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

Human Molecular Genetics

Volumn 12, Issue 20, 2003, Pages 2693-2702

  Antonicka, Hana ^a,b   Leary, Scot C ^a,b   Guercin, Guy Hellen ^a   Agar, Jeffrey N ^a   Horvath, Rita ^d   Kennaway, Nancy G ^c   Harding, Cary O ^c   Jaksch, Michaela ^d   Shoubridge, Eric A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d Institute of Clinical Chemistry Molecular Diagnostics and Mitochondrial Genetics   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CITRIC ACID; CYTOCHROME C OXIDASE; HEME; RETROVIRUS VECTOR; VINYL DERIVATIVE;

ALLELE; AMINO ACID SUBSTITUTION; ANEMIA; ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CASE REPORT; CATALYSIS; CHROMOSOME; CONTROLLED STUDY; CYTOCHROME C OXIDASE DEFICIENCY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; FAMILIAL DISEASE; FATALITY; FEMALE; FIBROBLAST; GENE MUTATION; GENE TRANSFER; GENETIC CONSERVATION; GENETIC MODEL; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; INFANT; INFANT DISEASE; KIDNEY TUBULE DISORDER; LACTIC ACIDOSIS; LEIGH DISEASE; LEUKODYSTROPHY; MALE; MITOCHONDRION; MUSCLE TISSUE; MUTATIONAL ANALYSIS; NONHUMAN; ORTHOLOGY; PERCEPTION DEAFNESS; PHENOTYPE; PRIORITY JOURNAL; PROKARYOTE; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; CARDIOMYOPATHIES; CATALYSIS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMOSOMES; CLONING, MOLECULAR; DNA MUTATIONAL ANALYSIS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXONS; FIBROBLASTS; GENETIC COMPLEMENTATION TEST; GENOME; HEME; HUMANS; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; RETROVIRIDAE;

ANIMALIA; PROKARYOTA; UNIDENTIFIED RETROVIRUS;

EID: 0142154270     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg284     Document Type: Article

References (49)

