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Massman LJ, Pereckas M, Zwagerman NT, Olivier-Van Stichelen S. O-GlcNAcylation Is Essential for Rapid Pomc Expression and Cell Proliferation in Corticotropic Tumor Cells. Endocrinology 2021 162(12) 34418053
Abstract:
Pituitary adenomas have a staggering 16.7% lifetime prevalence and can be devastating in many patients because of profound endocrine and neurologic dysfunction. To date, no clear genomic or epigenomic markers correlate with their onset or severity. Herein, we investigate the impact of the O-GlcNAc posttranslational modification in their etiology. Found in more than 7000 human proteins to date, O-GlcNAcylation dynamically regulates proteins in critical signaling pathways, and its deregulation is involved in cancer progression and endocrine diseases such as diabetes. In this study, we demonstrated that O-GlcNAc enzymes were upregulated, particularly in aggressive adrenocorticotropin (ACTH)-secreting tumors, suggesting a role for O-GlcNAcylation in pituitary adenoma etiology. In addition to the demonstration that O-GlcNAcylation was essential for their proliferation, we showed that the endocrine function of pituitary adenoma is also dependent on O-GlcNAcylation. In corticotropic tumors, hypersecretion of the proopiomelanocortin (POMC)-derived hormone ACTH leads to Cushing disease, materialized by severe endocrine disruption and increased mortality. We demonstrated that Pomc messenger RNA is stabilized in an O-GlcNAc-dependent manner in response to corticotrophin-releasing hormone (CRH). By affecting Pomc mRNA splicing and stability, O-GlcNAcylation contributes to this new mechanism of fast hormonal response in corticotropes. Thus, this study stresses the essential role of O-GlcNAcylation in ACTH-secreting adenomas' pathophysiology, including cellular proliferation and hypersecretion.
O-GlcNAc proteins:
GPTC8, ITB4, PTPRF, VIR, HMCN2, SETX, RTF1, MYH7B, FSIP2, TITIN, ARGAL, CO6A5, MMRN2, STOX1, PLXB2, AGRG4, F25A2, LOXH1, HMCN1, TM233, PIEZ1, TOPZ1, CE350, M3K19, RYR2, ACACB, RN213, CF251, ARHG5, BICRA, FOXM1, DLDH, PEX5, WRN, CELR1, PROM1, STK10, MYPC3, DTNB, IKKB, ACTN3, ALDOC, RPB1, LMNB1, MAP1B, HVM57, PAI1, MCM3, MIS, RGRF1, MSRE, CTND1, RB22A, ZO1, QOR, ANXA5, MSH6, EVC, KCNN2, DEPD5, NOE3, TBB4B, ROCK1, GSH1, G3BP1, ATS1, TBB5, NF1, PGBM, IF2P, FA8, GDF3, KCMA1, ZCH18, TANC1, NSUN7, SHRM4, FAT4, IGFN1, HMHA1, FA98A, SCRN3, CH048, K22E, SHLD2, BIG3, SDK1, BAHC1, SLMAP, TBCD9, RIMB3, DYH12, ITAD, CKAP2, IGS10, A3LT2, ITA1, HERC2, XIRP2, TR150, IQEC2, LRC8B, FAT2, S39AC, VP13A, MTUS1, GSTCD, TENS3, ACACA, UTP20, KLRA4, PAPOA, STAR3, EWS, KTN1, GRID1, DDX5, CP131, SEM3B, TLL1, MINT, CCPG1, BTF3, TPP2, RBL1, COBA2, TASOR, PDS5A, CE290, NAL14, A2MG, ZZZ3, FREM2, CPSF6, RPRD2, HEAT6, P4R3A, FIL1L, SNX6, GAPD1, PTN23, TRI37, MON1A, MSL1, SARM1, CENPE, DAPLE, TIAM2, UBE2O, KDM3B, SYNE1, CMYA5, FHOD3, TBB2A, MYCB2, SGO2, MCAF1, STAR9, CAPS1, PHF8, CUL9, CLAP1, ST18, SGSM2, TAF1, M18BP, UBP2L, FLNB, OFD1, PTHB1, PDK1, TMCO3, NRDC, MARF1, TM87B, UNC80, TCAF1, KTU, UBP43, CAPS2, ZN609, DOCK2, RHG24, NAKD2, LENG8, UFL1, CD158, CLASR, SSPO, SLTM, NAV1, FBX4, RFWD3, MICA3, STAU2, NEIL3, CCD14, DDX18, UBP45, AL1L1, CCD80, TF2H3, FYCO1, HNRPU, DYH5, DHX36, AGRV1, FLNC, REST, NDUS1, CREL1, CELR3, DYST, BRWD1, GOGA2, PDIA6, TM1L1, RT4I1, CSTN3, PRP19, TARA, UBP16, NOG2, MYO7B, BCDO2, RTN4, RRBP1, ZN318, DHX30, MITOS, RBM33, NARF, KLH35, ACSL3, SYRC, C16L2, NBEA, TBB3, XPO4, RBCC1, LRP1B, CAC1F, PRG4, BIR1B, SRCN1, SHRM3, ING1, MACF1, ACL7A, SMK2B, H17B6, RPGR, RHG07, MAST1, ADA11, TIM, PFKAP, IRAG1, DEMA, P2R3D, SETBP, NEK4, PLD1
Species: Mus musculus
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Burt RA, Dejanovic B, Peckham HJ, Lee KA, Li X, Ounadjela JR, Rao A, Malaker SA, Carr SA, Myers SA. Novel Antibodies for the Simple and Efficient Enrichment of Native O-GlcNAc Modified Peptides. Molecular & cellular proteomics : MCP 2021 20 34678516
Abstract:
Antibodies against posttranslational modifications (PTMs) such as lysine acetylation, ubiquitin remnants, or phosphotyrosine have resulted in significant advances in our understanding of the fundamental roles of these PTMs in biology. However, the roles of a number of PTMs remain largely unexplored due to the lack of robust enrichment reagents. The addition of N-acetylglucosamine to serine and threonine residues (O-GlcNAc) by the O-GlcNAc transferase (OGT) is a PTM implicated in numerous biological processes and disease states but with limited techniques for its study. Here, we evaluate a new mixture of anti-O-GlcNAc monoclonal antibodies for the immunoprecipitation of native O-GlcNAcylated peptides from cells and tissues. The anti-O-GlcNAc antibodies display good sensitivity and high specificity toward O-GlcNAc-modified peptides and do not recognize O-GalNAc or GlcNAc in extended glycans. Applying this antibody-based enrichment strategy to synaptosomes from mouse brain tissue samples, we identified over 1300 unique O-GlcNAc-modified peptides and over 1000 sites using just a fraction of sample preparation and instrument time required in other landmark investigations of O-GlcNAcylation. Our rapid and robust method greatly simplifies the analysis of O-GlcNAc signaling and will help to elucidate the role of this challenging PTM in health and disease.
O-GlcNAc proteins:
