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Liu X, Cai YD, Hou C, Liu X, Luo Y, Mendiola AJP, Xu X, Luo Y, Zheng H, Zhao C, Chen CH, Zhang Y, Xiang YK, Ma J, Chiu JC. O-GlcNAcylation of nuclear proteins in the mouse liver exhibit daily oscillations that are influenced by meal timing. PLoS biology 2025 23(9) 40997131
Abstract:
The liver circadian clock and hepatic transcriptome are highly responsive to metabolic signals generated from feeding-fasting rhythm. Previous studies have identified a number of nutrient-sensitive signaling pathways that could interpret metabolic input to regulate rhythmic hepatic biology. Here, we investigated the role of O-GlcNAcylation, a nutrient-sensitive post-translational modification (PTM) in mediating metabolic regulation of rhythmic biology in the liver. We observe daily oscillation of global nuclear protein O-GlcNAcylation in the liver of mice subjected to night-restricted feeding (NRF) using label-free global O-GlcNAc proteomics. Additional site-specific O-GlcNAc analysis by tandem mass tag mass spectrometry further supports temporal differences in O-GlcNAcylation by revealing day-night differences. Proteins involved in gene expression are enriched among rhythmically O-GlcNAcylated proteins, suggesting rhythmic O-GlcNAcylation may directly regulate the hepatic transcriptome. We show that rhythmic O-GlcNAcylation can also indirectly modulate nuclear proteins by interacting with phosphorylation. Several proteins harboring O-GlcNAcylation-phosphorylation interplay motif exhibit rhythmic O-GlcNAcylation and phosphorylation. Specifically, we show that O-GlcNAcylation occurs at a phospho-degron of a key circadian transcriptional activator, circadian locomotor output cycles kaput (CLOCK), thus regulating its stability and transcriptional output. Finally, we report that day-restricted feeding (DRF) in the nocturnal mouse significantly alters O-GlcNAcylation pattern. Whereas global O-GlcNAcylation analysis indicates dampening of global O-GlcNAcylation rhythm in mice fed under DRF, site-specific analysis reveals differential responses of O-GlcNAc sites when timing of food intake is altered. Notably, a substantial number of O-GlcNAcylation sites exhibit inverted day-night profiles when mice are subjected to DRF. This suggests the dysregulation of daily nuclear protein O-GlcNAcylation rhythm may contribute to the disruption in liver transcriptome previously observed in DRF condition. In summary, our results provide new mechanistic insights into metabolic regulation of hepatic transcriptional regulators via interplay between O-GlcNAcylation and phosphorylation and shed light on the deleterious effects of improper mealtimes.
O-GlcNAc proteins:
A0A075B680, A0A087WQ44, A0A087WSN6, A0A0A6YVV8, A0A0B6VMB2, A0A0F7QZE4, A0A0G2JGY6, A0A0R4J092, A0A0U1RNL9, A0A1I7Q4G8, A0A1N9PTV1, A0A1Y7VP67, A0A286YCY7, A2A654, ZMYM4, TM201, MED14, A2ADB1, A2AJ72, S35D1, BCORL, A2AQR4, A2ATN3, MGAP, KANL3, PHRF1, B1AR09, B1ASA5, B2RQG2, B2RR24, B2RT41, B2RUQ2, EP300, RBM25, B7ZNL9, D3YWX2, D3Z0K6, D3Z2U7, E9PUF4, E9PUH7, FIBA, E9PV38, SET1A, PARP4, PRR12, E9Q1A5, E9Q1M6, ICE1, E9Q3L4, ANR11, ARI1B, SETD2, YTDC1, ZC3HD, ARID2, E9Q7G1, E9Q9V3, E9Q9Y2, E9QAN9, E9QAP7, E9QKL0, E9QMD3, E9QNA7, F6R9G0, F6T8X6, BICRA, G3UVU2, G3X8Q1, G3X928, G3X961, G3X972, G3X9Q0, PCF11, G5E896, H9KV00, ERR1, GTPB1, HNF6, CLOCK, GLU2B, ATN1, IMA3, KLF12, CALU, AF10, ZN143, SP3, KDM6A, ZN106, ZFR, CCNK, PIAS1, LGMN, SP1, IGHG3, CFAH, EGR1, ITB1, ATX1L, CATB, ITPR1, B4GT1, HNF1A, PGH1, A1AT2, NFYA, PO2F1, 3BHS3, HNF1B, CEBPB, CELF1, RXRA, VTNC, NKTR, SUH, ANT3, G6PC1, FOXA1, FOXK1, STAT3, CBP, FKBP2, FOSL2, RFX1, LMNA, STS, MAT1, PON1, CEBPA, ATX1, RD23B, KMT2A, FUS, PAXB1, LMA2L, MRTFB, SUMO2, PP1B, RS11, SMD3, NFYB, SUMO1, ZHX1, TIAR, TBX3, NFYC, ATF1, ERG, NFIB, RBBP6, GABPA, CREB1, S30BP, NFIA, ZEP1, SPA3M, PPA5, CLUS, GATA4, CHD8, CDK12, Q3T9J2, KHDC4, Q3TGN5, PRC2C, CIART, K22E, YETS2, Q3U1M7, LMF1, FOXK2, PUF60, RREB1, ZEP2, UD3A1, ZCCHV, PRRC1, SFSWA, PRD10, ERMP1, Q3UXF4, TMED1, ZBT45, Q569X9, LIN54, TASO2, RESF1, ZN652, NUFP2, KDM6B, Q5PRE9, Q5RIM6, RBM27, UTP18, Q5SUT0, MED13, Q5SXC4, SFR19, UIMC1, A1CF, SIN3A, CSK21, CAPR1, MEF2A, RBBP7, KLF3, NCOA2, USF1, CTCF, GATA6, TS101, HCFC1, ZN148, HIRA, LASP1, RAI1, MAFK, PRG2, SPTB2, SSXT, TAF6, UD19, NUP62, UD11, MEF2D, TIF1A, USF2, CDK13, JHD2C, HECD1, Q6DI81, SCAF8, NOMO1, FND3B, Q6NXL1, ZMIZ1, NSD3, UGGG1, ALG8, AHDC1, PTN23, PIGS, NUP98, NFRKB, GNAS1, ONEC2, FNBP4, CNOT1, NU188, SPCS3, PICAL, HUWE1, CPEB4, PRR14, ATX2L, NACC1, MCAF1, KANL1, NU214, PR40B, UBN2, TNC18, UBP2L, ZN598, Q80ZX0, DDX42, LPP, TET3, E41L5, SP130, ZC3HE, SUN2, EST2E, NCEH1, ARI5B, EMSY, TM260, RFOX2, TM209, KMT2C, ASPH, SRRM2, NUP54, CPSF7, TOX4, IFIX, CREST, Z385B, PIGT, PGLT1, YTHD3, KAT6A, ASXL2, ZN609, POGZ, SREK1, ZHX2, ZHX3, P20D1, MBNL2, RBM14, PIAS2, CNOT2, ITCH, DIDO1, EPC1, SCYL2, G6PE, TCRG1, BCOR, CCAR1, Q8CHB3, ADNP2, BICRL, EP400, PHC3, P66A, FWCH1, PDLI5, NUP42, ZMIZ2, BTD, UD3A2, ESRP2, TAF10, ZBT20, Q8K154, GT251, ALG3, BRD3, I2BPL, PO121, SF3A1, EST2A, SF3B4, Q8R084, ZBT44, MTSS1, TMED4, ZC3HA, UBQL1, NUP58, BRD8, ATX7, STAB2, RBM12, RBPS2, MED25, MAVS, ALG12, HNRL1, CDIPT, SRSF4, P66B, TAF9, MCR, SFPQ, MBOA5, UBAP2, SMAP1, NCOA5, RBM47, CREL1, SC16B, BAZ2A, RBM5, RISC, ALS2, BCL7B, TMCO1, SYDC, CIC, MED15, WAC, MED1, GORS2, RBM10, ZN281, MLXPL, ANR17, ZN318, TRI33, PCYOX, NECP1, RBM33, SSRA, CREL2, PINX1, INT12, SP2, PHF14, SUN1, APMAP, FIP1, AP2B1, RPN2, LMAN2, AKAP8, MYPT1, RSRC1, EIF3F, Q9EQC8, ERAP1, SALL1, Q9ERL0, RBP2, RTN3, PALLD, TF2H2, ANM1, NUP50, HAKAI, HYOU1, ELOV1, ZN207, DOPP1, CCNT1, TBL1X, PO210, VKGC, QKI, UBQL2, HIPK2, COP1, PR40A, FOXO1, PIGN, MAN1, GANP, ENTP5, NFAT5, CARM1, FOXO3, FBLN5, IF2H, Q9Z1A1, DEAF1, HTAI2, HNRPF, ITPR2, S4R1W8, V9GX43
Species: Mus musculus
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Wu JL, Chiang MF, Hsu PH, Tsai DY, Hung KH, Wang YH, Angata T, Lin KI. O-GlcNAcylation is required for B cell homeostasis and antibody responses. Nature communications 2017 8(1) 29187734
Abstract:
O-linked N-acetylglucosamine (O-GlcNAc) transferase (Ogt) catalyzes O-GlcNAc modification. O-GlcNAcylation is increased after cross-linking of the B-cell receptor (BCR), but the physiological function of this reaction is unknown. Here we show that lack of Ogt in B-cell development not only causes severe defects in the activation of BCR signaling, but also perturbs B-cell homeostasis by enhancing apoptosis of mature B cells, partly as a result of impaired response to B-cell activating factor. O-GlcNAcylation of Lyn at serine 19 is crucial for efficient Lyn activation and Syk interaction in BCR-mediated B-cell activation and expansion. Ogt deficiency in germinal center (GC) B cells also results in enhanced apoptosis of GC B cells and memory B cells in an immune response, consequently causing a reduction of antibody levels. Together, these results demonstrate that B cells rely on O-GlcNAcylation to maintain homeostasis, transduce BCR-mediated activation signals and activate humoral immunity.
