HCOA3 stabilizes cytochrome c oxidase 1 (COX1) and promotes cytochrome c oxidase assembly in human mitochondria

Journal of Biological Chemistry

Volumn 288, Issue 12, 2013, Pages 8321-8331

  Clemente, Paula ^a,b,e   Peralta, Susana ^a,c   Cruz Bermudez, Alberto ^a,b   Echevarría, Lucía ^a,b,f   Fontanesi, Flavia ^c   Barrientos, Antoni ^c   Fernandez Moreno, Miguel A ^a,b,d   Garesse, Rafael ^a,b,d  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Instituto de Investigación Sanitaria Hospital 12 de Octubre ^*  (Spain)

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

^d Comunidad de Madrid ^*  (Spain)

^e KAROLINSKA INSTITUTE   (Sweden)

^f LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASSEMBLY PROCESS; CYTOCHROME C OXIDASE; ENERGY PRODUCTIONS; HUMAN MITOCHONDRIA; MITOCHONDRIAL DISEASE; MITOCHONDRIAL RESPIRATORY CHAIN; SEQUENCE SIMILARITY; TRANS-MEMBRANE PROTEINS;

DIAGNOSIS; MACHINERY; PROTEINS;

MITOCHONDRIA;

CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE ASSEMBLY FACTOR; MEMBRANE PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBUNIT; ENZYME SYNTHESIS; GENE SILENCING; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; RESPIRATORY CHAIN; SEQUENCE HOMOLOGY;

ELECTRON TRANSPORT COMPLEX IV; ENZYME STABILITY; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; PROTEOLYSIS; RNA, SMALL INTERFERING;

EID: 84875467758     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.422220     Document Type: Article

References (45)

1. Wallace, D. C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407 (Pubitemid 43011120)
2. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J., Staden, R., and Young, I. G. (1981) Sequence and organization of the human mitochondrial genome. Nature 290, 457-465 (Pubitemid 11159074)
3. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272, 1136-1144
4. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1995) Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A. Science 269, 1069-1074
5. 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 (Pubitemid 28289396)
6. Soto, I. C., Fontanesi, F., Liu, J., and Barrientos, A. (2012) Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core. Biochim. Biophys. Acta 1817, 883-897
7. Mick, D. U., Fox, T. D., and Rehling, P. (2011) Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat. Rev. Mol. Cell Biol. 12, 14-20
8. Shoubridge, E. A. (2001) Cytochrome c oxidase deficiency. Am. J. Med. Genet. 106, 46-52
9. Zee, J. M., and Glerum, D. M. (2006) Defects in cytochrome oxidase assembly in humans: lessons from yeast. Biochem. Cell Biol. 84, 859-869 (Pubitemid 46450686)
10. Barrientos, A., Gouget, K., Horn, D., Soto, I. C., and Fontanesi, F. (2009) Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process. Biochim. Biophys. Acta 1793, 97-107
11. Diaz, F. (2010) Cytochrome c oxidase deficiency: patients and animal models. Biochim. Biophys. Acta 1802, 100-110
12. Comi, G. P., Bordoni, A., Salani, S., Franceschina, L., Sciacco, M., Prelle, A., Fortunato, F., Zeviani, M., Napoli, L., Bresolin, N., Moggio, M., Ausenda, C. D., Taanman, J. W., and Scarlato, G. (1998) Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Ann. Neurol. 43, 110-116 (Pubitemid 28124656)
13. Clark, K. M., Taylor, R. W., Johnson, M. A., Chinnery, P. F., Chrzanowska- Lightowlers, Z. M., Andrews, R. M., Nelson, I. P., Wood, N. W., Lamont, P. J., Hanna, M. G., Lightowlers, R. N., and Turnbull, D. M. (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, 1330-1339 (Pubitemid 30468751)
14. Manfredi, G., Schon, E. A., Moraes, C. T., Bonilla, E., Berry, G. T., Sladky, J. T., and DiMauro, S. (1995) A new mutation associated with MELAS is located in a mitochondrial DNA polypeptide-coding gene. Neuromuscul. Disord. 5, 391-398
15. Shteyer, E., Saada, A., Shaag, A., Al-Hijawi, F. A., Kidess, R., Revel-Vilk, S., and Elpeleg, O. (2009) Exocrine pancreatic insufficiency, dyserythropoeitic anemia, and calvarial hyperostosis are caused by a mutation in the COX4I2 gene. Am. J. Hum. Genet. 84, 412-417
16. Massa, V., Fernandez-Vizarra, E., Alshahwan, S., Bakhsh, E., Goffrini, P., Ferrero, I., Mereghetti, P., D'Adamo, P., Gasparini, P., and Zeviani, M. (2008) Severe infantile encephalomyopathy caused by a mutation in COX6B1, a nucleus-encoded subunit of cytochrome c oxidase. Am. J. Hum. Genet. 82, 1281-1289
17. 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., and Franco, B. (2012) Mutations in COX7B cause microphthalmia with linear skin lesions, an unconventional mitochondrial disease. Am. J. Hum. Genet. 91, 942-949
18. Szklarczyk, R., Wanschers, B. F., Cuypers, T. D., Esseling, J. J., Riemersma, M., van den Brand, M. A., Gloerich, J., Lasonder, E., van den Heuvel, L. P., Nijtmans, L. G., and Huynen, M. A. (2012) Iterative orthology prediction uncovers new mitochondrial proteins and identifies C12orf62 as the human ortholog of COX14, a protein involved in the assembly of cytochrome c oxidase. Genome Biol. 13, R12
19. Weraarpachai, W., Sasarman, F., Nishimura, T., Antonicka, H., Auré, K., Rötig, A., Lombès, A., and Shoubridge, E. A. (2012) Mutations in C12orf62, a Factor that Couples COX I Synthesis with Cytochrome c Oxidase Assembly, Cause Fatal Neonatal Lactic Acidosis. Am. J. Hum. Genet. 90, 142-151
20. Peralta, S., Clemente, P., Sánchez-Martínez, A., Calleja, M., Hernández- Sierra, R., Matsushima, Y., Adán, C., Ugalde, C., Fernández-Moreno, M. Á., Kaguni, L. S., and Garesse, R. (2012) Coiled-coil domain-containing protein 56 (CCDC56) is a novel mitochondrial protein essential for cytochrome c oxidase function. J. Biol. Chem. 287, 24174-24185
21. Peña, P., and Garesse, R. (1993) The - subunit of the Drosophila melanogaster ATP synthase: cDNA cloning, amino acid analysis and identification of the protein in adult flies. Biochem. Biophys. Res. Commun. 195, 785-791
22. Calvaruso, M. A., Smeitink, J., and Nijtmans, L. (2008) Electrophoresis techniques to investigate defects in oxidative phosphorylation. Methods 46, 281-287
23. Chomyn, A. (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol. 264, 197-211
24. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
25. Schägger, H., and Pfeiffer, K. (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777-1783 (Pubitemid 30204389)
