Assembly factors of human mitochondrial respiratory chain complexes: Physiology and pathophysiology

Advances in Experimental Medicine and Biology

Volumn 748, Issue , 2012, Pages 65-106

  Ghezzi, Daniele ^a   Zeviani, Massimo ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACAD9 PROTEIN; BCS1L PROTEIN; C20ORF7 PROTEIN; C8ORF38 PROTEIN; CHAPERONE; CYTOCHROME C OXIDASE; EVOLUTIONARY CONSERVED SIGNALING INTERMEDIATE IN TOLL PATHWAY PROTEIN; FOXRED1 PROTEIN; HOLOCYTOCHROME C SYNTHASE; LYASE; MITOCHONDRIAL DNA; NDUFAF1 PROTEIN; NDUFAF2 PROTEIN; NDUFAF3 PROTEIN; NDUFAF4 PROTEIN; NUBPL PROTEIN; NUCLEAR PROTEIN; PENTATRICOPEPTIDE REPEAT DOMAIN PROTEIN 2; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE ASSEMBLY FACTOR 1; SUCCINATE DEHYDROGENASE ASSEMBLY FACTOR 2; SURF1 PROTEIN; SYNTHESIS OF CYTOCHROME OXIDASE 1; SYNTHESIS OF CYTOCHROME OXIDASE 2; TETRATRICOPEPTIDE REPEAT PROTEIN; TTC19 PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; ATAXIA; BRAIN DISEASE; CARDIOMYOPATHY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENCEPHALOMYOPATHY; ENZYME STABILITY; ENZYME SUBUNIT; GENE; GENE MUTATION; HUMAN; KIDNEY DISEASE; LACTIC ACIDOSIS; LEIGH DISEASE; LEUKODYSTROPHY; LIVER DISEASE; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MYOPATHY; NUCLEAR GENE; OXIDATIVE PHOSPHORYLATION; PARAGANGLIOMA; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RESPIRATORY CHAIN;

ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; HUMANS; MULTIENZYME COMPLEXES; OXIDATIVE PHOSPHORYLATION;

EID: 84863741781     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-3573-0_4     Document Type: Article

References (186)

1. Acin-Perez R, Bayona-Bafaluy MP, Fernandez-Silva P et al (2004) Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol Cell 13:805-815
2. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA (2008) Respiratory active mitochondrial supercomplexes. Mol Cell 32:529-539
3. Ackerman SH, Tzagoloff A (1990) Identification of two nuclear genes (ATP11, ATP12) required for assembly of the yeast F1-ATPase. Proc Natl Acad Sci USA 87:4986-4990
4. Andersson SG, Zomorodipour A, Andersson JO et al (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-140
5. Antonicka H, Leary SC, Guercin GH et al (2003) Mutations in COX10 result in a defect in mitochondrial heme A biosynthesis and account for multiple, early-onset clinical phenotypes associated with isolated COX deficiency. Hum Mol Genet 12:2693-2702
6. Arnold S, Kadenbach B (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome-c oxidase. Eur J Biochem 249:350-354
7. Arnold I, Pfeiffer K, Neupert W, Stuart RA, Schagger H (1998) Yeast mitochondrial F1F0-ATP synthase exists as a dimer: Identification of three dimer-specific subunits. EMBO J 17:7170-7178
8. Barghuti F, Elian K, Gomori JM, Shaag A, Edvardson S, Saada A, Elpeleg O (2008) The unique neuroradiology of complex I deficiency due to NDUFA12L defect. Mol Genet Metab 94:78-82
9. Barrientos A, Gouget K, Horn D, Soto IC, Fontanesi F (2009) Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process. Biochim Biophys Acta 1793:97-107
10. Barth PG, Wanders RJ, Vreken P, Janssen EA, Lam J, Baas F (1999) X-linked cardioskeletal myopathy and neutropenia (Barth syndrome) (MIM 302060). J Inherit Metab Dis 22:555-567
11. Bayley JP, Devilee P (2010) Warburg tumours and the mechanisms of mitochondrial tumour suppressor genes. Barking up the right tree? Curr Opin Genet Dev 20:324-329
12. Bayley JP, Kunst HP, Cascon A et al (2010) SDHAF2 mutations in familial and sporadic paraganglioma and phaeochromocytoma. Lancet Oncol 11:366-372
13. Belli G, Molina MM, Garcia-Martinez J, Perez-Ortin JE, Herrero E (2004) Saccharomyces cerevisiae glutaredoxin 5-deficient cells subjected to continuous oxidizing conditions are affected in the expression of specific sets of genes. J Biol Chem 279:12386-12395
