Advertisement

Mitochondrial Cytochrome c Oxidase Assembly in Health and Human Diseases

Chapter

Abstract

Deficiencies in the mitochondrial cytochrome c oxidase (COX) or complex IV, the last enzyme of the mitochondrial respiratory chain, are a frequent cause of mitochondrial diseases in human. Eukaryotic COX is a multimeric copper-heme a, a 3-type oxidase, formed by three catalytic core subunits encoded in the mitochondrial genome and ten nuclear-encoded subunits that act as a protective shield of the core. The biogenesis of the catalytic core subunits, the incorporation of their metal prosthetic groups, and their assembly with imported subunits synthesized in the cytoplasm, involves a growing number of nuclear-encoded ancillary factors. Mutations in the structural subunits and in the assembly factors have been recognized over the last 15 years as important causes of human diseases. In this chapter, we review the current knowledge on human COX biogenesis and discuss the molecular basis of human COX deficiencies due to mutations in proteins involved in the COX assembly process.

Keywords

Mitochondria Cytochrome c oxidase assembly Complex IV Mitochondrial diseases 

Notes

Acknowledgments

Our research is supported by National Institutes of Health Research Grant GM071775A (to A.B.) and a Research Grant (to A.B.) and a Development Grant (to F.F.) from the Muscular Dystrophy Association.

References

  1. 1.
    Shoubridge EA (2001) Cytochrome c oxidase deficiency. Am J Med Genet 106:46–52PubMedCrossRefGoogle Scholar
  2. 2.
    Solans A, Zambrano A, Barrientos A (2004) Cytochrome c oxidase deficiency: from yeast to human. Preclinica 2:336–348Google Scholar
  3. 3.
    Zee JM, Glerum DM (2006) Defects in cytochrome oxidase assembly in humans: lessons from yeast. Biochem Cell Biol 84:859–869PubMedCrossRefGoogle Scholar
  4. 4.
    Pecina P, Houstkova H, Hansikova H et al (2004) Genetic defects of cytochrome c oxidase assembly. Physiol Res 53:213–223Google Scholar
  5. 5.
    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 272:1136–1144Google Scholar
  6. 6.
    Ostermeier C, Harrenga A, Ermler U et al (1997) Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc Natl Acad Sci U S A 94:10547–10553Google Scholar
  7. 7.
    Yoshikawa S, Shinzawa-Itoh K, Nakashima R et al (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280:1723–1729PubMedCrossRefGoogle Scholar
  8. 8.
    Barrientos A, Barros MH, Valnot I et al (2002) Cytochrome oxidase in health and disease. Gene 286:53–63PubMedCrossRefGoogle Scholar
  9. 9.
    Fontanesi F, Soto IC, Horn D et al (2006) Assembly of mitochondrial cytochrome c oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 291:C1129–1147CrossRefGoogle Scholar
  10. 10.
    Cobine PA, Pierrel F, Winge DR (2006) Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta 1763:759–772PubMedCrossRefGoogle Scholar
  11. 11.
    Saraste M (1990) Structural features of cytochrome oxidase. Q Rev Biophys 23:331–366PubMedCrossRefGoogle Scholar
  12. 12.
    Mitchell P, Moyle J (1967) Chemiosmotic hypothesis of oxidative phosphorylation. Nature 213:137–139PubMedCrossRefGoogle Scholar
  13. 13.
    Babcock GT, Wikstrom M (1992) Oxygen activation and the conservation of energy in cell respiration. Nature 356:301–309PubMedCrossRefGoogle Scholar
  14. 14.
    Brunori M, Antonini G, Malatesta F et al Cytochrome-c oxidase. Subunit structure and proton pumping. Eur J Biochem 169:1–8Google Scholar
  15. 15.
    Riistama S, Puustinen A, Garcia-Horsman A et al (1996) Channelling of dioxygen into the respiratory enzyme. Biochim Biophys Acta 1275:1–4PubMedCrossRefGoogle Scholar
  16. 16.
    Hosler JP (2004) The influence of subunit III of cytochrome c oxidase on the D pathway, the proton exit pathway and mechanism-based inactivation in subunit I. Biochim Biophys Acta 1655:332–339PubMedCrossRefGoogle Scholar
  17. 17.
    Nijtmans LG, Taanman JW, Muijsers AO et al (1998) Assembly of cytochrome-c oxidase in cultured human cells. Eur J Biochem 254:389–394PubMedCrossRefGoogle Scholar
  18. 18.
    Khalimonchuk O, Bestwick M, Meunier B et al (2010) Formation of the redox cofactor centers during Cox1 maturation in yeast cytochrome oxidase. Mol Cell Biol 30:1004–1017PubMedCrossRefGoogle Scholar
  19. 19.
    Williams SL, Valnot I, Rustin P et al (2004) Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1, or SURF1. J Biol Chem 279:7462–7469PubMedCrossRefGoogle Scholar
  20. 20.
