Comparison of diverse protein sequences of the nuclear-encoded subunits of cytochrome c oxidase suggests conservation of structure underlies evolving functional sites

Molecular Biology and Evolution

Volumn 21, Issue 8, 2004, Pages 1572-1582

  Das, Jayatri ^a   Miller, Stephen T ^a   Stern, David L ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Cytochrome c oxidase; Evolution; Mitochondria; Nuclear encoded; Structure

Indexed keywords

CYTOCHROME C OXIDASE; HOLOENZYME;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME SUBUNIT; GENE MAPPING; GENETIC CONSERVATION; GENETIC VARIABILITY; MOLECULAR STABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT; YEAST;

ANIMALS; CATALYTIC DOMAIN; CATTLE; ELECTRON TRANSPORT COMPLEX IV; MITOCHONDRIA; MODELS, MOLECULAR; PLANTS; YEASTS;

ANIMALIA; BOVINAE;

EID: 3242748398     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh161     Document Type: Article

References (50)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Andersson, S. G., 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. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-140.
3. Anthony, G., A. Reimann, and B. Kadenbach. 1993. Tissue-specific regulation of bovine heart cytochrome-c oxidase activity by ADP via interaction with subunit VIa. Proc. Natl. Acad. Sci. USA 90:1652-1656.
4. Arnold, S., F. Goglia, and B. Kadenbach. 1998. 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 252:325-330.
5. Beauchemin, A. M., B. Gottlieb, L. K. Beitel, Y. A. Elhaji, L. Pinsky, and M. A. Trifiro. 2001. Cytochrome c oxidase subunit Vb interacts with human androgen receptor: a potential mechanism for neurotoxicity in spinobulbar muscular atrophy. Brain Res. Bull. 56:285-297.
6. Beauvoit, B., O. Bunoust, B. Guerin, and M. Rigoulet. 1999. ATP regulation of cytochrome oxidase in yeast mitochondria: role of subunit VIa. Eur. J. Biochem. 263:118-127.
7. Bender, E., and B. Kadenbach. 2000. The allosteric ATP-inhibition of cytochrome c oxidase activity is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett. 466:130-134.
8. Berg, O. G., and C. G. Kurland. 2000. Why mitochondrial genes are most often found in nuclei. Mol. Biol. Evol. 17:951-961.
9. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. The protein data bank. Nucleic Acids Res. 28:235-242.
10. Betts, M. J., and R. B. Russell. 2003. Amino acids properties and consequences of substitutions. Pp. 289-316 in M. R. Barnes, and I. C. Gray, eds. Bioinformatics for geneticists. Wiley, Chichester, UK.
11. Burke, P. V., D. C. Raitt, L. A. Allen, E. A. Kellogg, and R. O. Poyton. 1997. Effects of oxygen concentration on the expression of cytochrome c and cytochrome c oxidase genes in yeast. J. Biol. Chem. 272:14705-14712.
12. Capaldi, R. A. 1990. Structure and function of cytochrome c oxidase. Annu. Rev. Biochem. 59:569-596.
13. Capaldi, R. A., Y. Z. Zhang, R. Rizzuto, D. Sandona, G. Schiavo, and R. Bisson. 1990. The two oxygen-regulated subunits of cytochrome c oxidase in Dictyostelium discoideum derive from a common ancestor. FEBS Lett. 261:158-160.
14. DeLano, W. L. 2002. The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA, USA.
15. Edmands, S., and R. Burton. 1998. Variation in cytochrome-c oxidase activity is not maternally inherited in the copepod Tigriopus californicus. Heredity 80:668-674.
16. Ewart, G. D., Y. Z. Zhang, and R. A. Capaldi. 1991. Switching of bovine cytochrome c oxidase subunit VIa isoforms in skeletal muscle during development. FEBS Lett. 292:79-84.
17. Geier, B. M., H. Schagger, C. Ortwein, T. A. Link, W. R. Hagen, U. Brandt, and G. Von Jagow. 1995. 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: 296-302.
18. Goldberg, A., D. E. Wildman, T. R. Schmidt, M. Huttemann, M. Goodman, M. L. Weiss, and L. I. Grossman. 2003. Adaptive evolution of cytochrome c oxidase subunit VIII in anthropoid primates. Proc. Natl. Acad. Sci. USA 100:5873-5878.
19. Golding, G. B., and A. M. Dean. 1998. The structural basis of molecular adaptation. Mol. Biol. Evol. 15:355-369.
20. Hamanaka, S., K. Ohtsu, K. Kadowaki, M. Nakazono, and A. Hirai. 1999. Identification of cDNA encoding cytochrome c oxidase subunit 5c (COX5c) from rice: comparison of its expression with nuclear-encoded and mitochondrial- encoded COX genes. Genes Genet. Syst. 74:71-75.
21. Huttemann, M., S. Jaradat, and L. I. Grossman. 2003. Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb-the counterpart to testes-specific cytochrome c? Mol. Reprod. Dev. 66:8-16.
22. Huttemann, M., B. Kadenbach, and L. I. Grossman. 2001. Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267:111-123.
