A nonproteolytic proteasome activity controls organelle fission in yeast

Journal of Cell Science

Volumn 122, Issue 20, 2009, Pages 3673-3683

  Hofmann, Line ^a   Saunier, Rémy ^a   Cossard, Raynald ^a   Esposito, Michela ^b   Rinaldi, Teresa ^b   Delahodde, Agnès ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Fission; Mitochondria; Peroxisomes; Proteasome

Indexed keywords

PROTEASOME; PROTEIN FIS1; PROTEIN RPN11; UNCLASSIFIED DRUG;

ARTICLE; CELL FRACTIONATION; CELL ORGANELLE; CONTROLLED STUDY; DYNAMICS; FLUORESCENCE MICROSCOPY; FUNGAL CELL; FUNGAL STRAIN; MITOCHONDRION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CELL CYCLE; CELL DIVISION; GLUCOSE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; OLEIC ACID; ORGANELLES; PEROXISOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TEMPERATURE;

MAMMALIA;

EID: 70350366617     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.050229     Document Type: Article

References (73)

1. Altmann, K. and Westermann, B. (2005). Role of essential genes in mitochondrial morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 5410-5417.
2. Baumeister, W., Walz, J., Zuhl, F. and Seemuller, E. (1998). The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367-380.
3. Bleazard, W., McCaffery, J. M., King, E. J., Bale, S., Mozdy, A., Tieu, Q., Nunnari, J. and Shaw, J. M. (1999). The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1, 298-304.
4. Braun, B. C., Glickman, M., Kraft, R., Dahlmann, B., Kloetzel, P. M., Finley, D. and Schmidt, M. (1999). The base of the proteasome regulatory particle exhibits chaperone-like activity. Nat. Cell Biol. 1, 221-226.
5. Butow, R. A. and Avadhani, N. G. (2004). Mitochondrial signaling: the retrograde response. Mol. Cell 14, 1-15.
6. Cerveny, K. L., McCaffery, J. M. and Jensen, R. E. (2001). Division of mitochondria requires a novel DMN1-interacting protein, Net2p. Mol. Biol. Cell 12, 309-321.
7. Cohen, M. M., Leboucher, G. P., Livnat-Levanon, N., Glickman, M. H. and Weissman, A. M. (2008). Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol. Biol. Cell 19, 2457-2464.
8. Collins, G. A. and Tansey, W. P. (2006). The proteasome: a utility tool for transcription? Curr. Opin. Genet. Dev. 16, 197-202.
9. Demartino, G. N. and Gillette, T. G. (2007). Proteasomes: machines for all reasons. Cell 129, 659-662.
10. Durr, M., Escobar-Henriques, M., Merz, S., Geimer, S., Langer, T. and Westermann, B. (2006). Nonredundant roles of mitochondria-associated F-box proteins Mfb1 and Mdm30 in maintenance of mitochondrial morphology in yeast. Mol. Biol. Cell 17, 3745-3755.
11. Fekkes, P., Shepard, K. A. and Yaffe, M. P. (2000). Gag3p, an outer membrane protein required for fission of mitochondrial tubules. J. Cell Biol. 151, 333-340.
12. Ferdous, A., Gonzalez, F., Sun, L., Kodadek, T. and Johnston, S. A. (2001). The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol. Cell 7, 981-991.
13. Fisk, H. A. and Yaffe, M. P. (1999). A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J. Cell Biol. 145, 1199-1208.
14. Gancedo, C. and Flores, C. L. (2008). Moonlighting proteins in yeasts. Microbiol. Mol. Biol. Rev. 72, 197-210; table of contents.
15. Glickman, M. H. and Ciechanover, A. (2002). The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373-428.
16. Glickman, M. H., Rubin, D. M., Coux, O., Wefes, I., Pfeifer, G., Cjeka, Z., Baumeister, W., Fried, V. A. and Finley, D. (1998). A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615-623.
17. Glickman, M. H., Rubin, D. M., Fu, H., Larsen, C. N., Coux, O., Wefes, I., Pfeifer, G., Cjeka, Z., Vierstra, R., Baumeister, W. et al. (1999). Functional analysis of the proteasome regulatory particle. Mol. Biol. Rep. 26, 21-28.
18. Gonzalez, F., Delahodde, A., Kodadek, T. and Johnston, S. A. (2002). Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 296, 548-550.
19. Griffin, E. E., Graumann, J. and Chan, D. C. (2005). The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J. Cell Biol. 170, 237-248.
20. Gurvitz, A., Hiltunen, J. K., Erdmann, R., Hamilton, B., Hartig, A., Ruis, H. and Rottensteiner, H. (2001). Saccharomyces cerevisiae Adr1p governs fatty acid betaoxidation and peroxisome proliferation by regulating POX1 and PEX11. J. Biol. Chem. 276, 31825-31830.
21. Halbach, A., Landgraf, C., Lorenzen, S., Rosenkranz, K., Volkmer-Engert, R., Erdmann, R. and Rottensteiner, H. (2006). Targeting of the tail-anchored peroxisomal membrane proteins PEX26 and PEX15 occurs through C-terminal PEX19-binding sites. J. Cell Sci. 119, 2508-2517.
