Regulation of mitochondrial oxidative phosphorylation through cell signaling

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 12, 2007, Pages 1701-1720

  Hüttemann, Maik ^a   Lee, Icksoo ^a   Samavati, Lobelia ^a   Yu, Hong ^a   Doan, Jeffrey W ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP synthase; bc1 complex; Cancer; Cytochrome c oxidase; NADH dehydrogenase; Neurodegenerative disease

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOCHROME C; CYTOCHROME C OXIDASE; PROTEIN A; PROTEIN C; PROTEIN TYROSINE KINASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SUCCINATE DEHYDROGENASE;

ACETYLATION; AMINO TERMINAL SEQUENCE; AUTORADIOGRAPHY; CELL ENERGY; CELL PROLIFERATION; CELL RESPIRATION; CELLULAR DISTRIBUTION; DEGENERATIVE DISEASE; ENERGY YIELD; ENZYME ACTIVITY; HUMAN; IMMUNOPRECIPITATION; IN VIVO STUDY; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SPERMATID;

ANIMALS; APOPTOSIS; HUMANS; MITOCHONDRIA; NEOPLASMS; NEURODEGENERATIVE DISEASES; OXIDATIVE PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 36549046060     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.10.001     Document Type: Review

References (202)

1. Rich P. Chemiosmotic coupling: the cost of living. Nature 421 (2003) 583
2. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., and Walter P. The Molecular Biology of the Cell. 4th ed. (2002), Garland Science, New York
3. Morriss G.M., and New D.A. Effect of oxygen concentration on morphogenesis of cranial neural folds and neural crest in cultured rat embryos. J. Embryol. Exp. Morphol. 54 (1979) 17-35
4. Warburg O., Posener K., and Negelein E. Uber den Stoffwechsel der Carcinomzelle. Biochem. Z. 152 (1924) 309-344
5. Warburg O. On the origin of cancer cells. Science 123 (1956) 309-314
6. Scheffler I.E. Mitochondria (1999), John Wiley & Sons, New York
7. Chance B., and Williams G.R. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J. Biol. Chem. 217 (1955) 383-393
8. Pagliarini D.J., and Dixon J.E. Mitochondrial modulation: reversible phosphorylation takes center stage?. Trends Biochem. Sci. 31 (2006) 26-34
9. Salvi M., Brunati A.M., and Toninello A. Tyrosine phosphorylation in mitochondria: a new frontier in mitochondrial signaling. Free Radic. Biol. Med. 38 (2005) 1267-1277
10. Horbinski C., and Chu C.T. Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic. Biol. Med. 38 (2005) 2-11
11. Vogt S., Rhiel A., Koch V., and Kadenbach B. Regulation of oxidative phosphorylation by inhibition of its enzyme complexes via reversible phosphorylation. Curr Enz Inhibit 3 (2007) 189-206
12. Carroll J., Fearnley I.M., Skehel J.M., Runswick M.J., Shannon R.J., Hirst J., and Walker J.E. The post-translational modifications of the nuclear encoded subunits of complex I from bovine heart mitochondria. Mol. Cell Proteomics 4 (2005) 693-699
13. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
14. Gomperts B.D., Kramer I.M., and Tatham P.E.R. Signal Transduction (2003), Elsevier Academic Press, London, UK
15. Technikova-Dobrova Z., Sardanelli A.M., and Papa S. Phosphorylation of mitochondrial proteins in bovine heart. Characterization of kinases and substrates. FEBS Lett. 322 (1993) 51-55
16. Muller G., and Bandlow W. Protein phosphorylation in yeast mitochondria: cAMP-dependence, submitochondrial localization and substrates of mitochondrial protein kinases. Yeast 3 (1987) 161-174
17. Kondrashin A.A., Nesterova M.V., and Cho-Chung Y.S. Subcellular distribution of the R-subunits of cAMP-dependent protein kinase in LS-174T human colon carcinoma cells. Biochem. Mol. Biol. Int. 45 (1998) 237-244
18. Kleitke B., Sydow H., and Wollenberger A. Evidence for cyclic AMP-dependent protein kinase activity in isolated guinea pig and rat liver mitochondria. Acta Biol. Med. Ger. 35 (1976) K9-K17
19. Dimino M.J., Bieszczad R.R., and Rowe M.J. Cyclic AMP-dependent protein kinase in mitochondria and cytosol from different-sized follicles and corpora lutea of porcine ovaries. J. Biol. Chem. 256 (1981) 10876-10882
20. Burgess J.W., and Yamada E.W. cAMP-dependent protein kinase isozymes with preference for histone H2B as substrate in mitochondria of bovine heart. Biochem. Cell Biol. 65 (1987) 137-143
21. Pariset C., and Weinman S. Differential localization of two isoforms of the regulatory subunit RII alpha of cAMP-dependent protein kinase in human sperm: biochemical and cytochemical study. Mol. Reprod. Dev. 39 (1994) 415-422
22. Corso M., and Thomson M. Protein phosphorylation in mitochondria from human placenta. Placenta 22 (2001) 432-439
23. Technikova-Dobrova Z., Sardanelli A.M., Speranza F., Scacco S., Signorile A., Lorusso V., and Papa S. Cyclic adenosine monophosphate-dependent phosphorylation of mammalian mitochondrial proteins: enzyme and substrate characterization and functional role. Biochemistry 40 (2001) 13941-13947
