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Hou C, Zhang H, Deng J, Wang X, Byers S, Levi M, Pak DTS, Moremen KW, Pei H, Hart GW, Ma J. Comprehensive Evaluation of Cleavable Bioorthogonal Probes for Site-Specific O-GlcNAc Proteomics. Molecular & cellular proteomics : MCP 2025 24(10) 40885482
Abstract:
O-linked β-N-acetylglucosamine (O-GlcNAc) modification (i.e., O-GlcNAcylation) on proteins is an essential modification in physiology and pathology. Although O-GlcNAcylation is functionally critical, its analysis has been challenging. Despite the existence of a number of methods developed in the past years, which one(s) might have the best performance is largely unclear. To that end, we conducted a rigorous comparison of several cleavable bioorthogonal biotin-alkyne probes which showed promise for sensitive O-GlcNAc proteomics. In brief, we developed chemoenzymatic labeling/click chemistry-based analytical workflows for O-GlcNAc proteomics by utilizing four cleavable bioorthogonal probes, including photocleavabe-biotin-alkyne (PC-biotin-alkyne), dialkoxydiphenylsilane-biotin-alkyne (DADPS-biotin-alkyne); 1-(4,4-dimethyl-2,6-dioxocyclohex-1-ylidene)ethyl-biotin-alkyne (Dde-biotin-alkyne), and diazobenzene-biotin-alkyne (Diazo-biotin-alkyne). The analytical performance of these probes was evaluated with synthetic O-GlcNAc peptides and then benchmarked by using mouse brain lysates for O-GlcNAc proteomics. Besides providing valuable technical insights into O-GlcNAc proteomics methods, our work yielded an unprecedented O-GlcNAc proteome depth in the mouse brain. In total, 2906 O-GlcNAc sites were unambiguously assigned on 878 proteins. Among them, 1611 sites were newly identified, including 138 O-GlcNAcylated tyrosine residues. Our work will help guide the selection/development of O-GlcNAc proteomics methods for future studies, provide an invaluable resource for functional elucidation of protein O-GlcNAcylation in brain biology, and yield critical insights into tyrosine O-GlcNAcylation.
O-GlcNAc proteins:
QSER1, TANC2, ZEP3, MA7D2, CKAP5, AMRA1, CAMP1, LZTS3, AJM1, MA7D1, FRPD1, RPGP1, UBR4, SKT, BCORL, AGRIN, TITIN, SVEP1, ARI1A, SPAS1, KANL3, PHRF1, PTPRS, SCN2A, DLGP4, EP300, RBM25, ILDR2, CTTB2, PTPRZ, NLRC5, CCDC6, SHAN1, SET1A, PARP4, PRR12, TENS1, I2BP2, AKP13, C2CD2, ARI1B, ZC3HD, ARID2, NUMA1, PDZD7, SC16A, SYGP1, TPR, BICRA, SI1L3, PLGT3, DPYL2, EMD, STXB1, AKAP1, CLOCK, DCTN1, NUMBL, DBIL5, SYPL1, M3K5, SCRB2, ATN1, NOTC2, VIAAT, HAP1, CTND2, PITM1, OX2G, REPS1, AKAP2, ACK1, CNTP1, CAC1B, SYUA, PI51C, ATX2, E41L2, PDLI1, ULK1, UBR1, HCN4, KDM6A, ZN106, PDE8A, PPT1, ZFR, HCN2, HCN1, CTBP1, BSN, TOM1, AKA10, HIPK1, SYN1, LGMN, TPP1, THY1, LAMC1, MBP, ALDOA, GCR, CATL1, EGR1, HCK, ENPL, KCC4, NFL, NFM, ITB1, RC3H2, MAMD1, ATX1L, CATB, TAU, LAMP1, DMD, KCC2A, ITPR1, CNTN1, NCAM1, AT1B2, HSPB1, MAP1B, G3P, ATF2, PPIA, CATD, BASI, COF1, NFH, BIP, HEXB, MTAP2, MAG, CYTC, EMB, GRIA1, GRIA2, RS2, RGRF1, KCC2B, PABP1, C5AR1, AIMP1, DPOA2, RAB23, NMDE1, NMDZ1, FMR1, FOXK1, STAT3, EAA2, EGR3, RAD52, ITAV, CBP, AINX, NEDD4, STT3A, RP3A, EPB41, RFX1, SOX2, LMNA, MPIP1, INPP, DHI1, ARSB, VATA, DVL1, ADCY7, DBX1, E41LA, ARNT, SOX1, ATX1, RD23B, 3BP1, AMRP, CX6B1, CTBP2, MAZ, WFS1, PCBP3, PTPA, KCNN2, FOXP1, TB10A, TB182, GMEB2, KCNH8, CAPAM, RHG39, YTHD1, RPC2, PI5PA, MRTFB, DOCK4, IRPL1, MYPR, ABI2, GBB1, RAB3A, VAMP2, KCNA2, KCNJ3, ZHX1, DCC, NFIX, NCOA1, RGRF2, USP9X, TP53B, NACAM, LYAG, IRS2, TNIK, WNK1, G3BP2, ARG28, MPRIP, CAC1A, NPAS2, GRM1, XRN1, SHPS1, NEO1, G3BP1, NFIB, RLA2, GABPA, CBPE, NMDE2, NMDE3, NOTC1, CTNB1, PLAK, S30BP, NFIA, ZEP1, ENAH, KCNB1, RCN1, PGBM, EMAL1, LG3BP, TLE3, MITF, SSRP1, CHD8, TRIO, TANC1, RELCH, CDK12, MA6D1, F171B, SHRM4, PHAR1, GSK3A, PSD3, MLXIP, NELL1, ESP1, PLBL2, PDLI7, PRC2C, MILK2, YETS2, SRSF6, FUBP2, SRBP2, GSE1, F117B, WDR62, FOXK2, CARL3, DIP2B, WNK2, LIMC1, TNR6C, DAB2P, AGAP2, ZEP2, ZSWM8, AAK1, TEN4, TNR6A, CAMKV, MTCL1, PKHA7, COBL1, GRIN1, PRRC1, MINY4, FCHO2, SNX21, LIGO2, MRCKA, KSR2, GRM5, ARMX5, ELAP2, GARL3, 5NTC, PACS2, STOX2, UBN1, ABL2, OXR1, DSCL1, CDV3, PHAR4, ANR28, LRC47, SRRM1, EME2, LIN54, TAB3, STB5L, NEXMI, JCAD, NYNRI, NUFP2, UNKL, PRSR1, OSBP2, SMG7, LRRK2, RBM27, PHF12, CYFP2, TM1L2, ANR40, CCD42, SYNRG, RPGP2, NACAD, LHPL4, EPAB2, LMTK3, SIN3A, SRC8, ICAM5, LAMA2, ITF2, CAPR1, NCOR1, FOXG1, LAMA5, NCOA2, LAMC2, IL18R, NAB1, ASTN1, SPIN1, PAPOA, HCFC1, SAP, NELL2, APC, PGCB, ZN638, AP180, FXR1, GRID2, GRID1, PACN1, HIRA, RAI1, MAFK, NPM, NOTC3, CSPG2, M3K7, DAG1, RO52, SN, SPTB2, TAF6, SPEG, ASPP1, SRBS1, DBNL, SH3G1, TLE4, SP4, IF4G2, MINT, ZYX, OMGP, MEF2