Molecular base of biochemical complex I deficiency

Mitochondrion

Volumn 12, Issue 5, 2012, Pages 520-532

  Hoefs, Saskia J G ^a   Rodenburg, Richard J ^a   Smeitink, Jan A M ^a   van den Heuvel, Lambert P ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Complex I deficiency; Genetic defects; Mitochondrial disorder

Indexed keywords

MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

BIOGENESIS; BIPOLAR DISORDER; CELL METABOLISM; DEGENERATIVE DISEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; ENZYME DEFICIENCY; ENZYME LOCALIZATION; FRIEDREICH ATAXIA; GENE MUTATION; GENETIC VARIABILITY; HIGH THROUGHPUT SCREENING; HOMOZYGOSITY; HUMAN; MITOCHONDRIAL GENOME; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE) DEFICIENCY; RESPIRATORY CHAIN; REVIEW;

ELECTRON TRANSPORT COMPLEX I; ENERGY METABOLISM; HUMANS; MITOCHONDRIAL DISEASES;

EID: 84864567425     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.07.106     Document Type: Review

References (155)

1. Acin-Perez R., Fernandez-Silva P., Peleato M.L., Perez-Martos A., Enriquez J.A. Respiratory active mitochondrial supercomplexes. Mol. Cell 2008, 32:529-539.
2. Andreazza A.C., Shao L., Wang J.F., Young L.T. Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch. Gen. Psychiatry 2010, 67:360-368.
3. Andreu A.L., Tanji K., Bruno C., Hadjigeorgiou G.M., Sue C.M., Jay C., Ohnishi T., Shanske S., Bonilla E., DiMauro S. Exercise intolerance due to a nonsense mutation in the mtDNA ND4 gene. Ann. Neurol. 1999, 45:820-823.
4. Angell J.E., Lindner D.J., Shapiro P.S., Hofmann E.R., Kalvakolanu D.V. Identification of GRIM-19, a novel cell death-regulatory gene induced by the interferon-beta and retinoic acid combination, using a genetic approach. J. Biol. Chem. 2000, 275:33416-33426.
5. Arenas J., Campos Y., Ribacoba R., Martin M.A., Rubio J.C., Ablanedo P., Cabello A. Complex I defect in muscle from patients with Huntington's disease. Ann. Neurol. 1998, 43:397-400.
6. Arenas J., Campos Y., Bornstein B., Ribacoba R., Martin M.A., Rubio J.C., Santorelli F.M., Zeviani M., DiMauro S., Garesse R. A double mutation (A8296G and G8363A) in the mitochondrial DNA tRNA (Lys) gene associated with myoclonus epilepsy with ragged-red fibers. Neurology 1999, 52:377-382.
7. Atorino L., Silvestri L., Koppen M., Cassina L., Ballabio A., Marconi R., Langer T., Casari G. Loss of m-AAA protease in mitochondria causes complex I deficiency and increased sensitivity to oxidative stress in hereditary spastic paraplegia. J. Cell Biol. 2003, 163:777-787.
8. Au H.C., Seo B.B., Matsuno-Yagi A., Yagi T., Scheffler I.E. The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4354-4359.
9. Baker M.E., Grundy W.N., Elkan C.P. A common ancestor for a subunit in the mitochondrial proton-translocating NADH:ubiquinone oxidoreductase (complex I) and short-chain dehydrogenases/reductases. Cell. Mol. Life Sci. 1999, 55:450-455.
10. Bender A., Krishnan K.J., Morris C.M., Taylor G.A., Reeve A.K., Perry R.H., Jaros E., Hersheson J.S., Betts J., Klopstock T., Taylor R.W., Turnbull D.M. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 2006, 38:515-517.
11. Benit P., Chretien D., Kadhom N., de Lonlay-Debeney P., Cormier-Daire V., Cabral A., Peudenier S., Rustin P., Munnich A., Rotig A. Large-scale deletion and point mutations of the nuclear NDUFV1 and NDUFS1 genes in mitochondrial complex I deficiency. Am. J. Hum. Genet. 2001, 68:1344-1352.
12. Benit P., Beugnot R., Chretien D., Giurgea I., de Lonlay-Debeney P., Issartel J.P., Corral-Debrinski M., Kerscher S., Rustin P., Rotig A., Munnich A. Mutant NDUFV2 subunit of mitochondrial complex I causes early onset hypertrophic cardiomyopathy and encephalopathy. Hum. Mutat. 2003, 21:582-586.