    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 392:625–632PubMedCrossRefGoogle Scholar
  21. 21.
    Tzagoloff A, Dieckmann CL (1990) PET genes of Saccharomyces cerevisiae. Microbiol Rev 54:211–225PubMedGoogle Scholar
  22. 22.
    McEwen JE, Ko C, Kloeckner-Gruissem B et al (1986) Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. Characterization of mutants in 34 complementation groups. J Biol Chem 261:11872–11879PubMedGoogle Scholar
  23. 23.
    Fontanesi F, Soto IC, Horn D et al (2006) Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 291:C1129–1147CrossRefGoogle Scholar
  24. 24.
    Soto IC, Fontanesi F, Liu J et al (2012) Biogenesis and assembly of eukaryotic cytochrome C oxidase catalytic core. Biochim Biophys Acta 1817:883–897Google Scholar
  25. 25.
    Diaz F (2010) Cytochrome c oxidase deficiency: patients and animal models. Biochim Biophys Acta 1802:100–110Google Scholar
  26. 26.
    Barrientos A, Gouget K, Horn D et al (2009) Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process. Biochim Biophys Acta 1793:97–107PubMedCrossRefGoogle Scholar
  27. 27.
    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 41:833–837PubMedCrossRefGoogle Scholar
  28. 28.
    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 82:1281–1289PubMedCrossRefGoogle Scholar
  29. 29.
    Shteyer E, Saada A, Shaag A et al (2009) Exocrine pancreatic insufficiency, dyserythropoeitic anemia, and calvarial hyperostosis are caused by a mutation in the COX4I2 gene. Am J Hum Genet 84:412–417PubMedCrossRefGoogle Scholar
  30. 30.
    Zhu Z, Yao J, Johns T et al (1998) SURF1, encoding a factor involved in the biogenesis of cytochrome c oxidase, is mutated in Leigh syndrome. Nat Genet 20:337–343PubMedCrossRefGoogle Scholar
  31. 31.
    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 63:1609–1621PubMedCrossRefGoogle Scholar
  32. 32.
    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 88:488–493PubMedCrossRefGoogle Scholar
  33. 33.
    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 23:333–337PubMedCrossRefGoogle Scholar
  34. 34.
    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 67:1104–1109PubMedGoogle Scholar
  35. 35.
    Valnot I, von Kleist-Retzow JC, Barrientos A et al (2000) A mutation in the human heme A:farnesyltransferase gene (COX10) causes cytochrome c oxidase deficiency. Hum Mol Genet 9:1245–1249PubMedCrossRefGoogle Scholar
  36. 36.
    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 12:2693–2702PubMedCrossRefGoogle Scholar
  37. 37.
    Antonicka H, Mattman A, Carlson CG et al (2003) Mutations in COX15 produce a defect in the mitochondrial heme biosynthetic pathway, causing early-onset fatal hypertrophic cardiomyopathy. Am J Hum Genet 72:101–114PubMedCrossRefGoogle Scholar
  38. 38.
    Mootha VK, Lepage P, Miller K et al (2003) Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc Natl Acad Sci U S A 100:605–610PubMedCrossRefGoogle Scholar
  39. 39.
    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 41:833–837PubMedCrossRefGoogle Scholar
  40. 40.
    Scarpulla RC (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88:611–638PubMedCrossRefGoogle Scholar
  41. 41.
    Asin-Cayuela J, Gustafsson CM (2007) Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem Sci 32:111–117PubMedCrossRefGoogle Scholar
  42. 42.
    Shutt TE, Shadel GS (2010) A compendium of human mitochondrial gene expression machinery with links to disease. Environ Mol Mutagen 51:360–379PubMedGoogle Scholar
  43. 43.
    Bruno C, Martinuzzi A, Tang Y et al (1999) A stop-codon mutation in the human mtDNA cytochrome c oxidase I gene disrupts the functional structure of complex IV. Am J Hum Genet 65:611–620PubMedCrossRefGoogle Scholar
  44. 44.
    Varlamov DA, Kudin AP, Vielhaber S et al (2002) Metabolic consequences of a novel missense mutation of the mtDNA CO I gene. Hum Mol Genet 11:1797–1805PubMedCrossRefGoogle Scholar
  45. 45.
    Comi GP, Bordoni A, Salani S et al (1998) Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Ann Neurol 43:110–116PubMedCrossRefGoogle Scholar
  46. 46.
    Gattermann N, Retzlaff S, Wang YL et al (1997) Heteroplasmic point mutations of mitochondrial DNA affecting subunit I of cytochrome c oxidase in two patients with acquired idiopathic sideroblastic anemia. Blood 90:4961–4972PubMedGoogle Scholar
  47. 47.
