Sid2p, a Spindle Pole Body Kinase that Regulates the Onset of Cytokinesis

Correspondence to: Dannel McCollum, Department of Molecular Genetics and Microbiology, University of Massachusetts Medical School, 377 Plantation St., Worcester, MA 01605. Tel:(508) 856-8767 Fax:(508) 856-8774 E-mail:dannel.mccollum{at}umassmed.edu.

The fission yeast Schizosaccharomyces pombe divides by medial fission through the use of an actomyosin contractile ring. Precisely at the end of anaphase, the ring begins to constrict and the septum forms. Proper coordination of cell division with mitosis is crucial to ensure proper segregation of chromosomes to daughter cells. The Sid2p kinase is one of several proteins that function as part of a novel signaling pathway required for initiation of medial ring constriction and septation. Here, we show that Sid2p is a component of the spindle pole body at all stages of the cell cycle and localizes transiently to the cell division site during medial ring constriction and septation. A medial ring and an intact microtubule cytoskeleton are required for the localization of Sid2p to the division site. We have established an in vitro assay for measuring Sid2p kinase activity, and found that Sid2p kinase activity peaks during medial ring constriction and septation. Both Sid2p localization to the division site and activity depend on the function of all of the other septation initiation genes: cdc7, cdc11, cdc14, sid1, spg1, and sid4. Thus, Sid2p, a component of the spindle pole body, by virtue of its transient localization to the division site, appears to determine the timing of ring constriction and septum delivery in response to activating signals from other Sid gene products.