13. Benit P., Slama A., Cartault F., Giurgea I., Chretien D., Lebon S., Marsac C., Munnich A., Rotig A., Rustin P. Mutant NDUFS3 subunit of mitochondrial complex I causes Leigh syndrome. J. Med. Genet. 2004, 41:14-17.
14. Berger I., Hershkovitz E., Shaag A., Edvardson S., Saada A., Elpeleg O. Mitochondrial complex I deficiency caused by a deleterious NDUFA11 mutation. Ann. Neurol. 2008, 63:405-408.
15. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 2000, 3:1301-1306.
16. Blakely E.L., Mitchell A.L., Fisher N., Meunier B., Nijtmans L.G., Schaefer A.M., Jackson M.J., Turnbull D.M., Taylor R.W. A mitochondrial cytochrome b mutation causing severe respiratory chain enzyme deficiency in humans and yeast. FEBS J. 2005, 272:3583-3592.
17. Bradley J.L., Blake J.C., Chamberlain S., Thomas P.K., Cooper J.M., Schapira A.H. Clinical, biochemical and molecular genetic correlations in Friedreich's ataxia. Hum. Mol. Genet. 2000, 9:275-282.
18. Brandt U. Proton-translocation by membrane-bound NADH:ubiquinone-oxidoreductase (complex I) through redox-gated ligand conduction. Biochim. Biophys. Acta 1997, 1318:79-91.
19. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 2006, 75:69-92.
20. Brandt U., Kerscher S., Drose S., Zwicker K., Zickermann V. Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism?. FEBS Lett. 2003, 545:9-17.
21. Bridwell-Rabb J., Winn A.M., Barondeau D.P. Structure-function analysis of Friedreich's ataxia mutants reveals determinants of frataxin binding and activation of the Fe-S assembly complex. Biochemistry 2011, 50:7265-7274.
22. Brown M.D., Voljavec A.S., Lott M.T., Torroni A., Yang C.C., Wallace D.C. Mitochondrial DNA complex I and III mutations associated with Leber's hereditary optic neuropathy. Genetics 1992, 130:163-173.
23. Brown M.D., Starikovskaya E., Derbeneva O., Hosseini S., Allen J.C., Mikhailovskaya I.E., Sukernik R.I., Wallace D.C. The role of mtDNA background in disease expression: a new primary LHON mutation associated with Western Eurasian haplogroup. J. Hum. Genet. 2002, 110:130-138.
24. Budde S.M., van den Heuvel L.P., Janssen A.J., Smeets R.J., Buskens C.A., DeMeirleir L., van Coster R., Baethmann M., Voit T., Trijbels J.M., Smeitink J.A. Combined enzymatic complex I and III deficiency associated with mutations in the nuclear encoded NDUFS4 gene. Biochem. Biophys. Res. Commun. 2000, 275:63-68.
25. Bych K., Kerscher S., Netz D.J., Pierik A.J., Zwicker K., Huynen M.A., Lill R., Brandt U., Balk J. The iron-sulphur protein Ind1 is required for effective complex I assembly. EMBO J. 2008, 27:1736-1746.
26. Calvaruso M.A., Smeitink J., Nijtmans L. Electrophoresis techniques to investigate defects in oxidative phosphorylation. Methods 2008, 46:281-287.
27. Calvo S.E., Tucker E.J., Compton A.G., Kirby D.M., Crawford G., Burtt N.P., Rivas M., Guiducci C., Bruno D.L., Goldberger O.A., Redman M.C., Wiltshire E., Wilson C.J., Altshuler D., Gabriel S.B., Daly M.J., Thorburn D.R., Mootha V.K. High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency. Nat. Genet. 2010, 42:851-858.
28. Carroll J., Fearnley I.M., Shannon R.J., Hirst J., Walker J.E. Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol. Cell. Proteomics 2003, 2:117-126.
29. Carroll J., Fearnley I.M., Skehel J.M., Shannon R.J., Hirst J., Walker J.E. Bovine complex I is a complex of 45 different subunits. J. Biol. Chem. 2006, 281:32724-32727.
30. Chen R., Fearnley I.M., Peak-Chew S.Y., Walker J.E. The phosphorylation of subunits of complex I from bovine heart mitochondria. J. Biol. Chem. 2004, 279:26036-26045.
31. Chinnery P.F., Brown D.T., Andrews R.M., Singh-Kler R., Riordan-Eva P., Lindley J., Applegarth D.A., Turnbull D.M., Howell N. The mitochondrial ND6 gene is a hot spot for mutations that cause Leber's hereditary optic neuropathy. Brain 2001, 124:209-218.
