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. 1997 May;17(5):2688–2697. doi: 10.1128/mcb.17.5.2688

Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p.

S Vidan 1, A P Mitchell 1
PMCID: PMC232119  PMID: 9111339

Abstract

The Saccharomyces cerevisiae RIM15 gene was identified previously through a mutation that caused reduced ability to undergo meiosis. We report here an analysis of the cloned RIM15 gene, which specifies a 1,770-residue polypeptide with homology to serine/threonine protein kinases. Rim15p is most closely related to Schizosaccharomyces pombe cek1+. Analysis of epitope-tagged derivatives indicates that Rim15p has autophosphorylation activity. Deletion of RIM15 causes reduced expression of several early meiotic genes (IME2, SPO13, and HOP1) and of IME1, which specifies an activator of early meiotic genes. However, overexpression of IME1 does not permit full expression of early meiotic genes in a rim15delta mutant. Ime1p activates early meiotic genes through its interaction with Ume6p, and analysis of Rim15p-dependent regulatory sites at the IME2 promoter indicates that activation through Ume6p is defective. Two-hybrid interaction assays suggest that Ime1p-Ume6p interaction is diminished in a rim15 mutant. Glucose inhibits Ime1p-Ume6p interaction, and we find that Rim15p accumulation is repressed in glucose-grown cells. Thus, glucose repression of Rim15p may be responsible for glucose inhibition of Ime1p-Ume6p interaction.