14. Bernard DG, Gabilly ST, Dujardin G, Merchant S, Hamel PP (2003) Overlapping specificities of the mitochondrial cytochrome c and c1 heme lyases. J Biol Chem 278:49732-49742
15. Bianchi C, Genova ML, Parenti Castelli G, Lenaz G (2004) The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J Biol Chem 279:36562-36569
16. Birchmeier W, Kohler CE, Schatz G (1976) Interaction of integral and peripheral membrane proteins: affinity labeling of yeast cytochrome oxidase by modified yeast cytochrome c. Proc Natl Acad Sci USA 73:4334-4338
17. Blair PV (1967) Preparation and properties of repeating units of electron transfer. Methods Enzymol 10:208-212
18. Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating proteinprotein interactions. Bioessays 21:932-939
19. Bonnefoy N, Kermorgant M, Groudinsky O, Minet M, Slonimski PP, Dujardin G (1994) Cloning of a human gene involved in cytochrome oxidase assembly by functional complementation of an oxa1- mutation in Saccharomyces cerevisiae . Proc Natl Acad Sci USA 91:11978-11982
20. Boyer PD (1993) The binding change mechanism for ATP synthase-some probabilities and possibilities. Biochim Biophys Acta 1140:215-250
21. Boyer PD (1997) The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66:717-749
22. Brandt U, Yu L, Yu CA, Trumpower BL (1993) The mitochondrial targeting presequence of the Rieske iron-sulfur protein is processed in a single step after insertion into the cytochrome bc1 complex in mammals and retained as a subunit in the complex. J Biol Chem 268:8387-8390
23. Bugiani M, Invernizzi F, Alberio S et al (2004) Clinical and molecular findings in children with complex I deficiency. Biochim Biophys Acta 1659:136-147
24. Bundschuh FA, Hannappel A, Anderka O et al (2009) Surf1, associated with Leigh syndrome in humans, is a heme-binding protein in bacterial oxidase biogenesis. J Biol Chem 284:25735-25741
25. Bych K, Kerscher S, Netz DJA, Pierik AJ, Zwicker K, Huynen MA, Lill R, Brandt U, Balk J (2008) Ind1 is requie for effective complex I assembly. EMBO J 27:1736-1746
26. Calvo SE, Tucker EJ, Compton AG et al (2010) High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency. Nat Genet 42:851-858
27. Camaschella C, Campanella A, DeFalco L et al (2007) The human counterpart of zebrafish shiraz shows sideroblastic-like microcytic anemia and iron overload. Blood 110:1353-1358
28. Cameron JM, Levandovskiy V, Mackay N et al (2011a) Complex V TMEM70 deficiency results in mitochondrial nucleoid disorganization. Mitochondrion 11:191-199
29. Cameron JM, Janer A, Levandovskiy V et al (2011b) Mutations in iron-sulfur cluster scaffold genes NFU1 and BOLA3 cause a fatal deficiency of multiple respiratory chain and 2-oxoacid dehydrogenase enzymes. Am J Hum Genet 89:486-495
30. Campuzano V, Montermini L, Molt' MD et al (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271:1423-1427
31. Capaldi RA (1982) Arrangement of proteins in the mitochondrial inner membrane. Biochim Biophys Acta 694:291-306
32. Carrol J, Fearnley IM, Skehel JM et al (2006) Bovine complex I is a complex of 45 different subunits. J Biol Chem 281:32724-32727
33. Chance B, Williams GR (1955) A method for the localization of sites for oxidative phosphorylation. Nature 176:250-254
34. Cizkova A, Stranecky V, Mayr JA et al (2008) TMEM70 mutations cause isolated ATP synthase deficiency and neonatal mitochondrial encephalocardiomyopathy. Nat Genet 40:1288-1290
35. Coenen MJ, Smeitink JA, Smeets R, Trijbels FJ, van den Heuvel LP (2005) Mutation detection in four candidate genes (OXA1L, MRS2L, YME1L and MIPEP) for combined deficiencies in the oxidative phosphorylation system. J Inherit Metab Dis 28:1091-1097
36. Collinson IR, Skehel JM, Fearnley IM, Runswick MJ, Walker JE (1996) The F1F0-ATPase complex from bovine heart mitochondria: the molar ratio of the subunits in the stalk region linking the F1 and F0 domains. Biochemistry 35:12640-12646
