Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state

Biochemical Journal

Volumn 396, Issue 3, 2006, Pages 573-583

  Piccoli, Claudia ^a   Scrima, Rosella ^a   Boffoli, Domenico ^a   Capitanio, Nazzareno ^a  

^a UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Cytochrome c oxidase; Metabolic flux control; Mitochondrial transmembrane electrochemical potential; Oxidative phosphorylation; Respirasome

Indexed keywords

DISEASES; ENZYMES; METABOLISM; NEUROMUSCULAR REHABILITATION; OXIDATION; RESPIRATORY SYSTEM;

CYTOCHROME C OXIDASE; METABOLIC FLUX CONTROL; MITOCHONDRIAL TRANSMEMBRANE ELECTROCHEMICAL POTENTIAL; OXIDATIVE PHOSPHORYLATION; RESPIRASOME;

CELL CULTURE;

CYTOCHROME C OXIDASE; ASCORBIC ACID; N,N,N',N' TETRAMETHYL 1,4 PHENYLENEDIAMINE; OLIGOMYCIN; VALINOMYCIN;

ARTICLE; ENERGY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VIVO STUDY; MITOCHONDRION; NEUROMUSCULAR DISEASE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; CELL MEMBRANE POTENTIAL; DRUG EFFECT; ENERGY METABOLISM; KINETICS; METABOLISM; MITOCHONDRIAL MEMBRANE; OXYGEN CONSUMPTION; PHYSIOLOGY; TUMOR CELL LINE;

ASCORBIC ACID; CELL LINE, TUMOR; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; HUMANS; KINETICS; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; OLIGOMYCINS; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; TETRAMETHYLPHENYLENEDIAMINE; VALINOMYCIN;

EID: 33744987954     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060077     Document Type: Article

References (54)

