Mitochondrial diseases part I: Mouse models of OXPHOS deficiencies caused by defects in respiratory complex subunits or assembly factors

Mitochondrion

Volumn 21, Issue , 2015, Pages 76-91

  Torraco, Alessandra ^a   Peralta, Susana ^b   Iommarini, Luisa ^c   Diaz, Francisca ^b  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Mitochondria; Mitochondrial diseases; Mouse models; Oxidative phosphorylation; OXPHOS

Indexed keywords

COMPLEX V; CYCLOOXYGENASE 1; CYTOCHROME C; CYTOCHROME C OXIDASE; LYSINE TRANSFER RNA; MITOCHONDRIAL DNA; OXIDOREDUCTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN;

BCS1L GENE; CLINICAL FEATURE; COMPLEX I DEFICIENCY; COMPLEX II DEFICIENCY; COMPLEX III DEFICIENCY; COQ9 GENE; COX1 GENE; COX10 GENE; COX15 GENE; COX17 GENE; COX4-2 GENE; COX6A-2 GENE; COX7A-1 GENE; CYTOCHROME C OXIDASE DEFICIENCY; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE; GENE MUTATION; GENETIC DISORDER; HUMAN; MOUSE MODEL; ND6 GENE; NDUFA5 GENE; NDUFS4 GENE; NDUFS6 GENE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PDSS2 GENE; REVIEW; SCO2 GENE; SDHD GENE; SURF1 GENE; UQCRFS1 GENE; ANIMAL; DEFICIENCY; METABOLISM; MOUSE; PATHOPHYSIOLOGY;

MUS;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MICE; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; OXIDATIVE PHOSPHORYLATION;

EID: 84922981706     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2015.01.009     Document Type: Review

References (164)

1. Acin-Perez R., Gatti D.L., Bai Y., Manfredi G. Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab. 2011, 13:712-719.
2. Agostino A., Invernizzi F., Tiveron C., Fagiolari G., Prelle A., Lamantea E., Giavazzi A., Battaglia G., Tatangelo L., Tiranti V., Zeviani M. Constitutive knockout of Surf1 is associated with high embryonic lethality, mitochondrial disease and cytochrome c oxidase deficiency in mice. Hum. Mol. Genet. 2003, 12:399-413.
3. Anderson S.L., Chung W.K., Frezzo J., Papp J.C., Ekstein J., DiMauro S., Rubin B.Y. A novel mutation in NDUFS4 causes Leigh syndrome in an Ashkenazi Jewish family. J. Inherit. Metab. Dis. 2008, 31(Suppl. 2):S461-S467.
4. Antonicka H., Leary S.C., Guercin G.H., Agar J.N., Horvath R., Kennaway N.G., Harding C.O., Jaksch M., Shoubridge E.A. 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. 2003, 12:2693-2702.
5. Antonicka H., Mattman A., Carlson C.G., Glerum D.M., Hoffbuhr K.C., Leary S.C., Kennaway N.G., Shoubridge E.A. Mutations in COX15 produce a defect in the mitochondrial heme biosynthetic pathway, causing early-onset fatal hypertrophic cardiomyopathy. Am. J. Hum. Genet. 2003, 72:101-114.
6. Antonicka H., Ogilvie I., Taivassalo T., Anitori R.P., Haller R.G., Vissing J., Kennaway N.G., Shoubridge E.A. Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. J. Biol. Chem. 2003, 278:43081-43088.
7. Bacman S.R., Williams S.L., Pinto M., Peralta S., Moraes C.T. Specific elimination of mutant mitochondrial genomes in patient-derived cells by mitoTALENs. Nat. Med. 2013, 19:1111-1113.
8. Barrientos A., Gouget K., Horn D., Soto I.C., Fontanesi F. Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process. Biochim. Biophys. Acta 2009, 1793:97-107.
9. Bayley J.P., van Minderhout I., Hogendoorn P.C., Cornelisse C.J., van der Wal A., Prins F.A., Teppema L., Dahan A., Devilee P., Taschner P.E. Sdhd and SDHD/H19 knockout mice do not develop paraganglioma or pheochromocytoma. PLoS One 2009, 4:e7987.
10. Bénit P., Steffann J., Lebon S., Chretien D., Kadhom N., de Lonlay P., Goldenberg A., Dumez Y., Dommergues M., Rustin P., Munnich A., Rötig A. Genotyping microsatellite DNA markers at putative disease loci in inbred/multiplex families with respiratory chain complex I deficiency allows rapid identification of a novel nonsense mutation (IVS1nt -1) in the NDUFS4 gene in Leigh syndrome. Hum. Genet. 2003, 112:563-566.
11. Benit P., Lebon S., Rustin P. Respiratory-chain diseases related to complex III deficiency. Biochim. Biophys. Acta 2009, 1793:181-185.
12. 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.
13. Budde S.M., van den Heuvel L.P., Smeets R.J., Skladal D., Mayr J.A., Boelen C., Petruzzella V., Papa S., Smeitink J.A. Clinical heterogeneity in patients with mutations in the NDUFS4 gene of mitochondrial complex I. J. Inherit. Metab. Dis. 2003, 26:813-815.
14. Bugiani M., Invernizzi F., Alberio S., Briem E., Lamantea E., Carrara F., Moroni I., Farina L., Spada M., Donati M.A., Uziel G., Zeviani M. Clinical and molecular findings in children with complex I deficiency. Biochim. Biophys. Acta 2004, 1659:136-147.
15. Bugiani M., Tiranti V., Farina L., Uziel G., Zeviani M. Novel mutations in COX15 in a long surviving Leigh syndrome patient with cytochrome c oxidase deficiency. J. Med. Genet. 2005, 42:e28.
16. Calvaruso M.A., Willems P., van den Brand M., Valsecchi F., Kruse S., Palmiter R., Smeitink J., Nijtmans L. Mitochondrial complex III stabilizes complex I in the absence of NDUFS4 to provide partial activity. Hum. Mol. Genet. 2012, 21:115-120.
