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Jaiswal R, Liu Y, Petriello M, Zhang X, Yi Z, Fehl C. A reference dataset of O-GlcNAc proteins in quadriceps skeletal muscle from mice. Glycobiology 2025 35(3) 39927985
Abstract:
A key nutrient sensing process in all animal tissues is the dynamic attachment of O-linked N-acetylglucosamine (O-GlcNAc). Determining the targets and roles of O-GlcNAc glycoproteins has the potential to reveal insights into healthy and diseased metabolic states. In cell studies, thousands of proteins are known to be O-GlcNAcylated, but reference datasets for most tissue types in animals are lacking. Here, we apply a chemoenzymatic labeling study to compile a high coverage dataset of quadriceps skeletal muscle O-GlcNAc glycoproteins from mice. Our dataset contains over 550 proteins, and > 80% of the dataset matched known O-GlcNAc proteins. This dataset was further annotated via bioinformatics, revealing the distribution, protein interactions, and gene ontology (GO) functions of these skeletal muscle proteins. We compared these quadriceps glycoproteins with a high-coverage O-GlcNAc enrichment profile from mouse hearts and describe the key overlap and differences between these tissue types. Quadriceps muscles can be used for biopsies, so we envision this dataset to have potential biomedical relevance in detecting aberrant glycoproteins in metabolic diseases and physiological studies. This new knowledge adds to the growing collection of tissues with high-coverage O-GlcNAc profiles, which we anticipate will further the systems biology of O-GlcNAc mechanisms, functions, and roles in disease.
O-GlcNAc proteins:
A0A087WS16, A0A0N4SUN5, A0A286YCS6, A0A5F8MPM4, A0A5F8MPQ4, A0A668KL51, A0A7N9VR94, A2A6J0, A2A6Q8, OBSCN, A2AEX6, A2AI87, A2AKD7, TITIN, KLH41, ARMT1, OSBL8, SHAN1, D3Z0V7, D3Z2B4, CD054, E0CZE0, E9PYG6, E9PYI8, E9PZD8, RYR1, E9Q1W3, NU153, E9Q3P4, RN213, E9Q616, TRDN, E9QL12, E9QN70, E9QND8, F6QYF8, F6VY18, F6YT88, F8VPN4, F8WGD9, MYH2, G3UYC5, RGS22, G3X972, AT2B1, G5E895, G5E8L1, G5E8R7, H7BWZ9, J3QN31, M0QW57, HXK2, CA2D1, PRDX6, DLDH, HCD2, MK12, SYPL1, CASQ1, PHB2, CAN1, CALU, CAVN1, IMPA1, NIPS2, AT2A2, PDLI3, PGAM2, PDLI1, RTN2, NTR1, WDR1, PLIN4, ZFR, SEM3F, ACTN3, SYPL2, CAH2, CO3, LAMC1, NU5M, ATP8, FABP4, MYG, ALDOA, KAPCA, AATC, AATM, TBA3, LDHA, MAOX, KCRM, ANXA2, A1AT1, SPA3K, HS90A, PHKG1, SODC, MDHM, ITB1, PDIA1, PGK1, MYL3, SODM, UBB, CALM3, ANXA1, EF1A1, CATB, TAU, GSTM1, H2B1F, H10, FINC, FABPH, DMD, COX5A, TNNI2, MYH3, MYH8, CAH1, GPDA, RL7, MDHC, HSPB1, ANXA6, GLNA, B4GT1, H12, CAH3, LEG1, LDHB, HS71L, G3P, ENOA, PPIA, TPIS, CATD, COF1, FAS, GSTP1, SERPH, COX5B, COX41, BIP, VIME, TNNC2, PLMN, ENOB, VTDB, CLK1, EST1C, RS2, TLN1, RADI, DHE3, FKB1A, MAP4, PLAP, PDIA3, ADHX, KCC2B, PGS2, MUG1, PABP1, DESM, AIMP1, PRVA, UBP4, ODPA, FAAA, PRDX1, RL12, HSPA9, CAP1, ACSL1, ECI1, STA5B, H14, H11, H15, H13, ALDR, COF2, ACADM, MYO1B, ALDH2, CAZA2, PFKAM, CACP, RL5, CBR1, ADT1, SAHH, CSRP3, ACADV, FMOD, ACADL, CAV3, ADT2, EAA3, AAAT, KPYM, CPT2, ODB2, MOT1, IDHP, STMN1, RD23B, PUR8, ADK, ACYP2, CX6B1, UBP5, ATPB, UCP3, EF2, TPM1, IRPL1, ACTB, CDC42, RAB5B, RAB10, UB2D1, 1433G, RS7, PP1B, 1433E, RS11, EF1A2, H4, RAB1A, RAN, RL23, CYC, RS3, YBOX1, RAC1, LIS1, HSP7C, CH60, 1433Z, HMGB1, IF5A1, ACTS, TBA4A, TBB4B, MP2K6, PEBP1, STIM1, HINT1, MYBPH, NACAM, TCPH, TCPB, TCPD, TCPE, TCPZ, SGCB, WNK1, ARF5, ISC2A, CSRP1, RS3A, SPSY, MYL11, FUMH, LYPA1, ARVC, PRDX5, XDH, NDKB, TERA, UBA1, CAC1S, ATPA, CO6A1, PGBM, PYC, ACADS, KCMA1, PADI2, CD36, Q14BI5, FAT4, CNNM3, Q3TCF3, PDLI7, PRC2C, SCRN3, DDB1, K0930, Q3UER8, LIMC1, PRRC1, EID3, AMPD1, Q561M1, MYPN, Q5F247, MLIP, Q5MJ56, CLU, MYH4, MYH1, UBR3, MYPC2, ODO1, LAMA2, COCA1, STIP1, REEP5, VDAC2, VDAC3, VDAC1, COQ8A, PRDX2, HCFC1, LAMB2, HSP74, HCDH, FBN1, GDIB, PZP, NNTM, DDX3X, MYOM1, SPEG, NDUA4, NUP62, AT2A3, GPDM, VINC, PUR2, CLH1, MYOF, HECD1, F120A, HELZ, Q6NVF7, IF4G1, Q6P1B9, Q6P6L5, KCRS, LPPRC, KMT2D, AT1A2, Q6S9I0, CAND1, CAND2, CMYA5, VWA2, TLN2, 