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Individual Biochemical Behaviour Versus Biological Robustness: Spotlight on the Regulation of Cytochrome c Oxidase

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Mitochondrial Oxidative Phosphorylation

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

Abstract

During evolution from prokaryotes to eukaryotes, the main function of cytochrome c oxidase (COX), i.e., the coupling of oxygen reduction to proton translocation without the production of ROS (reactive oxygen species) remained unchanged demonstrating its robustness. A new regulation of respiration by the ATP/ADP ratio was introduced in eukaryotes based on nucleotide interaction with the added COX subunit IV. This allosteric ATP-inhibition was proposed to keep the mitochondrial membrane potential (ΔΨm) at low healthy values and thus prevents the formation of ROS at complexes I and III. ROS have been implicated in various degenerative diseases. The allosteric ATP-inhibition of COX is reversibly switched on and off by phosphorylation of COX at a serine or threonine. In more than 100 individual preparations of rat heart and liver mitochondria, prepared under identical conditions, the extent of allosteric ATP-inhibition varied. This variability correlates with the variable inhibition of uncoupled respiration in intact isolated mitochondria by ATP. It is concluded that in higher organisms the allosteric ATP-inhibition is continually switched on and off by neuronal signalling in order to change oxidative phosphorylation from optimal efficiency with lower rate of ATP synthesis under resting conditions (low ΔΨm and ROS production) to maximal rate of ATP synthesis under active (working, stress) conditions (elevated ΔΨm and ROS production).

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References

  • Acin-Perez R, Gatti DL, Bai Y, Manfredi G (2011) Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab 13:712–719

    PubMed  CAS  Google Scholar 

  • Anthony G, Stroh A, Lottspeich F, Kadenbach B (1990) Different isozymes of cytochrome c oxidase are expressed in bovine smooth muscle and skeletal or heart muscle. FEBS Lett 277:97–100

    PubMed  CAS  Google Scholar 

  • Anthony G, Reimann A, Kadenbach B (1993) Tissue-specific regulation of bovine heart cytochrome c oxidase by ADP via interaction with subunit VIa. Proc Natl Acad Sci USA 90:1652–1656

    PubMed  CAS  Google Scholar 

  • Arnold S (1997) The structure of the cytochrome c oxidase of various vertebrates and its regulation by thyreoid hormone and the energy metabolism of cells. Dissertation, Fachbereich Chemie, Philipps-Universität, Marburg

    Google Scholar 

  • Arnold S, Kadenbach B (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur J Biochem 249:350–354

    PubMed  CAS  Google Scholar 

  • Arnold S, Kadenbach B (1999) The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett 443:105–108

    PubMed  CAS  Google Scholar 

  • Arnold S, Goglia F, Kadenbach B (1998) 3,5-diiodothyronine binds to subunit Va of cytochrome c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur J Biochem 252:325–330

    PubMed  CAS  Google Scholar 

  • Baden KN, Murray J, Capaldi RA, Guillemin K (2007) Early developmental pathology due to cytochrome c oxidase deficiency is revealed by a new zebrafish model. J Biol Chem 282:34839–34849

    PubMed  CAS  Google Scholar 

  • Balaban RS (1990) Regulation of oxidative phosphorylation in the mammalian cell. Am J Physiol 258:C377–C389

    PubMed  CAS  Google Scholar 

  • Balaban RS, Kantor HL, Katz LA, Briggs RW (1986) Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science 232(4754):1121–1123

    PubMed  CAS  Google Scholar 

  • Beauvoit B, Rigoulet M (2001) Regulation of cytochrome c oxidase by adenylic nucleotides. Is oxidative phosphorylation feedback regulated by its end-products? IUBMB Life 52:143–152

    PubMed  CAS  Google Scholar 

  • Bender E, Kadenbach B (2000) The allosteric ATP-inhibition of cytochrome c oxidase is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett 466:130–134

    PubMed  CAS  Google Scholar 

  • Bjornson KP, Modrich P (2003) Differential and simultaneous adenosine di- and triphosphate binding by MutS. J Biol Chem 278:18557–18562

