Identification and functional analysis of mitochondrial complex I assembly factor homologues in C. elegans

Mitochondrion

Volumn 12, Issue 3, 2012, Pages 399-405

  van den Ecker, Daniela ^a   van den Brand, Mariël A ^b   Ariaans, Gerke ^a   Hoffmann, Michael ^a   Bossinger, Olaf ^c   Mayatepek, Ertan ^a   Nijtmans, Leo G ^b   Distelmaier, Felix ^a  

^a UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

BN PAGE; Chaperones; Complex I; Leigh syndrome; Metabolism; Mitochondrial disease; NDUF; NGM; NUAF 1 NUAF 3; OXPHOS; Respiratory chain; RNAi

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RNA; UBIQUINOL CYTOCHROME C REDUCTASE;

ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA INTERFERENCE;

ANIMALS; BIOGENESIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ELECTRON TRANSPORT COMPLEX I; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NADH DEHYDROGENASE; SEQUENCE HOMOLOGY, AMINO ACID;

CAENORHABDITIS ELEGANS;

EID: 84859737968     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.01.003     Document Type: Article

References (45)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
2. Apostolova N., Blas-García A., Esplugues J.V. Mitochondrial toxicity in HAART: an overview of in vitro evidence. Curr. Pharm. Des. 2011, 17:2130-2144.
3. Artal-Sanz M., Tsang W.Y., Willems E.M., Grivell L.A., Lemire B.D. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J. Biol. Chem. 2003, 278:32091-32099.
4. Bratic I., Hench J., Henriksson J., Antebi A., Burglin T.R. Mitochondrial DNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res. 2009, 37:1817-1828.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Calvaruso M.A., Smeitink J., Nijtmans L. Electrophoresis techniques to investigate defects in oxidative phosphorylation. Methods 2008, 46:281-287.
7. Curran S.P., Leverich E.P., Koehler C.M., Larsen P.L. Defective mitochondrial protein translocation precludes normal Caenorhabditis elegans development. J. Biol. Chem. 2004, 279:54655-54662.
8. Diaz F., Kotarsky H., Fellman V., Moraes C.T. Mitochondrial disorders caused by mutations in respiratory chain assembly factors. Semin. Fetal Neonatal. Med. 2011, 16:197-204.
9. Dingley S., Polyak E., Lightfoot R., Ostrovsky J., Rao M., Greco T., Ischiropoulos H., Falk M.J. Mitochondrial respiratory chain dysfunction variably increases oxidant stress in Caenorhabditis elegans. Mitochondrion 2010, 10:125-136.
10. Distelmaier F., Koopman W.J., van den Heuvel L.P., Rodenburg R.J., Mayatepek E., Willems P.H., Smeitink J.A. Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease. Brain 2009, 132:833-842.
11. Dunning C.J., McKenzie M., Sugiana C., Lazarou M., Silke J., Connelly A., Fletcher J.M., Kirby D.M., Thorburn D.R., Ryan M.T. Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J. 2007, 26:3227-3237.
12. Falk M.J., Rosenjack J.R., Polyak E., Suthammarak W., Chen Z., Morgan P.G., Sedensky M.M. Subcomplex Ilambda specifically controls integrated mitochondrial functions in Caenorhabditis elegans. PLoS One 2009, 4:e6607.
13. Gouda K., Matsunaga Y., Iwasaki T., Kawano T. An altered method of feeding RNAi that knocks down multiple genes simultaneously in the nematode Caenorhabditis elegans. Biosci. Biotechnol. Biochem. 2010, 74:2361-2365.
14. Grad L.I., Lemire B.D. Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis. Hum. Mol. Genet. 2004, 13:303-314.
15. Hoffmann M., Bellance N., Rossignol R., Koopman W.J., Willems P.H., Mayatepek E., Bossinger O., Distelmaier F. C. elegans ATAD-3 is essential for mitochondrial activity and development. PLoS One 2009, 4:e7644.
16. Hoogewijs D., Houthoofd K., Matthijssens F., Vandesompele J., Vanfleteren J.R. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol. 2008, 22:9.
17. Jones K.T., Greer E.R., Pearce D., Ashrafi K. Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1. PLoS Biol. 2009, 7:e60.
18. Kamath R.S., Martinez-Campos M., Zipperlen P., Fraser A.G., Ahringer J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2001, 2. RESEARCH0002.
19. Kanazawa T., Zappaterra M.D., Hasegawa A., Wright A.P., Newman-Smith E.D. The C. elegans Opa1 homologue EAT-3 is essential for resistance to free radicals. PLoS Genet. 2008, 4:e1000022.
20. Koopman W.J., Nijtmans L.G., Dieteren C.E., Roestenberg P., Valsecchi F., Smeitink J.A., Willems P.H. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal. Rev. 2010, 12:1431-1470.
21. Kruse S.E., Watt W.C., Marcinek D.J., Kapur R.P., Schenkman K.A., Palmiter R.D. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008, 7:312-320.
