Nuclear Suppression of Mitochondrial Defects in Cells without the ND6 Subunit

REFERENCES

• Acin-Perez, R., M. P. Bayona-Bafaluy, M. Bueno, C. Machicado, P. Fernandez-Silva, A. Perez-Martos, J. Montoya, M. J. Lopez-Perez, J. Sancho, and J. A. Enriquez. 2003. An intragenic suppressor in the cytochrome c oxidase I gene of mouse mitochondrial DNA. Hum. Mol. Genet. 12:329–339.
   PubMedGoogle Scholar
• Bai, Y., and G. Attardi. 1998. The mtDNA-encoded ND6 subunit of mitochondrial NADH dehydrogenase is essential for the assembly of the membrane arm and the respiratory function of the enzyme. EMBO J. 17:4848–4858.
   PubMed Web of Science ®Google Scholar
• Bai, Y., P. Hajek, A. Chomyn, E. Chan, B. B. Seo, A. Matsuno-Yagi, T. Yagi, and G. Attardi. 2001. Lack of complex I activity in human cells carrying a mutation in mtDNA-encoded ND4 subunit is corrected by the Saccharomyces cerevisiae NADH-quinone oxidoreductase (NDI1) gene. J. Biol. Chem. 276:38808–38813.
   PubMedGoogle Scholar
• Bai, Y., P. Hu, J. S. Park, J. H. Deng, X. Song, A. Chomyn, T. Yagi, and G. Attardi. 2004. Genetic and functional analysis of mitochondrial DNA-encoded complex I genes. Ann. N. Y. Acad. Sci. 1011:272–283.
   PubMedGoogle Scholar
• Bai, Y., R. M. Shakeley, and G. Attardi. 2000. Tight control of respiration by NADH dehydrogenase ND5 subunit gene expression in mouse mitochondria. Mol. Cell. Biol. 20:805–815.
   PubMed Web of Science ®Google Scholar
• Birch-Machin, M. A., and D. M. Turnbull. 2001. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol. 65:97–117.
   PubMedGoogle Scholar
• Cardol, P., R. F. Matagne, and C. Remacle. 2002. Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas: implication for the structural organization of the enzyme. J. Mol. Biol. 319:1211–1221.
   PubMed Web of Science ®Google Scholar
• Chance, B., and G. R. Williams. 1955. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J. Biol. Chem. 217:383–393.
   PubMed Web of Science ®Google Scholar
• Chen, L. B. 1988. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol. 4:155–181.
   PubMedGoogle Scholar
• Chinnery, P. F., D. T. Brown, R. M. Andrews, R. Singh-Kler, P. Riordan-Eva, J. Lindley, D. A. Applegarth, D. M. Turnbull, and N. Howell. 2001. The mitochondrial ND6 gene is a hot spot for mutations that cause Leber's hereditary optic neuropathy. Brain 124:209–218.
   PubMed Web of Science ®Google Scholar
• Chomyn, A. 1996. In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol. 264:197–211.
   PubMedGoogle Scholar
• Chomyn, A., M. W. Cleeter, C. I. Ragan, M. Riley, R. F. Doolittle, and G. Attardi. 1986. URF6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase subunit. Science 234:614–618.
   PubMed Web of Science ®Google Scholar
• De Vries, D. D., L. N. Went, G. W. Bruyn, H. R. Scholte, R. M. Hofstra, P. A. Bolhuis, and B. A. van Oost. 1996. Genetic and biochemical impairment of mitochondrial complex I activity in a family with Leber hereditary optic neuropathy and hereditary spastic dystonia. Am. J. Hum. Genet. 58:703–711.
   PubMed Web of Science ®Google Scholar
• DiMauro, S., and E. A. Schon. 2001. Mitochondrial DNA mutations in human disease. Am. J. Med. Genet. 106:18–26.
   PubMed Web of Science ®Google Scholar
• El Meziane, A., S. K. Lehtinen, N. Hance, L. G. Nijtmans, D. Dunbar, I. J. Holt, and H. T. Jacobs. 1998. A tRNA suppressor mutation in human mitochondria. Nat. Genet. 18:350–353.
   PubMedGoogle Scholar
• Folley, L. S., and T. D. Fox. 1994. Reduced dosage of genes encoding ribosomal protein S18 suppresses a mitochondrial initiation codon mutation in Saccharomyces cerevisiae. Genetics 137:369–379.
   PubMedGoogle Scholar
• Friedrich, T., U. Weidner, U. Nehls, W. Fecke, R. Schneider, and H. Weiss. 1993. Attempts to define distinct parts of NADH:ubiquinone oxidoreductase (complex I). J. Bioenerg. Biomembr. 25:331–337.
   PubMedGoogle Scholar
• Grigorieff, N. 1999. Structure of the respiratory NADH:ubiquinone oxidoreductase (complex I). Curr. Opin. Struct. Biol. 9:476–483.
   PubMedGoogle Scholar
• Grigorieff, N. 1998. Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 A in ice. J. Mol. Biol. 277:1033–1046.
   PubMedGoogle Scholar
• Guenebaut, V., R. Vincentelli, D. Mills, H. Weiss, and K. R. Leonard. 1997. Three-dimensional structure of NADH-dehydrogenase from Neurospora crassa by electron microscopy and conical tilt reconstruction. J. Mol. Biol. 265:409–418.
   PubMedGoogle Scholar
• Hao, H., L. E. Morrison, and C. T. Moraes. 1999. Suppression of a mitochondrial tRNA gene mutation phenotype associated with changes in the nuclear background. Hum. Mol. Genet. 8:1117–1124.
   PubMedGoogle Scholar
• Hayashi, J., S. Ohta, A. Kikuchi, M. Takemitsu, Y. Goto, and I. Nonaka. 1991. Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc. Natl. Acad. Sci. USA 88:10614–10618.
   PubMed Web of Science ®Google Scholar
• Hirst, J., J. Carroll, I. M. Fearnley, R. J. Shannon, and J. E. Walker. 2003. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 1604:135–150.
   PubMed Web of Science ®Google Scholar
• Hofhaus, G., and G. Attardi. 1995. Efficient selection and characterization of mutants of a human cell line which are defective in mitochondrial DNA-encoded subunits of respiratory NADH dehydrogenase. Mol. Cell. Biol. 15:964–974.
   PubMed Web of Science ®Google Scholar
• Hofhaus, G., R. M. Shakeley, and G. Attardi. 1996. Use of polarography to detect respiration defects in cell cultures. Methods Enzymol. 264:476–483.
   PubMedGoogle Scholar
• Hofhaus, G., H. Weiss, and K. Leonard. 1991. Electron microscopic analysis of the peripheral and membrane parts of mitochondrial NADH dehydrogenase (complex I). J. Mol. Biol. 221:1027–1043.
   PubMedGoogle Scholar
• Howell, N., C. Bogolin, R. Jamieson, D. R. Marenda, and D. A. Mackey. 1998. mtDNA mutations that cause optic neuropathy: how do we know? Am. J. Hum. Genet. 62:196–202.
   PubMed Web of Science ®Google Scholar
• Howell, N., I. Kubacka, M. Xu, and D. A. McCullough. 1991. Leber hereditary optic neuropathy: involvement of the mitochondrial ND1 gene and evidence for an intragenic suppressor mutation. Am. J. Hum. Genet. 48:935–942.
   PubMed Web of Science ®Google Scholar
• Janssen, R., J. Smeitink, R. Smeets, and L. van Den Heuvel. 2002. CIA30 complex I assembly factor: a candidate for human complex I deficiency? Hum. Genet. 110:264–270.
   PubMed Web of Science ®Google Scholar
• Johns, D. R., M. J. Neufeld, and R. D. Park. 1992. An ND-6 mitochondrial DNA mutation associated with Leber hereditary optic neuropathy. Biochem. Biophys. Res. Commun. 187:1551–1557.
   PubMed Web of Science ®Google Scholar
• Jun, A. S., M. D. Brown, and D. C. Wallace. 1994. A mitochondrial DNA mutation at nucleotide pair 14459 of the NADH dehydrogenase subunit 6 gene associated with maternally inherited Leber hereditary optic neuropathy and dystonia. Proc. Natl. Acad. Sci. USA 91:6206–6210.
   PubMed Web of Science ®Google Scholar
• King, M. P., and G. Attardi. 1989. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246:500–503.
   PubMed Web of Science ®Google Scholar
• Kirby, D. M., A. Boneh, C. W. Chow, A. Ohtake, M. T. Ryan, D. Thyagarajan, and D. R. Thorburn. 2003. Low mutant load of mitochondrial DNA G13513A mutation can cause Leigh's disease. Ann. Neurol. 54:473–478.
   PubMed Web of Science ®Google Scholar
• Kuffner, R., A. Rohr, A. Schmiede, C. Krull, and U. Schulte. 1998. Involvement of two novel chaperones in the assembly of mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Mol. Biol. 283:409–417.
   PubMedGoogle Scholar
• Lenaz, G., R. Fato, A. Baracca, and M. L. Genova. 2004. Mitochondrial quinone reductases: complex I. Methods Enzymol. 382:3–20.
   PubMedGoogle Scholar
• Lin, D. T., and J. D. Lechleiter. 2002. Mitochondrial targeted cyclophilin D protects cells from cell death by peptidyl prolyl isomerization. J. Biol. Chem. 277:31134–31141.
   PubMedGoogle Scholar
• Nicholls, D. G. 2002. Mitochondrial function and dysfunction in the cell: its relevance to aging and aging-related disease. Int. J. Biochem. Cell. Biol. 34:1372–1381.
   PubMed Web of Science ®Google Scholar
• Nicholls, D. G. 2004. Mitochondrial membrane potential and aging. Aging Cell 3:35–40.
   PubMed Web of Science ®Google Scholar
• Robinson, B. H., R. Petrova-Benedict, J. R. Buncic, and D. C. Wallace. 1992. Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem. Med. Metab. Biol. 48:122–126.
   PubMedGoogle Scholar
• Schagger, H. 1995. Native electrophoresis for isolation of mitochondrial oxidative phosphorylation protein complexes. Methods Enzymol. 260:190–202.
   PubMedGoogle Scholar
• Seo, B. B., A. Matsuno-Yagi, and T. Yagi. 1999. Modulation of oxidative phosphorylation of human kidney 293 cells by transfection with the internal rotenone-insensitive NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1412:56–65.
   PubMedGoogle Scholar
• Solano, A., M. Roig, C. Vives-Bauza, J. Hernandez-Pena, E. Garcia-Arumi, A. Playan, M. J. Lopez-Perez, A. L. Andreu, and J. Montoya. 2003. Bilateral striatal necrosis associated with a novel mutation in the mitochondrial ND6 gene. Ann. Neurol. 54:527–530.
   PubMedGoogle Scholar
• Triepels, R. H., L. P. Van Den Heuvel, J. M. Trijbels, and J. A. Smeitink. 2001. Respiratory chain complex I deficiency. Am. J. Med. Genet. 106:37–45.
   PubMedGoogle Scholar
• Ugalde, C., R. J. Janssen, L. P. van den Heuvel, J. A. Smeitink, and L. G. Nijtmans. 2004. Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum. Mol. Genet. 13:659–667.
   PubMed Web of Science ®Google Scholar
• Ugalde, C., R. H. Triepels, M. J. Coenen, L. P. van den Heuvel, R. Smeets, J. Uusimaa, P. Briones, J. Campistol, K. Majamaa, J. A. Smeitink, and L. G. Nijtmans. 2003. Impaired complex I assembly in a Leigh syndrome patient with a novel missense mutation in the ND6 gene. Ann. Neurol. 54:665–669.
   PubMedGoogle Scholar
• Ugalde, C., R. Vogel, R. Huijbens, B. Van Den Heuvel, J. Smeitink, and L. Nijtmans. 2004. Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Hum. Mol. Genet. 13:2461–2472.
   PubMed Web of Science ®Google Scholar
• Vanden Heuvel, J. P., G. C. Clark, M. C. Kohn, A. M. Tritscher, W. F. Greenlee, G. W. Lucier, and D. A. Bell. 1994. Dioxin-responsive genes: examination of dose-response relationships using quantitative reverse transcriptase-polymerase chain reaction. Cancer Res. 54:62–68.
   PubMed Web of Science ®Google Scholar
• Villani, G., and G. Attardi. 2001. In vivo measurements of respiration control by cytochrome c oxidase and in situ analysis of oxidative phosphorylation. Methods Cell Biol. 65:119–131.
   PubMedGoogle Scholar
• Vogel, R., L. Nijtmans, C. Ugalde, L. van den Heuvel, and J. Smeitink. 2004. Complex I assembly: a puzzling problem. Curr. Opin. Neurol. 17:179–186.
   PubMedGoogle Scholar
• Walker, J. E. 1992. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q. Rev. Biophys. 25:253–324.
   PubMed Web of Science ®Google Scholar
• Wallace, D. C. 1997. Mitochondrial DNA in aging and disease. Sci. Am. 277:40–47.
   PubMed Web of Science ®Google Scholar
• Wallace, D. C., G. Singh, M. T. Lott, J. A. Hodge, T. G. Schurr, A. M. Lezza, L. J. Elsas II, and E. K. Nikoskelainen. 1988. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science 242:1427–1430.
   PubMed Web of Science ®Google Scholar
• Weiss, H., T. Friedrich, G. Hofhaus, and D. Preis. 1991. The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur. J. Biochem. 197:563–576.
   PubMedGoogle Scholar
• Wissinger, B., D. Besch, B. Baumann, S. Fauser, M. Christ-Adler, B. Jurklies, E. Zrenner, and B. Leo-Kottler. 1997. Mutation analysis of the ND6 gene in patients with Lebers hereditary optic neuropathy. Biochem. Biophys. Res. Commun. 234:511–515.
   PubMed Web of Science ®Google Scholar
• Yagi, T., B. B. Seo, S. Di Bernardo, E. Nakamaru-Ogiso, M. C. Kao, and A. Matsuno-Yagi. 2001. NADH dehydrogenases: from basic science to biomedicine. J. Bioenerg Biomembr. 33:233–242.
   PubMedGoogle Scholar