Published 31 March 2003. doi:10.1083/jcb.200211126
© The Rockefeller University Press,
0021-9525/2003/3/1093 $5.00
The Journal of Cell Biology, Volume 160, Number 7, 1093-1103
An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation
Joseph J. Tasto2,
Jennifer L. Morrell1,2 and
Kathleen L. Gould1,2
1 Howard Hughes Medical Institute, Vanderbilt University School of Medicine, Nashville, TN 37232
2 Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232
Address correspondence to Kathleen L. Gould, Vanderbilt University School of Medicine, Department of Cell and Developmental Biology, B2309 MCN, 1161 21st Ave. South, Nashville, TN 37232. Tel.: (615) 343-9502. Fax: (615) 343-0723. E-mail: kathy.gould{at}vanderbilt.edu
Anillin is a conserved protein required for cell division (Field, C.M., and B.M. Alberts. 1995. J. Cell Biol. 131:165178; Oegema, K., M.S. Savoian, T.J. Mitchison, and C.M. Field. 2000. J. Cell Biol. 150:539552). One fission yeast homologue of anillin, Mid1p, is necessary for the proper placement of the division site within the cell (Chang, F., A. Woollard, and P. Nurse. 1996. J. Cell Sci. 109(Pt 1):131142; Sohrmann, M., C. Fankhauser, C. Brodbeck, and V. Simanis. 1996. Genes Dev. 10:27072719). Here, we identify and characterize a second fission yeast anillin homologue, Mid2p, which is not orthologous with Mid1p. Mid2p localizes as a single ring in the middle of the cell after anaphase in a septin- and actin-dependent manner and splits into two rings during septation. Mid2p colocalizes with septins, and mid2
cells display disorganized, diffuse septin rings and a cell separation defect similar to septin deletion strains. mid2 gene expression and protein levels fluctuate during the cell cycle in a sep1- and Skp1/Cdc53/F-box (SCF)dependent manner, respectively, implying that Mid2p activity must be carefully regulated. Overproduction of Mid2p depolarizes cell growth and affects the organization of both the septin and actin cytoskeletons. In the presence of a nondegradable Mid2p fragment, the septin ring is stabilized and cell cycle progression is delayed. These results suggest that Mid2p influences septin ring organization at the site of cell division and its turnover might normally be required to permit septin ring disassembly.
Key Words: S. pombe; cytokinesis; cell cycle; septin; mid2
The online version of this article includes supplemental material.
* Abbreviations used in this paper: APC, anaphase-promoting complex; LatA, latrunculin A; PEST, Pro/Glu/Ser/Thr; PH, pleckstrin homology; SCF, Skp1/Cdc53/F-box.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Reddit
Technorati What's this?
This article has been cited by other articles:
-
Tsang, C. W., Fedchyshyn, M., Harrison, J., Xie, H., Xue, J., Robinson, P. J., Wang, L.-Y., Trimble, W. S.
(2008). Superfluous Role of Mammalian Septins 3 and 5 in Neuronal Development and Synaptic Transmission. Mol. Cell. Biol.
28: 7012-7029
[Abstract]
[Full Text]
-
Clifford, D. M., Wolfe, B. A., Roberts-Galbraith, R. H., McDonald, W. H., Yates, J. R. III, Gould, K. L.
(2008). The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. JCB
181: 79-88
[Abstract]
[Full Text]
-
Ge, W., Balasubramanian, M. K.
(2008). Pxl1p, a Paxillin-related Protein, Stabilizes the Actomyosin Ring during Cytokinesis in Fission Yeast. Mol. Biol. Cell
19: 1680-1692
[Abstract]
[Full Text]
-
Shlomovitz, R., Gov, N. S.
(2008). Physical Model of Contractile Ring Initiation in Dividing Cells. Biophys. J
94: 1155-1168
[Abstract]
[Full Text]
-
Park, H.-O., Bi, E.
(2007). Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond. Microbiol. Mol. Biol. Rev.
71: 48-96
[Abstract]
[Full Text]
-
Moseley, J. B., Goode, B. L.
(2006). The Yeast Actin Cytoskeleton: from Cellular Function to Biochemical Mechanism. Microbiol. Mol. Biol. Rev.
70: 605-645
[Abstract]
[Full Text]
-
Jin, Q.-W., Zhou, M., Bimbo, A., Balasubramanian, M. K., McCollum, D.
(2006). A Role for the Septation Initiation Network in Septum Assembly Revealed by Genetic Analysis of sid2-250 Suppressors. Genetics
172: 2101-2112
[Abstract]
[Full Text]
-
Petit, C. S., Mehta, S., Roberts, R. H., Gould, K. L.
(2005). Ace2p contributes to fission yeast septin ring assembly by regulating mid2+ expression. J. Cell Sci.
118: 5731-5742
[Abstract]
[Full Text]
-
Morrell-Falvey, J. L., Ren, L., Feoktistova, A., Haese, G. D., Gould, K. L.
(2005). Cell wall remodeling at the fission yeast cell division site requires the Rho-GEF Rgf3p. J. Cell Sci.
118: 5563-5573
[Abstract]
[Full Text]
-
Wu, J.-Q., Pollard, T. D.
