Functional respiratory chain analyses in murid xenomitochondrial cybrids expose coevolutionary constraints of cytochrome b and nuclear subunits of complex III

Molecular Biology and Evolution

Volumn 20, Issue 7, 2003, Pages 1117-1124

  McKenzie, Matthew ^a   Chiotis, Maria ^a   Pinkert, Carl A ^a   Trounce, Ian A ^a  

^a NONE

Author keywords

Coevolution; Cybrid; Cytochrome b; mtDNA; Murids; Respiratory chain; Xenomitochondrial

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOPROTEIN; CELL NUCLEUS DNA; CYTOCHROME B; CYTOCHROME C OXIDASE; LACTIC ACID; MITOCHONDRIAL DNA; PROTEIN SUBUNIT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHIMERA; CONTROLLED STUDY; CORRELATION ANALYSIS; CYBRID; DNA SEQUENCE; ELECTRON TRANSPORT; ENZYME ANALYSIS; GENETIC ANALYSIS; GENETIC CODE; GENETIC VARIABILITY; MITOCHONDRIAL GENETICS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MOUSE; MURIDAE; MUS CAROLI; MUS DUNNI; MUS MUSCULUS DOMESTICUS; MUS PAHARI; MUS SPRETUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OTOMYS IRRORATUS; OXIDATION REDUCTION REACTION; PARSIMONY ANALYSIS; PROTEIN INTERACTION; RAT; RESPIRATORY CHAIN; SPECIES;

ANIMALIA; MURIDAE; MURINAE; MUS; MUS CAROLI; MUS DUNNI; MUS MUSCULUS; MUS MUSCULUS DOMESTICUS; MUS PAHARI; MUS SPRETUS; MUSCULUS; OTOMYS; OTOMYS IRRORATUS; RATTUS; RATTUS NORVEGICUS;

EID: 0038420036     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msg132     Document Type: Article

References (41)