17. Carelli V., Ross-Cisneros F.N., Sadun A.A. Optic nerve degeneration and mitochondrial dysfunction: genetic and acquired optic neuropathies. Neurochem. Int. 2002, 40:573-584.
18. 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.
19. Cizkova A., Stranecky V., Mayr J.A., Tesarova M., Havlickova V., Paul J., Ivanek R., Kuss A.W., Hansikova H., Kaplanova V., Vrbacky M., Hartmannova H., Noskova L., Honzik T., Drahota Z., Magner M., Hejzlarova K., Sperl W., Zeman J., Houstek J., Kmoch S. TMEM70 mutations cause isolated ATP synthase deficiency and neonatal mitochondrial encephalocardiomyopathy. Nat. Genet. 2008, 40:1288-1290.
20. Coenen M.J., van den Heuvel L.P., Ugalde C., Ten Brinke M., Nijtmans L.G., Trijbels F.J., Beblo S., Maier E.M., Muntau A.C., Smeitink J.A. Cytochrome c oxidase biogenesis in a patient with a mutation in COX10 gene. Ann. Neurol. 2004, 56:560-564.
21. Couplan E., Aiyar R.S., Kucharczyk R., Kabala A., Ezkurdia N., Gagneur J., St Onge R.P., Salin B., Soubigou F., Le Cann M., Steinmetz L.M., di Rago J.P., Blondel M. A yeast-based assay identifies drugs active against human mitochondrial disorders. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11989-11994.
22. Davoudi M., Kotarsky H., Hansson E., Fellman V. Complex I function and supercomplex formation are preserved in liver mitochondria despite progressive complex III deficiency. PLoS One 2014, 9:e86767.
23. de Lonlay P., Valnot I., Barrientos A., Gorbatyuk M., Tzagoloff A., Taanman J.W., Benayoun E., Chretien D., Kadhom N., Lombes A., de Baulny H.O., Niaudet P., Munnich A., Rustin P., Rotig A. A mutant mitochondrial respiratory chain assembly protein causes complex III deficiency in patients with tubulopathy, encephalopathy and liver failure. Nat. Genet. 2001, 29:57-60.
24. De Meirleir L., Seneca S., Lissens W., De Clercq I., Eyskens F., Gerlo E., Smet J., Van Coster R. Respiratory chain complex V deficiency due to a mutation in the assembly gene ATP12. J. Med. Genet. 2004, 41:120-124.
25. De Rocco D., Cerqua C., Goffrini P., Russo G., Pastore A., Meloni F., Nicchia E., Moraes C.T., Pecci A., Salviati L., Savoia A. Mutations of cytochrome c identified in patients with thrombocytopenia THC4 affect both apoptosis and cellular bioenergetics. Biochim. Biophys. Acta 2014, 1842:269-274.
26. Deepa S.S., Pulliam D., Hill S., Shi Y., Walsh M.E., Salmon A., Sloane L., Zhang N., Zeviani M., Viscomi C., Musi N., Van Remmen H. Improved insulin sensitivity associated with reduced mitochondrial complex IV assembly and activity. FASEB J. 2013, 27:1371-1380.
27. Dell'agnello C., Leo S., Agostino A., Szabadkai G., Tiveron C., Zulian A., Prelle A., Roubertoux P., Rizzuto R., Zeviani M. Increased longevity and refractoriness to Ca(2+)-dependent neurodegeneration in Surf1 knockout mice. Hum. Mol. Genet. 2007, 16:431-444.
28. Diaz F. Cytochrome c oxidase deficiency: patients and animal models. Biochim. Biophys. Acta 2010, 1802:100-110.
29. Diaz F., Thomas C.K., Garcia S., Hernandez D., Moraes C.T. Mice lacking COX10 in skeletal muscle recapitulate the phenotype of progressive mitochondrial myopathies associated with cytochrome c oxidase deficiency. Hum. Mol. Genet. 2005, 14:2737-2748.
30. Diaz F., Garcia S., Hernandez D., Regev A., Rebelo A., Oca-Cossio J., Moraes C.T. Pathophysiology and fate of hepatocytes in a mouse model of mitochondrial hepatopathies. Gut 2008, 57:232-242.
31. Diaz F., Kotarsky H., Fellman V., Moraes C.T. Mitochondrial disorders caused by mutations in respiratory chain assembly factors. Semin. Fetal Neonatal Med. 2011, 16:197-204.
32. Diaz F., Garcia S., Padgett K.R., Moraes C.T. A defect in the mitochondrial complex III, but not complex IV, triggers early ROS-dependent damage in defined brain regions. Hum. Mol. Genet. 2012, 21:5066-5077.
33. DiMauro S., Schon E.A. Mitochondrial disorders in the nervous system. Annu. Rev. Neurosci. 2008, 31:91-123.
34. DiMauro S., Tanji K., Schon E.A. The many clinical faces of cytochrome c oxidase deficiency. Adv. Exp. Med. Biol. 2012, 748:341-357.
35. Diomedi-Camassei F., Di Giandomenico S., Santorelli F.M., Caridi G., Piemonte F., Montini G., Ghiggeri G.M., Murer L., Barisoni L., Pastore A., Muda A.O., Valente M.L., Bertini E., Emma F. COQ2 nephropathy: a newly described inherited mitochondriopathy with primary renal involvement. J. Am. Soc. Nephrol. 2007, 18:2773-2780.
36. Duncan A.J., Bitner-Glindzicz M., Meunier B., Costello H., Hargreaves I.P., Lopez L.C., Hirano M., Quinzii C.M., Sadowski M.I., Hardy J., Singleton A., Clayton P.T., Rahman S. A nonsense mutation in COQ9 causes autosomal-recessive neonatal-onset primary coenzyme Q10 deficiency: a potentially treatable form of mitochondrial disease. Am. J. Hum. Genet. 2009, 84:558-566.
37. Emma F., Bertini E., Salviati L., Montini G. Renal involvement in mitochondrial cytopathies. Pediatr. Nephrol. 2012, 27:539-550.
38. Fan W., Waymire K.G., Narula N., Li P., Rocher C., Coskun P.E., Vannan M.A., Narula J., Macgregor G.R., Wallace D.C. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 2008, 319:958-962.
39. 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.
40. Feng J., Bussière F., Hekimi S. Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev. Cell 2001, 1:633-644.
41. Fernandez-Vizarra E., Tiranti V., Zeviani M. Assembly of the oxidative phosphorylation system in humans: what we have learned by studying its defects. Biochim. Biophys. Acta 2009, 1793:200-211.
42. Forbes J.M., Ke B.X., Nguyen T.V., Henstridge D.C., Penfold S.A., Laskowski A., Sourris K.C., Groschner L.N., Cooper M.E., Thorburn D.R., Coughlan M.T. Deficiency in mitochondrial complex I activity due to Ndufs6 gene trap insertion induces renal disease. Antioxid. Redox Signal. 2013, 19:331-343.
43. Formentini L., Pereira M.P., Sanchez-Cenizo L., Santacatterina F., Lucas J.J., Navarro C., Martinez-Serrano A., Cuezva J.M. In vivo inhibition of the mitochondrial H+-ATP synthase in neurons promotes metabolic preconditioning. EMBO J. 2014, 33:762-778.
44. Fukuda R., Zhang H., Kim J.W., Shimoda L., Dang C.V., Semenza G.L. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007, 129:111-122.
45. Funfschilling U., Supplie L.M., Mahad D., Boretius S., Saab A.S., Edgar J., Brinkmann B.G., Kassmann C.M., Tzvetanova I.D., Mobius W., Diaz F., Meijer D., Suter U., Hamprecht B., Sereda M.W., Moraes C.T., Frahm J., Goebbels S., Nave K.A. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012, 485:517-521.
46. Garcia-Corzo L., Luna-Sanchez M., Doerrier C., Garcia J.A., Guaras A., Acin-Perez R., Bullejos-Peregrin J., Lopez A., Escames G., Enriquez J.A., Acuna-Castroviejo D., Lopez L.C. Dysfunctional Coq9 protein causes predominant encephalomyopathy associated with CoQ deficiency. Hum. Mol. Genet. 2013, 22:1233-1248.
47. Guillausseau P.J., Massin P., Dubois-LaForgue D., Timsit J., Virally M., Gin H., Bertin E., Blickle J.F., Bouhanick B., Cahen J., Caillat-Zucman S., Charpentier G., Chedin P., Derrien C., Ducluzeau P.H., Grimaldi A., Guerci B., Kaloustian E., Murat A., Olivier F., Paques M., Paquis-Flucklinger V., Porokhov B., Samuel-Lajeunesse J., Vialettes B. Maternally inherited diabetes and deafness: a multicenter study. Ann. Intern. Med. 2001, 134:721-728.
48. Hallman T.M., Peng M., Meade R., Hancock W.W., Madaio M.P., Gasser D.L. The mitochondrial and kidney disease phenotypes of kd/kd mice under germfree conditions. J. Autoimmun. 2006, 26:1-6.
49. Hao Z., Duncan G.S., Chang C.C., Elia A., Fang M., Wakeham A., Okada H., Calzascia T., Jang Y., You-Ten A., Yeh W.C., Ohashi P., Wang X., Mak T.W. Specific ablation of the apoptotic functions of cytochrome C reveals a differential requirement for cytochrome C and Apaf-1 in apoptosis. Cell 2005, 121:579-591.
50. Hashizume O., Shimizu A., Yokota M., Sugiyama A., Nakada K., Miyoshi H., Itami M., Ohira M., Nagase H., Takenaga K., Hayashi J. Specific mitochondrial DNA mutation in mice regulates diabetes and lymphoma development. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10528-10533.
51. Haut S., Brivet M., Touati G., Rustin P., Lebon S., Garcia-Cazorla A., Saudubray J.M., Boutron A., Legrand A., Slama A. A deletion in the human QP-C gene causes a complex III deficiency resulting in hypoglycaemia and lactic acidosis. Hum. Genet. 2003, 113:118-122.
52. Heeringa S.F., Chernin G., Chaki M., Zhou W., Sloan A.J., Ji Z., Xie L.X., Salviati L., Hurd T.W., Vega-Warner V., Killen P.D., Raphael Y., Ashraf S., Ovunc B., Schoeb D.S., McLaughlin H.M., Airik R., Vlangos C.N., Gbadegesin R., Hinkes B., Saisawat P., Trevisson E., Doimo M., Casarin A., Pertegato V., Giorgi G., Prokisch H., Rotig A., Nurnberg G., Becker C., Wang S., Ozaltin F., Topaloglu R., Bakkaloglu A., Bakkaloglu S.A., Muller D., Beissert A., Mir S., Berdeli A., Varpizen S., Zenker M., Matejas V., Santos-Ocana C., Navas P., Kusakabe T., Kispert A., Akman S., Soliman N.A., Krick S., Mundel P., Reiser J., Nurnberg P., Clarke C.F., Wiggins R.C., Faul C., Hildebrandt F. COQ6 mutations in human patients produce nephrotic syndrome with sensorineural deafness. J. Clin. Invest. 2011, 121:2013-2024.
53. Hinson J.T., Fantin V.R., Schonberger J., Breivik N., Siem G., McDonough B., Sharma P., Keogh I., Godinho R., Santos F., Esparza A., Nicolau Y., Selvaag E., Cohen B.H., Hoppel C.L., Tranebjaerg L., Eavey R.D., Seidman J.G., Seidman C.E. Missense mutations in the BCS1L gene as a cause of the Bjornstad syndrome. N. Engl. J. Med. 2007, 356:809-819.
54. Hirano M., Garone C., Quinzii C.M. CoQ(10) deficiencies and MNGIE: two treatable mitochondrial disorders. Biochim. Biophys. Acta 2012, 1820:625-631.
55. 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.
56. Holt I.J., Harding A.E., Petty R.K., Morgan-Hughes J.A. A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am. J. Hum. Genet. 1990, 46:428-433.
57. Hughes B.G., Hekimi S. A mild impairment of mitochondrial electron transport has sex-specific effects on lifespan and aging in mice. PLoS ONE 2011, 6:e26116.
58. Huttemann M., Kadenbach B., Grossman L.I. Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 2001, 267:111-123.
59. Huttemann M., Klewer S., Lee I., Pecinova A., Pecina P., Liu J., Lee M., Doan J.W., Larson D., Slack E., Maghsoodi B., Erickson R.P., Grossman L.I. Mice deleted for heart-type cytochrome c oxidase subunit 7a1 develop dilated cardiomyopathy. Mitochondrion 2012, 12:294-304.
60. Huttemann M., Lee I., Gao X., Pecina P., Pecinova A., Liu J., Aras S., Sommer N., Sanderson T.H., Tost M., Neff F., Aguilar-Pimentel J.A., Becker L., Naton B., Rathkolb B., Rozman J., Favor J., Hans W., Prehn C., Puk O., Schrewe A., Sun M., Hofler H., Adamski J., Bekeredjian R., Graw J., Adler T., Busch D.H., Klingenspor M., Klopstock T., Ollert M., Wolf E., Fuchs H., Gailus-Durner V., Hrabe de Angelis M., Weissmann N., Doan J.W., Bassett D.J., Grossman L.I. Cytochrome c oxidase subunit 4 isoform 2-knockout mice show reduced enzyme activity, airway hyporeactivity, and lung pathology. FASEB J. 2012, 26:3916-3930.
61. Indrieri A., van Rahden V.A., Tiranti V., Morleo M., Iaconis D., Tammaro R., D'Amato I., Conte I., Maystadt I., Demuth S., Zvulunov A., Kutsche K., Zeviani M., Franco B. Mutations in COX7B cause microphthalmia with linear skin lesions, an unconventional mitochondrial disease. Am. J. Hum. Genet. 2012, 91:942-949.
62. Ingraham C.A., Burwell L.S., Skalska J., Brookes P.S., Howell R.L., Sheu S.S., Pinkert C.A. NDUFS4: creation of a mouse model mimicking a complex I disorder. Mitochondrion 2009, 9:204-210.
63. Inoue K., Nakada K., Ogura A., Isobe K., Goto Y., Nonaka I., Hayashi J.I. Generation of mice with mitochondrial dysfunction by introducing mouse mtDNA carrying a deletion into zygotes. Nat. Genet. 2000, 26:176-181.
64. Ishikawa K., Hashizume O., Koshikawa N., Fukuda S., Nakada K., Takenaga K., Hayashi J. Enhanced glycolysis induced by mtDNA mutations does not regulate metastasis. FEBS Lett. 2008, 582:3525-3530.
65. Iwasaki N., Babazono T., Tsuchiya K., Tomonaga O., Suzuki A., Togashi M., Ujihara N., Sakka Y., Yokokawa H., Ogata M., Nihei H., Iwamoto Y. Prevalence of A-to-G mutation at nucleotide 3243 of the mitochondrial tRNA(Leu(UUR)) gene in Japanese patients with diabetes mellitus and end stage renal disease. J. Hum. Genet. 2001, 46:330-334.
66. Jaksch M., Ogilvie I., Yao J., Kortenhaus G., Bresser H.G., Gerbitz K.D., Shoubridge E.A. Mutations in SCO2 are associated with a distinct form of hypertrophic cardiomyopathy and cytochrome c oxidase deficiency. Hum. Mol. Genet. 2000, 9:795-801.
67. Jenuth J.P., Peterson A.C., Shoubridge E.A. Tissue-specific selection for different mtDNA genotypes in heteroplasmic mice. Nat. Genet. 1997, 16:93-95.
68. Johns D.R., Neufeld M.J. Cytochrome b mutations in Leber hereditary optic neuropathy. Biochem. Biophys. Res. Commun. 1991, 181:1358-1364.
69. Johnson A., Gin P., Marbois B.N., Hsieh E.J., Wu M., Barros M.H., Clarke C.F., Tzagoloff A. COQ9, a new gene required for the biosynthesis of coenzyme Q in Saccharomyces cerevisiae. J. Biol. Chem. 2005, 280:31397-31404.
70. Johnston P.B., Gaster R.N., Smith V.C., Tripathi R.C. A clinicopathologic study of autosomal dominant optic atrophy. Am J. Ophthalmol. 1979, 88:868-875.
71. Jonckheere A.I., Hogeveen M., Nijtmans L.G., van den Brand M.A., Janssen A.J., Diepstra J.H., van den Brandt F.C., van den Heuvel L.P., Hol F.A., Hofste T.G., Kapusta L., Dillmann U., Shamdeen M.G., Smeitink J.A., Rodenburg R.J. A novel mitochondrial ATP8 gene mutation in a patient with apical hypertrophic cardiomyopathy and neuropathy. J. Med. Genet. 2008, 45:129-133.
72. Karamanlidis G., Lee C.F., Garcia-Menendez L., Kolwicz S.C., Suthammarak W., Gong G., Sedensky M.M., Morgan P.G., Wang W., Tian R. Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab. 2013, 18:239-250.
73. Kasahara A., Ishikawa K., Yamaoka M., Ito M., Watanabe N., Akimoto M., Sato A., Nakada K., Endo H., Suda Y., Aizawa S., Hayashi J. Generation of trans-mitochondrial mice carrying homoplasmic mtDNAs with a missense mutation in a structural gene using ES cells. Hum. Mol. Genet. 2006, 15:871-881.
74. Kawamukai M. Biosynthesis and bioproduction of coenzyme Q10 by yeasts and other organisms. Biotechnol. Appl. Biochem. 2009, 53:217-226.
75. Ke B.X., Pepe S., Grubb D.R., Komen J.C., Laskowski A., Rodda F.A., Hardman B.M., Pitt J.J., Ryan M.T., Lazarou M., Koleff J., Cheung M.M., Smolich J.J., Thorburn D.R. Tissue-specific splicing of an Ndufs6 gene-trap insertion generates a mitochondrial complex I deficiency-specific cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6165-6170.
76. Keightley J.A., Anitori R., Burton M.D., Quan F., Buist N.R., Kennaway N.G. Mitochondrial encephalomyopathy and complex III deficiency associated with a stop-codon mutation in the cytochrome b gene. Am. J. Hum. Genet. 2000, 67:1400-1410.
