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Yu SB, Wang H, Sanchez RG, Carlson NM, Nguyen K, Zhang A, Papich ZD, Abushawish AA, Whiddon Z, Matysik W, Zhang J, Whisenant TC, Ghassemian M, Koberstein JN, Stewart ML, Myers SA, Pekkurnaz G. Neuronal activity-driven O-GlcNAcylation promotes mitochondrial plasticity. Developmental cell 2024 38843836
Abstract:
Neuronal activity is an energy-intensive process that is largely sustained by instantaneous fuel utilization and ATP synthesis. However, how neurons couple ATP synthesis rate to fuel availability is largely unknown. Here, we demonstrate that the metabolic sensor enzyme O-linked N-acetyl glucosamine (O-GlcNAc) transferase regulates neuronal activity-driven mitochondrial bioenergetics in hippocampal and cortical neurons. We show that neuronal activity upregulates O-GlcNAcylation in mitochondria. Mitochondrial O-GlcNAcylation is promoted by activity-driven glucose consumption, which allows neurons to compensate for high energy expenditure based on fuel availability. To determine the proteins that are responsible for these adjustments, we mapped the mitochondrial O-GlcNAcome of neurons. Finally, we determine that neurons fail to meet activity-driven metabolic demand when O-GlcNAcylation dynamics are prevented. Our findings suggest that O-GlcNAcylation provides a fuel-dependent feedforward control mechanism in neurons to optimize mitochondrial performance based on neuronal activity. This mechanism thereby couples neuronal metabolism to mitochondrial bioenergetics and plays a key role in sustaining energy homeostasis.
O-GlcNAc proteins:
A0A096MIX2, A0A0G2JUA5, IQEC1, A0A0G2JUI5, A0A0G2JUT7, A0A0G2JVC2, A0A0G2JVU1, A0A0G2JVW3, A0A0G2JVZ6, A0A0G2JW69, A0A0G2JWG6, A0A0G2JWK6, A0A0G2JXD0, A0A0G2JXD6, A0A0G2JXE4, TRI46, A0A0G2JXZ9, A0A0G2JY48, A0A0G2JY73, A0A0G2JYE0, A0A0G2JYI7, A0A0G2JYU3, A0A0G2JZ52, A0A0G2JZ94, A0A0G2JZA1, A0A0G2JZA7, A0A0G2JZB7, A0A0G2JZH9, A0A0G2JZX5, A0A0G2K0W3, ABCA3, A0A0G2K2B5, A0A0G2K2Y2, A0A0G2K315, A0A0G2K3H2, A0A0G2K459, A0A0G2K490, A0A0G2K548, A0A0G2K5E4, A0A0G2K5L1, GHC1, A0A0G2K618, A0A0G2K654, A0A0G2K6F2, A0A0G2K6T9, A0A0G2K719, A0A0G2K782, A0A0G2K7L2, A0A0G2K7P9, A0A0G2K847, A0A0G2K8I5, A0A0G2K8S6, A0A0G2K929, A0A0G2K999, A0A0G2K9J0, A0A0G2KAE2, A0A0G2KBB9, A0A0H2UHM7, A0A0U1RS25, A0A140TAA1, NUMBL, PBIP1, A5I9F0, ROA2, H2AJ, B0BN30, B0BNK1, LRFN3, B0K026, FLRT3, B1H2A6, B1WC18, ACAD9, BRSK1, B2GUY8, B2GV74, PTPRE, B2RYB1, B2RYC9, B2RYD7, CTL2, B5DEJ9, TTC17, B5DEZ8, SNPH, B5DFC3, D3Z981, D3Z9D0, D3Z9L0, D3ZA31, ATPK, D3ZAG0, LRRT3, D3ZB81, D3ZBM3, D3ZC55, D3ZC56, D3ZC81, D3ZCT7, D3ZD23, D3ZD73, D3ZDX5, D3ZE26, D3ZEH1, SIDT2, D3ZEI4, D3ZEK5, D3ZES7, D3ZFQ8, D3ZFT1, D3ZG43, D3ZH14, D3ZH36, D3ZH41, D3ZHA1, D3ZHG3, D3ZHL1, MACF1, D3ZK41, D3ZKV7, D3ZLE2, D3ZMJ7, D3ZN27, HCFC1, D3ZN99, D3ZPJ0, D3ZPN0, PLXA3, D3ZQ57, TRIM2, D3ZQM3, D3ZQN7, D3ZRH1, D3ZRN3, D3ZSY8, D3ZT20, D3ZT36, D3ZT47, D3ZTG3, D3ZTL0, D3ZTW6, D3ZU13, D3ZUJ8, D3ZUM4, D3ZUY8, D3ZW09, D3ZW15, D3ZW19, D3ZWP6, D3ZWQ0, D3ZXQ2, D3ZXX3, D3ZYD7, D3ZYM4, D3ZYR4, D3ZYS7, D3ZZK3, D3ZZU4, D4A062, D4A0A1, D4A1G8, LRFN5, D4A2H4, D4A2I9, D4A2Q3, D4A3H5, D4A3L3, D4A3N4, D4A435, D4A507, D4A517, D4A567, D4A5F1, D4A5I4, D4A5X7, D4A604, D4A628, D4A644, LRRT1, D4A6G2, D4A6H8, MGLYR, D4A6T9, D4A732, D4A758, D4A7M0, D4A7Y4, D4A831, D4A833, D4A885, D4A8N1, D4A9F4, D4A9U6, D4AA63, D4AA77, D4ABA9, D4ABI7, LRFN4, D4ACK1, PCD16, D4AD89, D4ADS4, D4ADU2, D4AE63, D4AEB3, E9PT51, E9PT53, E9PT92, E9PTA4, E9PTR4, F1LM47, F1LMW0, F1LNL3, F1LP13, F1LPD7, F1LPJ1, F1LPV0, F1LR12, F1LS01, F1LT36, F1LUC0, F1LUT4, F1LUZ4, F1LV44, F1LVL5, S2512, F1LXC7, F1LXD6, F1LYJ8, FARP1, F1LZ38, F1LZB7, F1M049, F1M1E4, F1M2D4, F1M2E9, F1M2K6, F1M3H3, F1M3J7, F1M3P6, F1M3T8, F1M4B6, F1M4J1, F1M5G8, F1M6P8, F1M853, F1M8K0, F1M949, F1MA42, F1MA97, F1MAK3, F1MAP4, F1MAS4, F7EL93, F7EYB9, F7F3I7, G3V667, G3V6K6, G3V6N7, G3V6U3, G3V728, G3V765, G3V7D4, G3V7K5, G3V7N0, G3V7V3, G3V824, G3V881, G3V886, G3V8D0, LRP1, PGLT1, M0R4G0, M0R557, RN157, M0R5P8, M0R5T4, M0R6E0, M0R715, M0R757, M0R7B4, M0R868, M0R9U3, M0RAP5, M0RB22, M0RC17, M0RDA4, MARK1, MARK2, SYT11, DCLK1, CD166, CTND2, NRP2, ACSL4, NPTXR, ENTP2, C1QBP, DNJA2, PICAL, SEM6B, TRIM3, ANK3, CELR3, SLIT1, SLIT3, VKGC, PACS1, BSN, GABR2, PTN23, AGRL1, AGRL2, CATB, OX2G, ROA1, ENOA, G3P, GNAI2, AT1A1, AT1A2, AT1A3, BIP, GDN, RPN1, AT1B1, CPSM, SYPH, KCC2B, SYN1, MAP1S, LRFN1, LRC4B, ATPB, KCC2A, CLH1, AT2B1, AT2B2, AT2A2, KCC2G, SUCA, RS14, NCAM1, AT1B2, PRIO, LAMP1, INSR, MTAP2, MAP1B, GBRB1, KCC2D, H14, ATPA, S25A3, SPTN1, ABCD3, LAMP2, RL9, RL35, THIL, GSK3B, RL27A, AP2A2, GBRG2, CSK21, GRIA1, GRIA2, GRIA3, GRIA4, AT5F1, NFL, GNAZ, RLA0, GBRA5, GBRA3, CNR1, PPAL, PGFRA, EDNRB, SYT1, PERI, AINX, GBRA2, RL17, RS5