Skip to main content
SpringerLink
Log in

Bigenomic Regulation of Cytochrome c Oxidase in Neurons and the Tight Coupling Between Neuronal Activity and Energy Metabolism

  • Chapter
  • First Online:
Mitochondrial Oxidative Phosphorylation

Part of the book series: Advances in Experimental Medicine and Biology ((volume 748))

Abstract

Cytochrome c oxidase is the terminal enzyme of the mitochondrial electron transport chain, without which oxidative metabolism cannot be carried to completion. It is one of only four unique, bigenomic proteins in mammalian cells. The holoenzyme is made up of three mitochondrial-encoded and ten nuclear-encoded subunits in a 1:1 stoichiometry. The ten nuclear subunit genes are located in nine different chromosomes. The coordinated regulation of such a multisubunit, multichromosomal, bigenomic enzyme poses a challenge. It is especially so for neurons, whose mitochondria are widely distributed in extensive dendritic and axonal processes, resulting in the separation of the mitochondrial from the nuclear genome by great distances. Neuronal activity dictates COX activity that reflects protein amount, which, in turn, is regulated at the transcriptional level. All 13 COX transcripts are up- and downregulated by neuronal activity. The ten nuclear COX transcripts and those for Tfam and Tfbms important for mitochondrial COX transcripts are transcribed in the same transcription factory. Bigenomic regulation of all 13 transcripts is mediated by nuclear respiratory factors 1 and 2 (NRF-1 and NRF-2). NRF-1, in addition, also regulates critical neurochemicals of glutamatergic synaptic transmission, thereby ensuring the tight coupling of energy metabolism and neuronal activity at the molecular level in neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145

    PubMed  CAS  Google Scholar 

  • Au HC, Scheffler IE (1998) Promoter analysis of the human succinate dehydrogenase iron-protein gene – both nuclear respiratory factors NRF-1 and NRF-2 are required. Eur J Biochem 251:164–174

    PubMed  CAS  Google Scholar 

  • Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen M, Kelly DP, Holloszy JO (2002) Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 16:1879–1886

    PubMed  CAS  Google Scholar 

  • Babb TL, Mikuni N, Najm I, Wylie C, Olive M, Dollar C, MacLennan H (2005) Pre- and postnatal expression of NMDA receptors 1 and 2B subunit proteins in the normal rat cortex. Epilepsy Res 64:23–30

    PubMed  CAS  Google Scholar 

  • Bachman NJ, Yang TL, Dasen JS, Ernst RE, Lomax MI (1996) Phylogenetic footprinting of the human cytochrome c oxidase subunit VB promoter. Arch Biochem Biophys 333:152–162

    PubMed  CAS  Google Scholar 

  • Bai X, Wong-Riley MTT (2003) Neuronal activity regulates protein and gene expressions of GluR2 in postnatal rat visual cortical neurons in culture. J Neurocytol 32:71–78

    PubMed  CAS  Google Scholar 

  • Batchelor AH, Piper DE, De la Brousse FC, McKnight SL, Wolberger C (1998) The structure of GABPalpha/beta: an ETS domain-ankyrin repeat heterodimer bound to DNA. Science 279:1037–1041

    PubMed  CAS  Google Scholar 

  • Becker TS, Burgess SM, Amsterdam AH, Allende ML, Hopkins N (1998) Not really finished is crucial for development of the zebrafish outer retina and encodes a transcription factor highly homologous to human nuclear respiratory factor-1 and avian initiation binding repressor. Development 125:4369–4378

    PubMed  CAS  Google Scholar 

  • Blesa JR, Prieto-Ruiz JA, Hernández JM, Hernández-Yago J (2007) NRF-2 transcription factor is required for human TOMM20 gene expression. Gene 391:198–208

    PubMed  CAS  Google Scholar 

  • Bruni F, Polosa PL, Gadaleta MN, Cantatore P, Roberti M (2010) Nuclear respiratory factor 2 induces the expression of many but not all human proteins acting in mitochondrial DNA transcription and replication. J Biol Chem 285:3939–3948

    PubMed  CAS  Google Scholar 

  • Burnashev N, Monyer H, Seeburg PH, Sakmann B (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8:189–198