    Karadimas CL, Greenstein P, Sue CM et al (2000) Recurrent myoglobinuria due to a nonsense mutation in the COX I gene of mitochondrial DNA. Neurology 55:644–649PubMedCrossRefGoogle Scholar
  48. 48.
    Kollberg G, Moslemi AR, Lindberg C et al (2005) Mitochondrial myopathy and rhabdomyolysis associated with a novel nonsense mutation in the gene encoding cytochrome c oxidase subunit I. J Neuropathol Exp Neurol 64:123–128PubMedGoogle Scholar
  49. 49.
    Tam EW, Feigenbaum A, Addis JB et al (2008) A novel mitochondrial DNA mutation in COX1 leads to strokes, seizures, and lactic acidosis. Neuropediatrics 39:328–334PubMedCrossRefGoogle Scholar
  50. 50.
    Rahman S, Taanman JW, Cooper JM et al (1999) A missense mutation of cytochrome oxidase subunit II causes defective assembly and myopathy. Am J Hum Genet 65:1030–1039PubMedCrossRefGoogle Scholar
  51. 51.
    Campos Y, Garcia-Redondo A, Fernandez-Moreno MA et al (2001) Early-onset multisystem mitochondrial disorder caused by a nonsense mutation in the mitochondrial DNA cytochrome C oxidase II gene. Ann Neurol 50:409–413PubMedCrossRefGoogle Scholar
  52. 52.
    Clark KM, Taylor RW, Johnson MA et al (1999) An mtDNA mutation in the initiation codon of the cytochrome C oxidase subunit II gene results in lower levels of the protein and a mitochondrial encephalomyopathy. Am J Hum Genet 64:1330–1339PubMedCrossRefGoogle Scholar
  53. 53.
    Zhadanov SI, Atamanov VV, Zhadanov NI et al (2006) De novo COX2 mutation in a LHON family of Caucasian origin: implication for the role of mtDNA polymorphism in human pathology. J Hum Genet 51:161–170PubMedCrossRefGoogle Scholar
  54. 54.
    Keightley JA, Hoffbuhr KC, Burton MD et al (1996) A microdeletion in cytochrome c oxidase (COX) subunit III associated with COX deficiency and recurrent myoglobinuria. Nat Genet 12:410–416PubMedCrossRefGoogle Scholar
  55. 55.
    Manfredi G, Schon EA, Moraes CT et al (1995) A new mutation associated with MELAS is located in a mitochondrial DNA polypeptide-coding gene. Neuromuscul Disord 5:391–398PubMedCrossRefGoogle Scholar
  56. 56.
    Hanna MG, Nelson IP, Rahman S et al (1998) Cytochrome c oxidase deficiency associated with the first stop-codon point mutation in human mtDNA. Am J Hum Genet 63:29–36PubMedCrossRefGoogle Scholar
  57. 57.
    Choi BO, Hwang JH, Kim J et al (2008) A MELAS syndrome family harboring two mutations in mitochondrial genome. Exp Mol Med 40:354–360PubMedCrossRefGoogle Scholar
  58. 58.
    Johns DR, Neufeld MJ (1993) Cytochrome c oxidase mutations in Leber hereditary optic neuropathy. Biochem Biophys Res Commun 196:810–815PubMedCrossRefGoogle Scholar
  59. 59.
    Tiranti V, Corona P, Greco M et al (2000) A novel frameshift mutation of the mtDNA COIII gene leads to impaired assembly of cytochrome c oxidase in a patient affected by Leigh-like syndrome. Hum Mol Genet 9:2733–2742PubMedCrossRefGoogle Scholar
  60. 60.
    Merante F, Petrova-Benedict R, MacKay N et al (1993) A biochemically distinct form of cytochrome oxidase (COX) deficiency in the Saguenay-Lac-Saint-Jean region of Quebec. Am J Hum Genet 53:481–487PubMedGoogle Scholar
  61. 61.
    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 21:1315–1323PubMedCrossRefGoogle Scholar
  62. 62.
    Seeger J, Schrank B, Pyle A et al (2010) Clinical and neuropathological findings in patients with TACO1 mutations. Neuromuscul Disord 20:720–724PubMedCrossRefGoogle Scholar
  63. 63.
    Fox TD (1996) Genetics of mitochondrial translation. In: Hershey JWB, Matthews MB and Sonenberg N (eds) Translational control, pp. 733–758. Cold Spring Harbor Press, Cold Spring HarborGoogle Scholar
  64. 64.
    Manthey GM, Przybyla-Zawislak BD, McEwen JE (1998) The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane. Eur J Biochem 255:156–161PubMedCrossRefGoogle Scholar
  65. 65.
    Mili S, Shu HJ, Zhao Y et al (2001) Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA. Mol Cell Biol 21:7307–7319PubMedCrossRefGoogle Scholar
  66. 66.
    Mili S, Pinol-Roma S (2003) LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs. Mol Cell Biol 23:4972–4982PubMedCrossRefGoogle Scholar
  67. 67.
