Mechanisms of mitochondrial translational regulation

IUBMB Life

Volumn 65, Issue 5, 2013, Pages 397-408

  Fontanesi, Flavia ^a  

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

Author keywords

ATP synthase; cytochrome c oxidase; mitochondria; Saccharomyces cerevisiae; translational regulation; ubiquinol cytochrome c oxidoreductase

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME C; CYTOCHROME C OXIDASE; DEOXYRIBONUCLEASE; MESSENGER RNA; MESSENGER RNA PRECURSOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE;

5' UNTRANSLATED REGION; ANIMAL; AUTOREGULATION; BIOGENESIS; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CHLOROPLAST GENE; CONFORMATIONAL TRANSITION; DIMERIZATION; ELECTRON TRANSPORT; GENE EXPRESSION; HUMAN; LIVER MITOCHONDRION; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONCENTRATION; PHOTOSYSTEM I; PHOTOSYSTEM II; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTON TRANSPORT; REPORTER GENE; RESPIRATORY CHAIN; REVIEW; RIBOSOME SUBUNIT; RNA BINDING; RNA PROCESSING; RNA TRANSLATION; SPONTANEOUS MUTATION; TRANSLATION REGULATION;

ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 84876941987     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1156     Document Type: Review

References (62)

1. Babitzke, P., Baker, C. S., and, Romeo, T., (2009) Regulation of translation initiation by RNA binding proteins. Annu. Rev. Microbiol. 63, 27-44.
2. Kehrein, K., Bonnefoy, N., and, Ott, M., (2012) Mitochondrial protein synthesis: efficiency and accuracy. Antioxid. Redox. Signal. Epub ahead of print Jan 22.
3. Choquet, Y., Stern, D. B., Wostrikoff, K., Kuras, R., Girard-Bascou, J., et al. (1998) Translation of cytochrome f is autoregulated though the 5′ untranslated region of perA mRNA in Chlamydomonas chloroplasts. Proc. Natl. Acad. Sci. USA 95, 4380-4385.
4. Choquet, Y., and, Wollman, F. A., (2009) The CES process. In The Chlamydomonas Source Book, 2nd edn. (, Harris, E. E., Stern, D. B., Whitman, G., eds.). pp. 1027-1064, Academic Press, Elsevier, New York, London, Amsterdam.
5. Boulouis, A., Raynaud, C., Bujaldon, S., Aznar, A., Wollman, F. A., et al. (2011) The nucleus-encoded trans-acting factor MCA1 plays a critical role in the regulation of cytochrome f synthesis in Chlamydomonas chloroplasts. Plant Cell 23, 333-349.
6. Steele, D. F., Butler, C. A., and, Fox, T. D., (1996) Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc. Natl. Acad. Sci. USA 93, 5253-5257. (Pubitemid 26159435)
7. 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.
8. 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)
9. 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)
10. 1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase. Proc. Natl. Acad. Sci. USA 106, 18509-18514.
11. Gruschke, S., Rompler, K., Hildenbeutel, M., Kehrein, K., Kuhl, I., et al. (2012) The Cbp3-Cbp6 complex coordinates cytochrome b synthesis with bc(1) complex assembly in yeast mitochondria. J. Cell Biol. 199, 137-150.
12. Wielburski, A., and, Nelson, B. D., (1983) Evidence for the sequential assembly of cytochrome oxidase subunits in rat liver mitochondria. Biochem. J. 212, 829-834.
13. 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)
14. 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)
15. Horan, S., Bourges, I., Taanman, J. W., and, Meunier, B., (2005) Analysis of COX2 mutants reveals cytochrome oxidase subassemblies in yeast. Biochem. J. 390, 703-708. (Pubitemid 41395353)
16. Church, C., Goehring, B., Forsha, D., Wazny, P., and, Poyton, R. O., (2005) A role for Pet100p in the assembly of yeast cytochrome c oxidase: interaction with a subassembly that accumulates in a pet100 mutant. J. Biol. Chem. 280, 1854-1863.
17. Moreno-Lastres, D., Fontanesi, F., Garcia-Consuegra, I., Martin, M. A., Arenas, J., et al. (2012) Mitochondrial complex I plays an essential role in human respirasome assembly. Cell Metab. 15, 324-335.
18. Mick, D. U., Wagner, K., van der Laan, M., Frazier, A. E., Perschil, I., et al. (2007) Shy1 couples Cox1 translational regulation to cytochrome c oxidase assembly. EMBO J. 26, 4347-4358. (Pubitemid 47587664)