    PubMed  CAS  Google Scholar 

  • Carter RS, Avadhani NG (1994) Cooperative binding of GA-binding protein transcription factors to duplicated transcription initiation region repeats of cytochrome c oxidase subunit IV gene. J Biol Chem 269:4381–4387

    PubMed  CAS  Google Scholar 

  • Carter RS, Bhat NK, Basu A, Avadhani NG (1992) The basal promoter elements of murine cytochrome c oxidase subunit IV gene consist of tandemly duplicated ETS motifs that bind to GABP-related transcription factors. J Biol Chem 267:23418–23426

    PubMed  CAS  Google Scholar 

  • De la Brousse FC, Birkenmeier EH, King DS, Rowe LB, McKnight SL (1994) Molecular and genetic characterization of GABP beta. Genes Dev 8:1853–1865

    PubMed  Google Scholar 

  • Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295:1306–1311

    PubMed  CAS  Google Scholar 

  • DeYoe EA, Trusk TC, Wong-Riley MTT (1995) Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey. Vis Neurosci 12:629–639

    PubMed  CAS  Google Scholar 

  • Dhar SS, Wong-Riley MTT (2009) Coupling of energy metabolism and synaptic transmission at the transcriptional level: role of nuclear respiratory factor 1 in regulating both cytochrome c oxidase and NMDA glutamate receptor subunit genes. J Neurosci 29:483–492

    PubMed  CAS  Google Scholar 

  • Dhar SS, Wong-Riley MTT (2010) Chromosome conformation capture of transcriptional interactions between cytochrome c oxidase genes and genes of glutamatergic synaptic transmission in neurons. J Neurochem 115:676–683

    PubMed  CAS  Google Scholar 

  • Dhar SS, Wong-Riley MTT (2011) The kinesin superfamily protein KIF17 is regulated by the same transcription factor (NRF-1) as its cargo NR2B in neurons. BBA – Mol. Cell Res 1813:403–411

    CAS  Google Scholar 

  • Dhar SS, Ongwijitwat S, Wong-Riley MTT (2008) Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J Biol Chem 283:3120–3129

    PubMed  CAS  Google Scholar 

  • Dhar SS, Ongwijitwat S, Wong-Riley MTT (2009a) Chromosome conformation capture of all 13 genomic loci in the transcriptional regulation of the multi-subunit bigenomic cytochrome c oxidase in neurons. J Biol Chem 284:18644–18650

    PubMed  CAS  Google Scholar 

  • Dhar SS, Liang HL, Wong-Riley MTT (2009b) Nuclear respiratory factor 1 co-regulates AMPA glutamate receptor subunit 2 and cytochrome c oxidase: tight coupling of glutamatergic transmission and energy metabolism in neurons. J Neurochem 108:1595–1606

    PubMed  CAS  Google Scholar 

  • Dhar SS, Liang HL, Wong-Riley MTT (2009c) Transcriptional coupling of synaptic transmission and energy metabolism: role of nuclear respiratory factor 1 in co-regulating neuronal nitric oxide synthase and cytochrome c oxidase genes in neurons. BBA – Mol. Cell Res 1793:1604–1613

    CAS  Google Scholar 

  • Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7–61

    PubMed  CAS  Google Scholar 

  • Evans MJ, Scarpulla RC (1989) Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. J Biol Chem 264:14361–14368

    PubMed  CAS  Google Scholar 

  • Evans MJ, Scarpulla RC (1990) NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev 4:1023–1034

    PubMed  CAS  Google Scholar 

  • Falkenberg M, Gaspari M, Rantanen A, Trifunovic A, Larsson NG, Gustafsson CM (2002) Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat Genet 31:289–294

    PubMed  CAS  Google Scholar 

  • Fisher RP, Clayton DA (1988) Purification and characterization of human mitochondrial transcription factor 1. Mol Cell Biol 8:3496–3509

    PubMed  CAS  Google Scholar 

  • Fonnum F (1984) Glutamate: a neurotransmitter in mammalian brain. J Neurochem 42:1–11

