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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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Clark PM, Dweck JF, Mason DE, Hart CR, Buck SB, Peters EC, Agnew BJ, Hsieh-Wilson LC. Direct in-gel fluorescence detection and cellular imaging of O-GlcNAc-modified proteins. Journal of the American Chemical Society 2008 130(35) 18683930
Abstract:
We report an advanced chemoenzymatic strategy for the direct fluorescence detection, proteomic analysis, and cellular imaging of O-GlcNAc-modified proteins. O-GlcNAc residues are selectively labeled with fluorescent or biotin tags using an engineered galactosyltransferase enzyme and [3 + 2] azide-alkyne cycloaddition chemistry. We demonstrate that this approach can be used for direct in-gel detection and mass spectrometric identification of O-GlcNAc proteins, identifying 146 novel glycoproteins from the mammalian brain. Furthermore, we show that the method can be exploited to quantify dynamic changes in cellular O-GlcNAc levels and to image O-GlcNAc-glycosylated proteins within cells. As such, this strategy enables studies of O-GlcNAc glycosylation that were previously inaccessible and provides a new tool for uncovering the physiological functions of O-GlcNAc.
O-GlcNAc proteins:
A0A0G2JYI7, A0A0G2K931, A0A0G2KAS9, ROA2, OTUB1, SEP11, B5DFG5, D3ZM69, HCFC1, D3ZQM0, D3ZUY8, D3ZVQ0, D4A0B4, D4A133, D4A1L2, D4A554, D4AA63, D4ABT8, D4ACB8, E9PT29, E9PTR4, S2512, RPGF2, F1M3L4, F1M3W5, F1M7Y3, F1M8R0, F1M949, F1M9V7, G3V7M0, G3V8Q8, HNRPC, SERA, AMPH, DCLK1, NCDN, CTND2, DNM1L, PICAL, CLIP2, ANK3, PACS1, HSP74, BSN, PTN23, AATM, CRYAA, ROA1, ENOA, HXK1, ENOG, ODP2, ALDOC, GLNA, SYN1, SORL, PLCB1, ATPB, DHE3, KCC2A, AT2A2, PDIA3, KPYM, FAS, AATC, MTAP2, MAP1B, ATPA, SPTN1, PGK1, HMCS1, AP2A2, CSK21, PO3F1, DYN1, MK03, AINX, THOP1, PGAM1, VPP1, ODPA, DCTN1, MARCS, MAP1A, 1433B, DYHC1, TERA, RP3A, PFKAM, PFKAP, ANXA6, TPIS, ODPB, NU153, GDIA, HUWE1, PYGB, GBB1, SNAA, NCKP1, OGT1, ACTB, HNRPK, 1433G, RS8, 1433E, RL7A, EF1A1, ACTA, VATB2, RS3, AP2B1, CH60, RACK1, PP2BA, KAPCB, 1433T, EF2K, VDAC2, GNAQ, TBB2A, FSCN1, ARPC2, CAND1, AP180, ADT1, ANXA2, ADT2, MYPT1, MIC60, TBB2B, CARM1, SRPRB, RD23B, TBB3, RBMX, OXR1, Q4V8F6, ZFR, WASF1, E41L5, RUFY3, DTBP1, SHLB2, Q5RJQ1, WDR1, IF4A2, CAPZB, ODO1, TBA4A, TCPB, SPTB2, 4EBP1, CAPS1, SYNJ1, DPYL1, DPYL4, DPYL3, CAMKV, KCC1A, MAP6, NDUS2, BACH, HS105, NDUS1, MAVS, PURB, QCR1, Q6AY07, Q6AYI1, PLAK, TBB4B, ROA3, Q6XLI7, PGAP1, FMR1, RB6I2, COR1A, IDH3A, PABP1, TALDO, DPYL5, WNK1, RIMS1, SEPT5, UBQL1, PCLO, MYH10, Q9JMB3, NSF, FKBP4, SHAN2, SRCN1, MYO5A, CRYM, GORS2, E41L1, GUAD, SEPT7, PACN1, Q9Z1X8, HOME1, GIT1, CTBP1, SC31A
Species: Mus musculus, Rattus norvegicus, Bos taurus
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Park J, Kwon H, Kang Y, Kim Y. Proteomic analysis of O-GlcNAc modifications derived from streptozotocin and glucosamine induced beta-cell apoptosis. Journal of biochemistry and molecular biology 2007 40(6) 18047804
Abstract:
The post-translational modifications of Ser and Thr residues by O-linked beta-N-acetylglucosamine (O-GlcNAc), i.e., O-GlcNAcylation, is considered a key means of regulating signaling, in a manner analogous to protein phosphorylation. Furthermore, it has been suggested that the increased flux of glucose through the hexosamine biosynthetic pathway (HBP) stimulates O-GlcNAcylation, and that this may be responsible for many of the manifestations of type 2 diabetes mellitus. To determine whether excessive O-GlcNAcylation of target proteins results in pancreatic beta cell dysfunction, we increased nucleocytoplasmic protein O-GlcNAcylation levels in beta cells by exposing them to streptozotocin and/or glucosamine. Streptozotocin and glucosamine co-treatment increased OGlcNAcylated proteomic patterns as assessed by immunoblotting, and these increases in nuclear and cytoplasmic protein O-GlcNAcylations were accompanied by impaired insulin secretion and enhanced apoptosis in pancreatic beta cells. This observed beta cell dysfunction prompted us to examine Akt and Bcl-2 family member proteins to determine which proteins are O-GlcNAcylated under conditions of high HBP throughput, and how these proteins are associated with beta cell apoptosis. Eventually, we identified ten new O-GlcNAcylated proteins that were expressed during beta cell apoptosis, and analyzed the functional implications of these proteins in relation to pancreatic beta cell dysfunction.
O-GlcNAc proteins:
ENOA, PDIA1, EF2, KCRB, ATPB, RSSA, TERA, ANXA4, CH60, ACTG, TBB5, K2C8, TCPE, QCR1, CLIC1, Q6P3V8, IDH3A
Species: Rattus norvegicus
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