Riboflavin enhances the assembly of mitochondrial cytochrome c oxidase in C. elegans NADH-ubiquinone oxidoreductase mutants

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 2, 2006, Pages 115-122

  Grad, Leslie I ^a   Lemire, Bernard D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

C. elegans; Complex I; Complex IV; Mitochondria

Indexed keywords

CYTOCHROME C OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RIBOFLAVIN;

ARTICLE; CAENORHABDITIS ELEGANS; CATALYSIS; ENZYME ACTIVITY; ENZYME DEFICIENCY; GEL ELECTROPHORESIS; LACTIC ACIDOSIS; MITOCHONDRION; MUTATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

ANIMALS; CAENORHABDITIS ELEGANS; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; MITOCHONDRIA; RIBOFLAVIN;

CAENORHABDITIS ELEGANS;

EID: 33645001946     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2005.11.009     Document Type: Article

References (52)

1. J.L. Loeffen, J.A. Smeitink, J.M. Trijbels, A.J. Janssen, R.H. Triepels, R.C. Sengers, and L.P. van den Heuvel Isolated complex I deficiency in children: clinical, biochemical and genetic aspects Hum. Mutat. 15 2000 123 134
2. F. Scaglia, J.A. Towbin, W.J. Craigen, J.W. Belmont, E.O. Smith, S.R. Neish, S.M. Ware, J.V. Hunter, S.D. Fernbach, G.D. Vladutiu, L.J. Wong, and H. Vogel Clinical spectrum, morbidity, and mortality in 113 pediatric patients with mitochondrial disease Pediatrics 114 2004 925 931
3. B.H. Robinson Human complex I deficiency: clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect Biochim. Biophys. Acta 1364 1998 271 286
4. E.A. Shoubridge Nuclear genetic defects of oxidative phosphorylation Hum. Mol. Genet. 10 2001 2277 2284
5. J. Carroll, I.M. Fearnley, R.J. Shannon, J. Hirst, and J.E. Walker Analysis of the subunit composition of complex I from bovine heart mitochondria Mol. Cell Proteomics 2 2003 117 126
6. G. Attardi, and G. Schatz Biogenesis of mitochondria Annu. Rev. Cell Biol. 4 1988 289 333
7. J.E. Walker The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains Q. Rev. Biophys. 25 1992 253 324
8. T. Yagi, and A. Matsuno-Yagi The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked Biochemistry 42 2003 2266 2274
9. T. Yano The energy-transducing NADH: quinone oxidoreductase, complex I Mol. Aspects Med. 23 2002 345 368
10. T. Ohnishi Iron-sulfur clusters/semiquinones in complex I Biochim. Biophys. Acta 1364 1998 186 206
11. B.E. Schultz, and S.I. Chan Structures and proton-pumping strategies of mitochondrial respiratory enzymes Annu. Rev. Biophys. Biomol. Struct. 30 2001 23 65
12. J. Smeitink, and L. van den Heuvel Human mitochondrial complex I in health and disease Am. J. Hum. Genet. 64 1999 1505 1510
13. L.I. Grad, and B.D. Lemire Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis Hum. Mol. Genet. 13 2004 303 314
14. W.Y. Tsang, L.C. Sayles, L.I. Grad, D.B. Pilgrim, and B.D. Lemire Mitochondrial respiratory chain deficiency in Caenorhabditis elegans results in developmental arrest and increased lifespan J. Biol. Chem. 276 2001 32240 32246
15. T. Gabaldón, D. Rainey, and M.A. Huynen Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I) J. Mol. Biol. 348 2005 857 870
16. W.Y. Tsang, and B.D. Lemire The role of mitochondria in the life of the nematode, Caenorhabditis elegans Biochim. Biophys. Acta 1638 2003 91 105
17. M. Schuelke, J. Smeitink, E. Mariman, J. Loeffen, B. Plecko, F. Trijbels, S. Stockler-Ipsiroglu, and L. van den Heuvel Mutant NDUFV1 subunit of mitochondrial complex I causes leukodystrophy and myoclonic epilepsy Nat. Genet. 21 1999 260 261