24. Schwoch G., Trinczek B., and Bode C. Localization of catalytic and regulatory subunits of cyclic AMP-dependent protein kinases in mitochondria from various rat tissues. Biochem. J. 270 (1990) 181-188
25. Griffioen G., and Thevelein J.M. Molecular mechanisms controlling the localisation of protein kinase A. Curr. Genet. 41 (2002) 199-207
26. Lin R.Y., Moss S.B., and Rubin C.S. Characterization of S-AKAP84, a novel developmentally regulated A kinase anchor protein of male germ cells. J. Biol. Chem. 270 (1995) 27804-27811
27. Newhall K.J., Criniti A.R., Cheah C.S., Smith K.C., Kafer K.E., Burkart A.D., and McKnight G.S. Dynamic anchoring of PKA is essential during oocyte maturation. Curr. Biol. 16 (2006) 321-327
28. Chen Q., Lin R.Y., and Rubin C.S. Organelle-specific targeting of protein kinase AII (PKAII). Molecular and in situ characterization of murine A kinase anchor proteins that recruit regulatory subunits of PKAII to the cytoplasmic surface of mitochondria. J. Biol. Chem. 272 (1997) 15247-15257
29. Cardone L., Carlucci A., Affaitati A., Livigni A., DeCristofaro T., Garbi C., Varrone S., Ullrich A., Gottesman M.E., Avvedimento E.V., and Feliciello A. Mitochondrial AKAP121 binds and targets protein tyrosine phosphatase D1, a novel positive regulator of src signaling. Mol. Cell. Biol. 24 (2004) 4613-4626
30. Harada H., Becknell B., Wilm M., Mann M., Huang L.J., Taylor S.S., Scott J.D., and Korsmeyer S.J. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 3 (1999) 413-422
31. Affaitati A., Cardone L., de Cristofaro T., Carlucci A., Ginsberg M.D., Varrone S., Gottesman M.E., Avvedimento E.V., and Feliciello A. Essential role of A-kinase anchor protein 121 for cAMP signaling to mitochondria. J. Biol. Chem. 278 (2003) 4286-4294
32. Sardanelli A.M., Signorile A., Nuzzi R., Rasmo D.D., Technikova-Dobrova Z., Drahota Z., Occhiello A., Pica A., and Papa S. Occurrence of A-kinase anchor protein and associated cAMP-dependent protein kinase in the inner compartment of mammalian mitochondria. FEBS Lett. 580 (2006) 5690-5696
33. Papa S., Sardanelli A.M., Cocco T., Speranza F., Scacco S.C., and Technikova-Dobrova Z. The nuclear-encoded 18 kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett. 379 (1996) 299-301
34. Papa S., Sardanelli A.M., Scacco S., and Technikova-Dobrova Z. cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of the cAMP-mediated intracellular signal transduction. FEBS Lett. 444 (1999) 245-249
35. Pasdois P., Deveaud C., Voisin P., Bouchaud V., Rigoulet M., and Beauvoit B. Contribution of the phosphorylable complex I in the growth phase-dependent respiration of C6 glioma cells in vitro. J. Bioenerg. Biomembranes 35 (2003) 439-450
36. Chen R., Fearnley I.M., Peak-Chew S.Y., and Walker J.E. The phosphorylation of subunits of complex I from bovine heart mitochondria. J. Biol. Chem. 279 (2004) 26036-26045
37. Schilling B., Aggeler R., Schulenberg B., Murray J., Row R.H., Capaldi R.A., and Gibson B.W. Mass spectrometric identification of a novel phosphorylation site in subunit NDUFA10 of bovine mitochondrial complex I. FEBS Lett. 579 (2005) 2485-2490
38. Pocsfalvi G., Cuccurullo M., Schlosser G., Scacco S., Papa S., and Malorni A. Phosphorylation of B14.5a subunit from bovine heart complex I identified by titanium dioxide selective enrichment and shotgun proteomics. Mol. Cell Proteomics 6 (2006) 231-237
39. Hopper R.K., Carroll S., Aponte A.M., Johnson D.T., French S., Shen R.F., Witzmann F.A., Harris R.A., and Balaban R.S. Mitochondrial matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry 45 (2006) 2524-2536
40. Bykova N.V., Egsgaard H., and Moller I.M. Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett. 540 (2003) 141-146
41. Augereau O., Claverol S., Boudes N., Basurko M.J., Bonneu M., Rossignol R., Mazat J.P., Letellier T., and Dachary-Prigent J. Identification of tyrosine-phosphorylated proteins of the mitochondrial oxidative phosphorylation machinery. Cell. Mol. Life Sci. 62 (2005) 1478-1488
42. Gingrich J.R., Pelkey K.A., Fam S.R., Huang Y., Petralia R.S., Wenthold R.J., and Salter M.W. Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 6237-6242
43. Salvi M., Brunati A.M., Bordin L., La Rocca N., Clari G., and Toninello A. Characterization and location of Src-dependent tyrosine phosphorylation in rat brain mitochondria. Biochim. Biophys. Acta 1589 (2002) 181-195
44. Miyazaki T., Neff L., Tanaka S., Horne W.C., and Baron R. Regulation of cytochrome c oxidase activity by c-Src in osteoclasts. J. Cell Biol. 160 (2003) 709-718
45. Lascano H.R., Casano L.M., Martin M., and Sabater B. The activity of the chloroplastic Ndh complex is regulated by phosphorylation of the NDH-F subunit. Plant Physiol. 132 (2003) 256-262
46. T. Cocco, C. Pacelli, P. Sgobbo, G. Villani, Control of OXPHOS efficiency by complex I in brain mitochondria, Neurobiol. Aging (in press).
