Protein-protein interfaces from cytochrome c oxidase i evolve faster than nonbinding surfaces, yet negative selection is the driving force

Genome Biology and Evolution

Volumn 6, Issue 11, 2014, Pages 3064-3076

  Aledo, Juan Carlos ^a   Valverde, Héctor ^a   Ruíz Camacho, Manuel ^a   Morilla, Ian ^a   López, Francisco Demetrio ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

COX; Cytonuclear coevolution; Evolutionary rates; Mitochondria; Oxidative phosphorylation; Protein evolution

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; PROTEIN BINDING; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BOVINE; CHEMISTRY; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATTLE; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; EVOLUTION, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN SUBUNITS; SELECTION, GENETIC;

EID: 84942318924     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu240     Document Type: Article

References (41)

1. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA. 2008. Respiratory active mitochondrial supercomplexes. Mol Cell 32: 529-539.
2. Alba MM, Castresana J. 2005. Inverse relationship between evolutionary rate and age of mammalian genes. Mol Biol Evol. 22:598-606.
3. Aledo JC. 2004. Glutamine breakdown in rapidly dividing cells: waste or investment? Bioessays 26:778-785.
4. Aledo JC, Li Y, de Magalhaes JP, Ruiz-Camacho M, Perez-Claros JA. 2011. Mitochondrially encoded methionine is inversely related to longevity in mammals. Aging Cell 10:198-207.
5. Aledo JC, Valverde H, Ruiz-Camacho M. 2012. Thermodynamic stability explains the differential evolutionary dynamics of cytochrome b and COX I in mammals. J Mol Evol. 74:69-80.
6. Althoff T, Mills DJ, Popot JL, Kuhlbrandt W. 2011. Arrangement of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. EMBO J. 30:4652-4664.
7. Azevedo L, et al. 2009. Epistatic interactions modulate the evolution of mammalian mitochondrial respiratory complex components. BMC Genomics 10:266.
8. Barrientos A, Muller S, Dey R, Wienberg J, Moraes CT. 2000. Cytochrome c oxidase assembly in primates is sensitive to small evolutionary variations in amino acid sequence. Mol Biol Evol. 17:1508-1519.
9. Castellana S, Vicario S, Saccone C. 2011. Evolutionary patterns of the mitochondrial genome in Metazoa: exploring the role of mutation and selection in mitochondrial protein coding genes. Genome Biol Evol. 3:1067-1079.
10. Castresana J, Lubben M, Saraste M, Higgins DG. 1994. Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13:2516-2525.
11. Das J, Miller ST, Stern DL. 2004. 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. 21:1572-1582.
12. de Magalhaes JP. 2005. Human disease-associated mitochondrial mutations fixed in nonhuman primates. J Mol Evol. 61:491-497.
13. Dudkina NV, Kudryashev M, Stahlberg H, Boekema EJ. 2011. Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc Natl Acad Sci U S A. 108: 15196-15200.
14. Edmands SB, Ronald S. 1999. Cytochrome c oxidase activity in interpopulation hybrids of a marine copepod: a test for nuclear-nuclear or nuclear-cytoplasmic coadaptation. Evolution 53:1972-1978.
15. Glaser F, et al. 2003. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19:163-164.
16. Guerois R, Nielsen JE, Serrano L. 2002. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol. 320:369-387.
17. Kenyon L, Moraes CT. 1997. Expanding the functional human mitochon-drial DNA database by the establishment of primate xenomitochon-drial cybrids. Proc Natl Acad Sci U S A. 94:9131-9135.
18. Little AG, Kocha KM, Lougheed SC, Moyes CD. 2010. Evolution of the nuclear-encoded cytochrome oxidase subunits in vertebrates. Physiol Genomics. 42:76-84.
19. Markovska B, Efremov GD, Vuk-pavlovic S, Benko B, Maricic S. 1975. Structural nonequivalence of the alpha- and beta-heme-pockets in human methemoglobin. A proton magnetic relaxation study in solution. Arch Biochem Biophys. 171:337-342.
20. Martin PD, Malkowski MG, Box J, Esmon CT, Edwards BF. 1997. New insights into the regulation of the blood clotting cascade derived from the X-ray crystal structure of bovine meizothrombin des F1 in complex with PPACK. Structure 5:1681-1693.
21. McKenzie M, Chiotis M, Pinkert CA, Trounce IA. 2003. Functional respiratory chain analyses in murid xenomitochondrial cybrids expose co-evolutionary constraints of cytochrome b and nuclear subunits of complex III. Mol Biol Evol. 20:1117-1124.
22. Michel H, Behr J, Harrenga A, Kannt A. 1998. Cytochrome c oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct. 27: 329-356.
23. Osada N, Akashi H. 2012. Mitochondrial-nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome C oxidase complex. Mol Biol Evol. 29:337-346.
24. Reedy CJ, Elvekrog MM, Gibney BR. 2008. Development of a heme protein structure-electrochemical function database. Nucleic Acids Res. 36:D307-D313.
25. Schagger H, Pfeiffer K. 2000. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19:1777-1783.
26. Schagger H, Pfeiffer K. 2001. The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. J Biol Chem. 276:37861-37867.
27. Schmidt TR, et al. 2005. Rapid electrostatic evolution at the binding site for cytochrome c on cytochrome c oxidase in anthropoid primates. Proc Natl Acad Sci U S A. 102:6379-6384.
28. Schmidt TR, Wu W, Goodman M, Grossman LI. 2001. Evolution of nuclear- and mitochondrial-encoded subunit interaction in cytochrome c oxidase. Mol Biol Evol. 18:563-569.
29. Schymkowitz J, et al. 2005. The FoldX web server: an online force field. Nucleic Acids Res. 33:W382-W388.
30. Soto IC, Fontanesi F, Liu J, Barrientos A. 2012. Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core. Biochim Biophys Acta. 1817:883-897.
31. Suen DF, Norris KL, Youle RJ. 2008. Mitochondrial dynamics and apoptosis. Genes Dev. 22:1577-1590.
32. Vishnoi A, Kryazhimskiy S, Bazykin GA, Hannenhalli S, Plotkin JB. 2010. Young proteins experience more variable selection pressures than old proteins. Genome Res. 20:1574-1581.
33. Willett CS, Burton RS. 2004. Evolution of interacting proteins in the mitochondrial electron transport system in a marine copepod. Mol Biol Evol. 21:443-453.
34. Winge DR. 2012. Sealing the mitochondrial respirasome. Mol Cell Biol. 32: 2647-2652.
35. Wong WS, Yang Z, Goldman N, Nielsen R. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041-1051.
36. Yang Z. 2000. Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. J Mol Evol. 51:423-432.
37. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
38. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 17:32-43.
39. Yang Z, Swanson WJ. 2002. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes. Mol Biol Evol. 19:49-57.
40. Yoshikawa S, et al. 1998. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280:1723-1729.
41. Yoshikawa S, Muramoto K, Shinzawa-Itoh K. 2011. Proton-pumping mechanism of cytochrome C oxidase. Annu Rev Biophys. 40:205-223.