Functional characterization of Rpn3 uncovers a distinct 19S proteasomal subunit requirement for ubiquitin-dependent proteolysis of cell cycle regulatory proteins in budding yeast

Molecular and Cellular Biology

Volumn 19, Issue 10, 1999, Pages 6872-6890

  Bailly, Eric ^a,b,c   Reed, Steven I ^b  

^a INSTITUT CURIE   (France)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Lab d'Ingenierie Systemes M   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSE; GLUCOSE; REGULATOR PROTEIN;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; ENZYME ACTIVATION; FUNGUS GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STRAIN DIFFERENCE; TEMPERATURE SENSITIVE MUTANT;

FUNGI; SACCHAROMYCETALES;

EID: 0032826785     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.10.6872     Document Type: Article

References (68)

1. Amon, A., S. Irniger, and K. Nasmyth. 1994. Closing the cell cycle circle: G2 cyclin proteolysis initiated at mitosis persists until activation of G1 cyclins in the next cell cycle. Cell 77:1037-1050.
2. Bai, C., P. Sen, K. Hofmann, L. Ma, M. Goebl, J. W. Harper, and S. J. Elledge. 1996. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263-274.
3. Bailly, E. Unpublished results.
4. Barral, Y., S. Jentsch, and C. Mann. 1995. G1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast. Genes Dev. 9:399-409.
5. Baumeister, W., J. Walz, F. Zhul, and E. Seemuller. 1998. The proteasome: paradigm of a self-compartmentalizing protease. Cell 92:367-380.
6. Cohen-Fix, O., J.-M. Peters, M. W. Kirschner, and D. Koshland. 1996. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10: 3081-3093.
7. Coux, O., K. Tanaka, and A. L. Goldberg. 1996. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:639-650.
8. Deshaies, R. J. 1995. The self-destructive personality of a cell cycle in transition. Curr. Opin. Cell Biol. 7:781-789.
9. Deshaies, R. J. 1997. Phosphorylation and proteolysis: partners in the regulation of cell division in budding yeast. Curr. Opin. Genet. Dev. 7:7-16.
10. Deshaies, R. J., V. Chau, and M. W. Kirschner. 1995. Ubiquitination of the G1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J. 14:303-314.
11. Elble, R. 1992. A simple and efficient procedure for transformation of yeasts. BioTechniques 13:18-20.
12. Feldman, R. M. R., C. C. Correll, K. B. Kaplan, and R. J. Deshaies. 1997. A complex of Cdc4p, Skp1p and Cdc53/Cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91:221-230.
13. Finley, D., K. Tanaka, C. Mann, H. Feldmann, M. Hochstrasser, R. Vierstra, S. Johnston, R. Hampton, J. Haber, J. McCusker, P. Silver, L. Frontali, P. Thorsness, A. Varshavsky, B. Byers, K. Madura, S. I. Reed, D. Wolf, S. Jentsch, T. Sommer, W. Baumeister, A. Goldberg, V. Fried, D. M. Rubin, M. H. Glickman, and A. Toh-e. 1998. Unified nomenclature for subunits of the Saccharomyces cerevisiae proteasome regulatory particle. Trends Biochem. Sci. 23:244-245.
14. Fu, H., S. Sadis, D. M. Rubin, M. Glickman, S. van Nocker, D. Finley, and R. D. Vierstra. 1998. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26S proteasome subunit Mcb1. J. Biol. Chem. 273:1970-1981.
15. Fujimoro, M., K. Tanaka, H. Yokosawa, and A. Toh-e. 1998. Son1 is a component of the 26S proteasome of the yeast Saccharomyces cerevisiae. FEBS Lett. 423:149-154.
16. Funabiki, H., H. Yamano, K. Kumada, K. Nagao, T. Hunt, and M. Yanagida. 1996. Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature 381:438-441.
17. GenomeWet. 5 February 1998, revision date. [Online.] Sequence interpretation tools, Clustal W program, Institute of Medical Science, University of Tokyo, Tokyo, Japan. www.genome.ad.jp/SIT/SIT.html. [10 August 1999, last date accessed.]
18. Germain, D., J. Hendley, and B. Futcher. 1997. DNA damage inhibits proteolysis of the B-type cyclin Clb5 in S. cerevisiae. J. Cell Sci. 110:1813-1820.