    PubMed  CAS  Google Scholar 

  • Bolli R, Nalecz KA, Azzi A (1985) The interconversion between monomeric and dimeric bovine heart cytochrome c oxidase. Biochimie 67:119–128

    PubMed  CAS  Google Scholar 

  • Bonne G, Seibel P, Possekel S, Marsac C, Kadenbach B (1993) Expression of humen cytochrome c oxidase subunits during fetal development. Eur J Biochem 217:1099–1107

    PubMed  CAS  Google Scholar 

  • Bylund-Fellenius AC, Davidsson M, Arvidsson A, Elander A, Scherstén T (1982) Optimal conditions for assay of cytochrome-c-oxidase activity in human skeletal muscle tissue. Clin Physiol 2:71–79

    PubMed  CAS  Google Scholar 

  • Capaldi RA, Marusich MF, Taanman JW (1995) Mammalian cytochrome-c oxidase: characterization of enzyme and immunological detection of subunits in tissue extracts and whole cells. Methods Enzymol 260:117–132

    PubMed  CAS  Google Scholar 

  • Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem 217:409–427

    PubMed  CAS  Google Scholar 

  • Chrzanowska-Lightowlers ZM, Turnbull DM, Lightowlers RN (1993) A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Anal Biochem 214:45–49

    PubMed  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52:601–623

    PubMed  CAS  Google Scholar 

  • Dalmonte ME, Forte E, Genova ML, Giuffrè A, Sarti P, Lenaz G (2009) Control of respiration by cytochrome c oxidase in intact cells: role of the membrane potential. J Biol Chem 284:32331–32335

    PubMed  CAS  Google Scholar 

  • Dröse S, Brandt U (2008) The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J Biol Chem 283:21649–21654

    PubMed  Google Scholar 

  • Fang J-K, Prabu SK, Sepuri NB, Raza H, Anandatheerthavarada HK, Galati D, Spear J, Avadhani NG (2007) Site specific phosphorylation of cytochrome c oxidase subunits I, IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion. FEBS Lett 581:1302–1310

    PubMed  CAS  Google Scholar 

  • Ferguson-Miller S, Brautigan DL, Margoliash E (1976) Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes c with binding to mitochondrial cytochrome c oxidase. J Biol Chem 251:1104–1115

    PubMed  CAS  Google Scholar 

  • Ferguson-Miller S, Brautigan DL, Margoliash E (1978) Definition of cytochrome c binding domains by chemical modification. III. Kinetics of reaction of carboxydinitrophenyl cytochromes c with cytochrome c oxidase. J Biol Chem 253:149–159

    PubMed  CAS  Google Scholar 

  • Follmann K, Arnold S, Ferguson-Miller S, Kadenbach B (1998) Cytochrome c oxidase activity from eukaryotes but not from prokaryotes is allosterically inhibited by ATP. Biochem Mol Biol Intern 45:1047–1055

    CAS  Google Scholar 

  • Frank V, Kadenbach B (1996) Regulation of the H+/e- stoichiometry of cytochrome c oxidase from bovine heart by intraliposomal ATP/ADP ratios. FEBS Lett 382:121–124

    PubMed  CAS  Google Scholar 

  • Freeman M (2000) Feedback control of intercellular signalling in development. Nature 408(6810):313–319

    PubMed  CAS  Google Scholar 

  • From AHL, Zimmer SD, Michurski SP, Mohanakrishnan P, Ulstad VK, Thoma WJ, Ugurbil K (1990) Regulation of the oxidative phosphorylation rate in the intact cell. Biochemistry 29:3731–3743

    PubMed  CAS  Google Scholar 

  • Groen AK, Wanders RJA, Westerhoff HV, van der Meer R, Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257:2754–2757

    PubMed  CAS  Google Scholar 

  • Hakvoort TBM, Moolenaar K, Lankvelt AHM, Singorgo KMC, Dekker HL, Muijsers OA (1987) Separation, stability and kinetics of monomeric and dimeric bovine heart cytochrome c oxidase. Biochim Biophys Acta 894:347–354