37. Cree LM, Samuels DC, Chinnery PF (2009) The inheritance of pathogenic mitochondrial DNA mutations. Biochim Biophys Acta 1792:1097-1102
38. Cruciat CM, Hell K, Folsch H, Neupert W, Stuart RA (1999) Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc(1) complex. EMBO J 18:5226-5233
39. Darley-Usmar VM, Georgevich G, Capaldi RA (1984) Reaction of thionitrobenzoate-modified yeast cytochrome c with monomeric and dimeric forms of beef heart cytochrome c oxidase. FEBS Lett 166:131-135
40. De Lonlay P, Valnot I, Barrientos A et al (2001) A mutant mitochondrial respiratory chain assembly protein causes complex III deficiency in patients with tubulopathy, encephalopathy and liver failure. Nat Genet 29:57-60
41. De Meirleir L, Seneca S, Lissens W et al (2004) Respiratory chain complex V deficiency due to a mutation in the assembly gene ATP12. J Med Genet 41:120-124
42. Dell'agnello C, Leo S, Agostino A, Szabadkai G et al (2007) Increased longevity and refractoriness to Ca(2+)-dependent neurodegeneration in Surf1 knockout mice. Hum Mol Genet 16:431-444
43. Devenish RJ, Prescott M, Rodgers AJ (2008) The structure and function of mitochondrial F1F0- ATP synthases. Int Rev Cell Mol Biol 267:1-58
44. 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
45. Dibrov E, Fu S, Lemire BD (1998) The Saccharomyces cerevisiae TCM62 gene encodes a chaperone necessary for the assembly of the mitochondrial succinate dehydrogenase (complex II). J Biol Chem 273:32042
46. DiMauro S, Davidzon G (2005) Mitochondrial DNA and disease. Ann Med 37:222-232
47. Distelmaier F, Koopman WJ, van den Heuvel LP et al (2009) Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease. Brain 132:833-842
48. Dunning CJ, McKenzie M, Sugiana C et al (2007) Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J 1126:3227-3237
49. Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465:441-445
50. Ernster L, Dallner G (1995) Biochemical, physiological and medical aspects of ubiquinone function. Biochim Biophys Acta 1271:195-204
51. Fassone E, Duncan AJ, Taanman JW et al (2010) FOXRED1, encoding an FAD-dependent oxidoreductase complex-I-specific molecular chaperone, is mutated in infantile onset mitochondrial encephalopathy. Hum Mol Genet 19:4837-4847
52. Feichtinger RG, Zimmermann F, Mayr JA et al (2010) Low aerobic mitochondrial energy metabolism in poorly- or undifferentiated neuroblastoma. BMC Cancer 10:149
53. Fernandez-Vizarra E, Bugiani M, Goffrini P et al (2007) Impaired complex III assembly associated with BCS1L gene mutations in isolated mitochondrial encephalopathy. Hum Mol Genet 16:1241-1252
54. Fernandez-Vizarra E, Tiranti V, Zeviani M (2009) Assembly of the oxidative phosphorylation system in humans: what we have learned by studying its defects. Biochim Biophys Acta 1793:200-211
55. 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
56. Fowler LR, Richardson SH (1963) Studies on the electron transfer system. On the mechanism of reconstitution of the mitochondrial electron transfer system. J Biol Chem 238:456-463
57. Gerards M, Sluiter W, van den Bosch BJ et al (2010) Defective complex I assembly due to C20orf7 mutations as a new cause of Leigh syndrome. J Med Genet 47:507-512
58. Gerards M, van den Bosch BJ, Danhauser K et al (2011) Riboflavin-responsive oxidative phosphorylation complex I deficiency caused by defective ACAD9: new function for an old gene. Brain 134:210-219
59. Ghezzi D, Zeviani M (2011) Mitochondrial disorders: nuclear gene mutations. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester. DOI: 10.1002/9780470015902
60. Ghezzi D, Goffrini P, Uziel G et al (2009) SDHAF1, encoding a LYR complex-II specific assembly factor, is mutated in SDH-defective infantile leukoencephalopathy. Nat Genet 41:654-656
