAC, ARAF, H14, ODP2, MGST1, ESTD, GTR3, UMPS, ODB2, ACADM, TOP1, TOP2A, G6PD, PYC, C1TC, ADHX, PRPS2, PABP1, ADT1, TPR, KCRB, RINI, K2C5, ACPH, GYS1, ENOB, CD59, MTDC, MIF, CX7A2, CCNB1, CX6B1, PO2F1, SYDC, PLAK, QCR7, ERF3A, EZRI, UCHL3, MCP, PHKG2, RS2, RFA2, CBR1, BGAL, EPCAM, NCPR, AT2A2, UBF1, NDUB7, KAPCA, CAN2, PYRG1, DDX5, LEG3, TCPA, PTN1, RL7, NELFE, PGAM1, RCC1, XRCC1, RPAB1, NDUV2, SPEE, IF2B, BTF3, H2A1D, COX5A, LMNB1, IMDH1, FLNA, ACOHC, ODBB, MUTA, OSBP1, PIMT, FBRL, PUR2, HEMH, TCEA1, AT2B4, CPT2, KTHY, RIR1, EF1B, AT5F1, THIL, CDK2, APC, MCM3, THTM, RS12, TYY1, ITA3, DDX6, DNMT1, U2AF2, HMGB2, SYVC, EF1G, AOFB, RL10, RFA1, APEX1, MAP4, CALX, PSA5, NDUS1, RXRB, AMPL, T2EA, T2EB, IMPA1, 3MG, CO4A5, SPB3, ATPD, PDIA3, 2AAB, CDC27, NMT1, PURA2, AMRP, PUR8, CLIP1, GSTT1, CTR1, AL1B1, RPB2, METK2, RIR2, HNRH3, HNRH1, STIP1, L1CAM, P5CR1, TF2H1, ACSL1, CSTF2, MCM4, MCM5, MCM7, RFC4, RFC2, RL22, T2FA, GDE, SOAT1, BASI, NU214, DEK, K22E, PRS7, HEM6, RL4, LONM, SRP14, NUP62, TALDO, RBMX, COIL, RS19, FEN1, CAP2, TCPZ, NNMT, PSB10, RL13A, PEX19, MDHM, RFC5, RFC3, BUD31, GARS, SYIC, EIF1, LAP2A, LAP2B, MTREX, AK1C3, LPPRC, THIM, MATR3, GPDM, SSRA, SSRB, RANG, PRS6B, EFTS, VDAC2, UBP5, RECQ1, ATRX, IF2M, MP2K3, BRCC3, RL27A, RS10, GNPI1, CAPZB, IF1AX, SYQ, RL29, MAOX, PTSS1, IDHP, PIPNB, DPOD2, TCPG, RM19, INPP, SRP09, SYCC, PSB2, MCM2, ACADV, TMEDA, RBM25, NU153, RBP2, NDUV1, GSK3B, 5NTC, SPS1, GUAA, DNLI3, GDIB, CPT1A, F10A1, DYN2, MAP2, CDK7, CDK9, LRBA, RL14, PAPOA, FXR1, FXR2, RAB7A, RB27A, RT29, SMCA4, SSRD, TPMT, HCFC1, SSDH, DHB4, PSMD7, STA5B, UBP11, DYLT3, CCNH, ROA3, HNRPM, IMA1, NCBP2, MP2K6, KIF11, HXK2, BIEA, PLK1, NUBP1, MAP11, SUCA, MVD1, PGTB2, CATC, CCHL, IST1, TCP4, PMS2, SYYC, UBP14, RD23A, P5CS, IF5, PSMD4, BI1, MFAP1, AFAD, NP1L1, CASP9, ADK, DSRAD, SEC13, HNRH2, SCOT1, EIF3B, ATP5E, IF6, CF298, TMM33, CORO7, SELB, MTPN, YBEY, ARPC4, CD81, SC61B, ROMO1, MYL6, ACTB, IF4A1, PRPS1, PSA6, CDC42, DEST, GMFB, RAB8A, SPCS3, SRP54, RAB5B, UBC12, UBE2K, RAB14, TM258, CSN2, RAP1B, RS3A, VA0D1, NAA20, S61A1, B2MG, COPZ1, UFM1, AP1S1, HNRPK, TIM10, PRS4, RS15A, RS23, RUXE, SMD3, PRS10, ERF1, RS6, RAN, RL23, RS15, RS24, RS25, RS26, RBX1, RL39, RL31, RL10A, RL32, PPIA, TRA2B, AP2B1, DYL1, DYLT1, RL38, SKP1, ACTG