47. Schilling B., Murray J., Yoo C.B., Row R.H., Cusack M.P., Capaldi R.A., and Gibson B.W. Proteomic analysis of succinate dehydrogenase and ubiquinol-cytochrome c reductase (Complex II and III) isolated by immunoprecipitation from bovine and mouse heart mitochondria. Biochim. Biophys. Acta 1762 (2006) 213-222
48. 1 complex. Science 281 (1998) 64-71
49. Li K., Li Y., Shelton J.M., Richardson J.A., Spencer E., Chen Z.J., Wang X., and Williams R.S. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 101 (2000) 389-399
50. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 102 (2000) 1-4
51. Kroemer G., Dallaporta B., and Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60 (1998) 619-642
52. Skulachev V.P. Cytochrome c in the apoptotic and antioxidant cascades. FEBS Lett. 423 (1998) 275-280
53. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritow V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., Vlasova I.I., Zhao Q., Zou M., Di P., Svistunenko D.A., Kurnikov I.V., and Borisenko G.G. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 1 (2005) 223-232
54. Pereverzev M.O., Vygodina T.V., Konstantinov A.A., and Skulachev V.P. Cytochrome c, an ideal antioxidant. Biochem. Soc. Trans. 31 (2003) 1312-1315
55. Hennig B. Change of cytochrome c structure during development of the mouse. Eur. J. Biochem. 55 (1975) 167-183
56. Goldberg E., Sberna D., Wheat T.E., Urbanski G.J., and Margoliash E. Cytochrome c: immunofluorescent localization of the testis-specific form. Science 196 (1977) 1010-1012
57. Hess R.A., Miller L.A., Kirby J.D., Margoliash E., and Goldberg E. Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol. Reprod. 48 (1993) 1299-1308
58. Liu Z., Lin H., Ye S., Liu Q.Y., Meng Z., Zhang C.M., Xia Y., Margoliash E., Rao Z., and Liu X.J. Remarkably high activities of testicular cytochrome c in destroying reactive oxygen species and in triggering apoptosis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8965-8970
59. Hüttemann M., Jaradat S., and Grossman L.I. Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb-the counterpart to testes-specific cytochrome c?. Mol. Reprod. Dev. 66 (2003) 8-16
60. Ferguson-Miller S., Brautigan D.L., and Margoliash E. Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes c with binding to mitochondrial cytochrome c oxidase. J. Biol. Chem. 251 (1976) 1104-1115
61. McIntosh D.B., Parrish J.C., and Wallace C.J. Definition of a nucleotide binding site on cytochrome c by photoaffinity labeling. J. Biol. Chem. 271 (1996) 18379-18386
62. Lee I., Salomon A.R., Yu K., Doan J.W., Grossman L.I., and Hüttemann M. New prospects for an old enzyme: mammalian cytochrome c is tyrosine-phosphorylated in vivo. Biochemistry 45 (2006) 9121-9128
63. Roberts V.A., and Pique M.E. Definition of the interaction domain for cytochrome c on cytochrome c oxidase. III. Prediction of the docked complex by a complete, systematic search. J. Biol. Chem. 274 (1999) 38051-38060
64. Staudenmayer N., Ng S., Smith M.B., and Millett F. Effect of specific trifluoroacetylation of individual cytochrome c lysines on the reaction with cytochrome oxidase. Biochemistry 16 (1977) 600-604
65. Smith H.T., Staudenmayer N., and Millett F. Use of specific lysine modifications to locate the reaction site of cytochrome c with cytochrome oxidase. Biochemistry 16 (1977) 4971-4974
66. Ferguson-Miller S., Brautigan D.L., and Margoliash E. 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 (1978) 149-159
67. Dickerson R.E., Takano T., Eisenberg D., Kallai O.B., Samson L., Cooper A., and Margoliash E. Ferricytochrome c. I. General features of the horse and bonito proteins at 2.8 A resolution. J. Biol. Chem. 246 (1971) 1511-1535
68. Yu T., Wang X., Purring-Koch C., Wei Y., and McLendon G.L. A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 276 (2001) 13034-13038
69. Jemmerson R., Liu J., Hausauer D., Lam K.P., Mondino A., and Nelson R.D. A conformational change in cytochrome c of apoptotic and necrotic cells is detected by monoclonal antibody binding and mimicked by association of the native antigen with synthetic phospholipid vesicles. Biochemistry 38 (1999) 3599-3609
70. Rytomaa M., and Kinnunen P.K. Evidence for two distinct acidic phospholipid-binding sites in cytochrome c. J. Biol. Chem. 269 (1994) 1770-1774
71. Ruitenberg M., Kannt A., Bamberg E., Fendler K., and Michel H. Reduction of cytochrome c oxidase by a second electron leads to proton translocation. Nature 417 (2002) 99-102
72. Yoshikawa S., Muramoto K., Shinzawa-Itoh K., Aoyama H., Tsukihara T., Shimokata K., Katayama Y., and Shimada H. Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochim. Biophys. Acta 1757 (2006) 1110-1116