2AAA, MIC27, Q7TPG0, MBB1A, SRCA, ATX2L, Q7TQS8, KPBB, Q80T54, NU214, PANK4, Q810Q0, EFTU, H2A3, LPP, PSD11, S2512, ECHM, EIF2A, ODPX, MAON, ODP2, ECHA, Q8BPI2, Q8BUY2, DHPR, SYP2L, THIM, STAC3, ASGL1, TLK1, PRR33, STBD1, MIC60, SYNPO, CPLN1, SYEP, UN45B, PGP, DRS7C, EI2BE, PDLI5, AGO3, EFGM, FIBB, COQ9, SDHA, VRK3, NNRE, HIBCH, THIL, AIMP2, BLMH, CMBL, UBQL1, TSN8, SLF1, CACB1, AT2A1, CLYBL, PRAF3, LSM1, MAVS, MYLK2, EST1D, MYH9, PSMD2, HNRL1, LMCD1, HNRPU, S25A3, FLNC, NDUS1, RINI, ATPG, DDX1, UBAP2, NDUS2, CISD1, SH319, HEMO, SYNP2, NDUV1, MYH7, PCCA, UGPA, ETFD, MACD1, C1TC, CLIP1, MPI, CPT1B, TALDO, THTM, GORS2, ECHB, ACON, NAMPT, 3HIDH, DHRS4, NDUAA, ETFA, PARK7, ASPN, MCCA, PPR3A, GDIR1, LGUL, NDUC2, DECR, NDUA2, SDHB, TMED6, GLRX3, AT5F1, ACO13, RL14, NDUB7, M2OM, UCRI, CHSP1, SFT2C, PUR9, SGT1, CENPV, SERB1, SPCS2, QCR1, NSF1C, CISY, ODPB, PGM1, SCOT1, GAL3A, RAB1B, ODO2, NDUV2, FUND2, IDH3A, RL4, EF1G, CA074, ATPO, PXL2B, QCR2, ACDSB, MYPT1, Q9DBT6, DCAF6, OCTC, NDUA9, NDUA8, PUR6, NDUBA, NDUS3, ETFB, ATP5H, MIC26, MMSA, RB27A, JPH2, JPH1, IVD, DYHC1, NIT2, ACTN2, MYOTI, PROF2, MYOZ1, PRELP, YBOX3, MBNL1, LDB3, HIG1A, TRXR1, B4GT5, PPCE, PLEC, S2513, NDRG2, DNJA2, UBQL2, FHL3, GLYG, ESTD, KAD1, PDC6I, PYGM, SUCA, ECI2, SH3BG, ARC1B, ABEC2, VAPA, AIFM1, GYS1, STRAP, LETM1, SUCB1, S4R1W1
Species: Mus musculus
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Shu XE, Mao Y, Jia L, Qian SB. Dynamic eIF3a O-GlcNAcylation controls translation reinitiation during nutrient stress. Nature chemical biology 2022 18(2) 34887587
Abstract:
In eukaryotic cells, many messenger RNAs (mRNAs) possess upstream open reading frames (uORFs) in addition to the main coding region. After uORF translation, the ribosome could either recycle at the stop codon or resume scanning for downstream start codons in a process known as reinitiation. Accumulating evidence suggests that some initiation factors, including eukaryotic initiation factor 3 (eIF3), linger on the early elongating ribosome, forming an eIF3-80S complex. Very little is known about how eIF3 is carried along with the 80S during elongation and whether the eIF3-80S association is subject to regulation. Here, we report that eIF3a undergoes dynamic O-linked N-acetylglucosamine (O-GlcNAc) modification in response to nutrient starvation. Stress-induced de-O-GlcNAcylation promotes eIF3 retention on the elongating ribosome and facilitates activating transcription factor 4 (ATF4) reinitiation. Eliminating the modification site from eIF3a via CRISPR genome editing induces ATF4 reinitiation even under the nutrient-rich condition. Our findings illustrate a mechanism in balancing ribosome recycling and reinitiation, thereby linking the nutrient stress response and translational reprogramming.
O-GlcNAc proteins:
A0A075B5P4, A0A087WNV1, A0A087WPT1, A0A087WQF8, A0A087WS88, A0A0A0MQM6, A0A0A6YVP0, A0A0A6YY72, A0A0B4J1E2, A0A0G2JFJ6, A0A0G2JFN8, A0A0G2JFY0, A0A0G2JG10, A0A0G2JG59, A0A0G2JG60, A0A0G2JG65, A0A0G2JGL8, A0A0H2UH17, A0A0J9YTU3, A0A0J9YUT8, A0A0J9YUY8, A0A0N4SV00, A0A0N4SV32, A0A0N4SW94, A0A0N5E9G7, A0A0R4J060, A0A0R4J169, A0A0R4J1E3, A0A0R4J1Y4, A0A0R4J260, A1BN54, A1L341, A1L3S7, A2A485, A2A513, A2A5N3, A2A8V8, A2AGK3, LZTS3, A2AM70, A2AMY5, A2APQ6, A2AS44, A2AVJ7, A2AWT6, A2BGG7, K1C28, A6X8Z3, A8Y5K6, B0V2N8, B1AU25, TBD2A, THOC2, TPC11, PLXB2, RBM25, B7FAU9, B7ZWM8, B8JK33, B9EHJ3, D3YTT9, D3YUW7, D3YV30, D3YV43, D3YVH4, D3YX49, D3YX64, D3YX85, SAFB1, D3YYT0, D3YZ62, D3YZL1, D3YZT4, D3Z1X3, D3Z2H7, D3Z3E8, D3Z4B0, CCD78, D3Z6N3, CILP2, D6RCG1, E0CY31, E0CYH0, E9PUA5, E9PUJ2, E9PUX0, GCN1, E9PVC6, E9PVG8, KI67, E9PW24, E9PYF4, SET1A, E9PYI8, E9PZW0, E9Q066, E9Q0F0, E9Q0M9, E9Q0U7, E9Q0Y4, E9Q133, E9Q166, E9Q175, E9Q1Z0, E9Q2X6, NU153, NOLC1, E9Q5F6, E9Q616, MYO1E, E9Q6A9, E9Q6M7, E9Q6T8, E9Q8F0, E9Q9C7, E9Q9H2, E9QA74, E9QAT0, E9QKG6, E9QLM4, E9QN31, E9QNH6, E9QNN1, E9QPE7, E9QPI5, F2Z480, F6S6G6, F6T0G2, F6TFN2, F6TW20, F6WTC8, F6XWD4, F6YRW4, F6YUI5, F7B296, F7C312, FARP1, F8VPX1, F8VQ29, F8WHR6, G3UWP5, G3UWZ0, G3UX48, G3UYD0, G3UYG6, G3UYW3, G3UYZ0, G3X8P9, G3X8Q0, G3X956, SI1L3, G5E839, G5E846, G5E866, G5E879, G5E8C3, G5E8J8, G5E8N3, G5E8T6, H3BJU7, H3BKF6, H3BKM0, H3BKN0, H3BKT5, H3BL49, J3QMC5, J3QNW0, CAN2, ATN1, SRSF5, IMA3, PININ, EIF3D, ATX2, E41L2, UGDH, SP3, IF2B1, ZFR, HIPK1, IGKC