, UBC9, CSK2B, UB2L3, EF1A1, CSK21, SERB, IF4G2, RPP38, GTF2I, RAE1L, GSTO1, PRKDC, IN35, RT25, RT35, RT05, RT11, RT15, RT06, RT09, LACTB, RL36A, ARF5, ERH, H33, FOXK1, PRR5, RBM10, TFAM, PIPNA, TF2B, CDK16, NFKB2, FKBP3, HNRPU, U2AF1, SET, GALK2, FABP5, CAP1, HMCS1, IFM3, RL18A, NUCB1, RL6, M2OM, LMNB2, TAP1, TAP2, CEBPZ, TF65, UBXN1, IF4G1, ATP7A, CSTF1, FAK1, SRS11, EF1A2, PUR1, PSME1, GABPA, FMR1, RL18, C1QBP, KHDR1, KLC1, SRSF1, QOR, LG3BP, PPID, SSRP1, CAMP2, NSUN2, RBBP4, NCBP1, HSP7E, BST2, MPPA, WASC5, TBL3, SNF5, STX4, GRSF1, NFIA, SF3A3, TP53B, ILF2, ILF3, PTPRJ, TRAP1, TRAF2, MYO1E, PP1R8, BNIP2, CSTF3, STRN3, RM28, ACACA, CSN1, CAF1B, TADBP, ROA0, AIMP2, PAK2, CBX3, STK3, STX5, SRSF5, SRSF6, TIF1B, PABP4, EIF3I, 2A5G, UB2V1, RM49, DC1I2, ILK, SNTB2, PPIG, TCOF, SF3B2, HAP28, ROCK1, PICAL, SQSTM, PRP4K, HDAC1, DCTN2, SNW1, STIM1, PWP1, MTMR2, CUL2, CUL4A, FCL, RAB31, RAB32, NOG2, TBB2A, BYST, PEBB, HNRPD, IL18, VEZF1, TRI29, TTL12, DPOA2, ICT1, DCTN1, ELOA1, TRI25, FASTK, PDE3A, RBM39, HLTF, MCM6, ITPR1, TRIPC, PUM1, EPN4, SMC1A, RRP1B, PSF1, UBP10, GANAB, LBR, CHD4, NOLC1, NUMA1, PSME4, GAPD1, CND2, SPCS2, EMC2, FL2D, PSMD6, ABRX2, SART3, CND1, EXOS7, U5S1, SYLM, WDR43, ACOX1, EBP, PCM1, NOMO1, PON2, TEBP, NONO, RAB35, RNPS1, PCBP2, ELOC, UBE3C, DHC24, SF3B3, RSU1, SF3B4, SF3A1, SKI2, MARE2, NHRF2, TSN, SF01, CIP4, TRIPB, PCH2, ELAV1, SMAD2, TBCE, VAMP3, ZYX, SEPT7, CCDC6, UAP1, PSMD5, MK14, RM23, DPYL2, SYPL1, RBBP7, IF16, KYNU, CAH9, NDUA9, PCKGM, HCDH, UGPA, MIC60, HNRL2, INF2, PDS5A, TSR1, ALG11, QRIC1, SMU1, LRRF1, RPA43, LSM12, ACSF3, PPCEL, TB10B, MIX23, RHG29, PDCD4, Q53FH6, DHB12, SNUT2, LACB2, EIPR1, H90B4, TM41B, HERC4, PP6R3, PREP, PSMG4, RRP12, TOIP1, SYAM, PCID2, S27A3, SAMD9, CYTSB, TDIF2, TTC38, EXOS6, NU188, CE170, SNPC4, CHCH9, DDX59, GPTC4, HECD3, SKT, RM02, UBAP2, LCE1C, ACBD5, EEIG2, RBM26, DCAF8, ATPF1, DDI2, NT5D1, LYRM7, EMC10, RIF1, OBSCN, CE350, AXA81, PR38B, BRE1A, ARHGG, LYPL1, ECM29, MIC13, MAP1S, UTP25, TENS3, INT3, C19L1, CPIN1, SMYD5, PTRD1, CNDH2, MRM1, P4R3A, ACD10, DE10B, SCMC1, TM214, HIBCH, TTI2, DHX57, CDC73, RM14, L2GL2, MET2B, PRP8, TTC27, SKI3, RICTR, LCLT1, WDR82, HACD2, GGYF2, KAT3, UBR3, LARP4, SPT6H, SND1, COX15, DDX46, TM10C, 