18. M. Schuelke, A. Detjen, L. van den Heuvel, C. Korenke, A. Janssen, A. Smits, F. Trijbels, and J. Smeitink New nuclear encoded mitochondrial mutation illustrates pitfalls in prenatal diagnosis by biochemical methods Clin. Chem. 48 2002 772 775
19. P. Bénit, D. Chretien, N. Kadhom, P. de Lonlay-Debeney, V. Cormier-Daire, A. Cabral, S. Peudenier, P. Rustin, A. Munnich, and A. Rötig Large-scale deletion and point mutations of the nuclear NDUFV1 and NDUFS1 genes in mitochondrial complex I deficiency Am. J. Hum. Genet. 68 2001 1344 1352
20. P.F. Chinnery, and D.M. Turnbull Epidemiology and treatment of mitochondrial disorders Am. J. Med. Genet. 106 2001 94 101
21. R.W. Taylor, P.F. Chinnery, K.M. Clark, R.N. Lightowlers, and D.M. Turnbull Treatment of mitochondrial disease J. Bioenerg. Biomembranes 29 1997 195 205
22. A.M. Roodhooft, K.J. Van Acker, J.J. Martin, C. Ceuterick, H.R. Scholte, and I.E. Luyt-Houwen Benign mitochondrial myopathy with deficiency of NADH-CoQ reductase and cytochrome c oxidase Neuropediatrics 17 1986 221 226
23. W.F. Arts, H.R. Scholte, J.M. Bogaard, K.F. Kerrebijn, and I.E. Luyt-Houwen NADH-CoQ reductase deficient myopathy: successful treatment with riboflavin Lancet 2 1983 581 582
24. 31P magnetic resonance spectroscopy during treatment with nicotinamide and riboflavin Neurology 42 1992 2147 2152
25. P.L. Bernsen, F.J. Gabreels, W. Ruitenbeek, R.C. Sengers, A.M. Stadhouders, and W.O. Renier Successful treatment of pure myopathy, associated with complex I deficiency, with riboflavin and carnitine Arch. Neurol. 48 1991 334 338
26. V. Petruzzella, R. Vergari, I. Puzziferri, D. Boffoli, E. Lamantea, M. Zeviani, and S. Papa A nonsense mutation in the NDUFS4 gene encoding the 18 kDa (AQDQ) subunit of complex I abolishes assembly and activity of the complex in a patient with Leigh-like syndrome Hum. Mol. Genet. 10 2001 529 535
27. G. Hofhaus, and G. Attardi Lack of assembly of mitochondrial DNA-encoded subunits of respiratory NADH dehydrogenase and loss of enzyme activity in a human cell mutant lacking the mitochondrial ND4 gene product EMBO J. 12 1993 3043 3048
28. H. Antonicka, I. Ogilvie, T. Taivassalo, R.P. Anitori, R.G. Haller, J. Vissing, N.G. Kennaway, and E.A. Shoubridge Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency J. Biol. Chem. 278 2003 43081 43088
29. R.H. Triepels, L.P. Van Den Heuvel, J.M. Trijbels, and J.A. Smeitink Respiratory chain complex I deficiency Am. J. Med. Genet. 106 2001 37 45
30. P. Pecina, H. Houstková, H. Hansíková, J. Zeman, and J. Houstek Genetic defects of cytochrome c oxidase assembly Physiol. Res. 53 Suppl. 1 2004 S213 S223
31. E.A. Shoubridge Cytochrome c oxidase deficiency Am. J. Med. Genet. 106 2001 46 52
32. J.A. Lewis, and J.T. Fleming Basic culture methods Methods Cell Biol. 48 1995 3 29
33. E. Dibrov, S. Fu, and B.D. Lemire The Saccharomyces cerevisiae TCM62 gene encodes a chaperone necessary for the assembly of the mitochondrial succinate dehydrogenase (complex II) J. Biol. Chem. 273 1998 32042 32048
34. H. Schägger, and G. von Jagow Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Anal. Biochem. 199 1991 223 231
35. P.J.T. Dekker, F. Martin, A.C. Maarse, U. Bomer, H. Muller, B. Guiard, M. Meijer, J. Rassow, and N. Pfanner The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44 EMBO J. 16 1997 5408 5419