23. Jansch, L., V. Kruft, U. K. Schmitz, and H. P. Braun. 1996. New insights into the composition, molecular mass and stoichiometry of the protein complexes of plant mitochondria. Plant J. 9:357-368.
24. Kenyon, L., and C. T. Moraes. 1997. Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids. Proc. Natl. Acad. Sci. USA 94:9131-9135.
25. Kim, Y., E. D. Davari, V. Sevala, and K. G. Davey. 1999. Functional binding of a vertebrate hormone, L-3,5,3′-triiodothyronine (T3), on insect follicle cell membranes. Insect Biochem. Mol. Biol. 29:943-950.
26. Lang, B. F., G. Burger, C. J. O'Kelly, R. Cedergren, G. B. Golding, C. Lemieux, D. Sankoff, M. Turmel, and M. W. Gray. 1997. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493-497.
27. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26:283-291.
28. Ludwig, B., E. Bender, S. Arnold, M. Huttemann, I. Lee, and B. Kadenbach. 2001. Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chem. Biochem. 2:392-403.
29. Matthews, J. M., and M. Sunde. 2002. Zinc fingers-folds for many occasions. IUBMB Life 54:351-355.
30. Napiwotzki, J., K. Shinzawa-Itoh, S. Yoshikawa, and B. Kadenbach. 1997. ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol. Chem. 378:1013-1021.
31. Ohtsu, K., M. Nakazono, N. Tsutsumi, and A. Hirai. 2001. Characterization and expression of the genes for cytochrome c oxidase subunit VIb (COX6b) from rice and Arabidopsis thaliana. Gene 264:233-239.
32. Palmer, J. D., K. L. Adams, Y. Cho, C. L. Parkinson, Y. L. Qiu, and K. Song. 2000. Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc. Natl. Acad. Sci. USA 97:6960-6966.
33. Poyton, R. O., and J. E. McEwen. 1996. Crosstalk between nuclear and mitochondrial genomes. Annu. Rev. Biochem. 65:563-607.
34. Reimann, A., F. J. Huther, J. A. Berden, and B. Kadenbach. 1988. Anions induce conformational changes and influence the activity and photoaffinity-labelling by 8-azido-ATP of isolated cytochrome c oxidase. Biochem. J. 254:723-730.
35. Ruitenberg, M., A. Kannt, E. Bamberg, K. Fendler, and H. Michel. 2002. Reduction of cytochrome c oxidase by a second electron leads to proton translocation. Nature 417: 99-102.
36. Russell, R. B., and G. J. Barton. 1994. Structural features can be unconserved in proteins with similar folds: an analysis of side-chain to side-chain contacts secondary structure and accessibility. J. Mol. Biol. 244:332-350.
37. Sackton, T. B., R. A. Haney, and D. M. Rand. 2003. Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57:2315-2325.
38. Schiavo, G., and R. Bisson. 1989. Oxygen influences the subunit structure of cytochrome c oxidase in the slime mold Dictyostelium discoideum. J. Biol. Chem. 264:7129-7134.
39. Schmidt, T. R., M. Goodman, and L. I. Grossman. 1999. Molecular evolution of the COX7A gene family in primates. Mol. Biol. Evol. 16:619-626.
40. Schmidt, T. R., W. Wu, M. Goodman, and L. I. Grossman. 2001. Evolution of nuclear- and mitochondrial-encoded subunit interaction in cytochrome c oxidase. Mol. Biol. Evol. 18:563-569.
41. Schueler, O., and H. Margalit. 1995. Conservation of salt bridges in protein families. J. Mol. Biol. 248:125-135.
42. Szuplewski, S., and R. Terracol. 2001. The cyclope gene of Drosophila encodes a cytochrome c oxidase subunit VIc homolog. Genetics 158:1629-1643.
43. Taanman, J. W., P. Turina, and R. A. Capaldi. 1994. Regulation of cytochrome c oxidase by interaction of ATP at two binding sites, one on subunit VIa. Biochemistry 33:11833-11841.
44. Takayama, I., Y. Diago, S. M. Ward, K. M. Sanders, T. Yamanaka, and M. A. Fujino. 2001. Differential gene expression in the small intestines of wildtype and W/W-V mice. Neurogastroenterol. Motil. 13:163-168.
45. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
46. Tsukihara, T., H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa. 1996. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 angstrom. Science 272:1136-1144.
47. Tsukihara, T., K. Shimokata, Y. Katayama, et al. (12 co-authors). 2003. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. USA 100:15304-15309.
48. Welchen, E., R. L. Chan, and D. H. Gonzalez. 2002. Metabolic regulation of genes encoding cytochrome c and cytochrome c oxidase subunit Vb in Arabidopsis. Plant Cell Environ. 25:1605-1615.
49. Wheeler, D. E., and H. F. Nijhout. 2003. A perspective for understanding the modes of juvenile hormone action as a lipid signaling system. Bioessays 25:994-1001.
50. Yang, W. L., L. Iacono, W. M. Tang, and K. V. Chin. 1998. Novel function of the regulatory subunit of protein kinase A: regulation of cytochrome c oxidase activity and cytochrome c release. Biochemistry 37:14175-14180.