(2005). Counting Cytokinesis Proteins Globally and Locally in Fission Yeast. Science
310: 310-314
[Abstract]
[Full Text]
-
Santos, B., Martin-Cuadrado, A. B., Vazquez de Aldana, C. R., del Rey, F., Perez, P.
(2005). Rho4 GTPase Is Involved in Secretion of Glucanases during Fission Yeast Cytokinesis. Eukaryot Cell
4: 1639-1645
[Abstract]
[Full Text]
-
Martin-Cuadrado, A. B., Morrell, J. L., Konomi, M., An, H., Petit, C., Osumi, M., Balasubramanian, M., Gould, K. L., del Rey, F., de Aldana, C. R. V.
(2005). Role of Septins and the Exocyst Complex in the Function of Hydrolytic Enzymes Responsible for Fission Yeast Cell Separation. Mol. Biol. Cell
16: 4867-4881
[Abstract]
[Full Text]
-
Zhao, W.-m., Fang, G.
(2005). Anillin Is a Substrate of Anaphase-promoting Complex/Cyclosome (APC/C) That Controls Spatial Contractility of Myosin during Late Cytokinesis. J. Biol. Chem.
280: 33516-33524
[Abstract]
[Full Text]
-
Douglas, L. M., Alvarez, F. J., McCreary, C., Konopka, J. B.
(2005). Septin Function in Yeast Model Systems and Pathogenic Fungi. Eukaryot Cell
4: 1503-1512
[Full Text]
-
Maddox, A. S., Habermann, B., Desai, A., Oegema, K.
(2005). Distinct roles for two C. elegans anillins in the gonad and early embryo. Development
132: 2837-2848
[Abstract]
[Full Text]
-
Field, C. M., Coughlin, M., Doberstein, S., Marty, T., Sullivan, W.
(2005). Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development
132: 2849-2860
[Abstract]
[Full Text]
-
Venkatram, S., Jennings, J. L., Link, A., Gould, K. L.
(2005). Mto2p, a Novel Fission Yeast Protein Required for Cytoplasmic Microtubule Organization and Anchoring of the Cytokinetic Actin Ring. Mol. Biol. Cell
16: 3052-3063
[Abstract]
[Full Text]
-
Monzo, P., Gauthier, N. C., Keslair, F., Loubat, A., Field, C. M., Le Marchand-Brustel, Y., Cormont, M.
(2005). Clues to CD2-associated Protein Involvement in Cytokinesis. Mol. Biol. Cell
16: 2891-2902
[Abstract]
[Full Text]
-
Lee, K. M., Miklos, I., Du, H., Watt, S., Szilagyi, Z., Saiz, J. E., Madabhushi, R., Penkett, C. J., Sipiczki, M., Bahler, J., Fisher, R. P.
(2005). Impairment of the TFIIH-associated CDK-activating Kinase Selectively Affects Cell Cycle-regulated Gene Expression in Fission Yeast. Mol. Biol. Cell
16: 2734-2745
[Abstract]
[Full Text]
-
Gladfelter, A. S., Kozubowski, L., Zyla, T. R., Lew, D. J.
(2005). Interplay between septin organization, cell cycle and cell shape in yeast. J. Cell Sci.
118: 1617-1628
[Abstract]
[Full Text]
-
Alonso-Nunez, M. L., An, H., Martin-Cuadrado, A. B., Mehta, S., Petit, C., Sipiczki, M., del Rey, F., Gould, K. L., Vazquez de Aldana, C. R.
(2005). Ace2p Controls the Expression of Genes Required for Cell Separation in Schizosaccharomyces pombe. Mol. Biol. Cell
16: 2003-2017
[Abstract]
[Full Text]
-
Straight, A. F., Field, C. M., Mitchison, T. J.
(2005). Anillin Binds Nonmuscle Myosin II and Regulates the Contractile Ring. Mol. Biol. Cell
16: 193-201
[Abstract]
[Full Text]
-
An, H., Morrell, J. L., Jennings, J. L., Link, A. J., Gould, K. L.
(2004). Requirements of Fission Yeast Septins for Complex Formation, Localization, and Function. Mol. Biol. Cell
15: 5551-5564
[Abstract]
[Full Text]
-
Morrell, J. L., Nichols, C. B., Gould, K. L.
(2004). The GIN4 family kinase, Cdr2p, acts independently of septins in fission yeast. J. Cell Sci.
117: 5293-5302
[Abstract]
[Full Text]
-
Dekker, N., Speijer, D., Grun, C. H., van den Berg, M., de Haan, A., Hochstenbach, F.
(2004). Role of the {alpha}-Glucanase Agn1p in Fission-Yeast Cell Separation. Mol. Biol. Cell
15: 3903-3914
[Abstract]
[Full Text]
-
Dobbelaere, J., Barral, Y.
(2004). Spatial Coordination of Cytokinetic Events by Compartmentalization of the Cell Cortex. Science
305: 393-396
[Abstract]
[Full Text]
-
Venkatram, S., Tasto, J. J., Feoktistova, A., Jennings, J. L., Link, A. J., Gould, K. L.
(2004). Identification and Characterization of Two Novel Proteins Affecting Fission Yeast {gamma}-tubulin Complex Function. Mol. Biol. Cell
15: 2287-2301
[Abstract]
[Full Text]