36. L.G. Nijtmans, N.S. Henderson, and I.J. Holt Blue native electrophoresis to study mitochondrial and other protein complexes Methods 26 2002 327 334
37. M.A. Birch-Machin, and D.M. Turnbull Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues Methods Cell Biol. 65 2001 97 117
38. C. Ugalde, R.J. Janssen, L.P. Van Den Heuvel, J.A. Smeitink, and L.G. Nijtmans Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency Hum. Mol. Genet. 13 2004 659 667
39. R.H. Triepels, B.J. Hanson, L.P. van Den Heuvel, L. Sundell, M.F. Marusich, J.A. Smeitink, and R.A. Capaldi Human complex I defects can be resolved by monoclonal antibody analysis into distinct subunit assembly patterns J. Biol. Chem. 276 2001 8892 8897
40. S. Scacco, V. Petruzzella, S. Budde, R. Vergari, R. Tamborra, D. Panelli, L.P. van den Heuvel, J.A. Smeitink, and S. Papa Pathological mutations of the human NDUFS4 gene of the 18-kDa (AQDQ) subunit of complex I affect the expression of the protein and the assembly and function of the complex J. Biol. Chem. 278 2003 44161 44167
41. C. Ugalde, 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 Impaired complex I assembly in a Leigh syndrome patient with a novel missense mutation in the ND6 gene Ann. Neurol. 54 2003 665 669
42. M. Duarte, U. Schulte, A.V. Ushakova, and A. Videira Neurospora strains harboring mitochondrial disease-associated mutations in iron-sulfur subunits of complex I Genetics 171 2005 91 99
43. P. Hinchliffe, and L.A. Sazanov Organization of iron-sulfur clusters in respiratory complex I Science 309 2005 771 774
44. T. Friedrich, and B. Böttcher The gross structure of the respiratory complex I: a Lego System Biochim. Biophys. Acta 1608 2004 1 9
45. C. Ugalde, R. Vogel, R. Huijbens, B. Van Den Heuvel, J. Smeitink, and L. Nijtmans Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies Hum. Mol. Genet. 13 2004 2461 2472
46. R. Vogel, L. Nijtmans, C. Ugalde, L. Van Den Heuvel, and J. Smeitink Complex I assembly: a puzzling problem Curr. Opin. Neurol. 17 2004 179 186
47. E. Lamantea, F. Carrara, C. Mariotti, L. Morandi, V. Tiranti, and M. Zeviani A novel nonsense mutation (Q352X) in the mitochondrial cytochrome b gene associated with a combined deficiency of complexes I and III Neuromuscul. Disord. 12 2002 49 52
48. H. Schägger, and K. Pfeiffer Supercomplexes in the respiratory chains of yeast and mammalian mitochondria EMBO J. 19 2000 1777 1783
49. G.C. Korenke, H.A. Bentlage, W. Ruitenbeek, R.C. Sengers, W. Sperl, J.M. Trijbels, F.J. Gabreels, F.A. Wijburg, V. Wiedermann, F. Hanefeld, U. Wendel, M. Reckmann, V. Griebel, and H. Wölk Isolated and combined deficiencies of NADH dehydrogenase (complex I) in muscle tissue of children with mitochondrial myopathies Eur. J. Pediatr. 150 1990 104 108
50. W. Sperl, W. Ruitenbeek, R.C. Sengers, J.M. Trijbels, H. Bentlage, J.E. Wraith, C. Heilmann, S. Stöckler, C. Binder, G.C. Korenke, and F. Hanefeld Combined deficiencies of the pyruvate dehydrogenase complex and enzymes of the respiratory chain in mitochondrial myopathies Eur. J. Pediatr. 151 1992 192 195
51. J.A. Morgan-Hughes, A.H. Schapira, J.M. Cooper, and J.B. Clark Molecular defects of NADH-ubiquinone oxidoreductase (complex I) in mitochondrial diseases J. Bioenerg. Biomembranes 20 1988 365 382
52. J.M. Herrmann, H. Koll, R.A. Cook, W. Neupert, and R.A. Stuart Topogenesis of cytochrome oxidase subunit II. Mechanisms of protein export from the mitochondrial matrix J. Biol. Chem. 270 1995 27079 27086