Assembly of cytochrome c oxidase within the mitochondrion

Accounts of Chemical Research

Volumn 36, Issue 5, 2003, Pages 309-316

  Carr, Heather S ^a   Winge, Dennis R ^a  

^a UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ION; CYTOCHROME C OXIDASE; HEME; HEME A; MAGNESIUM ION; OLIGOMER; SODIUM ION; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; CYTOPLASM; ENZYME LOCALIZATION; ENZYME STRUCTURE; ENZYME SUBUNIT; ENZYME SYNTHESIS; ION TRANSPORT; MITOCHONDRION; NONHUMAN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REACTION ANALYSIS; STRUCTURE ANALYSIS;

ELECTRON TRANSPORT COMPLEX IV; MITOCHONDRIA; MODELS, MOLECULAR;

EID: 0038518286     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar0200807     Document Type: Article

References (63)

1. Iwata, S.; Ostermeier, C.; Ludwig, B.; Michel, H. Structure at 2.8 A of cytochrome c oxidase from Paracoccus denitrificans. Nature 1995, 376, 660-669.
2. Tsukihara, T.; Aoyama, H.; Yamashita, E.; Tomizaki, T.; Yamaguchi, H.; Shinzawa-Itoh, K.; Hakashima, R.; Yaono, R.; Yoshikawa, S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 1995, 269, 1069-1074.
3. Scorrano, L.; Ashiya, M.; Buttle, K.; Weiler, S.; Oakes, S. A.; Mannella, C. A.; Korsmeyer, S. J. A distinct pathway remodels mitochondrial cristas and mobilizes cytochrome c during apoptosis. Dev. Cell 2002, 2, 55-67.
4. Frey, T. G.; Mannella, C. A. The internal structure of mitochondria. Trends Biochem. Sci. 2000, 25, 319-324.
5. Mannella, C. A.; Pfeiffer, D. R.; Bradshaw, P. C.; Moraru, I. I.; Slepchenko, B.; Loew, L. M.; Hsieh, C.; Buttle, K.; Marko, M. Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications. IUBMB Life 2002, 52, 1-7.
6. Perotti, M. E.; Anderson, W. A.; Swift, H. Quantitative cytochemistry of the diaminobenzidine cytochrome oxidase reaction product in mitochondria of cardiac muscle and pancreas. J. Histochem. Cytochem. 1983, 31, 351-365.
7. Gibney, B. R.; Isogai, Y.; Rabanal, F.; Reddy, K. S.; Grosset, A. M.; Moser, C. C.; Dutton, P. L. Self-assembly of heme A and heme B in a designed four-helix bundle: Implications for a cytochrome c oxidase maquette. Biochemistry 2000, 39, 11041-11049.
8. Beinert, H. Crystals and structures of cytochrome c oxidases- the end of an arduous road. Chem. Biol. 1995, 2, 781-785.
9. Zhen, Y.; Hoganson, C. W.; Babcock, G. T.; Ferguson-Miller, S. Definition of the interaction domain for cytochrome c on cytochrome c oxidase. J. Biol. Chem. 1999, 274, 38032-38041.
10. Kirichenko, A.; Vygodina, T. V.; Mkrtchyan, H. M.; Konstantinov, A. A. Specific cation binding site in mammalian cytochrome oxidase. FEBS Lett. 1998, 423, 329-333.
11. Lee, A.; Kirichenko, A.; Vygodina, T.; Siletsky, S. A.; Das, T. K.; Rousseau, D. L.; Gennis, R.; Konstantinov, A. A. Ca2+-binding site in Rhodobacter sphaeroides cytochrome c oxidase. Biochemistry 2002, 41, 8886-8898.
12. Tzagoloff, A.; Dieckmann, C. L. PET genes of Saccharomyces cerevisiae. Microbiol. Rev. 1990, 54, 211-225.
13. Tzagoloff, A.; Capitanio, N.; Nobrega, M. P.; Gatti, D. Cytochrome oxidase assembly in yeast requires the product of COX11, a homologue of the P. denitrificans protein encoded by ORF3. EMBO J. 1990, 9, 2759-2764.
14. Gavin, A.-C.; Bosche, M.; Krause, R.; Grandi, P.; Marzioch, M., et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415, 141-147.
15. Glerum, D. M.; Tzagoloff, A. Submitochondrial distributions and stabilities of subunits 4, 5, and 6 of yeast cytochrome oxidase in assembly defective mutants. FEBS Lett. 1997, 412, 410-414.
16. Green-Willms, N. S.; Butler, C. A.; Dunstan, H. M.; Fox, T. D. Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2. J. Biol. Chem. 2001, 276, 6392-6397.
17. Fox, T. D. Translational control of endogenous and recoded nuclear genes in yeast mitochondria: regulation and membrane targeting. Experientia 1996, 52, 1130-1135.
18. Hell, K.; Herrmann, J. M.; Pratje, E.; Neupert, W.; Stuart, R. A. Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 2250-2255.
19. Preuss, M.; Leonhard, K.; Hell, K.; Stuart, R. A.; Neupert, W.: Herrmann, J. M. Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae. J. Cell. Biol. 2001, 153, 1085-1096.
20. Hell, K.; Tzagoloff, A.; Neupert, W.; Stuart, R. A. Identification of Cox20p, a novel protein involved in the maturation and assembly of cytochrome oxidase subunit 2. J. Biol. Chem. 2000, 275, 4571-4578.
21. Saracco, S. A.; Fox, T. D. Cox18p is required for export of the mitochondrially encoded Saccharomyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane. Mol. Biol. Cell 2002, 773, 1122-1131.
22. Nijtmans, L. G.; Taanman, J. W.; Muijsers, A. O.; Speijer, D.; Van den Bogert, C. Assembly of cytochrome c oxidase in cultured human cells. Eur. J. Biochem. 1998, 254, 389-394.
23. Lemaire, C.; Robineau, S.; Netter, P. Molecular and biochemical analysis of Saccharomyces cerevisiae cox1 mutants. Curr. Genet. 1998, 34, 138-145.
24. Stevens, B. Mitochondrial Structure; Cold Spring Harbor Laboratory, 1981.
25. Tzagoloff, A.; Nobrega, M.; Gorman, N.; Sinclair, P. On the functions of the yeast COX10 and COX11 gene products. Biochem. Mol. Biol. Int. 1993, 31, 593-598.
26. Barros, M. H.; Tzagoloff, A. Regulation of the heme A biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett. 2002, 516, 119-123.
27. Brown, K. R.; Allan, B. M.; Do, P.; Hegg, E. L. Identification of Novel Hemes Generated by Heme A Synthase: Evidence for Two Successive Monooxygenase Reactions. Biochemistry 2002, 41, 10906-10913.
28. Barros, M. H.; Nobrega, F. G.; Tzagoloff, A. Mitochondrial ferredoxin is required for heme A synthesis in Saccharomyces cerevisiae. J. Biol. Chem. 2002, 277, 9997-10002.
29. Barros, M. H.; Carlson, C. G.; Glerum, D. M.; Tzagoloff, A. Involvement of mitochondrial ferredoxin and Cox15p in hydroxylation of heme O. FEBS Lett. 2001, 492, 133-138.
30. Glerum, D. M.; Shtanko, A.; Tzagoloff, A. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J. Biol. Chem. 1996, 271, 14504-14509.
31. Beers, J.; Glerum, D. M.; Tzagoloff, A. Purification, characterization, and localization of yeast Cox17p, a mitochondrial copper shuttle. J. Biol. Chem. 1997, 272, 33191-33196.
32. Heaton, D.; Nittis, T.; Srinivasan, C.; Winge, D. R. Mutational analysis of the mitochondrial copper metallochaperone Cox17. J. Biol. Chem. 2000, 275, 37582-37587.
33. Heaton, D. N.; George, G. N.; Garrison, G.; Winge, D. R. The mitochondrial copper metallochaperone Cox17 exists as an oligomeric polycopper complex. Biochemistry 2001, 40, 743-751.
34. Dance, I. G. The structural chemistry of metal thiolate complexes. Polyhedron 1986, 5, 1037-1104.
35. Sturtz, L. A.; Diekert, K.; Jensen, L. T.; Lill, R.; Culotta, V. C. A fraction of yeast Cu,Zn- superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. J. Biol. Chem. 2001, 276, 38084-38089.
36. Rae, R. D.; Schmidt, P. J.; Pufahl, R. A.; Culotta, V. C.; O'Halloran, T. V. Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase. Science 1999, 284, 805-807.
37. Nobrega, M. P.; Bandeira, S. C. B.; Beers, J.; Tzagoloff, A. Characterization of COX19, a widely distributed gene required for expression of mitochondrial cytochrome c oxidase. J. Biol. Chem. 2002, 277, 40206-40211.
38. Glerum, D. M.; Shtanko, A.; Tzagoloff, A. SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J. Biol. Chem. 1996, 271, 20531-20535.
39. Buchwald, P.; Krummeck, G.; Rodel, G. Immunological identificationn of yeast Sco1 protein as a component of the inner mitochondrial membrane. Mol. Gen. Genet. 1991, 229, 413-420.
40. Beers, J.; Glerum, D. M.; Tzagoloff, A. Purification and characterization of yeast Sco1p, a mitochondrial copper protein. J. Biol. Chem. 2002, 277, 22185-22190.
41. Schulze, M.; Rodel, G. SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II. Mol. Gen. Genet. 1988, 211, 492-498.
42. Krummeck, G.; Rödel, G. Yeast SCO1 protein is required for a post-translational step in the accumulation of mitochondrial cytochrome c oxidase subunits I and II. Curr. Genet. 1990, 18, 13-15.