    PubMed  CAS  Google Scholar 

  • Helling S, Vogt S, Rhiel A, Ramzan R, Wen L, Marcus K, Kadenbach B (2008) Phosphorylation and kinetics of mammalian cytochrome c oxidase. Mol Cell Proteomics 7:1714–1724

    PubMed  CAS  Google Scholar 

  • Helling S, Hüttemann H, Ramzan R, Kim SH, Lee I, Müller T, Langenfeld E, Meyer HE, Kadenbach B, Vogt S, Marcus K (2012) Multiple phosphorylations of cytochrome c oxidase and their functions. Proteomics 12:950–959

    Google Scholar 

  • Hendler RW, Pardhasaradhi K, Reynafarje B, Ludwig B (1991) Comparison of energy-transducing capabilities of the two- and three-subunit cytochromes aa3 from Paracoccus denitrificans and the 13-subunit beef heart enzyme. Biophys J 60:415–423

    PubMed  CAS  Google Scholar 

  • Hüther F-J, Kadenbach B (1987) ADP increases the affinity for cytochrome c by interaction with the matrix side of bovine heart cytochrome c oxidase. Biochem Biophys Res Commun 147:1268–1275

    PubMed  Google Scholar 

  • Hüttemann M, Kadenbach B, Grossman LI (2001) Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267:111–123

    PubMed  Google Scholar 

  • Hüttemann M, Jaradat S, Grossman LI (2003) Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb – the counterpart to testes-specific cytochrome c? Mol Reprod Dev 66:8–16

    PubMed  Google Scholar 

  • Hüttemann M, Lee I, Pecinova A, Pecina P, Przyklenk K, Doan JW (2008) Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. J Bioenerg Biomembr 40:445–456

    PubMed  Google Scholar 

  • Hüttemann M, Helling S, Sanderson TH, Sinkler C, Samavati L, Mahapatra G, Varughese A, Lu G, Liu J, Ramzan R, Vogt S, Grossman LI, Doan JW, Marcus K, Lee I (2012) Regulation of mitochondrial respiration and apoptosis through cell signaling: cytochrome c oxidase and cytochrome c in ischemia/reperfusion injury and inflammation. Biochim Biophys Acta 1817:598–609

    Google Scholar 

  • Inoue Y, Shingyoji C (2007) The roles of noncatalytic ATP binding and ADP binding in the regulation of dynein motile activity in flagella. Cell Motil Cytoskeleton 64:690–704

    PubMed  CAS  Google Scholar 

  • Kadenbach B, Arnold S (1999) A second mechanism of respiratory control. FEBS Lett 447:131–134

    PubMed  CAS  Google Scholar 

  • Kadenbach B, Arnold S, Lee I, Hüttemann M (2004) The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases. Biochim Biophys Acta 1655:400–408

    PubMed  CAS  Google Scholar 

  • Kadenbach B, Ramzan R, Wen L, Vogt S (2010) New extension of the Mitchell Theory for oxidative phosphorylation in mitochondria of living organisms. Biochim Biophys Acta 1800:205–212

    PubMed  CAS  Google Scholar 

  • Kaim G, Dimroth P (1999) ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18:4118–4127

    Google Scholar 

  • Kitano H (2004) Biological robustness. Nat Rev Genet 5:826–837

    PubMed  CAS  Google Scholar 

  • Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15–18

    PubMed  CAS  Google Scholar 

  • Kussmaul L, Hirst J (2006) The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci USA 103:7607–7612

    PubMed  CAS  Google Scholar 

  • Kuznetsov AV, Gnaiger E (2010) Oxygraph assay of cytochrome c oxidase activity: chemical background correction. Mitochondr Physiol Netw 06(06):1–4

    Google Scholar 

  • Lamb HK, Mee C, Xu W, Liu L, Blond S, Cooper A, Charles IG, Hawkins AR (2006) The affinity of a major Ca2+ binding site on GRP78 is differentially enhanced by ADP and ATP. J Biol Chem 281:8796–8805

    PubMed  CAS  Google Scholar 

  • Lardy HA, Wellman H (1952) Oxidative phosphorylations; role of inorganic phosphate and acceptor systems in control of metabolic rates. J Biol Chem 195:215–224