61. Ghezzi D, Arzuf fiP, Zordan M et al (2011) Mutations in TTC19 cause mitochondrial complex III deficiency and neurological impairment in humans and flies. Nat Genet 43:259-263
62. Gilkerson RW, Selker JM, Capaldi RA (2003) The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett 546:355-358
63. Gonzalez-Cabo P, Vazquez-Manrique RP, Garcia-Gimeno MA, Sanz P, Palau F (2005) Frataxin interacts functionally with mitochondrial electron transport chain proteins. Hum Mol Genet 14:2091-2098
64. Grossman LI, Lomax MI (1997) Nuclear genes for cytochrome c oxidase. Biochim Biophys Acta 1352:174-192
65. Haack TB, Danhauser K, Haberberger B et al (2010) Exome sequencing identi fies ACAD9 mutations as a cause of complex I deficiency. Nat Genet 42:1131-1134
66. Hackenbrock CR, Chazotte B, Gupte SS (1986) The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J Bioenerg Biomembr 18:331-368
67. Hagerhall C (1997) Succinate: quinone oxidoreductases. Variations on a conserved theme. Biochim Biophys Acta 1320:107-141
68. Hagerhall C, Hederstedt L (1997) A structural model for the membrane-integral domain of succinate: quinone oxidoreductases. FEBS Lett 389:25
69. Hao HX, Khalimonchuk O, Schraders M et al (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 28:1139-1142
70. Hederstedt L (2002) Succinate:quinone oxidoreductase in the bacteria Paracoccus denitrificans and Bacillus subtilis . Biochim Biophys Acta 1553:74-83
71. Hinson JT, Fantin VR, Schonberger J et al (2007) Missense mutations in the BCS1L gene as a cause of the Bjornstad syndrome. N Engl J Med 356:809-819
72. Honzik T, Tesarova M, Mayr JA et al (2010) Mitochondrial encephalocardio-myopathy with early neonatal onset due to TMEM70 mutation. J Arch Dis Child 95:296-301
73. Houstek J, Klement P, Floryk D et al (1999) A novel deficiency of mitochondrial ATPase of nuclear origin. Hum Mol Genet 8:1967-1974
74. Houstek J, Pickova A, Vojtiskova A, Mracek T, Pecina P, Jesina P (2006) Mitochondrial diseases and genetic defects of ATP synthase. Biochim Biophys Acta 1757:1400-1405
75. Houstek J, Kmoch S, Zeman J (2009) TMEM70 protein - a novel ancillary factor of mammalian ATP synthase. Biochim Biophys Acta 1787:529-532
76. Huigsloot M, Nijtmans LG, Szklarczyk R et al (2011) A mutation in C2orf64 causes impaired cytochrome c oxidase assembly and mitochondrial cardiomyopathy. Am J Hum Genet 88:488-493
77. Hunte C, Zickermann V, Brandt U (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329:448-451
78. Huynen MA, Spronk CA, Gabaldon T, Snel B (2005) Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin. FEBS Lett 579:591-596
79. Iwata S, Lee JW, Okada K et al (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281:64-71
80. Janssen RJ, Nijtmans LG, van den Heuvel LP, Smeitink JA (2006) Mitochondrial complex I: structure, function and pathology. J Inherit Metab Dis 29:499-515
81. Jiang X, Wang X (2004) Cytochrome c-mediated apoptosis. Annu Rev Biochem 73:87-106
82. Jonckheere A, Hogeveen M, Nijtmans L et al (2008) A novel mitochondrial ATP8 (MT-ATP8) gene mutation in a patient with apical hypertrophic cardiomyopathy and neuropathy. J Med Genet 45:129-133
83. Joost K, Rodenburg R, Piirsoo A et al (2010) A novel mutation in the SCO2 gene in a neonate with early-onset cardioencephalomyopathy. Pediatr Neurol 42:227-230
84. Kim KD, Chung WH, Kim HJ, Lee KC, Roe JH (2010) Monothiol glutaredoxin Grx5 interacts with Fe-S scaffold proteins Isa1 and Isa2 and supports Fe-S assembly and DNA integrity in mitochondria of fission yeast. Biochem Biophys Res Commun 392:467-472
85. Ko YH, Delannoy M, Hullihen J, Chiu W, Pedersen PL (2003) Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J Biol Chem 278:12305-12309
86. Kollberg G, Tulinius M, Melberg A et al (2009) Clinical manifestation and a new ISCU mutation in iron-sulphur cluster deficiency myopathy. Brain 132:2170-2179
