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PMID: 10567524 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The elm1 kinase functions in a mitotic signaling network in budding yeast.

Molecular and cellular biology ·Vol. 19 ·No. 12 ·1999-12-00 ·Pages 7983-94

Sreenivasan A, Kellogg D

Abstract

In budding yeast, the Clb2 mitotic cyclin initiates a signaling network that negatively regulates polar bud growth during mitosis. This signaling network appears to require the function of a Clb2-binding protein called Nap1, the Cdc42 GTPase, and two protein kinases called Gin4 and Cla4. In this study, we demonstrate that the Elm1 kinase also plays a role in the control of bud growth during mitosis. Cells carrying a deletion of the ELM1 gene undergo a prolonged mitotic delay, fail to negatively regulate polar bud growth during mitosis, and show defects in septin organization. In addition, Elm1 is required in vivo for the proper regulation of both the Cla4 and Gin4 kinases and interacts genetically with Cla4, Gin4, and the mitotic cyclins. Previous studies have suggested that Elm1 may function to negatively regulate the Swe1 kinase. To further understand the functional relationship between Elm1 and Swe1, we have characterized the phenotype of Deltaelm1 Deltaswe1 cells. We found that Deltaelm1 Deltaswe1 cells are inviable at 37 degrees C and that a large proportion of Deltaelm1 Deltaswe1 cells grown at 30 degrees C contain multiple nuclei, suggesting severe defects in cytokinesis. In addition, we found that Elm1 is required for the normal hyperphosphorylation of Swe1 during mitosis. We propose a model in which the Elm1 kinase functions in a mitotic signaling network that controls events required for normal bud growth and cytokinesis, while the Swe1 kinase functions in a checkpoint pathway that delays nuclear division in response to defects in these events.

