Yeast cytochrome c oxidase: A model system to study mitochondrial forms of the haem-copper oxidase superfamily

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 4, 2012, Pages 620-628

  Maréchal, Amandine ^a   Meunier, Brigitte ^b   Lee, David ^a   Orengo, Christine ^a   Rich, Peter R ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

Author keywords

Complex IV; Cytochrome c oxidase; Keywords; Mitochondria; Mutants; Supernumerary subunits; Yeast

Indexed keywords

COPPER COMPLEX; CYTOCHROME C OXIDASE; HEME;

COW; ENZYME STRUCTURE; ENZYME SUBUNIT; FUNGAL GENETICS; GENE MUTATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; REVIEW; YEAST;

ANIMALS; CATTLE; ELECTRON TRANSPORT COMPLEX IV; HEME; MITOCHONDRIA; MODELS, MOLECULAR; MUTATION; OXIDOREDUCTASES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

BOVINAE;

EID: 84857914883     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.08.011     Document Type: Review

References (73)

1. P.R. Rich, and A. Maréchal The mitochondrial respiratory chain Essays Biochem. 47 2010 1 23
2. 2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria J. Biol. Chem. 257 1982 13028 13033
3. M. Wikström Proton pump coupled to cytochrome c oxidase in mitochondria Nature 266 1977 271 273
4. V.R.I. Kaila, M.I. Verkhovsky, and M. Wikström Proton-coupled electron transfer in cytochrome oxidase Chem. Rev. 110 2010 7062 7081
5. P. Brzezinski, and R.B. Gennis Cytochrome c oxidase: exciting progress and remaining mysteries J. Bioenerg. Biomembr. 40 2008 521 531
6. J.P. Hosler, S. Ferguson-Miller, and D.A. Mills Energy transduction: proton transfer through the respiratory complexes Annu. Rev. Biochem. 75 2006 165 187
7. B. Kadenbach, J. Jarausch, R. Hartmann, and P. Merle Separation of mammalian cytochrome c oxidase into 13 polypeptides by a sodium dodecylsulfate-gel electrophoretic procedure Analytical Biochemistry 129 1983 517 521
8. S. Iwata, C. Ostermeier, B. Ludwig, and H. Michel Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans Nature 376 1995 660 669
9. M. Svensson-Ek, J. Abramson, G. Larsson, S. Törnroth, P. Brzezinski, and S. Iwata The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides J. Mol. Biol. 321 2002 329 339
10. J. Abramson, S. Riistama, G. Larrson, A. Jasaitis, M. Svensson-Ek, L. Laakkonen, A. Puustinen, S. Iwata, and M. Wikström The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site Nat. Struct. Biol. 7 2000 910 917
11. 3-cytochrome c oxidase from Thermus thermophilus EMBO J. 19 2000 1766 1776
12. 3 cytochrome oxidase provides insights into proton pumping Science 329 2010 327 330
13. 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 Å Science 272 1996 1136 1144
14. M.M. Pereira, M. Santana, and M. Teixeira A novel scenario for the evolution of haem-copper oxygen reductases Biochim. Biophys. Acta Bioenerg. 1505 2001 185 208
15. D. Zaslavsky, and R. Gennis Proton pumping by cytochrome oxidase: progress, problems and postulates Biochim. Biophys. Acta 1458 2000 164 179
16. K. Shimokata, Y. Katayama, H. Murayama, M. Suematsu, T. Tsukihara, K. Muramoto, H. Aoyama, S. Yoshikawa, and H. Shimada The proton pumping pathway of bovine heart cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 104 2007 4200 4205
17. H.-M. Lee, T.K. Das, D.L. Rousseau, D. Mills, S. Ferguson-Miller, and R.B. Gennis Mutations in the putative H-channel in the cytochrome c oxidase from Rhodobacter sphaeroides show that this channel is not important for proton conduction but reveal modulation of the properties of heme a Biochemistry 39 2000 2989 2996
18. P.R. Rich Towards an understanding of the chemistry of oxygen reduction and proton translocation in the iron-copper respiratory oxidases Aust. J. Plant. Physiol. 22 1995 479 486
19. K. Faxén, G. Gilderson, P. Ädelroth, and P. Brzezinski A mechanistic principle for proton pumping by cytochrome c oxidase Nature 437 2005 286 289
20. J. Das, S.T. Miller, and D.L. Stern Comparisons 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
21. G. Anthony, A. Stroh, F. Lottspeich, and B. Kadenbach Different isozymes of cytochrome c oxidase are expressed in bovine smooth muscle and skeletal or heart muscle FEBS Lett. 277 1990 97 100
22. 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
23. G. Anthony, A. Reimann, and B. Kadenbach Tissue-specific regulation of bovine heart cytochrome-c oxidase activity by ADP via interaction with subunit VIa Proc. Natl. Acad. Sci. U. S. A. 90 1993 1652 1656
24. - stoichiometry of cytochrome c oxidase from bovine heart by intramitochondrial ATP/ADP ratios FEBS Lett. 382 1996 121 124
25. B. Ludwig, E. Bender, S. Arnold, M. Hüttemann, I. Lee, and B. Kadenbach Cytochrome c oxidase and the regulation of oxidative phosphorylation Chem. Biochem. 2 2001 392 403
26. A.M.J. Beauchemin, B. Gottlieb, L.K. Beitel, Y.A. Elhaji, L. Pinsky, and M.A. Trifiro 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
27. K.A. Lipinski, A. Kania-Golik, and P. Golik Maintenance and expression of the S. cerevisiae mitochondrial genome - from genetics to evolution and systems biology Biochim. Biophys. Acta 1797 2010 1088 1098
28. S. Naithani, S.A. Saracco, C.A. Butler, and T.D. Fox Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae Mol. Biol. Cell 14 2003 324 333
29. W. Neupert, and J.M. Herrmann Translocation of proteins into mitochondria Annu. Rev. Biochem. 76 2007 723 749
30. H. Schägger, and K. Pfeiffer Supercomplexes in the respiratory chains of yeast and mammalian mitochondria EMBO J. 19 2000 1773 1783
31. 1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria J. Biol. Chem. 275 2000 18093 18098
32. 1-cytochrome oxidase supercomplex and its association with the TIM23 machinery J. Biol. Chem. 283 2008 6677 8666
33. 1-COX supercomplex and the TIM23 machinery Mol. Biol. Cell 19 2008 3934 3943
34. A. Tzagoloff, and C.L. Dieckmann PET genes of Saccharomyces cerevisiae Microbiol. Rev. 54 1990 211 225
35. H.J. Pel, A. Tzagoloff, and L.A. Grivell The identification of 18 nuclear genes required for the expression of the yeast mitochondrial gene encoding cytochrome c oxidase subunit 1 Curr. Genet. 21 1992 139 146
36. J.M. Herrmann, and S. Funes Biogenesis of cytochrome oxidase - sophisticated assembly lines in the mitochondrial inner membrane Gene 354 2005 43 52
37. 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
38. C. Ugalde, M.J.H. Coenen, M.H. Farhoud, S. Gilinsky, W.J.H. Koopman, L.P. van den Heuvel, J.A.M. Smeitink, and L.G.J. Nijtmans New perspectives on the assembly process of mitochondrial respiratory chain complex cytochrome c oxidase Mitochondrion 2 2002 117 128
39. T. Langer AAA proteases: cellular machines for degrading membrane proteins Trends Biochem. Sci. 25 2000 247 251
40. T. Tatsuta, and T. Langer AAA proteases in mitochondria: diverse functions of membrane-bound proteolytic machines Res. Microbiol. 120 2009 711 717
41. O. Khalimonchuk, M. Bestwick, B. Meunier, T.C. Watts, and D.R. Winge Formation of the redox cofactor centers during Cox1 maturation in yeast cytochrome oxidase Mol. Cell. Biol. 30 2010 1004 1017
42. O. Khalimonchuk, A. Bird, and D.R. Winge Evidence for pro-oxidant intermediate in the assembly of cytochrome oxidase J. Biol. Chem. 282 2007 17442 17449
43. F. Fontanesi, I.C. Soto, and A. Barrientos Cytochrome c oxidase biogenesis: new levels of regulation IUBMB Life 60 2008 557 568
44. D.U. Mick, T.D. Fox, and P. Rehling Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation Nat. Rev. Mol. Cell Biol. 12 2011 14 20
45. 3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I J. Bioenerg. Biomembr. 30 1998 89 97
46. R.A. Capaldi, D. González-Halphen, and S. Takamiya Sequence homologies and structural similarities between the polypeptides of yeast and beef heart cytochrome c oxidase FEBS Lett. 207 1986 11 17
47. R.O. Poyton, and J.E. McEwen Crosstalk between nuclear and mitochondrial genomes Annu. Rev. Biochem. 65 1996 563 607
48. 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
49. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
50. T. Tsukihara, K. Shimokata, Y. Katayama, H. Shimada, K. Muramoto, H. Aoyama, M. Mochizuki, K. Shinozawa-Itoh, E. Yamashita, M. Yao, Y. Ishimura, and S. Yoshikawa 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
51. K. Katoh, K. Misawa, K. Kuma, and T. Miyata MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Nucleic Acids Res. 30 2002 3059 3066