1. Robinson, B.H. (2000) Human cytochrome oxidase deficiency. Pediatr. Res., 48, 581-585.
2. Shoubridge, E.A. (2001) Cytochrome c oxidase deficiency. Am. J. Med. Genet., 106, 46-52.
3. Shoubridge, E.A. (2001) Nuclear genetic defects of oxidative phosphorylation. Hum. Mol. Genet., 10, 2277-2284.
4. Barrientos, A., Barros, M.H., Valnot, I., Rotig, A., Rustin, P. and Tzagoloff, A. (2002) Cytochrome oxidase in health and disease. Gene, 286, 53-63.
5. Capaldi, R.A. (1990) Structure and assembly of cytochrome c oxidase. Arch. Biochem. Biophys., 280, 252-262.
6. Yoshikawa, S., Shinzawa-Itoh, K. and Tsukihara, T. (1998) Crystal structure of bovine heart cytochrome c oxidase at 2.8 A resolution. J. Bioenerg. Biomembr, 30, 7-14.
7. Grivell, L.A., Artal-Sanz, M., Hakkaart, G., de Jong, L., Nijtmans, L.G., van Oosterum, K., Siep, M. and van der Spek, H. (1999) Mitochondrial assembly in yeast. FEBS Lett., 452, 57-60.
8. McEwen, J.E., Ko, C., Kloeckner-Gruissem, B. and Poyton, R.O. (1986) Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. Characterization of mutants in 34 complementation groups. J. Biol. Chem., 261, 11872-11879.
9. Tzagoloff, A. and Dieckmann, C.L. (1990) PET genes of Saccharomyces cerevisiae. Microbiol. Rev., 54, 211-225.
10. Jaksch, M., Ogilvie, I., Yao, J., Kortenhaus, G., Bresser, H.G., Gerbitz, K.D. and Shoubridge, E.A. (2000) Mutations in SCO2 are associated with a distinct form of hypertrophic cardiomyopathy and cytochrome c oxidase deficiency. Hum. Mol. Genet., 9, 795-801.
11. Adams, P.L., Lightowlers, R.N. and Turnbull, D.M. (1997) Molecular analysis of cytochrome c oxidase deficiency in Leigh's syndrome. Ann. Neurol., 41, 268-270.
12. Jaksch, M., Hofmann, S., Kleinle, S., Liechti-Gallati, S., Pongratz, D.E., Muller-Hocker, J., Jedele, K.B., Meitinger, T. and Gerbitz, K.D. (1998) A systematic mutation screen of 10 nuclear and 25 mitochondrial candidate genes in 21 patients with cytochrome c oxidase (COX) deficiency shows tRNA(Ser)(UCN) mutations in a subgroup with syndromal encephalopathy. J. Med. Genet., 35, 895-900.
13. Tiranti, V., Hoertnagel, K., Carrozzo, R., Galimberti, C., Munaro, M., Granatiero, M., Zelante, L., Gasparini, P., Marzella, R., Rocchi, M., Bayona-Bafaluy, M.P. et al. (1998) Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency. Am. J. Hum. Genet., 63, 1609-1621.
14. Zhu, Z., Yao, J., Johns, T., Fu, K., De Bie, I., Macmillan, C., Cuthbert, A.P., Newbold, R.F., Wang, J., Chevrette, M., Brown, G.K., Brown, R.M. and Shoubridge, E.A. (1998) SURF1, encoding a factor involved in the biogenesis of cytochrome c oxidase, is mutated in Leigh syndrome. Nat. Genet., 20, 337-343.
15. 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. et al. (1999) Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat. Genet., 23, 333-337.
16. Antonicka, H., Mattman, A., Carlson, C.G., Glerum, D.M., Hoffbuhr, K.C., Leary, S.C., Kennaway, N.G. and Shoubridge, E.A. (2003) Mutations in COX15 produce a defect in the mitochondrial heme biosynthetic pathway, causing early-onset fatal hypertrophic cardiomyopathy. Am. J. Hum. Genet., 72, 101-114.
17. Valnot, I., Osmond, S., Gigarel, N., Mehaye, B., Amiel, J., Cormier-Daire, V., Munnich, A., Bonnefont, J.P., Rustin, P. and Rotig, A. (2000) Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am. J. Hum. Genet., 67, 1104-1109.
18. Valnot, I., von Kleist-Retzow, J.C., Barrientos, A., Gorbatyuk, M., Taanman, J.W., Mehaye, B., Rustin, P., Tzagoloff, A., Munnich, A. and Rotig, A. (2000) A mutation in the human heme A:farnesyltransferase gene (COX10) causes cytochrome c oxidase deficiency. Hum. Mol. Genet., 9, 1245-1249.
19. Mootha, V.K., Lepage, P., Miller, K., Bunkenborg, J., Reich, M., Hjerrild, M., Delmonte, T., Villeneuve, A., Sladek, R., Xu, F. et al. (2003) Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc. Natl Acad. Sci. USA, 100, 605-610.
20. Nobrega, M.P., Nobrega, F.G. and Tzagoloff, A. (1990) COX10 codes for a protein homologous to the ORF1 product of Paracoccus denitrificans and is required for the synthesis of yeast cytochrome oxidase. J. Biol. Chem., 265, 14220-14226.
21. Barros, M.H., Carlson, C.G., Glerum, D.M. and Tzagoloff, A. (2001) Involvement of mitochondrial ferredoxin and Cox15p in hydroxylation of heme O. FEBS Lett., 492, 133-138.
22. Barros, M.H., Nobrega, F.G. and Tzagoloff, A. (2002) Mitochondrial ferredoxin is required for heme A synthesis in Saccharomyces cerevisiae. J. Biol. Chem., 277, 9997-10002.
23. Barros, M.H. and Tzagoloff, A. (2002) Regulation of the heme A biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett., 516, 119-123.
24. Brown, K.R., Allan, B.M., Do, P. and Hegg, E.L. (2002) Identification of novel hemes generated by heme A synthase: evidence for two successive monooxygenase reactions. Biochemistry, 41, 10906-10913.
