Transcriptional regulation of meiosis in yeast

Current Opinion in Cell Biology

Volumn 12, Issue 3, 2000, Pages 334-339

  Vershon, Andrew K ^a   Pierce, Michael ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; YEAST;

EID: 0034020067     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(00)00104-6     Document Type: Review

References (52)

1. Mitchell A.P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 58:1994;56-70.
2. Chu S., DeRisi J., Eisen M., Mulholland J., Botstein D., Brown P.O., Herskowitz I. The transcriptional program of sporulation in budding yeast. Science. 282:1998;699-705. This study uses genomic microarrays to monitor expression throughout the different stages of meiosis. Genes within a temporal class were examined for common regulatory elements in their promoters. This analysis has shown that the early genes can be further broken into several sub-groups that may be differentially regulated. The paper also establishes which genes are targets for activation by the Ndt80 protein. The database from this study has proved extremely useful in identifying potential genes that may be involved in a specific process of meiosis.
3. Kupiec M., Byers B., Esposito R., Mitchell A. Meiosis and Sporulation in Saccharomyces cerevisiae. Pringle J.R., Broach J.R., Jones E.N. The Molecular and Cellular Biology of the Yeast Saccharomyces. 1997;889-1036 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
4. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 52:1988;853-862.
5. Smith H.E., Su S.S., Neigeborn L., Driscoll S.E., Mitchell A.P. Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 10:1990;6103-6113.
6. Covitz P.A., Mitchell A.P. Repression by the yeast meiotic inhibitor RME1. Genes Dev. 7:1993;1598-1608.
7. Sagee S., Sherman A., Shenhar G., Robzyk K., Ben-Doy N., Simchen G., Kassir Y. Multiple and distinct activation and repression sequences mediate the regulated transcription of IME1, a transcriptional activator of meiosis- specific genes in Saccharomyces cerevisiae. Mol Cell Biol. 18:1998;1985-1995. Through a series of promoter deletions and analysis of isolated elements in heterologous promoters, the authors show that there are at least ten different regulatory elements in the 2.1 kb IME1 promoter. The authors determine which elements are repressors or activators and which are involved in cell-type control or the response to changes in glucose, acetate and nitrogen. The authors show that Msn2 or Msn4 proteins, targets of the RAS-cAPK signal pathway, bind to sites in the IME1 promoter in response to low levels of glucose.
8. Covitz P.A., Herskowitz I., Mitchell A.P. The yeast RME1 gene encodes a putative zinc finger protein that is directly repressed by a1-alpha 2. Genes Dev. 5:1991;1982-1989.
9. Covitz P.A., Song W., Mitchell A.P. Requirement for RGR1 and SIN4 in RME1-dependent repression in Saccharomyces cerevisiae. Genetics. 138:1994;577-586.
10. Strathern J., Hicks J., Herskowitz I. Control of cell type in yeast by the mating type locus. The alpha 1-alpha 2 hypothesis. J Mol Biol. 147:1981;357-372.
11. Shah J.C., Clancy M.J. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 12:1992;1078-1086.
12. Matsuura A., Treinin M., Mitsuzawa H., Kassir Y., Uno I., Simchen G. The adenylate cyclase/protein kinase cascade regulates entry into meiosis in Saccharomyces cerevisiae through the gene IME1. EMBO J. 9:1990;3225-3232.
13. Neigeborn L., Mitchell A.P. The yeast MCK1 gene encodes a protein kinase homolog that activates early meiotic gene expression. Genes Dev. 5:1991;533-548.
14. Su S.S., Mitchell A.P. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics. 133:1993;67-77.
15. Su S.S., Mitchell A.P. Molecular characterization of the yeast meiotic regulatory gene RIM1. Nucleic Acids Res. 21:1993;3789-3797.
16. Li W., Mitchell A.P. Proteolytic activation of Rim1p, a positive regulator of yeast sporulation and invasive growth. Genetics. 145:1997;63-73.
