• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of molcellbPermissionsJournals.ASM.orgJournalMCB ArticleJournal InfoAuthorsReviewers
Mol Cell Biol. Dec 1994; 14(12): 7909–7919.
PMCID: PMC359330

Analysis of RIM11, a yeast protein kinase that phosphorylates the meiotic activator IME1.


Many yeast genes that are essential for meiosis are expressed only in meiotic cells. Known regulators of early meiotic genes include IME1, which is required for their expression, and SIN3 and UME6, which prevent their expression in nonmeiotic cells. We report here the molecular characterization of the RIM11 gene, which we find is required for expression of several early meiotic genes. A close functional relationship between RIM11 and IME1 is supported by two observations. First, sin3 and ume6 mutations are epistatic to rim11 mutations; prior studies have demonstrated their epistasis to ime1 mutations. Second, overexpression of RIM11 can suppress an ime1 missense mutation (ime1-L321F) but not an ime1 deletion. Sequence analysis indicates that RIM11 specifies a protein kinase related to rat glycogen synthase kinase 3 and the Drosophila shaggy/zw3 gene product. Three partially defective rim11 mutations alter residues involved in ATP binding or catalysis, and a completely defective rim11 mutation alters a tyrosine residue that corresponds to the site of an essential phosphorylation for glycogen synthase kinase 3. Immune complexes containing a hemagglutinin (HA) epitope-tagged RIM11 derivative, HA-RIM11, phosphorylate two proteins, p58 and p60, whose biological function is undetermined. In addition, HA-RIM11 immune complexes phosphorylate a functional IME1 derivative but not the corresponding ime1-L321F derivative. We propose that RIM11 stimulates meiotic gene expression through phosphorylation of IME1.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.7M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bianchi MW, Plyte SE, Kreis M, Woodgett JR. A Saccharomyces cerevisiae protein-serine kinase related to mammalian glycogen synthase kinase-3 and the Drosophila melanogaster gene shaggy product. Gene. 1993 Nov 30;134(1):51–56. [PubMed]
  • Bowdish KS, Mitchell AP. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol Cell Biol. 1993 Apr;13(4):2172–2181. [PMC free article] [PubMed]
  • Buckingham LE, Wang HT, Elder RT, McCarroll RM, Slater MR, Esposito RE. 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. [PMC free article] [PubMed]
  • Fields S, Song O. A novel genetic system to detect protein-protein interactions. Nature. 1989 Jul 20;340(6230):245–246. [PubMed]
  • Geiger T, Clarke S. Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J Biol Chem. 1987 Jan 15;262(2):785–794. [PubMed]
  • Gibbs CS, Zoller MJ. 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]
  • Gonzalez GA, Montminy MR. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell. 1989 Nov 17;59(4):675–680. [PubMed]
  • Hanks SK, Quinn AM. Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods Enzymol. 1991;200:38–62. [PubMed]
  • Hanks SK, Quinn AM, Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. [PubMed]
  • Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Dec;52(4):536–553. [PMC free article] [PubMed]
  • Hollingsworth NM, Goetsch L, Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990 Apr 6;61(1):73–84. [PubMed]
  • Honigberg SM, McCarroll RM, Esposito RE. Regulatory mechanisms in meiosis. Curr Opin Cell Biol. 1993 Apr;5(2):219–225. [PubMed]
  • Hughes K, Nikolakaki E, Plyte SE, Totty NF, Woodgett JR. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 1993 Feb;12(2):803–808. [PMC free article] [PubMed]
  • Kao G, Shah JC, Clancy MJ. An RME1-independent pathway for sporulation control in Saccharomyces cerevisiae acts through IME1 transcript accumulation. Genetics. 1990 Dec;126(4):823–835. [PMC free article] [PubMed]
  • Kassir Y, Granot D, Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. [PubMed]
  • Knighton DR, Zheng JH, Ten Eyck LF, Ashford VA, Xuong NH, Taylor SS, Sowadski JM. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science. 1991 Jul 26;253(5018):407–414. [PubMed]
  • Koff A, Giordano A, Desai D, Yamashita K, Harper JW, Elledge S, Nishimoto T, Morgan DO, Franza BR, Roberts JM. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science. 1992 Sep 18;257(5077):1689–1694. [PubMed]
  • Law DT, 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. [PMC free article] [PubMed]
  • Luche RM, Smart WC, Marion T, Tillman M, Sumrada RA, Cooper TG. 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. [PMC free article] [PubMed]
  • Malone RE. Dual regulation of meiosis in yeast. Cell. 1990 May 4;61(3):375–378. [PubMed]
