The Cbp3-Cbp6 complex coordinates cytochrome b synthesis with bc1 complex assembly in yeast mitochondria

Journal of Cell Biology

Volumn 199, Issue 1, 2012, Pages 137-150

  Gruschke, Steffi ^a   Römpler, Katharina ^a   Hildenbeutel, Markus ^a   Kehrein, Kirsten ^a   Kühl, Inge ^b   Bonnefoy, Nathalie ^b   Ott, Martin ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B; MESSENGER RNA; MITOCHONDRIAL DNA;

5' UNTRANSLATED REGION; ARTICLE; COMPLEX FORMATION; ENZYME KINETICS; ENZYME SUBUNIT; ENZYME SYNTHESIS; GENOME; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; YEAST;

CYTOCHROME B GROUP; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84869106350     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201206040     Document Type: Article

References (41)

1. Atkinson, A., P. Smith, J.L. Fox, T.Z. Cui, O. Khalimonchuk, and D.R. Winge. 2011. The LYR protein Mzm1 functions in the insertion of the Rieske Fe/S protein in yeast mitochondria. Mol. Cell. Biol. 31:3988-3996. http://dx.doi.org/10.1128/MCB.05673-11
2. Barrientos, A., D. Korr, and A. Tzagoloff. 2002. Shy1p is necessary for full expression of mitochondrial COX1 in the yeast model of Leigh's syndrome. EMBO J. 21:43-52. http://dx.doi.org/10.1093/emboj/21.1.43
3. Barrientos, A., A. Zambrano, and A. Tzagoloff. 2004. Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. EMBO J. 23:3472-3482. http://dx.doi.org/10.1038/sj.emboj.7600358
4. Bonnefoy, N., and T.D. Fox. 2000. In vivo analysis of mutated initiation codons in the mitochondrial COX2 gene of Saccharomyces cerevisiae fused to the reporter gene ARG8m reveals lack of downstream reinitiation. Mol. Gen. Genet. 262:1036-1046. http://dx.doi.org/10.1007/PL00008646
5. Bonnefoy, N., and T.D. Fox. 2007. Directed alteration of Saccharomyces cerevisiae mitochondrial DNA by biolistic transformation and homologous recombination. Methods Mol. Biol. 372:153-166. http://dx.doi.org/10.1007/978-1-59745-365-3_11
6. Chacinska, A., C.M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell. 138:628-644. http://dx.doi.org/10.1016/j.cell.2009.08.005
7. Crivellone, M.D. 1994. Characterization of CBP4, a new gene essential for the expression of ubiquinol-cytochrome c reductase in Saccharomyces cerevisiae. J. Biol. Chem. 269:21284-21292.
8. Cruciat, C.M., K. Hell, H. Fölsch, W. Neupert, and R.A. Stuart. 1999. Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc(1) complex. EMBO J. 18:5226-5233. http://dx.doi.org/10.1093/emboj/18.19.5226
9. Cruciat, C.M., S. Brunner, F. Baumann, W. Neupert, and R.A. Stuart. 2000. The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 275:18093-18098. http://dx.doi.org/10.1074/jbc.M001901200
10. Decoster, E., M. Simon, D. Hatat, and G. Faye. 1990. The MSS51 gene product is required for the translation of the COX1 mRNA in yeast mitochondria. Mol. Gen. Genet. 224:111-118. http://dx.doi.org/10.1007/BF00259457
11. DeRisi, J.L., V.R. Iyer, and P.O. Brown. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science. 278:680-686. http://dx.doi.org/10.1126/science.278.5338.680
12. Ding, M.G., C.A. Butler, S.A. Saracco, T.D. Fox, F. Godard, J.P. di Rago, and B.L. Trumpower. 2008. Introduction of cytochrome b mutations in Saccharomyces cerevisiae by a method that allows selection for both functional and non-functional cytochrome b proteins. Biochim. Biophys. Acta. 1777:1147-1156. http://dx.doi.org/10.1016/j.bbabio.2008.04.029
13. Fontanesi, F., I.C. Soto, D. Horn, and A. Barrientos. 2006. Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am. J. Physiol. Cell Physiol. 291:C1129-C1147. http://dx.doi.org/10.1152/ajpcell.00233.2006
14. Fontanesi, F., I.C. Soto, and A. Barrientos. 2008. Cytochrome c oxidase biogenesis: new levels of regulation. IUBMB Life. 60:557-568. http://dx.doi.org/10.1002/iub.86
15. Fox, T.D. 1979. Five TGA "stop" codons occur within the translated sequence of the yeast mitochondrial gene for cytochrome c oxidase subunit II. Proc. Natl. Acad. Sci. USA. 76:6534-6538. http://dx.doi.org/10.1073/pnas.76.12.6534
16. Fox, T.D., M.C. Costanzo, C.A. Strick, D.L. Marykwas, E.C. Seaver, and J.K. Rosenthal. 1988. Translational regulation of mitochondrial gene expression by nuclear genes of Saccharomyces cerevisiae. Philos. Trans. R. Soc. Lond. B Biol. Sci. 319:97-105. http://dx.doi.org/10.1098/rstb.1988.0034
17. Gruschke, S., K. Kehrein, K. Römpler, K. Gröne, L. Israel, A. Imhof, J.M. Herrmann, and M. Ott. 2011. Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J. Cell Biol. 193:1101-1114. http://dx.doi.org/10.1083/jcb.201103132