MeSH Terms
Animals CDC28 Protein Kinase, S cerevisiae/metabolism Cell Cycle Proteins Cyclin B/metabolism Cyclin-Dependent Kinases/genetics,metabolism,physiology Enzyme Activation Fungal Proteins/genetics,metabolism,physiology Genes, Fungal Mitosis Mutagenesis Phosphorylation Protein Serine-Threonine Kinases/genetics,metabolism,physiology Protein-Tyrosine Kinases/genetics,metabolism Rabbits Saccharomyces cerevisiae/enzymology,growth & development Saccharomyces cerevisiae Proteins Signal Transduction
Chemicals
CLB2 protein, S cerevisiae Cell Cycle Proteins Cyclin B Fungal Proteins Saccharomyces cerevisiae Proteins SWE1 protein, S cerevisiae Protein-Tyrosine Kinases CLA4 protein, S cerevisiae GIN4 protein, S cerevisiae Protein Serine-Threonine Kinases CDC28 Protein Kinase, S cerevisiae Cyclin-Dependent Kinases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sreenivasan A
Sinsheimer Laboratories, Department of Biology, University of California, Santa Cruz, California 95064, USA.
Kellogg D
References (49)
49 references, click to expand
  1. Negative regulation of the wee1 protein kinase by direct action of the nim1/cdr1 mitotic inducer.
    Cell. 1993 Mar 26;72(6):919-29 PMID: 7681363
  2. Control of mitotic events by the Cdc42 GTPase, the Clb2 cyclin and a member of the PAK kinase family.
    Curr Biol. 1998 Sep 10;8(18):991-1000 PMID: 9740799
  3. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins.
    Cell. 1993 Sep 24;74(6):993-1007 PMID: 8402888
  4. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins.
    EMBO J. 1993 Sep;12(9):3417-26 PMID: 8253069
  5. Two distinct mechanisms for negative regulation of the Wee1 protein kinase.
    EMBO J. 1993 Sep;12(9):3427-36 PMID: 7504624
  6. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast.
    Genetics. 1993 Nov;135(3):677-91 PMID: 8293973
  7. The yeast TEM1 gene, which encodes a GTP-binding protein, is involved in termination of M phase.
    Mol Cell Biol. 1994 Nov;14(11):7476-82 PMID: 7935462
  8. The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase.
    Mol Cell Biol. 1994 Dec;14(12):8282-91 PMID: 7969164
  9. A cell cycle checkpoint monitors cell morphogenesis in budding yeast.
    J Cell Biol. 1995 May;129(3):739-49 PMID: 7730408
  10. Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle.
    EMBO J. 1995 May 1;14(9):1878-91 PMID: 7743995
  11. Processing of adenovirus 2-induced proteins.
    J Virol. 1973 Aug;12(2):241-52 PMID: 4747985
  12. Genetic control of the cell division cycle in yeast.
    Science. 1974 Jan 11;183(4120):46-51 PMID: 4587263
  13. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis.
    Exp Cell Res. 1971 Dec;69(2):265-76 PMID: 4950437
  14. Genetic control of cell size at cell division in yeast.
    Nature. 1975 Aug 14;256(5518):547-51 PMID: 1165770
  15. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog.
    Cell. 1987 May 22;49(4):559-67 PMID: 3032459
  16. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck.
    Mol Cell Biol. 1987 Oct;7(10):3678-87 PMID: 3316985
  17. The product of the Saccharomyces cerevisiae cell cycle gene DBF2 has homology with protein kinases and is periodically expressed in the cell cycle.
    Mol Cell Biol. 1990 Apr;10(4):1358-66 PMID: 2181271
  18. Classical mutagenesis techniques.
    Methods Enzymol. 1991;194:273-81 PMID: 2005792
  19. Immunofluorescence methods for yeast.
    Methods Enzymol. 1991;194:565-602 PMID: 2005809
  20. CDC15, an essential cell cycle gene in Saccharomyces cerevisiae, encodes a protein kinase domain.
    Yeast. 1991 Apr;7(3):265-73 PMID: 1882551
  21. Twenty-five years of cell cycle genetics.
    Genetics. 1991 Dec;129(4):975-80 PMID: 1783298
  22. Purification of a multiprotein complex containing centrosomal proteins from the Drosophila embryo by chromatography with low-affinity polyclonal antibodies.
    Mol Biol Cell. 1992 Jan;3(1):1-11 PMID: 1372522
  23. Animal cell cycles and their control.
    Annu Rev Biochem. 1992;61:441-70 PMID: 1497317
  24. Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1992 Jul;3(7):805-18 PMID: 1387566
  25. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2.
    Genes Dev. 1992 Nov;6(11):2021-34 PMID: 1427070
  26. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins.
    J Cell Biol. 1993 Mar;120(6):1305-20 PMID: 8449978
  27. Cell cycle regulation of a Xenopus Wee1-like kinase.
    Mol Biol Cell. 1995 Jan;6(1):119-34 PMID: 7749193
  28. Cell cycle control of morphogenesis in budding yeast.
    Curr Opin Genet Dev. 1995 Feb;5(1):17-23 PMID: 7749320
  29. Cell cycle regulation of human WEE1.
    EMBO J. 1995 May 15;14(10):2166-75 PMID: 7774574
  30. Members of the NAP/SET family of proteins interact specifically with B-type cyclins.
    J Cell Biol. 1995 Aug;130(3):661-73 PMID: 7622566
  31. NAP1 acts with Clb1 to perform mitotic functions and to suppress polar bud growth in budding yeast.
    J Cell Biol. 1995 Aug;130(3):675-85 PMID: 7622567
  32. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast.
    Genes Dev. 1995 Aug 1;9(15):1817-30 PMID: 7649470
  33. Requirement of Saccharomyces cerevisiae Ras for completion of mitosis.
    Science. 1995 Nov 17;270(5239):1213-5 PMID: 7502049
  34. The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint.
    J Cell Biol. 1996 Jan;132(1-2):111-23 PMID: 8567717
  35. A search for proteins that interact genetically with histone H3 and H4 amino termini uncovers novel regulators of the Swe1 kinase in Saccharomyces cerevisiae.
    Genes Dev. 1996 Jun 1;10(11):1327-40 PMID: 8647431
  36. Control of mitotic events by Nap1 and the Gin4 kinase.
    J Cell Biol. 1997 Jul 14;138(1):119-30 PMID: 9214386
  37. Gin4 of S. cerevisiae is a bud neck protein that interacts with the Cdc28 complex.
    Genes Cells. 1997 Dec;2(12):753-70 PMID: 9544703
  38. The Polo-related kinase Cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae.
    Curr Biol. 1998 Apr 23;8(9):497-507 PMID: 9560342
  39. A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 Oct;9(10):2803-17 PMID: 9763445
  40. The septins are required for the mitosis-specific activation of the Gin4 kinase.
    J Cell Biol. 1998 Nov 2;143(3):709-17 PMID: 9813092
  41. Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function.
    J Cell Biol. 1998 Nov 2;143(3):719-36 PMID: 9813093
  42. Control of Swe1p degradation by the morphogenesis checkpoint.
    EMBO J. 1998 Nov 16;17(22):6678-88 PMID: 9822611
  43. The protein kinase Cdr2, related to Nim1/Cdr1 mitotic inducer, regulates the onset of mitosis in fission yeast.
    Mol Biol Cell. 1998 Dec;9(12):3321-34 PMID: 9843572
  44. The cdr2(+) gene encodes a regulator of G2/M progression and cytokinesis in Schizosaccharomyces pombe.
    Mol Biol Cell. 1998 Dec;9(12):3399-415 PMID: 9843577
  45. Control of Saccharomyces cerevisiae filamentous growth by cyclin-dependent kinase Cdc28.
    Mol Cell Biol. 1999 Feb;19(2):1369-80 PMID: 9891070
  46. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast.
    Genes Dev. 1999 Jan 15;13(2):176-87 PMID: 9925642
  47. Analysis of genetic interactions between DHH1, SSD1 and ELM1 indicates their involvement in cellular morphology determination in Saccharomyces cerevisiae.
    Yeast. 1999 Apr;15(6):481-96 PMID: 10234786
  48. A morphogenesis checkpoint monitors the actin cytoskeleton in yeast.
    J Cell Biol. 1998 Sep 21;142(6):1487-99 PMID: 9744879
  49. Regulation of dimorphism in Saccharomyces cerevisiae: involvement of the novel protein kinase homolog Elm1p and protein phosphatase 2A.
    Mol Cell Biol. 1993 Sep;13(9):5567-81 PMID: 8395007
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1999-12-00
Pages
7983-94
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC84883
Subset
IM
Grants
NIGMS NIH HHS · R01 GM053959 · United States
NIGMS NIH HHS · GM53959 · United States
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