5MP2, EIF3M, MEPCE, CYFP1, ENOF1, FAKD5, MOB1B, KDM3B, HS2ST, K2C74, TRM1L, ZCCHV, NUP54, MAVS, DHX29, COMD6, HDDC2, LIMS2, I2BP2, PATL1, SETD3, PABP2, MTA70, ZN598, AACS, LUZP1, GP180, CAND1, CMTD1, PRSR2, CARM1, COMD2, DDX42, SPAS2, CONA1, NDUAB, DAAF5, STX12, DLP1, P66A, HORN, RB6I2, FABD, CEP97, CTL2, PHF6, UBR1, CHERP, ANKH1, DJC10, NELFD, MIRO1, RB12B, RAVR1, SPB1, SRRM1, CA174, MICU2, TRM2A, PELP1, ABI1, CCAR2, NDUF2, NUP93, LRC47, GPD1L, TOM5, OGFD1, TTC9C, JAGN1, CPSF7, PAF1, ZN433, F241A, ENAH, CL029, NHLC2, SUMF2, UBAC2, RDH13, UXS1, FA98A, NNRE, LS14A, PAPD5, CNNM3, MCU, FBX22, FAD1, NUP35, Q8NFH9, ABHDB, KNL1, OR1M1, ATLA2, MSPD2, DDX55, NCOA7, THOC2, WDR36, G45IP, CX038, FBX30, S35B2, PUM2, KLDC4, UBA3, KISHA, TBC15, RM30, PNPT1, SSH3, GEMI5, IPO4, ABHD5, ZC3HF, TF3C2, TM263, PTPM1, NU133, CHAC2, THEM6, LEO1, CPLX3, NUDC2, TFB1M, SCFD1, HNRLL, CD003, SEN15, SPRY4, TRUB1, LMO7, ARAP3, PRP31, PALLD, CTBL1, DDB2, DDX1, DHB8, PSMF1, RTF1, RT27, AP3S1, LAR4B, GCN1, PRP16, NU205, TFG, RBP56, DDX17, RAD50, CELF1, OSTF1, ARHG1, UFD1, RENT1, SMRC1, FUBP2, ARHG2, UBP13, USP9X, SCAM4, OSBP2, F162A, RM24, SYAP1, EXOC4, FERM2, PBIP1, RPE, EXOS8, OTUL, CHCH1, PPWD1, COA7, TAM41, F136A, P5CR2, DCPS, FAF2, FXRD1, AP2M1, GCP3, F241B, NMD3, RMD1, MSI2H, SNR40, RM38, RRFM, SIR1, YIPF6, KBP, GNA1, RT24, MOCOS, DAZP1, SAAL1, SIM12, DNJA3, TMA16, PTCD3, OTUB1, TRM61, HMCES, DUS3L, OTUD5, VMP1, DCNL1, SMRD1, TOE1, DDX27, MTNB, ZC21A, PGAM5, FUBP3, SPF45, SUCB2, HPDL, ATPMK, BT3L4, CLP1L, SCYL1, SNX27, YTDC1, ZN830, NSUN5, RBM14, UHRF2, PUS7, TRNT1, TEFM, EFGM, NUDC1, PRPK, PIGS, WRIP1, RANB9, NEB2, IWS1, SIN3A, OSBL9, INT14, ZSC10, RUFY1, MMS19, UHRF1, NIBA2, YMEL1, MYCBP, TBCB, PSB7, CNN2, CDC5L, PSMD1, PFD5, MPH6, TSNAX, TTC1, CSN8, KIF2C, MGLL, HCD2, NP1L4, ACON, TCPH, ANM1, VRK1, CND3, ARP5L, DDX50, RNZ2, GRWD1, MACD1, CMS1, MEP50, RT63, TBA1C, MBB1A, FERM1, CG050, PDD2L, MIC25, UQCC2, UTP23, LXN, NTPCR, TACO1, GCP2, SEN34, ALG1, PSMG3, CSN4, DIDO1, RBM42, MCMBP, AASD1, DCNL5, AN32E, P4K2A, MMTA2, TBB6, PAXX, HNRL1, MTNA, WDR18, THUM3, NTM1A, ASHWN, TM109, GNL3, NUP85, ELOV1, IFT27, SYTM, THIC, FUND2, SF3B5, SFXN3, CARD6, OSB10, B2L13, SRRT, HDHD5, HDAC8, RTF2, EIF2A, PDIP3, RM13, RM04, RM01, MK67I, YTHD1, RT26, NEUL, ABCA2, RM37, UACA, WDR11, CRNL1, TBL1R, UBL5, API5, FTO, UBE2O, XPO4, S39A8, WDR12, YIPF3, DERL2, SKI8, SLIRP, EGLN1, UBA5, MKRN2, T126A, PAIP1, CLPB, LSG1, NAT10, ILKAP, XRN2, NSRP1, CSTFT, 