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Novel alleles ofcdc13 andcdc2 isolated as suppressors of mitotic catastrophe inSchizosaccharomyces pombe

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Abstract

Cell cycle control in the fission yeastSchizosaccharomyces pombe involves interplay amongst a number of regulatory molecules, including thecdc2, cdc13, cdc25, weel, andmik1 gene products. Cdc2, Cdc13, and Cdc25 act as positive regulators of cell cycle progression at the G2/M boundary, while Wee1 and Mik1 play a negative regulatory role. Here, we have screened for suppressors of the lethal premature entry into mitosis, termed mitotic catastrophe, which results from simultaneous loss of function of both Wee1 and Mik1. Through such a screen, we hoped to identify additional components of the cell cycle regulatory network, and/or G2/M-specific substrates of Cdc2. Although we did not identify such molecules, we isolated a number of alleles of bothcdc2 andcdc13, including a novel wee allele ofcdc2, cdc2-5w. Here, we characterizecdc2-5w and two alleles ofcdc13, which have implications for the understanding of details of the interactions amongst Cdc2, Cdc13, and Wee1.

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References

  • Ayscough K, Hayles J, MacNeill SA, Nurse P (1992) Cold-sensitive mutants of p34cdc2 that suppress a mitotic catastrophe phenotype in fission yeast. Mol Gen Genet 232:344–350

    Google Scholar 

  • Barbet N, Muriel WJ, Carr AM (1992) Versatile shuttle vectors and genomic libraries for use withSchizosaccharomyces pombe. Gene 114:59–66

    Google Scholar 

  • Bueno A, Russell P (1993) Two fission yeast B-type cyclins, Cig2 and Cdc13, have different functions in mitosis. Mol Cell Biol 13:2286–2297

    Google Scholar 

  • Booher R, Beach D (1987) Interaction betweencdc13 + andcdc2 + in the control of mitosis in fission yeast: dissociation of the G1 and G2 roles of thecdc2 + protein kinase. EMBO J 6:3441–3447

    Google Scholar 

  • Booher R, Beach D (1988) Involvement ofcdc13 + in mitotic control inSchizosaccharomyces pombe: possible interaction of the gene product with microtubules. EMBO J 7:2321–2327

    Google Scholar 

  • Booher RN, Alfa CA, Hyams JS, Beach DH (1989) The fission yeastcdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization. Cell 58:485–497

    Google Scholar 

  • Booher RN, Deshaies RJ, Kirschner MW (1993) Properties ofSchizosaccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J 12:3417–3426

    Google Scholar 

  • Burke JD, Gould KL (1994) Molecular cloning and characterization of theSchizosaccharomyces pombe his3 gene for use as a selectable marker. Mol Gen Genet 242:169–176

    Google Scholar 

  • Carr AM, MacNeill SA, Hayles J, Nurse P (1989) Molecular cloning and sequence analysis of mutant alleles of the fission yeastcdc2 protein kinase gene: implications forcdc2 + protein structure and function. Mol Gen Genet 218:41–49

    Google Scholar 

  • Coleman TR, Dunphy WG (1994) Cdc2 regulatory factors. Curr Opin Cell Biol 6:877–882

    Google Scholar 

  • DeBondt HL, Rosenblatt J, Jancarik J, Jones HD, Morgan DO, Kim S-H (1993) Crystal structure of cyclin-dependent kinase 2. Nature 36:595–602

    Google Scholar 

  • Den Haese GJ, Walworth N, Carr AM, Gould KL (1995) The Wee1 protein kinase regulates T14 phosphorylation of fission yeast Cdc2. Mol Biol Cell 6:371–385

    Google Scholar 

  • Fantes PA (1981) Isolation of cell size mutants of a fission yeast by a new selective method: characterization of mutants and implications for division control mechanisms. J Bacteriol 146:746–754

    Google Scholar 

  • Featherstone C, Russell P (1991) Fission yeast p107wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature 349:808–811

    Google Scholar 

  • Feilotter H, Nurse P, Young PG (1991) Genetic and molecular analysis ofcdr1/nim1 inSchizosaccharomyces pombe. Genetics 127:1–10

    Google Scholar 

  • Fleig U and Nurse P (1991) Expression of a dominant negative allele ofcdc2 prevents activation of the endogenous p34cdc2 kinase. Mol Gen Genet 226:432–440

    Google Scholar 

  • Gould KL, Nurse P (1989) Tyrosine phosphorylation of fission yeastcdc2 + protein kinase regulates entry into mitosis. Nature 342:39–42

    Google Scholar 

  • Gould KL, Moreno S, Owen DJ, Sazer S, Nurse P (1991) Phosphorylation of Thr 167 is required forSchizosaccharomyces pombe p34cdc2 function EMBO J 10:3297–3307

    Google Scholar 

  • Hagan IH, Hayles J, Nurse P (1988) Cloning and sequencing of the cyclin-relatedcdc13 + gene and a cytological study of its role in fission yeast mitosis. J Cell Sci 91:587–595