18. Kühl, I., T.D. Fox, and N. Bonnefoy. 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. http://dx.doi.org/10.1016/j.mito.2012.02.002
19. Manthey, G.M., and J.E. McEwen. 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.
20. Mathieu, L., S. Marsy, Y. Saint-Georges, C. Jacq, and G. Dujardin. 2011. A transcriptome screen in yeast identifies a novel assembly factor for the mitochondrial complex III. Mitochondrion. 11:391-396. http://dx.doi.org/10.1016/j.mito.2010.12.002
21. Mick, D.U., T.D. Fox, and P. Rehling. 2011. Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat. Rev. Mol. Cell Biol. 12:14-20. http://dx.doi.org/10.1038/nrm3029
22. Neupert, W., and J.M. Herrmann. 2007. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76:723-749. http://dx.doi.org/10.1146/annurev.biochem.76.052705.163409
23. Nobrega, F.G., M.P. Nobrega, and A. Tzagoloff. 1992. BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. EMBO J. 11:3821-3829.
24. Ohlmeier, S., A.J. Kastaniotis, J.K. Hiltunen, and U. Bergmann. 2004. The yeast mitochondrial proteome, a study of fermentative and respiratory growth. J. Biol. Chem. 279:3956-3979. http://dx.doi.org/10.1074/jbc.M310160200
25. Perez-Martinez, X., S.A. Broadley, and T.D. Fox. 2003. Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J. 22:5951-5961. http://dx.doi.org/10.1093/emboj/cdg566
26. Pierrel, F., M.L. Bestwick, P.A. Cobine, O. Khalimonchuk, J.A. Cricco, and D.R. Winge. 2007. Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBO J. 26:4335-4346. http://dx.doi.org/10.1038/sj.emboj.7601861
27. Prestele, M., F. Vogel, A.S. Reichert, J.M. Herrmann, and M. Ott. 2009. Mrpl36 is important for generation of assembly competent proteins during mitochondrial translation. Mol. Biol. Cell. 20:2615-2625. http://dx.doi.org/10.1091/mbc.E08-12-1162
28. Rak, M., and A. Tzagoloff. 2009. F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase. Proc. Natl. Acad. Sci. USA. 106:18509-18514. http://dx.doi.org/10.1073/pnas.0910351106
29. Rak, M., S. Gokova, and A. Tzagoloff. 2011. Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30:920-930. http://dx.doi.org/10.1038/emboj.2010.364
30. Rödel, 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. http://dx.doi.org/10.1007/BF00389424
31. Siep, M., K. van Oosterum, H. Neufeglise, H. van der Spek, and L.A. Grivell. 2000. Mss51p, a putative translational activator of cytochrome c oxidase subunit-1 (COX1) mRNA, is required for synthesis of Cox1p in Saccharomyces cerevisiae. Curr. Genet. 37:213-220. http://dx.doi.org/10.1007/s002940050522
32. Smith, P.M., J.L. Fox, and D.R. Winge. 2012. Biogenesis of the cytochrome bc(1) complex and role of assembly factors. Biochim. Biophys. Acta. 1817:276-286. http://dx.doi.org/10.1016/j.bbabio.2011.11.009
33. Steele, D.F., C.A. Butler, and T.D. Fox. 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. http://dx.doi.org/10.1073/pnas.93.11.5253
34. Thorsness, P.E., and T.D. Fox. 1993. Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics. 134:21-28.
35. Wagener, N., M. Ackermann, S. Funes, and W. Neupert. 2011. A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol. Cell. 44:191-202. http://dx.doi.org/10.1016/j.molcel.2011.07.036
36. Wittig, I., H.P. Braun, and H. Schägger. 2006. Blue native PAGE. Nat. Protoc. 1:418-428. http://dx.doi.org/10.1038/nprot.2006.62
37. Wu, M., and A. Tzagoloff. 1989. Identification and characterization of a new gene (CBP3) required for the expression of yeast coenzyme QH2-cytochrome c reductase. J. Biol. Chem. 264:11122-11130.
38. Zara, V., I. Palmisano, L. Conte, and B.L. Trumpower. 2004. Further insights into the assembly of the yeast cytochrome bc1 complex based on analysis of single and double deletion mutants lacking supernumerary subunits and cytochrome b. Eur. J. Biochem. 271:1209-1218. http://dx.doi.org/10.1111/j.1432-1033.2004.04024.x
39. Zara, V., L. Conte, and B.L. Trumpower. 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. http://dx.doi.org/10.1111/j.1742-4658.2007.05982.x
40. Zara, V., L. Conte, and B.L. Trumpower. 2009a. Biogenesis of the yeast cytochrome bc1 complex. Biochim. Biophys. Acta. 1793:89-96. http://dx.doi.org/10.1016/j.bbamcr.2008.04.011
41. Zara, V., L. Conte, and B.L. Trumpower. 2009b. Evidence that the assembly of the yeast cytochrome bc1 complex involves the formation of a large core structure in the inner mitochondrial membrane. FEBS J. 276:1900-1914. http://dx.doi.org/10.1111/j.1742-4658.2009.06916.x