The Ime2 protein kinase enhances the disassociation of the Sum1 repressor from middle meiotic promoters

Molecular and Cellular Biology

Volumn 29, Issue 16, 2009, Pages 4352-4362

  Ahmed, Noreen T ^a   Bungard, David ^b   Shin, Marcus E ^a   Moore, Michael ^a,c   Winter, Edward ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b WISTAR INSTITUTE   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; IME2 PROTEIN; PROTEIN KINASE; SILENT INFORMATION REGULATOR PROTEIN 2; SMK1 PROTEIN; SUM1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NDT80; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DISSOCIATION; GENE EXPRESSION; GENE INTERACTION; GENETIC CODE; MEIOSIS; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; REPRESSOR GENE; SACCHAROMYCES CEREVISIAE; SPOROGENESIS;

DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEIOSIS; MITOGEN-ACTIVATED PROTEIN KINASES; NUCLEAR PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIRTUINS; TRANSCRIPTION FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 68949131048     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00305-09     Document Type: Article

References (44)

1. Allers, T., and M. Lichten. 2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47-57.
2. + levels in Saccharomyces cerevisiae. Mol. Cell. Biol. 23:7044-7054.
3. Byers, B. 1981. Cytology of the yeast life cycle, p. 59-96. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular and cellular biology of the yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Chen, X. L., A. Reindle, and E. S. Johnson. 2005. Misregulation of 2μm circle copy number in a SUMO pathway mutant. Mol. Cell. Biol. 25:4311-4320.
5. Chu, S., J. DeRisi, M. Eisen, J. Mulholland, D. Botstein, P. O. Brown, and I. Herskowitz. 1998. The transcriptional program of sporulation in budding yeast. Science 282:699-705. (Erratum, 282:1421.)
6. Chu, S., and I. Herskowitz. 1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1:685-696.
7. Crampton, A., F. Chang, D. L. Pappas, Jr., R. L. Frisch, and M. Weinreich. 2008. An ARS element inhibits DNA replication through a SIR2-dependent mechanism. Mol. Cell 30:156-166.
8. Hepworth, S. R., H. Friesen, and J. Segall. 1998. NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:5750-5761.
9. Hochwagen, A., and A. Amon. 2006. Checking your breaks: surveillance mechanisms of meiotic recombination. Curr. Biol. 16:R217-R228.
10. Holt, L. J., J. E. Hutti, L. C. Cantley, and D. O. Morgan. 2007. Evolution of Ime2 phosphorylation sites on Cdk1 substrates provides a mechanism to limit the effects of the phosphatase Cdc14 in meiosis. Mol. Cell 25:689-702.
11. Honigberg, S. M. 2004. Ime2p and Cdc28p: co-pilots driving meiotic development. J. Cell. Biochem. 92:1025-1033.
12. Irlbacher, H., J. Franke, T. Manke, M. Vingron, and A. E. Ehrenhofer-Murray. 2005. Control of replication initiation and heterochromatin formation in Saccharomyces cerevisiae by a regulator of meiotic gene expression. Genes Dev. 19:1811-1822.
13. Kassir, Y., N. Adir, E. Boger-Nadjar, N. G. Raviv, I. Rubin-Bejerano, S. Sagee, and G. Shenhar. 2003. Transcriptional regulation of meiosis in budding yeast. Int. Rev. Cytol. 224:111-171.
14. Krisak, L., R. Strich, R. S. Winters, J. P. Hall, M. J. Mallory, D. Kreitzer, R. S. Tuan, and E. Winter. 1994. Smk1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 8:2151-2161.
15. Lindgren, A., D. Bungard, M. Pierce, J. Xie, A. Vershon, and E. Winter. 2000. The pachytene checkpoint in Saccharomyces cerevisiae requires the Sum1 transcriptional repressor. EMBO J. 19:6489-6497.
16. Liti, G., D. M. Carter, A. M. Moses, J. Warringer, L. Parts, S. A. James, R. P. Davey, I. N. Roberts, A. Burt, V. Koufopanou, I. J. Tsai, C. M. Bergman, D. Bensasson, M. J. O'Kelly, A. van Oudenaarden, D. B. Barton, E. Bailes, A. N. Nguyen, M. Jones, M. A. Quail, I. Goodhead, S. Sims, F. Smith, A. Blomberg, R. Durbin, and E. J. Louis. 2009. Population genomics of domestic and wild yeasts. Nature 458:337-341.
17. Lo, H. C., L. Wan, A. Rosebrock, B. Futcher, and N. M. Hollingsworth. 2008. Cdc7-Dbf4 regulates NDT80 transcription as well as reductional segregation during budding yeast meiosis. Mol. Biol. Cell 19:4956-4967.
18. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
19. Mallory, M. J., K. F. Cooper, and R. Strich. 2007. Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/C. Mol. Cell 27: 951-961.
