Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease

EMBO Journal

Volumn 26, Issue 13, 2007, Pages 3227-3237

  Dunning, C J R ^a   McKenzie, M ^a   Sugiana, C ^b,c   Lazarou, M ^a   Silke, J ^a   Connelly, A ^a   Fletcher, J M ^d   Kirby, D M ^b,c   Thorburn, D R ^b,c   Ryan, M T ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Blue native PAGE; CIA30; Complex I; Lentivirus; Mitochondria

Indexed keywords

COMPLEX I INTERMEDIATE ASSOCIATED PROTEIN 30; LENTIVIRUS VECTOR; MITOCHONDRIAL DNA; PROTEIN; PROTEIN ANTIBODY; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ADULT; ARTICLE; BRAIN DISEASE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DISSOCIATION; EMBRYO; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME SUBUNIT; GENE MUTATION; GENETIC CODE; HUMAN; HUMAN CELL; HYPERTROPHIC CARDIOMYOPATHY; MALE; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; RNA TRANSLATION; STEADY STATE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE; CONSERVED SEQUENCE; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX I; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NADH DEHYDROGENASE; PROTEIN BINDING; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT;

LENTIVIRUS;

EID: 34447312250     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601748     Document Type: Article

References (49)

1. Acin-Perez R, Bayona-Bafaluy MP, Fernandez-Silva P, Moreno-Loshuertos R, Perez-Martos A, Bruno C, Moraes CT, Enriquez JA (2004) Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol Cell 13: 805-815
2. Amrani N, Sachs MS, Jacobson A (2006) Early nonsense: mRNA decay solves a translational problem. Nat Rev Mol Cell Biol 7: 415-425
3. Antonicka H, Ogilvie I, Taivassalo T, Anitori RP, Haller RG, Vissing J, Kennaway NG, Shoubridge EA (2003) Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. J Biol Chem 278: 43081-43088
4. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75: 69-92
5. Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J, Walker JE (2006) Bovine complex I is a complex of 45 different subunits. J Biol Chem 281: 32724-32727
6. Casanova E, Fehsenfeld S, Lemberger T, Shimshek DR, Sprengel R, Mantamadiotis T (2002) ER-based double iCre fusion protein allows partial recombination in forebrain. Genesis 34: 208-214
7. Chomyn A (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol 264: 197-211
8. Diaz F, Fukui H, Garcia S, Moraes CT (2006) Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol Cell Biol 26: 4872-4881
9. Fontanesi F, Soto IC, Horn D, Barrientos A (2006) Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 291: C1129-C1147
10. Gabaldon T, Rainey D, Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 348: 857-870
11. Grigorieff N (1998) Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 A in ice. J Mol Biol 277: 1033-1046
12. Harlow E, Lane D (1999) Using Antibodies: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press
13. Humphries AD, Streimann IC, Stojanovski D, Johnston AJ, Yano M, Hoogenraad NJ, Ryan MT (2005) Dissection of the mitochondrial import and assembly pathway for human Tom40. J Biol Chem 280: 11535-11543
14. Janssen R, Smeitink J, Smeets R, van Den Heuvel L (2002) CIA30 complex I assembly factor: a candidate for human complex I deficiency? Hum Genet 110: 264-270
15. Johnston AJ, Hoogenraad J, Dougan DA, Truscott KN, Yano M, Mori M, Hoogenraad NJ, Ryan MT (2002) Insertion and assembly of human tom7 into the preprotein translocase complex of the outer mitochondrial membrane. J Biol Chem 277: 42197-42204
16. Kirby DM, Crawford M, Cleary MA, Dahl HH, Dennett X, Thorburn DR (1999) Respiratory chain complex I deficiency: an under-diagnosed energy generation disorder. Neurology 52: 1255-1264
17. Kirby DM, McFarland R, Ohtake A, Dunning C, Ryan MT, Wilson C, Ketteridge D, Turnbull DM, Thorburn DR, Taylor RW (2004a) Mutations of the mitochondrial ND1 gene as a cause of MELAS. J Med Genet 41: 784-789
18. Kirby DM, Salemi R, Sugiana C, Ohtake A, Parry L, Bell KM, Kirk EP, Boneh A, Taylor RW, Dahl HH, Ryan MT, Thorburn DR (2004b) NDUFS6 mutations are a novel cause of lethal neonatal mitochondrial complex I deficiency. J Clin Invest 114: 837-845
19. Kuffner R, Rohr A, Schmiede A, Krull C, Schulte U (1998) Involvement of two novel chaperones in the assembly of mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 283: 409-417
20. Lazarou M, McKenzie M, Ohtake A, Thorburn DR, Ryan MT (2007) Analysis of the assembly profiles for mitochondrial and nuclear encoded subunits into Complex I. Mol Cell Biol 27: 4228-4237
21. Lingelbach KR, Graf LJ, Dunn AR, Hoogenraad NJ (1986) Effect of deletions within the leader peptide of pre-ornithine transcarbamylase on mitochondrial import. Eur J Biochem 161: 19-23