52. The UnitProt Consortium Ongoing and future developments at the Universal Protein Resource Nucleic Acids Res. 39 2011 D214 D219
53. J. Söding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 2005 W244 W248
54. K. Bryson, L.J. McGuffin, R.L. Marsden, J.J. Ward, J.S. Sodhi, and D.T. Jones Protein structure prediction servers at University College London Nucleic Acids Res. 33 2005 W36 W38
55. P.V. Burke, and R.O. Poyton Structure/function of oxygen-regulated isoforms in cytochrome c oxidase J. Exp. Bot. 201 1998 1163 1175
56. U. Pfitzner, K. Hoffmeier, A. Harenga, A. Kannt, H. Michel, E. Bamberg, O.-M.H. Richter, and B. Ludwig Tracing the D-pathway in reconstituted site-directed mutants of cytochome c oxidase from Paracoccus denitrificans Biochemistry 39 2000 6756 6762
57. 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
58. M. Hüttemann, B. Kadenbach, and L.I. Grossman Mammalian subunit IV isoforms of cytochrome c oxidase Gene 267 2001 111 123
59. P.V. Burke, D.C. Raitt, L.A. Allen, E.A. Kellog, and R.O. Poyton Effects of oxygen concentration on the expression of cytochrome c and cytochrome c oxidase genes in yeast J. Biol. Chem. 272 1997 14705 14712
60. L.A. Allen, X.-J. Zhao, W. Caughey, and R.O. Poyton Isoforms of yeast cytochrome c oxidase subunit V affect the binuclear reaction center and alter the kinetics of interaction with the isoforms of yeast cytochrome c J. Biol. Chem. 270 1995 110 118
61. S.D. Power, M.A. Lochrie, K.A. Sevarino, T.E. Patterson, and R.O. Poyton The nuclear-coded subunits of yeast cytochrome c oxidase. I. Fractionation of the holoenzyme into chemically pure polypeptides and the identification of two new subunits using solvent extraction and reversed phase high performance liquid chromatography J. Biol. Chem. 259 1984 6564 6570
62. J.-W. Taanman, and R.A. Capaldi Purification of yeast cytochrome c oxidase with a subunit composition resembling the mammalian enzyme J. Biol. Chem. 267 1992 22481 22485
63. B.M. Geier, H. Schägger, C. Ortwein, T.A. Link, W.R. Hagen, U. Brandt, and G. von Jagow Kinetic properties and ligand binding of the eleven subunit cytochrome c oxidase from Saccharomyces cerevisiae isolated with a novel large scale purification method Eur. J. Biochem. 227 1995 296 302
64. B. Meunier, P. Lemarre, and A.M. Colson Genetic screening in Saccharomyces cerevisiae for large numbers of mitochondrial point mutations which affect structure and function of catalytic subunits of cytochrome-c oxidase Eur. J. Biochem. 213 1993 129 135
65. B. Meunier, C. Ortwein, U. Brandt, and P.R. Rich Effect of mutation of residue I67 in yeast cytochrome c oxidase on redox-linked protonation processes Biochem. J. 330 1998 1197 1200
66. C. Ortwein, T.A. Link, B. Meunier, A.-M. Colson, P.R. Rich, and U. Brandt Structural and functional analysis of deficient mutants in subunit I of cytochrome c oxidase from Saccharomyces cerevisiae Biochim. Biophys. Acta 1321 1997 79 92
67. B. Meunier, and P.R. Rich Second-site reversion analysis is not a reliable method to determine distance in membrane proteins: an assessment using mutations in yeast cytochrome c oxidase subunits I and II J. Mol. Biol. 283 1998 727 730
68. N. Bonnefoy, and T.D. Fox Genetic transformation of Saccharomyces cerevisiae mitochondria Methods Cell Biol. 65 2001 381 396
69. B. Meunier, and J.-W. Taanman Mutations of cytochrome c oxidase subunits 1 and 3 in Saccharomyces cerevisiae: assembly defect and compensation Biochim. Biophys. Acta 1554 2002 101 107
70. D.A. Varlamov, A.P. Kudin, S. Vielhaber, R. Schröder, R. Sassen, A. Becker, D. Kunz, K. Haug, J. Rebstock, A. Heils, C.E. Elger, and W.S. Kunz Metabolic consequences of a novel missense mutation of the mtDNA CO I gene Hum. Mol. Genet. 11 2002 1 9
71. B. Meunier Site-direct mutations in the mitochondrially-encoded subunits I and III of yeast cytochrome oxidase Biochem. J. 354 2001 407 412
72. S. Bröker, B. Meunier, P.R. Rich, N. Gattermann, and G. Hofhaus MtDNA mutations associated with sideroblastic anaemia cause a defect of mitochondrial cytochrome c oxidase Eur. J. Biochem. 258 1998 132 138
73. M. Bratton, D. Mills, C.K. Castleden, J. Hosler, and B. Meunier Disease-related mutations in cytochrome c oxidase studied in yeast and bacterial models Eur. J. Biochem. 270 2003 1 9