Cytochrome c oxidase: Evolution of control via nuclear subunit addition

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 4, 2012, Pages 590-597

  Pierron, Denis ^a   Wildman, Derek E ^a   Hüttemann, Maik ^a   Markondapatnaikuni, Gopi Chand ^a   Aras, Siddhesh ^a   Grossman, Lawrence I ^a  

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

Author keywords

Endosymbiosis; Evolution; Mitochondria; Oxidative phosphorylation; Regulation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; OXYGEN;

ENDOSYMBIOSIS; ENZYME SUBUNIT; EUKARYOTE; EVOLUTION; GENE EXPRESSION REGULATION; GENOME; GLYCOLYSIS; HYPOXIA; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIMATE; PRIORITY JOURNAL; PROKARYOTE; REVIEW; TISSUE SPECIFICITY; VERTEBRATE;

ANIMALS; CELL NUCLEUS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; EVOLUTION, MOLECULAR; HUMANS; MODELS, GENETIC; OXIDATIVE PHOSPHORYLATION; OXYGEN; PROTEIN SUBUNITS;

EUKARYOTA; MAMMALIA; PRIMATES; VERTEBRATA;

EID: 84857922138     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.07.007     Document Type: Review

References (105)

1. T.A. Richards, and J.M. Archibald Cell evolution: gene transfer agents and the origin of mitochondria Curr. Biol. 21 2011 R112 R114
2. C. Zimmer Origins. On the origin of eukaryotes Science 325 2009 666 668
3. L. Sagan On the origin of mitosing cells J. Theor. Biol. 14 1967 255 274
4. R.L. Veech The metabolism of lactate NMR Biomed. 4 1991 53 58
5. S.V. Avery Molecular targets of oxidative stress Biochem. J. 434 2011 201 210
6. C. Pacelli, D. Latorre, T. Cocco, F. Capuano, C. Kukat, P. Seibel, and G. Villani Tight control of mitochondrial membrane potential by cytochrome c oxidase Mitochondrion 11 2011 334 341
7. G. Villani, and G. Attardi 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 1997 1166 1171
8. M. Hüttemann, S. Helling, T.H. Sanderson, C. Sinkler, L. Samavati, G. Mahapatra, A. Varughese, G. Lu, J. Liu, L.I. Grossman, J.W. Doan, K. Marcus, and I. Lee 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 2012 598 609
9. F. Fontanesi, I.C. Soto, D. Horn, and A. Barrientos Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process Am. J. Physiol. Cell Physiol. 291 2006 C1129 C1147
10. K. Follmann, S. Arnold, S. Ferguson-Miller, and B. Kadenbach Cytochrome c oxidase from eucaryotes but not from procaryotes is allosterically inhibited by ATP Biochem. Mol. Biol. Int. 45 1998 1047 1055
11. G. Benard, B. Faustin, E. Passerieux, A. Galinier, C. Rocher, N. Bellance, J.P. Delage, L. Casteilla, T. Letellier, and R. Rossignol Physiological diversity of mitochondrial oxidative phosphorylation Am. J. Physiol. Cell Physiol. 291 2006 C1172 C1182
12. C. Vijayasarathy, I. Biunno, N. Lenka, M. Yang, A. Basu, I.P. Hall, and N.G. Avadhani Variations in the subunit content and catalytic activity of the cytochrome c oxidase complex from different tissues and different cardiac compartments Biochim. Biophys. Acta 1371 1998 71 82
13. R.S. Seelan, and L.I. Grossman Cytochrome c oxidase subunit VIIa isoforms. Characterization and expression of bovine cDNAs J. Biol. Chem. 266 1991 19752 19757
14. M.I. Lomax, and L.I. Grossman Tissue-specific genes for respiratory proteins Trends Biochem. Sci. 14 1989 501 503
15. M. Huttemann, B. Kadenbach, and L.I. Grossman Mammalian subunit IV isoforms of cytochrome c oxidase Gene 267 2001 111 123