32. De Rasmo D., Panelli D., Sardanelli A.M., Papa S. cAMP-dependent protein kinase regulates the mitochondrial import of the nuclear encoded NDUFS4 subunit of complex I. Cell. Signal. 2008, 20:989-997.
33. 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.
34. DiMauro S., Bonilla E., De Vivo D.C. Does the patient have a mitochondrial encephalomyopathy?. J. Child Neurol. 1999, 14(Suppl. 1):S23-S35.
35. Distelmaier F., Visch H.J., Smeitink J.A., Mayatepek E., Koopman W.J., Willems P.H. The antioxidant Trolox restores mitochondrial membrane potential and Ca2+-stimulated ATP production in human complex I deficiency. J. Mol. Med. 2009, 87:515-522.
36. Dudkina N.V., Kouril R., Peters K., Braun H.P., Boekema E.J. Structure and function of mitochondrial supercomplexes. Biochim. Biophys. Acta 2010, 179:664-670.
37. 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.
38. Efremov R.G., Baradaran R., Sazanov L.A. The architecture of respiratory complex I. Nature 2010, 465:441-445.
39. Fassone E., Duncan A.J., Taanman J.W., Pagnamenta A.T., Sadowski M.I., Holand T., Qasim W., Rutland P., Calvo S.E., Mootha V.K., Bitner-Glindzicz M., Rahman S. FOXRED1, encoding a FAD-dependent oxidoreductase complex-I specific molecular chaperone, is mutated in infantile-onset mitochondrial encephalopathy. Hum. Mol. Genet. 2010, 19:4837-4847.
40. Fearnley I.M., Walker J.E. Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim. Biophys. Acta 1992, 1140:105-134.
41. Fearnley I.M., Carroll J., Shannon R.J., Runswick M.J., Walker J.E., Hirst J. GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 2001, 276:38345-38348.
42. Fernandez-Moreira D., Ugalde C., Smeets R., Rodenburg R.J., Lopez-Laso E., Ruiz-Falco M.L., Briones P., Martin M.A., Smeitink J.A., Arenas J. X-linked NDUFA1 gene mutations associated with mitochondrial encephalomyopathy. Ann. Neurol. 2007, 61:73-83.
43. Fischer J.C., Ruitenbeek W., Stadhouders A.M., Trijbels J.M., Sengers R.C., Janssen A.J., Veerkamp J.H. Investigation of mitochondrial metabolism in small human skeletal muscle biopsy specimens. Improvement of preparation procedure. Clin. Chim. Acta 1985, 145:89-99.
44. Flinn L., Mortiboys H., Volkmann K., Koster R.W., Ingham P.W., Bandmann O. Complex I deficiency and dopaminergic neuronal cell loss in parkin-deficient zebrafish (Danio rerio). Brain 2009, 132:1613-1623.
45. Friedrich T. Complex I: a chimaera of a redox and conformation-driven proton pump?. J. Bioenerg. Biomembr. 2001, 33:169-177.
46. Friedrich T., Bottcher B. The gross structure of the respiratory complex I: a Lego System. Biochim. Biophys. Acta 2004, 1608:1-9.
47. Gabaldon T., Rainey D., Huynen M.A. Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (Complex I). J. Mol. Biol. 2005, 348:857-870.
48. Gerards M., van den Bosch B.J., Danhauser K., Serre V., van Weeghel M., Wanders R.J., Nicolaes G.A., Sluiter W., Schoonderwoerd K., Scholte H.R., Prokisch H., Rotig A., de Coo I.F., Smeets H.J. Riboflavin-responsive oxidative phosphorylation complex I deficiency caused by defective ACAD9: new function for an old gene. Brain 2011, 134:210-219.
49. Haack T.B., Haberberger B., Frisch E.M., Wieland T., Iuso A., Gorza M., Strecker V., Graf E., Mayr J.A., Herberg U., Hennermann J.B., Klopstock T., Kuhn K.A., Ahting U., Sperl W., Wilichowski E., Hoffmann G.F., Tesarova M., Hansikova H., Zeman J., Plecko B., Zeviani M., Wittig I., Strom T.M., Schuelke M., Freisinger P., Meitinger T., Prokisch H. Molecular diagnosis in mitochondrial complex I deficiency using exome sequencing. J. Med. Genet. 2012, 49:277-283.