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Selected References

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  1. Bowdish K. S., Mitchell A. P. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol Cell Biol. 1993 Apr;13(4):2172–2181. doi: 10.1128/mcb.13.4.2172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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. 1994 Dec;14(12):7909–7919. doi: 10.1128/mcb.14.12.7909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bowdish K. S., Yuan H. E., Mitchell A. P. Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol. 1995 Jun;15(6):2955–2961. doi: 10.1128/mcb.15.6.2955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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 U S A. 1990 Dec;87(23):9406–9410. doi: 10.1073/pnas.87.23.9406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Christianson T. W., Sikorski R. S., Dante M., Shero J. H., Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene. 1992 Jan 2;110(1):119–122. doi: 10.1016/0378-1119(92)90454-w. [DOI] [PubMed] [Google Scholar]
  6. Durfee T., Becherer K., Chen P. L., Yeh S. H., Yang Y., Kilburn A. E., Lee W. H., Elledge S. J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 1993 Apr;7(4):555–569. doi: 10.1101/gad.7.4.555. [DOI] [PubMed] [Google Scholar]
  7. Estojak J., Brent R., Golemis E. A. Correlation of two-hybrid affinity data with in vitro measurements. Mol Cell Biol. 1995 Oct;15(10):5820–5829. doi: 10.1128/mcb.15.10.5820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Field J., Nikawa J., Broek D., MacDonald B., Rodgers L., Wilson I. A., Lerner R. A., Wigler M. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol. 1988 May;8(5):2159–2165. doi: 10.1128/mcb.8.5.2159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gibbs C. S., Zoller M. J. Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J Biol Chem. 1991 May 15;266(14):8923–8931. [PubMed] [Google Scholar]
  10. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
  11. Hardy T. A., Wu D., Roach P. J. Novel Saccharomyces cerevisiae gene, MRK1, encoding a putative protein kinase with similarity to mammalian glycogen synthase kinase-3 and Drosophila Zeste-White3/Shaggy. Biochem Biophys Res Commun. 1995 Mar 17;208(2):728–734. doi: 10.1006/bbrc.1995.1398. [DOI] [PubMed] [Google Scholar]
  12. Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Dec;52(4):536–553. doi: 10.1128/mr.52.4.536-553.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Honigberg S. M., McCarroll R. M., Esposito R. E. Regulatory mechanisms in meiosis. Curr Opin Cell Biol. 1993 Apr;5(2):219–225. doi: 10.1016/0955-0674(93)90106-z. [DOI] [PubMed] [Google Scholar]
  14. Hughes K., Nikolakaki E., Plyte S. E., Totty N. F., Woodgett J. R. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 1993 Feb;12(2):803–808. doi: 10.1002/j.1460-2075.1993.tb05715.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kane S. M., Roth R. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol. 1974 Apr;118(1):8–14. doi: 10.1128/jb.118.1.8-14.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. doi: 10.1016/0092-8674(88)90427-8. [DOI] [PubMed] [Google Scholar]
  17. Law D. T., Segall J. The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation. Mol Cell Biol. 1988 Feb;8(2):912–922. doi: 10.1128/mcb.8.2.912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee R. H., Honigberg S. M. Nutritional regulation of late meiotic events in Saccharomyces cerevisiae through a pathway distinct from initiation. Mol Cell Biol. 1996 Jun;16(6):3222–3232. doi: 10.1128/mcb.16.6.3222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Luche R. M., Smart W. C., Marion T., Tillman M., Sumrada R. A., Cooper T. G. Saccharomyces cerevisiae BUF protein binds to sequences participating in DNA replication in addition to those mediating transcriptional repression (URS1) and activation. Mol Cell Biol. 1993 Sep;13(9):5749–5761. doi: 10.1128/mcb.13.9.5749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mandel S., Robzyk K., Kassir Y. IME1 gene encodes a transcription factor which is required to induce meiosis in Saccharomyces cerevisiae. Dev Genet. 1994;15(2):139–147. doi: 10.1002/dvg.1020150204. [DOI] [PubMed] [Google Scholar]
  21. Michaelis S., Herskowitz I. The a-factor pheromone of Saccharomyces cerevisiae is essential for mating. Mol Cell Biol. 1988 Mar;8(3):1309–1318. doi: 10.1128/mcb.8.3.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mitchell A. P., Bowdish K. S. Selection for early meiotic mutants in yeast. Genetics. 1992 May;131(1):65–72. doi: 10.1093/genetics/131.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mitchell A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. doi: 10.1128/mr.58.1.56-70.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mitchell A. P., Herskowitz I. Activation of meiosis and sporulation by repression of the RME1 product in yeast. 1986 Feb 27-Mar 5Nature. 319(6056):738–742. doi: 10.1038/319738a0. [DOI] [PubMed] [Google Scholar]
  25. Murakami Y., Naitou M., Hagiwara H., Shibata T., Ozawa M., Sasanuma S., Sasanuma M., Tsuchiya Y., Soeda E., Yokoyama K. Analysis of the nucleotide sequence of chromosome VI from Saccharomyces cerevisiae. Nat Genet. 1995 Jul;10(3):261–268. doi: 10.1038/ng0795-261. [DOI] [PubMed] [Google Scholar]
  26. Myers A. M., Tzagoloff A., Kinney D. M., Lusty C. J. Yeast shuttle and integrative vectors with multiple cloning sites suitable for construction of lacZ fusions. Gene. 1986;45(3):299–310. doi: 10.1016/0378-1119(86)90028-4. [DOI] [PubMed] [Google Scholar]
  27. Ng R., Abelson J. Isolation and sequence of the gene for actin in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3912–3916. doi: 10.1073/pnas.77.7.3912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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. 1992 Apr 25;20(8):1909–1915. doi: 10.1093/nar/20.8.1909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Puziss J. W., Hardy T. A., Johnson R. B., Roach P. J., Hieter P. MDS1, a dosage suppressor of an mck1 mutant, encodes a putative yeast homolog of glycogen synthase kinase 3. Mol Cell Biol. 1994 Jan;14(1):831–839. doi: 10.1128/mcb.14.1.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Roach P. J. Multisite and hierarchal protein phosphorylation. J Biol Chem. 1991 Aug 5;266(22):14139–14142. [PubMed] [Google Scholar]
  31. Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. doi: 10.1016/0378-1119(87)90232-0. [DOI] [PubMed] [Google Scholar]
  32. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  33. 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. 1996 May;16(5):2518–2526. doi: 10.1128/mcb.16.5.2518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Samejima I., Yanagida M. Identification of cut8+ and cek1+, a novel protein kinase gene, which complement a fission yeast mutation that blocks anaphase. Mol Cell Biol. 1994 Sep;14(9):6361–6371. doi: 10.1128/mcb.14.9.6361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shah J. C., Clancy M. J. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Mar;12(3):1078–1086. doi: 10.1128/mcb.12.3.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sherman A., Shefer M., Sagee S., Kassir Y. Post-transcriptional regulation of IME1 determines initiation of meiosis in Saccharomyces cerevisiae. Mol Gen Genet. 1993 Mar;237(3):375–384. doi: 10.1007/BF00279441. [DOI] [PubMed] [Google Scholar]
  37. Shirahige K., Iwasaki T., Rashid M. B., Ogasawara N., Yoshikawa H. Location and characterization of autonomously replicating sequences from chromosome VI of Saccharomyces cerevisiae. Mol Cell Biol. 1993 Aug;13(8):5043–5056. doi: 10.1128/mcb.13.8.5043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sia R. A., Mitchell A. P. Stimulation of later functions of the yeast meiotic protein kinase Ime2p by the IDS2 gene product. Mol Cell Biol. 1995 Oct;15(10):5279–5287. doi: 10.1128/mcb.15.10.5279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Smith H. E., Driscoll S. E., Sia R. A., Yuan H. E., Mitchell A. P. Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics. 1993 Apr;133(4):775–784. doi: 10.1093/genetics/133.4.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith H. E., Mitchell A. P. A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1989 May;9(5):2142–2152. doi: 10.1128/mcb.9.5.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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. 1990 Dec;10(12):6103–6113. doi: 10.1128/mcb.10.12.6103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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 U S A. 1995 Dec 19;92(26):12490–12494. doi: 10.1073/pnas.92.26.12490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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. 1994 Apr 1;8(7):796–810. doi: 10.1101/gad.8.7.796. [DOI] [PubMed] [Google Scholar]
  45. Su S. S., Mitchell A. P. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics. 1993 Jan;133(1):67–77. doi: 10.1093/genetics/133.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Su S. S., Mitchell A. P. Molecular characterization of the yeast meiotic regulatory gene RIM1. Nucleic Acids Res. 1993 Aug 11;21(16):3789–3797. doi: 10.1093/nar/21.16.3789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Szent-Gyorgyi C. A bipartite operator interacts with a heat shock element to mediate early meiotic induction of Saccharomyces cerevisiae HSP82. Mol Cell Biol. 1995 Dec;15(12):6754–6769. doi: 10.1128/mcb.15.12.6754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Taylor S. S., Knighton D. R., Zheng J., Ten Eyck L. F., Sowadski J. M. Structural framework for the protein kinase family. Annu Rev Cell Biol. 1992;8:429–462. doi: 10.1146/annurev.cb.08.110192.002241. [DOI] [PubMed] [Google Scholar]
  49. Tyers M., Tokiwa G., Futcher B. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 1993 May;12(5):1955–1968. doi: 10.1002/j.1460-2075.1993.tb05845.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Woodgett J. R. A common denominator linking glycogen metabolism, nuclear oncogenes and development. Trends Biochem Sci. 1991 May;16(5):177–181. doi: 10.1016/0968-0004(91)90071-3. [DOI] [PubMed] [Google Scholar]

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