26. Antonicka, H., Leary, S. C., Guercin, G. H., Agar, J. N., Horvath, R., Kennaway, N. G., Harding, C. O., Jaksch, M., and Shoubridge, E. A. (2003) Mutations in COX10 result in a defect in mitochondrial heme A biosynthesis and account for multiple, early-onset clinical phenotypes associated with isolated COX deficiency. Hum. Mol. Genet. 12, 2693-2702 (Pubitemid 37304691)
27. Tam, E. W., Feigenbaum, A., Addis, J. B., Blaser, S., Mackay, N., Al-Dosary, M., Taylor, R. W., Ackerley, C., Cameron, J. M., and Robinson, B. H. (2008) A novel mitochondrial DNA mutation in COX1 leads to strokes, seizures, and lactic acidosis. Neuropediatrics 39, 328-334
28. Weraarpachai, W., Antonicka, H., Sasarman, F., Seeger, J., Schrank, B., Kolesar, J. E., Lochmüller, H., Chevrette, M., Kaufman, B. A., Horvath, R., and Shoubridge, E. A. (2009) Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat. Genet. 41, 833-837
29. Williams, S. L., Valnot, I., Rustin, P., and Taanman, J. W. (2004) Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1, or SURF1. J. Biol. Chem. 279, 7462-7469 (Pubitemid 38294623)
30. Stiburek, L., Vesela, K., Hansikova, H., Hulkova, H., and Zeman, J. (2009) Loss of function of Sco1 and its interaction with cytochrome c oxidase. Am. J. Physiol. Cell Physiol. 296, C1218-1226
31. Sasarman, F., Brunel-Guitton, C., Antonicka, H., Wai, T., and Shoubridge, E. A. (2010) LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell 21, 1315-1323
32. Bratic, A., Wredenberg, A., Grönke, S., Stewart, J. B., Mourier, A., Ruzzenente, B., Kukat, C., Wibom, R., Habermann, B., Partridge, L., and Larsson, N. G. (2011) The bicoid stability factor controls polyadenylation and expression of specific mitochondrial mRNAs in Drosophila melanogaster. PLoS Genet. 7, e1002324
33. Ruzzenente, B., Metodiev, M. D., Wredenberg, A., Bratic, A., Park, C. B., Cámara, Y., Milenkovic, D., Zickermann, V., Wibom, R., Hultenby, K., Erdjument-Bromage, H., Tempst, P., Brandt, U., Stewart, J. B., Gustafsson, C. M., and Larsson, N. G. (2012) LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J. 31, 443-456
34. Moreno-Lastres, D., Fontanesi, F., García-Consuegra, I., Martín, M. A., Arenas, J., Barrientos, A., and Ugalde, C. (2012) Mitochondrial complex I plays an essential role in human respirasome assembly. Cell Metab. 15, 324-335
35. Nijtmans, L. G., Artal Sanz, M., Bucko, M., Farhoud, M. H., Feenstra, M., Hakkaart, G. A., Zeviani, M., and Grivell, L. A. (2001) Shy1p occurs in a high molecular weight complex and is required for efficient assembly of cytochrome c oxidase in yeast. FEBS Lett. 498, 46-51 (Pubitemid 32522889)
36. Stiburek, L., Vesela, K., Hansikova, H., Pecina, P., Tesarova, M., Cerna, L., Houstek, J., and Zeman, J. (2005) Tissue-specific cytochrome c oxidase assembly defects due to mutations in SCO2 and SURF1. Biochem. J. 392, 625-632 (Pubitemid 43022743)
37. Mick, D. U., Vukotic, M., Piechura, H., Meyer, H. E., Warscheid, B., Deckers, M., and Rehling, P. (2010) Coa3 and Cox14 are essential for negative feedback regulation ofCOX1translation in mitochondria. J. Cell Biol. 191, 141-154
38. Fontanesi, F., Clemente, P., and Barrientos, A. (2011) Cox25 teams up with Mss51, Ssc1, and Cox14 to regulate mitochondrial cytochrome c oxidase subunit 1 expression and assembly in Saccharomyces cerevisiae. J. Biol. Chem. 286, 555-566
39. Perez-Martinez, X., Broadley, S. A., and Fox, T. D. (2003) Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J. 22, 5951-5961 (Pubitemid 37408830)
40. Barrientos, A., Zambrano, A., and Tzagoloff, A. (2004) Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. EMBO J. 23, 3472-3482 (Pubitemid 39265537)
41. Fontanesi, F., Soto, I. C., Horn, D., and Barrientos, A. (2010) Mss51 and Ssc1 facilitate translational regulation of cytochrome c oxidase biogenesis. Mol. Cell Biol. 30, 245-259
42. Perez-Martinez, X., Butler, C. A., Shingu-Vazquez, M., and Fox, T. D. (2009) Dual functions of Mss51 couple synthesis of Cox1 to assembly of cytochrome c oxidase in Saccharomyces cerevisiae mitochondria. Mol. Biol. Cell 20, 4371-4380
43. Soto, I. C., Fontanesi, F., Myers, R. S., Hamel, P., and Barrientos, A. (2012) A heme-sensing mechanism in the translational regulation of mitochondrial cytochrome c oxidase biogenesis. Cell Metab. 16, 801-813
44. Suzuki, H., Ueda, T., Taguchi, H., and Takeuchi, N. (2007) Chaperone properties of mammalian mitochondrial translation elongation factor Tu. J. Biol. Chem. 282, 4076-4084 (Pubitemid 47084433)
45. Mick, D. U., Dennerlein, S., Wiese, H., Reinhold, R., Pacheu-Grau, D., Lorenzi, I., Sasarman, F., Weraarpachai, W., Shoubridge, E. A., Warscheid, B., and Rehling, P. (2012) MITRAC Links Mitochondrial Protein Translocation to Respiratory-Chain Assembly and Translational Regulation. Cell 151, 1528-1541