Mitochondrial cytochrome c oxidase is inhibited by ATP only at very high ATP/ADP ratios

References

Arnold, S. and Kadenbach, B. (1997). Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur. J. Biochem. 249, 350–354.10.1111/j.1432-1033.1997.t01-1-00350.xSearch in Google Scholar

Arnold, S. and Kadenbach, B. (1999). The intramitochondrial ATP/ADP ratio controls cytochrome oxidase activity allosterically. FEBS Lett. 443, 105–108.10.1016/S0014-5793(98)01694-9Search in Google Scholar

Arnold, S., Goglia, F., and 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, 325–330.10.1046/j.1432-1327.1998.2520325.xSearch in Google Scholar

Babcock, G.T. and Wikström, M. (1992). Oxygen activation and the conservation of energy in cell respiration. Nature 356, 301–309.10.1038/356301a0Search in Google Scholar

Bender, E. and Kadenbach, B. (2000). The allosteric ATP-inhibition of cytochrome c oxidase activity reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett. 466, 130–134.10.1016/S0014-5793(99)01773-1Search in Google Scholar

Bisson, R., Schiavo, G., and Montecucco, C. (1987). ATP induces conformational changes in mitochondrial cytochrome c oxidase. Effect of the cytochrome c binding site. J. Biol. Chem. 262, 5992–5998.10.1016/S0021-9258(18)45527-5Search in Google Scholar

Capaldi, R.A. (1990) Structure and function of cytochrome c oxidase. Annu. Rev. Biochem. 59, 569–596.10.1146/annurev.bi.59.070190.003033Search in Google Scholar

Dobson, G.P. and Himmelreich, U. (2002). Heart design: free ADP scales with absolute mitochondrial and myofibrillar volumes from mouse to human. Biochim. Biophys. Acta 1553, 261–267.10.1016/S0005-2728(01)00247-XSearch in Google Scholar

Drahota, Z., Milerova, M., Stieglerova, A., Skarka, L., Houstek, J., and Ostadal, B. (2005). Development of cytochrome-c oxidase activity in rat heart. Down regulation in newborn rats. Cell. Biochem. Biophys. 43, 87–94.10.1385/CBB:43:1:087Search in Google Scholar

Errede, B. and Kamen, M.D. (1978). Comparative kinetic studies of cytochromes c in reactions with mitochondrial cytochrome c oxidase and reductase. Biochemistry 17, 1015–1027.10.1021/bi00599a012Search in Google Scholar

Ferguson-Miller, S., Brautigan, D.L., and Margoliash, E. (1976). Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes c with binding of mitochondrial cytochrome c oxidase. J. Biol. Chem. 251, 1104–1115.10.1016/S0021-9258(17)33807-3Search in Google Scholar

Ferguson-Miller, S., Brautigan, D.L., and Margoliash, E. (1978). Definition of cytochrome c binding domains by chemical modification. III. Kinetics of reaction of carboxydinitrophenyl cytochrome c with cytochrome c oxidase. J. Biol. Chem. 253, 149–159.10.1016/S0021-9258(17)38281-9Search in Google Scholar

From, A.H.L., Zimmer, S.D., Michurski, S.P., Mohanakrishnan, P., Ulstad, V.K., Thoma, W.J., and Ugurbil, K. (1990). Regulation of the oxidative phosphorylation rate in the intact cell. Biochemistry 29, 3731–3743.10.1021/bi00467a020Search in Google Scholar PubMed

Green, D.E. and Fry, M. (1980). On reagents that convert cytochrome oxidase from an inactive to an active coupling state. Proc. Natl. Acad. Sci. USA 77, 1951–1955.10.1073/pnas.77.4.1951Search in Google Scholar PubMed PubMed Central

Guzun, R., Timohhina, N., Tepp, K., Monge, C., Kaambre, T., Sikk, P., Kuznetsov, A.V., Pison, C., and Saks, V. (2009). Regulation of respiration controlled by mitochondrial creatine kinase in permeabilized cardiac cells in situ. Importance of system level properties. Biochim. Biophys. Acta 1787, 1089–1105.10.1016/j.bbabio.2009.03.024Search in Google Scholar PubMed

Helling, S., Vogt, S., Rhiel, A., Ramzan, R., Wen, L., Marcus, K., and Kadenbach, B. (2008). Phosphorylation and kinetics of mammalian cytochrome c oxidase. Mol. Cell. Proteomics 7, 1714–1724.10.1074/mcp.M800137-MCP200Search in Google Scholar PubMed PubMed Central