19. Ghislain, M., A. Udvardy, and C. Mann. 1993. S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature 366:358-362.
20. Glickman, M. H., D. M. Rubin, V. A. Fried, and D. Finley. 1998. The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell. Biol. 18:3149-3162.
21. Glickman, M. H., D. M. Rubin, O. Coux, I. Wefes, G. Pfeifer, Z. Cjeka, W. Baumeister, V. A. Fried, and D. Finley. 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.
22. Glotzer, M., A. W. Murray, and M. W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349:132-138.
23. Groll, M., L. Ditzel, J. Lowe, D. Stock, M. Bochtler, H. D. Bartunik, and R. Huber. 1997. Structure of the 20S proteasome from yeast at 2.4 Å resolution. Nature 386:463-471.
24. Henchoz, S., Y. Chi, B. Catarin, I. Herskowitz, R. J. Deshaies, and M. Peter. 1997. Phosphorylation- and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast. Genes Dev. 11:3046-3060.
25. Hershko, A. 1997. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr. Opin. Cell Biol. 9:788-799.
26. Hochstrasser, M. 1996. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30:405-439.
27. Hofmann, K., and P. Bucher. 1998. The PCI domain: a common theme in three multiprotein complexes. Trends Biochem. Sci. 23:204-205.
28. Hoyt, M. A. 1997. Eliminating all obstacles: regulated proteolysis in the eukaryotic cell cycle. Cell 91:149-151.
29. Irniger, S., S. Piatti, C. Michaelis, and K. Nasmyth. 1995. Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81:269-278.
30. Irniger, S., and K. Nasmyth. 1997. The anaphase-promoting complex is required in G1 arrested yeast cells to inhibit B-type cyclin accumulation and to prevent uncontrolled entry into S-phase. J. Cell Sci. 110:1523-1531.
31. ISREC Bioinformatics Groupe. 17 July 1999, revision date. [Online.] Box-shade program, version 3.21. Institut Suisse de Recherche Experimentale sur le Cancer, Epalinges, Switzerland. www.isrec.isb-sib.ch. [10 August 1999, last date accessed.]
32. Jentsch, S. 1992. The ubiquitin-conjugation system. Annu. Rev. Genet. 26: 179-207.
33. Kaiser, P., V. Moncollin, D. J. Clarke, M. H. Watson, B. L. Bertolaet, S. I. Reed, and E. Bailly. 1999. Cyclin-dependent kinase and Cks/Suc1 interact with the proteasome in yeast to control proteolysis of M-phase targets. Genes Dev. 13:1190-1202.
34. Kawamura, M., K. Kominami, J. Takeuchi, and A. Toh-e. 1996. A multicopy suppressor of nin1-1 of the yeast Saccharomyces cerevisiae is a counterpart of the Drosophila melanogaster diphenol oxidase A2 gene, Dox-A2. Mol. Gen. Genet. 251:146-152.
35. King, R. W., J.-M. Peters, S. Tugendreich, M. Rolfe, P. Hieter, and M. W. Kirschner. 1995. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81:279-288.
36. King, R. W., R. J. Deshaies, J.-M. Peters, and M. W. Kirschner. 1996. How proteolysis drives the cell cycle. Science 274:1652-1659.
37. Kominami, K., N. Okura, M. Kawamura, G. N. Demartino, C. A. Slaughter, N. Shimbara, C. H. Chung, M. Fujimuro, H. Yokosawa, Y. Shimizu, N. Tanahashi, K. Tanaka, and A. Toh-e. 1997. Yeast counterparts of subunits S5a and p58 (S3) of the human 26S proteasome are encoded by two multicopy suppressors of nin1-1. Mol. Biol. Cell 8:171-187.
38. Kominami, K., G. N. DeMartino, C. R. Moomaw, C. A. Slaughter, N. Shimbara, M. Fujimoro, H. Yokosawa, H. Hisamatsu, N. Tanahashi, Y. Shimizu, K. Tanaka, and A. Toh-e. 1995. Nin1p, a regulatory subunit of the 26S proteasome, is necessary for activation of Cdc28p kinase of Saccharomyces cerevisiae. EMBO J. 14:3105-3115.
39. Lanker, S., M. H. Valdivieso, and C. Wittenberg. 1996. Rapid degradation of the G1 cyclin Cln2 induced by CDK-dependent phosphorylation. Science 271:1597-1601.
40. Larsen, C. N., and D. Finley. 1997. Protein translocation channels in the proteasome and other proteases. Cell 91:431-434.
41. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