  • Mitchell AP. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. [PMC free article] [PubMed]
  • Mitchell AP, Bowdish KS. Selection for early meiotic mutants in yeast. Genetics. 1992 May;131(1):65–72. [PMC free article] [PubMed]
  • Mitchell AP, Driscoll SE, Smith HE. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2104–2110. [PMC free article] [PubMed]
  • Neigeborn L, Mitchell AP. The yeast MCK1 gene encodes a protein kinase homolog that activates early meiotic gene expression. Genes Dev. 1991 Apr;5(4):533–548. [PubMed]
  • Puziss JW, Hardy TA, Johnson RB, Roach PJ, 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. [PMC free article] [PubMed]
  • Roach PJ. Multisite and hierarchal protein phosphorylation. J Biol Chem. 1991 Aug 5;266(22):14139–14142. [PubMed]
  • Rose MD, Novick P, Thomas JH, Botstein D, Fink GR. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. [PubMed]
  • Shah JC, Clancy MJ. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Mar;12(3):1078–1086. [PMC free article] [PubMed]
  • Shero JH, Hieter P. A suppressor of a centromere DNA mutation encodes a putative protein kinase (MCK1). Genes Dev. 1991 Apr;5(4):549–560. [PubMed]
  • Sikorski RS, 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. [PMC free article] [PubMed]
  • Smith HE, Driscoll SE, Sia RA, Yuan HE, Mitchell AP. Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics. 1993 Apr;133(4):775–784. [PMC free article] [PubMed]
  • Smith HE, Mitchell AP. A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1989 May;9(5):2142–2152. [PMC free article] [PubMed]
  • Smith HE, Su SS, Neigeborn L, Driscoll SE, Mitchell AP. Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6103–6113. [PMC free article] [PubMed]
  • Stearns T, Hoyt MA, Botstein D. Yeast mutants sensitive to antimicrotubule drugs define three genes that affect microtubule function. Genetics. 1990 Feb;124(2):251–262. [PMC free article] [PubMed]
  • Strich R, Slater MR, Esposito RE. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10018–10022. [PMC free article] [PubMed]
  • Strich R, Surosky RT, Steber C, Dubois E, Messenguy F, Esposito RE. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 1994 Apr 1;8(7):796–810. [PubMed]
  • Su SS, Mitchell AP. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics. 1993 Jan;133(1):67–77. [PMC free article] [PubMed]
  • Su SS, Mitchell AP. Molecular characterization of the yeast meiotic regulatory gene RIM1. Nucleic Acids Res. 1993 Aug 11;21(16):3789–3797. [PMC free article] [PubMed]
  • Taylor SS, Knighton DR, Zheng J, Sowadski JM, Gibbs CS, Zoller MJ. A template for the protein kinase family. Trends Biochem Sci. 1993 Mar;18(3):84–89. [PubMed]
  • Treinin M, Simchen G. Mitochondrial activity is required for the expression of IME1, a regulator of meiosis in yeast. Curr Genet. 1993 Mar;23(3):223–227. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Vershon AK, Hollingsworth NM, Johnson AD. Meiotic induction of the yeast HOP1 gene is controlled by positive and negative regulatory sites. Mol Cell Biol. 1992 Sep;12(9):3706–3714. [PMC free article] [PubMed]
  • Vidal M, Gaber RF. RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Dec;11(12):6317–6327. [PMC free article] [PubMed]
  • Vidal M, Strich R, Esposito RE, Gaber RF. RPD1 (SIN3/UME4) is required for maximal activation and repression of diverse yeast genes. Mol Cell Biol. 1991 Dec;11(12):6306–6316. [PMC free article] [PubMed]
  • Wang H, Clark I, Nicholson PR, Herskowitz I, Stillman DJ. The Saccharomyces cerevisiae SIN3 gene, a negative regulator of HO, contains four paired amphipathic helix motifs. Mol Cell Biol. 1990 Nov;10(11):5927–5936. [PMC free article] [PubMed]
  • Wang HT, Frackman S, Kowalisyn J, Esposito RE, Elder R. Developmental regulation of SPO13, a gene required for separation of homologous chromosomes at meiosis I. Mol Cell Biol. 1987 Apr;7(4):1425–1435. [PMC free article] [PubMed]
  • Woodgett JR. A common denominator linking glycogen metabolism, nuclear oncogenes and development. Trends Biochem Sci. 1991 May;16(5):177–181. [PubMed]
  • Yamamoto KK, Gonzalez GA, Menzel P, Rivier J, Montminy MR. Characterization of a bipartite activator domain in transcription factor CREB. Cell. 1990 Feb 23;60(4):611–617. [PubMed]
  • Yang X, Hubbard EJ, Carlson M. A protein kinase substrate identified by the two-hybrid system. Science. 1992 Jul 31;257(5070):680–682. [PubMed]
  • Zhou Z, Elledge SJ. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell. 1993 Dec 17;75(6):1119–1127. [PubMed]

Articles from Molecular and Cellular Biology are provided here courtesy of American Society for Microbiology (ASM)


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...