Helling, S., Hüttemann, M., Ramzan, R., Kim, S.H., Lee, I., Müller, T., Langenfeld, E., Meyer, H.E., Kadenbach, B., Vogt, S., et al. (2012). Multiple phosphorylations of cytochrome c oxidase and their functions. Proteomics 12, 950–959.10.1002/pmic.201100618Search in Google Scholar PubMed PubMed Central

Kadenbach, B., Frank, V., Rieger, T., and Napiwotzki, J. (1997). Regulation of respiration and energy transduction in cytochrome c oxidase isozymes by allosteric effectors. Mol. Cell. Biochem. 174, 131–135.10.1007/978-1-4615-6111-8_20Search in Google Scholar

Kadenbach, B., Ramzan, R., Wen, L., and Vogt, S. (2010). New extension of the Mitchell Theory for oxidative phosphorylation in mitochondria of living organisms. Biochim. Biophys. Acta 1800, 205–212.10.1016/j.bbagen.2009.04.019Search in Google Scholar PubMed

Kadenbach, B., Ramzan, R., and Vogt, S. (2013). High efficiency versus maximal performance – the cause of oxidative stress in eukaryotes. Mitochondrion 13, 1–6.10.1016/j.mito.2012.11.005Search in Google Scholar PubMed

Kirichenko, A.V., Pfitzner, U., Ludwig, B., Soares, C.M., Vygodina, T.V., and Konstantinov, A.A. (2005). Cytochrome c oxidase as a calcium binding protein. Studies on the role of a conserved aspartate in helices XI-XII cytoplasmic loop in cation binding. Biochemistry 44, 12391–12401.10.1021/bi050376vSearch in Google Scholar

Kupriyanov, V.V., Korchazhkina, O.V., and Lakomkin, V.L. (1993). Regulation of cardiac energy turnover by coromary flow: a ³¹P-NMR study. J. Mol. Cell. Cardiol. 25, 1235–1247.10.1006/jmcc.1993.1135Search in Google Scholar

Lanza, I.R. and Nair, K.S. (2009). Functional assessment of isolated mitochondria in vitro. Methods Enzymol. 457, 349–372.10.1016/S0076-6879(09)05020-4Search in Google Scholar

Lee, I. and Kadenbach, B. (2001). Palmitate decreases proton pumping of liver-type cytochrome c oxidase. Eur. J. Biochem. 268, 6329–6334.10.1046/j.0014-2956.2001.02602.xSearch in Google Scholar

Lee, I., Bender, E., Arnold, S., and Kadenbach, B. (2001). New control of mitochondrial membrane potential and ROS-formation. Biol. Chem. 382, 1629–1633.10.1515/BC.2001.198Search in Google Scholar

Lee, I., Salomon, A.R., Ficarro, S., Mathes, I., Lottspeich, F., Grossman, L.I., and Hüttemann, M. (2005). cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J. Biol. Chem. 280, 6094–6100.10.1074/jbc.M411335200Search in Google Scholar

Lenaz, G. and Genova, M.L. (2010). Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid. Redox Signal. 12, 961–1008.10.1089/ars.2009.2704Search in Google Scholar

Miyazaki, T., Neff, L., Tanaka, S., Horne, W.C., and Baron, R. (2003). Regulation of cytochrome c oxidase activity by c-Src in osteoclasts. J. Cell. Biol. 160, 709–718.10.1083/jcb.200209098Search in Google Scholar

Murphy, M.P. (2009). How mitochondria produce reactive oxygen species. Biochem J. 417(Pt 1), 1–13.10.1042/BJ20081386Search in Google Scholar

Nalecz, K.A., Bolli, R., and Azzi, A. (1983). Preparation of monomeric cytochrome c oxidase: its kinetics differ from those of the dimeric enzyme. Biochem. Biophys. Res. Commun. 114, 822–828.10.1016/0006-291X(83)90855-0Search in Google Scholar

Napiwotzki, J. and Kadenbach, B. (1998). Extramitochondrial ATP/ADP-ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol. Chem. 379, 335–339.10.1515/bchm.1998.379.3.335Search in Google Scholar

Obatomi, D.K. and Bach, P.H. (1996). Inhibition of mitochondrial respiration and oxygen uptake in isolated rat renal tubular fragments by atractyloside. Toxicol Lett. 89, 155–161.10.1016/S0378-4274(96)03799-XSearch in Google Scholar