77. Khalimonchuk O., Rodel G. Biogenesis of cytochrome c oxidase. Mitochondrion 2005, 5:363-388.
78. 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.
79. Knuf M., Faber J., Huth R.G., Freisinger P., Zepp F., Kampmann C. Identification of a novel compound heterozygote SCO2 mutation in cytochrome c oxidase deficient fatal infantile cardioencephalomyopathy. Acta Paediatr. 2007, 96:130-132.
80. Kovacs G.G., Hoftberger R., Majtenyi K., Horvath R., Barsi P., Komoly S., Lassmann H., Budka H., Jakab G. Neuropathology of white matter disease in Leber's hereditary optic neuropathy. Brain 2005, 128:35-41.
81. Kruse S.E., Watt W.C., Marcinek D.J., Kapur R.P., Schenkman K.A., Palmiter R.D. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008, 7:312-320.
82. 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.
83. Leary S.C., Cobine P.A., Kaufman B.A., Guercin G.H., Mattman A., Palaty J., Lockitch G., Winge D.R., Rustin P., Horvath R., Shoubridge E.A. The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis. Cell Metab. 2007, 5:9-20.
84. Leary S.C., Sasarman F., Nishimura T., Shoubridge E.A. Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1. Hum. Mol. Genet. 2009, 18:2230-2240.
85. Lee I., Huttemann M., Liu J., Grossman L.I., Malek M.H. Deletion of heart-type cytochrome c oxidase subunit 7a1 impairs skeletal muscle angiogenesis and oxidative phosphorylation. J. Physiol. 2012, 590:5231-5243.
86. Leong D.W., Komen J.C., Hewitt C.A., Arnaud E., McKenzie M., Phipson B., Bahlo M., Laskowski A., Kinkel S.A., Davey G.M., Heath W.R., Voss A.K., Zahedi R.P., Pitt J.J., Chrast R., Sickmann A., Ryan M.T., Smyth G.K., Thorburn D.R., Scott H.S. Proteomic and metabolomic analyses of mitochondrial complex I-deficient mouse model generated by spontaneous B2 short interspersed nuclear element (SINE) insertion into NADH dehydrogenase (ubiquinone) Fe-S protein 4 (Ndufs4) gene. J. Biol. Chem. 2012, 287:20652-20663.
87. Leveen P., Kotarsky H., Morgelin M., Karikoski R., Elmer E., Fellman V. The GRACILE mutation introduced into Bcs1l causes postnatal complex III deficiency: a viable mouse model for mitochondrial hepatopathy. Hepatology 2011, 53:437-447.
88. Levy S.E., Waymire K.G., Kim Y.L., MacGregor G.R., Wallace D.C. Transfer of chloramphenicol-resistant mitochondrial DNA into the chimeric mouse. Transgenic Res. 1999, 8:137-145.
89. Li K., Li Y., Shelton J.M., Richardson J.A., Spencer E., Chen Z.J., Wang X., Williams R.S. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 2000, 101:389-399.
90. Lin C.S., Sharpley M.S., Fan W., Waymire K.G., Sadun A.A., Carelli V., Ross-Cisneros F.N., Baciu P., Sung E., McManus M.J., Pan B.X., Gil D.W., Macgregor G.R., Wallace D.C. Mouse mtDNA mutant model of Leber hereditary optic neuropathy. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:20065-20070.
91. Lopez L.C., Schuelke M., Quinzii C.M., Kanki T., Rodenburg R.J., Naini A., Dimauro S., Hirano M. Leigh syndrome with nephropathy and CoQ10 deficiency due to decaprenyl diphosphate synthase subunit 2 (PDSS2) mutations. Am. J. Hum. Genet. 2006, 79:1125-1129.
92. Majander A., Suomalainen A., Vettenranta K., Sariola H., Perkkio M., Holmberg C., Pihko H. Congenital hypoplastic anemia, diabetes, and severe renal tubular dysfunction associated with a mitochondrial DNA deletion. Pediatr. Res. 1991, 30:327-330.
93. Malfatti E., Bugiani M., Invernizzi F., de Souza C.F., Farina L., Carrara F., Lamantea E., Antozzi C., Confalonieri P., Sanseverino M.T., Giugliani R., Uziel G., Zeviani M. Novel mutations of ND genes in complex I deficiency associated with mitochondrial encephalopathy. Brain 2007, 130:1894-1904.
94. Marchington D.R., Barlow D., Poulton J. Transmitochondrial mice carrying resistance to chloramphenicol on mitochondrial DNA: developing the first mouse model of mitochondrial DNA disease. Nat. Med. 1999, 5:957-960.
95. Martin-Hernandez E., Garcia-Silva M.T., Vara J., Campos Y., Cabello A., Muley R., Del Hoyo P., Martin M.A., Arenas J. Renal pathology in children with mitochondrial diseases. Pediatr. Nephrol. 2005, 20:1299-1305.
96. Massa V., Fernandez-Vizarra E., Alshahwan S., Bakhsh E., Goffrini P., Ferrero I., Mereghetti P., D'Adamo P., Gasparini P., Zeviani M. Severe infantile encephalomyopathy caused by a mutation in COX6B1, a nucleus-encoded subunit of cytochrome c oxidase. Am. J. Hum. Genet. 2008, 82:1281-1289.
97. Mayr J.A., Havlickova V., Zimmermann F., Magler I., Kaplanova V., Jesina P., Pecinova A., Nuskova H., Koch J., Sperl W., Houstek J. Mitochondrial ATP synthase deficiency due to a mutation in the ATP5E gene for the F1 epsilon subunit. Hum. Mol. Genet. 2010, 19:3430-3439.
98. Mckenzie M., Ryan M.T. Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life 2010, 62:497-502.
99. Morais V.A., Haddad D., Craessaerts K., De Bock P.J., Swerts J., Vilain S., Aerts L., Overbergh L., Grunewald A., Seibler P., Klein C., Gevaert K., Verstreken P., De Strooper B. PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 ubiquinone uncoupling. Science 2014, 344:203-207.