87. Koopman WJ, Nijtmans LG, Dieteren CE et al (2010) Mammalian mitochondrial complex I: biogenesis, regulation and reactive oxygen species generation. Antioxid Redox Signal 12:1431-1470
88. Krause F, Scheckhuber CQ, Werner A, Rexroth S, Reifschneider NH, Dencher NA, Osiewacz HD (2004) Supramolecular organization of cytochrome c oxidaseand alternative oxidasedependent respiratory chains in the filamentous fungus Podospora anserine. J Biol Chem 279:26453-26461
89. Krause F, Reifschneider NH, Goto S, Dencher NA (2005) Active oligomeric ATP synthases in mammalian mitochondria. Biochem Biophys Res Commun 329:583-590
90. 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
91. Lamantea E, Carrara F, Mariotti C, Morandi L, Tiranti V, Zeviani M (2002) A novel nonsense mutation (Q352X) in the mitochondrial cytochrome b gene associated with a combined deficiency of complexes I and III. Neuromuscul Disord 12:49-52
92. Lancaster CR, Kroger A, Auer M, Michel H (1999) Structure of fumarate reductase from Wolinella succinogenes at 2.2 A resolution. Nature 402:377-385
93. Lazarou M, McKenzie M, Ohtake A, Thorburn DR, Ryan MT (2007) Analysis of the assembly pro files for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Mol Cell Biol 27:4228-4237
94. Lazarou M, Smith SM, Thorburn DR, Ryan MT, McKenzie M (2009) Assembly of nuclear DNAencoded subunits into mitochondrial complex IV, and their preferential integration into supercomplex forms in patient mitochondria. FEBS J 276:6701-6713
95. Leary SC, Kaufman BA, Pellecchia G et al (2004) Human SCO1 and SCO2 have independent, cooperative functions in copper delivery to cytochrome c oxidase. Hum Mol Genet 13:1839-1848
96. Leary SC, Cobine PA, Kaufman BA et al (2007) The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis. Cell Metab 5:9-20
97. Lee SJ, Yamashita E, Abe T et al (2001) Intermonomer interactions in dimer of bovine heart cytochrome c oxidase. Acta Crystallogr D: Biol Crystallogr 57:941-947
98. Lenaz G, Genova ML (2010) Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid Redox Signal 12:961-1008
99. Lenaz G, Baracca A, Carelli V, D'Aurelio M, Sgarbi G, Solaini G (2004) Bioenergetics of mitochondrial diseases associated with mtDNA mutations. Biochim Biophys Acta 1658:89-94
100. Leveen P, Kotarsky H, Morgelin M, Karikoski R, Elmer E, Fellman V (2011) The GRACILE mutation introduced into Bcs1l causes postnatal complex III deficiency: a viable mouse model for mitochondrial hepatopathy. Hepatology 53:437-447
101. Li K, Tong WH, Hughes RM, Rouault TA (2006) Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron-sulfur cluster assembly. J Biol Chem 281:12344-12351
102. Li H, Gakh O, Smith DY, Isaya G (2009) Oligomeric yeast frataxin drives assembly of core machinery for mitochondrial iron-sulfur cluster synthesis. J Biol Chem 284:21971-21980
103. Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem Sci 25:352-356
104. Lill R, Muhlenhoff U (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669-700
105. Loeffen JL, Smeitink JA, Trijbels JM et al (2000) Isolated complex I deficiency in children: clinical, biochemical and genetic aspects. Hum Mutat 15:123-134
106. Mancuso C, Scapagini G, Curr' D et al (2007) Mitochondrial dysfunction, free radical generation and cellular stress response in neurodegenerative disorders. Front Biosci 12:1107-1123
107. Mashkevich G, Repetto B, Glerum DM, Jin C, Tzagoloff A (1997) SHY1, the yeast homolog of the mammalian SURF-1 gene, encodes a mitochondrial protein required for respiration. J Biol Chem 272:14356-14364
108. Massa V, Fernandez-Vizarra E, Alshahwan S et al (2008) Severe infantile encephalomyopathy caused by a mutation in COX6B1, a nucleus-encoded subunit of cytochrome c oxidase. Am J Hum Genet 82:1281-1289
109. Mayr JA, Havlickova V, Zimmermann F et al (2010) Mitochondrial ATP synthase deficiency due to a mutation in the ATP5E gene for the F1 epsilon subunit. Hum Mol Genet 19:3430-3439
