Translocation of mitochondrially synthesized Cox2 domains from the matrix to the intermembrane space

Molecular and Cellular Biology

Volumn 27, Issue 13, 2007, Pages 4664-4673

  Fiumera, Heather L ^a   Broadley, Sarah A ^a,b   Fox, Thomas D ^a  

^a Department of Obstetrics Gynecology   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CYTOCHROME C OXIDASE; EPITOPE; FUNGAL PROTEIN; MITOCHONDRIAL DNA; MUTANT PROTEIN; PROTEIN OXA1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

ELECTRON TRANSPORT COMPLEX IV; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; THERMODYNAMICS;

SACCHAROMYCES CEREVISIAE;

EID: 34347337609     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01955-06     Document Type: Article

References (60)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
2. Bonnefoy, N., N. Bsat, and T. D. Fox. 2001. Mitochondrial translation of Saccharomyces cerevisiae COX2 mRNA is controlled by the nucleotide sequence specifying the pre-Cox2p leader peptide. Mol. Cell. Biol. 21:2359-2372.
3. Bonnefoy, N., F. Chalvet, P. Hamel, P. P. Slonimski, and G. Dujardin. 1994. OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J. Mol. Biol. 239:201-212.
4. Bonnefoy, N., and T. D. Fox. 2001. Genetic transformation of Saccharomyces cerevisiae mitochondria. Methods Cell Biol. 65:381-396.
5. 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.
6. Broadley, S. A., C. M. Demlow, and T. D. Fox. 2001. Peripheral mitochondrial inner membrane protein, Mss2p, required for export of the mitochondrially coded Cox2p C tail in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:7663-7672.
7. Carr, H. S., and D. R. Winge. 2003. Assembly of cytochrome c oxidase within the mitochondrion. Acc. Chem. Res. 36:309-316.
8. Celebi, N., L. Yi, S. J. Facey, A. Kuhn, and R. E. Dalbey. 2006. Membrane biogenesis of subunit II of cytochrome bo oxidase: contrasting requirements for insertion of N-terminal and C-terminal domains. J. Mol. Biol. 357:1428-1436.
9. Chan, N. C., V. A. Likic, R. F. Waller, T. D. Mulhern, and T. Lithgow. 2006. The C-terminal TPR domain of Tom70 defines a family of mitochondrial protein import receptors found only in animals and fungi. J. Mol. Biol. 358:1010-1022.
10. Cobine, P. A., L. D. Ojeda, K. M. Rigby, and D. R. Winge. 2004. Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J. Biol. Chem. 279:14447-14455.
11. Diekert, K., A. I. de Kroon, G. Kispal, and R. Lill. 2001. Isolation and subfractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol. 65:37-51.
12. du Plessis, D. J. F., N. Nouwen, and A. J. M. Driessen. 2006. Subunit a of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion. J. Biol. Chem. 281:12248-12252.
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.
14. Gaisne, M., and N. Bonnefoy. 2006. The COX18 gene, involved in mitochondrial biogenesis, is functionally conserved and tightly regulated in humans and fission yeast. FEMS Yeast Res. 6:869-882.
15. Gavel, Y., and G. von Heijne. 1992. The distribution of charged amino acids in mitochondrial inner-membrane proteins suggests different modes of membrane integration for nuclearly and mitochondrially encoded proteins. Eur. J. Biochem. 205:1207-1215.
16. Click. B. S., and L. A. Pon. 1995. Isolation of highly purified mitochondria from Saccharomyces cerevisiae. Methods Enzymol. 260:213-223.
17. Click. B. S., and G. Von Heijne. 1996. Saccharomyces cerevisiae mitochondria lack a bacterial-type sec machinery. Protein Sci. 5:2651-2652.
18. Green-Willms, N. S., C. A. Butler, H. M. Dunstan, and T. D. Fox. 2001. Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2. J. Biol. Chem. 276:6392-6397.
19. Guthrie, C., and G. R. Fink. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:1-863.
20. Harley, C. A., J. A. Holt, R. Turner, and D. J. Tipper. 1998. Transmembrane protein insertion orientation in yeast depends on the charge difference across transmembrane segments, their total hydrophobicity, and its distribution. J. Biol. Chem. 273:24963-24971.
21. He, S., and T. D. Fox. 1997. Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol. Biol. Cell 8:1449-1460.
22. He, S., and T. D. Fox. 1999. Mutations affecting a yeast mitochondrial inner membrane protein, Pnt1p, block export of a mitochondrially synthesized fusion protein from the matrix. Mol. Cell. Biol. 19:6598-6607.
23. Hell, K., J. Herrmann, E. Pratje, W. Neupert, and R. A. Stuart. 1997. Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 418:367-370.
24. Hell, K., W. Neupert, and R. A. Stuart. 2001. Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J. 20:1281-1288.
25. Hell, K., A. Tzagoloff, W. Neupert, and R. A. Stuart. 2000. Identification of Cox20p, a novel protein involved in the maturation and assembly of cytochrome oxidase subunit 2. J. Biol. Chem. 275:4571-4578.
26. Herrmann, J. M., and S. Funes. 2005. Biogenesis of cytochrome oxidase-sophisticated assembly lines in the mitochondrial inner membrane. Gene 354:43-52.
27. Jan, P. S., K. Esser, E. Pratje, and G. Michaelis. 2000. Som1, a third component of the yeast mitochondrial inner membrane peptidase complex that contains Imp1 and Imp2. Mol. Gen. Genet. 263:483-491.
28. Jia, L., M. Dienhart, M. Schramp, M. McCauley, K. Hell, and R. A. Stuart. 2003. Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1. EMBO J. 22:6438-6447.