73. Hosler J.P., Ferguson-Miller S., and Mills D.A. Energy transduction: proton transfer through the respiratory complexes. Annu. Rev. Biochem. 75 (2006) 165-187
74. Belevich I., Verkhovsky M.I., and Wikstrom M. Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase. Nature 440 (2006) 829-832
75. Faxen K., Gilderson G., Adelroth P., and Brzezinski P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437 (2005) 286-289
76. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272 (1996) 1136-1144
77. Grossman L.I., and Lomax M.I. Nuclear genes for cytochrome c oxidase. Biochim. Biophys. Acta 1352 (1997) 174-192
78. Hüttemann M., Kadenbach B., and Grossman L.I. Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267 (2001) 111-123
79. Hüttemann M., Schmidt T.R., and Grossman L.I. A third isoform of cytochrome c oxidase subunit VIII is present in mammals. Gene 312 (2003) 95-102
80. Radford N.B., Wan B., Richman A., Szczepaniak L.S., Li J.L., Li K., Pfeiffer K., Schägger H., Garry D.J., and Moreadith R.W. Cardiac dysfunction in mice lacking cytochrome-c oxidase subunit VIaH. Am. J. Physiol. Heart Circ. Physiol. 282 (2002) H726-H733
81. Merle P., and Kadenbach B. Kinetic and structural differences between cytochrome c oxidases from beef liver and heart. Eur. J. Biochem. 125 (1982) 239-244
82. Buge U., and Kadenbach B. Influence of buffer composition, membrane lipids and proteases on the kinetics of reconstituted cytochrome-c oxidase from bovine liver and heart. Eur. J. Biochem. 161 (1986) 383-390
83. Lee I., Salomon A.R., Ficarro S., Mathes I., Lottspeich F., Grossman L.I., and Hüttemann M. cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J. Biol. Chem. 280 (2005) 6094-6100
84. Suarez M.D., Revzin A., Narlock R., Kempner E.S., Thompson D.A., and Ferguson-Miller S. The functional and physical form of mammalian cytochrome c oxidase determined by gel filtration, radiation inactivation, and sedimentation equilibrium analysis. J. Biol. Chem. 259 (1984) 13791-13799
85. Napiwotzki J., Shinzawa-Itoh K., Yoshikawa S., and Kadenbach B. ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol. Chem. 378 (1997) 1013-1021
86. Arnold S., and Kadenbach B. The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett. 443 (1999) 105-108
87. Ludwig B., Bender E., Arnold S., Hüttemann M., Lee I., and Kadenbach B. Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chem. Bio. Chem. 2 (2001) 392-403
88. Arnold S., Goglia F., and Kadenbach B. 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 252 (1998) 325-330
89. Frank V., and Kadenbach B. Regulation of the H+/e- stoichiometry of cytochrome c oxidase from bovine heart by intramitochondrial ATP/ADP ratios. FEBS Lett. 382 (1996) 121-124
90. Lee I., and Kadenbach B. Palmitate decreases proton pumping of liver-type cytochrome c oxidase. Eur. J. Biochem. 268 (2001) 6329-6334
91. Boerner J.L., Demory M.L., Silva C., and Parsons S.J. Phosphorylation of Y845 on the epidermal growth factor receptor mediates binding to the mitochondrial protein cytochrome c oxidase subunit II. Mol. Cell. Biol. 24 (2004) 7059-7071
92. Kato M.V. The mechanisms of death of an erythroleukemic cell line by p53: involvement of the microtubule and mitochondria. Leuk. Lymphoma 33 (1999) 181-186
93. Beauchemin A.M., Gottlieb B., Beitel L.K., Elhaji Y.A., Pinsky L., and Trifiro M.A. Cytochrome c oxidase subunit Vb interacts with human androgen receptor: a potential mechanism for neurotoxicity in spinobulbar muscular atrophy. Brain Res. Bull. 56 (2001) 285-297
94. Yang W.L., Iacono L., Tang W.M., and Chin K.V. Novel function of the regulatory subunit of protein kinase A: regulation of cytochrome c oxidase activity and cytochrome c release. Biochemistry 37 (1998) 14175-14180
95. Brown G.C. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim. Biophys. Acta 1504 (2001) 46-57
96. Brookes P.S. Mitochondrial nitric oxide synthase. Mitochondrion 3 (2004) 187-204
97. Gorren A.C., and Mayer B. Nitric-oxide synthase: a cytochrome P450 family foster child. Biochim. Biophys. Acta 1770 (2006) 432-445
98. Tatoyan A., and Giulivi C. Purification and characterization of a nitric-oxide synthase from rat liver mitochondria. J. Biol. Chem. 273 (1998) 11044-11048
99. Persichini T., Mazzone V., Polticelli F., Moreno S., Venturini G., Clementi E., and Colasanti M. Mitochondrial type I nitric oxide synthase physically interacts with cytochrome c oxidase. Neurosci. Lett. 384 (2005) 254-259
100. Brown G.C., and Cooper C.E. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 356 (1994) 295-298
101. Giulivi C. Functional implications of nitric oxide produced by mitochondria in mitochondrial metabolism. Biochem. J. 332 Pt 3 (1998) 673-679