16. S.A. Jaradat, M.S. Ko, and L.I. Grossman Tissue-specific expression and mapping of the Cox7ah gene in mouse Genomics 49 1998 363 370
17. B. Ludwig, E. Bender, S. Arnold, M. Huttemann, I. Lee, and B. Kadenbach Cytochrome c oxidase and the regulation of oxidative phosphorylation Chembiochem 2 2001 392 403
18. M.K. Wikstrom Proton pump coupled to cytochrome c oxidase in mitochondria Nature 266 1977 271 273
19. P. Steinrucke, G.C. Steffens, G. Panskus, G. Buse, and B. Ludwig Subunit II of cytochrome c oxidase from Paracoccus denitrificans. DNA sequence, gene expression and the protein Eur. J. Biochem. 167 1987 431 439
20. M. Raitio, T. Jalli, and M. Saraste Isolation and analysis of the genes for cytochrome c oxidase in Paracoccus denitrificans EMBO J. 6 1987 2825 2833
21. S. Iwata, C. Ostermeier, B. Ludwig, and H. Michel Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans Nature 376 1995 660 669
22. T. Tsukihara, H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A Science 269 1995 1069 1074
23. T. Tsukihara, H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A Science 272 1996 1136 1144
24. S. Yoshikawa, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, E. Yamashita, N. Inoue, M. Yao, M.J. Fei, C.P. Libeu, T. Mizushima, H. Yamaguchi, T. Tomizaki, and T. Tsukihara Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase Science 280 1998 1723 1729
25. P. Mitchell Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 1961 144 148
26. J.P. Hosler, S. Ferguson-Miller, M.W. Calhoun, J.W. Thomas, J. Hill, L. Lemieux, J. Ma, C. Georgiou, J. Fetter, and J. Shapleigh Insight into the active-site structure and function of cytochrome oxidase by analysis of site-directed mutants of bacterial cytochrome aa3 and cytochrome bo J. Bioenerg. Biomembr. 25 1993 121 136
27. J.W. Thomas, L.J. Lemieux, J.O. Alben, and R.B. Gennis Site-directed mutagenesis of highly conserved residues in helix VIII of subunit I of the cytochrome bo ubiquinol oxidase from Escherichia coli: an amphipathic transmembrane helix that may be important in conveying protons to the binuclear center Biochemistry 32 1993 11173 11180
28. J.W. Thomas, A. Puustinen, J.O. Alben, R.B. Gennis, and M. Wikstrom Substitution of asparagine for aspartate-135 in subunit I of the cytochrome bo ubiquinol oxidase of Escherichia coli eliminates proton-pumping activity Biochemistry 32 1993 10923 10928
29. J.R. Fetter, J. Qian, J. Shapleigh, J.W. Thomas, A. Garcia-Horsman, E. Schmidt, J. Hosler, G.T. Babcock, R.B. Gennis, and S. Ferguson-Miller Possible proton relay pathways in cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 92 1995 1604 1608
30. R. Szklarczyk, and M.A. Huynen Mosaic origin of the mitochondrial proteome Proteomics 10 2010 4012 4024
31. X. Perez-Martinez, M. Vazquez-Acevedo, E. Tolkunova, S. Funes, M.G. Claros, E. Davidson, M.P. King, and D. Gonzalez-Halphen Unusual location of a mitochondrial gene. Subunit III of cytochrome c oxidase is encoded in the nucleus of Chlamydomonad algae J. Biol. Chem. 275 2000 30144 30152
32. X. Perez-Martinez, A. Antaramian, M. Vazquez-Acevedo, S. Funes, E. Tolkunova, d'Alayer J., M.G. Claros, E. Davidson, M.P. King, and D. Gonzalez-Halphen Subunit II of cytochrome c oxidase in chlamydomonad algae is a heterodimer encoded by two independent nuclear genes J. Biol. Chem. 276 2001 11302 11309