    PubMed  CAS  Google Scholar 

  • Lee I, Kadenbach B (2001) Palmitate decreases proton pumping of liver-type cytochrome c oxidase. Eur J Biochem 268:6329–6334

    PubMed  CAS  Google Scholar 

  • Lee I, Bender E, Arnold S, Kadenbach B (2001) New control of mitochondrial membrane potential and ROS-formation. Biol Chem 382:1629–1633

    PubMed  CAS  Google Scholar 

  • Lee I, Bender E, Kadenbach B (2002) Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. Mol Cell Biochem 234(235):63–70

    PubMed  Google Scholar 

  • Lee I, Salomon AR, Ficarro S, Mathes I, Lottspeich F, Grossman JI, Hüttemann M (2005) cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J Biol Chem 280:6094–6100

    PubMed  CAS  Google Scholar 

  • Lee I, Salomon AR, Yu K, Samavati L, Pecina P, Pecinova A, Hüttemann M (2009) Isolation of regulatory-competent, phosphorylated cytochrome c oxidase. Methods Enzymol 457:193–210

    PubMed  CAS  Google Scholar 

  • Lim TS, Dávila A, Wallace DC, Burke P (2010) Assessment of mitochondrial membrane potential using an on-chip microelectrode in a microfluidic device. Lab Chip 10:1683–1688

    PubMed  CAS  Google Scholar 

  • Lin J, Wu S, Chan SI (1995) Electron transfer from cytochrome c to 8-azido-ATP-modified cytochrome c oxidase. Biochemistry 34:6335–6343

    PubMed  CAS  Google Scholar 

  • Linder D, Freund R, Kadenbach B (1995) Species-specific expression of cytochrome c oxidase isozymes. Comp Biochem Physiol 112B:461–469

    CAS  Google Scholar 

  • Liu SS (1997) Generating, partitioning, targeting and functioning of superoxide in mitochondria. Biosci Rep 17:259–272

    PubMed  CAS  Google Scholar 

  • Ludwig B, Bender E, Arnold S, Hüttemann M, Lee I, Kadenbach B (2001) Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chembiochem 2:392–403

    PubMed  CAS  Google Scholar 

  • Malyan AN (2010a) Nucleotide binding to noncatalytic sites is essential for ATP-dependent stimulation and ADP-dependent inactivation of the chloroplast ATP synthase. Photosynth Res 105:243–248

    PubMed  CAS  Google Scholar 

  • Malyan AN (2010b) Role of short conserved segments of alpha- and beta-subunits that link F(1)-ATPase catalytic and noncatalytic sites. Biochemistry (Mosc) 75:81–84

    CAS  Google Scholar 

  • Marx MK, Mayer-Posner F, Souliname T, Buse G (1998) Matrix-assisted laser desorption/ionization mass spectrometry analysis and thiol-group determination of isoforms of bovine cytochrome c oxidase, a hydrophobic multisubunit membrane protein. Anal Biochem 256:192–199

    PubMed  CAS  Google Scholar 

  • McKenzie M, Lazarou M, Ryan MT (2009) Analysis of respiratory chain complex assembly with radiolabeled nuclear- and mitochondrial-encoded subunits. Methods Enzymol 456:321–339

    PubMed  CAS  Google Scholar 

  • Miró O, Cardellach F, Barrientos A, Casademont J, Rötig A, Rustin P (1998) Cytochrome c oxidase assay in minute amounts of human skeletal muscle using single wavelength spectrophotometers. J Neurosci Methods 80(1):107–111

    PubMed  Google Scholar 

  • Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41:445–502

    PubMed  CAS  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13

    PubMed  CAS  Google Scholar 

  • Murray J, Schilling B, Row RH, Yoo CB, Gibson BW, Marusich MF, Capaldi RA (2007) Small-scale immunopurification of cytochrome c oxidase for a high-throughput multiplexing analysis of enzyme activity and amount. Biotechnol Appl Biochem 48:167–178

    PubMed  CAS  Google Scholar 

  • Napiwotzki J, Shinzawa-Itoh K, Yoshikawa S, Kadenbach B (1997) ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol Chem 378:1013–1021

