Respiration of mitochondria in living organisms is controlled by the ATP/ADP ratio and phosphorylation pattern of cytochrome c oxidase

The "second mechanism of respiratory control" (allosteric ATP-inhibition of cytochrome c oxidase (CcO)) is demonstrated for the first time in intact isolated rat liver and heart mitochondria. The problems of measuring the kinetics of allosteric ATP-inhibition in isolated mitochondria we...

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Main Author: Ramzan, Rabia
Contributors: Kadenbach, Bernhard (Prof. Dr.) (Thesis advisor)
Format: Dissertation
Language:English
Published: Philipps-Universität Marburg 2010
Chemie
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1. Stark, R., Pasquel, F., Turcu, A., Pongratz, R.L., Roden, M., Cline, G.W., Shulman, G.I. and Kibbey, R.G. (2009) Phosphoenolpyruvate cycling via mitochondrial phosphoenolpyruvate carboxykinase links anaplerosis and mitochondrial GTP with insulin secretion. J. Biol. Chem. 284, 26578-26590.


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


3. Kadenbach, B., Hüttemann, M., Arnold, S., Lee I., Mühlenbein, N. and Bender E. (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic. Biol. Med. 29, 211-221.


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


5. Thingholm, T. E., Jorgensen, T. J., Jensen, O. N. and Larsen, M. R. (2006) Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nature Protoc. 1, 1929- 1935.


6. O'Brien, T.M., Oliveira, P.J. and Wallace, K.B. (2008) Inhibition of the adenine nucleotide translocator by N-acetyl perfluorooctane sulfonamides in vitro. Toxicol. Appl. Pharmacol. 227, 184-195.


7. Massa, V., Fernandez-Vizarra, E., Alshahwan, S., Bakhsh, E., Goffrini, P. Ferrero, I., Mereghetti, P., D'Adamo, P., Gasparini, P. and Zeviani, M. (2008) Severe infantile encephalomyopathy a nucleus-encoded subunit of cytochrome c oxidase caused by a mutation in COX6B1. Am. J. Hum. Genet. 82, 1281–1289.


8. Villani, G., Greco, M., Papa, S. and Attardi, G. (1998) Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem. 273, 31829-31836.


9. Villani, G. and 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.


10. Villani, G. and 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.


11. 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.


12. Burke, P.A. and Poyton, R.O. (1998) Structure/function of oxygen-regulated isoforms in cytochrome c oxidase. J. Exp. Biol. 201, 1163-1175.


13. Carabez, A. and Sandoval, F. (1974) A mitochondrial inner membrane preparation that sediments at 100 g. J. Cell Biol. 62, 877-881.


14. Eckerskorn, C., Mewes, W., Goretzki, H. and Lottspeich, F. (1988) A new siliconized-glass fiber as support for protein-chemical analysis of electroblotted proteins. Eur. J. Biochem. 176, 509-519.


15. Kadenbach, B. and Arnold, S. (1999) A second mechanism of respiratory control. FEBS Lett. 447, 131-134.


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


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


18. Wittig, I., Braun, H.-P. and Schägger, H. (2006) Blue native PAGE. Nature Protocols 1, 418- 428.


19. Mitchell, P. (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. 41, 445-502.


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


21. Lee, I., Bender, E. and 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.


22. Tager, J.M., Wanders, R.J., Groen, A.K., Kunz, W., Bohnensack, R., Kuster, U., Letko, G., Bohme, G., Dyszynski, J. and Wojtczak, L. (1983) Control of mitochondrial respiration. FEBS Lett. 151, 1-9.


23. Dalmonte, M.E., Forte, E., Genova, M.L., Giuffrè, A., Sarti, P. and Lenaz, G., (2009) Control of respiration by cytochrome c oxidase in intact cells: role of the membrane potential. J. Biol. Chem. 284(47), 32331-32335.


24. Letellier, T., Malgat, M. and Mazat, J.P. (1993) Control of respiration in rat muscle mitochondria: implications for mitochondrial myopathies. Biochim. Biophys. Acta 1141, 58-64.


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


26. (1998) Cytochrome c oxidase (heme aa3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I. J. Bioenerg. Biomembr. 30, 89-97.