110. McFarland R, Turnbull DM (2009) Batteries not included: diagnosis and management of mitochondrial disease. J Intern Med 265:210-228
111. McKenzie M, Ryan MT (2010) Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life 62:497-502
112. Mick DU, Wagner K, van der Laan M et al (2007) Shy1 couples Cox1 translational regulation to cytochrome c oxidase assembly. EMBO J 26:4347-4358
113. Mochel F, Knight MA, Tong WH et al (2008) Splice mutation in the iron-sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance. Am J Hum Genet 82:652-660
114. Mootha VK, Lepage P, Miller K (2003) Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc Natl Acad Sci USA 100:605-610
115. Mulkidjanian AY, Makarova KS, Galperin MY, Koonin EV (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol 5:892-899
116. Munnich A, Rustin P (2001) Clinical spectrum and diagnosis of mitochondrial disorders. Am J Med Genet 106:4-17
117. Nakamura K, Yamaki M, Sarada M et al (1996) Two hydrophobic subunits are essential for the heme b ligation and functional assembly of complex II (succinate-ubiquinone oxidoreductase) from Escherichia coli . J Biol Chem 271:521-527
118. Nargang FE, Preuss M, Neupert W, Herrmann JM (2002) The Oxa1 protein forms a homooligomeric complex and is an essential part of the mitochondrial export translocase in Neurospora crassa . J Biol Chem 277:12846-12853
119. Nijtmans LG, Klement P, Houstek J, van den Bogert C (1995) Assembly of mitochondrial ATP synthase in cultured human cells: implications for mitochondrial diseases. Biochim Biophys Acta 1272:190-198
120. Nijtmans LG, Taanman JW, Muijsers AO, Speijer D, Van den Bogert C (1998) Assembly of cytochrome- c oxidase in cultured human cells. Eur J Biochem 254:389-394
121. Nobrega FG, Nobrega MP, Tzagoloff A (1992) BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae . EMBO J 11:3821-3829
122. Nouws J, Nijtmans L, Houten SM et al (2010) Acyl-CoA dehydrogenase 9 is required for the biogenesis of oxidative phosphorylation complex I. Cell Metab 12:283-294
123. 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
124. Pagliarini DJ, Calvo SE, Chang B et al (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112-123
125. Papadopoulou LC, Sue CM, Davidson MM et al (1999) Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat Genet 23:333-337
126. Paumard P, Vaillier J, Coulary B et al (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J 21:221-230
127. Pecina P, Houstkova H, Hansikova H, Zeman J, Houstek J (2004) Genetic defects of cytochrome c oxidase assembly. Physiol Res 53:S213-S223
128. Piekutowska-Abramczuk D, Magner M, Popowska E et al (2009) SURF1 missense mutations promote a mild Leigh phenotype. Clin Genet 76:195-204
129. Pondarre C, Antiochos BB, Campagna DR et al (2006) The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulfur cluster biogenesis. Hum Mol Genet 15:953-964
130. Pronicki M, Kowalski P, Piekutowska-Abramczuk D et al (2010) A homozygous mutation in the SCO2 gene causes a spinal muscular atrophy like presentation with stridor and respiratory insuf ficiency. Eur J Paediatr Neurol 14:253-260
131. Rabl R, Soubannier V, Scholz R et al (2009) Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J Cell Biol 185:1047-1063
132. Rak M, Gokova S, Tzagoloff A (2011) Modular assembly of yeast mitochondrial ATP synthase. EMBO J 30:920-930
133. Remacle C, Barbieri MR, Cardol P, Hamel PP (2008) Eukaryotic complex I: functional diversity and experimental systems to unravel the assembly process. Mol Genet Genomics 280: 93-110
134. Robinson KM, Lemire BD (1996) Covalent attachment of FAD to the yeast succinate dehydrogenase flavoprotein requires import into mitochondria, presequence removal, and folding. J Biol Chem 271:4055-4060