43. Lode, A.; Paret, C.; Rodel, G. Molecular characterization of Saccharomyces cerevisiae Sco2p reveals a high degree of redundancy with Sco1p. Yeast 2002, 19, 909-922.
44. Nittis, T.; George, G. N.; Winge, D. R. Yeast Sco1, a protein essential for cytochrome c oxidase function is a Cu(I)-binding protein. J. Biol. Chem. 2001, 276, 42520-42526.
45. Rentzsch, N.; Krummeck-WeiB, G.; Hofer, A.; Bartuschka, A.; Ostermann, K.; Rodel, G. Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr. Genet. 1999, 35, 103-108.
46. Papadopolou, L. C.; Sue, C. M.; Davidson, M. M.; Tanji, K.; Nishion, I.; Sadlock, J. E., et al. Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat. Genet. 1999, 23, 333-337.
47. Valnot, I.; Osmond, S.; Gigarel, N.; Mehaye, B.; Amiel, J.; Ccormier-Daire, V.; Munnich, A.; Bonnefont, J.-P.; Rustin, P.; Rotig, A. Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am. J. Hum. Genet. 2000, 67, 1104-1109.
48. Jaksch, M.; Ogilvie, I.; Yao, J.; Kortenhaus, G.; Bresser, H.-G.; Gerbitz, K.-D.; Shoubridge, E. A. Mutations in SCO2 are associated with a distinct form of hypertrophic cardiomyopathy and cytochrome c oxidase deficiency. Hum. Mol. Genet. 2000, 9, 795-801.
49. Lode, A.; Kuschel, M.; Paret, C.; Rodel, G. Mitochondrial copper metabolism in yeast: interaction between Sco1p and Cox2p. FEBS Lett. 2000, 448, 1-6.
50. Hirotsu, S.; Abe, Y.; Okada, K.; Nagahara, N.; Hori, H.; Nishino, T.; Hakoshima, T. Crystal structure of a multifunctional 2-Cys peroxiredoxin heme-binding protein 23 kDa/proliferation-associated gene product. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 12333-12338.
51. Chinenov, Y. V. Cytochrome c oxidase assembly factors with a thioredoxin fold are conserved among prokaryotes and eukaryotes. J. Mol. Med. 2000, 78, 2399-242.
52. B and magnesium centers of cytochrome c oxidase. J. Biol. Chem. 2000, 275, 619-623.
53. Carr, H. S.; George, G. N.; Winge, D. R. Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I) binding protein. J. Biol. Chem. 2002, 277, 31237-31242.
54. Pickering, I. J.; George, G. N.; Dameron, C. T.; Kurz, B.; Winge, D. R.; Dance, I. G. X-ray absoption spectroscopy of cuprous-thiolate clusters in proteins and model systems. J. Am. Chem. Soc. 1993, 115, 9498-9505.
55. Saveanu, C.; Fromont-Racine, M.; Harington, A.; Ricard, F.; Namane, A.; Jacquier, A. Identification of 12 new yeast mitochondrial ribosomal proteins including 6 that have no prokaryotic homologues. J. Biol. Chem. 2001, 276, 15861-15867.
56. Lamb, A. L.; Torres, A. S.; O'Halloran, T. V.; Rosenzweig, A. C. Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat. Struct. Biol. 2001, 9, 751-755.
57. Das, T. K.; Pecoraro, C.; Tomson, F. L.; Gennis, R. B.; Rousseau, D. L. The post-translational modification in cytochrome c oxidase is required to establish a functional environment of the catalytic site. Biochemistry 1998, 37, 14471-14476.
58. Buse, G.; Soulimane, T.; Dewor, M.; Meyer, H. E.; Bluggel, M. Evidence for a copper-coordinated histidine-tyrosine cross-link in the active site of cytochrome oxidase. Protein Sci. 1999, 8, 985-990.
59. Pinakoulaki, E.; Pfitzner, U.; Ludwig, B.; Constantinos Varotsis, C. The role of the cross-link His-Tyr in the functional properties of the binuclear center in cytochrome c oxidase. J. Biol. Chem. 2002, 277, 13563-13568.
60. Cruciat, C. M.; Brunner, S.; Baumann, F.; Neupert, W.; Stuart, R. A. The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 2000, 275, 18093-18098.
61. Zhang, M.; Mileeykovskaya, E.; Dowhan, W. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 2002, 277, 43553-43556.
62. Sedlak, E.; Robinson, N. C. Phospholipase A(2) digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure. Biochemistry 1999, 38, 14966-14972.
63. Musatov, A.; Robinson, N. C. Cholate-induced dimerization of detergent- or phospholipid-solubilized bovine cytochrome c oxidase. Biochemistry 2002, 41, 4371-4376.