    PubMed  CAS  Google Scholar 

  • Garthwaite J (1991) Glutamate, nitric oxide and cell-cell signaling in the nervous system. Trends Neurosci 14:60–67

    PubMed  CAS  Google Scholar 

  • Gleyzer N, Vercauteren K, Scarpulla RC (2005) Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol Cell Biol 25:1354–1366

    PubMed  CAS  Google Scholar 

  • Gopalakrishnan L, Scarpulla RC (1995) Structure, expression, and chromosomal assignment of the human gene encoding nuclear respiratory factor 1. J Biol Chem 270:18019–18025

    PubMed  CAS  Google Scholar 

  • Goto M, Terada S, Kato M, Katoh M, Yokozeki T, Tabata I, Shimokawa T (2000) cDNA cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats. Biochem Biophys Res Commun 274:350–354

    PubMed  CAS  Google Scholar 

  • Gugneja S, Scarpulla RC (1997) Serine phosphorylation within a concise amino-terminal domain in nuclear respiratory factor 1 enhances DNA binding. J Biol Chem 272:18732–18739

    PubMed  CAS  Google Scholar 

  • Gugneja S, Virbasius CM, Scarpulla RC (1996) Nuclear respiratory factors 1 and 2 utilize similar glutamine-containing clusters of hydrophobic residues to activate transcription. Mol Cell Biol 16:5708–5716

    PubMed  CAS  Google Scholar 

  • Guo AL, Nie F, Wong-Riley MTT (2000) Human brain nuclear respiratory factor (NRF) 2α cDNA: isolation, subcloning, sequencing and in situ hybridization of transcripts in normal and visually deprived macaque visual system. J Comp Neurol 417:221–232

    PubMed  CAS  Google Scholar 

  • Hevner RF, Wong-Riley MTT (1989) Brain cytochrome oxidase: purification, antibody production, and immunohistochemical/histochemical correlations in the CNS. J Neurosci 9:3884–3898

    PubMed  CAS  Google Scholar 

  • Hevner RF, Wong-Riley MTT (1990) Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. J Neurosci 10:1331–1340

    PubMed  CAS  Google Scholar 

  • Hevner RF, Wong-Riley MTT (1991) Neuronal expression of nuclear and mitochondrial genes for cytochrome oxidase (CO) subunits analyzed by in situ hybridization; comparison with CO activity and protein. J Neurosci 11:1942–1958

    PubMed  CAS  Google Scholar 

  • Hevner RF, Wong-Riley MTT (1993) Mitochondrial and nuclear gene expression for cytochrome oxidase subunits are disproportionately regulated by functional activity in neurons. J Neurosci 13:1805–1819

    PubMed  CAS  Google Scholar 

  • Hevner RF, Liu S, Wong-Riley MTT (1995) A metabolic map of cytochrome oxidase in the rat brain: histochemical, densitometric and biochemical studies. Neuroscience 65:313–342

    PubMed  CAS  Google Scholar 

  • Hollmann M, Hartley M, Heinemann S (1991) Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252:851–853

    PubMed  CAS  Google Scholar 

  • Huo L, Scarpulla RC (1999) Multiple 5′-untranslated exons in the nuclear respiratory factor 1 gene span 47 kb and contribute to transcript heterogeneity and translational efficiency. Gene 233:213–224

    PubMed  CAS  Google Scholar 

  • Huo L, Scarpulla RC (2001) Mitochondrial DNA instability and peri-implantation lethality associated with targeted disruption of nuclear respiratory factor 1 in mice. Mol Cell Biol 21:644–654

    PubMed  CAS  Google Scholar 

  • Jackson DA, Iborra FJ, Manders EM, Cook PR (1998) Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HaLa nuclei. Mol Biol Cell 9:1523–1536

    PubMed  CAS  Google Scholar 

  • Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H (1994) Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12:1281–1289

    PubMed  CAS  Google Scholar 

  • Kadenbach B, Jaraush S, Hartmann R, Merle P (1983) Separation of mammalian cytochrome c oxidase into 13 polypeptides by a sodium dodecyl sulfate- gel electrophoresis procedure. Anal Biochem 129:517–521