50. Haack T.B., Madignier F., Herzer M., Lamantea E., Danhauser K., Invernizzi F., Koch J., Freitag M., Drost R., Hillier I., Haberberger B., Mayr J.A., Ahting U., Tiranti V., Rötig A., Iuso A., Horvath R., Tesarova M., Baric I., Uziel G., Rolinski B., Sperl W., Meitinger T., Zeviani M., Freisinger P., Prokisch H. Mutation screening of 75 candidate genes in 152 complex I deficiency cases identifies pathogenic variants in 16 genes including NDUFB9. J. Med. Genet. 2012, 49:83-89.
51. Hayashi T., Ishimori C., Takahashi-Niki K., Taira T., Kim Y.C., Maita H., Maita C., Ariga H., Iguchi-Ariga S.M. DJ-1 binds to mitochondrial complex I and maintains its activity. Biochem. Biophys. Res. Commun. 2009, 390:667-672.
52. Heidari M.M., Houshmand M., Hosseinkhani S., Nafissi S., Scheiber-Mojdehkar B., Khatami M. A novel mitochondrial heteroplasmic C13806A point mutation associated with Iranian Friedreich's ataxia. Cell. Mol. Neurobiol. 2009, 29:225-233.
53. Hinchliffe P., Sazanov L.A. Organization of iron-sulfur clusters in respiratory complex I. Science 2005, 309:771-774.
54. Hirst J., Carroll J., Fearnley I.M., Shannon R.J., Walker J.E. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 2003, 1604:135-150.
55. Hirst J., King M.S., Pryde K.R. The production of reactive oxygen species by complex I. Biochem. Soc. Trans. 2008, 36:976-980.
56. Hoefs S.J., Dieteren C.E., Distelmaier F., Janssen R.J., Epplen A., Swarts H.G., Forkink M., Rodenburg R.J., Nijtmans L.G., Willems P.H., Smeitink J.A., van den Heuvel L.P. NDUFA2 complex I mutation leads to Leigh disease. Am. J. Hum. Genet. 2008, 82:1306-1315.
57. Hoefs S.J., Dieteren C.E., Rodenburg R.J., Naess K., Bruhn H., Wibom R., Wagena E., Willems P.H., Smeitink J.A., Nijtmans L.G., van den Heuvel L.P. Baculovirus complementation restores a novel NDUFAF2 mutation causing complex I deficiency. Hum. Mutat. 2009, 30:E728-E736.
58. Hoefs S.J., Skjeldal O.H., Rodenburg R.J., Nedregaard B., van Kaauwen E.P., Spiekerkotter U., Kleist-Retzow J.C., Smeitink J.A., Nijtmans L.G., van den Heuvel L.P. Novel mutations in the NDUFS1 gene cause low residual activities in human complex I deficiencies. Mol. Genet. Metab. 2010, 100:251-256.
59. Hoefs S.J., van Spronsen F.J., Lenssen E.W., Nijtmans L.G., Rodenburg R.J., Smeitink J.A., van den Heuvel L.P. NDUFA10 mutations cause complex I deficiency in a patient with Leigh disease. Eur. J. Hum. Genet. 2011, 19:270-274.
60. Hofhaus G., Weiss H., Leonard K. Electron microscopic analysis of the peripheral and membrane parts of mitochondrial NADH dehydrogenase (complex I). J. Mol. Biol. 1991, 221:1027-1043.
61. Huang G., Lu H., Hao A., Ng D.C., Ponniah S., Guo K., Lufei C., Zeng Q., Cao X. GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol. Cell. Biol. 2004, 24:8447-8456.
62. Janssen A.J., Smeitink J.A., van den Heuvel L.P. Some practical aspects of providing a diagnostic service for respiratory chain defects. Ann. Clin. Biochem. 2003, 40:3-8.
63. Janssen R.J., Nijtmans L.G., van den Heuvel L.P., Smeitink J.A. Mitochondrial complex I: structure, function and pathology. J. Inherit. Metab. Dis. 2006, 29:499-515.
64. Johnson D.C., Dean D.R., Smith A.D., Johnson M.K. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 2005, 74:247-281.
65. Jun A.S., Trounce I.A., Brown M.D., Shoffner J.M., Wallace D.C. Use of transmitochondrial cybrids to assign a complex I defect to the mitochondrial DNA-encoded NADH dehydrogenase subunit 6 gene mutation at nucleotide pair 14459 that causes Leber hereditary optic neuropathy and dystonia. Mol. Cell. Biol. 1996, 16:771-777.
66. Karry R., Klein E., Ben Shachar D. Mitochondrial complex I subunits expression is altered in schizophrenia: a postmortem study. Biol. Psychiatry 2004, 55:676-684.