102. Cuzzocrea S. Role of nitric oxide and reactive oxygen species in arthritis. Curr. Pharm. Des. 12 (2006) 3551-3570
103. Assreuy J. Nitric oxide and cardiovascular dysfunction in sepsis. Endocr. Metab. Immune Disord Drug Targets 6 (2006) 165-173
104. Steiner J., Rafols D., Park H.K., Katar M.S., Rafols J.A., and Petrov T. Attenuation of iNOS mRNA exacerbates hypoperfusion and upregulates endothelin-1 expression in hippocampus and cortex after brain trauma. Nitric Oxide 10 (2004) 162-169
105. Fukumura D., Kashiwagi S., and Jain R.K. The role of nitric oxide in tumour progression. Nat. Rev. Cancer 6 (2006) 521-534
106. Stepp D.W. Impact of obesity and insulin resistance on vasomotor tone: nitric oxide and beyond. Clin. Exp. Pharmacol. Physiol. 33 (2006) 407-414
107. Moncada S., and Bolanos J.P. Nitric oxide, cell bioenergetics and neurodegeneration. J. Neurochem. 97 (2006) 1676-1689
108. Kirichenko A., Vygodina T., Mkrtchyan H.M., and Konstantinov A. Specific cation binding site in mammalian cytochrome oxidase. FEBS Lett. 423 (1998) 329-333
109. Ostermeier C., Harrenga A., Ermler U., and Michel H. Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10547-10553
110. Mills D.A., Schmidt B., Hiser C., Westley E., and Ferguson-Miller S. Membrane potential-controlled inhibition of cytochrome c oxidase by zinc. J. Biol. Chem. 277 (2002) 14894-14901
111. Kuznetsova S.S., Azarkina N.V., Vygodina T.V., Siletsky S.A., and Konstantinov A.A. Zinc ions as cytochrome c oxidase inhibitors: two sites of action. Biochemistry (Mosc) 70 (2005) 128-136
112. Faxen K., Salomonsson L., Adelroth P., and Brzezinski P. Inhibition of proton pumping by zinc ions during specific reaction steps in cytochrome c oxidase. Biochim. Biophys. Acta 1757 (2006) 388-394
113. Sorensen M.B., Stoltenberg M., Danscher G., and Ernst E. Chelation of intracellular zinc ions affects human sperm cell motility. Mol. Hum. Reprod. 5 (1999) 338-341
114. Steenaart N.A., and Shore G.C. Mitochondrial cytochrome c oxidase subunit IV is phosphorylated by an endogenous kinase. FEBS Lett. 415 (1997) 294-298
115. Bender E., and Kadenbach B. The allosteric ATP-inhibition of cytochrome c oxidase activity is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett. 466 (2000) 130-134
116. Lee I., Bender E., and Kadenbach B. Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. Mol. Cell. Biochem. 234-235 (2002) 63-70
117. Prabu S.K., Anandatheerthavarada H.K., Raza H., Srinivasan S., Spear J.F., and Avadhani N.G. Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J. Biol. Chem. 281 (2006) 2061-2070
118. Fang J.K., Prabu S.K., Sepuri N.B., Raza H., Anandatheerthavarada H.K., Galati D., Spear J., and Avadhani N.G. Site specific phosphorylation of cytochrome c oxidase subunits I, IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion. FEBS Lett 581 (2007) 1302-1310
119. Ainscow E.K., and Brand M.D. The responses of rat hepatocytes to glucagon and adrenaline. Application of quantified elasticity analysis. Eur. J. Biochem. 265 (1999) 1043-1055
120. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., and Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15304-15309
121. Miyazaki T., Tanaka S., Sanjay A., and Baron R. The role of c-Src kinase in the regulation of osteoclast function. Mod. Rheumatol. 16 (2006) 68-74
122. Ogbi M., and Johnson J.A. Protein kinase Cepsilon interacts with cytochrome c oxidase subunit IV and enhances cytochrome c oxidase activity in neonatal cardiac myocyte preconditioning. Biochem. J. 393 (2006) 191-199
123. Ogbi M., Chew C.S., Pohl J., Stuchlik O., Ogbi S., and Johnson J.A. Cytochrome c oxidase subunit IV as a marker of protein kinase Cepsilon function in neonatal cardiac myocytes: implications for cytochrome c oxidase activity. Biochem. J. 382 (2004) 923-932
124. Ping P., Zhang J., Zheng Y.T., Li R.C., Dawn B., Tang X.L., Takano H., Balafanova Z., and Bolli R. Demonstration of selective protein kinase C-dependent activation of Src and Lck tyrosine kinases during ischemic preconditioning in conscious rabbits. Circ. Res. 85 (1999) 542-550
125. Song C., Vondriska T.M., Wang G.W., Klein J.B., Cao X., Zhang J., Kang Y.J., D'Souza S., and Ping P. Molecular conformation dictates signaling module formation: example of PKCepsilon and Src tyrosine kinase. Am. J. Physiol. Heart Circ. Physiol. 282 (2002) H1166-H1171
126. Noji H., Yasuda R., Yoshida M., and Kinosita Jr. K. Direct observation of the rotation of F1-ATPase. Nature 386 (1997) 299-302
127. Sambongi Y., Iko Y., Tanabe M., Omote H., Iwamoto-Kihara A., Ueda I., Yanagida T., Wada Y., and Futai M. Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science 286 (1999) 1722-1724