100. Moran M., Marin-Buera L., Gil-Borlado M.C., Rivera H., Blazquez A., Seneca S., Vazquez-Lopez M., Arenas J., Martin M.A., Ugalde C. Cellular pathophysiological consequences of BCS1L mutations in mitochondrial complex III enzyme deficiency. Hum. Mutat. 2010, 31:930-941.
101. Morison I.M., Cramer Borde E.M., Cheesman E.J., Cheong P.L., Holyoake A.J., Fichelson S., Weeks R.J., Lo A., Davies S.M., Wilbanks S.M., Fagerlund R.D., Ludgate M.W., da Silva Tatley F.M., Coker M.S., Bockett N.A., Hughes G., Pippig D.A., Smith M.P., Capron C., Ledgerwood E.C. A mutation of human cytochrome c enhances the intrinsic apoptotic pathway but causes only thrombocytopenia. Nat. Genet. 2008, 40:387-389.
102. Mourmans J., Wendel U., Bentlage H.A.C.M., Trijbels J.M.F., Smeitink J.A.M., de Coo I.F.M., Gabreëls F.J.M., Sengers R.C.A., Ruitenbeek W. Clinical heterogeneity in respiratory chain complex III deficiency in childhood. J. Neurol. Sci. 1997, 149:111-117.
103. Nakamura J., Fujikawa M., Yoshida M. IF1, a natural inhibitor of mitochondrial ATP synthase, is not essential for the normal growth and breeding of mice. Biosci. Rep. 2013, 33.
104. Narisawa S., Hecht N.B., Goldberg E., Boatright K.M., Reed J.C., Millan J.L. Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy. Mol. Cell. Biol. 2002, 22:5554-5562.
105. Ngu L.H., Nijtmans L.G., Distelmaier F., Venselaar H., van Emst-de Vries S.E., van den Brand M.A., Stoltenborg B.J., Wintjes L.T., Willems P.H., van den Heuvel L.P., Smeitink J.A., Rodenburg R.J. A catalytic defect in mitochondrial respiratory chain complex I due to a mutation in NDUFS2 in a patient with Leigh syndrome. Biochim. Biophys. Acta 2012, 1822:168-175.
106. Niaudet P., Rotig A. The kidney in mitochondrial cytopathies. Kidney Int. 1997, 51:1000-1007.
107. 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.
108. Ohara S., Ohama E., Takahashi H., Ikuta F., Nishizawa M., Tanaka K., Miyatake T. Alterations of oligodendrocytes and demyelination in the spinal cord of patients with mitochondrial encephalomyopathy. J. Neurol. Sci. 1988, 86:19-29.
109. Olanow C.W., Tatton W.G. Etiology and pathogenesis of Parkinson's disease. Annu. Rev. Neurosci. 1999, 22:123-144.
110. Oquendo C.E., Antonicka H., Shoubridge E.A., Reardon W., Brown G.K. Functional and genetic studies demonstrate that mutation in the COX15 gene can cause Leigh syndrome. J. Med. Genet. 2004, 41:540-544.
111. Pagniez-Mammeri H., Rak M., Legrand A., Benit P., Rustin P., Slama A. Mitochondrial complex I deficiency of nuclear origin II. Non-structural genes. Mol. Genet. Metab. 2012, 105:173-179.
112. Palin E.J., Paetau A., Suomalainen A. Mesencephalic complex I deficiency does not correlate with parkinsonism in mitochondrial DNA maintenance disorders. Brain 2013, 136:2379-2392.
113. Pan-Montojo F., Anichtchik O., Dening Y., Knels L., Pursche S., Jung R., Jackson S., Gille G., Spillantini M.G., Reichmann H., Funk R.H. Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS One 2010, 5:e8762.
114. Papadopoulou L.C., Sue C.M., Davidson M.M., Tanji K., Nishino I., Sadlock J.E., Krishna S., Walker W., Selby J., Glerum D.M., Coster R.V., Lyon G., Scalais E., Lebel R., Kaplan P., Shanske S., De Vivo D.C., Bonilla E., Hirano M., DiMauro S., Schon E.A. Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat. Genet. 1999, 23:333-337.
115. Parsons W.J., Williams R.S., Shelton J.M., Luo Y., Kessler D.J., Richardson J.A. Developmental regulation of cytochrome oxidase subunit VIa isoforms in cardiac and skeletal muscle. Am. J. Physiol. 1996, 270:H567-H574.
116. Pecina P., Houstkova H., Hansikova H., Zeman J., Houstek J. Genetic defects of cytochrome c oxidase assembly. Physiol. Res. 2004, 53(Suppl. 1):S213-S223.
117. Peng M., Falk M.J., Haase V.H., King R., Polyak E., Selak M., Yudkoff M., Hancock W.W., Meade R., Saiki R., Lunceford A.L., Clarke C.F., Gasser D.L. Primary coenzyme Q deficiency in Pdss2 mutant mice causes isolated renal disease. PLoS Genet. 2008, 4:e1000061.
118. Peralta S., Torraco A., Wenz T., Garcia S., Diaz F., Moraes C.T. Partial complex I deficiency due to the CNS conditional ablation of Ndufa5 results in a mild chronic encephalopathy but no increase in oxidative damage. Hum. Mol. Genet. 2013, 23:1399-1412.
119. Petruzzella V., Vergari R., Puzziferri I., Boffoli D., Lamantea E., Zeviani M., Papa S. A nonsense mutation in the NDUFS4 gene encoding the 18kDa (AQDQ) subunit of complex I abolishes assembly and activity of the complex in a patient with Leigh-like syndrome. Hum. Mol. Genet. 2001, 10:529-535.
120. Piruat J.I., Pintado C.O., Ortega-Saenz P., Roche M., Lopez-Barneo J. The mitochondrial SDHD gene is required for early embryogenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia. Mol. Cell. Biol. 2004, 24:10933-10940.
121. Pullman M.E., Monroy G.C. A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. J. Biol. Chem. 1963, 238:3762-3769.
122. Quintana A., Kruse S.E., Kapur R.P., Sanz E., Palmiter R.D. Complex I deficiency due to loss of Ndufs4 in the brain results in progressive encephalopathy resembling Leigh syndrome. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10996-11001.
