© The Rockefeller University Press,
0021-9525/1998//709 $5.00
The Journal of Cell Biology, Volume 143, Number 3,
, 1998 709-717
The Septins Are Required for the Mitosis-specific Activation of the Gin4 Kinase
Christopher W. Carroll,
Roger Altman,
David Schieltz
,
John R. Yates, III
, and
Douglas Kellogg
Department of Biology, Sinsheimer Laboratories, University of California, Santa Cruz, California 95064; and
Center for Comprehensive Biology, University of Washington, Seattle, Washington 98195-7730
In budding yeast, a protein kinase called Gin4 is specifically activated during mitosis and functions in a pathway initiated by the Clb2 cyclin to control bud growth. We have used genetics and biochemistry to identify additional proteins that function with Gin4 in this pathway, and both of these approaches have identified members of the septin family. Loss of septin function produces a phenotype that is very similar to the phenotype caused by loss of Gin4 function, and the septins are required early in mitosis to activate Gin4 kinase activity. Furthermore, septin mutants display a prolonged mitotic delay at the short spindle stage, consistent with a role for the septins in the control of mitotic events. Members of the septin family bind directly to Gin4, demonstrating that the functions of Gin4 and the septins must be closely linked within the cell. These results demonstrate that the septins in budding yeast play an integral role in the mitosis-specific regulation of the Gin4 kinase and that they carry out functions early in mitosis.
Key Words: septins Gin4 cyclin-dependent kinase mitosis morphogenesis
Abbreviations used in this paper: GST, glutathione-S-transferase; ORF, open reading frame.
Address all correspondence to Douglas Kellogg, Department of Biology, Sinsheimer Laboratories, University of California, Santa Cruz, CA 95064. Tel.: (831) 459-5659. Fax: (831) 459-3139. E-mail: kellogg{at}darwin.ucsc.edu
C.W. Carroll's and R. Altman's present address is Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94143.

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-
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-
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-
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-
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-
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-
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-
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-
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[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
Song, S., Lee, K. S.
(2001). A Novel Function of Saccharomyces cerevisiae CDC5 in Cytokinesis. JCB
152: 451-470
[Abstract]
[Full Text]
-
Lord, M., Yang, M. C., Mischke, M., Chant, J.
(2000). Cell Cycle Programs of Gene Expression Control Morphogenetic Protein Localization. JCB
151: 1501-1512
[Abstract]
[Full Text]
-
Yang, H., Jiang, W., Gentry, M., Hallberg, R. L.
(2000). Loss of a Protein Phosphatase 2A Regulatory Subunit (Cdc55p) Elicits Improper Regulation of Swe1p Degradation. Mol. Cell. Biol.
20: 8143-8156
[Abstract]
[Full Text]
-
Russell, S. E. H., McIlhatton, M. A., Burrows, J. F., Donaghy, P. G., Chanduloy, S., Petty, E. M., Kalikin, L. M., Church, S. W., McIlroy, S., Harkin, D. P., Keilty, G. W., Cranston, A. N., Weissenbach, J., Hickey, I., Johnston, P. G.
(2000). Isolation and Mapping of a Human Septin Gene to a Region on Chromosome 17q, Commonly Deleted in Sporadic Epithelial Ovarian Tumors. Cancer Res.
60: 4729-4734
[Abstract]
[Full Text]
-
Adam, J. C., Pringle, J. R., Peifer, M.
(2000). Evidence for Functional Differentiation among Drosophila Septins in Cytokinesis and Cellularization. Mol. Biol. Cell
11: 3123-3135
[Abstract]
[Full Text]
-
Longtine, M. S., Theesfeld, C. L., McMillan, J. N., Weaver, E., Pringle, J. R., Lew, D. J.
(2000). Septin-Dependent Assembly of a Cell Cycle-Regulatory Module in Saccharomyces cerevisiae. Mol. Cell. Biol.