67. Keeney P.M., Xie J., Capaldi R.A., Bennett J.P. Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci. 2006, 26:5256-5264.
68. Kim S.H., Vlkolinsky R., Cairns N., Fountoulakis M., Lubec G. The reduction of NADH ubiquinone oxidoreductase 24- and 75-kDa subunits in brains of patients with Down syndrome and Alzheimer's disease. Life Sci. 2001, 68:2741-2750.
69. Kirby D.M., Crawford M., Cleary M.A., Dahl H.H., Dennett X., Thorburn D.R. Respiratory chain complex I deficiency: an underdiagnosed energy generation disorder. Neurology 1999, 52:1255-1264.
70. Kirby D.M., McFarland R., Ohtake A., Dunning C., Ryan M.T., Wilson C., Ketteridge D., Turnbull D.M., Thorburn D.R., Taylor R.W. Mutations of the mitochondrial ND1 gene as a cause of MELAS. J. Med. Genet. 2004, 41:784-789.
71. Kirby D.M., Salemi R., Sugiana C., Ohtake A., Parry L., Bell K.M., Kirk E.P., Boneh A., Taylor R.W., Dahl H.H., Ryan M.T., Thorburn D.R. NDUFS6 mutations are a novel cause of lethal neonatal mitochondrial complex I deficiency. J. Clin. Invest. 2004, 114:837-845.
72. 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. 2010, 12:1431-1470.
73. Kraytsberg Y., Kudryavtseva E., McKee A.C., Geula C., Kowall N.W., Khrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 2006, 38:518-520.
74. 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.
75. Langston J.W., Ballard P., Tetrud J.W., Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983, 219:979-980.
76. 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.
77. 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.
78. Lenaz G., Baracca A., Barbero G., Bergamini C., Dalmonte M.E., Del Sole M., Faccioli M., Falasca A., Fato R., Genova M.L., Sgarbi G., Solaini G. Mitochondrial respiratory chain super-complex I-III in physiology and pathology. Biochim. Biophys. Acta 2010, 1797:633-640.
79. Loeffen J., Smeitink J., Triepels R., Smeets R., Schuelke M., Sengers R., Trijbels F., Hamel B., Mullaart R., van den Heuvel L. The first nuclear-encoded complex I mutation in a patient with Leigh syndrome. Am. J. Hum. Genet. 1998, 63:1598-1608.
80. Loeffen J.L., Smeitink J.A., Trijbels J.M., Janssen A.J., Triepels R.H., Sengers R.C., van den Heuvel L.P. Isolated complex I deficiency in children: clinical, biochemical and genetic aspects. Hum. Mutat. 2000, 15:123-134.
81. Loeffen J., Elpeleg O., Smeitink J., Smeets R., Stockler-Ipsiroglu S., Mandel H., Sengers R., Trijbels F., van den Heuvel L. Mutations in the complex I NDUFS2 gene of patients with cardiomyopathy and encephalomyopathy. Ann. Neurol. 2001, 49:195-201.
82. Man P.Y., Griffiths P.G., Brown D.T., Howell N., Turnbull D.M., Chinnery P.F. The epidemiology of Leber hereditary optic neuropathy in the North East of England. Am. J. Hum. Genet. 2003, 72:333-339.
83. McKenzie M., Ryan M.T. Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life 2010, 62:497-502.
84. McKenzie M., Lazarou M., Thorburn D.R., Ryan M.T. Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J. Mol. Biol. 2006, 361:462-469.
85. Mizuno Y., Ohta S., Tanaka M., Takamiya S., Suzuki K., Sato T., Oya H., Ozawa T., Kagawa Y. Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem. Biophys. Res. Commun. 1989, 163:1450-1455.
86. Moran M., Rivera H., Sanchez-Arago M., Blazquez A., Merinero B., Ugalde C., Arenas J., Cuezva J.M., Martin M.A. Mitochondrial bioenergetics and dynamics interplay in complex I-deficient fibroblasts. Biochim. Biophys. Acta 2010, 1802:443-453.
87. Morris A.A., Leonard J.V., Brown G.K., Bidouki S.K., Bindoff L.A., Woodward C.E., Harding A.E., Lake B.D., Harding B.N., Farrell M.A., Bell J.E., Mirakhur M., Turnbull D.M. Deficiency of respiratory chain complex I is a common cause of Leigh disease. Ann. Neurol. 1996, 40:25-30.
88. Munakata K., Tanaka M., Mori K., Washizuka S., Yoneda M., Tajima O., Akiyama T., Nanko S., Kunugi H., Tadokoro K., Ozaki N., Inada T., Sakamoto K., Fukunaga T., Iijima Y., Iwata N., Tatsumi M., Yamada K., Yoshikawa T., Kato T. Mitochondrial DNA 3644T->C mutation associated with bipolar disorder. Genomics 2004, 84:1041-1050.
89. Nagashima T., Mori M., Katayama K., Nunomura M., Nishihara H., Hiraga H., Tanaka S., Goto Y., Nagashima K. Adult Leigh syndrome with mitochondrial DNA mutation at 8993. Acta Neuropathol. 1999, 97:416-422.
90. 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.
91. 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.
92. Ohnishi T., Salerno J.C. Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett. 2005, 579:4555-4561.
93. Ostergaard E., Rodenburg R.J., van den Brand M., Thomsen L.L., Duno M., Batbayli M., Wibrand F., Nijtmans L. Respiratory chain complex I deficiency due to NDUFA12 mutations as a new cause of Leigh syndrome. J. Med. Genet. 2011, 48:737-740.
94. 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.
95. Papa S., De Rasmo D., Scacco S., Signorile A., Technikova-Dobrova Z., Palmisano G., Sardanelli A.M., Papa F., Panelli D., Scaringi R., Santeramo A. Mammalian complex I: a regulable and vulnerable pacemaker in mitochondrial respiratory function. Biochim. Biophys. Acta 2008, 1777:719-728.
96. Papa S., Scacco S., De Rasmo D., Signorile A., Papa F., Panelli D., Nicastro A., Scaringi R., Santeramo A., Roca E., Trentadue R., Larizza M. cAMP-dependent protein kinase regulates post-translational processing and expression of complex I subunits in mammalian cells. Biochim. Biophys. Acta 2010, 1797:649-658.
97. Perales-Clemente E., Fernandez-Vizarra E., Acin-Perez R., Movilla N., Bayona-Bafaluy M.P., Moreno-Loshuertos R., Perez-Martos A., Fernandez-Silva P., Enriquez J.A. Five entry points of the mitochondrially encoded subunits in mammalian complex I assembly. Mol. Cell. Biol. 2010, 30:3038-3047.
98. Pitkanen S., Feigenbaum A., Laframboise R., Robinson B.H. NADH-coenzyme Q reductase (complex I) deficiency: heterogeneity in phenotype and biochemical findings. J. Inherit. Metab. Dis. 1996, 19:675-686.
99. Rahman S., Blok R.B., Dahl H.H., Danks D.M., Kirby D.M., Chow C.W., Christodoulou J., Thorburn D.R. Leigh syndrome: clinical features and biochemical and DNA abnormalities. Ann. Neurol. 1996, 39:343-351.
100. Rouault T.A. Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis. Model. Mech. 2012, 5:155-164.
101. Rubio-Gozalbo M.E., Dijkman K.P., van den Heuvel L.P., Sengers R.C., Wendel U., Smeitink J.A. Clinical differences in patients with mitochondriocytopathies due to nuclear versus mitochondrial DNA mutations. Hum. Mutat. 2000, 15:522-532.
102. 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.
103. 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.
104. Santorelli F.M., Tanji K., Kulikova R., Shanske S., Vilarinho L., Hays A.P., DiMauro S. Identification of a novel mutation in the mtDNA ND5 gene associated with MELAS. Biochem. Biophys. Res. Commun. 1997, 238:326-328.
105. Sazanov L.A. Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 2007, 46:2275-2288.
106. Sazanov L.A., Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 2006, 311:1430-1436.
107. Sazanov L.A., Peak-Chew S.Y., Fearnley I.M., Walker J.E. Resolution of the membrane domain of bovine complex I into subcomplexes: implications for the structural organization of the enzyme. Biochemistry 2000, 39:7229-7235.
108. Scacco S., Petruzzella V., Budde S., Vergari R., Tamborra R., Panelli D., van den Heuvel L.P., Smeitink J.A., Papa S. 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. 2003, 278:44161-44167.
109. Schagger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 2002, 1555:154-159.
110. Schagger H., Pfeiffer K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 2000, 19:1777-1783.
111. Schagger H., de Coo R., Bauer M.F., Hofmann S., Godinot C., Brandt U. Significance of respirasomes for the assembly/stability of human respiratory chain complex I. J. Biol. Chem. 2004, 279:36349-36353.
112. Schapira A.H. Primary and secondary defects of the mitochondrial respiratory chain. J. Inherit. Metab. Dis. 2002, 25:207-214.
