A novel two-step mechanism for removal of a mitochondrial signal sequence involves the mAAA complex and the putative rhomboid protease Pcp1

Journal of Molecular Biology

Volumn 323, Issue 5, 2002, Pages 835-843

  Esser, Karlheinz ^a   Tursun, Baris ^b   Ingenhoven, Martin ^a   Michaelis, Georg ^a   Pratje, Elke ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

Author keywords

AAA protease; Cytochrome c peroxidase; Mitochondrial protein sorting; PCP1 gene; Rhomboid family

Indexed keywords

CYTOCHROME C PEROXIDASE; GENE PRODUCT; PROTEIN; PROTEIN MAAA; PROTEIN PCP1; PROTEINASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ENZYME ACTIVITY; ENZYME SUBUNIT; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TARGETING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 0036424840     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01000-8     Document Type: Article

References (57)

1. Herrmann, J. M. & Neupert, W. (2000). What fuels polypeptide translocation? An energetical view on mitochondrial protein sorting. Biochim. Biophys. Acta, 1459, 331-338.
2. Pfanner, N. & Geissler, A. (2001). Versatility of the mitochondrial protein import machinery. Nature Rev. Mol. Cell. Biol. 5, 339-349.
3. Von Heijne, G. (ed.) (1994). Signal Peptidases, Landes Company, Austin
4. Kalousek, F., Neupert, W., Omura, T., Schatz, G. & Schmitz, U. K. (1993). Uniform nomenclature for the mitochondrial peptidades cleaving precursors of mitochondrial protens. Trends Biochem. Sci. 18, 249.
5. Isaya, G., Miklos, D. & Rollins, R. A. (1994). MIP1, a new yeast gene homologous to the rat mitochondrial intermediate peptidase gene, is required for oxidative metabolism in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 5603-5616.
6. Esser, K., Pratje, E. & Michaelis, G. (1996). SOM 1, a small new gene required for mitochondrial inner membrane peptidase function in Saccharomyces cerevisiae. Mol. Gen. Genet. 252, 437-445.
7. Nunnari, J., Fox, T. D. & Walter, P. A. (1993). A mitochondrial protease with two catalytic subunits of non-overlapping specificities. Science, 262, 1997-2004.
8. Schneider, A., Behrens, M., Scherer, P., Pratje, E., Michaelis, G. & Schatz, G. (1991). Inner membrane protease I, an enzyme mediating intramitochondrial protein sorting in yeast. EMBO J. 10, 247-254.
9. Gasser, S. M., Ohashi, A., Daum, G., Böhni, P. C., Gibson, J., Reid, G. A. et al. (1982). Imported mitochondrial proteins cytochrome b2 and cytochrome c1 are processed in two steps. Proc. Natl Acad. Sci. USA, 79, 267-271.
10. Daum, G., Böhni, P. C. & Schatz, G. (1982). Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem. 257, 13028-13033.
11. Maccecchini, M.-L., Rudin, Y. & Schatz, G. (1979). Transport of proteins across the mitochondrial outer membrane. A precursor form of the cytoplasmically made intermembrane enzyme cytochrome c peroxidase. J. Biol. Chem. 254, 7468-7471.
12. Kaput, J., Brandriss, M. C. & Prussak-Wieckowska, T. (1989). In vitro import of cytochrome c peroxidase into the intermembrane space: Release of the processed form by intact mitochondria. J. Cell Biol. 109, 101-112.
13. Pon, L. & Schatz, G. (1991). Biogenesis of yeast mitochondria. In The Molecular and Cellular Biology of the Yeast Saccharomyces (Broach, J. R., Pringle, J. & Jones, E., eds), pp. 333-406, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
14. Jan, P. S., Esser, K., Pratje, E. & Michaelis, G. (2000). Som1, a third component of the yeast mitochondrial inner membrane peptidase complex that contains Imp1 and Imp2. Mol. Gen. Genet. 263, 483-491.