22. Heinemeyer, W., Gruhler, A., Mohrle, V., Mahe, Y. and Wolf, D. H. (1993). PRE2, highly homologous to the human major histocompatibility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chrymotryptic activity and degradation of ubiquitinated proteins. J. Biol. Chem. 268, 5115-5120.
23. Hermann, G. J., Thatcher, J. W., Mills, J. P., Hales, K. G., Fuller, M. T., Nunnari, J. and Shaw, J. M. (1998). Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143, 359-373.
24. Hilt, W. and Wolf, D. H. (1996). Proteasomes: destruction as a programme. Trends Biochem. Sci. 21, 96-102.
25. Hilt, W., Heinemeyer, W. and Wolf, D. H. (1993). Studies on the yeast proteasome uncover its basic structural features and multiple in vivo functions. Enzyme Protein 47, 189-201.
26. Hilt, W., Heinemeyer, W. and Wolf, D. H. (1996). The proteasome and protein degradation in yeast. Adv. Exp. Med. Biol. 389, 197-202.
27. Hitchcock, A. L., Auld, K., Gygi, S. P. and Silver, P. A. (2003). A subset of membrane-associated proteins is ubiquitinated in response to mutations in the endoplasmic reticulum degradation machinery. Proc. Natl. Acad. Sci. USA 100, 12735-12740.
28. Hoepfner, D., Schildknegt, D., Braakman, I., Philippsen, P. and Tabak, H. F. (2005). Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122, 85-95.
29. Jensen, R. E., Hobbs, A. E., Cerveny, K. L. and Sesaki, H. (2000). Yeast mitochondrial dynamics: fusion, division, segregation, and shape. Microsc. Res. Tech. 51, 573-583.
30. Karbowski, M., Neutzner, A. and Youle, R. J. (2007). The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 178, 71-84.
31. Kleijnen, M. F., Kirkpatrick, D. S. and Gygi, S. P. (2007). The ubiquitin-proteasome system regulates membrane fusion of yeast vacuoles. EMBO J. 26, 275-287.
32. Kobayashi, S., Tanaka, A. and Fujiki, Y. (2007). Fis1, DLP1, and Pex11p coordinately regulate peroxisome morphogenesis. Exp. Cell Res. 313, 1675-1686.
33. Koch, A., Yoon, Y., Bonekamp, N. A., McNiven, M. A. and Schrader, M. (2005). A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 16, 5077-5086.
34. Kuravi, K., Nagotu, S., Krikken, A. M., Sjollema, K., Deckers, M., Erdmann, R., Veenhuis, M. and van der Klei, I. J. (2006). Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J. Cell Sci. 119, 3994-4001.
35. Lazarow, P. B. and Fujiki, Y. (1985). Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1, 489-530.
36. Li, X. and Gould, S. J. (2003). The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J. Biol. Chem. 278, 17012-17020.
37. 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.
38. Marshall, P. A., Krimkevich, Y. I., Lark, R. H., Dyer, J. M., Veenhuis, M. and Goodman, J. M. (1995). Pmp27 promotes peroxisomal proliferation. J. Cell Biol. 129, 345-355.
39. Mayor, T., Graumann, J., Bryan, J., MacCoss, M. J. and Deshaies, R. J. (2007). Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell Proteomics 6, 1885-1895.
40. Motley, A. M. and Hettema, E. H. (2007). Yeast peroxisomes multiply by growth and division. J. Cell Biol. 178, 399-410.
41. Motley, A. M., Ward, G. P. and Hettema, E. H. (2008). Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p. J. Cell Sci. 121, 1633-1640.
42. Mozdy, A. D., McCaffery, J. M. and Shaw, J. M. (2000). Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell Biol. 151, 367-380.
43. Nagotu, S., Krikken, A. M., Otzen, M., Kiel, J. A., Veenhuis, M. and van der Klei, I. J. (2008a). Peroxisome fission in Hansenula polymorpha requires Mdv1 and Fis1, two proteins also involved in mitochondrial fission. Traffic 9, 1471-1484.
44. Nagotu, S., Saraya, R., Otzen, M., Veenhuis, M. and van der Klei, I. J. (2008b). Peroxisome proliferation in Hansenula polymorpha requires Dnm1p which mediates fission but not de novo formation. Biochim. Biophys. Acta 1783, 760-769.
45. Nakamura, A., Kitami, T., Mori, H., Mizuno, Y. and Hattori, N. (2006). Nuclear localization of the 20S proteasome subunit in Parkinson's disease. Neurosci. Lett. 406, 43-48.
46. Narendra, D., Tanaka, A., Suen, D. F. and Youle, R. J. (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803.
47. Neutzner, A. and Youle, R. J. (2005). Instability of the mitofusin Fzo1 regulates mitochondrial morphology during the mating response of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 280, 18598-18603.
48. Otsuga, D., Keegan, B. R., Brisch, E., Thatcher, J. W., Hermann, G. J., Bleazard, W. and Shaw, J. M. (1998). The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143, 333-349.