33. R.M.R. Gawryluk, and M.W. Gray An ancient fission of mitochondrial cox1 Mol. Biol. Evol. 27 2010 7 10
34. J. Das, S.T. Miller, and D.L. Stern Comparison of diverse protein sequences of the nuclear-encoded subunits of cytochrome c oxidase suggests conservation of structure underlies evolving functional sites Mol. Biol. Evol. 21 2004 1572 1582
35. S.G. Andersson, A. Zomorodipour, J.O. Andersson, T. Sicheritz-Ponten, U.C. Alsmark, R.M. Podowski, A.K. Naslund, A.S. Eriksson, H.H. Winkler, and C.G. Kurland The genome sequence of Rickettsia prowazekii and the origin of mitochondria Nature 396 1998 133 140
36. B.F. Lang, G. Burger, C.J. O'Kelly, R. Cedergren, G.B. Golding, C. Lemieux, D. Sankoff, M. Turmel, and M.W. Gray An ancestral mitochondrial DNA resembling a eubacterial genome in miniature Nature 387 1997 493 497
37. R.A. Capaldi Structure and function of cytochrome c oxidase Annu. Rev. Biochem. 59 1990 569 596
38. P. Dolezal, V. Likic, J. Tachezy, and T. Lithgow Evolution of the molecular machines for protein import into mitochondria Science 313 2006 314 318
39. A.J. Perry, K.A. Rimmer, H.D.T. Mertens, R.F. Waller, T.D. Mulhern, T. Lithgow, and P.R. Gooley Structure, topology and function of the translocase of the outer membrane of mitochondria Plant Physiol. Biochem. 46 2008 265 274
40. F. Alcock, A. Clements, C. Webb, and T. Lithgow Evolution. Tinkering inside the organelle Science 327 2010 649 650
41. A. Clements, D. Bursac, X. Gatsos, A.J. Perry, S. Civciristov, N. Celik, V.A. Likic, S. Poggio, C. Jacobs-Wagner, R.A. Strugnell, and T. Lithgow The reducible complexity of a mitochondrial molecular machine Proc. Natl. Acad. Sci. U. S. A. 106 2009 15791 15795
42. J. Gross, and D. Bhattacharya Endosymbiont or host: who drove mitochondrial and plastid evolution? Biol. Direct 6 2011 12
43. J. Tong, P. Dolezal, J. Selkrig, S. Crawford, A.G. Simpson, N. Noinaj, S.K. Buchanan, K. Gabriel, and T. Lithgow Ancestral and derived protein import pathways in the mitochondrion of Reclinomonas americana Mol. Biol. Evol. 28 2011 1581 1591
44. R. Lucattini, V.A. Likic, and T. Lithgow Bacterial proteins predisposed for targeting to mitochondria Mol. Biol. Evol. 21 2004 652 658
45. T. Lithgow, and A. Schneider Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes Philos. Trans. R. Soc. Lond. B Biol. Sci. 365 2010 799 817
46. F. Arnesano, L. Banci, I. Bertini, and M. Martinelli Ortholog search of proteins involved in copper delivery to cytochrome c oxidase and functional analysis of paralogs and gene neighbors by genomic context J. Proteome Res. 4 2005 63 70
47. A. Barrientos, K. Gouget, D. Horn, I.C. Soto, and F. Fontanesi Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process Biochim. Biophys. Acta 1793 2009 97 107
48. A.E.P. LaMarche, M.I. Abate, S.H.P. Chan, and B.L. Trumpower Isolation and characterization of COX12, the nuclear gene for a previously unrecognized subunit of Saccharomyces cerevisiae cytochrome c oxidase J. Biol. Chem. 267 1992 22473 22480
49. S. Arnold, and B. Kadenbach The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically FEBS Lett. 443 1999 105 108
50. S. Arnold, F. Goglia, and B. Kadenbach 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
51. L.I. Grossman, and M.I. Lomax Nuclear genes for cytochrome c oxidase Biochim. Biophys. Acta 1352 1997 174 192
