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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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Fourneau J, Cieniewski-Bernard C, Canu MH, Duban-Deweer S, Hachani J, Bastide B, Dupont E. Optimization of 2-DE and multiplexed detection of O-GlcNAcome, phosphoproteome and whole proteome protocol of synapse-associated proteins within the rat sensorimotor cortex. Journal of neuroscience methods 2020 343 32574643
Abstract:
Several studies have shown the importance of phosphorylation, O-GlcNAcylation and their interplay in neuronal processes.
O-GlcNAc proteins:
NFL, SYT1, ACTB, NDUS8, NDUA8, VDAC1
Species: Mus musculus, Rattus norvegicus
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Dong DL, Xu ZS, Hart GW, Cleveland DW. Cytoplasmic O-GlcNAc modification of the head domain and the KSP repeat motif of the neurofilament protein neurofilament-H. The Journal of biological chemistry 1996 271(34) 8702840
Abstract:
Neurofilaments, the major intermediate filaments in large myelinated neurons, are essential for specifying proper axonal caliber. Mammalian neurofilaments are obligate heteropolymers assembled from three polypeptides, neurofilament (NF)-H, NF-M, and NF-L, each of which undergoes phosphorylation at multiple sites. NF-M and NF-L are known to be modified by O-linked N-acetylglucosamine (O-GlcNAc) (Dong, D. L.-Y., Xu, Z.-S., Chevrier, M. R., Cotter, R. J., Cleveland, D. W., and Hart, G. W. (1993) J. Biol. Chem. 268, 16679-16687). Here we further report that NF-H is extensively modified by O-GlcNAc at Thr53, Ser54, and Ser56 in the head domain and, somewhat surprisingly, at multiple sites within the Lys-Ser-Pro repeat motif in the tail domain, a region in assembled neurofilaments known to be nearly stoichiometrically phosphorylated on each of the approximately 50 KSP repeats. Beyond the earlier identified sites on NF-M and NF-L, O-GlcNAc sites on Thr19 and Ser34 of NF-M and Ser34 and Ser48 of NF-L are also determined here, all of which are localized in head domain sequences critical for filament assembly. The proximity of O-GlcNAc and phosphorylation sites in both head and tail domains of each subunit indicates that these modifications may influence one another and play a role in filament assembly and network formation.
O-GlcNAc proteins:
NFM, NFM, NFH, NFL
Species: Mus musculus, Rattus norvegicus
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