    Google Scholar 

  • Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52

    Google Scholar 

  • Hayles J, Nurse P (1995) A pre-Start checkpoint preventing mitosis in fission yeast acts independently of p34cdc2 tyrosine phosphorylation. EMBO J 14:2760–2771

    Google Scholar 

  • Hindley J, Phear GA (1984) Sequence of the cell division genecdc2 fromSchizosaccharomyces pombe: patterns of splicing and homology to protein kinases. Gene 31:129–134

    Google Scholar 

  • Knighton DR, Zheng JH, Ten Eyck LF, Xoung NH, Taylor SS, Sowadski JM (1991) Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:414–420

    Google Scholar 

  • Kohli J, Hottinger H, Munz P, Strauss A, Thuriaux P (1977) Genetic mapping inSchizosaccharomyces pombe by mitotic and meitotic analysis and induced haploidization. Genetics 87:471–489

    Google Scholar 

  • Labib K, Craven RA, Crawford K, Nurse P (1995) Dominant mutants identify new roles for p34cdc2 in mitosis. EMBO J 14:2155–2165

    Google Scholar 

  • Lee MS, Enoch T, Piwnica-Worms H (1994)mik1 + encodes a tyrosine kinase that phosphorylates p34cdc2 on tyrosine 15. J Biol Chem 269:30530–30537

    Google Scholar 

  • Lundgren K, Walworth N, Booher R, Dembski M, Kirschner M, Beach D (1991) Mik1 and Wee1 cooperate in the inhibitory tyrosine phosphorylation ofcdc2. Cell 64:1111–1122

    Google Scholar 

  • MacNeill SA, Nurse P (1993) Genetic analysis of human p34CDC2 function in fission yeast. Mol Gen Genet 240:315–322

    Google Scholar 

  • MacNeill SA, Creanor J, Nurse P (1991) Isolation, characterization, and molecular cloning of new mutant alleles of the fission yeast p34cdc2 protein kinase gene: identification of temperature-sensitive G2-arresting alleles. Mol Gen Genet 229:109–118

    Google Scholar 

  • Maundrell K (1991)nmt1 of fission yeast. J Biol Chem 265:10857–10864

    Google Scholar 

  • Maundrell K (1993) Thiamine-repressible vectors pREP and pRIP for fission yeast. Gene 123:127–130

    Google Scholar 

  • Millar JBA, Russell P (1992) Thecdc25 M-phase inducer: an unconventional protein phosphatase. Cell 68:407–410

    Google Scholar 

  • Moir D, Stewart SE, Osmond BC, Botstein D (1982) Cold-sensitive cell division cycle mutants of yeast:isolation, properties, and pseudoreversion studies. Genetics 100:547–563

    Google Scholar 

  • Molz L, Booher R, Young P, Beach D (1989)cdc2 and the regulation of mitosis: 6 interactingmcs genes. Genetics 122:773–782

    Google Scholar 

  • Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeastSchizosaccharomyces pombe. Methods Enzymol 194:795–823

    Google Scholar 

  • Nugent JHA, Alfa CE, Young T, Hyans JS (1991) Conserved structural motifs in cyclins identified by sequence analysis. J Cell Sci 99:669–674

    Google Scholar 

  • Nurse P (1975) Genetic control of cell size at cell division in yeast. Nature 256:547–551

    Google Scholar 

  • Nurse P, Bissett Y (1981) Gene required in G1 for commitment to the cell cycle and G2 for control of mitosis in the fission yeast. Nature 292:558–560

    Google Scholar 

  • Nurse P, Thuriaux P (1977) Controls over the timing of DNA replication during the cell cycle of fission yeast. Exp Cell Res 107:365–375

    Google Scholar 

  • Nurse P, Thuriaux P (1980) Regulatory genes controlling mitosis in the fission yeastSchizosaccharomyces pombe. Genetics 96:627–637

    Google Scholar 

  • Prentice HL (1991) High efficiency transformation ofSchizosaccharomyces pombe by electroporation. Nucleic Acids Res 20:621

    Google Scholar 

  • Russell P, Nurse P (1986) cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45:145–153

    Google Scholar 

  • Russell P, Nurse P (1987) Negative regulation of mitosis byweel +, a gene encoding a protein kinase homolog. Cell 49:559–567

    Google Scholar 

  • Sazer S, Sherwood SW (1990) Mitcohondrial growth and DNA synthesis occur in the absence of nuclear DNA replication in fission yeast. J Cell Sci 97:509–516

    Google Scholar 

  • Simanis V, Nurse P (1986) The cell cycle control genecdc2 + of fission yeast encodes a protein kinase potentially regulated by phosphorylation. Cell 45:261–268

    Google Scholar 

  • Young PG, Fantes P (1987)Schizosaccharomyces pombe mutants affected in their division response to starvation. J Cell Sci 88:295–304

    Google Scholar 

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Communicated by D. Y. Thomas

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Berry, L.D., Gould, K.L. Novel alleles ofcdc13 andcdc2 isolated as suppressors of mitotic catastrophe inSchizosaccharomyces pombe . Molec. Gen. Genet. 251, 635–646 (1996). https://doi.org/10.1007/BF02174112

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