52. M. Huttemann, T.R. Schmidt, and L.I. Grossman A third isoform of cytochrome c oxidase subunit VIII is present in mammals Gene 312 2003 95 102
53. R. Smeenk, and M. Hylkema Detection of antibodies to DNA: a technical assessment Mol. Biol. Rep. 17 1992 71 79
54. M. Huttemann, S. Jaradat, and L.I. Grossman 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
55. A.G. Little, K.M. Kocha, S.C. Lougheed, and C.D. Moyes Evolution of the nuclear-encoded cytochrome oxidase subunits in vertebrates Physiol. Genomics 42 2010 76 84
56. D. Mishmar, E. Ruiz-Pesini, M. Brandon, and D.C. Wallace Mitochondrial DNA-like sequences in the nucleus (NUMTs): insights into our African origins and the mechanism of foreign DNA integration Hum. Mutat. 23 2004 125 133
57. M. Huttemann, I. Lee, A. Pecinova, P. Pecina, K. Przyklenk, and J.W. Doan Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease J. Bioenerg. Biomembr. 40 2008 445 456
58. T. Blomme, K. Vandepoele, S. De Bodt, C. Simillion, S. Maere, and Y. Van de Peer The gain and loss of genes during 600 million years of vertebrate evolution Genome Biol. 7 2006 R43
59. L. Abi-Rached, A. Gilles, T. Shiina, P. Pontarotti, and H. Inoko Evidence of en bloc duplication in vertebrate genomes Nat. Genet. 31 2002 100 105
60. M. Lynch, M. O'Hely, B. Walsh, and A. Force The probability of preservation of a newly arisen gene duplicate Genetics 159 2001 1789 1804
61. M. Lynch, and A. Force The probability of duplicate gene preservation by subfunctionalization Genetics 154 2000 459 473
62. G. Bonne, P. Seibel, S. Possekel, C. Marsac, and B. Kadenbach Expression of human cytochrome c oxidase subunits during fetal development Eur. J. Biochem. 217 1993 1099 1107
63. D.A. Hood, R. Zak, and D. Pette Chronic stimulation of rat skeletal muscle induces coordinate increases in mitochondrial and nuclear mRNAs of cytochrome-c-oxidase subunits Eur. J. Biochem. 179 1989 275 280
64. L. Kuhn-Nentwig, and B. Kadenbach Isolation and properties of cytochrome c oxidase from rat liver and quantification of immunological differences between isozymes from various rat tissues with subunit-specific antisera Eur. J. Biochem. 149 1985 147 158
65. M.J. Kelly, R.K. Poole, M.G. Yates, and C. Kennedy Cloning and mutagenesis of genes encoding the cytochrome bd terminal oxidase complex in Azotobacter vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air J. Bacteriol. 172 1990 6010 6019
66. S. Hill, S. Viollet, A.T. Smith, and C. Anthony Roles for enteric D-type cytochrome-oxidase in N-2 fixation and microaerobiosis J. Bacteriol. 172 1990 2071 2078
67. I. Belevich, V.B. Borisov, A.A. Konstantinov, and M.I. Verkhovsky Oxygenated complex of cytochrome bd from Escherichia coli: stability and photolability FEBS Lett. 579 2005 4567 4570
68. B. Szal, Y. Jolivet, M.P. Hasenfratz-Sauder, P. Dizengremel, and A.M. Rychter Oxygen concentration regulates alternative oxidase expression in barley roots during hypoxia and post-hypoxia Physiol. Plantarum 119 2003 494 502
69. S. Biemelt, U. Keetman, and G. Albrecht Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings Plant Physiol. 116 1998 651 658
70. K.J. Gupta, A. Zabalza, and J.T. van Dongen Regulation of respiration when the oxygen availability changes Physiol. Plant. 137 2009 383 391
71. A. McDonald, and G. Vanlerberghe Branched mitochondrial electron transport in the Animalia: presence of alternative oxidase in several animal phyla IUBMB Life 56 2004 333 341
72. A.E. McDonald, G.C. Vanlerberghe, and J.F. Staples Alternative oxidase in animals: unique characteristics and taxonomic distribution J. Exp. Biol. 212 2009 2627 2634
73. A. Atteia, R. van Lis, J.J. van Hellemond, A.G. Tielens, W. Martin, and K. Henze Identification of prokaryotic homologues indicates an endosymbiotic origin for the alternative oxidases of mitochondria (AOX) and chloroplasts (PTOX) Gene 330 2004 143 148
74. A.E. McDonald, and G.C. Vanlerberghe Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase Comp. Biochem. Physiol. Part D Genomics Proteomics 1 2006 357 364
75. K.R. Wotton, and S.M. Shimeld Comparative genomics of vertebrate Fox cluster loci BMC Genomics 7 2006 271
76. R. Fukuda, H. Zhang, J.W. Kim, L. Shimoda, C.V. Dang, and G.L. Semenza HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells Cell 129 2007 111 122
77. M. Huttemann, I. Lee, J. Liu, and L.I. Grossman Transcription of mammalian cytochrome c oxidase subunit IV-2 is controlled by a novel conserved oxygen responsive element FEBS J. 274 2007 5737 5748
78. C. Wu, C. Orozco, J. Boyer, M. Leglise, J. Goodale, S. Batalov, C.L. Hodge, J. Haase, J. Janes, J.W. Huss III, and A.I. Su BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources Genome Biol. 10 2009 R130
79. P.V. Burke, and R.O. Poyton Structure/function of oxygen-regulated isoforms in cytochrome c oxidase J. Exp. Biol. 201 1998 1163 1175
80. D. Sandona, S. Gastaldello, R. Rizzuto, and R. Bisson Expression of cytochrome c oxidase during growth and development of Dictyostelium J. Biol. Chem. 270 1995 5587 5593
81. G. Schiavo, and R. Bisson Oxygen influences the subunit structure of cytochrome c oxidase in the slime mold Dictyostelium discoideum J. Biol. Chem. 264 1989 7129 7134
82. G.R. Scott, P.M. Schulte, S. Egginton, A.L. Scott, J.G. Richards, and W.K. Milsom Molecular evolution of cytochrome c oxidase underlies high-altitude adaptation in the bar-headed goose Mol. Biol. Evol. 28 2011 351 363
83. Y. Luo, W. Gao, Y. Gao, S. Tang, Q. Huang, X. Tan, J. Chen, and T. Huang Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation Mitochondrion 8 2008 352 357
84. R. Ramharack, and R.G. Deeley Structure and evolution of primate cytochrome c oxidase subunit II gene J. Biol. Chem. 262 1987 14014 14021
85. R.M. Adkins, and R.L. Honeycutt Evolution of the primate cytochrome c oxidase subunit II gene J. Mol. Evol. 38 1994 215 231
86. T.R. Schmidt, S.A. Jaradat, M. Goodman, M.I. Lomax, and L.I. Grossman Molecular evolution of cytochrome c oxidase: rate variation among subunit VIa isoforms Mol. Biol. Evol. 14 1997 595 601
87. W. Wu, M. Goodman, M.I. Lomax, and L.I. Grossman Molecular evolution of cytochrome c oxidase subunit IV: evidence for positive selection in simian primates J. Mol. Evol. 44 1997 477 491
88. T.R. Schmidt, M. Goodman, and L.I. Grossman Molecular evolution of the COX7A gene family in primates Mol. Biol. Evol. 16 1999 619 626
89. T.D. Andrews, and S. Easteal Evolutionary rate acceleration of cytochrome c oxidase subunit I in simian primates J. Mol. Evol. 50 2000 562 568
