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Xu S, Zheng J, Xiao H, Wu R. Simultaneously Identifying and Distinguishing Glycoproteins with O-GlcNAc and O-GalNAc (the Tn Antigen) in Human Cancer Cells. Analytical chemistry 2022 35132862
Abstract:
Glycoproteins with diverse glycans are essential to human cells, and subtle differences in glycan structures may result in entirely different functions. One typical example is proteins modified with O-linked β-N-acetylglucosamine (O-GlcNAc) and O-linked α-N-acetylgalactosamine (O-GalNAc) (the Tn antigen), in which the two glycans have very similar structures and identical chemical compositions, making them extraordinarily challenging to be distinguished. Here, we developed an effective method benefiting from selective enrichment and the enzymatic specificity to simultaneously identify and distinguish glycoproteins with O-GlcNAc and O-GalNAc. Metabolic labeling was combined with bioorthogonal chemistry for enriching glycoproteins modified with O-GlcNAc and O-GalNAc. Then, the enzymatic reaction with galactose oxidase was utilized to specifically oxidize O-GalNAc, but not O-GlcNAc, generating the different tags between glycopeptides with O-GlcNAc and O-GalNAc that can be easily distinguishable by mass spectrometry (MS). Among O-GlcNAcylated proteins commonly identified in three types of human cells, those related to transcription and RNA binding are highly enriched. Cell-specific features are also revealed. Among glycoproteins exclusively in Jurkat cells, those involved in human T-lymphotropic virus type 1 (HTLV-1) infection are overrepresented, which is consistent with the cell line source and suggests that protein O-GlcNAcylation participated in the response to the virus infection. Furthermore, glycoproteins with the Tn antigen have different subcellular distributions in different cells, which may be attributed to the distinct mechanisms for the formation of protein O-GalNAcylation.
O-GlcNAc proteins:
RBM47, E2F8, SBNO1, CNOT1, HMX3, BTBDB, RHG32, P121C, PDLI1, SNP23, PSMD9, TAF4, ARI1A, ABLM1, STX16, HGS, MYPT1, SC16A, SR140, SET1A, FYB1, TIF1A, PPM1G, SHIP2, EIF3D, NUP42, KDM6A, TET3, SI1L1, DC1L2, HNRPR, PRPF3, TPD54, E41L2, ZN207, BUB3, AKAP8, ZNRD2, MYPT2, GANP, HNRPQ, DIAP1, PLIN3, MAFK, TBL1X, MITF, N4BP1, ZC11A, T22D2, PP6R2, ANR17, BCAS1, NCOR1, SPAG7, TIPRL, SPF30, TOX4, TOX, PCF11, AGFG2, ZFPL1, KIF4A, SC24A, SC24B, CNOT4, ASML, M4K4, BPNT1, PX11B, CHK2, LMNA, GLPA, TFR1, ALDOA, GCR, HSPB1, GNAI2, RLA1, RLA2, RLA0, K1C18, K2C8, RB, CATD, SYEP, PTPRC, VIME, GSTP1, HMGB1, ROA1, ATX1L, DERPC, ZN865, TPR, LAMP2, EF2, PLSL, PLST, GLU2B, HCLS1, PO2F1, RAC2, ATF2, ZEP1, TFE2, MUC1, CREB1, JUNB, ATF7, PTN2, DDX5, SON, ATF1, CSK22, NFKB1, FLNA, PUR2, RFX1, CBL, COF1, PTBP1, ARNT, DCK, PYR1, MAP4, CALX, 3MG, PRDX6, CDC27, AMRP, CLIP1, ZEP2, HNRH1, 