O-GlcNAc proteins:
FAIM3, BLTP1, BCORL, M3K15, EXC6B, PLHD1, CTTB2, MYO1E, SCLT1, TAF4B, TCOF, FLOT1, OXLA, HDAC1, SYPL1, SEM4D, MA2B1, PPE2, PLD3, DPOD2, NOCT, HNRH1, API5, DFFA, MMP8, DPM1, EIF3D, ESS2, CTNL1, VTI1B, S28A2, FA5, CO4B, IGKC, LAC1, IGHA, IGHDM, HA11, LAMC1, TBA1B, LDHA, HVM51, SPTA1, ZFP1, EGR1, ENPL, RPB1, ITB1, ENV1, 4F2, HS90B, HA2B, HB2A, CD44, BLK, CN37, LAMP2, ZFP37, PTBP1, HB2I, BASI, FAS, EVI2A, MDR1A, BGAL, ITAL, LYN, TLN1, MOES, U2AF2, MAP4, GNA13, RL3, CATG, DPP4, PTN6, HEXA, NKTR, HMGB2, SUH, CEAM1, GTR3, DRG1, RAB5C, CD22, FMR1, VGFR1, HSPA9, CAP1, ECI1, FOXK1, STAT1, NKX25, TCPQ, H11, H13, IL12B, CAPZB, RL5, VDR, RET3, ADCY7, VA0D1, AAAT, IMA1, STOM, FUS, NICA, RU2A, EF2, AAAS, RUVB1, ABCE1, DCAF7, 1433G, ACTA, RS6, VATB2, RL23, RL8, PP2BA, RACK1, TBB4B, M4K1, ITPR3, SURF6, ELAV1, EVL, H2B1A, AT8A1, TCPH, TCPB, NXN, TBB5, HNRL2, CREB1, PLAK, 3MG, CO6A1, LG3BP, COE1, CNN2, NSUN2, HMHA1, SNUT2, SMCA4, TPC10, TGRM2, I20L2, ZSWM8, PRRC1, SC31A, CPZIP, ITAD, ULK4, ITA1, DYHC2, LIN54, JKIP3, GRHL3, MYO1G, SIN3A, IRAG2, SAMH1, KHDR1, LY75, RASA3, NPT2A, CAPR1, ARHG2, PML, IMA5, LAP2B, PRP4B, M4K2, TS101, PLSL, CTNA2, VSX2, CD37, SERA, PCBP2, TIF1B, COCH, NUP62, RALY, UT14A, ARG39, CLH1, ATS16, F120A, NOP58, TEDC2, U520, RRP12, SMHD1, ANO6, TTBK1, CHD4, SARM1, NUP98, RASL2, TNKS1, AT1A2, NFRKB, DDX55, DNA2, H2B1C, CMYA5, GIMA8, CYFP1, SPAG5, HNRPQ, RPF1, MBB1A, PRC2A, ADCY2, MOGS, SDA1, FA98B, WIPI2, TRRAP, XYLT1, WDR82, GNS, ERLN2, S38A9, WASF2, S2512, NIM1, TBL1R, ZN526, CARF, HES7, UNC80, RBGPR, ECHA, ELMO1, ATOSB, KMT2C, FLNA, TPC2, RBBP5, POGZ, DOC10, SYFA, SMKZ, COR2A, RBM14, DOCK2, CASP9, RAE1L, NUP88, RPB2, UACA, SYEP, P66A, VPS50, COPA, VWF, TXTP, ZN536, LMBD1, R4RL1, C2D1A, URP2, STX5, GT251, SDHA, PO121, ABLM1, COL12, ALAT1, RORB, PDLI2, ERO1B, CD177, PSPC1, NUP58, STAB2, LRC8C, COX18, MAVS, PLBL1, UN93B, EVI2B, MYH9, ESIP1, VIGLN, PSMD2, HNRL1, CCAR2, SP7, RECQ5, SFXN3, IF4A3, RINI, DDX1, UBAP2, S15A4, DNJC9, MASP2, UXS1, CSCL1, BMP2K, CYRIB, SYDC, C1TC, GLYR1, PDIA6, S12A6, ATAD3, MYO5A, MCLN1, ABEC3, STML2, SFXN1, PRP19, TARA, MCRS1, RTCB, NDUS5, S12A9, SF3B1, ANR17, NU155, TR34A, BAP1, PRP8, NUDC2, TSN31, RN138, RTRAF, RU2B, YETS4, M2OM, MIC19, SNX2, DDX28, CXXC1, RUSD4, ILF2, CHTOP, LUC7L, DIM1, MCES, SEC13, SP2, NOP56, U2AF1, EF1G, MCEM1, EVPL, PRP4, CMTR1, WWP2, DHB11, PESC, TLR9, IRX6, KRT81, RBP2, AFF4, KAT2B, STK3, NUP50, DDX21, ACINU, SIGIR, ZN207, SLAF1, SON, H2AY, MTA2, SAE1, MYO1C, RUVB2, TRPV2, PFKAP, ARC1B, ASAH1, VAPA, EHD1, IF2G, CLIC1, HNRPF
Species: Mus musculus
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