20. McCord, R., M. Pierce, J. Xie, S. Wonkatal, C. Mickel, and A. K. Vershon. 2003. Rfm1, a novel tethering factor required to recruit the Hst1 histone deacetylase for repression of middle sporulation genes. Mol. Cell. Biol. 23:2009-2016.
21. McDonald, C. M., K. F. Cooper, and E. Winter. 2005. The Ama1-directed APC/C ubiquitin ligase regulates the Smk1 MAPK during meiosis in yeast. Genetics 171:901-911.
22. Moore, M., M. E. Shin, A. Bruning, K. Schindler, A. Vershon, and E. Winter. 2007. Arg-Pro-X-Ser/Thr is a consensus phosphoacceptor sequence for the meiosis-specific Ime2 protein kinase in Saccharomyces cerevisiae. Biochemistry 46:271-278.
23. Ozsarac, N., M. J. Straffon, H. E. Dalton, and I. W. Dawes. 1997. Regulation of gene expression during meiosis in Saccharomyces cerevisiae: SPR3 is controlled by both ABFI and a new sporulation control element. Mol. Cell. Biol. 17:1152-1159.
24. Padmore, R., L. Cao, and N. Kleckner. 1991. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66:1239-1256.
25. Pak, J., and J. Segall. 2002. Regulation of the premiddle and middle phases of expression of the NDT80 gene during sporulation of Saccharomyces cerevisiae. Mol. Cell. Biol. 22:6417-6429.
26. Pak, J., and J. Segall. 2002. Role of Ndt80, Sum1, and Swe1 as targets of the meiotic recombination checkpoint that control exit from pachytene and spore formation in Saccharomyces cerevisiae. Mol. Cell. Biol. 22:6430-6440.
27. +-dependent Sir2p histone deacetylase is a negative regulator of chromosomal DNA replication. Genes Dev. 18:769-781.
28. Pierce, M., K. R. Benjamin, S. P. Montano, M. M. Georgiadis, E. Winter, and A. K. Vershon. 2003. Sum1 and Ndt80 proteins compete for binding to middle sporulation element sequences that control meiotic gene expression. Mol. Cell. Biol. 23:4814-4825.
29. Pierce, M., M. Wagner, J. Xie, V. Gailus-Durner, J. Six, A. K. Vershon, and E. Winter. 1998. Transcriptional regulation of the SMK1 mitogen-activated protein kinase gene during meiotic development in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:5970-5980.
30. Primig, M., R. Williams, E. Winzeler, G. Tevzadze, A. Conway, S. Hwang, R. Davis, and R. Esposito. 2000. The core meiotic transcriptome in budding yeasts. Nat. Genet. 26:415-423.
31. Roeder, G. S., and J. M. Bailis. 2000. The pachytene checkpoint. Trends Genet. 16:395-403.
32. Schaber, M., A. Lindgren, K. Schindler, D. Bungard, P. Kaldis, and E. Winter. 2002. CAK1 promotes meiosis and spore formation in Saccharomyces cerevisiae in a CDC28-independent fashion. Mol. Cell. Biol. 22:57-68.
33. Simchen, G. 2009. Commitment to meiosis: what determines the mode of division in budding yeast? Bioessays 31:169-177.
34. Sopko, R., S. Raithatha, and D. Stuart. 2002. Phosphorylation and maximal activity of Saccharomyces cerevisiae meiosis-specific transcription factor Ndt80 is dependent on Ime2. Mol. Cell. Biol. 22:7024-7040.
35. Sopko, R., and D. T. Stuart. 2004. Purification and characterization of the DNA binding domain of Saccharomyces cerevisiae meiosis-specific transcription factor Ndt80. Protein Expr. Purif. 33:134-144.
36. Sourirajan, A., and M. Lichten. 2008. Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev. 22:2627-2632.
37. Strahl-Bolsinger, S., A. Hecht, K. Luo, and M. Grunstein. 1997. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev. 11:83-93.
38. Tung, K. S., E. J. Hong, and G. S. Roeder. 2000. The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80. Proc. Natl. Acad. Sci. USA 97:12187-12192.
39. Vershon, A. K., and M. Pierce. 2000. Transcriptional regulation of meiosis in yeast. Curr. Opin. Cell Biol. 12:334-339.
40. Wang, W., J. M. Cherry, Y. Nochomovitz, E. Jolly, D. Botstein, and H. Li. 2005. Inference of combinatorial regulation in yeast transcriptional networks: a case study of sporulation. Proc. Natl. Acad. Sci. USA 102:1998-2003.
41. Weber, J. M., H. Irlbacher, and A. E. Ehrenhofer-Murray. 2008. Control of replication initiation by the Sum1/Rfm1/Hst1 histone deacetylase. BMC Mol. Biol. 9:100.
42. Xie, J., M. Pierce, V. Gailus-Durner, M. Wagner, E. Winter, and A. K. Vershon. 1999. Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J. 18:6448-6454.
43. Xu, L., M. Ajimura, R. Padmore, C. Klein, and N. Kleckner. 1995. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6572-6581.
44. Zill, O. A., and J. Rine. 2008. Interspecies variation reveals a conserved repressor of alpha-specific genes in Saccharomyces yeasts. Genes Dev. 22: 1704-1716.