SCF ubiquitin protein ligases and phosphorylation-dependent proteolysis

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1389, 1999, Pages 1533-1550

  Willems, Andrew R ^a   Goh, Theo ^a   Taylor, Lorne ^b   Chernushevich, Igor ^b   Shevchenko, Andrej ^c   Tyers, Mike ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MDS SCIEX   (Canada)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Cdc34; Cell cycle; Cyclin dependent kinase; E3 ubiquitin protein ligase; Skp1 Cdc53 F box protein

Indexed keywords

SACCHAROMYCES CEREVISIAE;

EID: 0033615329     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0497     Document Type: Article

References (100)

1. Adams, A., Gottschling, D. E., Kaiser, C. A. & Stearns, T. 1998 Methods in yeast cenetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. Aso, T., Haque, D., Barstead, R. J., Conaway, R. C. & Conaway, J. W. 1996 The inducible elongin A elongation activation domain: structure, function and interaction with the elongin BC complex. EMBO J. 15, 5557-5566.
3. Bai, C., Sen, P., Hofmann, K., Ma, L., Goebl, M., Harper, J. W. & Elledge, S. J. 1996 SKP1 connects cell cycle regulators to the ubiquitin protcolysis machinery through a novel motif, the F-box, Cell 86, 263-274.
4. Barral, Y., Jentsch, S. & Mann, C. 1995 G1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast. Genes Dev. 9, 399-409.
5. Baumeister, W., Walz, J., Zubl, F. & Seemuller, E. 1998 The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367-380.
6. Biemann, K. 1988 Contributions of mass spectrometry to peptide and protein structure. Biomed. Env. Mass Spectrom, 16, 99-111.
7. Brown, J. L., Jaquenoud, M., Gulli, M.-P., Chant, J. & Peter, M. 1997 Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev. 11. 2972-2982.
8. Chen, G. C., Kim, Y. J. & Chan, C. S. M. 1997 The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev. 11, 2958-2971.
9. Cho, R. J. (and 10 others) 1998 A genome-wide transcriptional analysis of the mitotic cell cycle. Mol. Cell 2, 65-73.
10. Chu, S., DeRisi, J., Eisen, M., Mulholland, J., Botstein, D., Brown, P. O. & Herskowitz, I. 1998 The transcriptional program of sporulation in budding yeast. Science 282, 699-705.
11. Coffino, P. 1998 Degradation of ornithine decarboxylase. In Ubiquitin and the biology of the cell (ed. J.-M. Peters, J. R. Harris & D. Finley), pp. 411-428. New York: Plenum Press.
12. Connelly, C. & Hieter, P. 1996 Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 86, 275-285.
13. Cross, F. R. 1988 DAFI, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae. Mol. Cell. Biol. 8, 4675-4684.
14. Deshaies, R. J., Chau, V. & Kirschner, M. 1995 Ubiquitination of the G1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J. 14, 303-312.
15. SDR25, a putative CDK inhibitor, has a role in the M/G1 transition in Saccharomyces cerevisiae. Genes Dev. 8, 1640-1653.
16. Drury, L. S., Perkins, G. & Diffley, J. F. X. 1997 The Cdc4/34/ 53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 16, 5966-5976.
17. Epstein, C. B. & Cross, F. R. 1994 Genes that can bypass the CLN requirement for Saccharomyces cerevisiae cell cycle START. Mol. Cell. Biol. 14, 2041-2047.
18. Feldman, R. M. R., Correll, C. C., Kaplan, K. B. & Deshaies, R. J. 1997 A complex of Cdc4, Skp1, and Cdc53/Cullin catalyses ubiquitination of the phosphorylated CDK inhibitor Sic1. Cell 91, 221-230.
19. Flick, J. S. & Johnston, M. 1991 Grrl of Saccharomyces cerevisiae is required for glucose repression and encodes a protein with leucine-rich repeats. Mol. Cell. Biol. 11, 5101-5112.
20. Gartner, A., Joavnovic, A., Jeoung, D. I., Bourlat, S., Cross, F. R. & Ammerer, G. 1998 Pheromone-dependent G1 cell cycle arrest requires Farl phosphorylation, but may not involve inhibition of Cdc28-Cln2 kinase, in vivo. Mol. Cell. Biol. 18, 3681-3691.
21. Germain, D., Hendley, J. & Futcher, B. 1997 DNA damage inhibits proteolysis of the B-type cyclin Clb5 in S. cerevisiae. J. Cell Sci. 110, 1813-1820.
22. Goebl, M. G., Yochem, J., Jentsch, S., McGrath, J. P., Varshavsky, A. & Byers, B. 1988 The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme. Science 241, 1331-1335.
23. Hadwiger, J. A., Wittenberg, C., Richardson, H. E., De Barros Lopes, M. & Reed, S. I. 1989 A family of cyclin homologs that control the G1 phase in yeast. Proc. Natl Acad. Sci. USA 86, 6255-6259.
24. Harper, J. W. & Elledge, S. J. 1996 Cdk inhibitors in development and cancer. Curr. Opin. Gen. Dev. 6, 56-64.
25. Henchoz, S., Chi, Y., Catarin, B., Herskowitz, I., Deshaies, R. J. & Peter, M. 1997 Phosphorylation and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Farlp in budding yeast. Genes Dev. 11, 3046-3060.
26. Hershko, A. & Ciechanover, A. 1998 The ubiquitin system. A. Rev. Biochem. 67, 425-479.
27. Hershko, A., Heller, H., Elias, S. & Ciechanover, A. 1983 Components of ubiquitin protein ligase system. Resolution, affinity purification, and role in protein breakdown, J. Biol. Chem. 258, 8206-8214.
28. Ingram, G. C., Doyle, S., Carpenter, R., Schultz, E. A., Simon, R. & Coen, E. S. 1997 Dual role for fimbriata in regulating floral homeotic genes and cell division in Antirrhinum. EMBO J. 16, 6521-6534.
29. cdcl8 by CDK phosphorylation. Genes Dev. 11, 2767-2779.
30. Jallepalli, P. V., Tien, D. & Kelly, T. J. 1998 sud1(+) targets cyclin-dependent kinase-phosphorylated Cdcl8 and Ruml proteins for degradation and stops unwanted diploidization in fission yeast. Proc., Natl Acad. Sci. USA 95, 8159-8164.
31. Grrl complex. EMBO J. 17, 5360-5373.
32. Jiang, J. & Struhl, G. 1998 Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391, 493-496.
33. Kaclin, W. G. & Maher, E. R. 1998 The VHL tumour-suppressor gene paradigm. Trends Genet. 14, 423-426.
34. Kaiser, P., Sia, R. A. L., Bardes, E. G. S., Lew, D. J. & Reed, S. I. 1998 Cdc34 and the F-box protein Met30 are required for degradation of the Cdk-inhibitory kinase Swel. Genes Dev. 12, 2587-2597.
35. Kamura, T. (and 11 others) 1999 Rbxl, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 284, 657-661.
36. Kaplan, K. B., Hyman, A. A. & Sorger, P. K. 1997 Regulating the yeast kinetochore by ubiquitin-dependent degradation and Skplp-mediated phosphorylation. Cell 91, 491-500.
37. Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. W. & Hedgecock, E. M. 1996 cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829-839.
38. Kishi, T. & Yamao, F. 1998 An essential function of Grrl for the degradation of Cln2 is to act as a binding core that links Cln2 to Skp1. J. Cell Sci. 111, 3655-3661.
39. Kishi, T., Seno, T. & Yamao, F. 1998 Grrl functions in the ubiquitin pathway in Saccharomyces cerevisiae through association with Skp1. Mol. Gen. Genet. 257, 143-148.
40. Kominami, K. & Toda, T. 1997 Fission yeast WD-repeat protein popl regulates genome ploidy through ubiquitin-proteasome-mediated degradation of the CDK inhibitor Ruml and the S-phase initiator Cdcl8. Genes Dev. 11. 1548-1560.
41. Kornitzer, D., Raboy, B., Kulka, R. G. & Fink, G. R. 1994 Regulated degradation of the transcription factor Gen4. EMBO J. 13, 6021-6030.
42. Krek, W. 1998 Proteolysis and the G1/S transition: the SCF conncection. Curr. Opin. Gen. Dev. 8, 36-42.
43. Kumar, A. & Paietta, J. V. 1998 An additional role for the F-box motif: gene regulation within the Neurospora crassa sulfur control network. Proc. Natl. Acad. Sci. USA 95, 2417-2422.
44. Cdc4 complex. Genes Dev. 12, 914-926.
45. Lanker, S., Valdivieso, M. H. & Wittenberg, C. 1996 Rapid degradation of the G1 cyclin Cln2 induced by CDK-dependent phosphorylation. Science 271, 1597-1601.
46. Lee, I., Wolfe, D. S., Nilsson, O. & Weigel, D. 1997 A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr. Biol. 7, 95-104.
47. Li, F. N. & Johnston, M. 1997 Grrl of S. cerevisiae is connected to the ubiquitination machinery through Skp1: coupling glucose sensing to gene expression and the cell cycle. EMBO J. 16, 5629-5638.
48. Liakopoulos, D., Doenges, G., Matuschewski, K. & Jentsch, S. 1998 A novel protein modification pathway related to the ubiquitin system. EMBO J. 17, 2208-2214.