D, TFE3, PAN3, HECAM, SF01, SYN2, TBR1, DHSO, CGT, CH058, SBNO1, CRTC1, BEGIN, K1549, GIT1, SLAI1, PKP4, SYMC, CDK13, GBA2, SH3R1, PREX1, JHD2C, HECD1, MOR2A, ABLM3, TBC12, ARMX2, CE170, LAR4B, RHG21, HELZ, MEG10, SCAF8, LIGO3, ZZZ3, F135A, FBX41, SPKAP, RPRD2, WWC2, ZN532, DPP10, TAF9B, S23IP, IF4G1, RBM26, NSD3, SNX19, FHOD1, FKB15, MTSS2, BCR, AHDC1, AAKB2, PTN23, LPPRC, PAPD7, MFF, PIGS, TRAK1, PHLB1, KMT2D, RN220, DLGP3, RA54B, GMIP, WASC2, ERC2, KCC2D, NFRKB, ALEX, MAGI1, CENPE, DNMBP, GGYF2, TEX2, PF21A, KDM3B, FNBP4, CNOT1, LARP1, NU188, SYNE1, IF2A, UB2R2, CMYA5, SEM6D, SOX11, PICAL, ASAP2, HUWE1, SMAP2, PLPR3, PRC2B, C2CD5, TPPP, MACOI, AMPH, ATX2L, PRC2A, TMM94, PP6R1, MAP6, MCAF1, DAAF9, SI1L2, LRRC7, ERBIN, PHF24, R3HD2, NAV3, AGRL1, DEND, AUXI, RERE, SNPH, MADD, RIMB2, PUM1, NU214, SEPT9, SESD1, CBPM, SRA1, EPN1, AKNA, HYDIN, UBN2, AGFG2, CHST2, UBP2L, T106B, C2C2L, REPS2, WNK3, DDHD1, CNKR2, BCAS1, ZN598, SHAN2, PKHL1, S2611, ZFYV1, NRCAM, DLG1, MAST4, RHG32, GPHB5, RN214, LPP, MYPT2, TB10B, CSTP1, SP130, ZC3HE, DLGP2, ZC21A, ZNT6, SUN2, EME1, TNR6B, BAIP2, ABLM2, NCEH1, LRFN3, EMSY, SHC2, SEN34, FAT3, DMXL2, GORAB, CLAP2, K1671, FAKD3, LIPA2, CNOT4, RALYL, SRRM2, TOX4, PAMR1, F163B, GEPH, CREST, KCC1D, GRIN3, LARP4, Z385B, IFFO1, OSBL6, CC169, TENR, YTHD3, STON2, TM266, POGZ, DOC10, ZHX2, EPC2, SWAHC, ZHX3, SI1L1, SH3R3, FRS2, RBM14, CNOT2, MOR2B, HYCC2, ANK2, ELFN1, TM163, DIDO1, SMAG1, SYNPO, BCAS3, VCIP1, BAKOR, TAB1, SCYL2, NED4L, MEF2C, ASPP2, TENS2, F193A, OGT1, CHERP, NAV1, SYNJ1, RPGF2, EP400, PHC3, DPYD, VP37A, EPN2, P66A, PDLI5, ANM5, DOCK3, PLXB1, DNER, SPAT2, SCAM1, SAM14, ZBT20, PHYIP, RTN1, HS12A, C2D1A, UNC5A, PACS1, TRI68, BRD3, LS14A, AGFG1, MATR3, DEN1A, I2BPL, PO121, ABLM1, MRTFA, RPTOR, PLCE1, SPNS1, CACL1, KCNC4, DC1L1, MTSS1, SPART, LRC42, ZN445, RFIP5, IGSF8, BRD8, WIPI1, CDK8, PP6R2, SHLB2, CS047, NTNG2, PP14C, STAB2, LUZP1, RBM12, STAB1, OTU7A, SC6A8, ULA1, CLPT1, MAVS, GRAP1, SGIP1, PI3R4, PHIP, SIR2, GOLI, AMOT, AGAP3, WASF3, P66B, CCG8, TAF9, ZCH14, MCR, SFPQ, WDR13, UBAP2, SMAP1, NCOA5, CXXC5, FRS3, SPS2L, FUBP1, SH319, ZFN2B, VPS36, DLG2, DYH8, DCP1A, YTHD2, PTBP2, SRGP2, SRGP1, BMP2K, DYST, LRP1, SYUB, ALS2, TRFE, GPS2, CLIP1, CIC, WAC, SPRE1, MED1, NRBP, NPTXR, GGT7, GORS2, NONO, TAB2, DPP3, EPN4, RNF34, GAK, DDAH2, ZN281, HGS, RB6I2, RIMS1, ANR17, RTN4, RRBP1, ZN318, TRI33, MZT2, PCYOX, NECP1, FLIP1, NRX1A, SNX2, DDAH1, YIF1B, NOPC1, CYGB, GFOD2, TPD54, CEP97, CD37L, SSBP3, SARNP, SP2, UB2V2, DLGP1, NDUV2, SH24A, FIP1, ST1C2, F135B, TM263, CNPY3, RM12, BTBDH, AL7A1, PLIN3, MYPT1, LNEBL, DCAF6, KC1D, CRIP2, TSC1, NBEA, TCF20, CPSF1, DPYL5, RIMS2, ZN704, RBP2, RTN3, SPN90, SP6, GILT, CLD12, ELF2, TSSC4, LRP1B, NUDT3, CATR, PPR3F, NUP50, TULP4, ORC3, ATR, HYOU1, ADRM1, FMN2, NCOA6, BAG3, MINK1, ZN207, PHC2, SRCN1, ASAP1, SON, SALL2, LIMD1, TBL1X, APBB1, PLEC, MACF1, ULK2, ADDB, ADDA, PCX1, GOGA5, NDRG2, MAGD1, MAP1A, QKI, PCLO, GAB1, MAGL2, FBX6, NPAS3, HIPK2, SH2D3, CATJ, YLPM1, CELR2, RHG07, GUAD, FOXO1, TAGL3, ADA22, AKA12, TEN1, TEN3, NCOR2, ATRN, COR1B, SR5A3, GANP, NFAT5, ASAH1, GSK3B, DEMA, E41L3, CARM1, JIP1, KCNH3, MAGI2, FXR2, SYUG, CLIP2, PALM, ITSN1, ITSN2, ZO2, DYR1B, APCL, BAG6, DPP6, MTMR1, MECP2, SE1L1, E41L1, GRIA3, HOME1
Species: Mus musculus
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Hao Y, Li X, Qin K, Shi Y, He Y, Zhang C, Cheng B, Zhang X, Hu G, Liang S, Tang Q, Chen X. Chemoproteomic and Transcriptomic Analysis Reveals that O-GlcNAc Regulates Mouse Embryonic Stem Cell Fate through the Pluripotency Network. Angewandte Chemie (International ed. in English) 2023 62(17) 36852467
Abstract:
Self-renewal and differentiation of embryonic stem cells (ESCs) are influenced by protein O-linked β-N-acetylglucosamine (O-GlcNAc) modification, but the underlying mechanism remains incompletely understood. Herein, we report the identification of 979 O-GlcNAcylated proteins and 1340 modification sites in mouse ESCs (mESCs) by using a chemoproteomics method. In addition to OCT4 and SOX2, the third core pluripotency transcription factor (PTF) NANOG was found to be modified and functionally regulated by O-GlcNAc. Upon differentiation along the neuronal lineage, the O-GlcNAc stoichiometry at 123 sites of 83 proteins-several of which were PTFs-was found to decline. Transcriptomic profiling reveals 2456 differentially expressed genes responsive to OGT inhibition during differentiation, of which 901 are target genes of core PTFs. By acting on the core PTF network, suppression of O-GlcNAcylation upregulates neuron-related genes, thus contributing to mESC fate determination.