29. Kermorgant, M., N. Bonnefoy, and G. Dujardin. 1997. Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane. Curr. Genet. 31:302-307.
30. Leonhard, K., B. Guiard, G. Pellecchia, A. Tzagoloff, W. Neupert, and T. Langer. 2000. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol. Cell 5:629-638.
31. Leonhard, K., J. M. Herrmann, R. A. Stuart, G. Mannhaupt, W. Neupert, and T. Langer. 1996. AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 15:4218-4229.
32. Luirink, J., G. von Heijne, E. N. Houben, and J. W. Gier. 2005. Biogenesis of inner membrane proteins in Escherichia coli. Annu. Rev. Microbiol. 59: 329-355.
33. Mulero, J. J., and T. D. Fox. 1993. PET111 acts in the 5′-leader of the Saccharomyces cerevisiae mitochondrial COX2 mRNA to promote its translation. Genetics 133:509-516.
34. Naithani, S., S. A. Saracco, C. A. Butler, and T. D. Fox. 2003. Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol. Biol. Cell 14:324-333.
35. Nakai, T., T. Yasuhara, Y. Fujiki, and A. Ohashi. 1995. Multiple genes, including a member of the AAA family, are essential for degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol. Cell. Biol. 15:4441-4452.
36. Neff, N. F., J. H. Thomas, P. Grisafi, and D. Botstein. 1983. Isolation of the beta-tubulin gene from yeast and demonstration of its essential function in vivo. Cell 33:211-219.
37. Nittis, T., G. N. George, and D. R. Winge. 2001. Yeast Sco1, a protein essential for cytochrome c oxidase function is a Cu(I)-binding protein. J. Biol. Chem. 276:42520-42526.
38. Nunnari, J., T. D. Fox, and P. Walter. 1993. A mitochondrial protease with two catalytic subunits of nonoverlapping specificities. Science 262: 1997-2004.
39. Pearce, D. A., and F. Sherman. 1995. Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of YME1. J. Biol. Chem. 270:20879-20882.
40. 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.
41. Preuss, M., M. Ott, S. Funes, J. Luirink, and J. M. Herrmann. 2005. Evolution of mitochondrial Oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. J. Biol. Chem. 280:13004-13011.
42. Rentzsch, A., G. Krummeck-Weiss, A. Hofer, A. Bartuschka, K. Ostermann, and G. Rodel. 1999. Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr. Genet. 35:103-108.
43. Rojo, E. E., B. Guiard, W. Neupert, and R. A. Stuart. 1999. N-terminal tail export from the mitochondrial matrix. Adherence to the prokaryotic "positive-inside" rule of membrane protein topology. J. Biol. Chem. 274:19617-19622.
44. Sanchirico, M. E., T. D. Fox, and T. L. Mason. 1998. Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs. EMBO J. 17:5796-5804.
45. Saracco, S. A. 2003. Analysis of the export of Saccharomyces cerevisiae Cox2p from the mitochondrial matrix. Ph.D. thesis. Cornell University, Ithaca, NY.
46. Saracco, S. A., and T. D. Fox. 2002. Cox18p is required for export of the mitochondrially encoded Saccharomyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane. Mol. Biol. Cell 13:1122-1131.
47. Schneider, B. L., W. Seufert, B. Steiner, Q. H. Yang, and A. B. Futcher. 1995. Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae. Yeast 11:1265-1274.
48. Souza, R. L., N. S. Green-Willms, T. D. Fox, A. Tzagoloff, and F. G. Nobrega. 2000. Cloning and characterization of COX18, a Saccharomyces cerevisiae PET gene required for the assembly of cytochrome oxidase. J. Biol. Chem. 275:14898-15902.
49. Speno, H., M. R. Taheri, D. Sieburth, and C. T. Martin. 1995. Identification of essential amino acids within the proposed CuA binding site in subunit II of Cytochrome c oxidase. J. Biol. Chem. 270:25363- 25369.
50. Szyrach, G., M. Ott, N. Bonnefoy, W. Neupert, and J. M. Herrmann. 2003. Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria. EMBO J. 22:6448-6457.
51. Teter, S. A., and D. J. Klionsky. 1999. How to get a folded protein across a membrane. Trends Cell Biol. 9:428-431.
52. Thorsness, P. E., K. H. White, and T. D. Fox. 1993. Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:5418-5426.
53. van Bloois, E., G. J. Haan, J. W. de Gier, B. Oudega, and J. Luirink. 2006. Distinct requirements for translocation of the N-tail and C-tail of the Escherichia coli inner membrane protein CyoA. J. Biol. Chem. 281:10002-10009.
54. Van Der Laan, M., M. L. Urbanus, C. M. Ten Hagen-Jongman, N. Nouwen, B. Oudega, N. Harms, A. J. Driessen, and J. Luirink. 2003. A conserved function of YidC in the biogenesis of respiratory chain complexes. Proc. Natl. Acad. Sci. USA 100:5801-5806.
55. Wach, A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12:259-265.
56. Wach, A., A. Brachat, R. Pohlmann, and P. Philippsen. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793-1808.
57. Weber, E. R., T. Hanekamp, and P. E. Thorsness. 1996. Biochemical and functional analysis of the YME1 gene product, an ATP and zinc-dependent mitochondrial protease from S. cerevisiae. Mol. Biol. Cell 7:307-317.
58. Westermann, B., J. M. Herrmann, and W. Neupert. 2001. Analysis of mitochondrial translation products in vivo and in organello in yeast. Methods Cell Biol. 65:429-438.
59. Yi, L., and R. E. Dalbey. 2005. Oxa1/Alb3/YidC system for insertion of membrane proteins in mitochondria, chloroplasts and bacteria (review). Mol. Membr. Biol. 22:101-111.
60. Young, J. C., N. J. Hoogenraad, and F. U. Hartl. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:41-50.