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Ramirez DH, Aonbangkhen C, Wu HY, Naftaly JA, Tang S, O'Meara TR, Woo CM. Engineering a Proximity-Directed O-GlcNAc Transferase for Selective Protein O-GlcNAcylation in Cells. ACS chemical biology 2020 15(4) 32119511
Abstract:
O-Linked β-N-acetylglucosamine (O-GlcNAc) is a monosaccharide that plays an essential role in cellular signaling throughout the nucleocytoplasmic proteome of eukaryotic cells. Strategies for selectively increasing O-GlcNAc levels on a target protein in cells would accelerate studies of this essential modification. Here, we report a generalizable strategy for introducing O-GlcNAc into selected target proteins in cells using a nanobody as a proximity-directing agent fused to O-GlcNAc transferase (OGT). Fusion of a nanobody that recognizes GFP (nGFP) or a nanobody that recognizes the four-amino acid sequence EPEA (nEPEA) to OGT yielded nanobody-OGT constructs that selectively delivered O-GlcNAc to a series of tagged target proteins (e.g., JunB, cJun, and Nup62). Truncation of the tetratricopeptide repeat domain as in OGT(4) increased selectivity for the target protein through the nanobody by reducing global elevation of O-GlcNAc levels in the cell. Quantitative chemical proteomics confirmed the increase in O-GlcNAc to the target protein by nanobody-OGT(4). Glycoproteomics revealed that nanobody-OGT(4) or full-length OGT produced a similar glycosite profile on the target protein JunB and Nup62. Finally, we demonstrate the ability to selectively target endogenous α-synuclein for O-GlcNAcylation in HEK293T cells. These first proximity-directed OGT constructs provide a flexible strategy for targeting additional proteins and a template for further engineering of OGT and the O-GlcNAc proteome in the future. The use of a nanobody to redirect OGT substrate selection for glycosylation of desired proteins in cells may further constitute a generalizable strategy for controlling a broader array of post-translational modifications in cells.
O-GlcNAc proteins:
SBNO1, CNOT1, P121C, DX39A, GTPB1, AP3B1, PGRC1, TAF4, EIF3F, IPO5, IF2B3, NOP56, DDX3X, ARI1A, IRS4, ANM5, TCRG1, PSA7, HGS, MYPT1, HNRDL, XPO1, SET1A, PUR4, NPC1, TIF1A, NKRF, OGT1, PPM1G, EIF3D, EIF3H, DHX15, SERA, HNRPR, IF4G3, E41L2, ZN207, BUB3, ACTN4, HTSF1, AP1G1, SYNC, AKAP8, CALU, SMCA5, JIP4, OGA, HNRPQ, DIAP1, TSN3, SNX2, DKC1, CLAP2, CPNE3, PHF2, ANR17, H2AY, FLNB, NCOR1, CISY, PR40A, SF3B1, CSDE1, U520, EIF3G, PRAF3, SRP72, MTA2, TOX4, SC24D, SC31A, SCAF4, ZRAB2, LC7L3, VAPB, IPO7, SC24B, ACSL3, AP2A1, AIFM1, LDHA, COX2, HPRT, AATM, PGK1, LMNA, TFR1, ALDOA, OAT, G3P, RPN1, RPN2, AT1A1, ADT2, PCCA, IF2A, RLA0, ITB1, ATPB, ENOA, PYGL, G6PI, NPM, LDHB, PDIA1, H10, TBB5, HEXB, PROF1, SYEP, HS90A, HNRPC, 