25. Schmidt, T.R., Goodman, M. and Grossman, L.I. (2002) Amino acid replacement is rapid in primates for the mature polypeptides of COX subunits, but not for their targeting presequences. Gene, 286, 13-19.
26. Chepuri, V. and Gennis, R.B. (1990) The use of gene fusions to determine the topology of all of the subunits of the cytochrome o terminal oxidase complex of Escherichia coli. J. Biol. Chem., 265, 12978-12986.
27. Mogi, T., Saiki, K. and Anraku, Y. (1994) Biosynthesis and functional role of haem O and haem A. Mol. Microbiol., 14, 391-398.
28. Saiki, K., Mogi, T., Hori, H., Tsubaki, M. and Anraku, Y. (1993) Identification of the functional domains in heme O synthase. Site-directed mutagenesis studies on the cyoE gene of the cytochrome bo operon in Escherichia coli. J. Biol. Chem., 268, 26927-26934.
29. Nijtmans, L.G., Taanman, J.W., Muijsers, A.O., Speijer, D. and Van den Bogert, C. (1998) Assembly of cytochrome-c oxidase in cultured human cells. Eur. J. Biochem., 254, 389-394.
30. Bratton, M.R., Hiser, L., Antholine, W.E., Hoganson, C. and Hosler, J.P. (2000) Identification of the structural subunits required for formation of the metal centers in subunit I of cytochrome c oxidase of Rhodohacter sphaeroides. Biochemistry, 39, 12989-12995.
31. Coenen, M.J., van den Heuvel, L.P., Nijtmans, L.G., Morava, E., Marquardt, I., Girschick, H.J., Trijbels, F.J., Grivell, L.A. and Smeitink, J.A. (1999) SURFEIT-1 gene analysis and two-dimensional blue native gel electrophoresis in cytochrome c oxidase deficiency. Biochem. Biophys. Res. Commun., 265, 339-344.
32. Tiranti, V., Galimberti, C., Nijtmans, L., Bovolenta, S., Perini, M.P. and Zeviani, M. (1999) Characterization of SURF-1 expression and Sort-1p function in normal and disease conditions. Hum. Mol. Genet., 8, 2533-2540.
33. Atamna, H., Liu, J. and Ames, B.N. (2001) Heme deficiency selectively interrupts assembly of mitochondrial complex IV in human fibroblasts: revelance to aging. J. Biol. Chem., 276, 48410-48416.
34. Rotig, A., Cormier, V., Blanche, S., Bonnefont, J.P., Ledeist, F., Romero, N., Schmitz, J., Rustin, P., Fischer, A., Saudubray, J.M. et al. (1990) Pearson's marrow-pancreas syndrome. A multisystem mitochondrial disorder in infancy. J. Clin. Invest., 86, 1601-1608.
35. Benit, P., Chretien, D., Kadhom, N., de Lonlay-Debeney, P., Cormier-Daire, V., Cabral, A., Peudenier, S., Rustin, R., Munnich, A. and Rotig, A. (2001) Large-scale deletion and point mutations of the nuclear NDUFV1 and NDUFS1 genes in mitochondrial complex I deficiency. Am. J. Hum. Genet., 68, 1344-1352.
36. Gattermann, N., Retzlaff, S., Wang, Y.L., Hofhaus, G., Heinisch, J., Aul, C. and Schneider, W. (1997) Heteroplasmic point mutations of mitochondrial DNA affecting subunit I of cytochrome c oxidase in two patients with acquired idiopathic sideroblastic anemia. Blood, 90, 4961-4972.
37. Yao, J. and Shoubridge, E.A. (1999) Expression and functional analysis of SURF1 in Leigh syndrome patients with cytochrome c oxidase deficiency. Hum. Mol. Genet., 8, 2541-2549.
38. Keightley, J.A., Hoffbuhr, K.C., Burton, M.D., Salas, V.M., Johnston, W.S., Penn, A.M., Buist, N.R. and Kennaway, N.G. (1996) A microdeletion in cytochrome c oxidase (COX) subunit III associated with COX deficiency and recurrent myoglobinuria. Nat. Genet., 12, 410-416.
39. Schagger, H. and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem., 199, 223-231.
40. Klement, P., Nijtmans, L.G., Van den Bogert, C. and Houstek, J. (1995) Analysis of oxidative phosphorylation complexes in cultured human fibroblasts and ammocytes by blue-native-electrophoresis using mitoplasts isolated with the help of digitonin. Anal. Biochem., 231, 219-224.
41. Zerbetto, E., Vergani, L. and Dabbeni-Sala, F. (1997) Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis, 18, 2059-2064.
42. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem., 166, 368-379.
43. Capaldi, R.A., Marusich, M.F. and Taanman, J.W. (1995) Mammalian cytochrome-c oxidase: characterization of enzyme and immunological detection of subunits in tissue extracts and whole cells. Meth. Enzymol., 260, 117-132.
44. Srere, P.A. (1969) Citrate synthase. Meth. Enzymol., 13, 326.
45. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
46. Miller, A.D., Miller, D.G., Garcia, J.V. and Lynch, C.M. (1993) Use of retroviral vectors for gene transfer and expression. Meth. Enzymol., 217, 581-599.
47. Markowitz, D.G., Goff, S.P. and Bank, A. (1988) Safe and efficient ecotropic and amphotropic packaging lines for use in gene transfer experiments. Trans. Assoc. Am. Physicians, 101, 212-218.
48. Miller, A.D. and Buttimore, C. (1986) Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell. Biol., 6, 2895-2902.
49. Lochmuller, H., Johns, T. and Shoubridge, E.A. (1999) Expression of the E6 and E7 genes of human papillomavirus (HPV16) extends the life span of human myoblasts. Exp. Cell. Res., 248, 186-193.