19. Langer, T., Kaser, M., Klanner, C., and, Leonhard, K., (2001) AAA proteases of mitochondria: quality control of membrane proteins and regulatory functions during mitochondrial biogenesis. Biochem. Soc. Trans. 29, 431-436. (Pubitemid 32783632)
20. Khalimonchuk, O., Jeong, M. Y., Watts, T., Ferris, E., and, Winge, D. R., (2012) Selective Oma1 protease-mediated proteolysis of Cox1 subunit of cytochrome oxidase in assembly mutants. J. Biol. Chem. 287, 7289-7300.
21. Manthey, G. M., and, McEwen, J. E., (1995) The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 14, 4031-4043.
22. Decoster, E., Simon, M., Hatat, D., and, Faye, G., (1990) The MSS51 gene product is required for the translation of the COX1 mRNA in yeast mitochondria. Mol. Gen. Genet. 224, 111-118. (Pubitemid 20364642)
23. Zambrano, A., Fontanesi, F., Solans, A., de Oliveira, R. L., Fox, T. D., et al. (2007) Aberrant translation of cytochrome c oxidase subunit 1 mRNA species in the absence of Mss51p in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 18, 523-535. (Pubitemid 46213221)
24. Barrientos, A., Korr, D., and, Tzagoloff, A., (2002) Shy1p is necessary for full expression of mitochondrial COX1 in the yeast model of Leigh's syndrome. EMBO J. 21, 43-52. (Pubitemid 34087073)
25. Mashkevich, G., Repetto, B., Glerum, D. M., Jin, C., and, Tzagoloff, A., (1997) SHY1, the yeast homolog of the mammalian SURF-1 gene, encodes a mitochondrial protein required for respiration. J. Biol. Chem. 272, 14356-14364. (Pubitemid 27232851)
26. 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.
27. Pierrel, F., Bestwick, M. L., Cobine, P. A., Khalimonchuk, O., Cricco, J. A., et al. (2007) Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBO J. 26, 4335-4346. (Pubitemid 47587663)
28. 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.
29. Mick, D. U., Vukotic, M., Piechura, H., Meyer, H. E., Warscheid, B., et al. (2010) Coa3 and Cox14 are essential for negative feedback regulation of COX1 translation in mitochondria. J. Cell Biol. 191, 141-154.
30. Fontanesi, F., Jin, C., Tzagoloff, A., and, Barrientos, A., (2008) Transcriptional activators HAP/NF-Y rescue a cytochrome c oxidase defect in yeast and human cells. Hum. Mol. Genet. 17, 775-788. (Pubitemid 351359694)
31. Khalimonchuk, O., Bestwick, M., Meunier, B., Watts, T. C., and, Winge, D. R., (2010) Formation of the redox cofactor centers during Cox1 maturation in yeast cytochrome oxidase. Mol. Cell. Biol. 30, 1004-1017.
32. 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.
33. Veniamin, S., Sawatzky, L. G., Banting, G. S., and, Glerum, D. M., (2011) Characterization of the peroxide sensitivity of COX-deficient yeast strains reveals unexpected relationships between COX assembly proteins. Free Radic. Biol. Med. 51, 1589-1600.
34. Shingu-Vazquez, M., Camacho-Villasana, Y., Sandoval-Romero, L., Butler, C. A., Fox, T. D., et al. (2010) The carboxyl-terminal end of Cox1 is required for feedback assembly regulation of Cox1 synthesis in Saccharomyces cerevisiae mitochondria. J. Biol. Chem. 285, 34382-34389.
35. Westermann, B., Gaume, B., Herrmann, J. M., Neupert, W., and, Schwarz, E., (1996) Role of the mitochondrial DnaJ homolog Mdj1p as a chaperone for mitochondrially synthesized and imported proteins. Mol. Cell. Biol. 16, 7063-7071. (Pubitemid 26389765)
36. Mense, S. M., and, Zhang, L., (2006) Heme: a versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res. 16, 681-692. (Pubitemid 44258921)
37. Barros, M. H., and, Tzagoloff, A., (2002) Regulation of the heme A biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett. 516, 119-123. (Pubitemid 34311946)
38. O-ATP synthase. Biochim. Biophys. Acta 1793, 1776-1786.
39. Barrientos, A., Pierre, D., Lee, J., and, Tzagoloff, A., (2003) Cytochrome oxidase assembly does not require catalytically active cytochrome C. J. Biol. Chem. 278, 8881-8887. (Pubitemid 36800363)
40. Smith, P. M., Fox, J. L., and, Winge, D. R., (2012) Biogenesis of the cytochrome bc(1) complex and role of assembly factors. Biochim. Biophys. Acta 1817, 276-286.
41. Rho, S. B., and, Martinis, S. A., (2000) The bI4 group I intron binds directly to both its protein splicing partners, a tRNA synthetase and maturase, to facilitate RNA splicing activity. RNA 6, 1882-1894. (Pubitemid 32001957)