5NT3A, GBRL1, DDX47, RM18, SNAB, ATG5, GAN, DPH5, DHX36, IPYR2, SPNS1, RM46, PININ, GPT, GHITM, NELFA, OSGL1, HEAT1, TFB2M, YTDC2, RPAP3, WDR26, CH033, UBE2Z, ANKZ1, ZWILC, MED20, ARMT1, L2HDH, ELP3, RPA2, KT3K, SYCM, PPCS, NJMU, XPO5, GRPE1, RHOF, POPD2, EMAL4, GLOD4, MCCB, MOV10, SYF1, TM9S3, WDR6, TRXR2, SYSM, RT30, M1IP1, UBE2T, NOP10, OSGEP, MED4, RM40, RTN4, RPR1B, RRAGD, PFD4, EXOS3, ANLN, XPP1, BIRC6, ACSA, DBLOH, DDX21, SAR1A, DPOE4, SIAS, SHLB2, EI2BG, MBNL1, PYRG2, DPOE3, CHRC1, COXM2, ABC3C, PNO1, RM17, HELLS, SYFB, SYIM, ATG3, SMC4, OLA1, CUTC, ECHD1, RBM12, MDN1, DECR2, ABHDA, LIN7C, TXLNG, SPS2L, ABCF3, DD19A, UQCC1, EXD2, DJC11, FANCI, ATD3A, ARL8B, ANM7, FAIM1, RT18A, ARMC1, RPC5, SDA1, RBM28, RBM22, DMAC2, WDR70, PK1IP, RM22, CZIB, BABA1, NDUBB, RM16, NHP2, OCAD1, ADPRS, LYAR, MIC19, THUM1, TRM1, PP4R2, DPP3, BCLF1, FKB11, TMOD3, ELOV5, GTSE1, TECR, ERAP1, ARP10, CISD1, F120A, IF2B1, COQ3, HPBP1, MAT2B, CNOT2, OGFR, CNIH4, RM15, THYN1, KCMF1, TM14C, HM20B, RCC2, RELCH, BCCIP, STK26, FPRP, IBTK, RRBP1, SYLC, SUCB1, DPM3, ATX10, TFP11, SAE1, COMD3, MTRR, ASH2L, DHCR7, EIF3K, SAE2, WNT16, CSN7A, QCR9, ZO2, LRWD1, ABCF2, SYWM, SEC63, SRP68, CHRD1, BAP29, S30BP, PFD2, GPN3, PUF60, NRBP, ENOPH, NDUAC, EI2BD, VATH, XPO7, VPS51, S2513, DCTN4, FBX2, CCNL1, DBR1, FEM1B, DJC12, MRT4, CPSF3, NUDT5, RCOR1, TF3C4, PACN3, ACINU, AGO2, PSME2, PALD, COR1C, AKP8L, ALK, DD19B, PRP19, UBQL1, SNX12, CHIP, PACN2, MAGD2, SNX6, SSRG, FAF1, PPIE, MINP1, SCAF8, TRI33, PHF8, LIMC1, UBP24, SMC3, SCML2, PIN4, PSF2, EIF3L, PLAP, RUVB1, BCS1, SYFA, CNPY2, PKHA6, RRP44, RT07, PDIP2, WBP11, NOP58, SGT1, ACOT9, AAR2, MEMO1, TMX2, LC7L2, DHRS7, RT02, SBDS, TMED5, EXOS1, SF3B6, RM11, RRP15, NOP16, TPRKB, PPIL1, CIA2B, RT16, RT23, PTH2, RTCB, FBX7, NOC2L, RL36, SAMH1, HBS1L, DCAF1, UBP15, TBL2, TELO2, LAS1L, AFG32, ARI1, SAM50, PRC2C, PPME1, AP4S1, YTHD2, CTDP1, SP16H, UTP18, TNPO3, GMPPB, RBM8A, SNX8, FHOD1, SERC, NCOR2, ORNT1, ALG5, RT18B, CLIC4, NFS1, SPCS1, MD1L1, STK24, 5MP1, COMDA, DC1L1, TX264, S4A7, NDUB9, MORC2, S23IP
Species: Homo sapiens
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