27. Seelan, R.S., and Grossman, L.I. (1991) Cytochrome c oxidase subunit VIIa isoforms. Characterization and expression of bovine cDNAs. J. Biol. Chem. 266, 19752-19757.


28. Veech, R.L., Lawson, J.W.R., Cornell, N.W. and Krebs, H.A. (1979) Cytosolic phosphorylation potential. J. Biol. Chem. 254, 6538-6547.


29. Kadenbach, B., Ramzan, R. and Vogt, S. (2009) Degenerative diseases, oxidative stress and cytochrome c oxidase function. Trends Mol. Med. 15(4) 139-147.


30. Murastugu, M., Kamo, N., Kobatake, Y. and Kimura, K. (1979) Determination of membrane potential of "Eschirichia coli" with use of an electrode sensitive to tetraphenyl phosponium, Bioelectrochem. Bioenerg. 6, 477-491.


31. Parsons, W.J., Williams, R.S., Shelton, J.M., Luo, Y., Kessler, D.J. and Richardson, J.A. (1996) Developmental regulation of cytochrome oxidase subunit VIa isoforms in cardiac and skeletal muscle. Am. J. Physiol. 270, H567-574.


32. Palmieri, F. (2008) Diseases caused by defects of mitochondrial carriers: A review. Biochim. Biophys. Acta 1777, 564–578.


33. 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.


34. Kyhse-Andersen, J. (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10, 203-209.


35. Schnaitman, C. and Greenawalt, J.W. (1968) Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J. Cell Biol. 38, 158-175.


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


37. 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.


38. 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.


39. Saraste, M. (1983) How complex is a respiratory complex? Trends Biochem. Sci. 8, 139-142.


40. Kadenbach, B. (2003) Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta 1604, 77-94.


41. Salje, J., Ludwig, B. and Richter, O.M. (2005) Is a third proton-conducting pathway operative in bacterial cytochrome c oxidase? Biochem. Soc. Trans. 33, 829-831.


42. Lightowlers, R., Ewart, G., Aggeler, R., Zhang, Y.Z., Calavetta, L. and Capaldi, R.A. (1990) Isolation and characterization of the cDNAs encoding two isoforms of subunit CIX of bovine cytochrome c oxidase. J. Biol. Chem. 265, 2677-2681.


43. Kadenbach, B., Stroh, A., Ungibauer, M., Kuhn-Nentwig, L., Büge, U., and Jarausch, J. (1986) Isozymes of cytochrome c oxidase: characterization and isolation from different tissues. Methods Enzymol. 126, 32-45.


44. Kamo, N., Murastugu, M., Hongoh, R. and Kobatake, Y. (1979) Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state, J. Membr. Biol. 49, 105-121.


45. Pagliarini, D. J. and Dixon, J. E. (2006) Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem. Sci. 31, 26–34


46. 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, in press.


47. Merten, K.E., Feng, W., Zhang, L., Pierce, W., Cai, J., Klein, J.B. and Kang, Y.J. (2005) Modulation of cytochrome c oxidase-Va is possibly involved in metallothionein protection from doxorubicin cardiotoxicity. J. Pharmacol. Exp. Therapeutics 315, 1314- 1319.


48. 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.


49. Lardy, H.A. and Wellman, H. (1952) Oxidative phosphorylations; role of inorganic phosphate and acceptor systems in control of metabolic rates. J. Biol. Chem. 195(1), 215-224.


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


51. MacDonald, M.J., Bentle, L.A. and Lardy, H.A. (1978) P-enolpyruvate carboxykinase ferroactivator. Distribution and the influence of diabetes and starvation. J. Biol. Chem. 253, 116-124.


52. Saks, V., Monge, C. and Guzun, R. (2009) Philisophical basis and some historical aspects of systems biology: from Hegel to Noble – applications for bioenergetic research. Int. J. Mol. Sci. 10(3), 1161-92.


53. Kadenbach, B., Bender, E., Reith, A., Becker, A., Hammerschmidt, S., Lee, I. Arnold, S. and Hüttemann, M. (1999) Possible influence of metabolic activity on aging. J. Anti-Aging Med. 2, 255-264.