    Google Scholar 

  • Napiwotzki J, Kadenbach B (1998) Extramitochondrial ATP/ADP-ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol Chem 379:335–339

    Google Scholar 

  • Nicholls DG, Ferguson SJ (2002) Bioenergetics 3. Academic, San Diego, pp 63–66

    Google Scholar 

  • O’Brien TM, Oliveira PJ, Wallace KB (2008) Inhibition of the adenine nucleotide translocator by N-acetyl perfluorooctane sulfonamides in vitro. Toxicol Appl Pharmacol 227:184–195

    PubMed  Google Scholar 

  • Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3:ra3

    PubMed  Google Scholar 

  • Pacelli C, Latorre D, Cocco T, Capuano F, Kukat C, Seibel P, Villani G (2011) Tight control of mitochondrial membrane potential by cytochrome c oxidase. Mitochondrion 11(2):334–341

    PubMed  CAS  Google Scholar 

  • Pardhasaradhi K, Ludwig B, Hendler RW (1991) Potentiometric and spectral studies with the two-subunit cytochrome aa3 from Paracoccus denitrificans. Comparison with the 13-subunit beef heart enzyme. Biophys J 60:408–414

    PubMed  CAS  Google Scholar 

  • Pearson RB, Kemp BE (1991) Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol 200:62–81

    PubMed  CAS  Google Scholar 

  • Piccoli C, Scrima R, Boffoli D, Capitanio N (2006) Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state. Biochem J 396:573–583

    PubMed  CAS  Google Scholar 

  • Prabu SK, Anandatheerthavarada HK, Raza H, Srinivasan S, Spear JF, Avadhani NG (2006) Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J Biol Chem 281:2061–2070

    PubMed  CAS  Google Scholar 

  • Rajagopalan K, Watt DS, Haley BE (1999) Orientation of GTP and ADP within their respective binding sites in glutamate dehydrogenase. Eur J Biochem 265:564–571

    PubMed  CAS  Google Scholar 

  • Ramzan R, Staniek K, Kadenbach B, Vogt S (2010) Mitochondrial respiration and membrane potential are regulated by the allosteric ATP-inhibition of cytochrome c oxidase. Biochim Biophys Acta 1797:1672–1680

    PubMed  CAS  Google Scholar 

  • Rieger T, Napiwotzki J, Kadenbach B (1995) On the number of nucleotide binding sites in cytochrome c oxidase. Biochem Biophys Res Commun 217:34–40

    PubMed  CAS  Google Scholar 

  • Rohdich F, Kadenbach B (1993) Tissue-specific regulation of cytochrome c oxidase efficiency by nucleotides. Biochemistry 32:8499–8503

    PubMed  CAS  Google Scholar 

  • Rottenberg H, Covian R, Trumpower BL (2009) Membrane potential greatly enhances superoxide generation by the cytochrome bc1 complex reconstituted into phospholipid vesicles. J Biol Chem 284:19203–19210

    PubMed  CAS  Google Scholar 

  • Samavati L, Lee I, Mathes I, Lottspeich F, Hüttemann M (2008) Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J Biol Chem 283:21134–21144

    PubMed  CAS  Google Scholar 

  • Schwenke W-D, Soboll S, Seitz HJ, Sies H (1981) Mitochondrial and cytosolic ATP/ADP ratios in rat liver in vivo. Biochem J 200:405–408

    PubMed  CAS  Google Scholar 

  • Stelling J, Sauer U, Szallasi Z, Doyle FJ 3rd, Doyle J (2004) Robustness of cellular functions. Cell 118:675–685

    PubMed  CAS  Google Scholar 

  • Suarez MD, Revzin A, Natlock R, Keper ES, Thompson DA, Ferguson-Miller S (1984) The functional and physical form of mammalian cytochrome c oxidase determined by gel filtration, radiation inactivation, and sedimentation equilibrium analysis. J Biol Chem 259:13791–13799

    PubMed  CAS  Google Scholar 

  • Thompson DA, Ferguson-Miller S (1983) Lipid and subunit III depleted cytochrome c oxidase purified by horse cytochrome c affinity chromatography in lauryl maltoside. Biochemistry 22(13):3178–3187