O-GlcNAc proteins:
AMRA1, SETX, SKT, BCORL, AGRIN, MGAP, ARI1A, CHD6, PHRF1, ZCH24, EP300, KIF7, KI67, CE350, ANR11, NUMA1, TPR, MORC3, TAF4B, KMT2B, EMD, AKAP1, TCOF, DCTN1, MNT, NCOA3, ATN1, ECP3, DPOD2, CTND2, PIAS3, AF10, ACK1, GET3, DSG2, ESS2, ATX2, PDLI1, ULK1, BARD1, KDM6A, ZN106, NSD1, ZFR, HIPK1, SETB1, LAMC1, MYCN, GCR, EGR1, RC3H2, ATX1L, DERPC, K2C8, HSPB1, JUND, FGFR1, G3P, ATF2, COF1, HEXB, VIME, PO5F1, CBL, CCNB1, PO2F1, RS2, NFKB1, MAX, PABP1, NEDD1, PTN12, FMR1, ELK1, FOXK1, STAT3, SOX15, PLIN2, CBP, NEDD4, YAP1, RFX1, SOX2, LMNA, ROA1, S1PR2, ARNT, RD23A, PLTP, KMT2A, KLF16, FOXP1, TB182, GMEB2, SENP1, YTHD1, MRTFB, DOCK4, STIM1, TBX3, NCOA1, ERF, SIAE, NACAM, ATF1, WNK1, G3BP2, DNLI3, G3BP1, RLA2, GABPA, S30BP, ZEP1, ENAH, SOX13, CAPR2, APLP2, CLUS, TLE3, GATA4, MITF, CHD8, ZCH18, TANC1, CDK12, SAP25, LIN41, MLXIP, HROB, VRTN, CO039, PDLI7, SMCA4, PRC2C, MILK2, MIDN, YETS2, PBIP1, FUBP2, TFPT, SRBP2, GSE1, F117B, ZN865, WDR62, QRIC1, FOXK2, RREB1, TNR6C, DAB2P, TNR6A, RHG17, PKHA7, COBL1, FCHO2, TET1, ARMX5, GARL3, TET2, CDV3, PHAR4, C2CD3, LIN54, NPA1P, TAB3, TASO2, RESF1, NUFP2, UNKL, COBL, KDM6B, PRSR1, SMG7, RBM27, PHF12, ZDBF2, PUR4, SYNRG, UIMC1, SIN3A, NFAC2, SRC8, SKIL, ELF1, KLF4, NCOR1, KLF3, NCOA2, FOXD3, PAPOA, HCFC1, P3C2A, SIX4, ZFHX3, TOB1, AP180, GLI3, ATRX, MAFK, NPM, M3K7, DAG1, SPTB2, TAF6, TIF1B, SPT6H, SH3G1, ARI3A, TLE1, TLE4, IF4G2, MINT, ZIC3, ZYX, NUP62, PHC1, TFE3, TIF1A, SF01, DAZL, RBL1, KNL1, BCL9L, SBNO1, SLAI1, PKP4, CDK13, SH3R1, JHD2C, HECD1, ARMX2, LAR4B, RHG21, HELZ, SCAF8, UTF1, PKHG2, NIPBL, CCD66, F135A, RPRD2, WWC2, ZN532, KRBA1, TAF9B, RBM26, INT1, BCR, AHDC1, PTN23, PAPD7, KDM3A, KMT2D, CHD4, RN220, NUP98, NFRKB, GGYF2, LCOR, TEX2, PF21A, KDM3B, FNBP4, CNOT1, LARP1, RHG26, NU188, CNDD3, SPAG5, HUWE1, SMAP2, CPEB3, MYCB2, PRC2B, PRR14, MACOI, ATX2L, CKP2L, PRC2A, MCAF1, SI1L2, KANL1, ERBIN, R3HD2, RERE, PUM2, PUM1, NU214, WNK4, TCAM1, SAS6, CAMP3, UBN2, TNC18, AGFG2, WNK3, ZN598, CTIP, SHAN2, NANOG, DDX42, RHG32, VGLU3, LPP, TET3, MYPT2, IF4B, CNO10, MISSL, TB10B, CARF, TGO1, ZN879, SP130, ZC3HE, ZNT6, SUN2, TNR6B, ARI5B, BNC2, KAT6B, KMT2C, CLAP2, CNOT4, SRRM2, TOX4, GEPH, SYP2L, LARP4, KANK2, SALL4, YTHD3, TOIP2, KAT6A, ASXL2, POGZ, TAF5, ZHX2, EPC2, SI1L1, CND2, RBM14, SUCO, CNOT2, DIDO1, SMAG1, LENG8, CDAN1, DPPA4, LRIF1, VCIP1, MB214, TAB1, SCYL2, ASPP2, LS14B, SYEP, F193A, BCOR, OGT1, SUGP1, NAV1, SYNJ1, ADNP2, RPGF2, BICRL, EP400, PHC3, VP37A, EPN2, P66A, PDLI5, ELYS, ZBT20, ANLN, AGFG1, MATR3, CASC3, I2BPL, PO121, ALMS1, SF3A1, GRHL2, ATF7, CACL1, DC1L1, MTSS1, SPART, TDIF2, HBP1, NUP58, RFIP5, BRD8, WIPI1, CDK8, CS047, ATX7, NUP35, LUZP1, RPAP2, NDC1, MAVS, AMOT, CSKI2, P66B, TAF9, IPO4, ZCH14, UBAP2, NCOA5, FUBP1, RBM47, AJUBA, VPS36, DCP1A, EGLN2, YTHD2, SRGP2, GRHL1, BCL7B, P4R3B, PLRG1, WAC, TRPS1, MED1, ACATN, NRBP, RP25L, NONO, TAB2, EPN4, DDAH2, NOG2, ZN281, HGS, NASP, ARIP4, ANR17, ZN318, TRI33, MZT2, ZWINT, ECD, YIF1B, ROA0, DHRS7, TPD54, SSBP3, PSRC1, SARNP, BCL9, SP2, NOP56, SH24A, FIP1, PLIN3, MYPT1, KC1D, TCF20, TOR3A, SALL1, ZN704, RBP2, UBE4B, TBX20, AFF4, RBCC1, 