54. Michel, H. (1999) Proton pumping by cytochrome c oxidase. Nature 402, 602-603.


55. Siegbahn, P.E.M. and Blomberg, M.R.A. (2008) Proton Pumping Mechanism in Cytochrome c Oxidase. J. Phys. Chem. A 112, 12772–12780.


56. Yoshikawa, S., Muramoto, K., Shinzawa-Itoh, K., Aoyama, H., Tsukihara, T., Ogura, T., Shimokata, K., Katayama, Y. and Shimada, H. (2006) Reaction mechanism of bovine heart cytochrome c oxidase. Biochim Biophys Acta. 1757, 395-400.


57. Yoshikawa, S., Shinzawa-Itoho, K., Nakashima, R., Yaono, R., Yamashita, E., Inoue, N., Yao, M., Fei, M.J., Libeu, C.P., Mizyshima, T., Yamaguchi, H., Tomizaki, T. and Tsukihara, T. (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280, 1723-1729.


58. 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.


59. Starkov, A.A. and Fiskum, G. (2003) Regulation of brain mitochondrial H 2 O 2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86, 1101-1107.


60. Kupriyanov, V.V., Korchazhkina, O.V. and Lakomkin, V.L. (1993) Regulation of cardiac energy turnover by coromary flow: a 31 P-NMR study. J. Mol. Cell. Cardiol. 25, 1235- 1247.


61. Vogt, S., Rhiel, A., Koch, V., and Kadenbach, B. (2007) Regulation of oxidative phosphorylation by inhibition of its enzyme complexes via reversible phosphorylation. Curr. Enzyme Inhib. 3, 189–206


62. Chance, B. and Williams, G.R. (1955a) Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J. Biol. Chem. 217(1) 383-393.


63. Klumpp, S. and Krieglstein, J. (2002) Serine/threonine protein phosphatases in apoptosis, Curr. Opin. Pharmacol. 2, 458-462.


64. Linder, D., Freund, R. and Kadenbach, B. (1995) Species-specific expression of cytochrome c oxidase isozymes. Comp. Biochem. Physiol. 112B, 461-469.Liu, S.S. (1997) Generating, References 81 partitioning, targeting and functioning of superoxide in mitochondria. Biosci. Rep. 17, 259-272.


65. Mollica, M.P., Iossa, S., Liverine, G. and Soboll, S. (1998) Steady state changes in mitochondrial electrical potential and proton gradient in perfused liver from rats fed a high fat diet. Mol. Cell. Biochem. 178, 213-217.


66. Taanman, J.W., Herzberg, N.H., de Vries, H., Bolhuis, P.A. and van den Bogert, C. (1992) Steady-state transcript levels of cytochrome c oxidase genes during human myogenesis indicate subunit switching of subunit VIa and co-expression of subunit VIIa isoforms. Biochim. Biophys. Acta. 1139, 155-162.


67. Peiffer, W.E., Ingle, R.T, and Ferguson-Miller, S. (1990) Structurally unique plant cytochrome c oxidase isolated from wheat germ, a rich source of plant mitochondrial enzymes. Biochemistry 29, 8696-8701.


68. Soboll, S., Scholz, R. and Heldt, H.W. (1978) Subcellular metabolite concentrations. Dependence of mitochondrial and cytosolic ATP systems on the metabolic state of perfused liver. Eur. J. Biochem. 87, 377-390.


69. Weiss, J.N., Yang, L. and Qu, Z. (2006) Systems biology approaches zo metabolic and cardiovascular disorders: network perspectives of cardiovascular metabolism. J. Lipid Res. 47(11) 2355-2366.


70. Wiese, T.J., Lambeth, D.O. and Ray, P.D. (1991) The intracellular distribution and activities of phosphoenolpyruvate carboxykinase isozymes in various tissues of several mammals and birds. Comp. Biochem. Physiol. B. 100(2), 297-302.


71. III. The steady state, J. Biol. Chem. 217, 409-427.


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


73. Rossignol, R., Malgat, M., Mazat, J.P. and Letellier, T. (1999) Threshold effect and tissue specificity. Implication for mitochondrial cytopathies. J. Biol. Chem. 274, 33426-33432.