    PubMed  CAS  Google Scholar 

  • Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P (2008) (2008) Redox regulation of cell survival. Antioxid Redox Signal 10:1343–1374

    PubMed  CAS  Google Scholar 

  • Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272:1136–1144

    PubMed  CAS  Google Scholar 

  • Tsukihara T, Shimokata K, Katayama Y, Shimada H, Muramoto K, Aoyama H, Mochizuki M, Shinzawa-Itoh K, Yamashita E, Yao M, Ishimura Y, Yoshikawa S (2003) The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc Natl Acad Sci USA 100:15304–15309

    PubMed  CAS  Google Scholar 

  • Valko M, Leibfritz D, Moncola J, Cronin MTD, Mazura M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    PubMed  CAS  Google Scholar 

  • Veech RL, Lawson JWR, Cornell NW, Krebs HA (1979) Cytosolic phosphorylation potential. J Biol Chem 254:6538–6547

    PubMed  CAS  Google Scholar 

  • Villani G, Attardi G (1997) In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc Natl Acad Sci USA 94:1166–1171

    PubMed  CAS  Google Scholar 

  • Villani G, Attardi G (2001) In vivo measurements of respiration control by cytochrome c oxidase and in situ analysis of oxidative phosphorylation. Methods Cell Biol 65:119–131

    PubMed  CAS  Google Scholar 

  • Wan B, Doumen C, Duszynski J, Salama G, Vary TC, LaNoue KF (1993) Effects of cardiac work on electrical potential gradient across mitochondrial membrane in perfused rat hearts. Am J Physiol 265:H453–H460

    PubMed  CAS  Google Scholar 

  • Warnock LJ, Raines SA (2004) Restoration of wild-type conformation to full-length and truncated p53 proteins: specific effects of ATP and ADP. Cancer Biol Ther 3:634–637

    PubMed  CAS  Google Scholar 

  • Weishaupt A, Kadenbach B (1992) Selective removal of subunit VIb increases the activity of cytochrome c oxidase. Biochemistry 31:11477–11481

    PubMed  CAS  Google Scholar 

  • Wiseman RW, Kushmerick MJ (1997) Phosphorus metabolite distribution in skeletal muscle: quantitative bioenergetics using creatine analogs. Mol Cell Biochem 174:23–28

    PubMed  CAS  Google Scholar 

  • Yegutkin GG, Burnstock G (1999) Steady-state binding of adenine nucleotides ATP, ADP and AMP to rat liver and adipose plasma membranes. J Recept Signal Transduct Res 19:437–448

    PubMed  CAS  Google Scholar 

  • Yu MA, Egawa T, Shinzawa-Itoh K, Yoshikawa S, Yeh SR, Rousseau DL, Gerfen GJ (2011) Radical formation in cytochrome c oxidase. Biochim Biophys Acta 1807(10):1295–1304

    PubMed  CAS  Google Scholar 

  • Zhang H, Huang HM, Carson RC, Mahmood J, Thomas HM, Gibson GE (2001) Assessment of membrane potentials of mitochondrial populations in living cells. Anal Biochem 298:170–180

    PubMed  CAS  Google Scholar 

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Acknowledgements

Annika Rhiel is gratefully acknowledged for excellent technical assistance. Dominic Böth is acknowledged for help in respiratory measurements. This paper was supported by the Deutsche Forschungsgemeinschaft (DFG Ka 192/40-1).

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Authors and Affiliations

  1. Biomedical Research Center, Cardiovascular Laboratory, Philipps-University, Marburg, 35032, Germany

    Rabia Ramzan, Petra Weber & Sebastian Vogt

  2. Fachbereich Chemie, Philipps-University Marburg, Marburg, 35032, Germany

    Bernhard Kadenbach

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  1. Rabia Ramzan
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Correspondence to Bernhard Kadenbach .

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    Bernhard Kadenbach

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Ramzan, R., Weber, P., Kadenbach, B., Vogt, S. (2012). Individual Biochemical Behaviour Versus Biological Robustness: Spotlight on the Regulation of Cytochrome c Oxidase. 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_11

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