42. Nasmyth, K. 1996. At the heart of the budding yeast cell cycle. Trends Genet. 12:405-412.
43. Nigg, E. A. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17:471-480.
44. Pagano, M. 1997. Cell cycle regulation by the ubiquitin pathway. FASEB J. 11:1067-1075.
45. Patton, E. E., A. R. Willems, and M. Tyers. 1998. Combinatorial control in ubiquitin-dependent proteolysis: don't Skp the F-box hypothesis. Trends Genet. 14:236-243.
46. Peter, M., and I. Herskowitz. 1994. Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell 79:181-184.
47. Pickart, C. M. 1997. Targeting of substrates to the 26S proteasome. FASEB J. 11:1055-1066.
48. Pines, J., and T. Hunter. 1991. Cyclin-dependent kinases: a new cell cycle motif? Trends Cell Biol. 1:117-121.
49. Pringle, J. R., A. E. M. Adams, D. G. Drubin, and B. K. Haarer. 1991. Immunofluorescence methods for yeast. Methods Enzymol. 194:565-602.
50. Reed, S. I., J. A. Hadwiger, and A. Lorincz. 1985. Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. Proc. Natl. Acad. Sci. USA 82:4055-4059.
51. Rubin, D. M., M. H. Glickman, C. N. Larsen, S. Dhruvakumar, and D. Finley. 1998. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 17:4909-4919.
52. Schneider, B. L., Q.-H. Yang, and A. B. Futcher. 1996. Linkage of replication to Start by the Cdk inhibitor Sic1. Science 272:560-562.
53. Schneider, B. L., E. E. Patton, S. Lanker, M. D. Mendenhall, C. Wittenberg, B. Futcher, and M. Tyers. 1998. Yeast G1 cyclins are unstable in G1 phase. Nature 395:86-89.
54. S1C1 controls the G1 to S transition in S. cerevisiae. Cell 79:239-244.
55. Seufert, W., B. Futcher, and S. Jentsch. 1995. Role of ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature 373:78-81.
56. Sherman, F., G. Fink, and J. B. Hicks. 1982. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
57. Shirayama, M., W. Zachariae, R. Ciosk, and K. Nasmyth. 1998. The polo-like kinase Cdc5p and the WD-repeat protein Cdc20p/fizzy are regulators and substrates of the anaphase promoting complex in Saccharomyces cerevisiae. EMBO J. 17:1336-1349.
58. Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219.
59. CDC28 histone H1 kinase activity is unable to promote entry into mitosis in checkpoint-arrested cells of the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 13:3744-3755.
60. Sudakin, V., D. Ganoth, A. Dahan, A. Heller, J. Hershko, F. C. Luca, J. V. Ruderman, and A. Hershko. 1995. The cyclosome, a large complex containing ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 6:185-198.
61. Surana, U., A. Amon, C. Dowzer, J. McGrew, B. Byers, and K. Nasmyth. 1993. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. EMBO J. 12:1969-1978.
62. Tang, Y., and S. I. Reed. 1993. The Cdk-associated protein Cks1 functions both in G1 and G2 in Saccharomyces cerevisiae. Genes Dev. 7:822-832.
63. S1C1 imposes the requirement for Cln G1 cyclin function at Start. Proc. Natl. Acad. Sci. USA 93:7772-7776.
64. van Nocker, S., S. Sadis, D. M. Rubin, M. Glickman, H. Fu, O. Coux, I. Wefes, D. Finley, and R. D. Vierstra. 1996. The multiubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome and plays a nonessential, substrate-specific role in protein turnover. Mol. Cell. Biol. 16:6020-6028.
65. Verma, R., R. S. Annan, M. J. Huddleston, S. A. Carr, G. Reynard, and R. J. Deshaies. 1997. Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278:455-460.
66. Willems, A. R., S. Lanker, E. E. Patton, K. L. Craig, T. F. Nason, N. Mathias, R. Kobayashi, C. Wittenberg, and M. Tyers. 1996. Cdc53 targets phosphorylated G1 cyclins for degradation by the ubiquitin proteolytic pathway. Cell 86:453-463.
67. CDC28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol. 15:731-741.
68. Yamamoto, A., V. Guacci, and D. Koshland. 1996. Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J. Cell Biol. 133:99-110.