    PubMed  CAS  Google Scholar 

  • Kadenbach B, Huttermann M, Arnold S, Lee I, Bender E (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic Biol Med 29:211–221

    PubMed  CAS  Google Scholar 

  • Keinänen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249:556–560

    PubMed  Google Scholar 

  • Kelly DP, Scarpulla RC (2004) Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18:357–368

    PubMed  CAS  Google Scholar 

  • Knutti D, Kralli A (2001) PGC-1, a versatile coactivator. Trends Endocrinol Metab 12:360–365

    PubMed  CAS  Google Scholar 

  • LaMarco K, Thompson CC, Byers BP, Walton EM, McKnight SL (1991) Identification of Ets- and Notch-related subunits in GA-binding protein. Science 253:789–792

    PubMed  CAS  Google Scholar 

  • Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP (2000) Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106:847–856

    PubMed  CAS  Google Scholar 

  • Leone TC, Lehman JJ, Finck BN, Schaeffer PJ, Wende AR, Boudina S, Courtois M, Wozniak DF, Sambandam N, Bernal-Mizrachi C, Chen Z, Holloszy JO, Medeiros DM, Schmidt RE, Saffitz JE, Abel ED, Semenkovich CF, Kelly DP (2005) PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 3:e101

    PubMed  Google Scholar 

  • Liang HL, Wong-Riley MTT (2006) Activity-dependent regulation of nuclear respiratory factor-1, nuclear respiratory factor-2, and peroxisome proliferators-activated receptor gamma coactivator-1 in neurons. Neuroreport 17:401–405

    PubMed  CAS  Google Scholar 

  • Liang HL, Ongwijitwat S, Wong-Riley MTT (2006) Bigenomic functional regulation of all 13 cytochrome c oxidase subunit transcripts in rat neurons in vitro and in vivo. Neuroscience 140:177–190

    PubMed  CAS  Google Scholar 

  • Liang HL, Dhar SS, Wong-Riley MTT (2010) p38 Mitogen-activated protein kinase and calcium channels mediate signaling in depolarization-induced activation of peroxisome proliferator-activated receptor gamma coactivator-1α in neurons. J Neurosci Res 88:640–649

    PubMed  CAS  Google Scholar 

  • Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jager S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, Spiegelman BM (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119:121–135

    PubMed  CAS  Google Scholar 

  • Ling JQ, Li T, Hu JF, Vu TH, Chen HL, Qiu XW, Cherry AM, Hoffman AR (2006) CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312:269–272

    PubMed  CAS  Google Scholar 

  • Liu S, Wong-Riley M (1994) Nuclear-encoded mitochondrial precursor protein: intramitochondrial delivery to dendrites and axon terminals of neurons and regulation by neuronal activity. J Neurosci 14:5338–5351

    PubMed  CAS  Google Scholar 

  • Loftis JM, Janowsky A (2003) The N-methyl-D-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol Ther 97:55–85

    PubMed  CAS  Google Scholar 

  • Lomeli H, Mosbacher J, Melcher T, Höger T, Geiger JRP, Kuner T, Monyer H, Higuchi M, Bach A, Seeburg PH (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266:1709–1713

    PubMed  CAS  Google Scholar 

  • Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R (2006) Interchromosomal interactions and olfactory receptor choice. Cell 126:403–413

    PubMed  CAS  Google Scholar 

  • Lowry OH (1975) Energy metabolism in brain and its control. In: Ingvar DH, Lassen NA (eds) Brain work: the coupling of function, metabolism, and blood flow in the brain. Alfred Benzon symposium VIII. Academic, New York, pp 48–64

    Google Scholar 

  • Meng H, Liang HL, Wong-Riley M (2007) Quantitative immune-electron microscopic analysis of depolarization-induced expression of PGC-1alpha in cultured rat visual cortical neurons. Brain Res 1175:10–16

    PubMed  CAS  Google Scholar 

  • Miele A, Dekker J (2009) Mapping cis- and trans-chromatin interaction networks using chromosome conformation capture (3C). Methods Mol Biol 464:105–121

    PubMed  Google Scholar 

  • Mori H, Mishina M (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219–1237