123. Quintana A., Zanella S., Koch H., Kruse S.E., Lee D., Ramirez J.M., Palmiter R.D. Fatal breathing dysfunction in a mouse model of Leigh syndrome. J. Clin. Invest. 2012, 122:2359-2368.
124. Quintens R., Singh S., Lemaire K., De Bock K., Granvik M., Schraenen A., Vroegrijk I.O., Costa V., Van Noten P., Lambrechts D., Lehnert S., Van Lommel L., Thorrez L., De Faudeur G., Romijn J.A., Shelton J.M., Scorrano L., Lijnen H.R., Voshol P.J., Carmeliet P., Mammen P.P., Schuit F. Mice deficient in the respiratory chain gene Cox6a2 are protected against high-fat diet-induced obesity and insulin resistance. PLoS One 2013, 8:e56719.
125. Quinzii C.M., Garone C., Emmanuele V., Tadesse S., Krishna S., Dorado B., Hirano M. Tissue-specific oxidative stress and loss of mitochondria in CoQ-deficient Pdss2 mutant mice. FASEB J. 2013, 27:612-621.
126. Radford N.B., Wan B., Richman A., Szczepaniak L.S., Li J.L., Li K., Pfeiffer K., Schagger H., Garry D.J., Moreadith R.W. Cardiac dysfunction in mice lacking cytochrome-c oxidase subunit VIaH. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H726-H733.
127. Rak M., Rustin P. Supernumerary subunits NDUFA3, NDUFA5 and NDUFA12 are required for the formation of the extramembrane arm of human mitochondrial complex I. FEBS Lett. 2014, 588:1832-1838.
128. Rotig A., Goutieres F., Niaudet P., Rustin P., Chretien D., Guest G., Mikol J., Gubler M.C., Munnich A. Deletion of mitochondrial DNA in patient with chronic tubulointerstitial nephritis. J. Pediatr. 1995, 126:597-601.
129. Rusanen H., Majamaa K., Tolonen U., Remes A.M., Myllyla R., Hassinen I.E. Demyelinating polyneuropathy in a patient with the tRNA(Leu)(UUR) mutation at base pair 3243 of the mitochondrial DNA. Neurology 1995, 45:1188-1192.
130. Rustin P., Rotig A. Inborn errors of complex II-unusual human mitochondrial diseases. Biochim. Biophys. Acta 2002, 1553:117-122.
131. Rutter J., Winge D.R., Schiffman J.D. Succinate dehydrogenase - assembly, regulation and role in human disease. Mitochondrion 2010, 10:393-401.
132. Saiki R., Lunceford A.L., Shi Y., Marbois B., King R., Pachuski J., Kawamukai M., Gasser D.L., Clarke C.F. Coenzyme Q10 supplementation rescues renal disease in Pdss2kd/kd mice with mutations in prenyl diphosphate synthase subunit 2. Am. J. Physiol. Renal Physiol. 2008, 295:F1535-F1544.
133. Schoenfeld R., Wong A., Silva J., Li M., Itoh A., Horiuchi M., Itoh T., Pleasure D., Cortopassi G. Oligodendroglial differentiation induces mitochondrial genes and inhibition of mitochondrial function represses oligodendroglial differentiation. Mitochondrion 2010, 10:143-150.
134. Shimizu A., Mito T., Hayashi C., Ogasawara E., Koba R., Negishi I., Takenaga K., Nakada K., Hayashi J. Transmitochondrial mice as models for primary prevention of diseases caused by mutation in the tRNALys gene. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:3104-3109.
135. Shoubridge E.A. Cytochrome c oxidase deficiency. Am. J. Med. Genet. 2001, 106:46-52.
136. Shteyer E., Saada A., Shaag A., Al-Hijawi F.A., Kidess R., Revel-Vilk S., Elpeleg O. Exocrine pancreatic insufficiency, dyserythropoeitic anemia, and calvarial hyperostosis are caused by a mutation in the COX4I2 gene. Am. J. Hum. Genet. 2009, 84:412-417.
137. Sligh J.E., Levy S.E., Waymire K.G., Allard P., Dillehay D.L., Nusinowitz S., Heckenlively J.R., MacGregor G.R., Wallace D.C. Maternal germ-line transmission of mutant mtDNAs from embryonic stem cell-derived chimeric mice. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14461-14466.
138. Spiegel R., Shaag A., Mandel H., Reich D., Penyakov M., Hujeirat Y., Saada A., Elpeleg O., Shalev S.A. Mutated NDUFS6 is the cause of fatal neonatal lactic acidemia in Caucasus Jews. Eur. J. Hum. Genet. 2009, 17:1200-1203.
139. Spiegel R., Khayat M., Shalev S.A., Horovitz Y., Mandel H., Hershkovitz E., Barghuti F., Shaag A., Saada A., Korman S.H., Elpeleg O., Yatsiv I. TMEM70 mutations are a common cause of nuclear encoded ATP synthase assembly defect: further delineation of a new syndrome. J. Med. Genet. 2011, 48:177-182.
140. Sterky F.H., Lee S., Wibom R., Olson L., Larsson N.G. Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons in vivo. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:12937-12942.
141. Sterky F.H., Hoffman A.F., Milenkovic D., Bao B., Paganelli A., Edgar D., Wibom R., Lupica C.R., Olson L., Larsson N.G. Altered dopamine metabolism and increased vulnerability to MPTP in mice with partial deficiency of mitochondrial complex I in dopamine neurons. Hum. Mol. Genet. 2012, 21:1078-1089.
142. Stiburek L., Vesela K., Hansikova H., Hulkova H., Zeman J. Loss of function of Sco1 and its interaction with cytochrome c oxidase. Am. J. Physiol. Cell Physiol. 2009, 296:C1218-C1226.
143. Stock D., Leslie A.G., Walker J.E. Molecular architecture of the rotary motor in ATP synthase. Science 1999, 286:1700-1705.