74. Kadenbach, B., Stroh, A., Becker, A., Eckerskorn, C. and Lottspeich, F. (1990) Tissue-and species-specific expression of cytochrome c oxidase isozymes in vertebrates. Biochim. Biophys. Acta 1015, 368-372.


75. Mazanek, M., Mituloviae, G., Herzog, F., Stingl, C., Hutchins, J. R., Peters, J. M. and Mechtler, K. (2007) Titanium dioxide as a chemo-affinity solid phase in offline phosphopeptide chromatography prior to HPLC-MS/MS analysis. Nature Protoc. 2, 1059-1069.


76. Korshunov, S.S., Skulachev, V.P. and Starkov, A.A. (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416, 15-18.


77. Schägger, H. and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231.


78. Mörikofer-Zwez, S. and Walter, P. (1989) Binding of ADP to rat liver cytosolic proteins and its influence on the ratio of free ATP/free ADP. Biochem. J. 259, 117-124.


79. O'Shea, P.S., Petrone, G., Casey, R.P. and Azzi, A. (1984) The current-voltage relationships of liposomes and mitochondria. Biochem. J. 219, 719-726.


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


81. Li, Y., Park, J.-S., Deng, J.-H. and Bai, Y. (2006) Cytochrome c oxidase subunit IV is essential for assembly and respiratory function of the enzyme complex. J. Bioenerg. Biomembr. 38, 283-291.


82. Liu, W., Gnanasambandam, R., Benjamin, J., Kaur, G., Getman, P.B., Siegel, A.J., Shortridge, R.D. and Singh, S. (2007) Mutations in cytochrome c oxidase subunit VIa cause neurodegeneration and motor dysfunction in drosophila. Genetics 176, 937–946.


83. Mookherjee, P., Quintanilla, R., Roh, M.S., Zmijewska, A.A., Jope, R.S. and Johnson, G.V. (2007) Mitochondrial-targeted Akt protects SH-SY5Y neuroblastoma cells from staurosporine-induced apoptotic cell death. J. Cell Biochem. 102(1), 196-210.


84. Sharpe, M.A. and Ferguson-Miller, S. (2008) A chemically explicit model for the mechanism of proton pumping in heme-copper oxidases. J. Bioenerg. Biomembr. 40, 541-549.


85. Qin, L., Mills, D.A., Buhrow, L., Hiser, C. and Ferguson-Miller, S. (2008) A Conserved Steroid Binding Site in Cytochrome c Oxidase. Biochemistry 47, 9931–9933.


86. Qin, L., Liu, J., Mills, D.A., Proshlyakov, D.A., Hiser, C. and Ferguson-Miller, S. (2009) Redox-dependent conformational changes in cytochrome c oxidase suggest a gating mechanism for proton uptake. Biochemistry 48, 5121–5130.


87. Rottenberg, H. Covian, R. and Trumpower, B.L. (2009) Membrane potential greatly enhances superoxide generation by the cytochrome bc 1 complex reconstituted into phospholipid vesicles, J. Biol. Chem. 284, 19203-19210.


88. Muramoto, K., Ohta, K., Shinzawa-Itoh, K., Kanda, K., Taniguchi, M., Nabekura, H., Yamashita, E., Tsukihara, T. and Yoshikawa, S. (2010) Bovine cytochrome c oxidase structures enable O 2 reduction with minimization of reactive oxygens and provide a proton-pumping gate. Proc. Natl. Acad. Sci. USA 107, 7740-7745.


89. Yang, J.Y., Yeh, H.Y., Lin, K. and Wang, P.H. (2009) Insulin stimulates Akt translocation to mitochondria: implications on dysregulation of mitochondrial oxidative phosphorylation in diabetic myocardium. J. Mol. Cell Cardiol. 46, 919-926.


90. Schlerf, A., Droste, M., Winter, M. and Kadenbach, B. (1988) Characterization of two different genes (cDNA) for cytochrome c oxidase subunit VIa from heart and liver of the rat. EMBO J. 7, 2387-2391.