128. Kaim G., and Dimroth P. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. Embo J. 18 (1999) 4118-4127
129. Lalanne E., Mathieu C., Vedel F., and De Paepe R. Tissue-specific expression of genes encoding isoforms of the mitochondrial ATPase beta subunit in Nicotiana sylvestris. Plant Mol. Biol. 38 (1998) 885-888
130. Rouslin W. Regulation of the mitochondrial ATPase in situ in cardiac muscle: role of the inhibitor subunit. J. Bioenerg. Biomembranes 23 (1991) 873-888
131. Garcia J.J., Morales-Rios E., Cortes-Hernandez P., and Rodriguez-Zavala J.S. The inhibitor protein (IF1) promotes dimerization of the mitochondrial F1F0-ATP synthase. Biochemistry 45 (2006) 12695-12703
132. 0 ATPase delta-subunit is regulated by platelet-derived growth factor in mouse cortical neurons in vitro. J. Neurochem. 65 (1995) 2812-2815
133. Ko Y.H., Pan W., Inoue C., and Pedersen P.L. Signal transduction to mitochondrial ATP synthase: evidence that PDGF-dependent phosphorylation of the delta-subunit occurs in several cell lines, involves tyrosine, and is modulated by lysophosphatidic acid. Mitochondrion 1 (2002) 339-348
134. Vosseller K., Hansen K.C., Chalkley R.J., Trinidad J.C., Wells L., Hart G.W., and Burlingame A.L. Quantitative analysis of both protein expression and serine/threonine post-translational modifications through stable isotope labeling with dithiothreitol. Proteomics 5 (2005) 388-398
135. Struglics A., Fredlund K.M., Moller I.M., and Allen J.F. Two subunits of the F0F1-ATPase are phosphorylated in the inner mitochondrial membrane. Biochem. Biophys. Res. Commun. 243 (1998) 664-668
136. Del Riego G., Casano L.M., Martin M., and Sabater B. Multiple phosphorylation sites in the beta subunit of thylakoid ATP synthase. Photosynth. Res. 89 (2006) 11-18
137. Hojlund K., Wrzesinski K., Larsen P.M., Fey S.J., Roepstorff P., Handberg A., Dela F., Vinten J., McCormack J.G., Reynet C., and Beck-Nielsen H. Proteome analysis reveals phosphorylation of ATP synthase beta-subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes. J. Biol. Chem. 278 (2003) 10436-10442
138. Krause-Buchholz U., Becker J.S., Zoriy M., Pickhardt C., Przybylski M., Rödel G., and Becker J.S. Detection of phosphorylated subunits by combined LA-ICP-MS and MALDI-FTICR-MS analysis in yeast mitochondrial membrane complexes separated by blue native/SDS-PAGE. Int. J. Mass Spectr. 248 (2006) 56-60
139. Chen C., Ko Y., Delannoy M., Ludtke S.J., Chiu W., and Pedersen P.L. Mitochondrial ATP synthasome: three-dimensional structure by electron microscopy of the ATP synthase in complex formation with carriers for Pi and ADP/ATP. J. Biol. Chem. 279 (2004) 31761-31768
140. Ko Y.H., Delannoy M., Hullihen J., Chiu W., and Pedersen P.L. Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J. Biol. Chem. 278 (2003) 12305-12309
141. Arnold I., Pfeiffer K., Neupert W., Stuart R.A., and Schägger H. Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. Embo J. 17 (1998) 7170-7178
142. Schägger H., and Pfeiffer K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. Embo J. 19 (2000) 1777-1783
143. Paumard P., Vaillier J., Coulary B., Schaeffer J., Soubannier V., Mueller D.M., Brethes D., di Rago J.P., and Velours J. The ATP synthase is involved in generating mitochondrial cristae morphology. Embo J. 21 (2002) 221-230
144. Arselin G., Vaillier J., Salin B., Schaeffer J., Giraud M.F., Dautant A., Brethes D., and Velours J. The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J. Biol. Chem. 279 (2004) 40392-40399
145. Bornhovd C., Vogel F., Neupert W., and Reichert A.S. Mitochondrial membrane potential is dependent on the oligomeric state of F1F0-ATP synthase supracomplexes. J. Biol. Chem. 281 (2006) 13990-13998
146. Di Pancrazio F., Bisetto E., Alverdi V., Mavelli I., Esposito G., and Lippe G. Differential steady-state tyrosine phosphorylation of two oligomeric forms of mitochondrial F0F1ATPsynthase: a structural proteomic analysis. Proteomics 6 (2006) 921-926
147. Schägger H., and von Jagow G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199 (1991) 223-231
148. Wittig I., Carrozzo R., Santorelli F.M., and Schägger H. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta 1757 (2006) 1066-1072
149. Schägger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 1555 (2002) 154-159
150. Genova M.L., Bianchi C., and Lenaz G. Supercomplex organization of the mitochondrial respiratory chain and the role of the Coenzyme Q pool: pathophysiological implications. Biofactors 25 (2005) 5-20
151. Lenaz G., and Genova M.L. Kinetics of integrated electron transfer in the mitochondrial respiratory chain: random collisions versus solid state electron channeling. Am. J. Physiol. Cell Physiol. 292 (2006) C1221-C1239