, IGHG1, HBA, K2C1, TBA1B, ALBU, HS90A, NUCL, ATX1L, EF1A1, H2B1F, CO1A1, HS90B, TCPA, GELS, HS71L, AP2A2, K1C19, BIP, VIME, MFGM, EIF3A, MCM3, MOES, CTNA1, U2AF2, PDIA3, GRN, PABP1, FKBP4, KIF4, TSP1, HSPA9, TKT, BCL6, FOXK1, H14, NEDD4, LMNA, MCM5, K2C6A, IMA1, KPYM, DDX6, ACTN4, EF2, ASXL1, ACTB, ABCE1, RRAS2, H4, HSP7C, CH60, TBA1A, TBB4B, H31, IMB1, TCPB, TCPE, TCPZ, WNK1, H32, MPRIP, G3BP1, TBB5, HNRL2, TOP2A, UBA1, PLAK, IF2P, EPS8, LRIQ1, ZCH18, LMTD2, FA83H, CDCA2, CYTSA, SPP2B, Q3TJ56, K22E, FUBP2, Q3U6F1, Q3U8S1, FOXK2, Q3UID0, Q3UJB0, Q3UNN4, SFSWA, K22O, CFA74, Q3UYN2, LRRF1, ESF1, KIF22, Q3V3Y9, Q45VK5, Q4FJZ2, Q4KL80, Q4TU83, PDS5B, DDX17, LRC47, Q52KR6, TR150, NEXMI, JCAD, NUFP2, PRSR1, RBM27, PHF12, UTP18, LC7L3, Q5SUT0, TSR1, MYO1D, Q5U4C5, SIN3A, SRC8, MYL6, STIP1, CAPR1, IMA5, LAP2A, HCFC1, K1C15, SMRD1, FXR1, DDX5, HS71A, SERA, KINH, MYH10, SIN3B, DDX3X, TIF1B, NUP62, K1C12, SQSTM, TOP2B, Q68EM3, CLH1, CDC5L, F120A, CNDG2, NOP58, SCAF8, K1C42, K2C1B, SR140, ZC11A, ABCF1, RRP12, Q6P5B5, UGGG1, XPO1, KIF11, FHOD1, LPPRC, NUP98, Q6PGF5, NEB2, DAPLE, UBE2O, LARP1, NU188, WDR43, 2AAA, Q792Z1, UHRF2, MBB1A, Q7TQE2, NU214, WNK4, KIRR1, FLNB, WNK3, Q80ZX0, LPP, ACTBL, P4HTM, MYPT2, HTSF1, IF4B, NU107, WDR3, NOC4L, CE128, NUP93, SUN2, RCC2, SYLC, CKAP4, SRRM2, NUP54, PWP2, SYIC, RL1D1, MAP1S, TTC34, SI1L1, RBM14, Q8C872, DIDO1, ATAD2, NUP88, Q8CFQ9, SMC2, UACA, SYEP, TCRG1, OGT1, CCAR1, SLTM, BICRL, P66A, COPA, HMCS1, Q8JZN2, EIF3B, BCLF1, PHLB2, NAT10, ANLN, SDHA, LS14A, MATR3, DDX18, PO121, EIF3L, HNRPL, NU133, EIF3C, ZC3HA, TDIF2, NUP58, CD109, LUZP1, UTP6, MYH9, UHRF1, VIGLN, CCAR2, CUL7, K2C79, Q8VGW3, DHX36, SFPQ, ACLY, DDX1, U3IP2, SYYC, RPN1, YTHD2, BMP2K, SNX18, SMCA5, Q921K2, SF3B3, DDX27, Q921S6, SMTN, PP6R3, K2C5, DEN2B, NXF1, NONO, ACON, NMD3, RTCB, CT2NL, HSP7E, NU155, IF2B3, Q9CPN9, SMC1A, SMC3, CXXC1, GARS, CEP72, SC23B, Q9D6D0, NOP56, FIP1, SPB1, MYPT1, NVL, EIF3F, RAI14, CPSF1, PESC, VPS35, LIMA1, DKC1, PALLD, NUP50, DDX21, FLII, YBOX3, IQGA1, Q9QUK9, CAF1A, K1C17, MAGD1, MTA2, PR40A, MYO1C, COR1C, E41L3, EHD1, WDR46, ZO2, NU160, ADNP, SYVC, Q9Z1R9, BAZ1B, K1C16, SNUT1, S4R2A9, S4R2J9, V9GX87
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, E9PUL3, PRRT2, E9PUR0, E9PV26, E9PVY8, SET1A, E9Q0N0, E9Q3E2, NU153, 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, 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, PLPR4, PLPR3, CCNT2, PRC2A, MAP6, MCAF1, RERE, NU214, SESD1, C2C2L, CNKR2, SLIK5, RHG32, LPP, NELFA, C42S2, TB10B, TGO1, RFOX3, SP130, ANS1B, ZC3HE, ZC21A, BAIP2, 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, TENS2, 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, GRIP1, GORS2, NONO, ZN281, CT2NL, RN111, ANR17, PPP6, RBM7, CYGB, SARNP, DLGP1, SUN1, TM263, GON4L, PLIN3, MYPT1, NBEA, 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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Qin K, Zhu Y, Qin W, Gao J, Shao X, Wang YL, Zhou W, Wang C, Chen X. Quantitative Profiling of Protein O-GlcNAcylation Sites by an Isotope-Tagged Cleavable Linker. ACS chemical biology 2018 13(8) 30059200
Abstract:
Large-scale quantification of protein O-linked β- N-acetylglucosamine (O-GlcNAc) modification in a site-specific manner remains a key challenge in studying O-GlcNAc biology. Herein, we developed an isotope-tagged cleavable linker (isoTCL) strategy, which enabled isotopic labeling of O-GlcNAc through bioorthogonal conjugation of affinity tags. We demonstrated the application of the isoTCL in mapping and quantification of O-GlcNAcylation sites in HeLa cells. Furthermore, we investigated the O-GlcNAcylation sensitivity to the sugar donor by quantifying the levels of modification under different concentrations of the O-GlcNAc labeling probe in a site-specific manner. In addition, we applied isoTCL to compare the O-GlcNAcylation stoichiometry levels of more than 100 modification sites between placenta samples from male and female mice and confirmed site-specifically that female placenta has a higher O-GlcNAcylation than its male counterpart. The isoTCL platform provides a powerful tool for quantitative profiling of O-GlcNAc modification.
