Molecular gene therapy: Overexpression of the alternative NADH dehydrogenase NDI1 restores overall physiology in a fungal model of respiratory complex I deficiency

Journal of Molecular Biology

Volumn 399, Issue 1, 2010, Pages 31-40

  Maas, Marc F P M ^a   Sellem, Carole H ^a   Krause, Frank ^b   Dencher, Norbert A ^b   Sainsard Chanet, Annie ^a,c  

^a CNRS   (France)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Alternative respiratory pathway; Life span; NADH:ubiquinone oxidoreductase; Podospora anserina; Respiratory supercomplexes

Indexed keywords

CYTOCHROME C OXIDASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME DEFICIENCY; FEMALE FERTILITY; GENE DISRUPTION; GENE OVEREXPRESSION; GENE THERAPY; LETHALITY; LIFESPAN; MITOCHONDRIAL RESPIRATION; MOLECULAR STABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOSPORA ANSERINA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; RESPIRATORY CHAIN; STEADY STATE; WILD TYPE;

PODOSPORA ANSERINA;

EID: 77953082947     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.04.015     Document Type: Article

References (47)

1. Kaul M.L.H. Male Sterility in Higher Plants 1988, Springer, Berlin, Germany.
2. DiMauro S., Bonilla E., Davidson M., Hirano M., Schon E.A. Mitochondria in neuromuscular disorders. Biochim. Biophys. Acta 1998, 1366:199-210.
3. Lorin S., Dufour E., Sainsard-Chanet A. Mitochondrial metabolism and aging in the filamentous fungus Podospora anserina. Biochim. Biophys. Acta 2006, 1757:604-610.
4. Cristina D., Cary M., Lunceford A., Clarke C., Kenyon C. A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans. PLoS Genet. 2009, 5:e1000450.
5. Copeland J.M., Cho J., Lo T., Hur J.H., Bahadorani S., Arabyan T., et al. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr. Biol. 2009, 19:1591-1598.
6. Dufour E., Boulay J., Rincheval V., Sainsard-Chanet A. A causal link between respiration and senescence in Podospora anserina. Proc. Natl Acad. Sci. USA 2000, 97:4138-4143.
7. Sellem C.H., Marsy S., Boivin A., Lemaire C., Sainsard-Chanet A. A mutation in the gene encoding cytochrome c1 leads to a decreased ROS content and to a long-lived phenotype in the filamentous fungus Podospora anserina. Fungal Genet. Biol. 2007, 44:648-658.
8. Maas M.F.P.M., Krause F., Dencher N.A., Sainsard-Chanet A. Respiratory complexes III and IV are not essential for the assembly/stability of complex I in fungi. J. Mol. Biol. 2009, 387:259-269.
9. Lorin S., Dufour E., Boulay J., Begel O., Marsy S., Sainsard-Chanet A. Overexpression of the alternative oxidase restores senescence and fertility in a long-lived respiration-deficient mutant of Podospora anserina. Mol. Microbiol. 2001, 42:1259-1267.
10. Sellem C.H., Bovier E., Lorin S., Sainsard-Chanet A. Mutations in two zinc cluster proteins activate alternative respiratory and gluconeogenic pathways and restore senescence in long-lived respiratory mutants of Podospora anserina. Genetics 2009, 182:69-78.
11. Maas M.F.P.M., Sellem C.H., Hoekstra R.F., Debets A.J.M., Sainsard-Chanet A. Integration of a pAL2-1 homologous mitochondrial plasmid associated with life span extension in Podospora anserina. Fungal Genet. Biol. 2007, 44:659-671.
12. Acín-Peréz R., Bayona-Bafaluy M.P., Fernández-Silva P., Moreno-Loshuertos R., Pérez-Martos A., Bruno C., et al. Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol. Cell 2004, 13:805-815.
13. Diaz F., Fukui H., Garcia S., Moraes C.T. Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol. Cell. Biol. 2006, 26:4872-4881.
14. Wittig I., Carrozzo R., Santorelli F.M., Schägger H. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta 2006, 1757:1066-1072.
15. Krause F. Oxidative phosphorylation supercomplexes in various eukaryotes: a paradigm change gains critical momentum. Complex I and Alternative NADH Dehydrogenases 2007, 179-213. Kerala, India, Transworld Research Network. M.I. González-Siso (Ed.).
16. Krause F., Scheckhuber C.Q., Werner A., Rexroth S., Reifschneider N.H., Dencher N.A., Osiewacz H.D. Supramolecular organization of cytochrome c oxidase- and alternative oxidase-dependent respiratory chains in the filamentous fungus Podospora anserina. J. Biol. Chem. 2004, 279:26453-26461.
17. Duarte M., Videira A. Effects of mitochondrial complex III disruption in the respiratory chain of Neurospora crassa. Mol. Microbiol. 2009, 72:246-258.
18. Duarte M., Pópulo H., Videira A., Friedrich T., Schulte U. Disruption of iron-sulphur cluster N2 from NADH:ubiquinone oxidoreductase by site-directed mutagenesis. Biochem. J. 2002, 364:833-839.
19. Espagne E., Lespinet O., Malagnac F., Da Silva C., Jaillon O., Porcel B.M., et al. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 2008, 9:R77.
20. El-Khoury R., Sellem C.H., Coppin E., Boivin A., Maas M.F.P.M, Debuchy R., Sainsard-Chanet A. Gene deletion and allelic replacement in the filamentous fungus Podospora anserina. Curr. Genet. 2008, 53:249-258.