IQIP1, A0A0A6YWG7, A0A0G2JF55, A0A0N4SW93, A0A0R4J060, A0A0U1RPL0, A0A140LIW3, A0A140T8K9, A0A1B0GS41, A0A1B0GS91, A0A1D5RMI8, A0A1L1M1J8, A0A1L1SR84, A0A1N9NPH8, A0A1Y7VNZ6, A0A286YDB3, A0JNY3, A2A482, A2A654, TANC2, LZTS3, AJM1, BCORL, A2AUD5, A2AWN8, B1ASA5, B1ATC3, B1AUX2, B2RQL0, CSPP1, B2RY58, B7ZNA5, CTTB2, D3YU22, D3YUV1, D3YWX2, D3YZ21, SHAN1, D3Z5K8, E0CXZ9, E9PU87, E9PUL3, PRRT2, E9PUR0, E9PV26, E9PVY8, SET1A, E9Q0N0, E9Q3E2, E9Q3G8, E9Q4K0, ARI1B, SETD2, E9Q6H8, E9Q6L9, E9Q828, E9Q9C0, E9Q9Y4, E9QAQ7, E9QAU4, E9QAU9, E9QKI2, E9QLZ9, E9QM77, F2Z3U3, F6RQA2, SYGP1, F7C376, BICRA, F8VQL9, F8WIS9, G3UZM1, G3X8R8, G3X928, RFIP2, H3BKF3, H3BKP8, H9KV00, J3QNT7, DPYL2, PRDX6, MNT, NUMBL, PEX5, BMPR2, CTND2, PITM1, ACK1, CAC1B, SYUA, DSG2, SPT5H, E41L2, SP3, KDM6A, CPNS1, ZFR, HCN1, CTBP1, BSN, STAM2, SYN1, MBP, EGR1, NFL, NFM, ITB1, RC3H2, ATX1L, RL7A, MAP1B, VIME, EIF3A, RGRF1, PABP1, FOXK1, EAA2, CBP, RFX1, SOX2, KPYM, CTBP2, GCP3, TB182, GMEB2, PI5PA, DOCK4, PCBP1, LIPA3, RS3, PAX6, KCNJ3, PP2BA, TBA4A, STAM1, NCOA1, CXB6, WNK1, PSME2, WBP2, SHPS1, NRSN1, CTNB1, PLAK, S30BP, NFIA, ZEP1, YES, CAPR2, MITF, GRD2I, Q0VF59, HDX, MA6D1, F171B, ZFHX2, MLXIP, PDLI7, PRC2C, CIART, YETS2, SRBP2, Q3U2K8, GSE1, RREB1, WNK2, DAB2P, ZEP2, AAK1, TNR6A, GRIN1, SRBS2, GRM5, Q3UZG4, RBM44, Q3ZB57, PHAR4, RESF1, Q5EBP8, UNKL, VP13A, COBL, KDM6B, PRSR1, Q5RIM6, SMG7, RBM27, TM1L2, Q5SVJ0, Q5SXC4, SIN3A, GAS7, CAPR1, KLF3, SIX4, AP180, GRID2, PACN1, LASP1, RAI1, NOTC3, SALL3, SPTB2, ARI3A, NUP62, PHC1, TFE3, PAN3, TIF1A, SF01, SYN2, SBNO1, CRTC1, RIPR1, GIT1, PKP4, ABLM3, ARMX2, CE170, Q6AXD2, NIPBL, FBX41, RPRD2, WWC2, Q6P1J1, Q6P5E3, UGGG1, SPRE3, Q6P9N8, AHDC1, PTN23, TRAK1, DLGP3, NYAP1, DHX29, NFRKB, MAGI1, Q6XZL8, CNOT1, SYNE2, IF2A, PICAL, PLPR4, PLPR3, CCNT2, PRC2A, MAP6, MCAF1, RERE, NU214, SESD1, UBP2L, C2C2L, CNKR2, SLIK5, RHG32, LPP, NELFA, C42S2, TB10B, TGO1, RFOX3, SP130, ANS1B, ZC3HE, ZC21A, BAIP2, EMSY, KAT6B, RELL2, LIPA2, CNOT4, TOX4, GASP2, CREST, KDM4A, GRIN3, KAT6A, ZN609, PAK5, A16L1, SI1L1, SH3R3, SKA3, RBM14, Q8C5J0, CNOT2, WDR26, UBA6, ANK2, DIDO1, SYNPO, VCIP1, FHI2A, NUP88, NED4L, SET1B, TNS2, OGT1, NAV1, STAU2, AFG32, S4A8, ZBT20, HS12A, GLT18, UNC5A, AGFG1, FRRS1, KCNQ3, PO121, T2FB, MTSS1, Q8R2E1, NUP35, MAVS, SGIP1, HNRL1, PP16B, CCG8, SFPQ, UBAP2, NCOA5, AJUBA, DCP1A, TWF1, ALS2, ETFD, CIC, GRIP1, GORS2, NONO, ZN281, CT2NL, RN111, ANR17, RTN4, PPP6, RBM7, CYGB, SARNP, DLGP1, SUN1, TM263, GON4L, PLIN3, MYPT1, NBEA, RENT1, ZN704, RBP2, ARHG7, RTN3, NUDT3, TULP4, Q9JIZ5, PAR6G, SCAM5, PRG4, ZN207, SRCN1, ASAP1, DREB, ULK2, ADDA, PCLO, UBQL2, FBX6, PCM1, SYT7, CRY2, FOXO1, MAST1, LYPA2, TEN3, GANP, DEMA, E41L3, ZO2, BAG6, E41L1, RM40, GRIA3, S4R294, V9GWU7, V9GX40
Species: Mus musculus