1. Mitchell, P. (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. 41, 445-502
2. Chance, B. and Williams, C. R. (1955) Respiratory enzymes in oxidative phosphorylation. III. The steady state. J. Biol. Chem. 217, 409-427
3. Saraste, M. (1999) Oxidative phosphorylation at the fin de siecle. Science 283, 1488-1493
4. Kang, D. and Hamasaki, N. (2005) Alterations of mitochondrial DNA in common diseases and disease states: aging, neurodegeneration, heart failure, diabetes, and cancer. Curr. Med Chem. 12, 429-441
5. Kacser, A. and Burns, J. A. (1973) The control of flux. In Rate Control of Biological Processes (Davies, D. D., ed.), pp. 65-104, Cambridge University Press, Cambridge
6. Heinrich, R. and Rapoport, T. A. (1974) A linear steady-state treatment of enzymatic chains. Critique of the crossover theorem and a general procedure to identify interaction sites with an effector. Eur. J. Biochem. 42, 97-105
7. Tager, J. M., Wanders, R. J., Groen, A. K., Kunz, W., Bohnensack, R., Kuster, U., Letko, G., Bohme, G., Duszynski, J. and Wojtczak, L. (1983) Control of mitochondrial respiration. FEBS Lett. 151, 1-9
8. Mazat, J. P., Letellier, T., Bedes, F., Malgat, M., Korzeniewski, B., Jouaville, L. S. and Morkuniene, R. (1997) Metabolic control analysis and threshold effect in oxidative phosphorylation: implications tor mitochondrial pathologies. Mol. Cell. Biochem. 174, 143-148
9. Rossignol, R., Letellier, T., Malgat, M., Rocher, C. and Mazat, J. P. (2000) Tissue variation in the control of oxidative phosphorylation: implication for mitochondrial diseases. Biochem. J. 347, 45-53
10. Saks, V. A., Veksler, V. I., Kuznetsov, A. V., Kay, L., Sikk, P., Tiivel, T., Tranqui, L., Olivares, J., Winkler, K., Wiedemann, F. and Kunz, W. S. (1998) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol. Cell. Biochem. 184, 81-100
11. Kunz, W. S., Kudin, A., Vielhaber, S., Elger, C. E., Attardi, G. and Villani, G. (2000) Flux control of cytochrome c oxidase in human skeletal muscle. J. Biol. Chem. 275, 27741-27745
12. 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. U.S.A. 94, 1166-1171
13. 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
14. Villani, G. and Attardi, G. (2000) In vivo control of respiration by cytochrome c oxidase in human cells. Free Radicals Biol. Med. 29, 202-210
15. 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
16. Low, H. and Vallin, I. (1963) Succinate-linked diphosphopyridine nucleotide reduction in submitochondrial particles. Biochim. Biophys. Acta 69, 301-302
17. Bustamante, E., Soper, J. W. and Pedersen, P. L. (1977) A high-yield preparative method for isolation of rat liver mitochondria. Anal. Biochem. 80, 401-408
18. Errede, B., Kamen, M. O. and Hatefi, Y. (1978) Preparation and properties of Complex IV (ferrocytochrome c:oxygen oxidoreductase EC 1.9.3.1). Methods Enzymol. 53, 40-47
19. Capitanio, N., Vygodina, T. V., Capitanio, G., Konstantinov, A. A., Nicholls, P. and Papa, S. (1997) Redox-linked protolytic reactions in soluble cytochrome c oxidase from beef-heart mitochondria: redox Bohr effects. Biochim. Biophys. Acta 1318, 255-265
20. Papa, S., Capitanio, N. and De Nitto, E. (1987) Characteristics of the redox-linked proton ejection in beef-heart cytochrome c oxidase reconstituted in liposomes. Eur. J. Biochem. 164, 507-516
21. Gellerich, F. N., Kunz, W. S. and Bohnensack, R. (1990) Estimation of flux control coefficients from inhibitor titrations by non-linear regression. FEBS Lett. 274, 167-170
22. Gillespie, D. T. (1976) A general method for numerically the stochastic time evolution of coupled chemical reactions. J. Comput. Phys. 22, 403
23. Pinti, M., Troiano, L., Nasi, M., Ferraresi, R., Dobrucki, J. and Cossarizza, A. (2003) Hepatoma HepG2 cells as a model for in vitro studies on mitochondrial toxicity of antiviral drugs: which correlation with the patient? J. Biol. Regul. Homeostatic Agents 17, 166-171
24. Di Lisa, F., Blank, P. S., Colonna, R., Gambassi, G., Silverman, H. S., Stern, M. D. and Hansford, R. G. (1995) Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition. J. Physiol. (Cambridge) 486, 1-13
25. +/e- stoichiometry in mitochondrial cytochrome c oxidase: influence of the rate of electron flow and transmembrane ΔpH. Biochemistry 35, 10800-10806
26. Panda, M. and Robinson, N. C. (1995) Kinetics and mechanism for the binding of HCN to cytochrome c oxidase. Biochemistry 34, 10009-10018
27. 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
28. Mazat, J. P., Rossignol, R., Malgat, M., Rocher, C., Faustin, B. and Letellier, T. (2001) What do mitochondrial diseases teach us about normal mitochondrial functions that we already knew: threshold expression of mitochondrial defects. Biochim. Biophys. Acta 1504, 20-30