17. Sherman A., Shefer M., Sagee S., Kassir Y. Post-transcriptional regulation of IME1 determines initiation of meiosis in Saccharomyces cerevisiae. Mol Gen Genet. 237:1993;375-384.
18. Bowdish K.S., Yuan H.E., Mitchell A.P. Analysis of RIM11, a yeast protein kinase that phosphorylates the meiotic activator IME1. Mol Cell Biol. 14:1994;7909-7919.
19. Vidan S., Mitchell A.P. Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol Cell Biol. 17:1997;2688-2697.
20. Malathi K., Xiao Y., Mitchell A.P. Interaction of yeast repressor-activator protein Ume6p with glycogen synthase kinase 3 homolog Rim11p. Mol Cell Biol. 17:1997;7230-7236.
21. Rubin-Bejerano I., Mandel S., Robzyk K., 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.
22. Thevelein J.M., de Winde J.H. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol. 33:1999;904-918.
23. Reinders A., Burckert N., Boller T., Wiemken A., De Virgilio C. Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev. 12:1998;2943-2955.
24. Buckingham L.E., Wang H.T., Elder R.T., McCarroll R.M., Slater M.R., Esposito R.E. Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 87:1990;9406-9410.
25. Strich R., Surosky R.T., Steber C., Dubois E., Messenguy F., Esposito R.E. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8:1994;796-810.
26. Park H.D., Luche R.M., 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.
27. Anderson S.F., Steber C.M., Esposito R.E., Coleman J.E. UME6, a negative regulator of meiosis in Saccharomyces cerevisiae, contains a C-terminal Zn2Cys6 binuclear cluster that binds the URS1 DNA sequence in a zinc-dependent manner. Protein Sci. 4:1995;1832-1843.
28. Kadosh D., 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. This paper examines how remodeling chromatin structure can be used as a mechanism to repress transcription of early sporulation-specific genes. The DNA-binding protein Ume6 recruits the co-repressor Sin3 and the histone deacetylase Rpd3 to create localized domains of repressed chromatin by deacetylation of the histones H3 and H4.
29. Kadosh D., Struhl K. Histone deacetylase activity of Rpd3 is important for transcriptional repression in vivo. Genes Dev. 12:1998;797-805.
30. Kadosh D., Struhl K. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell. 89:1997;365-371.
31. Rundlett S.E., Carmen A.A., Suka N., Turner B.M., Grunstein M. Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature. 392:1998;831-835.
32. Strich R., Slater M.R., 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.
33. Bowdish K.S., Yuan H.E., Mitchell A.P. Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol. 15:1995;2955-2961.
34. Steber C.M., 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.
35. Malathi K., Xiao Y., Mitchell A.P. Catalytic roles of yeast GSK3beta/Shaggy homolog rim11p in meiotic activation. Genetics. 153:1999;1145-1152. This paper investigates the catalytic role of the Rim11 kinase in promoting the interaction between Ime1 and Ume6. Through kinase assays, immunoprecipitations and site-directed point mutations in Ime1, the authors show that Rim11 phosphorylates tyrosine residues in the carboxy-terminal tail of Ime1. The authors also show evidence that Ime1 and Rim11 have additional roles in promoting meiosis through mechanisms that are independent of each other and Ume6.
36. Gailus-Durner V., Chintamaneni C., Wilson R., Brill S.J., Vershon A.K. Analysis of a meiosis-specific URS1 site: sequence requirements and involvement of replication protein A. Mol Cell Biol. 17:1997;3536-3546.
37. Bowdish K.S., Mitchell A.P. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol Cell Biol. 13:1993;2172-2181.
38. Nojima H., Leem S.H., Araki H., Sakai A., Nakashima N., Kanaoka Y., Ono Y. Hac1: a novel yeast bZIP protein binding to the CRE motif is a multicopy suppressor for cdc10 mutant of Schizosaccharomyces pombe. Nucleic Acids Res. 22:1994;5279-5288.