O-GlcNAc proteins:
A0A0A6YVU8, A0A1B0GSG7, RBM47, ZN335, A2A8N0, SBNO1, CNOT1, PHRF1, ZN462, TAGAP, D3YUK0, E9PUR0, E9PVW1, E9PWI7, PARP4, E9PZS2, E9Q2C0, NU153, E9Q616, BD1L1, E9Q732, ARHG5, E9Q7N9, E9Q842, E9Q9B4, E9Q9Q2, E9QA22, E9QAE1, F6Y6L6, F8VQ29, F8VQM5, J9JI28, PDLI1, SPT5H, TAF4, ARI1A, ABLM1, KMT2D, MYPT1, ZN609, SET1A, SYNEM, PUR4, TNC18, KDM6A, DPOD2, M3K7, TPD54, SYNJ1, ZN207, SRPK2, ACK1, SYUA, MYPT2, KIF1B, HBP1, OGA, VINEX, PLIN3, MAFK, BRD4, PDLI1, KDM6A, SRPK1, N4BP1, ANR17, NCOR1, CREG1, CRTAP, MYO1A, MTR1L, CREG1, TOX4, SUN1, M3K6, PSMG1, SC24B, CNOT4, ABL1, ABL1, EGFR, LAMC1, LMNA, GBA1, GCR, HSPB1, PPBT, RLA2, ITB1, K1C18, K2C8, SAP, CATL1, LAMB1, ENPL, BGLR, NFIC, VIME, SNRPA, ROA1, ATX1L, TGAP1, GLI2, HLAC, CATB, TAU, BIP, FINC, K2C8, TPR, MSH3, ENPL, PO2F1, ATF2, GNS, ZEP1, RS2, MUC1, JUNB, ATF7, CATD, SON, SERPH, NELFE, BIP, ROA2, CBL, IF4B, APC, ARNT, MAP4, TEAD1, RXRA, RXRB, RXRG, CLIP1, AIMP1, HXA11, ELF1, NU214, MP2K2, VATA, CUX1, PBX2, MLH1, STAT3, SSRB, KI67, STT3A, RFX5, LMNA, DPOD2, PAXI, CDK8, YLPM1, NU153, RBP2, TAF6, EMD, PPT1, FXR1, ICAL, AGFG1, NUP98, ATX1, ATN1, PTN5, AF17, DSRAD, AMRP, ACYP2, NU107, ACOT8, S26A1, TB182, YTHD1, ASXL1, PI5PA, RIN3, MRTFB, RL37, KCNA2, RALA, STIM1, PITX1, IF4G2, SRPK2, RENBP, COG7, WNK1, SERF2, RPTN, SPSY, DAB2, RBM10, HNRPU, SPTB2, FOXK2, EWS, MEF2A, SP2, CO7A1, S30BP, NUCB1, ENL, IF4G1, K1C17, TLE4, TOP1, SUH, CBG, ACK1, DEMA, AHNK, FOXO1, TROAP, BPTF, NFIA, ROA0, G3BP1, PABP4, ATM, PICAL, MAMD1, RIPK1, STIM1, MTMR1, CUL4B, ASPP2, KLF5, NFYC, CDK13, VEZF1, DSG2, TRI29, UBP2L, SRC8, PUM1, EPN4, RRP1B, NCOA6, DIP2A, MEF2D, NUMA1, R3HD1, KIF14, EBP, RCN1, KS6A1, RBMS2, TAF1C, NCOA2, SF01, JHD2C, MARE1, ELF2, TAB1, ZFHX3, ZYX, ADRM1, CCDC6, TAF9, STX1A, RFX7, QSER1, QRIC1, PRC2C, PBIP1, GSE1, TNR6A, CEAM5, Q3UKP4, COBL1, ARH40, SC31A, PEG3, SRBS2, Q3UU43, Q3UUE0, F91A1, ARBK2, Q497W2, Q4KL65, PHAR4, EPC2, CRTC2, BCORL, BRD10, TGO1, PRC2B, TOIP1, SPG17, SHRM1, ZN362, LRIF1, RHG21, UBAP2, RBM26, RPRD2, ZN318, NCOR1, LAMA5, HCFC1, P3C2A, SAP, AP180, MAFK, SPTB2, SH3G1, ZYX, TSH3, INADL, WAPL, KAZRN, SBNO1, ARID2, DYH17, SAM9L, CDK13, LAR4B, BICRL, RHG21, HELZ, TTLL5, PANX2, PKHG2, NIPBL, LIN54, F135A, RPRD2, IF4G1, SPIC, SCYL2, NFRKB, INT1, ZN182, UGGG1, MDEAS, ZC3HE, RICTR, FIP1, CRTC3, SAS6, MCAF1, BCOR, GGYF2, NU188, CO039, UBN2, HAKAI, ASXL2, SPT6H, DDX46, KDM3B, PRC2B, OOG2, ZIC5, NRK, POGZ, MAVS, CLAP1, EMSY, I2BP2, SRGP1, SH3R1, HUWE1, YTHD3, NU214, TMC5B, ZN598, TOPRS, SHAN2, Q80ZX0, ZNF18, Q810G1, BCL9L, LUZP1, PRSR1, DDX42, PALB2, P66A, GNS, LPP, TB10B, TGO1, Q8BIB6, ZN771, ZNT6, AAPK2, CNOT4, SP110, IFFO1, YTHD3, NCBP3, DEFI6, RBM14, CNOT2, CABS1, Q8C6L9, TCAL5, TAB1, SCYL2, ASPP2, PHC3, EPN2, PDLI5, I2BP1, RN135, AHNK2, NAV2, MISP, MGAP, ANKH1, PHAR4, XRN1, PELP1, Q8JZK6, Q8K0U8, AGFG1, TXD11, IL23R, ARHG6, SPART, SPICE, NUP93, CLASR, ZN786, SYNPO, FNBP4, ARFG1, ENAH, TNR6A, PHC3, SP20H, NAV1, VP37A, KMT2C, BD1L1, NUP35, STXB6, KNL1, TCAL3, MTSS1, SPART, NUP35, PUM2, STT3B, ALMS1, GEMI5, WIPF2, MAVS, UTP6, PI3R4, AMOT, P66B, STAG1, PCNP, LMO7, ATX2L, CSKI2, P66B, BBX, TITIN, HNMT, UBAP2, DCP1A, NRIF1, SMG7, RTF1, MAML1, ZN592, LAR4B, TAF4B, SHIP1, DDX17, RENT1, GPKOW, FUBP2, LPP, TTC28, PF21A, INT12, RCN3, CERS2, PDLI5, FUBP3, MY15B, ANCHR, CLP1L, Z512B, ZFR, EP400, NOL4L, RBM14, CIC, MED15, PIGS, DCR1C, SIN3A, MINT, EYA3, TEAD3, ATX2, RFC4, DHX58, ANX13, GORS2, TAB2, EPN4, ANR17, DPH2, WAC, DIDO1, YTHD1, AMRA1, TANC1, TXD12, F133B, RBM33, GPI8, Q9D2U0, ZC21B, FUND2, F162A, APMAP, Q9D809, FIP1, CNPY3, Q9DAV5, Q9DB24, ALG2, PLIN3, MYPT1, WWTR1, Q9EQC8, SALL1, RBP2, GILT, MFF, SP130, APC1, I2BPL, RBNS5, EPC1, ADNP, ZN106, TM245, CPVL, PTN23, WNK1, E41L1, ZHX3, ZN335, PKHG2, CCSE2, CQ10B, MLXIP, PKHA5, RC3H2, TAF9B, ZBT20, NCOA5, ZN532, APMAP, HYOU1, ADRM1, GIT2, BAG3, UBN1, PDLI7, DIAP3, RBM12, CARF, ETAA1, HXC10, TAB2, UGGG1, CDK12, ITSN2, CNOT2, TMEM9, DAPLE, NYAP2, KANL3, SON, LIMD1, KI21B, KI21A, PPIE, PCM1, GALK1, MRP5, SE1L1, LIMD1, TCF20, SUN2, AFF4, UBQL2, S30BP, NRBP, SIX4, TASOR, GMEB2, PARP4, NUP50, ZHX1, YETS2, HECD1, SCAF8, SRRM2, SCML2, S22AL, NCOR2, DEMA, POLH, R3HD2, ZN281, FBX7, RPGF2, IRS2, HYOU1, PRC2C, NCOR2, GMEB1, S23IP, SRPK3, SLFN1, VNN1, KLK4, SE1L1, RGS6, E41L1
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Chuh KN, Batt AR, Zaro BW, Darabedian N, Marotta NP, Brennan CK, Amirhekmat A, Pratt MR. The New Chemical Reporter 6-Alkynyl-6-deoxy-GlcNAc Reveals O-GlcNAc Modification of the Apoptotic Caspases That Can Block the Cleavage/Activation of Caspase-8. Journal of the American Chemical Society 2017 139(23) 28528544