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Huynh VN, Wang S, Ouyang X, Wani WY, Johnson MS, Chacko BK, Jegga AG, Qian WJ, Chatham JC, Darley-Usmar VM, Zhang J. Defining the Dynamic Regulation of O-GlcNAc Proteome in the Mouse Cortex---the O-GlcNAcylation of Synaptic and Trafficking Proteins Related to Neurodegenerative Diseases. Frontiers in aging 2021 2 35822049
Abstract:
O-linked conjugation of ß-N-acetyl-glucosamine (O-GlcNAc) to serine and threonine residues is a post-translational modification process that senses nutrient availability and cellular stress and regulates diverse biological processes that are involved in neurodegenerative diseases and provide potential targets for therapeutics development. However, very little is known of the networks involved in the brain that are responsive to changes in the O-GlcNAc proteome. Pharmacological increase of protein O-GlcNAcylation by Thiamet G (TG) has been shown to decrease tau phosphorylation and neurotoxicity, and proposed as a therapy in Alzheimer's disease (AD). However, acute TG exposure impairs learning and memory, and protein O-GlcNAcylation is increased in the aging rat brain and in Parkinson's disease (PD) brains. To define the cortical O-GlcNAc proteome that responds to TG, we injected young adult mice with either saline or TG and performed mass spectrometry analysis for detection of O-GlcNAcylated peptides. This approach identified 506 unique peptides corresponding to 278 proteins that are O-GlcNAcylated. Of the 506 unique peptides, 85 peptides are elevated by > 1.5 fold in O-GlcNAcylation levels in response to TG. Using pathway analyses, we found TG-dependent enrichment of O-GlcNAcylated synaptic proteins, trafficking, Notch/Wnt signaling, HDAC signaling, and circadian clock proteins. Significant changes in the O-GlcNAcylation of DNAJC6/AUXI, and PICALM, proteins that are risk factors for PD and/or AD respectively, were detected. We compared our study with two key prior O-GlcNAc proteome studies using mouse cerebral tissue and human AD brains. Among those identified to be increased by TG, 15 are also identified to be increased in human AD brains compared to control, including those involved in cytoskeleton, autophagy, chromatin organization and mitochondrial dysfunction. These studies provide insights regarding neurodegenerative diseases therapeutic targets.
O-GlcNAc proteins:
TANC2, AMRA1, CAMP1, SKT, AGRIN, KANL3, TTLL3, NHSL2, CTTB2, CCDC6, SHAN1, SYGP1, DPYL2, STXB1, CLOCK, NOTC2, VIAAT, CTND2, TPD53, REPS1, NLK, ACK1, SYUA, ATX2, PDLI1, ZFR, HCN1, BSN, TOM1, SYN1, GCR, EGR1, NFL, NFM, ATX1L, DERPC, KCC2A, CNTN1, HSPB1, MAP1B, G3P, ATF2, MTAP2, RS2, FOXK1, STAT3, AINX, EPB41, RFX1, LMNA, INPP, VATA, DVL1, CNBP, ATX1, NCAN, GOGA3, PTPA, GCP3, TB182, GMEB2, YTHD1, PI5PA, MRTFB, LIPA3, NACAM, TNIK, WNK1, NPTN, NEO1, S30BP, ZEP1, APOC2, EMAL1, RELCH, PRC2C, YETS2, FUBP2, QRIC1, LIMC1, DAB2P, ZEP2, AAK1, TNR6A, FCHO2, DRC1, SRBS2, GRM5, PACS2, OXR1, PHAR4, LIN54, MLIP, UNKL, SMG7, RBM27, CYFP2, SYNRG, SRC8, SKIL, NCOR1, LAMA5, HCFC1, P3C2A, SAP, APC, TOB1, AP180, FXR1, HS71A, LASP1, MAFK, M3K7, TAF6, ASPP1, SRBS1, DBNL, SH3G1, TLE4, IF4G2, MINT, ZYX, NUP62, OMGP, TFE3, SYN2, TBR1, RBL2, SBNO1, SLAI1, PKP4, SH3R1, JHD2C, ABLM3, ARMX2, LAR4B, HELZ, S23IP, RBM26, BCR, AHDC1, PAPD7, MFF, KMT2D, ERC2, NFRKB, WDFY3, GGYF2, TEX2, CNOT1, IF2A, PICAL, PLPR3, PRC2B, C2CD5, TPPP, ATX2L, MAP6, NAV3, AUXI, RIMB2, AVL9, NU214, AP4E1, UBP2L, C2C2L, IF4G3, ZN598, SHAN2, LPP, MYPT2, PHIPL, TB10B, CCD40, ZC3HE, DLGP2, ZC21A, BAIP2, EMSY, CLAP2, LIPA2, SRRM2, PAMR1, GEPH, YTHD3, POGZ, EPC2, SI1L1, RBM14, F126B, ANK2, CDAN1, SYNPO, VCIP1, TAB1, MEF2C, F193A, OGT1, EP400, EPN2, P66A, PDLI5, GTPBA, ZBT20, RTN1, BRD3, AGFG1, ABLM1, MRTFA, DC1L1, SPART, RFIP5, NUP35, WASF1, SC6A8, SGIP1, AGAP3, P66B, TAF9, WDR13, LRP5, UBAP2, BASP1, DCP1A, SYUB, TRFE, TRIM7, CIC, S12A6, GORS2, TAB2, EPN4, RNF34, ANR17, NECP1, FLIP1, ROA0, RBM33, TPD54, ODO2, DLGP1, FIP1, TM263, PLIN3, LNEBL, KC1D, NBEA, INP4A, RIMS2, RBP2, RTN3, NUDT3, ATR, ADRM1, FMN2, NCOA6, SON, ULK2, ADDA, MAGD1, MAP1A, GRM3, PCLO, GAB1, FBX6, NPAS3, GUAD, NCOR2, ATRN, NFAT5, DEMA, E41L3, SLIT3, CARM1, DYR1B, MECP2, E41L1, HDAC6
Species: Mus musculus
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Lee BE, Kim HY, Kim HJ, Jeong H, Kim BG, Lee HE, Lee J, Kim HB, Lee SE, Yang YR, Yi EC, Hanover JA, Myung K, Suh PG, Kwon T, Kim JI. O-GlcNAcylation regulates dopamine neuron function, survival and degeneration in Parkinson disease. Brain : a journal of neurology 2020 143(12) 33300544
Abstract:
The dopamine system in the midbrain is essential for volitional movement, action selection, and reward-related learning. Despite its versatile roles, it contains only a small set of neurons in the brainstem. These dopamine neurons are especially susceptible to Parkinson's disease and prematurely degenerate in the course of disease progression, while the discovery of new therapeutic interventions has been disappointingly unsuccessful. Here, we show that O-GlcNAcylation, an essential post-translational modification in various types of cells, is critical for the physiological function and survival of dopamine neurons. Bidirectional modulation of O-GlcNAcylation importantly regulates dopamine neurons at the molecular, synaptic, cellular, and behavioural levels. Remarkably, genetic and pharmacological upregulation of O-GlcNAcylation mitigates neurodegeneration, synaptic impairments, and motor deficits in an animal model of Parkinson's disease. These findings provide insights into the functional importance of O-GlcNAcylation in the dopamine system, which may be utilized to protect dopamine neurons against Parkinson's disease pathology.