49. SKP2: evidence for evolutionary conservation in the subunit composition of the Cdc34-SCF pathway. EMBO J. 17, 368-383.
50. Lyapina, S. A., Correll, C. C., Kiprcos, E. T. & Deshaies, R. J. 1998 Human CUL1 forms an evolutionarily conserved ubiquitin ligase complex (SCF) with SKP1 and an F-box protein. Proc. Natl Acad. Sci. USA 95. 7451-7456.
51. McKinney, J. D., Chang, F., Heintz, N. & Cross, F. R. 1993 Negative regulation of FAR1 at the Start of the yeast cell cycle. Genes Dev. 7, 833-843.
52. McKinney, J. D. & Cross, F. R. 1995 FAR1 and the G1 phase specificity of cell cycle arrest by mating factor in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 2509-2516.
53. Mann, M. & Wilm, M. 1994 Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal. Chem. 66, 4390-4399.
54. Mathias, N., Johnson, S. L., Winey, M., Adams, A. E., Goetsch, L., Pringle, J. R., Byers, B. & Goebl, M. G. 1996 Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identifies a conserved family of proteins. Mol. Cell. Biol. 16, 6634-6643.
55. CDC28 protein kinase activity from Saccharomyces cerevisiae. Science 259, 216-219.
56. Michel, J. J. & Xiong, Y. 1998 Human CUL-1, but not other cullin family members, selectively interacts with SKP1 to form a complex with SKP2 and cyclin A. Cell Growth Differ. 9, 435-449.
57. Nash, R., Tokiwa, G., Anand, S., Erickson, K. & Futcher, A. B. 1988 The WHI1 + gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog. EMBO J. 7, 4335-4346.
58. Nasmyth, K. 1996 At the heart of the budding yeast cell cycle. Trench Genet. 12, 405-412.
59. Newlon, C. S. 1997 Putting it all together: building a prereplicative complex. Cell 91, 717-720.
60. Ohta, T. Michel, J. J., Schottelius, A. J. & Xiong, Y. 1999 ROCl, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol. Cell 3, 535-541.
61. Ozcan, S. & Johnston, M. 1995. Three different regulatory mechanisms enable yeast hexose transporter (ILXT) genes to be induced by different levels of glucose. Mol. Cell. Biol. 15, 1564-1572.
62. Patton, E. E., Willems, A. R. & Tyers, M. 1998a Combinatorial control in ubiquitin-dependent protocolysis: don't Skp the F-box hypothesis. Trends Genet. 14, 236-243.
63. Patton, E. E., Willems, A. R., Sa, D., Kuras, L., Thomas, D., Craig, K. L. & Tyres, M. 1998b Cdc53 is a scaffold protein for multiple Cdc34/Skp1/F-box protein complexes that regulate cell division and methionine biosynthesis in yeast. Genes Dev. 12, 692-705.
64. Pawson, T. 1995 Protein modules and signalling networks. Nature 373, 573-580.
65. Peter, M. & Herskowitz, I. 1994 Direct inhibition of the yeast cyclin-dependent kinase Cdc28-Cln by Farl. Science 265, 1228-1231.
66. Peters, J. M. 1998 SCF and APC: the yin and yang of cell cycle regulated proteolysis. Curr. Opin. Cell Biol. 6, 759-768.
67. Rogers, S., Wells, R. & Rechsteiner, M. 1986 Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234, 364-368.
68. Scheffner, M., Nuber, U. & Huibregtse, J. M. 1995 Protein ubiquitination involving an E1 E2 E3 enzyme ubiquitin thioester cascade. Nature 373, 81-83.
69. Schneider, B. L., Steiner, B., Scufert, W. & Futcher, A. B. 1996a pMPY-ZAP: a reusable polymerase chain reaction-directed gene disruption cassette for Saccharomyces cerevisiae. Yeast 12, 129-134.
70. Schneider, B. L., Yang, Q.-H. & Further, A. B. 1996b Linkage of replication to Start by the Cdk inhibitor Sicl. Science 272, 560-562.
71. Schneider, B. L., Pattton, E. E., Lanker, S., Mendenhall, M., Wittenberg, C., Futcher, B. & Tyers, M. 1998 Yeast G1 cyclins are unstable in G1 phase. Nature 395, 86-89.
72. Schwab, M., Lutum, A. S. & Seufert, W. 1997 Yeast Hetl is a regulator of Clb2 cyclin protcolysis. Cell 90, 683-693.
73. SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79, 233-244.
74. Seol, J. H. (and 12 others) 1999 Cdc53/cullin and the essential Hrtl RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev. 13, 1614-1626.
75. Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. 1996 Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
