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-β homolog Rim11

Molecular and Cellular Biology

Volumn 24, Issue 16, 2004, Pages 6967-6979

  Rubin Bejerano, Ifat ^a,b   Sagee, Shira ^a   Friedman, Osnat ^a   Pnueli, Lilach ^a   Kassir, Yona ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; CARBON; CYCLIC AMP DEPENDENT PROTEIN KINASE; GENE PRODUCT; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN IME1; PROTEIN RIM11; SERINE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; DELETION MUTANT; DIPLOIDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EUKARYOTE; GENETIC TRANSCRIPTION; MEIOSIS; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SPOROGENESIS; VEGETATIVE GROWTH;

ACETATES; CULTURE MEDIA; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; MEIOSIS; NITROGEN; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SECOND MESSENGER SYSTEMS; SERINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES; TYROSINE;

EUKARYOTA; MAMMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 3543014938     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.16.6967-6979.2004     Document Type: Article

References (58)

1. Anderson, S. F., C. M. Steber, R. E. Esposito, and J. E. Coleman. 1995. 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. 4:1832-1843.
2. Ansari, K., S. Martin, M. Farkasovsky, I. M. Ehbrecht, and H. Kuntzel. 1999. Phospholipase C binds to the receptor-like GPR1 protein and controls pseudohyphal differentiation in Saccharomyces cerevisiae. J. Biol. Chem. 274:30052-30058.
3. Bowdish, K. S., H. E. Yuan, and A. P. Mitchell. 1994. Analysis of RIMI1, a yeast protein kinase that phosphorylates the meiotic activator IME1. Mol. Cell. Biol. 14:7909-7919.
4. Bowdish, K. S., H. E. Yuan, and A. P. Mitchell. 1995. Positive control of yeast meiotic genes by the negative regulator UME6. Mol. Cell. Biol. 15:2955-2961.
5. Broek, D., T. Toda, T. Michaeli, L. Levin, C. Birchmeier, M. Zoller, S. Powers, and M. Wigler. 1987. The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell 48:789-799.
6. Chien, C. T., P. L. Bartel, R. Sternglanz, and S. Fields. 1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88:9578-9582.
7. Cohen, P., and S. Frame. 2001. The renaissance of GSK3. Nat. Rev. Mol. Cell. Biol. 2:769-776.
8. Colomina, N., E. Gari, C. Gallego, E. Herrero, and M. Aldea. 1999. G1 cyclins block the Ime1 pathway to make mitosis and meiosis incompatible in budding yeast. EMBO J. 18:320-329.
9. Colomina, N., Y. Liu, M. Aldea, and E. Gari. 2003. TOR regulates the subcellular localization of Ime1, a transcriptional activator of meiotic development in budding yeast. Mol. Cell. Biol. 23:7415-7424.
10. Dajani, R., E. Fraser, S. M. Roe, N. Young, V. Good, T. C. Dale, and L. H. Pearl. 2001. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 105:721-732.
11. Donzeau, M., and W. Bandlow. 1999. The yeast trimeric guanine nucleotide-binding protein alpha subunit, Gpa2p, controls the meiosis-specific kinase Ime2p activity in response to nutrients. Mol. Cell. Biol. 19:6110-6119.
12. Foiani, M., G. Liberi, G. Lucchini, and P. Plevani. 1995. Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase alpha-primase B subunit. Mol. Cell. Biol. 15:883-891.
13. Foiani, M., F. Marini, D. Gamba, G. Lucchini, and P. Plevani. 1994. The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol. Cell. Biol. 14:923-933.
14. Frame, S., and P. Cohen. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359:1-16.
15. Frame, S., P. Cohen, and R. M. Biondi. 2001. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol. Cell 7:1321-1327.
16. Gietz, R. D., R. H. Schiestl, A. R. Willems, and R. A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355-360.
17. Goldmark, J. P., T. G. Fazzio, P. W. Estep, G. M. Church, and T. Tsukiyama. 2000. The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103:423-433.
18. Guldener, U., S. Heck, T. Fielder, J. Beinhauer, and J. H. Hegemann. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24:2519-2524.
19. Guttmann-Raviv, N., and Y. Kassir. 2002. Ime2, a meiosis-specific kinase in yeast, is required for destabilization of its transcriptional activator, Ime1. Mol. Cell. Biol. 22:2047-2056.
20. Harwood, A. J. 2001. Regulation of GSK-3: a cellular multiprocessor. Cell 105:821-824.
21. Kadosh, D., and K. Struhl. 1997. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365-371.
22. Kassir, Y., N. Adir, E. Boger-Nadja, N. Guttmann-Raviv, I. Rubin-Bejerano, S. Sagee, and G. Shenhar. 2003. Transcriptional regulation of meiosis in budding yeast. Int. J. Cytol. Surv. Cell Biol. 224:111-171.
23. Kassir, Y., D. Granot, and G. Simchen. 1988. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell 52:853-862.
24. Kassir, Y., and G. Simchen. 1991. Monitoring meiosis and sporulation in Saccharomyces cerevisiae. Methods Enzymol. 194:94-110.
25. Kim, L., A. Harwood, and A. R. Kimmel. 2002. Receptor-dependent and tyrosine phosphatase-mediated inhibition of GSK3 regulates cell fate choice. Dev. Cell 3:523-532.
26. Kim, L., and A. R. Kimmel. 2000. GSK3, a master switch regulating cell-fate specification and tumorigenesis. Curr. Opin. Genet. Dev. 10:508-514.