    Xu F, Morin C, Mitchell G et al (2004) The role of the LRPPRC (leucine-rich pentatricopeptide repeat cassette) gene in cytochrome oxidase assembly: mutation causes lowered levels of COX (cytochrome c oxidase) I and COX III mRNA. Biochem J 382:331–336PubMedCrossRefGoogle Scholar
  68. 68.
    Cooper MP, Qu L, Rohas LM et al (2006) Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1alpha/LRP130 complex. Genes Dev 20:2996–3009PubMedCrossRefGoogle Scholar
  69. 69.
    Cooper MP, Uldry M, Kajimura S et al (2008) Modulation of PGC-1 coactivator pathways in brown fat differentiation through LRP130. J Biol Chem 283:31960–31967PubMedCrossRefGoogle Scholar
  70. 70.
    Horn D, Barrientos A (2008) Mitochondrial copper metabolism and delivery to cytochrome c oxidase. IUBMB Life 60:421–429PubMedCrossRefGoogle Scholar
  71. 71.
    Banci L, Bertini I, Cavallaro G et al (2007) The functions of Sco proteins from genome-based analysis. J Proteome Res 6:1568–1579PubMedCrossRefGoogle Scholar
  72. 72.
    Horng YC, Cobine PA, Maxfield AB et al (2004) Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J Biol Chem 279:35334–35340PubMedCrossRefGoogle Scholar
  73. 73.
    Glerum DM, Shtanko A, Tzagoloff A (1996) SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J Biol Chem 271:20531–20535PubMedCrossRefGoogle Scholar
  74. 74.
    Hiser L, Di Valentin M, Hamer AG et al (2000) Cox11p is required for stable formation of the Cu(B) and magnesium centers of cytochrome c oxidase. J Biol Chem 275:619–623PubMedCrossRefGoogle Scholar
  75. 75.
    Carr HS, George GN, Winge DR (2002) Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I)-binding protein. J Biol Chem 277:31237–31242PubMedCrossRefGoogle Scholar
  76. 76.
    Beers J, Glerum DM, Tzagoloff A (1997) Purification, characterization, and localization of yeast Cox17p, a mitochondrial copper shuttle. J Biol Chem 272:33191–33196PubMedCrossRefGoogle Scholar
  77. 77.
    Carr HS, Maxfield AB, Horng YC et al (2005) Functional analysis of the domains in Cox11. J Biol Chem 280:22664–22669PubMedCrossRefGoogle Scholar
  78. 78.
    Oswald C, Krause-Buchholz U, Rodel G (2009) Knockdown of human COX17 affects assembly and supramolecular organization of cytochrome c oxidase. J Mol Biol 389:470–479PubMedCrossRefGoogle Scholar
  79. 79.
    Krummeck G, Rodel G (1990) Yeast SCO1 protein is required for a post-translational step in the accumulation of mitochondrial cytochrome c oxidase subunits I and II. Curr Genet 18:13–15PubMedCrossRefGoogle Scholar
  80. 80.
    Glerum DM, Shtanko A, Tzagoloff A (1996) SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J Biol Chem 271:20531–20535PubMedCrossRefGoogle Scholar
  81. 81.
    Lode A, Kuschel M, Paret C et al (2000) Mitochondrial copper metabolism in yeast: interaction between Sco1p and Cox2p. FEBS Lett 485:19–24PubMedCrossRefGoogle Scholar
  82. 82.
    Rentzsch A, Krummeck-Weiss G, Hofer A et al (1999) Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr Genet 35:103–108PubMedCrossRefGoogle Scholar
  83. 83.
    Chinenov YV (2000) Cytochrome c oxidase assembly factors with a thioredoxin fold are conserved among prokaryotes and eukaryotes. J Mol Med (Berl) 78:239–242CrossRefGoogle Scholar
  84. 84.
    Abajian C, Rosenzweig AC (2006) Crystal structure of yeast Sco1. J Biol Inorg Chem 11:459–466PubMedCrossRefGoogle Scholar
  85. 85.
    Ye Q, Imriskova-Sosova I, Hill BC et al (2005) Identification of a disulfide switch in BsSco, a member of the Sco family of cytochrome c oxidase assembly proteins. Biochem 44:2934–2942CrossRefGoogle Scholar
  86. 86.
    Smits PH, De Haan M, Maat C et al (1994) The complete sequence of a 33 kb fragment on the right arm of chromosome II from Saccharomyces cerevisiae reveals 16 open reading frames, including ten new open reading frames, five previously identified genes and a homologue of the SCO1 gene. Yeast (10 Suppl A):S75–80Google Scholar
  87. 87.
    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 13:1839–1848PubMedCrossRefGoogle Scholar
  88. 88.