4F2, HS90B, ASNS, ODPA, RU17, RSSA, SNRPA, GSTP1, HMGB1, DLDH, ROA1, PARP1, LKHA4, HS71B, H14, ODP2, THIO, CH60, BIP, HSP7C, EPB41, ODPB, LAMP1, ACADM, TOP1, TOP2A, PYC, C1TC, MPRI, PRPS2, PABP1, PCNA, HARS1, IMDH2, TPR, KCRB, XRCC6, XRCC5, EF2, PDIA4, PLST, GLU2B, KPYM, ENPL, PO2F1, HNRPL, SYDC, PLAK, ALDR, EZRI, GNS, RS2, CREB1, H12, AT2A2, JUNB, PYRG1, DDX5, PRS6A, TCPA, RL35A, RL7, VINC, SON, RCC1, NUCL, HXK1, E2AK2, SPEE, IF2B, ANXA7, LMNB1, FLNA, VDAC1, FBRL, PUR2, PUR6, UBA1, NDKB, ROA2, RFX1, TCEA1, SFPQ, PPIB, RS3, NFYA, SAHH, COF1, IF4B, EF1B, MCM3, BRD2, ATPA, PSA1, PSA3, PSA4, PAX6, U2AF2, RL13, PTBP1, SYTC, SYVC, EF1G, RFA1, APEX1, PYR1, CALR, MAP4, CALX, PSB5, TKT, PRDX6, PRDX5, PRDX3, RL12, PEBP1, PDIA3, 2AAA, CDC27, AMRP, SDHA, QCR1, PUR9, HNRH1, STIP1, PRDX2, RL9, CSTF2, MCM4, MCM5, MCM7, GLYM, HSP74, PHB, MYH9, COPB2, ADDA, BASI, FUS, NU214, DEK, MP2K2, ATPG, RL4, SRP14, NUP62, RBMX, GRP75, IF4A3, RS19, RL3, TXLNA, TCPZ, MDHC, MDHM, ECHA, IF2G, GARS, SYIC, LAP2A, LAP2B, MTREX, RS27, LPPRC, MATR3, RANG, VDAC2, UBP5, KI67, RAGP1, NOP2, CRKL, BAG6, RL27A, RL5, RL21, RL28, RS9, STT3A, COPD, PRC2A, TCPE, AL9A1, RL34, NASP, FAS, TCPG, EFTU, SYAC, SYSC, PSB3, MCM2, YLPM1, TMEDA, RBM25, NU153, RBP2, GSK3A, TAF6, GUAA, MRE11, GDIB, EMD, F10A1, LRBA, RL14, TCPQ, TCPD, ANX11, PAPOA, RAB7A, SMCA4, HCFC1, DHB4, ROA3, 6PGD, HNRPM, IMA1, AGFG1, HNRPF, MSH6, RBM5, NUP98, ACLY, COPB, COPA, MOT1, SC24C, SYRC, SYYC, AT1B3, RD23B, P5CS, IF5, XPO2, TERA, AFAD, DSRAD, PSA, SYMC, CTBP2, NU107, TPIS, ACTB, IF4A1, PSA6, ARF3, ABCE1, RAP1B, RS3A, RL26, RL15, S61A1, HNRPK, RS7, RS8, 1433E, RS14, RS23, RS11, SMD1, RL7A, RS4X, H4, RAN, RL23, GBB2, RL10A, RL11, RL8, PPIA, RL40, TRA2B, AP2B1, IF5A1, RACK1, YBOX1, EF1A1, TBB4B, CSK21, IF4G2, GTF2I, TCPB, PRKDC, RL24, RL19, SRSF3, FOXK1, RBM10, MPCP, CLH1, HNRPU, SPTB2, FOXK2, CAP1, LAT1, EXOSX, EWS, RL18A, FKBP4, RL6, TOP2B, KMT2A, LMNB2, TF65, IF4G1, TLE3, SRS11, PUR1, SUH, GABPA, PRDX1, RL18, C1QBP, KHDR1, SRSF1, DHX9, CD47, SSRP1, RBBP4, AHNK, AP1B1, NU160, BPTF, TP53B, AIMP1, ILF2, ILF3, LMAN2, TRAP1, PP1R8, ACACA, ROA0, PRDX4, CBX3, PSMD2, SRSF6, TIF1B, PTK7, PABP4, EIF3I, TCOF, SF3B2, TMED1, PICAL, RIPK1, HDAC1, CUL4B, CD166, IDI1, NFYC, CKAP5, HNRPD, SCRB2, DSG2, EIF3A, UBP2L, SCRIB, TTL12, DCTN1, DYHC1, SRC8, CAPR1, RBM39, MCM6, MDC1, EPN4, SMC1A, RRP1B, UBP10, GANAB, LBR, ZN638, IMB1, NUMA1, SEPT2, SART3, U5S1, SYK, BRD3, PDIA6, IPYR, TEBP, NONO, PWP2, RCN1, PCBP1, PCBP2, SF3B3, SAFB1, SF3A1, NCOA2, SF01, MARE1, NSDHL, TAB1, AAAT, VAS1, ZYX, CCDC6, PKN2, DDB1, CDC37, SRSF7, CPSF6, NRF1, H31T, QSER1, QRIC1, P3H1, TB10B, AMOT, DHB12, PRC2B, H2B2F, HP1B3, CE170, ZC3HD, RBM26, RIF1, RPRD2, ZN318, ECM29, ZMYM4, MAP1S, LIN54, EDC4, PRP8, SCYL2, NFRKB, ZC3HE, LARP1, FIP1, MCAF1, GGYF2, SPT6H, SND1, DHX30, KDM3B, ZCCHV, NUP54, POGZ, NUFP2, MAVS, I2BP2, RBBP6, HUWE1, YTHD3, CENPV, LYRIC, ZN598, GP180, CAND1, CARM1, DDX42, P66A, ARI3B, MGAP, PHF6, CHERP, ANKH1, SUGP1, CCAR1, SPB1, PHAR4, SPART, CCAR2, NUP93, S11IP, FNBP4, CPSF7, ARFG1, ENAH, AFG2H, TXND5, LS14A, Z280C, TNR6A, SMRC2, TBC15, PNPT1, HM13, PO210, GEMI5, ZN384, SMAP2, NU133, PDC6I, PCNP, CKAP2, ATX2L, P66B, ELYS, DDX1, GBF1, NICA, UBXN4, HS105, LAR4B, NU205, AKAP1, TFG, CBP, DDX17, CELF1, RENT1, SMRC1, FUBP2, TNPO1, UBP7, NCLN, FUBP1, FKB10, KBP, PDLI5, FUBP3, CHAP1, Z512B, ZFR, PRRC1, DOCK7, RBM14, VPS35, CIC, EFGM, SIN3A, MINT, CDC5L, PSMD1, EYA3, ATX2, HCD2, ACON, TS101, TCPH, ANM1, SH3G1, COR1B, DIDO1, HNRL1, DDX23, TMED9, NUP58, RBM4, NAA15, B2L13, YTHD1, UNK, ILKAP, SP130, BRD8, I2BPL, SLK, S6A15, PININ, NELFA, PTN23, WNK1, AMPB, GORS2, CYBP, TAF9B, GLOD4, CBX8, NCOA5, CHD8, APMAP, DCP1A, RTN4, ANLN, GEPH, PDLI7, DDX21, SYFB, SYIM, SMC4, RBM12, DDX18, CARF, UGGG1, CDK12, TECR, IF2B1, HPBP1, ITSN2, CNOT2, HACD3, RCC2, SYLC, SUCB1, UBQL2, PCYOX, S30BP, PUF60, NRBP, DACH1, BAZ2A, BAZ1B, CDC23, TASOR, ACINU, CDV3, MRTFB, YETS2, HECD1, PKCB1, DD19B, PRP19, MAGD2, FAF1, TRI33, SRRM2, PA2G4, RUVB2, RUVB1, VDAC3, E41L3, TR150, NOP58, SHLB1, LC7L2, TMED7, STRAP, RTCB, HBS1L, TLN1, HYOU1, PRC2C, SP16H, COPG1, DC1L1, S23IP
Species: Homo sapiens
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Xu S, Sun F, Wu R. A Chemoenzymatic Method Based on Easily Accessible Enzymes for Profiling Protein O-GlcNAcylation. Analytical chemistry 2020 92(14) 32574038
Abstract:
O-GlcNAcylation has gradually been recognized as a critically important protein post-translational modification in mammalian cells. Besides regulation of gene expression, its crosstalk with protein phosphorylation is vital for cell signaling. Despite its importance, comprehensive analysis of O-GlcNAcylation is extraordinarily challenging due to the low abundances of many O-GlcNAcylated proteins and the complexity of biological samples. Here, we developed a novel chemoenzymatic method based on a wild-type galactosyltransferase and uridine diphosphate galactose (UDP-Gal) for global and site-specific analysis of protein O-GlcNAcylation. This method integrates enzymatic reactions and hydrazide chemistry to enrich O-GlcNAcylated peptides. All reagents used are more easily accessible and cost-effective as compared to the engineered enzyme and click chemistry reagents. Biological triplicate experiments were performed to validate the effectiveness and the reproducibility of this method, and the results are comparable with the previous chemoenzymatic method using the engineered enzyme and click chemistry. Moreover, because of the promiscuity of the galactosyltransferase, 18 unique O-glucosylated peptides were identified on the EGF domain from nine proteins. Considering that effective and approachable methods are critical to advance glycoscience research, the current method without any sample restrictions can be widely applied for global analysis of protein O-GlcNAcylation in different samples.