76. Shevchenko, A., Chernushevich, I., Ens, W., Standing, K. G., Thomson, B., Wilm, M. & Mann, M. 1997 Rapid 'de novo' peptide sequencing by a combination of nanoelectrospray, isotopic labeling and a quadrupole/time-of-flight mass spectrometer. Rapid Comm. Mass Spectrom. 11, 1015-1024.
77. Sikorski, R. S. & Hieter, P. 1989 A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
78. Skowyra, D., Craig, K. I., Tyers, M., Elledge, S. J. & Harper, J. W. 1997 F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91, 209-219.
79. Grrl and Rbxl. Science 284, 662-665.
80. Stemmann, O. & Lechner, J. 1996 The Saccharomyces cerevisiae kinetochore contains a cyclin-CDK complexing homologue, as identified by in vitro reconstitution. EMBO J. 15, 3611-3620.
81. Tan, P., Fuchs, S. Y., Chen, A., Wu, K., Gomez, C., Ronai, Z. & Pan, Z. Q. 1999 Recruitment of a ROCl-CUL1 ubiquitin ligase by Skp1 and HOS to catalyse the ubiquitination of I kappa B alpha. Mol. Cell 3, 527-533.
82. Thomas, D. & Surdin-Kerjan, Y. 1997 Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Biol. Rev. 61, 503-532.
83. Thomas, D., Kuras, L., Barbey, R., Cherest, H., Blaiseau, P. L. & Surdin, K. Y. 1995 Met30p, a yeast transcriptional inhibitor that responds to S-adenosylmethionine, is an essential protein with WD10 repeats, Mol. Cell. Biol. 15, 6526-6534.
84. SIC1 imposes the requirement for CLN G1 cyclin function at Start. Proc. Natl Acad. Sci. USA 93, 7772-7776.
85. Tyers, M., Tokiwa, G., Nash, R. & Futcher, B. 1992 The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J. 11, 1773-1784.
86. Tyers, M., Tokiwa, G. & Futcher, B. 1993 Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 12. 1955-1968.
87. Verma, R., Annan, R. S., Huddleston, M. J., Carr, S. A., Reynard, G. & Deshaies, R. J. 1997 Phosphorylation of Siclp by G1 Cdk required for its degradation and entry into S phase, Science 278, 455-460.
88. Visintin, R., Prinz, S. & Amon, A. 1997 Cdc20 and Cdh1, a family of substrate-specific activators of APC-dependent proteolysis. Science 278, 460-463.
89. Visintin, R., Craig, K., Hwang, E. S., Prinz, S., Tyers, M. & Amon, A. 1998 The phosphatase Cdcl4 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2, 709-718.
90. Willems, A. R., Lanker, S., Patton, E. E., Craig, K. L., Nason, T. E., Mathias, N., Kobayashi, R., Wittenberg, C. & Tyers, M. 1996 Cdc53 targets phosphorylated G1 cyclins for degradation by the ubiquitin proteolytic pathway. Cell 86, 453-463.
91. Wilm, M. & Mann, M. 1996 Analytical properties of the nano-electrospray ion source. Anal. Chem. 66, 1-8.
92. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T. & Mann, M. 1996 Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469.
93. Wray, W., Boulikas, T., Wray, V. P. & Hancock, R. 1981 Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118, 197-203.
94. CDC28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol. 15, 731-741.
95. Yaron, A., Gonen, H., Alkalay, I., Hatzubai, A., Jung, S., Beyth, S., Mercurio, F., Manning, A. M., Ciechanover, A. & Ben-Neriah, Y. 1997 Inhibition of NF-κB cellular function via specific targeting of the 1κB-ubiquitin ligase. EMBO J. 16, 6486-6494.
96. Yaron, A., Hatzubai A., Davis, M., Lavon, I., Amit, S., Manning, A. M., Andersen, J. S., Mann, M., Mercurio, F. & Ben-Neriah, Y. 1998 Identification of the receptor component of the 1κBα-ubiquitin ligase. Nature 396, 590-594.
97. Yochem, J. & Byers, B. 1987 Structural comparison of the yeast cell division cycle gene CDC4 and a related pseudogene. J. Mol. Biol. 195, 233-245.
98. Yu, Z. K., Gervais, J. L. & Zhang, H. 1998 Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21 (CIP1/WAF1) and cyclin D proteins. Proc. Natl Acad. Sci. USA 95, 11324-11329.
99. Zachariae, W., Shevchenko, A., Andrews, P., Galova, M., Stark, M., Mann, M. & Nasmyth, K. 1998 Mass spectrometric analysis of the anaphase promoting complex from budding yeast: identification of a subunit related to cullins. Science 279, 1216-1219.
100. Skp2 are essential elements of the cyclin A-CDK2 S phase kinase. Cell 82, 915-925.