4ET, PALLD, ELF2, TSSC4, NUDT3, HAKAI, ADRM1, NCOA6, FANCA, GIT2, BAG3, TOB2, ZN207, SON, TBL1X, PLEC, MACF1, GOGA5, QKI, GAB1, DMRT1, YLPM1, PCM1, RHG07, TAF7, FOXO1, ADA23, AKA12, UXT, MAN1, NCOR2, AKT3, COR1B, TNIP1, GANP, DEMA, CARM1, RGAP1, ITSN2, ZO2, KLF5, ADNP, ARI3B, BCL3, SE1L1, E41L1, ZN292
Species: Mus musculus
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Alfaro JF, Gong CX, Monroe ME, Aldrich JT, Clauss TR, Purvine SO, Wang Z, Camp DG 2nd, Shabanowitz J, Stanley P, Hart GW, Hunt DF, Yang F, Smith RD. Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proceedings of the National Academy of Sciences of the United States of America 2012 109(19) 22517741
Abstract:
O-linked N-acetylglucosamine (O-GlcNAc) is a reversible posttranslational modification of Ser and Thr residues on cytosolic and nuclear proteins of higher eukaryotes catalyzed by O-GlcNAc transferase (OGT). O-GlcNAc has recently been found on Notch1 extracellular domain catalyzed by EGF domain-specific OGT. Aberrant O-GlcNAc modification of brain proteins has been linked to Alzheimer's disease (AD). However, understanding specific functions of O-GlcNAcylation in AD has been impeded by the difficulty in characterization of O-GlcNAc sites on proteins. In this study, we modified a chemical/enzymatic photochemical cleavage approach for enriching O-GlcNAcylated peptides in samples containing ∼100 μg of tryptic peptides from mouse cerebrocortical brain tissue. A total of 274 O-GlcNAcylated proteins were identified. Of these, 168 were not previously known to be modified by O-GlcNAc. Overall, 458 O-GlcNAc sites in 195 proteins were identified. Many of the modified residues are either known phosphorylation sites or located proximal to known phosphorylation sites. These findings support the proposed regulatory cross-talk between O-GlcNAcylation and phosphorylation. This study produced the most comprehensive O-GlcNAc proteome of mammalian brain tissue with both protein identification and O-GlcNAc site assignment. Interestingly, we observed O-β-GlcNAc on EGF-like repeats in the extracellular domains of five membrane proteins, expanding the evidence for extracellular O-GlcNAcylation by the EGF domain-specific OGT. We also report a GlcNAc-β-1,3-Fuc-α-1-O-Thr modification on the EGF-like repeat of the versican core protein, a proposed substrate of Fringe β-1,3-N-acetylglucosaminyltransferases.
