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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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Denis M, Dupas T, Persello A, Dontaine J, Bultot L, Betus C, Pelé T, Dhot J, Erraud A, Maillard A, Montnach J, Leroux AA, Bigot-Corbel E, Vertommen D, Rivière M, Lebreton J, Tessier A, Waard M, Bertrand L, Rozec B, Lauzier B. An O-GlcNAcylomic Approach Reveals ACLY as a Potential Target in Sepsis in the Young Rat. International journal of molecular sciences 2021 22(17) 34502162

Abstract:
Sepsis in the young population, which is particularly at risk, is rarely studied. O-GlcNAcylation is a post-translational modification involved in cell survival, stress response and metabolic regulation. O-GlcNAc stimulation is beneficial in adult septic rats. This modification is physiologically higher in the young rat, potentially limiting the therapeutic potential of O-GlcNAc stimulation in young septic rats. The aim is to evaluate whether O-GlcNAc stimulation can improve sepsis outcome in young rats. Endotoxemic challenge was induced in 28-day-old rats by lipopolysaccharide injection (E. Coli O111:B4, 20 mg·kg^-1) and compared to control rats (NaCl 0.9%). One hour after lipopolysaccharide injection, rats were randomly assigned to no therapy, fluidotherapy (NaCl 0.9%, 10 mL·kg^-1) ± NButGT (10 mg·kg^-1) to increase O-GlcNAcylation levels. Physiological parameters and plasmatic markers were evaluated 2h later. Finally, untargeted mass spectrometry was performed to map cardiac O-GlcNAcylated proteins. Lipopolysaccharide injection induced shock with a decrease in mean arterial pressure and alteration of biological parameters (p < 0.05). NButGT, contrary to fluidotherapy, was associated with an improvement of arterial pressure (p < 0.05). ATP citrate lyase was identified among the O-GlcNAcylated proteins. In conclusion, O-GlcNAc stimulation improves outcomes in young septic rats. Interestingly, identified O-GlcNAcylated proteins are mainly involved in cellular metabolism.

O-GlcNAc proteins:
A0A096MJ01, A0A096MK30, A0A096MKD4, A0A096P6L8, A0A0G2JSH9, A0A0G2JSP8, A0A0G2JSR0, A0A0G2JSU7, A0A0G2JSW3, A0A0G2JTG7, A0A0G2JTP6, A0A0G2JV65, A0A0G2JVG3, A0A0G2JVH4, A0A0G2JW41, A0A0G2JW94, A0A0G2JWK2, A0A0G2JWS2, A0A0G2JYK0, A0A0G2JZF0, A0A0G2K0F5, A0A0G2K3K2, A0A0G2K3Z9, A0A0G2K401, A0A0G2K5P5, A0A0G2K654, A0A0G2K719, A0A0G2K7F7, A0A0G2K9P4, A0A0G2K9Q9, A0A0G2KAK2, A0A0G2KB63, A0A0H2UHM5, A0A0H2UHQ9, A0A0H2UHZ6, A0A0H2UI36, A0A0U1RRV7, ROA2, B0BNG3, CAH1, SCOT1, B2RYW3, C0JPT7, D3ZCV0, D3ZG43, D3ZIC4, D3ZQM0, D3ZUB0, D3ZZ68, D3ZZN3, D4A0T0, D4A5E5, D4A6Q4, SYNP2, D4A7X7, D4A8X8, D4AA63, D4ACC2, F1LM30, F1LM47, F1LMP9, DESP, F1LP05, F1LP30, F1LSC3, S2512, S2513, F1M3H8, F1M820, F1M865, F1M944, F1M953, F1MAA7, F1MAF7, G3V6E1, G3V6H0, G3V6H5, G3V6P7, G3V6S0, G3V6T7, G3V6Y6, G3V7C6, G3V7J0, G3V826, G3V885, G3V8B0, G3V8L3, G3V8V3, G3V9A3, G3V9U2, M0R5J4, M0R735, M0R757, M0R7S5, M0R9L0, PRDX6, C1QBP, HSPB2, ACOT2, HCD2, PARK7, MDHC, AATM, HBA, FIBG, GPX1, ROA1, MDHM, LDHA, PDIA1, G3P, GSTP1, ALDOA, EF2, AT1A1, BIP, RPN1, ODP2, MLRV, KCRS, HS71A, ATPB, CLH1, AT2A2, DMD, ALDH2, KPYM, AL1A7, ETFA, A1I3, CAH3, FIBB, ECHM, ACADL, PGAM2, MYL3, PGK1, ACLY, THIL, ACSL1, CPT2, CSK21, NDUV2, AT5F1, NDKB, NB5R3, IGG2A, IGG2B, LAC2, UCRI, SDHB, TNNI3, CRYAB, PPIB, PGAM1, RPN2, CAH2, TCPA, VIME, PEBP1, ATP5H, EZRI, QCR2, HS90B, 1433B, ATPG, CRIP2, RSSA, CAV1, LDHB, HSPB1, COF1, TERA, DPYL2, TPIS, DESM, ODPB, TNNT2, AL1A1, ES1, IDHP, MYPC, PSA6, ARF3, 1433G, 1433E, EF1A2, H4, RAN, RS3, AP2B1, RL40, HSP7C, CH60, PHB1, ACTC, 1433T, TBA1A, 1433F, TBB5, NUP54, VDAC2, HS90A, EFTU, PNPH, HSPB6, PTBP1, H2B1, MUG1, ATPO, ANXA2, ADT2, K2C8, PRRC1, NIT2, Q498N4, ACSF2, H2A3, K2C6A, Q4G079, AGFG1, Q4PP99, Q4V8E1, EHD2, Q52KS1, NDUAA, Q5BJZ3, Q5D059, Q5M9H2, Q5RJR9, UBA1, Q5XFV4, LPP, Q5XI38, GDIR1, ODO1, TBA4A, Q5XIH3, ECHB, PDLI5, A1M, CPT1B, NDUS2, ECHA, ENPL, NDUS1, Q66HF3, MAVS, AMPL, ETFB, QCR1, K1C42, Q6IFU9, K1C14, K1C15, K1C13, K1C10, K2C75, K2C1, HNRPU, Q6IMZ3, TS101, RAB1A, PLAK, K2C5, DLDH, SYWC, TBA1B, Q6P9Y4, Q6PDV6, CNDP2, ROA3, CACP, DEST, Q7TQ70, CISY, Q91XN6, SDHA, IDH3A, ACON, AIFM1, MYG, TGM2, HCDH, VDAC1, SC31A