Characterization of Mmp37p, a Saccharomyces cerevisiae mitochondrial matrix protein with a role in mitochondrial protein import

Molecular Biology of the Cell

Volumn 17, Issue 9, 2006, Pages 4051-4062

  Gallas, Michelle R ^a   Dienhart, Mary K ^b   Stuart, Rosemary A ^b   Long, Roy M ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Marquette University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; MITOCHONDRIAL PROTEIN; MMP37P PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ORGANELLE; MEMBRANE VESICLE; MITOCHONDRION; NONHUMAN; OPEN READING FRAME; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; TEMPERATURE SENSITIVITY; YEAST;

CELL SURVIVAL; CHAPERONINS; DNA, MITOCHONDRIAL; HAPLOIDY; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; MEIOSIS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; OPEN READING FRAMES; PROTEIN FOLDING; PROTEIN PRECURSORS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 33748108494     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-04-0366     Document Type: Article

References (53)

1. o-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17, 7170-7178.
2. Chacinska, A. et al. (2005). Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120, 817-829.
3. Chacinska, A., Rehling, P., Guiard, B., Frazier, A. E., Schulze-Specking, A., Pfanner, N., Voos, W., and Meisinger, C. (2003). Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex. EMBO J. 22, 5370-5381.
4. Curran, S. P., Leuenberger, D., Oppliger, W., and Koehler, C. M. (2002a). The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier. EMBO J. 21, 942-953.
5. Curran, S. P., Leuenberger, D., Schmidt, E., and Koehler, C. M. (2002b). The role of the Tim8p-Tim13p complex in a conserved import pathway for mitochondrial polytopic inner membrane proteins. J. Cell Biol. 158, 1017-1027.
6. D'Silva, P. D., Schilke, B., Walter, W., Andrew, A., and Craig, E. A. (2003). J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix. Proc. Natl. Acad. Sci. USA 100, 13839-13844.
7. Dunn, C. D., and Jensen, R. E. (2003). Suppression of a defect in mitochondrial protein import identifies cytosolic proteins required for viability of yeast cells lacking mitochondrial DNA. Genetics 165, 35-45.
8. Entian, K. D. et al. (1999). Functional analysis of 150 deletion mutants in Saccharomyces cerevisiae by a systematic approach. Mol. Gen. Genet. 262, 683-702.
9. Gaume, B., Klaus, C., Ungermann, C., Guiard, B., Neupert, W., and Brunner, M. (1998). Unfolding of preproteins upon import into mitochondria. EMBO J. 17, 6497-6507.
10. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
11. Giaever, G. et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
12. Gietz, R. D., and 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.
13. Glick, B. S., Wachter, C., Reid, G. A., and Schatz, G. (1993). Import of cytochrome b2 to the mitochondrial intermembrane space: the tightly folded heme-binding domain makes import dependent upon matrix ATP. Protein Sci. 2, 1901-1917.
14. Guldener, U., Heck, S., Fielder, T., Beinhauer, J., and Hegemann, J. H. (1996). A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24, 2519-2524.
15. Herrmann, J. M., Folsch, H., Neupert, W., and Stuart, R. A. (1994). Cell Biology: A Laboratory Handbook, San Diego, CA: Academic Press.
16. Huang, S., Murphy, S., and Matouschek, A. (2000). Effect of the protein import machinery at the mitochondrial surface on precursor stability. Proc. Natl. Acad. Sci. USA 97, 12991-12996.
17. Ishikawa, D., Yamamoto, H., Tamura, Y., Moritoh, K., and Endo, T. (2004). Two novel proteins in the mitochondrial outer membrane mediate beta-barrel protein assembly. J. Cell Biol. 166, 621-627.
18. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
19. Jansen, R. P., Dowzer, C., Michaelis, C., Galova, M., and Nasmyth, K. (1996). Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Cell 84, 687-697.
20. Johnston, S. A., and Hopper, J. E. (1982). Isolation of the yeast regulatory gene GAL4 and analysis of its dosage effects on the galactose/melibiose regulon. Proc. Natl. Acad. Sci. USA 79, 6971-6975.
21. Kang, P. J., Ostermann, J., Shilling, J., Neupert, W., Craig, E. A., and Pfanner, N. (1990). Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348, 137-143.
22. Kerscher, O., Sepuri, N. B., and Jensen, R. E. (2000). Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane. Mol. Biol. Cell 11, 103-116.
23. Koehler, C. M. (2004). New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol. 20, 309-335.
24. Koehler, C. M., Jarosch, E., Tokatlidis, K., Schmid, K., Schweyen, R. J., and Schatz, G. (1998). Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279, 369-373.