, IGF1R, CATD, AKAP5, EAA1, RPN2, VPP1, AGRIN, KAPCA, RS2, DCTN1, TCPA, SC6A9, BDH, RS9, SERPH, ITPR1, PLEC, PFKAL, VIME, ATP5H, GRM2, GRM3, GRM4, GRM5, EAA2, S6A11, EZRI, TXTP, CPT1A, QCR2, HS90B, MAP1A, GRM7, ATPG, NMDZ1, DYHC1, MPC2, ANPRC, GRIK2, GRIK3, DPP6, GFAP, PFKAM, PFKAP, SYT5, DPYL2, NPTX1, S1PR1, GRP75, ITB1, RS3A, AP1B1, MOT1, P4HA1, CACB1, CA2D1, GBB2, AT12A, EPHA5, NCAN, PGCB, OGT1, IDHP, GNAO, ACTB, ARF3, STXB1, HNRPK, 1433G, RS7, PP1B, RS16, 1433E, RS23, RS13, RS11, EF1A1, RS4X, RL23A, RS6, H4, GBRA1, RAN, RL23, RS24, RS3, RL32, RL11, AP2B1, RS27A, RL40, HSP7C, CYH2, DNJA1, GBRB3, GBRB2, ACTC, TBA1A, NEUA, TBB5, APC, MFGM, NUP54, FOLH1, IF2G, RL24, ENPP5, AP2M1, H33, RMXRL, STIM1, TBB2A, MDGA1, EFTU, PURA, MET, CNTN5, NPTN, GPAT1, NEO1, LCAP, KC1A, NFASC, NRCAM, M2OM, SHPS1, CD47, CNTP1, S27A1, DHB4, CSPG4, NMDE2, CAC1B, SV2A, PTPRA, NTRK3, TENR, L1CAM, ADT1, KC1D, ATPO, TGFB2, NRX3A, CAC1E, ADT2, MYPT1, ADA10, K2C8, Q14U74, KINH, Q32KJ5, MIC60, ATAD3, TBB2B, LONP2, AMZ2, LRFN2, Q498C9, DJC10, CARM1, K2C6A, TBB3, MACOI, S39A6, RBMX, Q4V8H7, LRC8A, Q505J7, SYFA, S2551, ZFR, PGAM5, Q566E4, NOE2, NDUA9, ARHG2, PLD3, NONO, FA98A, RM16, CAPR1, DCLK2, PMGT2, NSDHL, ITM2C, LRC59, DRS7B, Q5RK08, Q5U2P5, Q5U302, LRC8D, KIF2B, Q5XIA6, ECSIT, TBA4A, Q5XIH3, EPDR1, TMX2, MGRN1, ECHB, NOE1, GSLG1, NMDE4, PTPRZ, SYT7, KC1G3, FPRP, Q62797, CNTN4, GGH, NLGN2, NLGN3, NELL2, DPYL1, DPYL3, ERBB4, SCNAA, CAMKV, Q63116, CNTN1, GRIK5, PHLB1, MYO9B, NRX1A, NRX2A, MAP6, NTRK2, HYOU1, S12A5, SFXN1, OST48, NDUS2, DDX1, TECR, ECHA, AT1A4, AT2B4, PTPRF, PTPRS, PACC1, FACR1, C2D1A, ENPL, NDUS1, S12A9, TBA3, SIR5, SIAT9, HEXB, Q6AY21, SCPDL, Q6AYI1, Q6AYM8, RTCB, ABD12, K1C15, K1C10, K2C4, K2C1B, K22E, K2C73, K2C1, TS101, PRC2A, ABHGA, PLAK, Q6P3V8, TCPG, MEST, K2C5, DAB2P, Q6P762, LYAG, DHB12, TBB4B, RL10, DPP10, GNA13, KIF5A, ROA3, RS27, PGAP1, PCDA4, ANR46, 4F2, PLPR3, PLPR4, SSRA, QCR8, R4RL2, T132A, SE1L1, MAST1, TFB1M, RB6I2, SFXN5, CA2D3, AGAP2, NICA, SGPL1, Q8CJE3, BRNP2, ERC2, AGRG1, L2GL1, LGI1, Q8R490, TIP, FAT3, AFAP1, MARK3, CCG8, KHDR1, BRNP1, TFR1, ATRN, CLAP2, RTN4R, Q99PS2, PABP1, XYLT1, SO1C1, KDIS, TPP1, CSPG2, DCX, PSD1, ABCA2, CBPD, SFXN3, WNK1, RIMS1, RIMS2, CHD8, HNRPD, HCN4, HCN3, HCN2, HCN1, PCLO, TAOK2, SYGP1, NRP1, SRCN1, MEGF8, CELR2, S22AN, PDZD2, CXAR, TEN2, PODXL, CTNB1, SHAN1, KIF2A, SLIT2, NEGR1, GABR1, FADS2, TMM33, AGRL3, RPGF4, FLOT1, MYO9A, CADH2, HOME1, DHCR7