Paradies, G., Petrosillo, G., and Ruggiero, F.M. (1997). Cardiolipin-dependent decrease of cytochrome c oxidase activity in heart mitochondria from hypothyroid rats. Biochim. Biophys. Acta 1319, 5–8.10.1016/S0005-2728(97)00012-1Search in Google Scholar

Penefsky, H.S. (1985). Mechanism of inhibition of mitochondrial adenosine triphosphatase by dicyclohexylcarbodiimide and oligomycin: relationship to ATP synthesis. Proc. Natl. Acad. Sci USA 82, 1589–1593.10.1073/pnas.82.6.1589Search in Google Scholar PubMed PubMed Central

Prabu, S.K., Anandatheerthavarada, H.K., Raza, H., Srinivasan, S., Spear, J.F., and Avadhani, N.G. (2006). Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J. Biol. Chem. 281, 2061–2070.10.1074/jbc.M507741200Search in Google Scholar PubMed PubMed Central

Ramzan, R., Staniek, K., Kadenbach, B., and Vogt, S. (2010). Mitochondrial respiration and membrane potential are regulated by the allosteric ATP-inhibition of cytochrome c oxidase. Biochim. Biophys. Acta 1797, 1672–1680.10.1016/j.bbabio.2010.06.005Search in Google Scholar PubMed

Ramzan, R., Weber, P., Kadenbach, B., and Vogt, S. (2012) Individual biochemical behaviour versus biological robustness: spotlight on the regulation of cytochrome c oxidase. Adv. Exp. Med. Biol. 748, 265–281.10.1007/978-1-4614-3573-0_11Search in Google Scholar PubMed

Reimann, A., Röhm, K.H., and Kadenbach, B. (1993). Ferricytochrome c modulates the oxidation of ferrocytochrome c by reconstituted cytochrome c oxidase in a complex manner. J. Bioenerg. Biomembr. 25, 393–399.10.1007/BF00762465Search in Google Scholar PubMed

Robinson, N.C. (1993). Functional binding of cardiolipin to cytochrome c oxidase. J. Bioenerg. Biomembr. 25, 153–163.10.1007/BF00762857Search in Google Scholar PubMed

Robinson, N.C. and Capaldi, R.A. (1977). Interaction of detergents with cytochrome c oxidase. Biochemistry 16, 375–380.10.1021/bi00622a006Search in Google Scholar PubMed

Robinson, N.C. and Wiginton, D. (1985). Diphosphatidylglycerol reactivation of lipid-depleted beef heart cytochrome c oxidase: effect of subunit III removal. J. Inorg. Biochem. 23, 171–176.10.1016/0162-0134(85)85022-4Search in Google Scholar

Rohdich, F. and Kadenbach, B. (1993). Tissue-specific regulation of cytochrome c oxidase efficiency by nucleotides. Biochemistry 32, 8499–8503.10.1021/bi00084a015Search in Google Scholar

Rosevear, P., VanAken, T., Baxter, J., and Ferguson-Miller, S. (1980). Alkyl glycoside detergents: a simpler synthesis and their effects on kinetic and physical properties of cytochrome c oxidase. Biochemistry 19, 4108–4115.10.1021/bi00558a032Search in Google Scholar

Rottenberg, H., Covian, R., and Trumpower, B.L. (2009). Membrane potential greatly enhances superoxide generation by the cytochrome bc₁ complex reconstituted into phospholipid vesicles. J. Biol. Chem. 284, 19203–19210.10.1074/jbc.M109.017376Search in Google Scholar

Saks, V.A., Kuznetsov, A.V., Kupriyanov, V.V., Miceli, M.V., and Jacobus, W.E. (1985). Creatine kinase of rat heart mitochondria. The demonstration of functional coupling to oxidative phosphorylation in an inner membrane-matrix preparation. J. Biol. Chem. 260, 7757–7764.10.1016/S0021-9258(17)39672-2Search in Google Scholar

Samavati, L., Lee, I., Mathes, I., Lottspeich, F., and Huttemann, M. (2008). Tumor necrosis factor α inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J. Biol. Chem. 283, 21134–21144.10.1074/jbc.M801954200Search in Google Scholar PubMed PubMed Central

Sarti, P., Colosimo, A., Brunori, M., Wilson, M.T., and Antonini, E. (1983). Kinetic studies on cytochrome c oxidase inserted into liposomal vesicles. Effect of ionophores. Biochem. J. 209, 81–89.10.1042/bj2090081Search in Google Scholar PubMed PubMed Central