1. Abramson, J., M. Svensson-Ek, B. Byrne, and S. Iwata. 2001. Structure of cytochrome c oxidase: a comparison of the bacterial and mitochondrial enzymes. Biochim. Biophys. Acta 1544:1-9.
2. Adkins, R. M., R. L. Honeycutt, and T. R. Disotell. 1996. Evolution of eutherian cytochrome c oxidase subunit II: heterogeneous rates of protein evolution and altered interaction with cytochrome c. Mol. Biol. Evol. 13:1393-1404.
3. Andrews, T. D., L. S. Jermiin, and S. Easteal. 1998. Accelerated evolution of cytochrome b in simian primates: adaptive evolution in concert with other mitochondrial proteins? J. Mol. Evol. 47:249-257.
4. Barrientos, A., S. Muller, R. Dey, J. Wienberg, and C. T. Moraes. 2000. Cytochrome c oxidase assembly in primates is sensitive to small evolutionary variations in amino acid sequence. Mol. Biol. Evol. 17:1508-1519.
5. Bibb, M. J., R. A. Van Etten, C. T. Wright, M. W. Walberg, and D. A. Clayton. 1981. Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167-180.
6. Blier, P. U., F. Dufresne, and R. S. Burton. 2001. Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17:400-406.
7. Bonhomme, F., and J.-L. Guenet. 1996. The laboratory mouse and its wild relatives. Pp. 1577-1596 in M. F. Lyon, S. Raston, and S. D. M. Brown, eds. Genetic variants and strains of the laboratory mouse. Oxford University Press, Oxford.
8. Cann, R. L., W. M. Brown, and A. C. Wilson. 1984. Polymorphic sites and the mechanism of evolution in human mitochondrial DNA. Genetics 106:479-499.
9. Carroll, J., R. J. Shannon, I. M. Fearnley, J. E. Walker, and J. Hirst. 2002. Definition of the nuclear encoded protein composition of bovine heart mitochondrial complex I: identification of two new subunits. J. Biol. Chem. 277:50311-50317.
10. Catzeflis, F. M., A. W. Dickerman, J. Michaux, and J. A. W. Kirsch. 1993. DNA hybridization and rodent phylogeny. Pp. 159-172 in F. S. Szalay, M. J. Novacek, and M. McKenna, eds. Mammal phylogeny. Vol. 2. Placentals. Springer-Verlag, New York.
11. o site catalysis. J. Biol. Chem. 277:3471-3476.
12. Dey, R., A. Barrientos, and C. T. Moraes. 2000. Functional constraints of nuclear-mitochondrial DNA interactions in xenomitochondrial rodent cell lines. J. Biol. Chem. 275:31520-31527.
13. Ducroz, J. F., V. Volobouev, and L. Granjon. 2001. An assessment of the systematics of arvicanthine rodents using mitochondrial DNA sequences: evolutionary and biogeographical implications. J. Mammal. Evol. 8:173-206.
14. Edmunds, S., and R. S. Burton. 1999. Cytochrome c oxidase activity in interpopulation hybrids of a marine copepod: a test for nuclear-cytoplasmic coadaptation. Evolution 53: 1972-1978.
15. Friedrich, T., A. Abelmann, B. Brors et al. (11 co-authors) 1998. Redox components and structure of the respiratory NADH: ubiquinone oxidoreductase (complex I). Biochim. Biophys. Acta 1365:215-219.
16. Gadaleta, G., G. Pepe, G. De Candia, C. Quagliariello, E. Sbisa, and C. Saccone. 1989. The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J. Mol. Evol. 28:497-516.
17. 1 complex. Science 281:64-71.
18. Janke, A., G. Feldmaier-Fuchs, W. K. Thomas, A. Von Haessler, and S. Pääbo. 1994. The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243-256.
19. Jansa, S. A., S. M. Goodman, and P. K. Tucker. 1999. Molecular phylogeny and biogeography of the native rodents of Madagascar (Muridae: Nesomyinae): a test of the single-origin hypothesis. Cladistics 15:253-270.
20. 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.
21. King, M. P., and G. Attardi. 1989. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246:500-503.
22. Lomax, M. I., D. Hewett-Emmett, T. L. Yang, and L. I. Grossman. 1992. Rapid evolution of the human gene for cytochrome c oxidase subunit IV. Proc. Natl. Acad. Sci. USA 89:5266-5270.
23. Lundrigan, B. L., S. A. Jansa, and P. K. Tucker. 2002. Phylogenetic relationships in the genus Mus, based on paternally, maternally, and biparentally inherited characters. Syst. Biol. 51:410-431.
24. Lundrigan, B. L., and P. K. Tucker. 1994. Tracing paternal ancestry in mice, using the Y-linked, sex-determining locus, Sry. Mol. Biol. Evol. 11:483-492.
25. Ma, D-P., A. Zharkikh, D. Graur, J. L. VendeBerg, and W-H. Li. 1993. Structure and evolution of opossum, guinea pig and porcupine cytochrome b genes. J. Mol. Evol. 36:327-334.
26. McKenzie, M., and I. Trounce. 2000. Expression of Rattus norvegicus mtDNA in Mus musculus cells results in multiple respiratory chain defects. J. Biol. Chem. 275:31514-31519.
27. Michaux, J., and F. Catzeflis. 2000. The bushlike radiation of muroid rodents is exemplified by the molecular phylogeny of the LCAT nuclear gene. Mol. Phylog. Evol. 17:280-293.
28. Michaux, J., A. Reyes, and F. Catzeflis. 2001. Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Mol. Biol. Evol. 18:2017-2031.
29. Morais, R., P. Desjardins, C. Turmel, and K. Zinkewich-Peotti. 1988. Development and characterization of continuous avian cell lines depleted of mitochondrial DNA. In Vitro Cell. Dev. Biol. 24:649-658.
30. Osheroff, N., S. H. Speck, E. Margoliash, E. C. I. Veerman, J. Wilms, B. W. Konig, and A. O. Muijsers. 1983. The reaction of primate cytochromes c with cytochrome oxidase. J. Biol. Chem. 258:5731-5738.
31. Rawson, P. D., and R. S. Burton. 2002. Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc. Natl. Acad. Sci. USA 99:12955-12958.
32. Saraste, M. 1999. Oxidative phosphorylation at the fin de siecle. Science 283:1488-1493.
33. Silver, L. M. 1995. Mouse genetics. Oxford University Press, Oxford.
34. Taylor, R. W., M. A. Birch-Machin, K. Bartlett, and D. M. Turnbull. 1993. Succinate-cytochrome c reductase: assessment of its value in the investigation of defects of the respiratory chain. Biochim. Biophys. Acta 1181:261-265.
35. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
36. Trounce I., Y. L. Kim, A. S. Jun, and D. C. Wallace. 1996. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts and transmitochondrial cell lines. Methods Enzymol. 264:484-509.
37. Trounce, I., J. Schmiedel, H. C. Yen, S. Hosseini, M. D. Brown, J. J. Olson, and D. C. Wallace. 2000. Cloning of neuronal mtDNA variants in cultured cells by synaptosome fusion with mtDNA-less cells. Nucleic Acids Res. 28:2164-2170.
38. 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 oxidised cytochrome c oxidase at 2.8 Å. Science 272:1136-1144.
39. Walker, J. E. 1992. The NADH: ubiquinone oxidoreductase (complex I) of respiratory chains. Q. Rev. Biophys. 25:253-324.
40. Wu, W., T. R. Schmidt, M. Goodman, and L. I. Grossman. 2000. Molecular evolution of cytochrome c oxidase subunit I in primates: Is there coevolution between mitochondrial and nuclear genomes? Mol. Phylogenet. Evol. 17:294-304.
41. Yamaoka, M., K. Isobe, H. Shitara, H. Yonekawa, S. Miyabayashi, and J. I. Hayashi. 2000. Complete repopulation of mouse mitochondrial DNA-less cells with rat mitochondrial DNA restores mitochondrial translation but not mitochondrial respiratory function. Genetics 155:301-307.