15. Pratje, E. & Guiard, B. (1986). One nuclear gene controls the removal of transient pre-sequences from two yeast proteins: One encoded by the nuclear the other by the mitochondrial genome. EMBO J. 5, 1313-1317.
16. Claros, M. G. & Vincens, P. (1996). Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786.
17. Horton, P. & Nakai, K. (1997). Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5, 147-152.
18. Langer, T. (2000). AAA proteases: Cellular machines for degrading membrane proteins. Trends Biochem. Sci. 25, 247-251.
19. Steglich, G., Neupert, W. & Langer, T. (1999). Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol. Cell. Biol. 19, 3435-3442.
20. Young, L., Leonhard, K., Tatsuta, T., Trowsdale, J. & Langer, T. (2001). Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science, 291, 2135-2138.
21. Saier, M., Jr, Reizer, J. & Reizer, A. (1992). A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Protein Sci. 1, 1326-1332.
22. Bier, E., Jan, L. Y. & Jan, Y. N. (1990). Rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4, 190-203.
23. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S. R. et al. (2002). The Pfam protein families database. Nucl. Acids Res. 30, 276-280.
24. Guélin, E., Rep, M. & Grivell, L. A. (1994). Sequence of the AFG3 gene encoding a new member of the FtsH/Yme1/Tma subfamily of the AAA-protein family. Yeast, 10, 1389-1394.
25. Arlt, H., Steglich, G., Perryman, R., Guiard, B., Neupert, W. & Langer, T. (1998). The formation of respiratory chain complexes in mitochondria is under the proteolytic control of the m-AAA protease. EMBO J. 17, 4837-4847.
26. Urban, S., Lee, J. & Freeman, M. (2001). Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell, 107, 173-182.
27. Reid, G. A., Yonetani, T. & Schatz, G. (1982). Import of proteins into mitochondria. Import and maturation of the mitochondrial intermembrane space enzymes cytochrome b2 and cytochrome c peroxidase in intact yeast cells. J. Biol. Chem. 257, 13068-13074.
28. Branda, S. S. & Isaya, G. (1995). Prediction and identification of new natural substrates of the yeast mitochondrial intermediate peptidase. J. Biol. Chem. 270, 27366-27373.
29. Suzuki, C. K., Rep, M., van Dijl, J. M., Suda, K., Grivell, L. A. & Schatz, G. (1997). ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem. Sci. 4, 118-123.
30. Langer, T., Käser, M., Klanner, C. & Leonhard, K. (2001). AAA proteases of mitochondria: Quality control of membrane proteins and regulatory functions during mitochondrial biogenesis. Biochem. Soc. Trans. 29, 431-436.
31. Lightowlers, R. N. & Lill, R. (2001). High-level mitochondriology at high altitude. Workshop on mitochondrial (dys-)function. EMBO Rep. 12, 1074-1077.
32. Schmidt, M., Lupas, A. N. & Finley, D. (1999). Structure and mechanism of ATP-dependent proteases. Curr. Opin. Chem. Biol. 3, 584-591.
33. Karata, K., Inagawa, T., Wilkinson, A. J., Tatsuta, T. & Ogura, T. (1999). Dissecting the role of a conserved motif (the second region of homology) in the AAA family of ATPases. Site-directed mutagenesis of the ATP-dependent protease FtsH. J. Biol. Chem. 274, 26225-26232.
34. Wagner, I., van Dyck, L., Savel'ev, A. S., Neupert, W. & Langer, T. (1997). Autocatalytic processing of the ATP-dependent PIM1 protease: Crucial function of a pro-region for sorting to mitochondria. EMBO J. 16, 7317-7325.
35. Rep, M., Nooy, J., Guélin, E. & Grivell, L. A. (1996). Three genes for mitochondrial proteins suppress null-mutations in both Afg3 and Rca1 when over-expressed. Curr. Genet. 30, 206-211.
36. Preuss, M., Leonhard, K., Hell, K., Stuart, R. A., Neupert, W. & Herrmann, J. M. (2001). Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae. J. Cell Biol. 153, 1085-1096.