135. Rouault TA, Tong WH (2008) Iron-sulfur cluster biogenesis and human disease. Trends Genet 24:398-407
136. Saada A, Edvardson S, Rapoport M et al (2008) C6ORF66 is an assembly factor of mitochondrial complex I. Am J Hum Genet 82:32-38
137. Saada A, Vogel RO, Hoefs SJ et al (2009) Mutations in NDUFAF3 (C3ORF60), encoding an NDUFAF4 (C6ORF66)-interacting complex I assembly protein, cause fatal neonatal mitochondrial disease. Am J Hum Genet 84:718-727
138. Saada A, Edvardson S, Shaag A et al (2012) Combined OXPHOS complex I and IV defect, due to mutated complex I assembly factor C20ORF7. J Inherit Metab Dis 35(1):125-131
139. Sasarman F, Brunel-Guitton C, Antonicka H et al (2010) LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol Biol Cell 21:1315-1323
140. Schaefer AM, Taylor RW, Turnbull DM, Chinnery PF (2004) The epidemiology of mitochondrial disorders: past, present and future. Biochim Biophys Acta 1659:115-120
141. Schafer E, Dencher NA, Vonck J, Parcej DN (2007) Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry 46:12579-12585
142. Schagger H (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta 1555:154-159
143. Schagger H, Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19:1777-1783
144. Schagger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223-231
145. Schatz G (1968) Impaired binding of mitochondrial adenosine triphosphatase in the cytoplasmic petite mutant of Saccharomyces cerevisiae . J Biol Chem 243:2192-2199
146. Scheffler IE, Yadava N, Potluri P (2004) Molecular genetics of complex I-deficient Chinese hamster cell lines. Biochim Biophys Acta 1659:160-171
147. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663-670
148. Schneider D, Pohl T, Walter J et al (2008) Assembly of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I). Biochim Biophys Acta 1777:735-739
149. Schon EA, Santra S, Pallotti F, Girvin ME (2001) Pathogenesis of primary defects in mitochondrial ATP synthesis. Semin Cell Dev Biol 12:441-448
150. Seeger J, Schrank B, Pyle A et al (2010) Clinical and neuropathological findings in patients with TACO1 mutations. Neuromuscul Disord 20:720-724
151. Sheftel AD, Stehling O, Pierik AJ et al (2009) Human ind1, an iron-sulfur cluster assembly factor for respiratory complex I. Mol Cell Biol 29:6059-6073
152. Sperl W, Jesina P, Zeman J et al (2006) Deficiency of mitochondrial ATP synthase of nuclear genetic origin. Neuromuscul Disord 16:821-829
153. Spiegel R, Khayat M, Shalev SA et al (2011) TMEM70 mutations are a common cause of nuclear encoded ATP synthase assembly defect: further delineation of a new syndrome. J Med Genet 48:177-182
154. Stiburek L, Vesela K, Hansikova H et al (2005) Tissue-specific cytochrome c oxidase assembly defects due to mutations in SCO2 and SURF1. Biochem J 392:625-632
155. Stiburek L, Hansikova H, Tesarova M, Cerna L, Zeman J (2006) Biogenesis of eukaryotic cytochrome c oxidase. Physiol Res 55:S27-S41
156. Stiburek L, Fornuskova D, Wenchich L, Pejznochova M, Hansikova H, Zeman J (2007) Knockdown of human Oxa1l impairs the biogenesis of F1Fo-ATP synthase and NADH:ubiquinone oxidoreductase. J Mol Biol 374:506-516
157. Stiburek L, Vesela K, Hansikova H, Hulkova H, Zeman J (2009) Loss of function of Sco1 and its interaction with cytochrome c oxidase. Am J Physiol Cell Physiol 296:C1218-C1226
158. Sugiana C, Pagliarini DJ, McKenzie M et al (2008) Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am J Hum Genet 83:468-478
159. Sun F, Huo X, Zhai Y et al (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121:1043-1057
160. Tatuch Y, Robinson BH (1993) The mitochondrial DNA mutation at 8993 associated with NARP slows the rate of ATP synthesis in isolated lymphoblast mitochondria. Biochem Biophys Res Commun 192:124-128
161. Thorburn DR, Sugiana C, Salemi R et al (2004) Biochemical and molecular diagnosis of mitochondrial respiratory chain disorders. Biochim Biophys Acta 1659:121-128