    PubMed  CAS  Google Scholar 

  • Mori M, Morita T, Ikeda F, Amaya Y, Tatibana M, Cohen PP (1981) Synthesis, intracellular transport, and processing of the precursor for mitochondrial ornithine transcarbamylase and carbamoylphosphate synthetase I in isolated hepatocytes. Proc Natl Acad Sci USA 78:6056–6060

    PubMed  CAS  Google Scholar 

  • Myers SJ, Peters J, Huang Y, Comer MB, Barthel F, Dingledine R (1998) Transcriptional regulation of the GluR2 gene: neural-specific expression, multiple promoters, and regulatory elements. J Neurosci 18:6723–6739

    PubMed  CAS  Google Scholar 

  • Nakanishi S (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258:597–603

    PubMed  CAS  Google Scholar 

  • Nie F, Wong-Riley M (1999) Nuclear respiratory factor-2 subunit protein: correlation with cytochrome oxidase and regulation by functional activity in the monkey primary visual cortex. J Comp Neurol 404:310–320

    PubMed  CAS  Google Scholar 

  • Ongwijitwat S, Wong-Riley MTT (2004) Functional analysis of the rat cytochrome c oxidase subunit 6A1 promoter in primary neurons. Gene 337:163–171

    PubMed  CAS  Google Scholar 

  • Ongwijitwat S, Wong-Riley MTT (2005) Is nuclear respiratory factor 2 a master transcriptional coordinator for all ten nuclear-encoded cytochrome c oxidase subunits in neurons? Gene 360:65–77

    PubMed  CAS  Google Scholar 

  • Ongwijitwat S, Liang HL, Graboyes EM, Wong-Riley MTT (2006) Nuclear respiratory factor 2 senses changing cellular energy demands and its silencing down-regulates cytochrome oxidase and other target gene mRNAs. Gene 374:39–49

    PubMed  CAS  Google Scholar 

  • Orrego F, Villanueva S (1993) The chemical nature of the main central excitatory transmitter: a critical appraisal based upon release studies and synaptic vesicle localization. Neuroscience 56:539–555

    PubMed  CAS  Google Scholar 

  • Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P (2004) Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36:1065–1071

    PubMed  CAS  Google Scholar 

  • Palmer CL, Lin W, Hastie PGR, Toward M, Korolchuk VI, Burbidge SA, Banting G, Collingridge GL, Isaac JTR, Henley JM (2005) Hippocalcin functions as a calcium sensor in hippocampal LTD. Neuron 47:487–494

    PubMed  CAS  Google Scholar 

  • Pellegrini-Giampietro DE, Gorter JA, Bennett MV, Zukin RS (1997) The GluR2 (GluR-B) hypothesis: Ca2+-permeable AMPA receptors in neurologic disorders. Trends Neurosci 20:464–470

    PubMed  CAS  Google Scholar 

  • Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829–839

    PubMed  CAS  Google Scholar 

  • Reid GA, Yonetani T, Schatz G (1982) Import of proteins into mitochondria: import and maturation of the mitochondrial intermembrane space enzyme cytochemistry b 2 and cytochrome c peroxidase in intact yeast cells. J Biol Chem 257:13068–13074

    PubMed  CAS  Google Scholar 

  • Ristevski S, O’Leary DA, Thornell AP, Owen MJ, Kola I, Hertzog PJ (2004) The ETS transcription factor GABPalpha is essential for early embryogenesis. Mol Cell Biol 24:5844–5849

    PubMed  CAS  Google Scholar 

  • Salussolia CL, Prodromou ML, Borker P, Wollmuth LP (2011) Arrangement of subunits in functional NMDA receptors. J Neurosci 31:11295–11304

    PubMed  CAS  Google Scholar 

  • Scarpulla RC (1997) Nuclear control of respiratory chain expression in mammalian cells. J Bioenerg Biomembr 29:109–119

    PubMed  CAS  Google Scholar 

  • Scarpulla RC (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576:1–14

    PubMed  CAS  Google Scholar 

  • Scarpulla RC (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1 related coactivator. Ann N Y Acad Sci 1147:321–334

    PubMed  CAS  Google Scholar 

  • Scarpulla RC (2011) Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 1813:1269–1278