Smith, L. and Camerino, P.W. (1963). Comparison of polarographic and spectrophotometric assays for cytochrome c oxidase activity. Biochemistry 2, 1428–1432.10.1021/bi00906a039Search in Google Scholar PubMed

Starkov, A. A. and Fiskum, G. (2003). Regulation of brain mitochondrial H₂O₂ production by membrane potential and NAD(P)H redox state. J. Neurochem. 86, 1101–1107.10.1046/j.1471-4159.2003.01908.xSearch in Google Scholar PubMed

Stieglerova, A., Drahota, Z., Ostadal, B., and Houstek, J. (2000). Optimal Conditions for determination of cytochrome c oxidase activity in the rat heart. Physiol. Res. 49, 245–250.Search in Google Scholar

Taanman, J.W., Turina, P., and Capaldi, R.A. (1994). Regulation of cytochrome c oxidase by interaction of ATP at two binding sites, one on subunit Via. Biochemistry 33, 11833–11841.10.1021/bi00205a020Search in Google Scholar PubMed

Tarasev, M. and Hill, B.C. (2002). Detergent modulation of electron and proton transfer reactions in bovine cytochrome c oxidase. Arch. Biochem. Biophys. 400, 162–170.10.1016/S0003-9861(02)00011-5Search in Google Scholar

Thompson, D.A. and Ferguson-Miller, S. (1983). Lipid and subunit III depleted cytochrome c oxidase purified by horse cytochrome c affinity chromatography in lauryl maltoside. Biochemistry 22, 3178–3187.10.1021/bi00282a022Search in Google Scholar

Thompson, D.A., Suarez-Villafane, M., and Ferguson-Miller, S. (1982). The active form of cytochrome c oxidase. Effects of detergent, the intact membrane, and radiation inactivation. Biophys. J. 37, 285–292.10.1016/S0006-3495(82)84677-8Search in Google Scholar

Trachootham, D., Lu, W., Ogasawara, M.A., Nilsa, R.D., and Huang, P. (2008). Redox regulation of cell survival. Antioxid. Redox. Signal. 10, 1343–1374.10.1089/ars.2007.1957Search in Google Scholar PubMed PubMed Central

Valko, M., Leibfritz, D., Moncola, J., Cronin, M.T.D., Mazura, M., and Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell. Biol. 39, 44–84.10.1016/j.biocel.2006.07.001Search in Google Scholar PubMed

Vogt, S., Ramzan, R., Weber, P., Troitzsch, D., Rhiel, A., Sattler, A., Irqsusi, M., Ruppert, V., and Moosdorf, R. (2013). Ischemic preconditioning results in an ATP-dependent inhibition of cytochrome c oxidase. Shock 40, 407–413.10.1097/SHK.0b013e3182a51a06Search in Google Scholar PubMed

Wan, B., Doumen, C., Duszynski, J., Salama, G., Vary, T.C., and LaNoue, K.F. (1993). Effects of cardiac work on electrical potential gradient across mitochondrial membrane in perfused rat hearts. Am. J. Physiol. 265, H453–H460.10.1152/ajpheart.1993.265.2.H453Search in Google Scholar PubMed

Weishaupt, A. and Kadenbach, B. (1992). Selective removal of subunit VIb increases the activity of cytochrome c oxidase. Biochemistry 31, 11477–11481.10.1021/bi00161a028Search in Google Scholar PubMed

Wenchich, L., Drahota, Z., Honzik, T., Hansikova, H., Tesarova, M., Zeman, J., and Houstek, J. (2003). Polarographic evaluation of mitochondrial enzymes activity in isolated mitochondria and in permeabilized human muscle cells with inherited mitochondrial defects. Physiol. Res. 52, 781–788.Search in Google Scholar

Wilson, D.F. (1994). Factors affecting the rate and energetics of mitochondrial oxidative phosphorylation. Med. Sci. Sports Exerc. 26, 37–43.10.1249/00005768-199401000-00008Search in Google Scholar

Zhang, H., Huang, H.M., Carson, R.C., Mahmood, J., Thomas, H.M., and Gibson, G.E. (2001). Assessment of membrane potentials of mitochondrial populations in living cells. Anal. Biochem. 298, 170–180.10.1006/abio.2001.5348Search in Google Scholar PubMed