152. Kadenbach B. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta 1604 (2006) 77-94
153. Kadenbach B., Arnold S., Lee I., and Hüttemann M. The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases. Biochim. Biophys. Acta 1655 (2004) 400-408
154. Pfeiffer K., Gohil V., Stuart R.A., Hunte C., Brandt U., Greenberg M.L., and Schägger H. Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278 (2003) 52873-52880
155. Brandner K., Mick D.U., Frazier A.E., Taylor R.D., Meisinger C., and Rehling P. Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth Syndrome. Mol. Biol. Cell 16 (2005) 5202-5214
156. Li G., Chen S., Thompson M.N., and Greenberg M.L. New insights into the regulation of cardiolipin biosynthesis in yeast: implications for Barth syndrome. Biochim. Biophys. Acta 1771 (2006) 432-441
157. McKenzie M., Lazarou M., Thorburn D.R., and Ryan M.T. Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J. Mol. Biol. 361 (2006) 462-469
158. Hood D.A. Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 90 (2001) 1137-1157
159. Freyssenet D., Di Carlo M., and Hood D.A. Calcium-dependent regulation of cytochrome c gene expression in skeletal muscle cells. Identification of a protein kinase c-dependent pathway. J. Biol. Chem. 274 (1999) 9305-9311
160. Pilegaard H., Saltin B., and Neufer P.D. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J. Physiol. 546 (2003) 851-858
161. Takahashi M., Chesley A., Freyssenet D., and Hood D.A. Contractile activity-induced adaptations in the mitochondrial protein import system. Am. J. Physiol. 274 (1998) C1380-C1387
162. Ito Y., Pandey P., Mishra N., Kumar S., Narula N., Kharbanda S., Saxena S., and Kufe D. Targeting of the c-Abl tyrosine kinase to mitochondria in endoplasmic reticulum stress-induced apoptosis. Mol. Cell. Biol. 21 (2001) 6233-6242
163. Livigni A., Scorziello A., Agnese S., Adornetto A., Carlucci A., Garbi C., Castaldo I., Annunziato L., Avvedimento E.V., and Feliciello A. Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol. Biol. Cell 17 (2006) 263-271
164. Bijur G.N., and Jope R.S. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J. Neurochem. 87 (2003) 1427-1435
165. Li L., Lorenzo P.S., Bogi K., Blumberg P.M., and Yuspa S.H. Protein kinase Cdelta targets mitochondria, alters mitochondrial membrane potential, and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector. Mol. Cell. Biol. 19 (1999) 8547-8558
166. Churchill E.N., and Szweda L.I. Translocation of deltaPKC to mitochondria during cardiac reperfusion enhances superoxide anion production and induces loss in mitochondrial function. Arch. Biochem. Biophys. 439 (2005) 194-199
167. Salvi M., Stringaro A., Brunati A.M., Agostinelli E., Arancia G., Clari G., and Toninello A. Tyrosine phosphatase activity in mitochondria: presence of Shp-2 phosphatase in mitochondria. Cell. Mol. Life Sci. 61 (2004) 2393-2404
168. Tartaglia M., Mehler E.L., Goldberg R., Zampino G., Brunner H.G., Kremer H., van der Burgt I., Crosby A.H., Ion A., Jeffery S., Kalidas K., Patton M.A., Kucherlapati R.S., and Gelb B.D. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat. Genet. 29 (2001) 465-468
169. Neel B.G., Gu H., and Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem. Sci. 28 (2003) 284-293
170. Uhlen P., Burch P.M., Zito C.I., Estrada M., Ehrlich B.E., and Bennett A.M. Gain-of-function/Noonan syndrome SHP-2/Ptpn11 mutants enhance calcium oscillations and impair NFAT signaling. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2160-2165
171. Liu S.S. Cooperation of a "reactive oxygen cycle" with the Q cycle and the proton cycle in the respiratory chain-superoxide generating and cycling mechanisms in mitochondria. J. Bioenerg. Biomembranes 31 (1999) 367-376
172. Korshunov S.S., Skulachev V.P., and Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416 (1997) 15-18
173. Mackler B., Person R.E., Nguyen T.D., and Fantel A.G. Studies of the cellular distribution of superoxide dismutases in adult and fetal rat tissues. Free Radic. Res. 28 (1998) 125-129
174. Fantel A.G., and Person R.E. Involvement of mitochondria and other free radical sources in normal and abnormal fetal development. Ann. N. Y. Acad. Sci. 959 (2002) 424-433
175. Conrad M., Jakupoglu C., Moreno S.G., Lippl S., Banjac A., Schneider M., Beck H., Hatzopoulos A.K., Just U., Sinowatz F., Schmahl W., Chien K.R., Wurst W., Bornkamm G.W., and Brielmeier M. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24 (2004) 9414-9423
176. M. Siman, Congenital malformations in experimental diabetic pregnancy: aetiology and antoxidative treatment. Minireview based on a doctoral thesis, Ups J Med Sci 102 (1997) 61-98.