O-GlcNAc proteins:
BIG2, F1712, VIR, AJM1, RPGP1, UBR4, SCN1A, AGRIN, TITIN, KALRN, STPG3, FXL16, TT23L, PTPRS, GRIK3, SCN2A, DLGP4, OSBL8, PTPRZ, PGBD5, GLSK, GCN1, CE350, PI4KA, RYR2, AGRF2, UBE4A, NRX2A, FRY, SYGP1, OTOGL, AT2B1, ANK3, CA2D1, DPYL2, STXB1, DCTN1, U5S1, GFRA2, GALT1, SEM4D, KIF3C, PLCA, PHB2, NCAM2, GRAK, PURB, IMA3, IMA7, PLD3, FOLH1, FKBP8, STX1A, PSDE, VIAAT, AP1B1, C1QBP, SYT3, HNRH1, SATT, CTND2, SDC4, AP3D1, RGS9, RGS7, CSK22, OX2G, AAKG1, CRYM, PROM1, CNTP1, ENTP2, BCKD, SNG1, NIPS1, NIPS2, SEPT7, AT2A2, DHX9, PI51C, PI42A, ITB5, GPX4, NPTX2, GNAZ, WDR1, S4A4, MTX2, CNTFR, ZFR, CSN3, HCN2, HCN1, CTBP1, BSN, MPP3, NOE1, CBPD, LGMN, COR1A, CYB, COX1, COX2, COX3, HPRT, ATP6, THY1, H3C, LAMC1, NU1M, NU2M, NU4M, NU5M, ATP8, GFAP, MBP, PRIO, ALDOA, KAPCA, AATM, TBA1B, TBA3, KIT, LDHA, G6PI, MDR1B, ENPP1, HS90A, ENPL, KCC4, NFL, NFM, RASN, PGK2, ITB1, PPBT, NUCL, PGK1, ACE, LRC4B, UBB, UBC, EF1A1, IF4A2, GSTM1, 4F2, H10, LAMP1, HS90B, L1CAM, ITA5, KCC2A, ITB2, ITPR1, TCPA, PFKAL, CNTN1, NCAM1, AT1B1, C1QB, RS16, RL7, AT1B2, PSMD3, MAP1B, GLNA, CADH2, INSR, NTRK2, KCNC1, SPTB1, H12, KPCE, LDHB, CN37, DDX3L, KCNA1, KCNA3, AMPE, ASSY, SPTN1, G3P, LAMP2, ENOA, AP2A1, AP2A2, HXK1, GTR1, PTPRA, COF1, GNAO, FAS, LAMA1, NFH, COX41, BIP, HEXB, VIME, MTAP2, MAG, GNA11, GNAQ, MDR1A, ACES, GBRG2, AP1G1, GBRD, EIF3A, CXA1, GRIA1, GRIA2, TY3H, RS2, GBRA2, RL3, BRAF, KCC2B, NP1L1, NCKP1, SNAB, KIF2A, KIF3A, PABP1, GBB4, KCRU, GNA14, KAP3, SC6A1, S6A11, MP2K1, GTR3, LA, RASK, SYWC, KIF1A, HYES, RAB3D, RAB5C, RAB6A, RAB21, NMDZ1, ODPA, RET, FBRL, KCNJ2, CD81, GPM6A, GPM6B, GNL1, DYN1, DYN2, GRIK2, CAP1, ABCA2, PURA, HD, EAA2, H14, H15, H13, ITAV, SYT1, NSF, RB11B, AINX, MYO1B, NEDD4, ALDH2, GRM8, CAZA2, CAPZB, MP2K4, PFKAM, RL6, RL29, RL5, GLRB, DCE1, DCE2, CBR1, GSTM5, ADT1, INPP, CDK5, SAHH, GDIA, VATA, VATE1, GBRB1, RAB7A, ACADL, VA0D1, ADT2, EAA3, KCNJ4, KPYM, RAB2A, PRS6B, PTN5, NCAN, ABCD3, RAB8A, ATPK, ATP5E, UBP5, ATPB, CTBP2, EAA1, WFS1, FUS, NICA, ACTN4, ASM3B, EF2, OPA1, DOCK4, IRPL1, ARPC4, MYPR, PLPP, ACTB, MDGA2, NEUG, RAC3, IF4A1, MEGF8, RAB5B, RAB10, RAB8B, ARP2, ACTZ, CSN2, ARF3, ARL1, CAH10, RAP2B, STX1B, RAB6B, RL27, ARF4, GABT, HNRPK, 1433G, RS7, PP1A, RS8, SMD1, KCAB2, ABI2, RB11A, EF1A2, RS4X, PP2AB, RL18A, ACTA, AP2S1, RL23A, VISL1, H4, GBRA1, VATB2, RAB1A, RAB3C, RAN, RAP1A, RS24, GBB1, GBB2, RS3, RL8, RS27A, RL40, RAC1, RAB3A, HSP7C, CH60, VAMP2, NOE3, GBRB3, VATL, PP1G, 