113. Schapira A.H., Cooper J.M., Dexter D., Jenner P., Clark J.B., Marsden C.D. Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1989, 1:1269.
114. Schapira A.H., Cooper J.M., Dexter D., Clark J.B., Jenner P., Marsden C.D. Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 1990, 54:823-827.
115. Scheffler I.E., Yadava N., Potluri P. Molecular genetics of complex I-deficient Chinese hamster cell lines. Biochim. Biophys. Acta 2004, 1659:160-171.
116. Schuelke M., Smeitink J., Mariman E., Loeffen J., Plecko B., Trijbels F., Stockler-Ipsiroglu S., van den Heuvel L. Mutant NDUFV1 subunit of mitochondrial complex I causes leukodystrophy and myoclonic epilepsy. Nat. Genet. 1999, 21:260-261.
117. Shanske S., Coku J., Lu J., Ganesh J., Krishna S., Tanji K., Bonilla E., Naini A.B., Hirano M., DiMauro S. The G13513A mutation in the ND5 gene of mitochondrial DNA as a common cause of MELAS or Leigh syndrome: evidence from 12 cases. Arch. Neurol. 2008, 65:368-372.
118. Sherer T.B., Kim J.H., Betarbet R., Greenamyre J.T. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp. Neurol. 2003, 179:9-16.
119. Sherer T.B., Richardson J.R., Testa C.M., Seo B.B., Panov A.V., Yagi T., Matsuno-Yagi A., Miller G.W., Greenamyre J.T. Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson's disease. J. Neurochem. 2007, 100:1469-1479.
120. Shi R., Proteau A., Villarroya M., Moukadiri I., Zhang L., Trempe J.F., Matte A., Armengod M.E., Cygler M. Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions. PLoS Biol. 2010, 8:e1000354.
121. Shoubridge E.A. Nuclear genetic defects of oxidative phosphorylation. Hum. Mol. Genet. 2001, 10:2277-2284.
122. Smeitink J., Sengers R., Trijbels F., van den Heuvel L. Human NADH:ubiquinone oxidoreductase. J. Bioenerg. Biomembr. 2001, 33:259-266.
123. Smeitink J., van den Heuvel L., DiMauro S. The genetics and pathology of oxidative phosphorylation. Nat. Rev. Genet. 2001, 2:342-352.
124. Starkov A.A. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann. N. Y. Acad. Sci. 2008, 1147(37-52):37-52.
125. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., Beal M.F. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 2004, 24:7779-7788.
126. Stroh A., Anderka O., Pfeiffer K., Yagi T., Finel M., Ludwig B., Schagger H. Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J. Biol. Chem. 2004, 279:5000-5007.
127. Sugiana C., Pagliarini D.J., McKenzie M., Kirby D.M., Salemi R., bu-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.
128. Sun X., Wang J.F., Tseng M., Young L.T. Downregulation in components of the mitochondrial electron transport chain in the postmortem frontal cortex of subjects with bipolar disorder. J. Psychiatry Neurosci. 2006, 31:189-196.
129. Swerdlow R.H., Parks J.K., Miller S.W., Tuttle J.B., Trimmer P.A., Sheehan J.P., Bennett J.P., Davis R.E., Parker W.D. Origin and functional consequences of the complex I defect in Parkinson's disease. Ann. Neurol. 1996, 40:663-671.
130. Taylor R.W., Singh-Kler R., Hayes C.M., Smith P.E., Turnbull D.M. Progressive mitochondrial disease resulting from a novel missense mutation in the mitochondrial DNA ND3 gene. Ann. Neurol. 2001, 50:104-107.
131. Triepels R.H., van den Heuvel L.P., Loeffen J.L., Buskens C.A., Smeets R.J., Rubio Gozalbo M.E., Budde S.M., Mariman E.C., Wijburg F.A., Barth P.G., Trijbels J.M., Smeitink J.A. Leigh syndrome associated with a mutation in the NDUFS7 (PSST) nuclear encoded subunit of complex I. Ann. Neurol. 1999, 45:787-790.
132. Triepels R.H., van den Heuvel L.P., Trijbels J.M., Smeitink J.A. Respiratory chain complex I deficiency. Am. J. Med. Genet. 2001, 106:37-45.
133. Trimmer P.A., Bennett J.P. The cybrid model of sporadic Parkinson's disease. Exp. Neurol. 2009, 218:320-325.
134. Ugalde C., Triepels R.H., Coenen M.J., van den Heuvel L.P., Smeets R., Uusimaa J., Briones P., Campistol J., Majamaa K., Smeitink J.A., Nijtmans L.G. Impaired complex I assembly in a Leigh syndrome patient with a novel missense mutation in the ND6 gene. Ann. Neurol. 2003, 54:665-669.