Species: Rattus norvegicus
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Ma J, Liu T, Wei AC, Banerjee P, O'Rourke B, Hart GW. O-GlcNAcomic Profiling Identifies Widespread O-Linked β-N-Acetylglucosamine Modification (O-GlcNAcylation) in Oxidative Phosphorylation System Regulating Cardiac Mitochondrial Function. The Journal of biological chemistry 2015 290(49) 26446791
Abstract:
Dynamic cycling of O-linked β-N-acetylglucosamine (O-GlcNAc) on nucleocytoplasmic proteins serves as a nutrient sensor to regulate numerous biological processes. However, mitochondrial protein O-GlcNAcylation and its effects on function are largely unexplored. In this study, we performed a comparative analysis of the proteome and O-GlcNAcome of cardiac mitochondria from rats acutely (12 h) treated without or with thiamet-G (TMG), a potent and specific inhibitor of O-GlcNAcase. We then determined the functional consequences in mitochondria isolated from the two groups. O-GlcNAcomic profiling finds that over 88 mitochondrial proteins are O-GlcNAcylated, with the oxidative phosphorylation system as a major target. Moreover, in comparison with controls, cardiac mitochondria from TMG-treated rats did not exhibit altered protein abundance but showed overall elevated O-GlcNAcylation of many proteins. However, O-GlcNAc was unexpectedly down-regulated at certain sites of specific proteins. Concomitantly, TMG treatment resulted in significantly increased mitochondrial oxygen consumption rates, ATP production rates, and enhanced threshold for permeability transition pore opening by Ca(2+). Our data reveal widespread and dynamic mitochondrial protein O-GlcNAcylation, serving as a regulator to their function.
O-GlcNAc proteins:
A9UMV9, B0BNC0, B2RYW3, B2RYX1, B5DEL8, D3ZUX5, D4A7L4, D4A898, F1LM47, F1LXA0, O70253, AATM, MDHM, NU4M, SODM, ODP2, ATPB, DHE3, COX5A, ALDH2, CX6C2, THIM, ETFA, ECHM, PCCA, ACADL, ACADS, ATPA, ACSL1, CPT2, NDUV2, ATP5J, SDHB, 3HIDH, ATP5E, ATP5I, ATP5H, CX7A2, ATPD, ACADV, ODPB, IDHP, CH60, EFTU, M2OM, MMSA, ADT1, ATPO, MIC60, Q3V5X8, ACSF2, Q4FZZ4, TGT, NDUAA, Q5BJZ3, NDUA9, ODO1, ECHB, NDUS2, ECHA, PDK2, NDUS1, Q66HF3, ETFB, QCR1, DLDH, Q6PCU0, ATP5L, CACP, QCR8, CISY, SDHA, ACON, PRDX3, VDAC1
Species: Rattus norvegicus
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