    PubMed  CAS  Google Scholar 

  • Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei CL, Ruan Y, Bieker JJ, Fraser P (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42:53–61

    PubMed  CAS  Google Scholar 

  • Seelan RS, Gopalakrishnan L, Scarpulla RC, Grossman LI (1996) Cytochrome c oxidase subunit VIIa liver isoform. Characterization and identification of promoter elements in the bovine gene. J Biol Chem 271:2112–2120

    PubMed  CAS  Google Scholar 

  • Setou M, Nakagawa T, Seog DH, Hirokawa N (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288:1796–1802

    PubMed  CAS  Google Scholar 

  • Sommer B, Keinänen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Köhler M, Takagi T, Sakmann B, Seeburg PH (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249:1580–1585

    PubMed  CAS  Google Scholar 

  • Spilianakis CG, Flavell RA (2004) Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat Immunol 5:1017–1027

    PubMed  CAS  Google Scholar 

  • St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397–408

    PubMed  CAS  Google Scholar 

  • Streit P (1984) Glutamate and aspartate as transmitter candidate for systems of the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 2, Functional properties of cortical cells. Plenum, New York, pp 119–143

    Google Scholar 

  • Tanaka H, Grooms SY, Bennett MVL, Zukin RS (2000) The AMPAR subunit GluR2: still front and center-stage. Brain Res 886:190–207

    PubMed  CAS  Google Scholar 

  • Thompson CC, Brown TA, McKnight SL (1991) Convergence of Ets- and notch-related structural motifs in a heteromeric DNA binding complex. Science 253:762–768

    PubMed  CAS  Google Scholar 

  • Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B (1991) Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252:1715–1718

    PubMed  CAS  Google Scholar 

  • Virbasius JV, Scarpulla RC (1991) Transcriptional activation through ETS domain binding sites in the cytochrome c oxidase subunit IV gene. Mol Cell Biol 11:5631–5638

    PubMed  CAS  Google Scholar 

  • Virbasius JV, Scarpulla RC (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci USA 91:1309–1313

    PubMed  CAS  Google Scholar 

  • Virbasius JV, Virbasius CA, Scarpulla RC (1993a) Identity of GABP with NRF-2: a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev 7:380–392

    PubMed  CAS  Google Scholar 

  • Virbasius CA, Virbasius JV, Scarpulla RC (1993b) NRF-1, an activator involved in nuclear-mitochondrial interaction, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes Dev 7:2431–2445

    PubMed  CAS  Google Scholar 

  • Washburn MS, Numberger M, Zhang S, Dingledine R (1997) Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17:9393–9406

    PubMed  CAS  Google Scholar 

  • Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94–101

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT (2010) Energy metabolism of the visual system. Eye Brain 2:99–116

    Google Scholar 

  • Wong-Riley M, Carroll EW (1984) Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307:262–264

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT, Jacobs P (2002) AMPA glutamate receptor subunit 2 in normal and visually deprived macaque visual cortex. Vis Neurosci 19:563–573

    PubMed  Google Scholar 

  • Wong-Riley MTT, Tripathi SC, Trusk TC, Hoppe DA (1989a) Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: I. Quantitative electron-microscopic (EM) analysis of neurons. Vis Neurosci 2:483–497

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT, Trusk TC, Tripathi SC, Hoppe DA (1989b) Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: II. Quantitative electron-microscopic (EM) analysis of neuropil. Vis Neurosci 2:499–514

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT, Mullen MA, Huang Z, Guyer C (1997) Brain cytochrome oxidase subunit complementary DNAs: isolation, subcloning, sequencing, light and electron microscopic in situ hybridization of transcripts, and regulation by neuronal activity. Neuroscience 76:1035–1055

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT, Nie F, Hevner RF, Liu S (1998a) Brain cytochrome oxidase. In: Gonzalez-Lima F (ed) Cytochrome oxidase in neuronal metabolism and Alzheimer’s disease. Plenum, New York, pp 1–53

    Google Scholar 

  • Wong-Riley M, Anderson B, Liebl W, Huang Z (1998b) Neurochemical organization of the macaque striate cortex: correlation of cytochrome oxidase with Na+K+ATPase, NADPH-diaphorase, nitric oxide synthase, and N-methyl-D-aspartate receptor subunit 1. Neuroscience 83:1025–1045