    Leary SC, Sasarman F, Nishimura T et al (2009) Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1. Hum Mol Genet 18:2230–2240PubMedCrossRefGoogle Scholar
  89. 89.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2010) Affinity gradients drive copper to cellular destinations. Nat 465:645–648CrossRefGoogle Scholar
  90. 90.
    Banci L, Bertini I, Ciofi-Baffoni S et al (2008) Mitochondrial copper(I) transfer from Cox17 to Sco1 is coupled to electron transfer. Proc Natl Acad Sci U S A 105:6803–6808PubMedCrossRefGoogle Scholar
  91. 91.
    Chinenov YV (2000) Cytochrome c oxidase assembly factors with a thioredoxin fold are conserved among prokaryotes and eukaryotes. J Mol Med (Berl) 78:239–242CrossRefGoogle Scholar
  92. 92.
    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 5:9–20PubMedCrossRefGoogle Scholar
  93. 93.
    Dodani SC, Leary SC, Cobine PA et al (2011) A targetable fluorescent sensor reveals that copper-deficient SCO1 and SCO2 patient cells prioritize mitochondrial copper homeostasis. J Am Chem Soc 133:8606–8616PubMedCrossRefGoogle Scholar
  94. 94.
    Yang H, Brosel S, Acin-Perez R et al (2010) Analysis of mouse models of cytochrome c oxidase deficiency owing to mutations in Sco2. Hum Mol Genet 19:170–180PubMedCrossRefGoogle Scholar
  95. 95.
    Horng YC, Leary SC, Cobine PA et al (2005) Human Sco1 and Sco2 function as copper-binding proteins. J Biol Chem 280:34113–34122PubMedCrossRefGoogle Scholar
  96. 96.
    Jaksch M, Ogilvie I, Yao J et al (2000) Mutations in SCO2 are associated with a distinct form of hypertrophic cardiomyopathy and cytochrome c oxidase deficiency. Hum Mol Genet 9:795–801PubMedCrossRefGoogle Scholar
  97. 97.
    Jaksch M, Horvath R, Horn N et al (2001) Homozygosity (E140K) in SCO2 causes delayed infantile onset of cardiomyopathy and neuropathy. Neurol 57:1440–1446CrossRefGoogle Scholar
  98. 98.
    Sacconi S, Salviati L, Sue CM et al (2003) Mutation screening in patients with isolated cytochrome c oxidase deficiency. Pediatr Res 53:224–230PubMedCrossRefGoogle Scholar
  99. 99.
    Salviati L, Sacconi S, Rasalan MM et al (2002) Cytochrome c oxidase deficiency due to a novel SCO2 mutation mimics Werdnig-Hoffmann disease. Arch Neurol 59:862–865PubMedCrossRefGoogle Scholar
  100. 100.
    Bohm M, Pronicka E, Karczmarewicz E et al (2006) Retrospective, multicentric study of 180 children with cytochrome C oxidase deficiency. Pediatr Res 59:21–26PubMedCrossRefGoogle Scholar
  101. 101.
    Vesela K, Hansikova H, Tesarova M et al (2004) Clinical, biochemical and molecular analyses of six patients with isolated cytochrome c oxidase deficiency due to mutations in the SCO2 gene. Acta Paediatr 93:1312–1317PubMedCrossRefGoogle Scholar
  102. 102.
    Tarnopolsky MA, Bourgeois JM, Fu MH et al (2004) Novel SCO2 mutation (G1521A) presenting as a spinal muscular atrophy type I phenotype. Am J Med Genet A 125A:310–314CrossRefGoogle Scholar
  103. 103.
    Knuf M, Faber J, Huth RG et al (2007) Identification of a novel compound heterozygote SCO2 mutation in cytochrome c oxidase deficient fatal infantile cardioencephalomyopathy. Acta Paediatr 96:130–132PubMedCrossRefGoogle Scholar
  104. 104.
    Verdijk RM, de Krijger R, Schoonderwoerd K et al (2008) Phenotypic consequences of a novel SCO2 gene mutation. Am J Med Genet A 146A:2822–2827Google Scholar
  105. 105.
    Leary SC, Mattman A, Wai T et al (2006) A hemizygous SCO2 mutation in an early onset rapidly progressive, fatal cardiomyopathy. Mol Genet Metab 89:129–133PubMedCrossRefGoogle Scholar
  106. 106.
    Mobley BC, Enns GM, Wong LJ et al (2009) A novel homozygous SCO2 mutation, p.G193S, causing fatal infantile cardioencephalomyopathy. Clin Neuropathol 28:143–149PubMedGoogle Scholar
  107. 107.
    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 42:227–230PubMedCrossRefGoogle Scholar
  108. 108.
    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 insufficiency. Eur J Paediatr Neurol 14:253–260PubMedCrossRefGoogle Scholar
  109. 109.