27. Kunkel, T. A., K. Bebenek, and J. McClary. 1991. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204:125-139.
28. Malathi, K., Y. Xiao, and A. P. Mitchell. 1999. Catalytic roles of yeast GSK3beta/shaggy homolog Rim11p in meiotic activation. Genetics 153:1145-1152.
29. Malathi, K., Y. Xiao, and A. P. Mitchell. 1997. Interaction of yeast repressor-activator protein Ume6p with glycogen synthase kinase 3 homolog Rim11p. Mol. Cell. Biol. 17:7230-7236.
30. Mandel, S., K. Robzyk, and Y. Kassir. 1994. IME1 gene encodes a transcription factor which is required to induce meiosis in Saccharomyces cerevisiae. Dev. Genet. 15:139-147.
31. Matsumoto, K., I. Uno, and T. Ishikawa. 1983. Initiation of meiosis in yeast mutants defective in adenylate cyclase and cyclic AMP-dependent protein kinase. Cell 32:417-423.
32. Matsuura, A., M. Treinin, H. Mitsuzawa, Y. Kassir, I. Uno, and G. Simchen. 1990. The adenylate cyclase/protein kinase cascade regulates entry into meiosis in Saccharomyces cerevisiae through the gene IME1. EMBO J. 9:3225-3232.
33. Miller, J. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
34. Mitchell, A. P., S. E. Driscoll, and H. E. Smith. 1990. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:2104-2110.
35. Pan, X., and J. Heitman. 1999. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:4874-4887.
36. Pnueli, L., I. Edry, M. Cohen, and Y. Kassir. 2004. Glucose and nitrogen regulate the switch from histone deacetylation to acetylation in early meiosis-specific genes of budding yeast. Mol. Cell. Biol. 24:5197-5208.
37. Puziss, J. W., T. A. Hardy, R. B. Johnson, P. J. Roach, and P. Hieter. 1994. MDS1, a dosage suppressor of an mck1 mutant, encodes a putative yeast homolog of glycogen synthase kinase 3. Mol. Cell. Biol. 14:831-539.
38. Robertson, L. S., and G. R. Fink. 1998. The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc. Natl. Acad. Sci. USA 95:13783-13787.
39. Rose, M., and D. Botstein. 1983. Construction and use of gene fusions to lacZ (beta-galactosidase) that are expressed in yeast. Methods Enzymol. 101:167-180.
40. Rubin-Bejerano, I., S. Mandel, K. Robzyk, and Y. Kassir. 1996. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional repressor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol. Cell. Biol. 16:2518-2526.
41. Sagee, S., A. Sherman, G. Shenhar, K. Robzyk, N. Ben-Doy, G. Simchen, and Y. Kassir. 1998. 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. 18:1985-1995.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
43. Shenhar, G., and Y. Kassir. 2001. A positive regulator of mitosis, Sok2, functions as a negative regulator of meiosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:1603-1612.
44. Sherman, A., M. Shefer, S. Sagee, and Y. Kassir. 1993. Posttranscriptional regulation of IME1 determines initiation of meiosis in Saccharomyces cerevisiae. Mol. Gen. Genet. 237:375-384.
45. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
46. Shilo, V., G. Simchen, and B. Shilo. 1978. Initiation of meiosis in cell cycle initiation mutants of Saccharomyces cerevisiae. Exp. Cell Res. 112:241-248.
47. Smith, H. E., S. E. Driscoll, R. A. Sia, H. E. Yuan, and A. P. Mitchell. 1993. Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics 133:775-784.
48. Steber, C. M., and R. E. Esposito. 1995. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc. Natl. Acad. Sci. USA 92:12490-12494.
49. Strich, R., R. T. Surosky, C. Steber, E. Dubois, F. Messenguy, and R. E. Esposito. 1994. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8:796-810.
50. Su, S. S., and A. P. Mitchell. 1993. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 133:67-77.
51. Toda, T., S. Cameron, P. Sass, M. Zoller, J. D. Scott, B. McMullen, M. Hurwitz, E. G. Krebs, and M. Wigler. 1987. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol. Cell. Biol. 7:1371-1377.
52. Vidan, S., and A. P. Mitchell. 1997. Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol. Cell. Biol. 17:2688-2697.
53. Wang, H., L. Reynolds-Hager, and D. J. Stillman. 1994. Genetic interactions between SIN3 mutations and the Saccharomyces cerevisiae transcriptional activators encoded by MCM1, STE12, and SWI1. Mol. Gen. Genet. 245:675-685.
54. Wang, Q. M., C. J. Fiol, A. A. DePaoli-Roach, and P. J. Roach. 1994. Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269:14566-14574.
55. Williams, R. M., M. Primig, B. K. Washburn, E. A. Winzeler, M. Bellis, C. Sarrauste de Menthiere, R. W. Davis, and R. E. Esposito. 2002. The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast. Proc. Natl. Acad. Sci. USA 99:13431-13436.
56. Xiao, Y., and A. P. Mitchell. 2000. Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol. Cell. Biol. 20:5447-5453.
57. Yoshida, M., H. Kawaguchi, Y. Sakata, K. Kominami, M. Hirano, H. Shima, R. Akada, and I. Yamashita. 1990. Initiation of meiosis and sporulation in Saccharomyces cerevisiae requires a novel protein kinase homologue. Mol. Gen. Genet. 221:176-186.
58. Zhan, X. L., Y. Hong, T. Zhu, A. P. Mitchell, R. J. Deschenes, and K. L. Guan. 2000. Essential functions of protein tyrosine phosphatases ptp2 and ptp3 and rim11 tyrosine phosphorylation in Saccharomyces cerevisiae meiosis and sporulation. Mol. Biol. Cell 11:663-676.