37. Ross-Macdonald, P., Coelho, P. S. R., Roemer, T., Agarwal, S., Kumar, A., Jansen, R. et al. (1999). Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature, 402, 413-418.
38. Kaput, J., Goltz, S. & Blobel, G. (1982). Nucleotide sequence of the yeast nuclear gene for cytochrome c peroxidase precursor. Functional implications of the pre sequence for protein transport into mitochondria. J. Biol. Chem. 257, 15054-15058.
39. Leonhard, K., Guiard, B., Pellecchia, G., Tzagoloff, A., Neupert, W. & Langer, T. (2000). Membrane protein degradation by AAA proteases in mitochondria: Extraction of substrates from either membrane surface. Mol. Cell, 5, 629-638.
40. Kihara, A., Akiyama, Y. & Ito, K. (1999). Dislocation of membrane proteins in FtsH-mediated proteolysis. EMBO J. 18, 2970-2981.
41. Nielsen, H., Engelbrecht, J., Brunak, S. & von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6.
42. Pellegrini, L., Passer, B. J., Canelles, M., Lefterov, I., Ganjei, J. K., Fowlkes, B. J. et al. (2001). PAMP and PARL, two novel putative metalloproteases interacting with the COOH-terminus of Presenilin-1 and 2. J. Alzheimer's Dis. 3, 181-190.
43. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P. & Boeke, J. D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast, 14, 115-132.
44. Bauer, M., Behrens, M., Esser, K., Michaelis, G. & Pratje, E. (1994). PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast. Mol. Gen. Genet. 245, 272-278.
45. Winston, F., Dollard, C. & Ricupero-Hovasse, S. L. (1995). Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast, 11, 53-55.
46. Prohl, C., Pelzer, W., Diekert, K., Kmita, H., Bedekovics, T., Kispal, G. & Lill, R. (2001). The yeast mitochondrial carrier Leu5p and its human homologue Graves' disease protein are required for accumulation of coenzyme A in the matrix. Mol. Cell. Biol. 21, 1089-1097.
47. Yaffe, M. P. & Schatz, G. (1984). Two nuclear mutations that block mitochondrial protein import in yeast. Proc. Natl Acad. Sci. USA, 81, 4819-4823.
48. Pratje, E., Mannhaupt, G., Michaelis, G. & Beyreuther, K. (1983). A nuclear mutation prevents processing of a mitochondrially encoded membrane protein in Saccharomyces cerevisiae. EMBO J. 2, 1049-1054.
49. Esser, K., Scholle, B. & Michaelis, G. (1999). Disruption of six open reading frames on chromosome X of Saccharomyces cerevisiae reveals a cluster of four essential genes. Yeast, 15, 921-933.
50. Hill, J. E., Myers, A. M., Koerner, T. J. & Tzagoloff, A. (1986). Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast, 2, 163-167.
51. Gietz, R. D. & Sugino, A. (1988). New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene, 74, 527-534.
52. Daley, D. O., Adams, K. L., Clifton, R., Qualmann, S., Millar, A. H., Palmer, J. D. et al. (2002). Gene transfer from the mitochondrion to the nucleus: Novel mechanisms for gene activation from Cox2. Plant J. 30, 11-21.
53. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning, A Laboratory Manual, 2nd Edit., vols. 1-3, Cold Spring Harbour Laboratory Press, Cold Spring Harbor, NY.
54. Holm, C., Meeks-Wagner, D. W., Fangman, W. L. & Botstein, D. (1986). A rapid, efficient method for isolating DNA from yeast. Gene, 42, 169-173.
55. Gietz, R. D., Schiestl, R. H., Willems, A. R. & Woods, R. A. (1995). Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast, 11, 355-360.
56. Nasmyth, K. A. & Reed, S. I. (1980). Isolation of genes by complementation in yeast: Molecular cloning of a cell-cycle gene. Proc. Natl Acad. Sci. USA, 77, 2119-2123.
57. Pratje, E. & Michaelis, G. (1977). Mapping of the two mitochondrial antimycin A resistance loci in Saccharomyces cerevisiae. Mol. Gen. Genet. 152, 167-174.