    Cobine PA, Pierrel F, Leary SC et al (2006) The P174L mutation in human Sco1 severely compromises Cox17-dependent metallation but does not impair copper binding. J Biol Chem 281:12270–12276PubMedCrossRefGoogle Scholar
  110. 110.
    Bohm M, Pronicka E, Karczmarewicz E et al (2006) Retrospective, multicentric study of 180 children with cytochrome C oxidase deficiency. Pediatr Res 59:21–26Google Scholar
  111. 111.
    Foltopoulou PF, Zachariadis GA, Politou AS et al (2004) Human recombinant mutated forms of the mitochondrial COX assembly Sco2 protein differ from wild-type in physical state and copper binding capacity. Mol Genet Metab 81:225–236PubMedCrossRefGoogle Scholar
  112. 112.
    Dickinson EK, Adams DL, Schon EA et al (2000) A human SCO2 mutation helps define the role of Sco1p in the cytochrome oxidase assembly pathway. J Biol Chem 275:26780–26785PubMedCrossRefGoogle Scholar
  113. 113.
    Stiburek L, Hansikova H, Tesarova M et al (2006) Biogenesis of eukaryotic cytochrome c oxidase. Physiol Res 55(Suppl 2):S27–41Google Scholar
  114. 114.
    Caughey WS, Smythe GA, O’Keeffe DH et al (1975) Heme A of cytochrome c oxicase. Structure and properties: comparisons with hemes B, C, and S and derivatives. J Biol Chem 250:7602–7622PubMedGoogle Scholar
  115. 115.
    Tzagoloff A, Nobrega M, Gorman N et al (1993) On the functions of the yeast COX10 and COX11 gene products. Biochem Mol Biol Int 31:593–598PubMedGoogle Scholar
  116. 116.
    Barros MH, Nobrega FG, Tzagoloff A (2002) Mitochondrial ferredoxin is required for heme A synthesis in Saccharomyces cerevisiae. J Biol Chem 277:9997–10002PubMedCrossRefGoogle Scholar
  117. 117.
    Brown KR, Allan BM, Do P et al (2002) Identification of novel hemes generated by heme A synthase: evidence for two successive monooxygenase reactions. Biochem 41:10906–10913CrossRefGoogle Scholar
  118. 118.
    Barros MH, Carlson CG, Glerum DM et al (2001) Involvement of mitochondrial ferredoxin and Cox15p in hydroxylation of heme O. FEBS Lett 492:133–138PubMedCrossRefGoogle Scholar
  119. 119.
    Glerum DM, Tzagoloff A (1994) Isolation of a human cDNA for heme A:farnesyltransferase by functional complementation of a yeast cox10 mutant. Proc Natl Acad Sci U S A 91:8452–8456PubMedCrossRefGoogle Scholar
  120. 120.
    Coenen MJ, Van Den Heuvel LP, Ugalde C et al (2004) Cytochrome c oxidase biogenesis in a patient with a mutation in COX10 gene. Ann Neurol 56:560–564PubMedCrossRefGoogle Scholar
  121. 121.
    Coenen MJ, Smeitink JA, Pots JM et al (2006) Sequence analysis of the structural nuclear encoded subunits and assembly genes of cytochrome c oxidase in a cohort of 10 isolated complex IV-deficient patients revealed five mutations. J Child Neuro 21:508–511Google Scholar
  122. 122.
    Bugiani M, Tiranti V, Farina L et al (2005) Novel mutations in COX15 in a long surviving Leigh syndrome patient with cytochrome c oxidase deficiency. J Med Genet 42:e28Google Scholar
  123. 123.
    Alfadhel M, Lillquist YP, Waters PJ et al (2011) Infantile cardioencephalopathy due to a COX15 gene defect: report and review. Am J Med Genet A 155A:840–844CrossRefGoogle Scholar
  124. 124.
    Oquendo CE, Antonicka H, Shoubridge EA et al (2004) Functional and genetic studies demonstrate that mutation in the COX15 gene can cause Leigh syndrome. J Med Genet 41:540–544PubMedCrossRefGoogle Scholar
  125. 125.
    Williams SL, Valnot I, Rustin P et al (2004) Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1, or SURF1. J Biol Chem 279:7462–7469PubMedCrossRefGoogle Scholar
  126. 126.
    Barros MH, Tzagoloff A (2002) Regulation of the heme A biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett 516:119–123PubMedCrossRefGoogle Scholar
  127. 127.
    Bestwick M, Khalimonchuk O, Pierrel F et al (2010) The role of Coa2 in hemylation of yeast Cox1 revealed by its genetic interaction with Cox10. Mol Cell Biol 30:172–185PubMedCrossRefGoogle Scholar
  128. 128.
    Leigh D (1951) Subacute necrotizing encephalomyelopathy in an infant. J Neurol Neurosurg Psychiatry 14:216–221PubMedCrossRefGoogle Scholar
  129. 129.