    PubMed  CAS  Google Scholar 

  • Wong-Riley MT, Huang Z, Liebl W, Nie F, Xu H, Zhang C (1998c) Neurochemical organization of the macaque retina: effect of TTX on levels and gene expression of cytochrome oxidase and nitric oxide synthase and on the immunoreactivity of Na+K+ATPase and NMDA receptor subunit 1. Vision Res 38:1455–1477

    PubMed  CAS  Google Scholar 

  • Wong-Riley MTT, Yang SJ, Liang HL, Ning G, Jacobs P (2005) Quantitative immuno-electron microscopic analysis of nuclear respiratory factor 2 alpha and beta subunits: normal distribution and activity-dependent regulation in mammalian visual cortex. Vis Neurosci 22:1–18

    PubMed  Google Scholar 

  • Wong-Riley MTT, Liang HL, Ongwijitwat S (2008) Activity-dependent bigenomic transcriptional regulation of cytochrome c oxidase in neurons, Chapter 11. In: Dudek SM (ed) Transcriptional regulation by neuronal activity: to the nucleus and back. Springer, New York, pp 209–228

    Google Scholar 

  • Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115–124

    PubMed  CAS  Google Scholar 

  • Yang SJ, Liang HL, Ning G, Wong-Riley MTT (2004) Ultrasturctural study of depolarization-induced translocation of NRF-2 transcription factor in cultured rat visual cortical neurons. Eur J Neurosci 19:1153–1162

    PubMed  Google Scholar 

  • Yang SJ, Liang HL, Wong-Riley MTT (2006) Activity-dependent transcriptional regulation of nuclear respiratory factor-1 in cultured rat visual cortical neurons. Neuroscience 141:1181–1192

    PubMed  CAS  Google Scholar 

  • Zhang C, Wong-Riley M (1999) Expression and regulation of NMDA receptor subunit R1 and neuronal nitric oxide synthase in cortical neuronal cultures: correlation with cytochrome oxidase. J Neurocytol 28:525–539

    PubMed  CAS  Google Scholar 

  • Zhang C, Wong-Riley MTT (2000a) Synthesis and degradation of cytochrome oxidase subunit mRNA in neurons: differential bigenomic regulation by neuronal activity. J Neurosci Res 60:338–344

    PubMed  CAS  Google Scholar 

  • Zhang C, Wong-Riley M (2000b) Depolarization stimulation upregulates GA-binding protein in neurons: a transcription factor involved in the bigenomic expression of cytochrome oxidase subunits. Eur J Neurosci 12:1013–1023

    PubMed  CAS  Google Scholar 

  • Zhou GL, Xin L, Song W, Di LJ, Liu G, Wu XS, Liu DP, Liang CC (2006) Active chromatin hub of the mouse alpha-globin locus forms in a transcription factory of clustered house-keeping genes. Mol Cell Biol 26:5096–5105

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author expresses her deep appreciation for the valuable contributions from her past and present colleagues in her laboratory as well as in the relevant fields of bioenergetics and neuroscience. She also appreciates the continuous support from the National Institutes of Health. The current support is from NIH grant EY018441.

Author information

Authors and Affiliations

  1. Department of Cell Biology, Neurobiology and Anatomy, Medical College of Wisconsin, Milwaukee, WI, 53226, USA

    Margaret T. T. Wong-Riley

Authors
  1. Margaret T. T. Wong-Riley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margaret T. T. Wong-Riley .

Editor information

Editors and Affiliations

  1. Philipps-Universitaet Marburg, Marburg, 35032, Germany

    Bernhard Kadenbach

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Wong-Riley, M.T.T. (2012). Bigenomic Regulation of Cytochrome c Oxidase in Neurons and the Tight Coupling Between Neuronal Activity and Energy Metabolism. In: Kadenbach, B. (eds) Mitochondrial Oxidative Phosphorylation. Advances in Experimental Medicine and Biology, vol 748. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3573-0_12

Download citation

Publish with us

Policies and ethics

Search

Navigation