25. Koehler, C. M., Merchant, S., and Schatz, G. (1999). How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem. Sci. 24, 428-432.
26. Kozany, C., Mokranjac, D., Sichting, M., Neupert, W., and Hell, K. (2004). The J domain-related cochaperone Tim16 is a constituent of the mitochondrial TIM23 preprotein translocase. Nat. Struct. Mol. Biol. 11, 234-241.
27. Leuenberger, D., Bally, N. A., Schatz, G., and Koehler, C. M. (1999). Different import pathways through the mitochondrial intermembrane space for inner membrane proteins. EMBO J. 18, 4816-4822.
28. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
29. Mokranjac, D., Paschen, S. A., Kozany, C., Prokisch, H., Hoppins, S. C., Nargang, F. E., Neupert, W., and Hell, K. (2003a). Tim50, a novel component of the TIM23 preprotein translocase of mitochondria. EMBO J. 22, 816-825.
30. Mokranjac, D., Sichting, M., Neupert, W., and Hell, K. (2003b). Tim14, a novel key component of the import motor of the TIM23 protein translocase of mitochondria. EMBO J. 22, 4945-4956.
31. Munn, A. L., Silveira, L., Elgort, M., and Payne, G. S. (1991). Viability of clathrin heavy-chain-deficient Saccharomyces cerevisiae is compromised by mutations at numerous loci: implications for the suppression hypothesis. Mol. Cell. Biol. 11, 3868-3878.
32. Neupert, W. (1997). Protein import into mitochondria. Annu. Rev. Biochem., 66, 863-917.
33. Perry, A. J., and Lithgow, T. (2005). Protein targeting: entropy, energetics and modular machines. Curr. Biol. 25, R423-R425.
34. Pfanner, N., Craig, E. A., and Honlinger, A. (1997). Mitochondrial preprotein translocase. Annu. Rev. Cell Dev. Biol. 13, 25-51.
35. Rassow, J., Hartl, F. U., Guiard, B., Pfanner, N., and Neupert, W. (1990). Polypeptides traverse the mitochondrial envelope in an extended state. FEBS Lett. 275, 190-194.
36. Rehling, P., Brandner, K., and Pfanner, N. (2004). Mitochondrial import and the twin-pore translocase. Nat. Rev. Mol. Cell Biol. 5, 519-530.
37. Rose, M. D., Winston, F., and Mieter, P. (1990). Methods in Yeast Genetics. A Laboratory Course Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Sanjuan Szklarz, L. K. et al. (2005). Inactivation of the mitochondrial heat shock protein zim17 leads to aggregation of matrix hsp70s followed by pleiotropic effects on morphology and protein biogenesis. J. Mol. Biol. 351, 206-218.
39. Schleyer, M., and Neupert, W. (1985). Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell 43, 339-350.
40. Sherman, F., Fink, G. R., and Hicks, J. (1986). Laboratory Course Manual for Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Press.
41. Sirrenberg, C., Endres, M., Folsch, H., Stuart, R. A., Neupert, W., and Brunner, M. (1998). Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature 391, 912-915.
42. Spencer, F., Gerring, S. L., Connelly, C., and Hieter, P. (1990). Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124, 237-249.
43. Stuart, R. A., Gruhler, A., van der Klei, I., Guiard, B., Koll, H., and Neupert, W. (1994). The requirement of matrix ATP for the import of precursor proteins into the mitochondrial matrix and intermembrane space. Eur. J. Biochem. 220, 9-18.
44. Teichmann, U., van Dyck, L., Guiard, B., Fischer, H., Glockshuber, R., Neupert, W., and Langer, T. (1996). Substitution of PIM1 protease in mitochondria by Escherichia coli Lon protease. J. Biol. Chem. 271, 10137-10142.
45. Thorsness, P. E., and Fox, T. D. (1993). Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 134, 21-28.
46. Thorsness, P. E., White, K. H., and Fox, T. D. (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.
47. Truscott, K. N. et al. (2003). A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. J. Cell Biol. 163, 707-713.
48. Ungermann, C., Neupert, W., and Cyr, D. M. (1994). The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266, 1250-1253.
49. van der Laan, M., Chacinska, A., Lind, M., Perschil, I., Sickmann, A., Meyer, H. E., Guiard, B., Meisinger, C., Pfanner, N., and Rehling, P. (2005). Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol. Cell. Biol. 25, 7449-7458.
50. Vestweber, D., and Schatz, G. (1988). Point mutations destabilizing a precursor protein enhance its post-translational import into mitochondria. EMBO J. 7, 1147-1151.
51. Winzeler, E. A. et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
52. Yokota, K. et al. (1996). cDNA cloning of p112, the largest regulatory subunit of the human 26s proteasome, and functional analysis of its yeast homologue, Sen3p. Mol. Biol. Cell 7, 853-870.
53. Zhong, Q., Gvozdenovic-Jeremic, J., Webster, P., Zhou, J., and Greenberg, M. L. (2005). Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids. Mol. Biol. Cell 16, 665-675.