    Von Kleist-Retzow JC, Yao J, Taanman JW et al (2001) Mutations in SURF1 are not specifically associated with Leigh syndrome. J Med Genet 38:109–113CrossRefGoogle Scholar
  130. 130.
    Williams SL, Taanman JW, Hansikova H et al (2001) 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 73:340–343PubMedCrossRefGoogle Scholar
  131. 131.
    Tay SK, Sacconi S, Akman HO et al (2005) Unusual clinical presentations in four cases of Leigh disease, cytochrome C oxidase deficiency, and SURF1 gene mutations. J Child Neurol 20:670–674PubMedCrossRefGoogle Scholar
  132. 132.
    Rahman S, Brown RM, Chong WK et al (2001) A SURF1 gene mutation presenting as isolated leukodystrophy. Ann Neurol 49:797–800PubMedCrossRefGoogle Scholar
  133. 133.
    Mashkevich G, Repetto B, Glerum DM et al (1997) SHY1, the yeast homolog of the mammalian SURF-1 gene, encodes a mitochondrial protein required for respiration. J Biol Chem 272:14356–14364PubMedCrossRefGoogle Scholar
  134. 134.
    Smith D, Gray J, Mitchell L et al (2005) Assembly of cytochrome-c oxidase in the absence of assembly protein Surf1p leads to loss of the active site heme. J Biol Chem 280:17652–17656PubMedCrossRefGoogle Scholar
  135. 135.
    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 284:25735–25741PubMedCrossRefGoogle Scholar
  136. 136.
    Pierrel F, Bestwick ML, Cobine PA et al (2007) Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBO J 26:4335–4346PubMedCrossRefGoogle Scholar
  137. 137.
    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 392:625–632PubMedCrossRefGoogle Scholar
  138. 138.
    Fontanesi F, Jin C, Tzagoloff A et al (2008) Transcriptional activators HAP/NF-Y rescue a cytochrome c oxidase defect in yeast and human cells. Hum Mol Genet 17:775–788PubMedCrossRefGoogle Scholar
  139. 139.
    Tiranti V, Jaksch M, Hofmann S et al (1999) Loss-of-function mutations of SURF-1 are specifically associated with Leigh syndrome with cytochrome c oxidase deficiency. Ann Neurol 46:161–166PubMedCrossRefGoogle Scholar
  140. 140.
    Tiranti V, Lamantea E, Uziel G et al (1999) Leigh syndrome transmitted by uniparental disomy of chromosome 9. J Med Genet 36:927–928PubMedGoogle Scholar
  141. 141.
    Yao J, Shoubridge EA (1999) Expression and functional analysis of SURF1 in Leigh syndrome patients with cytochrome c oxidase deficiency. Hum Mol Genet 8:2541–2549PubMedCrossRefGoogle Scholar
  142. 142.
    Poyau A, Buchet K, Bouzidi MF et al (2000) Missense mutations in SURF1 associated with deficient cytochrome c oxidase assembly in Leigh syndrome patients. Hum Genet 106:194–205PubMedCrossRefGoogle Scholar
  143. 143.
    Coenen MJ, Van Den Heuvel LP, Nijtmans LG et al (1999) SURFEIT-1 gene analysis and two-dimensional blue native gel electrophoresis in cytochrome c oxidase deficiency. Biochem Biophys Res Commun 265:339–344PubMedCrossRefGoogle Scholar
  144. 144.
    Reinhold R, Bareth B, Balleininger M et al (2011) Mimicking a SURF1 allele reveals uncoupling of cytochrome c oxidase assembly from translational regulation in yeast. Hum Mol Genet 20:2379–2393PubMedCrossRefGoogle Scholar
  145. 145.
    Piekutowska-Abramczuk D, Magner M, Popowska E et al (2009) SURF1 missense mutations promote a mild Leigh phenotype. Clin Genet 76:195–204PubMedCrossRefGoogle Scholar
  146. 146.
    Salviati L, Freehauf C, Sacconi S et al (2004) Novel SURF1 mutation in a child with subacute encephalopathy and without the radiological features of Leigh Syndrome. Am J Med Genet A 128A:195–198CrossRefGoogle Scholar
  147. 147.
    Teraoka M, Yokoyama Y, Ninomiya S et al (1999) Two novel mutations of SURF1 in Leigh syndrome with cytochrome c oxidase deficiency. Hum Genet 105:560–563PubMedCrossRefGoogle Scholar
  148. 148.
    Ogawa Y, Naito E, Ito M et al (2002) Three novel SURF-1 mutations in Japanese patients with Leigh syndrome. Pediatr Neurol 26:196–200PubMedCrossRefGoogle Scholar
  149. 149.
    von Kleist-Retzow JC, Vial E, Chantrel-Groussard K et al (1999) Biochemical, genetic and immunoblot analyses of 17 patients with an isolated cytochrome c oxidase deficiency. Biochim Biophys Acta 1455:35–44PubMedCrossRefGoogle Scholar
  150. 150.