162. Tiranti V, Hoertnagel K, Carrozzo R et al (1998) Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency. Am J Hum Genet 63:1609-1621
163. Tiranti V, Galimberti C, Nijtmans L, Bovolenta S, Perini MP, Zeviani M (1999) Characterization of SURF-1 expression and Surf-1p function in normal and disease conditions. Hum Mol Genet 8:2533-2540
164. Tong WH, Rouault TA (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis. Cell Metab 3:199-210
165. Tsukihara T, Aoyama H, Yamashita E et al (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272:1136-1144
166. Tzagoloff A (1969) Assembly of the mitochondrial membrane system. II. Synthesis of the mitochondrial adenosine triphosphatase, F1. J Biol Chem 244:5027-5033
167. Tzagoloff A, Jang J, Glerum M, Wu M (1996) FLX1 codes for a carrier protein involved in maintaining a proper balance of flavin nucleotides in yeast mitochondria. J Biol Chem 271:7392-7397
168. Ugalde C, Janssen RJ, van den Heuvel LP, Smeitink JA, Nijtmans LG (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
169. Valnot I, Osmond S, Gigarel N et al (2000) Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am J Hum Genet 67:1104-1109
170. van Nederveen FH, Gaal J, Favier J et al (2009) An immunohistochemical procedure to detect patients with paraganglioma and phaeochromocytoma with germline SDHB, SDHC, or SDHD gene mutations: a retrospective and prospective analysis. Lancet Oncol 10:764-771
171. Visapaa I, Fellman V, Vesa J et al (2002) GRACILE syndrome, a lethal metabolic disorder with iron overload, is caused by a point mutation in BCS1L. Am J Hum Genet 71:863-876
172. Vogel RO, Smeitink JA, Nijtmans LG (2007) Human mitochondrial complex I assembly: a dynamic and versatile process. Biochim Biophys Acta 1767:1215-1227
173. Wagner K, Perschil I, Fichter CD, van der Laan M (2010) Stepwise assembly of dimeric F(1)F(o)- ATP synthase in mitochondria involves the small F(o)-subunits k and i. Mol Biol Cell 21:1494-1504
174. Wang ZG, Sheluho D, Gatti DL, Ackerman SH (2000) The alpha-subunit of the mitochondrial F(1) ATPase interacts directly with the assembly factor Atp12p. EMBO J 19:1486-1493
175. Wang ZG, White PS, Ackerman SH (2001) Atp11p and Atp12p are assembly factors for the F(1)- ATPase in human mitochondria. J Biol Chem 276:30773-30778
176. Weraarpachai W, Antonicka H, Sasarman F et al (2009) Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat Genet 41:833-837
177. West AP, Brodsky IE, Rahner C et al (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472:476-480
178. Williams SL, Valnot I, Rustin P, Taanman JW (2004) Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1, or SURF1. J Biol Chem 279:7462-7469
179. Wittig I, Schagger H (2009) Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim Biophys Acta 1787:672-680
180. Wittig I, Carrozzo R, Santorelli FM, Schagger H (2006) Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 1757:1066-1072
181. Xu F, Ackerley C, Maj MC et al (2008) Disruption of a mitochondrial RNA-binding protein gene results in decreased cytochrome b expression and a marked reduction in ubiquinol-cytochrome c reductase activity in mouse heart mitochondria. Biochem J 416:15-26
182. Yankovskaya V, Horse field R, Tornroth S et al (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299:700-704
183. Yoshikawa S, Shinzawa-Itoh K, Tsukihara T (1998) Crystal structure of bovine heart cytochrome c oxidase at 2.8 A resolution. J Bioenerg Biomembr 30:7-14
184. Zara V, Conte L, Trumpower BL (2007) Identification and characterization
185. Zara V, Conte L, Trumpower BL (2009) Biogenesis of the yeast cytochrome bc(1) complex. Biochim Biophys Acta 1793:89-96
186. Zick M, Rabl R, Reichert AS (2009) Cristae formation-linking ultrastructure and function of mitochondria. Biochim Biophys Acta 1793:5-19