1433S, ELF1, LSP1, PTN7, IRS1, ADDA, NU214, CUX1, TXLNA, MLH1, ECHA, IF2G, HNF4A, LAP2B, GPDM, RANG, KI67, CRKL, CAPZB, RFX5, SOX2, CAMLG, NASP, FAS, CDK8, SRP09, YLPM1, NU153, RBP2, TAF6, EMD, LRBA, PAPOA, HCFC1, HDGF, AGFG1, HNRPF, HXK2, NUP98, ATX1, RD23B, AF10, AF17, DSRAD, FOXA1, HNRH2, NU107, TPIS, PSME3, TPM4, F193A, GTF2I, PHC1, PRKDC, MAP1A, SARNP, FOXK1, FBLN2, FAM3A, EM55, NFKB2, HNRPU, SPTB2, FOXK2, RUNX1, FLI1, SATB1, SP2, MP2K1, NUCB1, KMT2A, IF4G1, TLE3, TLE4, KPCT, PSME1, GABPA, PRDX1, ACK1, AHNK, IFFO1, GALT2, SRBP2, TROAP, BPTF, TP53B, CBX3, NFAC2, PICAL, CUL4B, ASPP2, NFYC, CDK13, VEZF1, UBP2L, SRC8, CAPR1, LAGE3, PUM1, MDC1, EPN4, RRP1B, NCOA6, GSE1, UBP10, 2A5D, MEF2D, LASP1, NUMA1, CND1, TEBP, PCBP1, RBMS2, SF3A1, TSN, SF01, MED1, TRIP6, ELF2, TAB1, ZFHX3, ZYX, ADRM1, DPYL2, TAF9, MAPK3, CSPP1, PDS5A, QSER1, AAK1, LRRF1, VP26B, ACSF3, TPRN, CRTC2, PAN3, YIF1B, PRC2B, CEP78, ZN362, FKB15, LRIF1, CAF17, UBAP2, NT5D1, AHDC1, LYRM7, RPRD2, ZN318, TASO2, TBC9B, ARID2, C19L1, ABLM2, TWF2, GRHL2, CPZIP, NIPBL, LIN54, ZCHC8, C2D1A, SCYL2, NFRKB, RSBNL, MDEAS, ZC3HE, LARP1, SAMD1, FIP1, CRTC3, SAS6, MCAF1, BCOR, GGYF2, NBEL2, CO039, SRCAP, UBN2, TM1L2, ASXL2, SPT6H, MEPCE, BOP, KDM3B, ERMP1, TRM1L, ZCCHV, KANL1, POGZ, ZFY16, NUFP2, MAVS, EMSY, RAI1, I2BP2, SRGP1, RHG30, SH3R1, HUWE1, YTHD3, GALT7, LYRIC, BCL9L, CASZ1, TSYL5, DDX42, CACL1, P66A, I2BP1, VRK3, FOXP4, ARI3B, TEX2, MGAP, ANKH1, SUGP1, MILK2, ERF3B, K2013, PHAR4, XRN1, ZN687, FNBP4, ARFG1, ENAH, NHLC2, AVL9, XXLT1, GOLM1, TXND5, PAIRB, CHSTE, SLAI1, TNR6A, PHC3, SP20H, VP37A, KMT2C, ARI1B, KNL1, NEDD1, ALMS1, PREX1, DLG5, GEMI5, PIGO, UBS3B, WIPF2, FRS2, PDC6I, ZFN2B, TPC12, SEN15, PCNP, LMO7, ATX2L, CSKI2, PSPC1, P66B, GBF1, SMG7, RTF1, TOPB1, PHF3, MAML1, TTC9A, PRCC, RREB1, CBP, DDX17, SEM4D, ARHG1, GPKOW, FUBP2, LPP, TTC28, PF21A, FAF2, ESS2, EDC3, A7L3B, P121A, PDLI5, FUBP3, VCIP1, PDLI2, Z512B, ZFR, EP400, PRRC1, NOL4L, RBM14, PURB, NACC1, CIC, MED15, NUDC1, SIN3A, AEDO, MINT, HTF4, CNN2, RGPD5, ATX2, HCD2, S29A1, ARI3A, SH3G1, TRIR, DPH2, MGME1, ERP44, ESYT1, CCM2, CNPY3, WAC, DIDO1, HGH1, MMTA2, PAXX, NTM1A, RBM4, SGPP1, HEMGN, HDHD5, YTHD1, FTO, CEP44, BC11B, PITH1, SP130, BRD8, RGAP1, I2BPL, ADNP, DHX36, FOXP1, CENPH, WNK1, E41L1, ZHX3, YTDC2, RANB3, PHAX, ECT2, CNO10, MLXIP, PKHA5, PKHA1, RC3H2, LY9, RDH14, TAF9B, NCOA5, TANC2, TNR6C, CHD8, SDF2L, ARFG3, UBN1, RTN4, PDLI7, CHSTC, STRN4, PNO1, BMP2K, RBM12, STAU2, TXLNG, PNPO, CARF, TAB2, TMOD3, CDK12, F120A, HPBP1, ITSN2, CNOT2, CHMP5, VAPA, CAMP3, RBM27, KANL3, RERE, ZN219, SE1L1, STAP2, LIMD1, TCF20, SEPT9, UBQL2, TRPS1, S30BP, NRBP, EI2BD, SIX4, APC7, TASOR, GMEB2, PARP4, MA1B1, ACINU, ZHX1, CDV3, MRTFB, ZBT21, YETS2, HECD1, PKCB1, SCAF8, PP6R1, TRI33, TNR6B, ZC3H4, SHAN2, SRRM2, CTND2, SCML2, ZN148, T3JAM, VDAC3, AKAP2, DDX52, NOP58, GIT1, ZN281, SIT1, SALL2, ARIP4, CRBG1, HYOU1, KLF12, PRC2C, YTHD2, CD2AP, TNPO3, SRPRB, TSSC4, NUBP2, HCFC2, FHOD1, NCOR2, GMEB1, NCOA3, S23IP
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, 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,