22. Marques I, Duarte M, Assuncao J, Ushakova AV, Videira A (2005) Composition of complex I from Neurospora crassa and disruption of two 'accessory' subunits. Biochim Biophys Acta 1707: 211-220
23. McKenzie M, Lazarou M, Thorburn DR, Ryan MT (2006) Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J Mol Biol 361: 462-469
24. McKenzie M, Lazarou M, Thorburn DR, Ryan MT (2007) Analysis of mitochondrial subunit assembly into respiratory chain complexes using blue native polyacrylamide gel electrophoresis. Anal Biochem 364: 128-137
25. Meisinger C, Ryan MT, Hill K, Model K, Lim JH, Sickmann A, Muller H, Meyer HE, Wagner R, Pfanner N (2001) Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors. Mol Cell Biol 21: 2337-2348
26. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267
27. Nehls U, Friedrich T, Schmiede A, Ohnishi T, Weiss H (1992) Characterization of assembly intermediates of NADH:ubiquinone oxidoreductase (complex I) accumulated in Neurospora mitochondria by gene disruption. J Mol Biol 227: 1032-1042
28. Ogilvie I, Kennaway NG, Shoubridge EA (2005) A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J Clin Invest 115: 2784-2792
29. Pallotti F, Lenaz G (2001) Isolation and subfractionation of mitochondria from animal cells and tissue culture lines. Methods Cell Biol 65: 1-35
30. Peralta D, Lithgow T, Hoogenraad NJ, Hoj PB (1993) Prechaperonin 60 and preornithine transcarbamylase share components of the import apparatus but have distinct maturation pathways in rat liver mitochondria. Eur J Biochem 211: 881-889
31. Rahman S, Blok RB, Dahl HH, Danks DM, Kirby DM, Chow CW, Christodoulou J, Thorburn DR (1996) Leigh syndrome: clinical features and biochemical and DNA abnormalities. Ann Neurol 39: 343-351
32. Ryan MT, Pfanner N (2001) Hsp70 proteins in protein translocation. Adv Protein Chem 59: 223-242
33. Ryan MT, Voos W, Pfanner N (2001) Assaying protein import into mitochondria. Methods Cell Biol 65: 189-215
34. Schagger H (2001) Respiratory chain supercomplexes. IUBMB Life 52: 119-128
35. Schagger H, Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19: 1777-1783
36. Schagger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379
37. Schagger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199: 223-231
38. Schapira AH (2006) Etiology of Parkinson's disease. Neurology 66: S10-S23
39. Shapiro MB, Senapathy P (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15: 7155-7174
40. Thorburn DR, Sugiana C, Salemi R, Kirby DM, Worgan L, Ohtake A, Ryan MT (2004) Biochemical and molecular diagnosis of mitochondrial respiratory chain disorders. Biochim Biophys Acta 1659: 121-128
41. Triepels RH, Hanson BJ, van den Heuvel LP, Sundell L, Marusich MF, Smeitink JA, Capaldi RA (2001) Human complex I defects can be resolved by monoclonal antibody analysis into distinct subunit assembly patterns. J Biol Chem 276: 8892-8897
42. Tuschen G, Sackmann U, Nehls U, Haiker H, Buse G, Weiss H (1990) Assembly of NADH: ubiquinone reductase (complex I) in Neurospora mitochondria. Independent pathways of nuclear-encoded and mitochondrially encoded subunits. J Mol Biol 213: 845-857
43. Ugalde C, Janssen RJ, van den Heuvel LP, Smeitink JA, Nijtmans LG (2004a) Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum Mol Genet 13: 659-667
44. Ugalde C, Vogel R, Huijbens R, Van Den Heuvel B, Smeitink J, Nijtmans L (2004b) 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
45. Vahsen N, Cande C, Briere JJ, Benit P, Joza N, Larochette N, Mastroberardino PG, Pequignot MO, Casares N, Lazar V, Feraud O, Debili N, Wissing S, Engelhardt S, Madeo F, Piacentini M, Penninger JM, Schagger H, Rustin P, Kroemer G (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J 23: 4679-4689
46. Vogel RO, Janssen RJ, Ugalde C, Grovenstein M, Huijbens RJ, Visch HJ, van den Heuvel LP, Willems PH, Zeviani M, Smeitink JA, Nijtmans LG (2005) Human mitochondrial complex I assembly is mediated by NDUFAF1. FEBS J 272: 5317-5326
47. Vogel RO, Janssen RJ, van den Brand MA, Dieteren CE, Verkaart S, Koopman WJ, Willems PH, Pluk W, van den Heuvel LP, Smeitink JA, Nijtmans LG (2007a) Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Genes Dev 21: 615-624
48. Vogel RO, van den Brand MA, Rodenburg RJ, van den Heuvel LP, Tsuneoka M, Smeitink JA, Nijtmans LG (2007b) Investigation of the complex I assembly chaperones B17.2L and NDUFAF1 in a cohort of CI deficient patients. Mol Genet Metab 91: 176-182
49. Wiedemann N, Frazier AE, Pfanner N (2004) The protein import machinery of mitochondria. J Biol Chem 279: 14473-14476