Meiosis-Specific Destruction of the Ume6p Repressor by the Cdc20-Directed APC/C

Molecular Cell

Volumn 27, Issue 6, 2007, Pages 951-961

  Mallory, Michael J ^a   Cooper, Katrina F ^b   Strich, Randy ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

CELLCYCLE; PROTEINS

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL PROTEIN; IME1P PROTEIN; REGULATOR PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UME6P PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CONTROLLED STUDY; DESTRUCTION; ENZYME PHOSPHORYLATION; GENE CONTROL; GENE INDUCTION; GENE MUTATION; MEIOSIS; MITOSIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN STABILITY; REPRESSOR GENE; TRANSCRIPTION REGULATION; UBIQUITINATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; CARBON; CELL CYCLE PROTEINS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; DOWN-REGULATION; GENES, FUNGAL; MEIOSIS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAS PROTEINS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 34748920975     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.08.019     Document Type: Article

References (57)

1. Arcangioli B., and Lescure B. Identification of proteins involved in the regulation of yeast iso-1-cytochrome C expression by oxygen. EMBO J. 4 (1985) 2627-2633
2. Boeke J.D., LaCroute F., and Fink G.R. A positive selection for mutants lacking orotidine-5″-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197 (1984) 345-346
3. Bowdish K.S., and Mitchell A.P. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol. Cell. Biol. 13 (1993) 2172-2181
4. Bowdish K.S., Yuan H.E., and Mitchell A.P. Positive control of yeast meiotic genes by the negative regulator UME6. Mol. Cell. Biol. 15 (1995) 2955-2961
5. Broek D., Toda T., Michaeli T., Levin L., Birchmeier C., Zoller M., Powere S., and Wigler M. The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell 48 (1987) 789-799
6. Burgess S.M., Ajimura M., and Kleckner N. GCN5-dependent histone H3 acetylation and RPD3-dependent histone H4 deacetylation have distinct, opposing effects on IME2 transcription, during meiosis and during vegetative growth, in budding yeast. Proc. Natl. Acad. Sci. USA 96 (1999) 6835-6840
7. Burton J.L., and Solomon M.J. D box and KEN box motifs in budding yeast Hsl1p are required for APC-mediated degradation and direct binding to Cdc20p and Cdh1p. Genes Dev. 15 (2001) 2381-2395
8. Burton J.L., Tsakraklides V., and Solomon M.J. Assembly of an APC-Cdh1-substrate complex is stimulated by engagement of a destruction box. Mol. Cell 18 (2005) 533-542
9. Chu S., DeRisi J., Eisen M., Mulholland J., Botstein D., Brown P.O., and Herskowitz I. The transcriptional program of sporulation in budding yeast. Science 282 (1998) 699-705
10. Coluccio A., Bogengruber E., Conrad M.N., Dresser M.E., Briza P., and Neiman A.M. Morphogenetic pathway of spore wall assembly in Saccharomyces cerevisiae. Eukaryot. Cell 3 (2004) 1464-1475
11. Cooper K.F., and Strich R. Saccharomyces cerevisiae C-type cyclin UME3/SRB11 is required for efficient induction and execution of meiotic development. Eukaryot. Cell 1 (2002) 67-76
12. Cooper K.F., Mallory M.J., Smith J.S., and Strich R. Stress and developmental regulation of the yeast C-type cyclin UME3 (SRB11/SSN8). EMBO J. 16 (1997) 4665-4675
13. Cooper K.F., Egeland D.E., Mallory M.J., Jarnik M., and Strich R. Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast. Proc. Natl. Acad. Sci. USA 97 (2000) 14548-14553
14. Dawson I.A., Roth S., and Artavanis-Tsakonas S. The Drosophila cell cycle gene fizzy is required for normal degradation of cyclins A and B during mitosis and has homology to the CDC20 gene of Saccharomyces cerevisiae. J. Cell Biol. 129 (1995) 725-737
15. Foiani M., Nadjar-Boger E., Capone R., Sagee S., Hashimshoni T., and Kassir Y. A meiosis-specific protein kinase, Ime2, is required for the correct timing of DNA replication and for spore formation in yeast meiosis. Mol. Gen. Genet. 253 (1996) 278-288
16. Glotzer M., Murray A.W., and Kirschner M.W. Cyclin is degraded by the ubiquitin pathway. Nature 349 (1991) 132-138
17. Goldmark J.P., Fazzio T.G., Estep P.W., Church G.M., and Tsukiyama T. The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103 (2000) 423-433
18. Guacci V., Hogan E., and Koshland D. Centromere position in budding yeast: evidence for anaphase A. Mol. Biol. Cell 8 (1997) 957-972
19. Harper J.W., Burton J.L., and Solomon M.J. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16 (2002) 2179-2206
20. Hartwell L.H., Culotti J., Pringle J.R., and Reid B.J. Genetic control of the cell cycle in yeast. Science 183 (1974) 46-51
21. Kadosh D., and Struhl K. Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol. Cell. Biol. 18 (1998) 5121-5127
22. Kassir Y., Granot D., and Simchen G. IME1, a positive regulator of meiosis in S. cerevisiae. Cell 52 (1988) 853-862
23. Kunkel T.A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82 (1985) 488-492
24. Kupiec M., Byers B., Esposito R.E., and Mitchell A.P. Meiosis and sporulation in Saccharomyces cerevisiae. In: Pringle J.R., Broach J.R., and Jones E.W. (Eds). The Molecular and Cellular Biology of the Yeast Saccharomyces (1997), Cold Spring Harbor Press, Cold Spring Harbor, NY 889-1036
25. Longtine M.S., McKenzie A.R., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., and Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 (1998) 953-961
26. Malathi K., Xiao Y., and Mitchell A.P. Interaction of yeast repressor-activator protein Ume6p with glycogen synthase kinase 3 homolog Rim11p. Mol. Cell. Biol. 17 (1997) 7230-7236
27. Mallory M.J., and Strich R. Ume1p represses meiotic gene transcription in S. cerevisiae through interaction with the histone deacetylase Rpd3p. J. Biol. Chem. 278 (2003) 44727-44734
28. Maniatis T., Fritsch E.F., and Sambrook J. Molecular Cloning: A Laboratory Manual (1982), Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
29. Mitchell A.P., Driscoll S.E., and Smith H.E. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol. Cell. Biol. 10 (1990) 2104-2110
30. Murai K., Naruse Y., Shaul Y., Agata Y., and Mori N. Direct interaction of NRSF with TBP: chromatin reorganization and core promoter repression for neuron-specific gene transcription. Nucleic Acids Res. 32 (2004) 3180-3189
31. Park H.D., Luche R.M., and Cooper T.G. The yeast UME6 gene product is required for transcriptional repression mediated by the CAR1 URS1 repressor binding site. Nucleic Acids Res. 20 (1992) 1909-1915
32. Passmore L.A., McCormack E.A., Au S.W., Paul A., Willison K.R., Harper J.W., and Barford D. Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J. 22 (2003) 786-796
33. Pnueli L., Edry I., Cohen M., and Kassir Y. Glucose and nitrogen regulate the switch from histone deacetylation to acetylation for expression of early meiosis-specific genes in budding yeast. Mol. Cell. Biol. 24 (2004) 5197-5208
34. Portela P., Van Dijck P., Thevelein J.M., and Moreno S. Activation state of protein kinase A as measured in permeabilised Saccharomyces cerevisiae cells correlates with PKA-controlled phenotypes in vivo. FEMS Yeast Res. 3 (2003) 119-126
35. Primig M., Williams R.M., Winzeler E.A., Tevzadze G.G., Conway A.R., Hwang S.Y., Davis R.W., and Esposito R.E. The core meiotic transcriptome in budding yeasts. Nat. Genet. 26 (2000) 415-423
36. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. In: Abelson J.N., and Simon M.I. (Eds). Methods in Enzymology (1991), Academic Press Inc., San Diego, CA 281-301
37. Rubin-Bejerano I., Mandel S., Robzyk K., and Kassir Y. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol. Cell. Biol. 16 (1996) 2518-2526
38. Rubin-Bejerano I., Sagee S., Friedman O., Pnueli L., and Kassir Y. The in vivo activity of Ime1, the key transcriptional activator of meiosis-specific genes in Saccharomyces cerevisiae, is inhibited by the cyclic AMP/protein kinase A signal pathway through the glycogen synthase kinase 3-beta homolog Rim11. Mol. Cell. Biol. 24 (2004) 6967-6979
39. Salah S.M., and Nasmyth K. Destruction of the securin Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 109 (2000) 27-34
40. Schwab M., Schulze Lutum A., and Seufert W. Yeast Hct1 is a regulator of Clb2 cyclin protolysis. Cell 90 (1997) 683-693
41. Schwab M., Neutzner M., Mocker D., and Seufert W. Yeast Hct1 recognizes the mitotic cyclin Clb2 and other substrates of the ubiquitin ligase APC. EMBO J. 20 (2001) 5165-5175
42. Searle J.S., Schollaert K.L., Wilkins B.J., and Sanchez Y. The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat. Cell Biol. 6 (2004) 138-145
43. Sia R.A., and Mitchell A.P. Stimulation of later functions of the yeast meiotic protein kinase Ime2p by the IDS2 gene product. Mol. Cell. Biol. 15 (1995) 5279-5287
44. Sigrist S.J., and Lehner C.F. Drosophila fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles. Cell 90 (1997) 671-681
45. Simchen G. Are mitotic functions required in meiosis?. Genetics 76 (1974) 745-753
46. Spellman P.T., Sherlock G., Zhang M.Q., Iyer V.R., Anders K., Eisen M.B., Brown P.O., Botstein D., and Futcher B. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9 (1998) 3273-3297
47. Steber C.M., and Esposito R.E. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc. Natl. Acad. Sci. USA 92 (1995) 12490-12494
48. Strich R., Surosky R.T., Steber C., Dubois E., Messenguy F., and Esposito R.E. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8 (1994) 796-810
49. Strich R., Slater M.R., and Esposito R.E. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc. Natl. Acad. Sci. USA 86 (1989) 10018-10022
50. Stroschein S.L., Bonni S., Wrana J.L., and Luo K. Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev. 15 (2001) 2822-2836
51. Surosky R.T., and Esposito R.E. Early meiotic transcripts are highly unstable in Saccharomyces cerevisiae. Mol. Cell. Biol. 12 (1992) 3948-3958
52. Toda T., Uno I., Ishikawa T., Powers S., Kataoka T., Broek D., Cameron S., Broach J., Matsumoto K., and Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40 (1985) 27-36
53. van Roessel P., Elliott D.A., Robinson I.M., Prokop A., and Brand A.H. Independent regulation of synaptic size and activity by the anaphase-promoting complex. Cell 119 (2004) 707-718
54. Visintin R., Prinz S., and Amon A. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278 (1997) 460-463
55. Washburn B.K., and Esposito R.E. Identification of the Sin3-binding site in Ume6 defines a two-step process for conversion of Ume6 from a transcriptional repressor to an activator in yeast. Mol. Cell. Biol. 21 (2001) 2057-2069
56. Wotton D., Knoepfler P.S., Laherty C.D., Eisenman R.N., and Massague J. The Smad transcriptional corepressor TGIF recruits mSin3. Cell Growth Differ. 12 (2001) 457-463
57. Xiao Y., and Mitchell A.P. Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol. Cell. Biol. 20 (2000) 5447-5453