    Sue CM, Karadimas C, Checcarelli N et al (2000) Differential features of patients with mutations in two COX assembly genes, SURF-1 and SCO2. Ann Neurol 47:589–595PubMedCrossRefGoogle Scholar
  151. 151.
    Santoro L, Carrozzo R, Malandrini A et al (2000) A novel SURF1 mutation results in Leigh syndrome with peripheral neuropathy caused by cytochrome c oxidase deficiency. Neuromuscul Disord 10:450–453PubMedCrossRefGoogle Scholar
  152. 152.
    Pequignot MO, Dey R, Zeviani M et al (2001) Mutations in the SURF1 gene associated with Leigh syndrome and cytochrome C oxidase deficiency. Hum Mutat 17:374–381PubMedCrossRefGoogle Scholar
  153. 153.
    Pequignot MO, Desguerre I, Dey R et al (2001) New splicing-site mutations in the SURF1 gene in Leigh syndrome patients. J Biol Chem 276:15326–15329PubMedCrossRefGoogle Scholar
  154. 154.
    Bruno C, Biancheri R, Garavaglia B et al (2002) A novel mutation in the SURF1 gene in a child with Leigh disease, peripheral neuropathy, and cytochrome-c oxidase deficiency. J Child Neurol 17:233–236PubMedCrossRefGoogle Scholar
  155. 155.
    Capkova M, Hansikova H, Godinot C et al (2002) A new missense mutation of 574C>T in the SURF1 gene—biochemical and molecular genetic study in seven children with Leigh syndrome. Cas Lek Cesk 141:636–641PubMedGoogle Scholar
  156. 156.
    Rossi A, Biancheri R, Bruno C et al (2003) Leigh syndrome with COX deficiency and SURF1 gene mutations: MR imaging findings. AJNR Am J Neuroradiol 24:1188–1191PubMedGoogle Scholar
  157. 157.
    Pecina P, Capkova M, Chowdhury SK et al (2003) Functional alteration of cytochrome c oxidase by SURF1 mutations in Leigh syndrome. Biochim Biophys Acta 1639:53–63PubMedCrossRefGoogle Scholar
  158. 158.
    Moslemi AR, Tulinius M, Darin N et al (2003) SURF1 gene mutations in three cases with Leigh syndrome and cytochrome c oxidase deficiency. Neurology 61:991–993PubMedCrossRefGoogle Scholar
  159. 159.
    Darin N, Moslemi AR, Lebon S et al (2003) Genotypes and clinical phenotypes in children with cytochrome-c oxidase deficiency. Neuropediatrics 34:311–317PubMedCrossRefGoogle Scholar
  160. 160.
    Head RA, Brown RM, Brown GK (2004) Diagnostic difficulties with common SURF1 mutations in patients with cytochrome oxidase-deficient Leigh syndrome. J Inherit Metab Dis 27:57–65PubMedCrossRefGoogle Scholar
  161. 161.
    Monnot S, Chabrol B, Cano A et al (2005) Cytochrome c oxydase-deficient Leigh syndrome with homozygous mutation in SURF1 gene. Arch Pediatr 12:568–571PubMedCrossRefGoogle Scholar
  162. 162.
    Ostergaard E, Bradinova I, Ravn SH et al (2005) Hypertrichosis in patients with SURF1 mutations. Am J Med Genet A 138:384–388PubMedGoogle Scholar
  163. 163.
    van Riesen AK, Antonicka H, Ohlenbusch A et al (2006) Maternal segmental disomy in Leigh syndrome with cytochrome c oxidase deficiency caused by homozygous SURF1 mutation. Neuropediatrics 37:88–94PubMedCrossRefGoogle Scholar
  164. 164.
    Piekutowska-Abramczuk D, Popowska E, Pronicki M et al (2009) High prevalence of SURF1 c.845_846delCT mutation in Polish Leigh patients. Eur J Paediatr Neurol 13:146–153PubMedCrossRefGoogle Scholar
  165. 165.
    Zhang Y, Yang YL, Sun F et al (2007) Clinical and molecular survey in 124 Chinese patients with Leigh or Leigh-like syndrome. J Inherit Metab Dis 30:265PubMedCrossRefGoogle Scholar
  166. 166.
    Sacconi S, Salviati L, Sue CM et al (2003) Mutation screening in patients with isolated cytochrome c oxidase deficiency. Pediatr Res 53:224–230PubMedCrossRefGoogle Scholar
  167. 167.
    Rotig A, Lebon S, Zinovieva E et al (2004) Molecular diagnostics of mitochondrial disorders. Biochim Biophys Acta 1659:129–135PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2013

Authors and Affiliations

  1. 1.Department of NeurologyMiller School of Medicine, University of MiamiMiamiUSA

Personalised recommendations