22. Kuffner R., Rohr A., Schmiede A., Krull C., Schulte U. Involvement of two novel chaperones in the assembly of mitochondrial NADH:Ubiquinone oxidoreductase (complex I). J. Mol. Biol. 1998, 283:409-417.
23. Lazarou M., McKenzie M., Ohtake A., Thorburn D.R., Ryan M.T. Analysis of the assembly profiles for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Mol. Cell. Biol. 2007, 27:4228-4237.
24. Lazarou M., Thorburn D.R., Ryan M.T., McKenzie M. Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta 2009, 1793:78-88.
25. McKenzie M., Ryan M.T. Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life Rev. 2010, 62:497-502.
26. McKay R.M., McKay J.P., Avery L., Graff J.M. C elegans: a model for exploring the genetics of fat storage. Dev. Cell. 2003, 4:131-142.
27. Nouws J., Nijtmans L., Houten S.M., van den Brand M., Huynen M., Venselaar H., Hoefs S., Gloerich J., Kronick J., Hutchin T., Willems P., Rodenburg R., Wanders R., van den Heuvel L., Smeitink J., Vogel R.O. Acyl-CoA dehydrogenase 9 is required for the biogenesis of oxidative phosphorylation complex I. Cell Metab. 2010, 12:283-294.
28. Nouws J., Nijtmans L.G., Smeitink J.A., Vogel R.O. Assembly factors as a new class of disease genes for mitochondrial complex I deficiency: cause, pathology and treatment options. Brain 2011, 10.1093/brain/awr261.
29. Ogilvie I., Kennaway N.G., Shoubridge E.A. A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J. Clin. Invest. 2005, 115:2784-2792.
30. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
31. Saada A., Edvardson S., Rapoport M., Shaag A., Amry K., Miller C., Lorberboum-Galski H., Elpeleg O. C6ORF66 is an assembly factor of mitochondrial complex I. Am. J. Hum. Genet. 2008, 82:32-38.
32. Saada A., Vogel R.O., Hoefs S.J., van den Brand M.A., Wessels H.J., Willems P.H., Venselaar H., Shaag A., Barghuti F., Reish O., Shohat M., Huynen M.A., Smeitink J.A., van den Heuvel L.P., Nijtmans L.G. Mutations in NDUFAF3 (C3ORF60), encoding an NDUFAF4 (C6ORF66)-interacting complex I assembly protein, cause fatal neonatal mitochondrial disease. Am. J. Hum. Genet. 2009, 84:718-727.
33. Sheftel A.D., Stehling O., Pierik A.J., Netz D.J., Kerscher S., Elsässer H.P., Wittig I., Balk J., Brandt U., Lill R. Human ind1, an iron-sulfur cluster assembly factor for respiratory complex I. Mol. Cell. Biol. 2009, 29:6059-6073.
34. Sugiana C., Pagliarini D.J., McKenzie M., Kirby D.M., Salemi R., Abu-Amero K.K., Dahl H.H., Hutchison W.M., Vascotto K.A., Smith S.M., Newbold R.F., Christodoulou J., Calvo S., Mootha V.K., Ryan M.T., Thorburn D.R. Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am. J. Hum. Genet. 2008, 83:468-478.
35. Suthammarak W., Yang Y.Y., Morgan P.G., Sedensky M.M. Complex I function is defective in complex IV-deficient Caenorhabditis elegans. J. Biol. Chem. 2009, 284:6425-6435.
36. Suzuki Y., Yandell M.D., Roy P.J., Krishna S., Savage-Dunn C., Ross R.M., Padgett R.W., Wood W.B. A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans. Development 1999, 126:241.
37. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
38. van den Ecker D., van den Brand M.A., Bossinger O., Mayatepek E., Nijtmans L.G., Distelmaier F. Blue native electrophoresis to study mitochondrial complex I in C. elegans. Anal. Biochem. 2010, 407:287-289.
39. Vogel R.O., Janssen R.J., Ugalde C., Grovenstein M., Huijbens R.J., Visch H.J., van den Heuvel L.P., Willems P.H., Zeviani M., Smeitink J.A., Nijtmans L.G. Human mitochondrial complex I assembly is mediated by NDUFAF1. FEBS J. 2005, 272:5317-5326.
40. Vogel R.O., Janssen R.J., van den Brand M.A., Dieteren C.E., Verkaart S., Koopman W.J., Willems P.H., Pluk W., van den Heuvel L.P., Smeitink J.A., Nijtmans L.G. Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Genes Dev. 2007, 21:615-624.
41. Vogel R.O., Dieteren C.E., van den Heuvel L.P., Willems P.H., Smeitink J.A., Koopman W.J., Nijtmans L.G. Identification of mitochondrial complex I assembly intermediates by tracing tagged NDUFS3 demonstrates the entry point of mitochondrial subunits. J. Biol. Chem. 2007, 282:7582-7590.
42. Vogel R.O., Smeitink J.A., Nijtmans L.G. Human mitochondrial complex I assembly: a dynamic and versatile process. Biochim. Biophys. Acta 2007, 1767:1215-1227.
43. Wang M.C., O'Rourke E.J., Ruvkun G. Fat metabolism links germline stem cells and longevity in C. elegans. Science 2008, 322:957-960.
44. Waters K., Yang A.Z., Reinke V. Genome-wide analysis of germ cell proliferation in C. elegans identifies VRK-1 as a key regulator of CEP-1/p53. Dev. Biol. 2010, 344:1011-1025.
45. Watts J.L. Fat synthesis and adiposity regulation in Caenorhabditis elegans. Trends Endocrinol. Metab. 2009, 20:58-65.