21. Krause F. Detection and analysis of protein-protein interactions in organellar and prokaryotic proteomes by native gel electrophoresis: (membrane) protein complexes and supercomplexes. Electrophoresis 2006, 27:2759-2781.
22. Marques I., Dencher N.A., Videira A., Krause F. Supramolecular organization of the respiratory chain in Neurospora crassa mitochondria. Eukaryot. Cell 2007, 6:2391-2405.
23. Duarte M., Peters M., Schulte U., Videira A. The internal alternative NADH dehydrogenase of Neurospora crassa mitochondria. Biochem. J. 2003, 371:1005-1011.
24. Carneiro P., Duarte M., Videira A. The main external alternative NAD(P)H dehydrogenase of Neurospora crassa mitochondria. Biochim. Biophys. Acta 2004, 1608:45-52.
25. Bartosz G. Use of spectroscopic probes for detection of reactive oxygen species. Clin. Chim. Acta 2006, 368:53-76.
26. Duarte M., Videira A. Respiratory chain complex I is essential for sexual development in Neurospora and binding of iron sulfur clusters are required for enzyme assembly. Genetics 2000, 156:607-615.
27. Selker E.U. Premeiotic instability of repeated sequences in Neurospora crassa. Annu. Rev. Genet. 1990, 24:579-613.
28. Seo B.B., Kitajima-Ihara T., Chan E.K., Scheffler I.E., Matsuno-Yagi A., Yagi T. Molecular remedy of complex I defects: rotenone-insensitive internal NADH-quinone oxidoreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex I-deficient mammalian cells. Proc. Natl Acad. Sci. USA 1998, 95:9167-9171.
29. Seo B.B., Nakamaru-Ogiso E., Flotte T.R., Yagi T., Matsuno-Yagi A. A single-subunit NADH-quinone oxidoreductase renders resistance to mammalian nerve cells against complex I inhibition. Mol. Ther. 2002, 6:336-341.
30. Perales-Clemente E., Bayona-Bafaluy M.P., Pérez-Martos A., Barrientos A., Fernández-Silva P., Enriquez J.A. Restoration of electron transport without proton pumping in mammalian mitochondria. Proc. Natl Acad. Sci. USA 2008, 105:18735-18739.
31. Marella M., Seo B.B., Matsuno-Yagi A., Yagi T. Mechanism of cell death caused by complex I defects in a rat dopaminergic cell line. J. Biol. Chem. 2007, 282:24146-24156.
32. Seo B.B., Matsuno-Yagi A., Yagi T. 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 1999, 1412:56-65.
33. Seo B.B., Wang J., Flotte T.R., Yagi T., Matsuno-Yagi A. Use of the NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae as a possible cure for complex I defects in human cells. J. Biol. Chem. 2000, 275:37774-37778.
34. Bai Y., Hajek P., Chomyn A., Chan E., Seo B.B., Matsuno-Yagi A., et al. 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. 2001, 276:38808-38813.
35. Park J.S., Li Y.F., Bai Y. Yeast NDI1 improves oxidative phosphorylation capacity and increases protection against oxidative stress and cell death in cells carrying a Leber's hereditary optic neuropathy mutation. Biochim. Biophys. Acta 2007, 1772:533-542.
36. DeCorby A., Gaskova D., Sayles L.C., Lemire B.D. Expression of Ndi1p, an alternative NADH:ubiquinone oxidoreductase, increases mitochondrial membrane potential in a C. elegans model of mitochondrial disease. Biochim. Biophys. Acta 2007, 1767:1157-1163.
37. Seo B.B., Nakamaru-Ogiso E., Flotte T.R., Matsuno-Yagi A., Yagi T. In vivo complementation of complex I by the yeast NDI1 enzyme. J. Biol. Chem. 2006, 281:14250-14255.
38. Marella M., Seo B.B., Nakamaru-Osigo E., Greenamyre J.T., Matsuno-Yagi A., Yagi T. Protection by the NDI1 gene against neurodegeneration in a rotenone rat model of Parkinson's disease. PLoS ONE 2008, 3:e1433.
39. Zensen R., Husmann H., Schneider R., Peine T., Weiss H. De novo synthesis and desaturation of fatty acids at the mitochondrial acyl-carrier protein, a subunit of NADH:ubiquinone oxidoreductase in Neurospora crassa. FEBS Lett. 1992, 310:179-181.
40. Schneider R., Brors B., Massow M., Weiss H. Mitochondrial fatty acid synthesis: a relic of endosymbiontic origin and a specialized means for respiration. FEBS Lett. 1997, 407:249-252.
41. Doonan R., McElwee J.J., Matthijssens F., Walker G.A., Houthoofd K., Back P., et al. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev. 2008, 22:3236-3241.
42. Schulz T.J., Zarse K., Voigt A., Urban N., Birringer M., Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 2007, 6:280-293.
43. Kirchman P.A., Kim S., Lai C.Y., Jazwinski S.M. Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae. Genetics 1999, 152:179-190.
44. Esser K. Podospora anserina. Handbook of Genetics 1974, 531-551. Plenum Press, New York, NY. R.C. King (Ed.).
45. Lecellier G., Silar P. Rapid methods for nucleic acids extraction from petri dish-grown mycelia. Curr. Genet. 1994, 25:122-123.
46. Gredilla R., Grief J., Osiewacz H.D. Mitochondrial free radical generation and lifespan control in the fungal aging model Podospora anserina. Exp. Gerontol. 2006, 41:439-447.
47. Krause F., Seelert H. Detection and analysis of protein-protein interactions in organellar and prokaryotic proteomes by blue-native and colorless-native gel electrophoresis. Curr. Protoc. Protein Sci. 2008, 51:14.11.1-14.11.36. Republished as 51: 19.18.1-19.18.36.