49. Peng, Z., Shen, Y., Feng, S., Wang, X., Chitteti, B. N., Vierstra, R. D. and Deng, X. W. (2003). Evidence for a physical association of the COP9 signalosome, the proteasome, and specific SCF E3 ligases in vivo. Curr. Biol. 13, R504-R505.
50. Picton, L. K., Casares, S., Monahan, A. C., Majumdar, A. and Hill, R. B. (2009). Evidence for conformational heterogeneity of fission protein Fis1 from Saccharomyces cerevisiae. Biochemistry 48, 6598-6609.
51. Reed, S. H. and Gillette, T. G. (2007). Nucleotide excision repair and the ubiquitin proteasome pathway-do all roads lead to Rome? DNA Repair (Amst.) 6, 149-156.
52. Rinaldi, T., Ricci, C., Porro, D., Bolotin-Fukuhara, M. and Frontali, L. (1998). A mutation in a novel yeast proteasomal gene, RPN11/MPR1, produces a cell cycle arrest, overreplication of nuclear and mitochondrial DNA, and an altered mitochondrial morphology. Mol. Biol. Cell 9, 2917-2931.
53. Rinaldi, T., Ricordy, R., Bolotin-Fukuhara, M. and Frontali, L. (2002). Mitochondrial effects of the pleiotropic proteasomal mutation mpr1/rpn11: uncoupling from cell cycle defects in extragenic revertants. Gene 286, 43-51.
54. Rinaldi, T., Pick, E., Gambadoro, A., Zilli, S., Maytal-Kivity, V., Frontali, L. and Glickman, M. H. (2004). Participation of the proteasomal lid subunit Rpn11 in mitochondrial morphology and function is mapped to a distinct C-terminal domain. Biochem. J. 381, 275-285.
55. Rinaldi, T., Hofmann, L., Gambadoro, A., Cossard, R., Livnat-Levanon, N., Glickman, M. H., Frontali, L. and Delahodde, A. (2008). Dissection of the carboxyl-terminal domain of the proteasomal subunit Rpn11 in maintenance of mitochondrial structure and function. Mol. Biol. Cell 19, 1022-1031.
56. Rubin, D. M., Glickman, M. H., Larsen, C. N., Dhruvakumar, S. and Finley, D. (1998). Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 17, 4909-4919.
57. Schauss, A. C., Bewersdorf, J. and Jakobs, S. (2006). Fis1p and Caf4p, but not Mdv1p, determine the polar localization of Dnm1p clusters on the mitochondrial surface. J. Cell Sci. 119, 3098-3106.
58. Serasinghe, M. N. and Yoon, Y. (2008). The mitochondrial outer membrane protein hFis1 regulates mitochondrial morphology and fission through self-interaction. Exp. Cell Res. 314, 3494-3507.
59. Sesaki, H. and Jensen, R. E. (1999). Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147, 699-706.
60. Sesaki, H. and Jensen, R. E. (2001). UGO1 encodes an outer membrane protein required for mitochondrial fusion. J. Cell Biol. 152, 1123-1134.
61. Shaw, J. M. and Nunnari, J. (2002). Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12, 178-184.
62. Sone, T., Saeki, Y., Toh-e, A. and Yokosawa, H. (2004). Sem1p is a novel subunit of the 26 S proteasome from Saccharomyces cerevisiae. J. Biol. Chem. 279, 28807-28816.
63. Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C. and Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature 402, 371-372.
64. Thompson, W. E., Ramalho-Santos, J. and Sutovsky, P. (2003). Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol. Reprod. 69, 254-260.
65. 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.
66. Tieu, Q. and Nunnari, J. (2000). Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J. Cell Biol. 151, 353-366.
67. Verma, R., Aravind, L., Oania, R., McDonald, W. H., Yates, J. R., 3rd, Koonin, E. V. and Deshaies, R. J. (2002). Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615.
68. Waterham, H. R., Koster, J., van Roermund, C. W., Mooyer, P. A., Wanders, R. J. and Leonard, J. V. (2007). A lethal defect of mitochondrial and peroxisomal fission. N. Engl. J. Med. 356, 1736-1741.
69. Wells, R. C., Picton, L. K., Williams, S. C., Tan, F. J. and Hill, R. B. (2007). Direct binding of the dynamin-like GTPase, Dnm1, to mitochondrial dynamics protein Fis1 is negatively regulated by the Fis1 N-terminal arm. J. Biol. Chem. 282, 33769-33775.
70. Wong, E. D., Wagner, J. A., Gorsich, S. W., McCaffery, J. M., Shaw, J. M. and Nunnari, J. (2000). The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J. Cell Biol. 151, 341-352.
71. Yaffe, M. P. (1999). The machinery of mitochondrial inheritance and behavior. Science 283, 1493-1497.
72. Yao, T. and Cohen, R. E. (2002). A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419, 403-407.
73. Yonashiro, R., Ishido, S., Kyo, S., Fukuda, T., Goto, E., Matsuki, Y., Ohmura-Hoshino, M., Sada, K., Hotta, H., Yamamura, H. et al. (2006). A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 25, 3618-3626.