Abstract:
O-GlcNAc modification (O-GlcNAcylation) is required for survival in mammalian cells. Genetic and biochemical experiments have found that increased modification inhibits apoptosis in tissues and cell culture and that lowering O-GlcNAcylation induces cell death. However, the molecular mechanisms by which O-GlcNAcylation might inhibit apoptosis are still being elucidated. Here, we first synthesize a new metabolic chemical reporter, 6-Alkynyl-6-deoxy-GlcNAc (6AlkGlcNAc), for the identification of O-GlcNAc-modified proteins. Subsequent characterization of 6AlkGlcNAc shows that this probe is selectively incorporated into O-GlcNAcylated proteins over cell-surface glycoproteins. Using this probe, we discover that the apoptotic caspases are O-GlcNAcylated, which we confirmed using other techniques, raising the possibility that the modification affects their biochemistry. We then demonstrate that changes in the global levels of O-GlcNAcylation result in a converse change in the kinetics of caspase-8 activation during apoptosis. Finally, we show that caspase-8 is modified at residues that can block its cleavage/activation. Our results provide the first evidence that the caspases may be directly affected by O-GlcNAcylation as a potential antiapoptotic mechanism.
O-GlcNAc proteins:
A2A4A6, A2A5R8, GPTC8, SPD2B, A2ACG7, A2AFQ9, A2AFW6, A2AG46, CKAP5, A2AH75, A2AJ72, MA7D1, A2AL12, A2AMW0, A2AMY5, TPX2, PPIG, LAS1L, A5A4Y9, A6PWC3, A6PWK7, UBP36, B1AT03, B1AT82, B1AU75, B2RQG2, OTUD4, B7ZCP4, B7ZP47, D3YUW8, D3YWF6, D3YWK1, D3YX62, SAFB1, D3YXM7, D3YZ06, D3YZP6, D3Z069, D3Z158, D3Z3F8, D3Z6W2, E0CYM1, E9PUH7, E9PVM7, E9PWG6, E9PWV3, E9PWW9, E9PY48, E9PYT3, E9PZM7, E9Q066, E9Q2X6, NU153, E9Q450, E9Q4K7, E9Q4Q2, KIF23, BD1L1, NUMA1, E9Q7M2, E9Q986, E9Q9E1, E9Q9H2, E9QKG3, E9QKG6, E9QKZ2, E9QLA5, E9QP49, E9QP59, E9QPI5, F2Z3X7, F6S5I0, F7AA26, F7BQE4, FARP1, F8VQ93, F8VQC7, F8VQE9, F8VQK5, F8WI30, G3UZ44, G3UZX6, G3X8R0, G3X8Y3, G3X928, G3X963, G3X972, G3X9V0, G5E896, G5E8E1, H3BJU7, H3BK31, H3BKK2, H7BX26, I1E4X0, I7HIK9, J3QNW0, DPYL2, GTPB1, AKAP1, TCOF, AIP, HDAC1, RL21, GSH0, KIF1C, DHX15, SC6A6, IF6, ILK, ATX2, NMT1, E41L2, DHB12, SRPK1, ZN326, ZFR, PARG, SPD2A, SP1, CASP8, HPRT, LDHA, G6PI, TYSY, RIR1, GNAI2, ITB1, 4F2, H2B1F, MAP1B, HMOX1, LEG1, G3P, KS6A3, COF1, GNAO, IFRD1, VIME, UBL4A, CBX3, CXA1, CATA, IMDH2, IL1RA, MCM3, CDK4, NKTR, FKBP4, CBX2, HMGB2, AIMP1, KAP3, MP2K1, SYWC, KIF4, NEDD1, DPOLA, RANG, UBP4, PTN11, RAB18, PTN1, PTN12, LDLR, DNLI1, CAP1, STAT3, STA5B, PURA, ALD2, RAGP1, NEDD4, STT3A, ALDH2, GSHR, GFPT1, PCY1A, MCM4, ICAL, PLCB3, CDN2A, HDGF, UBP10, KPYM, CCHL, IDHP, DDX6, GOGA3, COX17, ACTN4, GCP3, TB182, EIF3E, ABCE1, PFD3, 1433E, RAP1A, RS25, TCTP, DNJA1, HMGB1, IF5A1, RS17, RS12, UB2L3, HXD13, HDAC2, ELAV1, TP53B, CASP3, PYRG1, TCPB, STIM2, SRSF3, CSRP2, SPTC2, BOP1, SMAD4, M4K4, HNRL2, MARK3, LARP7, CNN2, PP4R2, PEPD, CDCA2, Q3TFP0, GUAA, PDE12, Q3TL72, PRC2C, NOL9, FUBP2, TRADD, CTU2, ZN865, Q3U4W8, Q3UG37, NAT9, NOL8, Q3UJQ9, SC31A, NCBP1, LRRF1, DDX17, LRC47, JIP4, EHMT1, CA050, AAPK1, NSRP1, Q5RL57, Q5SQB0, TENS3, PUR4, Q5UE59, SRC8, SAMH1, KHDR1, GRB10, HELLS, SPB6, RIPK1, CAPR1, ASNS, LAP2A, CDC37, TS101, SNTB2, FNTA, BAP31, PLPP1, FSCN1, FXR1, DDX5, ATRX, DDX3Y, DDX3X, TGFI1, DBNL, SH3G1, CYTB, SMAD2, NDRG1, ZYX, SQSTM, TPP2, ZN512, LAR4B, F120A, CNDG2, NOP58, LTV1, Q6NV52, Q6NXL1, Q6NZD2, ANKL2, Q6P5B5, XPO1, KIF15, FHOD1, TXLNA, PTN23, JUPI2, NUDC1, TACC1, UBE2O, LARP1, ACAP2, 2AAA, MTCH2, ZN503, CYFP1, HNRPQ, SPAG7, DEK, ACTN1, ATX2L, CKP2L, ZN516, ERBIN, SEPT9, PGRC2, Q80VB6, PI42B, ZN598, SAFB2, Q80ZX0, DLG1, LPP, PEF1, IF4B, FTO, TIPRL, Q8BH80, MISSL, ERC6L, CARF, PRUN1, NUP93, FBX30, HBAP1, AHSA1, RCC2, IPO5, SYLC, CKAP4, MAP11, PALM2, CPNE3, SENP7, CSN7B, NSD2, DPP9, Q8BWW3, KANK2, PXK, PIGT, ITPK1, NHLC2, MAP1S, GWL, PKHH2, CND2, THOP1, SEP11, SKA3, CA198, SEP10, AROS, UBA6, LIPB1, SMAG1, Q8CCM0, ZN276, NAA30, SNX8, SYEP, OGT1, GNL3, PDLI5, FERM2, AGO2, HMCS1, AMERL, SCNM1, DNM1L, NEK9, ANLN, EDC3, MATR3, CHAP1, MEPCE, ERF3A, CC137, TDIF2, VPS18, RFC3, MCMBP, HEXI1, LUZP1, SNP47, TMX1, MAVS, UBXN4, Q8VCQ8, ACSF2, PARN, VIGLN, PSMD2, NAA40, F1142, ZNG1, PAXI, SFPQ, CPIN1, RAB14, IPYR2, PUS7, CSDE1, PIP30, RABE2, CISD1, Q91X76, DUS3L, KCC1A, TTC1, SRGP2, SNX18, RISC, HNRLL, Q921K2, PP6R3, LRC59, UBXN1, DBR1, KCC2G, Q924B0, WAC, SMC6, PAWR, SIAS, STML2, PSIP1, NXF1, PDXD1, NONO, PLST, RRAGC, VMA5A, MAOM, DCTN2, ZN281, CT2NL, GRPE1, ABD12, NU155, OGFR, NPM3, NOP16, GLOD4, DUT, MTAP, IFM3, CYB5B, PAF15, PSMD9, WIPI3, SKA2, VATG1, CHSP1, LRC40, RANB3, SMC1A, MFR1L, ARHGP, DDX47, TBC15, PPIL4, MPPB, CYBP, TECR, SERB1, ZCHC8, SPCS2, Q9CZP3, CD37L, SSBP3, MMS19, MGRN1, ARPIN, HNRPM, SYRC, MCES, Q9D4G5, ATAD1, F162A, TRIR, IPYR, PHF10, ARFG3, ORN, BOLA1, CNN3, KAP0, PLIN3, AKAP8, XRN2, GNAI3, PUR6, RAI14, SENP3, ARFG1, SIL1, VPS35, DGCR8, SYCC, ELP4, LIMA1, XPO2, RBP2, RTN3, PALLD, TMOD3, STK3, COPB, NUP50, DDX21, SH3L1, DDX20, MBNL1, BAG3, GKAP1, ZN207, TRXR1, PPCE, CAF1A, LIMD1, NDRG3, DNJC7, NFU1, COPG1, NUBP1, SMAP, DEST, ACOT9, PR40A, FOXO1, FIZ1, NFKB2, KAD2, AKA12, PRKRA, PDC6I, CHIP, COR1C, VAPA, NDKM, E41L3, TAGL2, CARM1, MTNB, BCL10, IF2G, P5CS, COG1, MD2L1, EIF3G, SAE2, ILF3, TRIP6, USO1, BAZ1B, HNRPF, KEAP1
Species: Mus musculus
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Lee A, Miller D, Henry R, Paruchuri VD, O'Meally RN, Boronina T, Cole RN, Zachara NE. Combined Antibody/Lectin Enrichment Identifies Extensive Changes in the O-GlcNAc Sub-proteome upon Oxidative Stress. Journal of proteome research 2016 15(12) 27669760
Abstract:
O-Linked N-acetyl-β-d-glucosamine (O-GlcNAc) is a dynamic post-translational modification that modifies and regulates over 3000 nuclear, cytoplasmic, and mitochondrial proteins. Upon exposure to stress and injury, cells and tissues increase the O-GlcNAc modification, or O-GlcNAcylation, of numerous proteins promoting the cellular stress response and thus survival. The aim of this study was to identify proteins that are differentially O-GlcNAcylated upon acute oxidative stress (H2O2) to provide insight into the mechanisms by which O-GlcNAc promotes survival. We achieved this goal by employing Stable Isotope Labeling of Amino Acids in Cell Culture (SILAC) and a novel "G5-lectibody" immunoprecipitation strategy that combines four O-GlcNAc-specific antibodies (CTD110.6, RL2, HGAC39, and HGAC85) and the lectin WGA. Using the G5-lectibody column in combination with basic reversed phase chromatography and C18 RPLC-MS/MS, 990 proteins were identified and quantified. Hundreds of proteins that were identified demonstrated increased (>250) or decreased (>110) association with the G5-lectibody column upon oxidative stress, of which we validated the O-GlcNAcylation status of 24 proteins. Analysis of proteins with altered glycosylation suggests that stress-induced changes in O-GlcNAcylation cluster into pathways known to regulate the cell's response to injury and include protein folding, transcriptional regulation, epigenetics, and proteins involved in RNA biogenesis. Together, these data suggest that stress-induced O-GlcNAcylation regulates numerous and diverse cellular pathways to promote cell and tissue survival.
O-GlcNAc proteins:
NU153, ATX2, PTN23, NU214, CNOT2, ANR17, CILK1
Species: Mus musculus
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Trinidad JC, Barkan DT, Gulledge BF, Thalhammer A, Sali A, Schoepfer R, Burlingame AL. Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Molecular & cellular proteomics : MCP 2012 11(8) 22645316
Abstract:
O-linked N-acetylglucosamine (O-GlcNAc) is a dynamic, reversible monosaccharide modifier of serine and threonine residues on intracellular protein domains. Crosstalk between O-GlcNAcylation and phosphorylation has been hypothesized. Here, we identified over 1750 and 16,500 sites of O-GlcNAcylation and phosphorylation from murine synaptosomes, respectively. In total, 135 (7%) of all O-GlcNAcylation sites were also found to be sites of phosphorylation. Although many proteins were extensively phosphorylated and minimally O-GlcNAcylated, proteins found to be extensively O-GlcNAcylated were almost always phosphorylated to a similar or greater extent, indicating the O-GlcNAcylation system is specifically targeting a subset of the proteome that is also phosphorylated. Both PTMs usually occur on disordered regions of protein structure, within which, the location of O-GlcNAcylation and phosphorylation is virtually random with respect to each other, suggesting that negative crosstalk at the structural level is not a common phenomenon. As a class, protein kinases are found to be more extensively O-GlcNAcylated than proteins in general, indicating the potential for crosstalk of phosphorylation with O-GlcNAcylation via regulation of enzymatic activity.