1433Z, GBRB2, KCNA2, KCAB1, CRNL1, DYL1, ACTG, ACTH, KPCG, PP2BA, PP2AA, PHB, CSK2B, ACTC, RACK1, ACTS, KAPCB, TBA4A, TBA1A, TBB4B, KPCB, H31, IMB1, PLXA1, PLXA2, PLXA3, DCC, ITPR3, NCHL1, HNRH2, ELAV1, USP9X, IDHG1, LYAG, AT8A1, TCPH, TCPB, TCPD, TCPE, TCPZ, TCPG, TNIK, WNK1, RL36A, ARF1, ARF5, AP2M1, H32, H33, ADCY5, NPTN, RS3A, AT1B3, DPYL1, ZNT3, GRM1, SHPS1, NEO1, FUMH, M4K4, C1QA, TBB5, PDE4D, PDE1B, NMDE2, SC23A, TERA, C1QC, CTNB1, PLAK, EPHA4, MARK3, ATPA, CHLE, KCND1, KCRB, NF1, CDK18, RAC2, MARK2, PGBM, PTPRG, PYC, KCMA1, PADI2, INF2, TRIO, MDGA1, CTP5A, ITB8, PSA, GRM2, PTCD3, PHAR1, LRFN1, SPP2B, HP1B3, NLRX1, PRC2C, TM38A, VGLU1, BIG3, PLXD1, AGAP2, AAK1, TEN4, CAMKV, DOP2, RMD3, SMU1, MCCB, GPD1L, LIGO2, SRBS2, CDKL5, K22O, VPS51, GRM5, CBAR2, SHAN3, UN13A, SE6L2, KCTD8, KCD16, LRC8B, VP13A, C2C4C, S2551, MRS2, DIRA2, CYFP2, TM1L2, RHG44, MYO1D, RABL6, DJC11, UIMC1, ICAM5, FLOT2, HNRPD, PTPRN, CSK21, KHDR1, IGF1R, CLD11, SPB6, ARHG2, VDAC2, VDAC3, VDAC1, ABCB7, ASTN1, P3C2A, CAC1E, LAMB2, CTNA2, SC6A3, CNTN2, PGCB, NEP, KCNA4, CD166, 5NTD, GSLG1, EWS, AP180, FSCN1, GDIB, GRIK5, GRID1, DDX5, HS105, ITIH3, IL1AP, CD47, KINH, KIF3B, LASP1, MYH10, MOG, NPM, PCBP2, CSPG2, DDX3Y, DLG4, RHOC, DAG1, DDX3X, SYPH, TICN1, NDUA4, NPTX1, NUP62, OMGP, HECAM, AOFA, ARP3B, SURF4, SYN2, CP3AD, H2B1H, GLPK, SDC3, GPDM, H2A2C, H2B2B, GRM7, GRM4, CLH1, K1549, GIT1, PKP4, PPR29, CNTN4, NLGN2, SV2C, THS7A, CE170, UBP7, BRNP2, SCMC3, LIGO3, DGKB, RPRD2, DPP10, S23IP, PPRC1, 2ABA, TNPO3, SIK3, U520, S39AA, TTYH3, XPO1, SPCS, KCRS, CSKI1, NRX3A, BCR, SARM1, PRRT3, TEFF1, RAB35, CA2D2, KCC2D, AT1A3, AT1A2, GNAS1, SDK2, WDFY3, NTRK3, RAD9B, DGLA, KCD12, MTMR5, UBE2O, CAND1, UBP34, RS9, 2ABB, H2B1C, TLN2, CSPG5, 2AAA, NP1L4, MTCH2, OPALI, CYFP1, TBB2A, HUWE1, IGS21, ROBO2, ACTN1, IGSF1, TR143, TPPP, OTUB1, KPBB, PP6R1, MAP6, ELP1, RRAGD, MRCKB, GABR2, CSMD3, EPT1, VAT1L, LRRC7, CAPS1, CYLD, AGRL1, AGRL3, CLAP1, AUXI, DAAM2, MADD, MFN2, NU214, UBE3C, PLXA4, FBX2, KCMF1, CBPM, GSTM7, AGFG2, LRC8A, HPLN4, VAC14, UBP2L, C2C2L, LRRT4, BDH, MK15, CNKR2, TENA, ASTN2, NEGR1, RAP2A, THEM6, SLIK5, SLIK4, SLIK3, SLIK2, NFASC, NRCAM, RHG32, SRGP3, EFTU, VGLU3, ERLN2, ROA3, SV2B, MIRO1, EFR3A, LRRT2, U2AF4, ENPP6, SYAC, FLRT3, CBLN2, LRTM2, HPCL4, COR2B, CMC1, ATLA1, NU107, RB39B, RB39A, ZN526, ANS1B, DLGP2, AHSA1, IPO5, NCEH1, LSAMP, CADM2, NOE2, ODP2, RBGPR, ECHA, SPA2L, SYNC, RL24, DAAM1, DMXL2, RLGPB, CLAP2, VMAT2, ARF2, NDRG4, ENPP4, HSDL1, RAP2C, GEPH, VATH, PMGT2, TTC12, AOFB, LRFN5, PIGT, CTL2, TENR, NLGN3, LRRT3, DYN3, LRC4C, ARHGA, SYFA, SI1L1, LCAP, EXOG, CERS6, SEP11, IKZF4, GP158, CWC22, VPS52, SCAI, ANK2, PDE10, PGM2L, SHFL, MIC60, WDR37, ABI1, SYNPO, T132C, GLT13,