90. W. Wu, T.R. Schmidt, M. Goodman, and L.I. Grossman Molecular evolution of cytochrome c oxidase subunit I in primates: is there coevolution between mitochondrial and nuclear genomes? Mol. Phylogenet. Evol. 17 2000 294 304
91. A. Goldberg, D.E. Wildman, T.R. Schmidt, M. Hüttemann, M. Goodman, M.L. Weiss, and L.I. Grossman Adaptive evolution of cytochrome c oxidase subunit VIII in anthropoid primates Proc. Natl. Acad. Sci. U. S. A. 100 2003 5873 5878
92. M. Uddin, J.C. Opazo, D.E. Wildman, C.C. Sherwood, P.R. Hof, M. Goodman, and L.I. Grossman Molecular evolution of the cytochrome c oxidase subunit 5A gene in primates BMC Evol. Biol. 8 2008 8
93. J.W. Doan, T.R. Schmidt, D.E. Wildman, M. Uddin, A. Goldberg, M. Huttemann, M. Goodman, M.L. Weiss, and L.I. Grossman Coadaptive evolution in cytochrome c oxidase: 9 of 13 subunits show accelerated rates of nonsynonymous substitution in anthropoid primates Mol. Phylogenet. Evol. 33 2004 944 950
94. T.R. Schmidt, M. Goodman, and L.I. Grossman Amino acid replacement is rapid in primates for the mature polypeptides of COX subunits, but not for their targeting presequences Gene 286 2002 13 19
95. N. Osheroff, S.H. Speck, E. Margoliash, E.C. Veerman, J. Wilms, B.W. Konig, and A.O. Muijsers The reaction of primate cytochromes c with cytochrome c oxidase. Analysis of the polarographic assay J. Biol. Chem. 258 1983 5731 5738
96. A.B. Van Kuilenburg, A.C. Gorren, H.L. Dekker, P. Nieboer, B.F. Van Gelder, and A.O. Muijsers Presteady-state and steady-state kinetic properties of human cytochrome c oxidase. Identification of rate-limiting steps in mammalian cytochrome c oxidase Eur. J. Biochem. 205 1992 1145 1154
97. V. Rodriguez-Roldan, J.M. Garcia-Heredia, J.A. Navarro, M. Hervas, B. De la Cerda, F.P. Molina-Heredia, and M.A. De la Rosa A comparative kinetic analysis of the reactivity of plant, horse, and human respiratory cytochrome c towards cytochrome c oxidase Biochem. Biophys. Res. Commun. 346 2006 1108 1113
98. T.R. Schmidt, D.E. Wildman, M. Uddin, J.C. Opazo, M. Goodman, and L.I. Grossman Rapid electrostatic evolution at the binding site for cytochrome c on cytochrome c oxidase in anthropoid primates Proc. Natl. Acad. Sci. U. S. A. 102 2005 6379 6384
99. W.M. Brown, M. George Jr., and A.C. Wilson Rapid evolution of animal mitochondrial DNA Proc. Natl. Acad. Sci. U. S. A. 76 1979 1967 1971
100. L. Kenyon, and C.T. Moraes Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids Proc. Natl. Acad. Sci. U. S. A. 94 1997 9131 9135
101. A. Barrientos, S. Muller, R. Dey, J. Wienberg, and C.T. Moraes Cytochrome c oxidase assembly in primates is sensitive to small evolutionary variations in amino acid sequence Mol. Biol. Evol. 17 2000 1508 1519
102. T.R. Schmidt, W. Wu, M. Goodman, and L.I. Grossman Evolution of nuclear- and mitochondrial-encoded subunit interaction in cytochrome c oxidase Mol. Biol. Evol. 18 2001 563 569
103. D.C. Wallace Why do we still have a maternally inherited mitochondrial DNA? Insights from evolutionary medicine Annu. Rev. Biochem. 76 2007 781 821
104. I. Lee, A.R. Salomon, K. Yu, L. Samavati, P. Pecina, A. Pecinova, and M. Hüttemann Isolation of regulatory-competent, phosphorylated cytochrome c oxidase Methods Enzymol. 457 2009 193 210
105. F. Gnad, F. Forner, D.F. Zielinska, E. Birney, J. Gunawardena, and M. Mann Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria Mol. Cell. Proteomics 9 2010 2642 2653