177. Pedersen P.L. Tumor mitochondria and the bioenergetics of cancer cells. Prog. Exp. Tumor Res. 22 (1978) 190-274
178. Bui T., and Thompson C.B. Cancer's sweet tooth. Cancer Cells 9 (2006) 419-420
179. Krieg R.C., Knuechel R., Schiffmann E., Liotta L.A., Petricoin III E.F., and Herrmann P.C. Mitochondrial proteome: cancer-altered metabolism associated with cytochrome c oxidase subunit level variation. Proteomics 4 (2004) 2789-2795
180. von Wangenheim K.H., and Peterson H.P. Control of cell proliferation by progress in differentiation: clues to mechanisms of aging, cancer causation and therapy. J. Theor. Biol. 193 (1998) 663-678
181. Chatterjee A., Mambo E., and Sidransky D. Mitochondrial DNA mutations in human cancer. Oncogene 25 (2006) 4663-4674
182. Jakupciak J.P., Dakubo G.D., Maragh S., and Parr R.L. Analysis of potential cancer biomarkers in mitochondrial DNA. Curr. Opin. Mol. Ther. 8 (2006) 500-506
183. Ohta S. Contribution of somatic mutations in the mitochondrial genome to the development of cancer and tolerance against anticancer drugs. Oncogene 25 (2006) 4768-4776
184. Matoba S., Kang J.G., Patino W.D., Wragg A., Boehm M., Gavrilova O., Hurley P.J., Bunz F., and Hwang P.M. p53 regulates mitochondrial respiration. Science 312 (2006) 1650-1653
185. Fantin V.R., and Leder P. Mitochondriotoxic compounds for cancer therapy. Oncogene 25 (2006) 4787-4797
186. Grad J.M., Cepero E., and Boise L.H. Mitochondria as targets for established and novel anti-cancer agents. Drug Resist. Updat. 4 (2001) 85-91
187. Schiavi F., Boedeker C.C., Bausch B., Peczkowska M., Gomez C.F., Strassburg T., Pawlu C., Buchta M., Salzmann M., Hoffmann M.M., Berlis A., Brink I., Cybulla M., Muresan M., Walter M.A., Forrer F., Valimaki M., Kawecki A., Szutkowski Z., Schipper J., Walz M.K., Pigny P., Bauters C., Willet-Brozick J.E., Baysal B.E., Januszewicz A., Eng C., Opocher G., and Neumann H.P. Predictors and prevalence of paraganglioma syndrome associated with mutations of the SDHC gene. Jama 294 (2005) 2057-2063
188. Slane B.G., Aykin-Burns N., Smith B.J., Kalen A.L., Goswami P.C., Domann F.E., and Spitz D.R. Mutation of succinate dehydrogenase subunit C results in increased O2{radical dot}-, oxidative stress, and genomic instability. Cancer Res. 66 (2006) 7615-7620
189. Gonzalez-Cabo P., Vazquez-Manrique R.P., Garcia-Gimeno M.A., Sanz P., and Palau F. Frataxin interacts functionally with mitochondrial electron transport chain proteins. Hum. Mol. Genet. 14 (2005) 2091-2098
190. Calabrese V., Lodi R., Tonon C., D'Agata V., Sapienza M., Scapagnini G., Mangiameli A., Pennisi G., Stella A.M., and Butterfield D.A. Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia. J. Neurol. Sci. 233 (2005) 145-162
191. Parker Jr. W.D., Parks J., Filley C.M., and Kleinschmidt-DeMasters B.K. Electron transport chain defects in Alzheimer's disease brain. Neurology 44 (1994) 1090-1096
192. Bosetti F., Brizzi F., Barogi S., Mancuso M., Siciliano G., Tendi E.A., Murri L., Rapoport S.I., and Solaini G. Cytochrome c oxidase and mitochondrial F1F0-ATPase (ATP synthase) activities in platelets and brain from patients with Alzheimer's disease. Neurobiol. Aging 23 (2002) 371-376
193. Devi L., Prabhu B.M., Galati D.F., Avadhani N.G., and Anandatheerthavarada H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J. Neurosci. 26 (2006) 9057-9068
194. Kim S.H., Vlkolinsky R., Cairns N., and Lubec G. Decreased levels of complex III core protein 1 and complex V beta chain in brains from patients with Alzheimer's disease and Down syndrome. Cell. Mol. Life Sci. 57 (2000) 1810-1816
195. Abou-Sleiman P.M., Muqit M.M., and Wood N.W. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci. 7 (2006) 207-219
196. Elkon H., Don J., Melamed E., Ziv I., Shirvan A., and Offen D. Mutant and wild-type alpha-synuclein interact with mitochondrial cytochrome c oxidase. J. Mol. Neurosci. 18 (2002) 229-238
197. Sun F., Huo X., Zhai Y., Wang A., Xu J., Su D., Bartlam M., and Rao Z. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121 (2005) 1043-1057
198. Sanishvili R., Volz K.W., Westbrook E.M., and Margoliash E. The low ionic strength crystal structure of horse cytochrome c at 2.1 A resolution and comparison with its high ionic strength counterpart. Structure 3 (1995) 707-716
199. Rastogi V.K., and Girvin M.E. Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402 (1999) 263-268
200. Gibbons C., Montgomery M.G., Leslie A.G., and Walker J.E. The structure of the central stalk in bovine F(1)-ATPase at 2.4 A resolution. Nat. Struct. Biol. 7 (2000) 1055-1061
201. Dickson V.K., Silvester J.A., Fearnley I.M., Leslie A.G., and Walker J.E. On the structure of the stator of the mitochondrial ATP synthase. Embo J. 25 (2006) 2911-2918
202. Wilkens S., Borchardt D., Weber J., and Senior A.E. Structural characterization of the interaction of the delta and alpha subunits of the Escherichia coli F1F0-ATP synthase by NMR spectroscopy. Biochemistry 44 (2005) 11786-11794