Key Words: sid2, cdc7, spg1, cytokinesis, Schizosaccharomyces pombe

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

• Yan, H., Ge, W., Chew, T. G., Chow, J. Y., McCollum, D., Neiman, A. M., Balasubramanian, M. K. (2008). The Meiosis-Specific Sid2p-related Protein Slk1p Regulates Forespore Membrane Assembly in Fission Yeast. Mol. Biol. Cell 19: 3676-3690 [Abstract] [Full Text]  
• Daga, R. R., Nurse, P. (2008). Interphase microtubule bundles use global cell shape to guide spindle alignment in fission yeast. J. Cell Sci. 121: 1973-1980 [Abstract] [Full Text]  
• Perez-Hidalgo, L., Rozalen, A. E., Martin-Castellanos, C., Moreno, S. (2008). Slk1 is a meiosis-specific Sid2-related kinase that coordinates meiotic nuclear division with growth of the forespore membrane. J. Cell Sci. 121: 1383-1392 [Abstract] [Full Text]  
• Ohtaka, A., Okuzaki, D., Nojima, H. (2008). Mug27 is a meiosis-specific protein kinase that functions in fission yeast meiosis II and sporulation. J. Cell Sci. 121: 1547-1558 [Abstract] [Full Text]  
• Dischinger, S., Krapp, A., Xie, L., Paulson, J. R., Simanis, V. (2008). Chemical genetic analysis of the regulatory role of Cdc2p in the S. pombe septation initiation network. J. Cell Sci. 121: 843-853 [Abstract] [Full Text]  
• Krapp, A., Collin, P., Cano del Rosario, E., Simanis, V. (2008). Homoeostasis between the GTPase Spg1p and its GAP in the regulation of cytokinesis in S. pombe. J. Cell Sci. 121: 601-608 [Abstract] [Full Text]  
• Vjestica, A., Tang, X.-Z., Oliferenko, S. (2008). The Actomyosin Ring Recruits Early Secretory Compartments to the Division Site in Fission Yeast. Mol. Biol. Cell 19: 1125-1138 [Abstract] [Full Text]  
• Yabuta, N., Okada, N., Ito, A., Hosomi, T., Nishihara, S., Sasayama, Y., Fujimori, A., Okuzaki, D., Zhao, H., Ikawa, M., Okabe, M., Nojima, H. (2007). Lats2 Is an Essential Mitotic Regulator Required for the Coordination of Cell Division. J. Biol. Chem. 282: 19259-19271 [Abstract] [Full Text]  
• Rosenberg, J. A., Tomlin, G. C., McDonald, W. H., Snydsman, B. E., Muller, E. G., Yates, J. R. III, Gould, K. L. (2006). Ppc89 Links Multiple Proteins, Including the Septation Initiation Network, to the Core of the Fission Yeast Spindle-Pole Body. Mol. Biol. Cell 17: 3793-3805 [Abstract] [Full Text]  
• Krapp, A., Collin, P., Cokoja, A., Dischinger, S., Cano, E., Simanis, V. (2006). The Schizosaccharomyces pombe septation initiation network (SIN) is required for spore formation in meiosis. J. Cell Sci. 119: 2882-2891 [Abstract] [Full Text]  
• Mehta, S., Gould, K. L. (2006). Identification of Functional Domains within the Septation Initiation Network Kinase, Cdc7. J. Biol. Chem. 281: 9935-9941 [Abstract] [Full Text]  
• Bimbo, A., Liu, J., Balasubramanian, M. K. (2005). Roles of Pdk1p, a Fission Yeast Protein Related to Phosphoinositide-dependent Protein Kinase, in the Regulation of Mitosis and Cytokinesis. Mol. Biol. Cell 16: 3162-3175 [Abstract] [Full Text]  
• Champion, A., Jouannic, S., Guillon, S., Mockaitis, K., Krapp, A., Picaud, A., Simanis, V., Kreis, M., Henry, Y. (2004). AtSGP1, AtSGP2 and MAP4K{alpha} are nucleolar plant proteins that can complement fission yeast mutants lacking a functional SIN pathway. J. Cell Sci. 117: 4265-4275 [Abstract] [Full Text]  
• Hou, M.-C., Guertin, D. A., McCollum, D. (2004). Initiation of Cytokinesis Is Controlled through Multiple Modes of Regulation of the Sid2p-Mob1p Kinase Complex. Mol. Cell. Biol. 24: 3262-3276 [Abstract] [Full Text]  
• Simanis, V. (2003). Events at the end of mitosis in the budding and fission yeasts. J. Cell Sci. 116: 4263-4275 [Abstract] [Full Text]  
• Hwa Lim, H., Yeong, F. M., Surana, U. (2003). Inactivation of Mitotic Kinase Triggers Translocation of MEN Components to Mother-Daughter Neck in Yeast. Mol. Biol. Cell 14: 4734-4743 [Abstract] [Full Text]  
• Jin, Q.-W., McCollum, D. (2003). Scw1p Antagonizes the Septation Initiation Network To Regulate Septum Formation and Cell Separation in the Fission Yeast Schizosaccharomyces pombe. Eukaryot Cell 2: 510-520 [Abstract] [Full Text]  
• Hou, M.-C., Wiley, D. J., Verde, F., McCollum, D. (2003). Mob2p interacts with the protein kinase Orb6p to promote coordination of cell polarity with cell cycle progression. J. Cell Sci. 116: 125-135 [Abstract] [Full Text]  
• Cid, V. J., Jimenez, J., Molina, M., Sanchez, M., Nombela, C., Thorner, J. W. (2002). Orchestrating the cell cycle in yeast: sequential localization of key mitotic regulators at the spindle pole and the bud neck. Microbiology 148: 2647-2659 [Full Text]  
• Karagiannis, J., Oulton, R., Young, P. G. (2002). The Scw1 RNA-Binding Domain Protein Regulates Septation and Cell-Wall Structure in Fission Yeast. Genetics 162: 45-58 [Abstract] [Full Text]  