O-GlcNAc proteins:
SBNO1, CNOT1, SWAHB, P121C, PDLI1, TAF4, RNT2, PODXL, KMT2D, MYPT1, ZN609, SC16A, SET1A, ZN185, TNC18, PRPF3, TPD54, SYNJ1, PLIN3, MAFK, BRD4, N4BP1, ICOSL, ANR17, ZN217, NCOR1, ATRN, TOX4, ERLN2, AGFG2, VAPB, SC24A, SC24B, CNOT4, BAG3, LMNA, GCR, HSPB1, IF2A, K1C18, K2C8, K1C19, ROA1, TACD2, ATX1L, LYAG, PPAL, TPR, K1C13, ZEP1, SDC1, ATF1, CBL, GATA3, ARNT, MAP4, CLIP1, HXC9, NU214, MP2K2, CUX1, PBX2, MLH1, STAT3, LAP2A, KI67, RFX5, SOX2, NU153, RBP2, TAF6, HCFC1, AFF3, AGFG1, ATX1, AF17, DSRAD, FOXA1, NU107, FOXK1, SPTB2, TFAP4, EWS, SP2, KMT2A, IF4G1, NOTC2, TLE3, TLE4, REL, ACK1, LG3BP, AHNK, ARHG5, FOXO1, BPTF, RIPK1, NFYC, CDK13, UBP2L, LAGE3, MDC1, EPN4, RRP1B, NCOA6, GSE1, MEF2D, NUMA1, R3HD1, JHD2C, TRIP6, ELF2, TAB1, ZFHX3, ZYX, ADRM1, TAF9, RFX7, QSER1, QRIC1, TB10B, CRTC2, PRC2B, ZN362, UBAP2, RPRD2, ZN318, TASO2, ARID2, ANR40, BICRL, ABLM2, GRHL2, NIPBL, LIN54, TET2, NFRKB, KCD18, MDEAS, ZC3HE, FIP1, SAS6, MCAF1, BCOR, HAKAI, SPT6H, KDM3B, POGZ, MAVS, EMSY, RAI1, SRGP1, SH3R1, YTHD3, CASZ1, P66A, I2BP1, RB6I2, FOXP4, NAV2, GID4, MGAP, CDAN1, SUGP1, MILK2, NUP93, ZN687, FNBP4, ARFG1, ENAH, PHC3, SP20H, KMT2C, STT3B, DLG5, WIPF2, ZFN2B, LMO7, ATX2L, CSKI2, P66B, SMG7, CBP, SEM4D, FUBP2, LPP, PF21A, INT12, CERS2, GWL, PDLI5, CHAP1, ANCHR, Z512B, ZFR, EP400, RBM14, CIC, MINT, S29A1, DPH2, WAC, DIDO1, HNRL1, YTHD1, CEP44, SP130, I2BPL, FOXP1, WNK1, E41L1, ZHX3, GORS2, PKHA5, RC3H2, TAF9B, NCOA5, TANC2, CELR2, UBN1, PDLI7, RBM12, CARF, TAB2, CNOT2, KANL3, STAP2, TCF20, UBQL2, S30BP, SIX4, TASOR, GMEB2, ZHX1, YETS2, PKCB1, NOTC3, TRI33, SRRM2, CHM2B, SCML2, POLH, R3HD2, ZN281, WNK2, PRC2C, NCOR2, GMEB1, ZHX2
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, CMC1, 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, CBSL, 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, ACOC, 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, SL7A1, 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, PRP4B, 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, SKIV2, 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, F102B, 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, TTC37, RICTR, LCLT1, WDR82, HACD2, GGYF2, KAT3, UBR3, LARP4, SPT6H, SND1, COX15, DDX46, TM10C, BZW1, 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, WDR61, 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, OSGP2, 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, CMC2, 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, BZW2, COMDA, DC1L1, TX264, S4A7, NDUB9, MORC2, S23IP
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, TAU, 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, RT36, 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, TNS2, 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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