42. Rodel, G., (1986) Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5′-untranslated COB leader. Curr. Genet. 11, 41-45. (Pubitemid 17014075)
43. Gruschke, S., Kehrein, K., Rompler, K., Grone, K., Israel, L., et al. (2011) Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J. Cell Biol. 193, 1101-1114.
44. Mittelmeier, T. M., and, Dieckmann, C. L., (1995) In vivo analysis of sequences required for translation of cytochrome b transcripts in yeast mitochondria. Mol. Cell. Biol. 15, 780-789.
45. Krause-Buchholz, U., Schobel, K., Lauffer, S., and, Rodel, G., (2005) Saccharomyces cerevisiae translational activator Cbs1p is associated with translationally active mitochondrial ribosomes. Biol. Chem. 386, 407-415. (Pubitemid 41447582)
46. Krause-Buchholz, U., Barth, K., Dombrowski, C., and, Rodel, G., (2004) Saccharomyces cerevisiae translational activator Cbs2p is associated with mitochondrial ribosomes. Curr. Genet. 46, 20-28. (Pubitemid 39077333)
47. Zara, V., Conte, L., and, Trumpower, B. L., (2007) Identification and characterization of cytochrome bc(1) subcomplexes in mitochondria from yeast with single and double deletions of genes encoding cytochrome bc(1) subunits. FEBS J. 274, 4526-4539. (Pubitemid 47301714)
48. Zara, V., Conte, L., and, Trumpower, B. L., (2009) Evidence that assembly of the yeast cytochrome bc1 complex involves formation of a large core structure in the inner mitochondrial membrane. FEBS J. 276, 1900-1914.
49. Crivellone, M. D., Wu, M. A., and, Tzagoloff, A., (1988) Assembly of the mitochondrial membrane system. Analysis of structural mutants of the yeast coenzyme QH2-cytochrome c reductase complex. J. Biol. Chem. 263, 14323-14333.
50. Strogolova, V., Furness, A., Robb-McGrath, M., Garlich, J., and, Stuart, R. A., (2012) Rcf1 and Rcf2, members of the hypoxia-induced gene 1 protein family, are critical components of the mitochondrial cytochrome bc1-cytochrome c oxidase supercomplex. Mol. Cell. Biol. 32, 1363-1373.
51. O in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1793, 108-116.
52. Zeng, X., Hourset, A., and, Tzagoloff, A., (2007) The Saccharomyces cerevisiae ATP22 gene codes for the mitochondrial ATPase subunit 6-specific translation factor. Genetics 175, 55-63. (Pubitemid 46170778)
53. Rak, M., Gokova, S., and, Tzagoloff, A., (2011) Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30, 920-930.
54. Allen, J. F., (2003) Why chloroplasts and mitochondria contain genomes. Comp. Funct. Genomics 4, 31-36. (Pubitemid 36304736)
55. Diaz, F., Fukui, H., Garcia, S., and, Moraes, C. T., (2006) Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol. Cell. Biol. 26, 4872-4881. (Pubitemid 43955805)
56. Li, Y., D'Aurelio, M., Deng, J. H., Park, J. S., Manfredi, G., et al. (2007) An assembled complex IV maintains the stability and activity of complex I in mammalian mitochondria. J. Biol. Chem. 282, 17557-17562. (Pubitemid 47100296)
57. Weraarpachai, W., Antonicka, H., Sasarman, F., Seeger, J., Schrank, B., et al. (2009) Mutation in TACO1, encoding a translational activator of COXI, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat. Genet. 41, 833-837.
58. Szklarczyk, R., Wanschers, B. F., Cuypers, T. D., Esseling, J. J., Riemersma, M., et al. (2012) Iterative orthology prediction uncovers new mitochondrial proteins and identifies C12rf62 as the human ortholog of COX14, a protein involved in the assembly of cytochrome c oxidase. Genome Biol. 13, R12.
59. Weraarpachai, W., Sasarman, F., Nishimura, T., Antonicka, H., Aure, K., et al. (2012) Mutations in C12orf62, a factor that couples COXI synthesis with cytochrome c oxidase assembly, cause fatal neonatal lactic acidosis. Am. J. Hum. Genet. 90, 142-151.
60. Mick, D. U., Dennerlein, S., Wiese, H., Reinhold, R., Pacheu-Grau, D., et al. (2012) MITRAC links mitochondrial protein translocation to respiratory-chain assembly and translational regulation. Cell 151, 1528-1541.
61. Kuhl, I., Fox, T. D., and, Bonnefoy, N., (2012) Schizosaccharomyces pombe homologs of the Saccharomyces cerevisiae mitochondrial proteins Cbp6 and Mss51 function at a post-translational step of respiratory complex biogenesis. Mitochondrion 12, 381-390.
62. 1-depleted HeLa and yeast cells. FEBS Lett. 585, 2582-2586.