O-GlcNAc proteins:
A0JNY3, A2A653, A2A654, TANC2, ZEP3, MA7D2, CKAP5, CAMP1, LZTS3, A2AJ19, AJM1, MA7D1, A2ALK6, RPGP1, UBR4, A2AP92, SKT, ANR63, A2ATK9, A2AUD5, A2BI30, A6H6J9, A6MDD2, A8DUV1, B1AQX6, B1AR09, GRIK3, B1ATI9, B1AWT3, NHSL2, FRS1L, UBP24, DLGP4, B2RQ57, B2RQ80, PYR1, B2RQL0, B2RQQ5, GNAI1, B2RUE8, OTU7B, B2RWX1, B6ZHC4, B6ZHC5, B7ZCA7, B7ZMP8, B7ZNA4, B7ZNF6, B7ZWM6, B9EHE8, CTTB2, B9EKL9, PTPRZ, D1FNM8, D3YU59, D3YWX2, DGKH, D3YXR8, PGBD5, SHAN1, D3Z0V7, D3Z2J5, D9HP81, E0CYT1, E9PUA3, E9PUC4, DGKD, E9PUR0, E9PV14, E9PV26, KI67, E9PWL1, E9PWM3, E9PY55, E9PZP8, E9Q1M1, E9Q2B2, E9Q3D6, NU153, E9Q3M9, E9Q4N6, E9Q616, E9Q6T8, E9Q6Y8, NUMA1, E9Q828, E9Q9I2, E9Q9J6, E9QA16, E9QAP7, E9QAR5, SC16A, E9QJU8, E9QMJ1, SYGP1, RFIP2, HXK2, CAN2, SC22B, DPYL2, STXB1, TCOF, DCTN1, GLU2B, EF2K, PRDX4, AIP, NUMBL, GSTO1, GSH0, M3K5, PSMD4, DHX15, NPC1, BMPR2, VIAAT, BCAT2, CTND2, PITM1, CSK22, REPS1, ACK1, SLK, CAC1B, PGRC1, IMPA1, SYUA, AKA7A, STRN, RL35A, AT2A2, PGAM2, ATX2, NMT1, E41L2, GPX4, EMC8, DHB12, HCN4, KDM6A, ZN326, SORL, GRPE2, KLC1, ZFR, O88568, HCN2, HCN1, BSN, TOM1, RPP30, DNJB5, COX1, HA1D, HBA, K2C1, MBP, ALDOA, PGFRB, LDHA, G6PI, ENPP1, NEUM, ANXA2, RIR1, HS90A, EGR1, MDHM, KCC4, NFL, NFM, GNAI2, PDIA1, NUCL, CADH1, RC3H2, LRC4B, IGS11, DERPC, UBB, IFI5B, IFI4, ANXA1, EF1A1, H2B1F, PARP1, HS90B, DMD, KCC2A, TCPA, A4, COX5A, GELS, UMPS, NCAM1, GPDA, MDHC, SRP54, RLA0, GLNA, H12, LEG1, DDX3L, SPTN1, AP2A2, TPIS, KS6A3, COF1, GNAO, NFH, SERPH, VIME, MTAP2, EIF3A, CBX3, IMDH2, MCM3, CTNA1, MAP4, GNA12, GNA13, PDIA3, PSB8, NCKP1, PABP1, FKBP4, HMGB2, AIMP1, LA, ACM4, SYWC, RANG, RAB5C, RAB18, CALX, PRDX1, RL12, PPM1B, DNLI1, CAP1, STAT3, PURA, OPRM, TCPQ, CX6A1, MSH2, H14, H11, ALDR, ALD2, CBP, AINX, NEDD4, RP3A, CAPZB, SRPRB, RL36, SOX2, HS74L, ADT1, ROA1, INPP, PCY1A, MCM4, CSRP3, RAB7A, CDN2A, HDGF, ADT2, IMA1, UBP10, KPYM, RIDA, HMGA2, RL10A, CCHL, SOX1, RAB2A, ATX1, CACB3, HMCS2, GOGA3, ATPK, ATPB, ACTN4, IDI1, ACOT8, PTPA, KCNN2, KCNN3, TB10A, TB182, SF3B6, MRTFB, DOCK4, MYPR, EIF3E, PCBP1, LIPA3, ACTB, IF4A1, SNP25, RAB10, CSN2, RRAS2, PRS8, RS15A, 1433E, RS18, RS11, SMD1, ABI2, EF1A2, ACTA, VATB2, RL23, RS24, GBB1, HSP7C, TCTP, GNAS2, 1433Z, HMGB1, IF5A1, ACTG, RS17, RS12, UB2L3, RACK1, ACTS, TBA4A, TBA1A, TBB4B, PLXA2, DCC, EBP, NFIX, EM55, HNRH2, NCOA1, ELAV1, RGRF2, USP9X, TCPB, TCPE, TCPZ, NUCB2, IRS2, WNK1, RL36A, CSRP1, SEPR, RS3A, DPYL1, MPRIP, CAC1A, ATP5J, BOP1, RS5, WBP2, CXAR, PLPL9, G3BP1, RBBP6, CDS1, TBB5, IL6RB, NMDE2, NMDE3, TOP2A, NOTC1, NDKB, AQP1, UBA1, CTNB1, S30BP, NUCB1, MARK3, APLP1, ENAH, ATPA, TF65, YES, MARK2, PGBM, PYC, CAPR2, EMAL1, LARP7, BAX, CNN2, LYAR, CHD8, CNNM1, INF2, TT21B, Q0IJ77, TRIO, VGF, TANC1, CDK12, Q14B66, MA6D1, NSUN2, MCM9, PHAR1, PSD3, Q2Q7P0, FILA2, Q3TAD4, NB5R4, GUAA, METK2, PRC2C, Q3TRG3, PLPL6, K22E, YETS2, Q3TY93, FUBP2, F117B, Q3U882, LBR, TM109, FOXK2, Q3UFK1, Q3UGZ4, TNR6C, DAB2P, ZEP2, AAK1, Q3UHT7, DTX3L, EDC4, PARP3, WASC4, GRIN1, Q3UQ23, SRBS2, THSD4, MRCKA, SPRY3, KSR2, GRM5, TBCD9, LRRF1, ARMX5, STOX2, SHAN3, UBN1, OXR1, DDX17, PHAR4, ANR28, ZN608, Q571B7, PRAG1, TAB3, Q58DZ3, IQEC2, Q5DU62, AAPK1, NUFP2, UNKL, SMG7, RBM27, CYFP2, TM1L2, PSME4, ANR40, Q5SUH6, GGNB2, SYNRG, Q5SVJ0, RPGP2, TBC9B, ACACA, Q5SXC4, Q5XJV5, LMTK3, RN123, ZDHC8, SRC8, MYL6, SKI, SAMH1, IRGM1, CLD11, NPT2A, SPB6, VDAC2, VDAC3, VDAC1, STYX, RBBP4, ASNS, NCOA2, LAP2A, PPM1G, ASTN1, PRDX2, HCFC1, APC, KCNA4, AP180, FXR1, GDIB, GRID2, GRID1, CBX5, SERA, LASP1, NPM, PCBP2, M3K7, SRBS1, DBNL, SH3G1, CYTB, IF4G2, MINT, ZYX, RALY, TFE3, Q640L6, AR13B, HECAM, NPDC1, SYN2, TBR1, ISG15, ABCG1, ATP4A, MRC2, G3PT, PTN13, TPP2, CTNA3, SBNO1, BEGIN, K1549, GIT1, SLAI1, PKP4, PEAK1, CDK13, SH3R1, MYOF, ABLM3, ARMX2, CE170, LAR4B, NOP58, Q6GR78, TPM4, NIPBL, RRP5, FBX41, Q6NVA3, RPRD2, WWC2, ZN532, Q6NXW0, S23IP, SMHD1, NEST, CSKI1, Q6P9N8, MTSS2, AHDC1, PTN23, TRAK1, SRSF1, CHD4, DLGP3, NUP98, NYAP1, KCC2D, AT1A3, AT1A2, NFRKB, RIGI, MAGI1, WDFY3, TACC1, GGYF2, PF21A, KDM3B, CNOT1, LARP1, Q6ZQB7, NU188, Q6ZQJ9, Q6ZQK4, RS9, RL10, IF2A, SC6A5, SEM6D, 2AAA, EEIG1, MTCH2, MRO2B, SCN4B, PLPR4, HNRPQ, TBB2A, SMAP2, Q7TNS5, PLPR3, MBB1A, LNP, TPPP, ATX2L, OTUB1, EXOS3, MAP6, ELP1, SI1L2, LRRC7, ERBIN, PHF24, R3HD2, NAV3, AGRL3, Q80TS6, AUXI, MADD, AVL9, PUM1, UBP8, NU214, SEPT9, NAA15, CAMP3, FA98B, TDRKH, EPN1, TMCC2, AGFG2, Q80X68, C2C2L, FLNB, LRRT4, WNK3, PRIC2, CNKR2, ZN598, SHAN2, AGRB3, Q80ZX0, ZFYV1, MAST4, RHG32, ENTP3, LPP, PEF1, ACTBL, TET3, MYPT2, IF4B, SYAC, F168A, TBL1R, TB10B, CSTP1, CARF, TGO1, FRM4A, SYIM, ANS1B, DLGP2, ZNT6, RCC2, ABLM2, LSS, UNC80, NOE2, CF015, ODP2, GGA3, SYLC, DMXL2, IMP2L, CLAP2, LIPA2, ASPH, CNOT4, FLNA, F163B, GEPH, CREST, KCC1D, PGES2, KANK2, GEMI5, IFFO1, OSBL6, YTHD3, TM266, POGZ, LACC1, MAP1S, A16L1, SI1L1, PP4R4, MYO9A, THOP1, RBM14, Q8C2R1, CNOT2, Q8C6E9, CC134, ANK2, ELFN1, DIDO1, NHSL1, WDR37, DCTN4, SYNPO, BCAS3, VCIP1, Q8CE98, TAB1, SCYL2, NED4L, SYEP, F193A, GNAL, OGT1, NAV1, SYNJ1, RPGF2, EP400, PHC3, P66A, TBCE, VWF, STAU2, LIN7A, TBC23, ZBT20, RTN1, HS12A, DNM1L, UNC5B, UNC5A, ANLN, AGFG1, MATR3, Q8K314, AHI1, NDUS8, I2BPL, PREP, ABLM1, EIF3L, ERF3A, HNRPL, IQEC1, DOCK7, DC1L1, SPART, BST2, RFIP5, AT2A1, NUP35, LUZP1, MAVS, MYH9, PARN, AT1A1, SIR2, SNRK, ZDHC5, CC50A, AMOT, AGAP3, MARK1, Q8VHM5, FLNC, SFPQ, CPIN1, WDR13, BACH, S12A5, RAB14, ACLY, MIC25, ATPG, DDX1, SH3L3, UBAP2, NCOA5, CSDE1, FRS3, ZFN2B, DLG2, PTBP2, SRGP1, TMLH, DYST, SYUB, ELOV6, ALS2, TADBP, TBB6, CLIP1, LRC59, K2C5, UBXN1, SIR1, SPRE1, PAWR, MED1, MEP50, STML2, UBP11, NONO, RRAGC, VMA5A, MAOM, DCTN2, NEUA, DDAH2, DNJA3, TRXR3, RB6I2, SRRT, DSRAD, Q99NC2, RIMS1, ANR17, NU155, NTRI, RRBP1, ZN318, TRI33, ATP5L, RL17, GLOD4, DUT, SDHB, GLRX3, IFM3, NECP1, OCAD1, RRP44, TBB2B, DDAH1, YIF1B, ROA0, NIP7, MPPB, CYBP, RL11, TECR, CHTOP, SERB1, QCR1, NNRD, GARS, TOM70, RS19, SYRC, CNDP2, TMEDA, ODO2, DLGP1, TBB4A, IDH3A, IPYR, RL37, FIP1, TIM50, EF1G, RM17, GSDMD, DDA1, F135B, TM263, CNN3, PLIN3, PGAM1, XRN2, MYPT1, DJC10, KC1D, GNAI3, PUR6, S38A3, NDUBA, CRIP2, TSC1, RAI14, NBEA, TCF20, SORC2, DPYL5, TBB3, RBP2, ARHG7, RTN3, SPN90, RBCC1, PSMG2, DDX24, CLD12, PALLD, ELF2, TMOD3, NUDT3, COPB, NUP50, DDX21, TULP4, FLII, RPF2, CCG3, TBA8, IQGA1, NECT1, ADRM1, FMN2, PALS1, DCLK1, BAG3, CUL3, MINK1, REEP6, TRXR1, SYGP1, SON, APBB1, DREB, SPY2, MACF1, ULK2, ZBP1, TOM40, ADDA, GOGA5, DNJB1, MAP1A, PCLO, GAB1, RIPK3, NPAS3, SH2D3, NUBP2, ZEB2, SYT7, DEST, TEBP, SRS10, RPGR, PR40A, KHDR3, TPSN, CDYL, KAD2, TEN1, PDC6I, CHIP, IF4H, COR1B, COR1C, TNIP1, GANP, ARC, MPP2, SHAN1, VAPA, GSK3B, DEMA, E41L3, JIP1, GBP2, CAD20, P5CS, LAT1, DYR1B, MD2L1, SAE2, APCL, SYVC, MTMR1, MECP2, E41L1, SUCB1, HDAC6, GRIA4, HOME1, OSB10
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