39. Szent-Gyorgyi C. A bipartite operator interacts with a heat shock element to mediate early meiotic induction of Saccharomyces cerevisiae HSP82. Mol Cell Biol. 15:1995;6754-6769.
40. Gailus-Durner V., Xie J., Chintamaneni C., Vershon A.K. Participation of the yeast activator Abf1 in meiosis-specific expression of the HOP1 gene. Mol Cell Biol. 16:1996;2777-2786.
41. Ozsarac N., Straffon M.J., Dalton H.E., Dawes I.W. Regulation of gene expression during meiosis in Saccharomyces cerevisiae: SPR3 is controlled by both ABFI and a new sporulation control element. Mol Cell Biol. 17:1997;1152-1159.
42. Chu S., Herskowitz I. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell. 1:1998;685-696. Ndt80 is required for activation of middle genes and binds to consensus MSEs found in the promoters of several middle genes. Ndt80 is also necessary for expression of several of the CLB genes in a middle-sporulation-specific manner. This paper shows that some of the CLB genes, specifically CLB1, play a role in meiosis and that the target of the meiotic checkpoint is Ndt80.
43. Hepworth S.R., Friesen H., Segall J. NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol Cell Biol. 18:1998;5750-5761. Accumulation of double-strand breaks results in the arrest of the meiotic cell cycle and decreased levels of NDT80 expression. A checkpoint mutant that bypasses arrest allows for full expression of NDT80 and middle sporulation genes, suggesting that NDT80 is under the control of the meiotic recombination checkpoint. This paper also shows that Sin3 and Rpd3 are required for the expression of middle and late genes, suggesting that these proteins may be required to re-establish repression of the early genes at the later stages of sporulation.
44. Xu L., Ajimura M., Padmore R., Klein C., Kleckner N. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol. 15:1995;6572-6581.
45. Xie J., Pierce M., Gailus-Durner V., Wagner M., Winter E., Vershon A.K. Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J. 18:1999;6448-6454. This paper provides examples of how MSEs from different mid-sporulation specific genes vary in their ability to either repress or activate transcription. In the case of the SMK1 MSE the repression activity is shown to be dependent on Sum1 and Hst1, proteins previously associated with transcriptional silencing.
46. Pierce M., Wagner M., Xie J., Gailus-Durner V., Six J., Vershon A.K., Winter E. Transcriptional regulation of the SMK1 mitogen-activated protein kinase gene during meiotic development in Saccharomyces cerevisiae. Mol Cell Biol. 18:1998;5970-5980.
47. Friesen H., Hepworth S.R., Segall J. An Ssn6-Tup1-dependent negative regulatory element controls sporulation-specific expression of DIT1 and DIT2 in Saccharomyces cerevisiae. Mol Cell Biol. 17:1997;123-134.
48. Krisak L., Strich R., Winters R.S., Hall J.P., Mallory M.J., Kreitzer D., Tuan R.S., Winter E. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 8:1994;2151-2161.
49. Friesen H., Lunz R., Doyle S., Segall J. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation. Genes Dev. 8:1994;2162-2175.
50. Ufano S., San-Segundo P., del Rey F., Vazquez de Aldana C.R. SWM1, a developmentally regulated gene, is required for spore wall assembly in Saccharomyces cerevisiae. Mol Cell Biol. 19:1999;2118-2129. This paper shows that SWM1, a mid-sporulation specific gene, is required for full expression of mid-late and late genes involved in spore wall assembly. A swm1 mutant has no effect on expression of early or mid-sporulation genes and does not affect the meiotic divisions. Genetic analysis suggests that the function of Swm1 is independent from the Sps1 and Smk1 proteins in the sporulation-specific MAP-kinase cascade.
51. Mai B., Breeden L. CLN1 and its repression by Xbp1 are important for efficient sporulation in budding yeast. Mol Cell Biol. 20:2000;478-487.
52. Mai B., Breeden L. Xbp1, a stress-induced transcriptional repressor of the Saccharomyces cerevisiae Swi4/Mbp1 family. Mol Cell Biol. 17:1997;6491-6501.