135. Ugalde C., Vogel R., Huijbens R., Van Den Heuvel B., Smeitink J., Nijtmans L. Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Hum. Mol. Genet. 2004, 13:2461-2472.
136. Uhrigshardt H., Singh A., Kovtunovych G., Ghosh M., Rouault T.A. Characterization of the human HSC20, an unusual DnaJ type III protein, involved in iron-sulfur cluster biogenesis. Hum. Mol. Genet. 2010, 19:3816-3834.
137. Valentino M.L., Barboni P., Ghelli A., Bucchi L., Rengo C., Achilli A., Torroni A., Lugaresi A., Lodi R., Barbiroli B., Dotti M., Federico A., Baruzzi A., Carelli V. The ND1 gene of complex I is a mutational hot spot for Leber's hereditary optic neuropathy. Ann. Neurol. 2004, 56:631-641.
138. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
139. van den Bosch B.J., Gerards M., Sluiter W., Stegmann A.P., Jongen E.L., Hellbrekers D.M., Oegema R., Lambrichs E.H., Prokisch H., Danhauser K., Schoonderwoerd K., de Coo I.F., Smeets H.J. Defective NDUFA9 as a novel cause of neonatally fatal complex I disease. J. Med. Genet. 2012, 49:10-15.
140. van den Heuvel L., Ruitenbeek W., Smeets R., Gelman-Kohan Z., Elpeleg O., Loeffen J., Trijbels F., Mariman E., de B.D., Smeitink J. Demonstration of a new pathogenic mutation in human complex I deficiency: a 5-bp duplication in the nuclear gene encoding the 18-kD (AQDQ) subunit. Am. J. Hum. Genet. 1998, 62:262-268.
141. Vasta V., Ng S.B., Turner E.H., Shendure J., Hahn S.H. Next generation sequence analysis for mitochondrial disorders. Genome Med. 2009, 1:100.
142. Verkaart S., Koopman W.J., Cheek J., van Emst-de Vries S.E., van den Heuvel L.W., Smeitink J.A., Willems P.H. Mitochondrial and cytosolic thiol redox state are not detectably altered in isolated human NADH:ubiquinone oxidoreductase deficiency. Biochim. Biophys. Acta 2007, 1772:1041-1051.
143. Verkaart S., Koopman W.J., van Emst-de Vries S.E., Nijtmans L.G., van den Heuvel L.W., Smeitink J.A., Willems P.H. Superoxide production is inversely related to complex I activity in inherited complex I deficiency. Biochim. Biophys. Acta 2007, 1772:373-381.
144. 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.
145. 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.
146. 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.
147. 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.
148. Vogel R.O., van den Brand M.A., Rodenburg R.J., van den Heuvel L.P., Tsuneoka M., Smeitink J.A., Nijtmans L.G. Investigation of the complex I assembly chaperones B17.2L and NDUFAF1 in a cohort of CI deficient patients. Mol. Genet. Metab. 2007, 91:176-182.
149. Walker J.E. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q. Rev. Biophys. 1992, 25:253-324.
150. Washizuka S., Kakiuchi C., Mori K., Kunugi H., Tajima O., Akiyama T., Nanko S., Kato T. Association of mitochondrial complex I subunit gene NDUFV2 at 18p11 with bipolar disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2003, 120B:72-78.
151. Wiedemann N., Urzica E., Guiard B., Müller H., Lohaus C., Meyer H.E., Ryan M.T., Meisinger C., Mühlenhoff U., Lill R., Pfanner N. Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins. EMBO J. 2006, 25:184-195.
152. Wikstrom M. Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 1984, 169:300-304.
153. Yadava N., Potluri P., Smith E.N., Bisevac A., Scheffler I.E. Species-specific and mutant MWFE proteins. Their effect on the assembly of a functional mammalian mitochondrial complex I. J. Biol. Chem. 2002, 277:21221-21230.
154. Yadava N., Houchens T., Potluri P., Scheffler I.E. Development and characterization of a conditional mitochondrial complex I assembly system. J. Biol. Chem. 2004, 279:12406-12413.
155. Yadava N., Potluri P., Scheffler I.E. Investigations of the potential effects of phosphorylation of the MWFE and ESSS subunits on complex I activity and assembly. Int. J. Biochem. Cell Biol. 2008, 40:447-460.