29. Cossarizza, A., Baccarani-Conti, M., Kalashnikova, G. and Franceschi, C. (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′- tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun. 197, 40-45
30. Brand, M. D., Chien, L. F., Ainscow, E. K., Rolfe, D. F. and Porter, R. K. (1994) The causes and functions of mitochondrial proton leak. Biochim. Biophys. Acta 1187, 132-139
31. Zoratti, M., Favaron, M., Pietrobon, D. and Azione, G. F. (1986) Intrinsic uncoupling of mitochondrial proton pumps. 1. Non-ohmic conductance cannot account for the nonlinear dependence of static head respiration on ΔμH. Biochemistry 25, 760-767
32. Brand, M. D., Vallis, B. P. and Kesseler, A. (1994) The sum of flux control coefficients in the electron-transport chain of mitochondria. Eur. J. Biochem. 226, 819-829
33. Wrigglesworth, J. M., Cooper, C. E., Sharpe, M. A. and Nicholls, P. (1990) The proteoliposomal steady state. Effect of size, capacitance and membrane permeability on cytochrome oxidase-induced ion gradients. Biochem. J. 270, 109-118
34. Petersen, L. C., Degn, H. and Nicholls, P. (1977) Kinetics of the cytochrome c oxidase and reductase reactions in energized and de-energized mitochondria. Can. J. Biochem. 55, 706-713
35. Gregory, L. and Ferguson-Miller, S. (1989) Independent control of respiration in cytochrome c oxidase vesicles by pH and electrical gradients. Biochemistry 28, 2655-2662
36. Capitanio, N., De Nitto, E., Villani, G., Capitanio, G. and Papa, S. (1990) Protonmotive activity of cytochrome c oxidase: control of oxidoreduction of the heme centers by the protonmotive force in the reconstituted beef heart enzyme. Biochemistry 29, 2939-2945
37. Hackenbrock, C. R., Chazotte, B. and Gupte, S. S. (1986) The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J. Bioenerg. Biomembr. 18, 331-368
38. Schagger, H. (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 1555, 154-159
39. Bianchi, C., Genova, M. L., Parenti Castelli, G. and Lenaz, G. (2004) The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J. Biol. Chem. 279, 36562-36569
40. Heijnen, J. J., van Gulik, W. M., Shimizu, H. and Stepnanopoulos, G. (2004) Metabolic flux control analysis of branch points: an improved approach to obtain flux control coefficients from large perturbation data. Metab. Eng. 4, 391-400
41. Pfeiffer, K., Gohil, V., Stuart, R. A., Hunte, C., Brandt, U., Greenberg, M. L. and Schagger, H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278, 52873-52880
42. Zhang, M., Mileykovskaya, E. and Dowhan, W. (2005) Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J. Biol. Chem. 280, 29403-29408
43. Haines, T. H. and Dencher, N. A. (2002) Cardiolipin: a proton trap for oxidative phosphorylation. FEES Lett. 528, 35-39
44. Nichols-Smith, S. and Kuhl, T. (2005) Electrostatic interactions between model mitochondrial membranes. Colloids Surf. B Biointerfaces 41, 121-127
45. Lange, C., Nett, J. H., Trumpower, B. L. and Hunte, C. (2001) Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J. 20, 6591-6600
46. Mizushima, T., Yao, M., Inoue, N., Aoyama, H., Yamashita, E., Yamaguchi, H., Tsukihara, T., Nakashima, R., Shinzawa-Itoh, K., Yaono, R. and Yoshikawa, S. (1999) Acta Crystallogr. Sect. A 55, suppl., P06.04.069.
47. Agnati, L. F., Guidolin, D., Genedani, S., Ferre, S., Bigiani, A., Woods, A. S. and Fuxe, K. (2005) How proteins come together in the plasma membrane and function in macromolecular assemblies: focus on receptor mosaics. J. Mol. Neurosci. 26, 133-154
48. Fleischer, S., Rouser, G., Fleischer, B., Casu, A. and Kritchevsky, G. J. (1967) Lipid composition of mitochondria from bovine heart, liver, and kidney. Lipid Res. 8, 170-180
49. Pecina, P., Houstkova, H., Hansikova, H., Zeman, J. and Houstek, J. (2004) Genetic defects of cytochrome c oxidase assembly. Physiol. Res. 53 (Suppl. 1), S213-S223
50. Wallace, D. C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407
51. Lightowlers, R. N., Chinnery, P. F., Turnbull, D. M. and Howell, N. (1997) Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. Trends Genet, 13, 450-455
52. Taivassalo, T., Jensen, T. D., Kennaway, N., DiMauro, S., Vissing, J. and Haller, R. G. (2003) The spectrum of exercise tolerance in mitochondrial myopathies: a study of 40 patients. Brain 126, 413-423
53. Elliot, D. L., Buist, N. R., Goldberg, L., Kennaway, N. G., Powell, B. R. and Kuehl, K. S. (1989) Metabolic myopathies: evaluation by graded exercise testing. Medicine (Baltimore) 68, 163-172
54. Papa, S. and Skulachev, V. P. (1997) Reactive oxygen species, mitochondria, apoptosis and aging. Mol. Cell. Biochem. 174, 305-319