144. Swalwell H., Kirby D.M., Blakely E.L., Mitchell A., Salemi R., Sugiana C., Compton A.G., Tucker E.J., Ke B.X., Lamont P.J., Turnbull D.M., McFarland R., Taylor R.W., Thorburn D.R. Respiratory chain complex I deficiency caused by mitochondrial DNA mutations. Eur. J. Hum. Genet. 2011, 19:769-775.
145. Takahashi Y., Kako K., Kashiwabara S., Takehara A., Inada Y., Arai H., Nakada K., Kodama H., Hayashi J., Baba T., Munekata E. Mammalian copper chaperone Cox17p has an essential role in activation of cytochrome C oxidase and embryonic development. Mol. Cell. Biol. 2002, 22:7614-7621.
146. Tiranti V., Jaksch M., Hofmann S., Galimberti C., Hoertnagel K., Lulli L., Freisinger P., Bindoff L., Gerbitz K.D., Comi G.P., Uziel G., Zeviani M., Meitinger T. Loss-of-function mutations of SURF-1 are specifically associated with Leigh syndrome with cytochrome c oxidase deficiency. Ann. Neurol. 1999, 46:161-166.
147. Torraco A., Verrigni D., Rizza T., Meschini M.C., Vazquez-Memije M.E., Martinelli D., Bianchi M., Piemonte F., Dionisi-Vici C., Santorelli F.M., Bertini E., Carrozzo R. TMEM70: a mutational hot spot in nuclear ATP synthase deficiency with a pivotal role in complex V biogenesis. Neurogenetics 2012, 13:375-386.
148. Turunen M., Olsson J., Dallner G. Metabolism and function of coenzyme Q. Biochim. Biophys. Acta 2004, 1660:171-199.
149. Valnot I., von Kleist-Retzow J.C., Barrientos A., Gorbatyuk M., Taanman J.W., Mehaye B., Rustin P., Tzagoloff A., Munnich A., Rotig A. A mutation in the human heme A:farnesyltransferase gene (COX10) causes cytochrome c oxidase deficiency. Hum. Mol. Genet. 2000, 9:1245-1249.
150. van den Heuvel L., Ruitenbeek W., Smeets R., Gelman-Kohan Z., Elpeleg O., Loeffen J., Trijbels F., Mariman E., de Bruijn 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.
151. Van Kuilenburg A.B., Van Beeumen J.J., Van der Meer N.M., Muijsers A.O. Subunits VIIa, b, c of human cytochrome c oxidase. Identification of both 'heart-type' and 'liver-type' isoforms of subunit VIIa in human heart. Eur. J. Biochem. 1992, 203:193-199.
152. Vempati U.D., Torraco A., Moraes C.T. Mouse models of oxidative phosphorylation dysfunction and disease. Methods 2008, 46:241-247.
153. Vempati U.D., Han X., Moraes C.T. Lack of cytochrome c in mouse fibroblasts disrupts assembly/stability of respiratory complexes I and IV. J. Biol. Chem. 2009, 284:4383-4391.
154. Vesela K., Hulkova H., Hansikova H., Zeman J., Elleder M. Structural analysis of tissues affected by cytochrome C oxidase deficiency due to mutations in the SCO2 gene. APMIS 2008, 116:41-49.
155. Visapaa I., Fellman V., Vesa J., Dasvarma A., Hutton J.L., Kumar V., Payne G.S., Makarow M., Van Coster R., Taylor R.W., Turnbull D.M., Suomalainen A., Peltonen L. GRACILE syndrome, a lethal metabolic disorder with iron overload, is caused by a point mutation in BCS1L. Am. J. Hum. Genet. 2002, 71:863-876.
156. Viscomi C., Bottani E., Civiletto G., Cerutti R., Moggio M., Fagiolari G., Schon E.A., Lamperti C., Zeviani M. In vivo correction of COX deficiency by activation of the AMPK/PGC-1α axis. Cell Metab. 2011, 14:80-90.
157. Walker J.E., Collinson I.R., Van Raaij M.J., Runswick M.J. Structural analysis of ATP synthase from bovine heart mitochondria. Methods Enzymol. 1995, 260:163-190.
158. Watanabe T., Dewey M.J., Mintz B. Teratocarcinoma cells as vehicles for introducing specific mutant mitochondrial genes into mice. Proc. Natl. Acad. Sci. U. S. A. 1978, 75:5113-5117.
159. Weiher H., Noda T., Gray D.A., Sharpe A.H., Jaenisch R. Transgenic mouse model of kidney disease: insertional inactivation of ubiquitously expressed gene leads to nephrotic syndrome. Cell 1990, 62:425-434.
160. Wenz T., Diaz F., Spiegelman B.M., Moraes C.T. Activation of the PPAR/PGC-1alpha pathway prevents a bioenergetic deficit and effectively improves a mitochondrial myopathy phenotype. Cell Metab. 2008, 8:249-256.
161. Williams S.L., Taanman J.W., Hansikova H., Houst'kova H., Chowdhury S., Zeman J., Houstek J. A novel mutation in SURF1 causes skipping of exon 8 in a patient with cytochrome c oxidase-deficient Leigh syndrome and hypertrichosis. Mol. Genet. Metab. 2001, 73:340-343.
162. Yang H., Brosel S., Acin-Perez R., Slavkovich V., Nishino I., Khan R., Goldberg I.J., Graziano J., Manfredi G., Schon E.A. Analysis of mouse models of cytochrome c oxidase deficiency owing to mutations in Sco2. Hum. Mol. Genet. 2010, 19:170-180.
163. Yaplito-Lee J., Weintraub R., Jamsen K., Chow C.W., Thorburn D.R., Boneh A. Cardiac manifestations in oxidative phosphorylation disorders of childhood. J. Pediatr. 2007, 150:407-411.
164. Zordan M.A., Cisotto P., Benna C., Agostino A., Rizzo G., Piccin A., Pegoraro M., Sandrelli F., Perini G., Tognon G., De Caro R., Peron S., Kronnie T.T., Megighian A., Reggiani C., Zeviani M., Costa R. Post-transcriptional silencing and functional characterization of the Drosophila melanogaster homolog of human Surf1. Genetics 2006, 172:229-241.