20: 4049-4061
[Abstract]
[Full Text]
-
Xue, J., Wang, X., Malladi, C. S., Kinoshita, M., Milburn, P. J., Lengyel, I., Rostas, J. A. P., Robinson, P. J.
(2000). Phosphorylation of a New Brain-specific Septin, G-septin, by cGMP-dependent Protein Kinase. J. Biol. Chem.
275: 10047-10056
[Abstract]
[Full Text]
-
Bouquin, N, Barral, Y, Courbeyrette, R, Blondel, M, Snyder, M, Mann, C
(2000). Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae. J. Cell Sci.
113: 1435-1445
[Abstract]
-
Pruyne, D, Bretscher, A
(2000). Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci.
113: 365-375
[Abstract]
-
Song, S., Grenfell, T. Z., Garfield, S., Erikson, R. L., Lee, K. S.
(2000). Essential Function of the Polo Box of Cdc5 in Subcellular Localization and Induction of Cytokinetic Structures. Mol. Cell. Biol.
20: 286-298
[Abstract]
[Full Text]
-
Lee, K. S., Song, S., Erikson, R. L.
(1999). The polo-box-dependent induction of ectopic septal structures by a mammalian polo kinase, Plk, in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA
96: 14360-14365
[Abstract]
[Full Text]
-
Sreenivasan, A., Kellogg, D.
(1999). The Elm1 Kinase Functions in a Mitotic Signaling Network in Budding Yeast. Mol. Cell. Biol.
19: 7983-7994
[Abstract]
[Full Text]
-
Johnson, E. S., Blobel, G.
(1999). Cell Cycle-Regulated Attachment of the Ubiquitin-Related Protein Sumo to the Yeast Septins. JCB
147: 981-994
[Abstract]
[Full Text]
-
Holly, S. P., Blumer, K. J.
(1999). Pak-Family Kinases Regulate Cell and Actin Polarization Throughout the Cell Cycle of Saccharomyces cerevisiae. JCB
147: 845-856
[Abstract]
[Full Text]
-
Shulewitz, M. J., Inouye, C. J., Thorner, J.
(1999). Hsl7 Localizes to a Septin Ring and Serves as an Adapter in a Regulatory Pathway That Relieves Tyrosine Phosphorylation of Cdc28 Protein Kinase in Saccharomyces cerevisiae. Mol. Cell. Biol.
19: 7123-7137
[Abstract]
[Full Text]
-
Richman, T. J., Sawyer, M. M., Johnson, D. I.
(1999). The Cdc42p GTPase Is Involved in a G2/M Morphogenetic Checkpoint Regulating the Apical-Isotropic Switch and Nuclear Division in Yeast. J. Biol. Chem.
274: 16861-16870
[Abstract]
[Full Text]
-
Johnson, D. I.
(1999). Cdc42: An Essential Rho-Type GTPase Controlling Eukaryotic Cell Polarity. Microbiol. Mol. Biol. Rev.
63: 54-105
[Abstract]
[Full Text]
-
Barral, Y., Parra, M., Bidlingmaier, S., Snyder, M.
(1999). Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev.
13: 176-187
[Abstract]
[Full Text]
-
Longtine, M. S., Fares, H., Pringle, J. R.
(1998). Role of the Yeast Gin4p Protein Kinase in Septin Assembly and the Relationship between Septin Assembly and Septin Function. JCB
143: 719-736
[Abstract]
[Full Text]
-
Frazier, J. A., Wong, M. L., Longtine, M. S., Pringle, J. R., Mann, M., Mitchison, T. J., Field, C.
(1998). Polymerization of Purified Yeast Septins: Evidence That Organized Filament Arrays May Not Be Required for Septin Function. JCB
143: 737-749
[Abstract]
[Full Text]
-
Westfall, P. J., Momany, M.
(2002). Aspergillus nidulans Septin AspB Plays Pre- and Postmitotic Roles in Septum, Branch, and Conidiophore Development. Mol. Biol. Cell
13: 110-118
[Abstract]
[Full Text]