O-GlcNAc proteins:
ZEP3, CAMP1, FRPD1, SKT, DLGP4, DPYL2, STXB1, MAP2, NUMBL, M3K5, NOTC2, CTND2, CSK22, ACK1, SYUA, ATX2, ZFR, BSN, GCR, EGR1, NFL, NFM, RC3H2, MAMD1, ATX1L, DERPC, NCAM1, MAP1B, G3P, ATF2, MAP4, KCC2B, AIMP1, FOXK1, STAT3, AINX, NEDD4, RP3A, DVL1, GOGA3, FOXP1, TB182, GMEB2, PI5PA, MRTFB, DOCK4, ABI2, KCNJ3, NCOA1, RGRF2, TNIK, WNK1, G3BP2, MPRIP, XRN1, RLA2, S30BP, MARK3, ENAH, PGBM, CDK12, MA6D1, PHAR1, PSD3, NELL1, PRC2C, YETS2, FOXK2, WNK2, LIMC1, TNR6C, AGAP2, ZEP2, AAK1, TNR6A, CAMKV, PKHA7, GRIN1, FCHO2, GARL3, STOX2, UBN1, ABL2, CDV3, PHAR4, TAB3, NUFP2, UNKL, OSBP2, RBM27, CYFP2, TM1L2, ANR40, NACAD, SIN3A, NCOR1, LAMA5, NCOA2, AP180, RAI1, M3K7, TAF6, SRBS1, SH3G1, TLE4, MINT, ZYX, SF01, SYN2, TBR1, SBNO1, CRTC1, GIT1, SLAI1, PKP4, CDK13, RHG23, SH3R1, JHD2C, HECD1, ABLM3, ARMX2, LAR4B, RHG21, FBX41, RPRD2, WWC2, ZN532, BCR, DLGP3, NYAP1, GMIP, NFRKB, MAGI1, CNOT1, NU188, SMAP2, SPAG7, PRC2B, ATX2L, MAP6, MCAF1, PHF24, NAV3, AUXI, RERE, RIMB2, PUM1, NU214, KCMF1, EPN1, AGFG2, C2C2L, CNKR2, ZN598, SHAN2, MAST4, RHG32, MYPT2, TB10B, FRM4A, SP130, DLGP2, ZNT6, ABLM2, CLAP2, CNOT4, PAMR1, CREST, IFFO1, OSBL6, YTHD3, TM266, SI1L1, SH3R3, RBM14, CNOT2, ANK2, DIDO1, SYNPO, VCIP1, TAB1, SCYL2, ASPP2, F193A, OGT1, NAV1, SYNJ1, RPGF2, EP400, P66A, PDLI5, SCAM1, HS12A, AGFG1, I2BPL, PO121, ABLM1, SPART, RFIP5, CS047, SIR2, AMOT, CCG8, ZCH14, WDR13, UBAP2, NCOA5, FRS3, ZFN2B, BASP1, DCP1A, SRGP2, SRGP1, SYUB, CLIP1, UBXN1, GORS2, EPN4, RB6I2, ANR17, TXD12, NECP1, DLGP1, FIP1, F135B, TM263, PLIN3, MYPT1, CRIP2, TSC1, NBEA, RIMS2, ZN704, RBP2, RTN3, 4ET, ELF2, NUDT3, FMN2, NCOA6, SRCN1, ASAP1, RAD1, SON, PLEC, ULK2, ADDA, PCLO, HIPK2, SH2D3, YLPM1, RHG07, TEN1, NCOR2, COR1B, TNIP1, DEMA, E41L3, SYUG, APCL, MECP2, E41L1
Species: Mus musculus
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