• Guertin, D. A., Trautmann, S., McCollum, D. (2002). Cytokinesis in Eukaryotes. Microbiol. Mol. Biol. Rev. 66: 155-178 [Abstract] [Full Text]  
• Heitz, M. J., Petersen, J., Valovin, S., Hagan, I. M. (2002). MTOC formation during mitotic exit in fission yeast. J. Cell Sci. 114: 4521-4532 [Abstract] [Full Text]  
• Cueille, N., Salimova, E., Esteban, V., Blanco, M., Moreno, S., Bueno, A., Simanis, V. (2002). Flp1, a fission yeast orthologue of the S. cerevisiae CDC14 gene, is not required for cyclin degradation or rum1p stabilisation at the end of mitosis. J. Cell Sci. 114: 2649-2664 [Abstract] [Full Text]  
• Liu, J., Tang, X., Wang, H., Oliferenko, S., Balasubramanian, M. K. (2002). The Localization of the Integral Membrane Protein Cps1p to the Cell Division Site is Dependent on the Actomyosin Ring and the Septation-Inducing Network in Schizosaccharomyces pombe. Mol. Biol. Cell 13: 989-1000 [Abstract] [Full Text]  
• Arai, R., Mabuchi, I. (2002). F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 115: 887-898 [Abstract] [Full Text]  
• Mulvihill, D. P., Barretto, C., Hyams, J. S. (2001). Localization of Fission Yeast Type II Myosin, Myo2, to the Cytokinetic Actin Ring Is Regulated by Phosphorylation of a C-Terminal Coiled-Coil Domain and Requires a Functional Septation Initiation Network. Mol. Biol. Cell 12: 4044-4053 [Abstract] [Full Text]  
• Luca, F. C., Mody, M., Kurischko, C., Roof, D. M., Giddings, T. H., Winey, M. (2001). Saccharomyces cerevisiae Mob1p Is Required for Cytokinesis and Mitotic Exit. Mol. Cell. Biol. 21: 6972-6983 [Abstract] [Full Text]  
• Chang, L., Morrell, J. L., Feoktistova, A., Gould, K. L. (2001). Study of Cyclin Proteolysis in Anaphase-Promoting Complex (APC) Mutant Cells Reveals the Requirement for APC Function in the Final Steps of the Fission Yeast Septation Initiation Network. Mol. Cell. Biol. 21: 6681-6694 [Abstract] [Full Text]  
• Visintin, R., Amon, A. (2001). Regulation of the Mitotic Exit Protein Kinases Cdc15 and Dbf2. Mol. Biol. Cell 12: 2961-2974 [Abstract] [Full Text]  
• Jiang, W., Hallberg, R. L. (2001). Correct Regulation of the Septation Initiation Network in Schizosaccharomyces pombe Requires the Activities of par1 and par2. Genetics 158: 1413-1429 [Abstract] [Full Text]  
• Nanninga, N. (2001). Cytokinesis in Prokaryotes and Eukaryotes: Common Principles and Different Solutions. Microbiol. Mol. Biol. Rev. 65: 319-333 [Abstract] [Full Text]  
• Krishnan, R., Pangilinan, F., Lee, C., Spencer, F. (2000). Saccharomyces cerevisiae BUB2 Prevents Mitotic Exit in Response to Both Spindle and Kinetochore Damage. Genetics 156: 489-500 [Abstract] [Full Text]  
• Cullen, C. F., May, K. M., Hagan, I. M., Glover, D. M., Ohkura, H. (2000). A New Genetic Method for Isolating Functionally Interacting Genes: High plo1+-Dependent Mutants and Their Suppressors Define Genes in Mitotic and Septation Pathways in Fission Yeast. Genetics 155: 1521-1534 [Abstract] [Full Text]  
• Hirota, T., Morisaki, T., Nishiyama, Y., Marumoto, T., Tada, K., Hara, T., Masuko, N., Inagaki, M., Hatakeyama, K., Saya, H. (2000). Zyxin, a Regulator of Actin Filament Assembly, Targets the Mitotic Apparatus by Interacting with h-warts/LATS1 Tumor Suppressor. J. Cell Biol. 149: 1073-1086 [Abstract] [Full Text]  
• Chang, L., Gould, K. L. (2000). Sid4p is required to localize components of the septation initiation pathway to the spindle pole body in fission yeast. Proc. Natl. Acad. Sci. USA 97: 5249-5254 [Abstract] [Full Text]  
• Frenz, L., Lee, S., Fesquet, D, Johnston, L. (2000). The budding yeast Dbf2 protein kinase localises to the centrosome and moves to the bud neck in late mitosis. J. Cell Sci. 113: 3399-3408 [Abstract]  
• Balasubramanian, M., McCollum, D, Surana, U (2000). Tying the knot: linking cytokinesis to the nuclear cycle. J. Cell Sci. 113: 1503-1513 [Abstract]  
• Salimova, E, Sohrmann, M, Fournier, N, Simanis, V (2000). The S. pombe orthologue of the S. cerevisiae mob1 gene is essential and functions in signalling the onset of septum formation. J. Cell Sci. 113: 1695-1704 [Abstract]  
• Liu, J, Wang, H, Balasubramanian, M. (2000). A checkpoint that monitors cytokinesis in Schizosaccharomyces pombe. J. Cell Sci. 113: 1223-1230 [Abstract]  
• Tomlin, G. C., Morrell, J. L., Gould, K. L. (2002). The Spindle Pole Body Protein Cdc11p Links Sid4p to the Fission Yeast Septation Initiation Network. Mol. Biol. Cell 13: 1203-1214 [Abstract] [Full Text]  
• Wang, H., Tang, X., Liu, J., Trautmann, S., Balasundaram, D., McCollum, D., Balasubramanian, M. K. (2002). The Multiprotein Exocyst Complex Is Essential for Cell Separation in Schizosaccharomyces pombe. Mol. Biol. Cell 13: 515-529 [Abstract] [Full Text]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents