This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Song, S.
Right arrow Articles by Lee, K. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Song, S.
Right arrow Articles by Lee, K. S.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, January 2000, p. 286-298, Vol. 20, No. 1
0270-7306/0/$04.00+0

Essential Function of the Polo Box of Cdc5 in Subcellular Localization and Induction of Cytokinetic Structures

Sukgil Song,1 Tallessyn Z. Grenfell,2 Susan Garfield,3 Raymond L. Erikson,2 and Kyung S. Lee1,*

Laboratory of Metabolism1 and Laboratory of Experimental Carcinogenesis,3 Division of Basic Sciences, National Cancer Institute, National Institutes of Health, Bethesda, Maryland 20892, and Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 021382

Received 2 August 1999/Returned for modification 9 September 1999/Accepted 4 October 1999

Members of the polo subfamily of protein kinases play pivotal roles in cell proliferation. In addition to the kinase domain, polo kinases have a strikingly conserved sequence in the noncatalytic C-terminal domain, termed the polo box. Here we show that the budding-yeast polo kinase Cdc5, when fused to green fluorescent protein and expressed under its endogenous promoter, localizes at spindle poles and the mother bud neck. Overexpression of Cdc5 can induce a class of cells with abnormally elongated buds in a polo box- and kinase activity-dependent manner. In addition to localizing at the spindle poles and cytokinetic neck filaments, Cdc5 induces and localizes to additional septin ring structures within the elongated buds. Without impairing kinase activity, conservative mutations in the polo box abolish the ability of Cdc5 to functionally complement the defect associated with a cdc5-1 temperature-sensitive mutation, to localize to the spindle poles and cytokinetic neck filaments, and to induce elongated cells with ectopic septin ring structures. Consistent with the polo box-dependent subcellular localization, the C-terminal domain of Cdc5, but not its polo box mutant, is sufficient for subcellular localization, and its overexpression appears to inhibit cytokinesis. These data provide evidence that the polo box is required to direct Cdc5 to specific subcellular locations and induce or organize cytokinetic structures.


* Corresponding author. Mailing address: Laboratory of Metabolism, Division of Basic Sciences, National Cancer Institute, National Institutes of Health, 9000 Rockville Pike, Bldg. 37, Rm. 3D25, Bethesda, MD 20892. Phone: (301) 435-8894. Fax: (301) 496-8419. E-mail: kyunglee{at}pop.nci.nih.gov.


Molecular and Cellular Biology, January 2000, p. 286-298, Vol. 20, No. 1
0270-7306/0/$04.00+0



This article has been cited by other articles:

  • Kishi, K., van Vugt, M. A. T. M., Okamoto, K.-i., Hayashi, Y., Yaffe, M. B. (2009). Functional Dynamics of Polo-Like Kinase 1 at the Centrosome. Mol. Cell. Biol. 29: 3134-3150 [Abstract] [Full Text]  
  • Schoffski, P. (2009). Polo-Like Kinase (PLK) Inhibitors in Preclinical and Early Clinical Development in Oncology. The Oncologist 14: 559-570 [Abstract] [Full Text]  
  • Asiedu, M., Wu, D., Matsumura, F., Wei, Q. (2008). Phosphorylation of MyoGEF on Thr-574 by Plk1 Promotes MyoGEF Localization to the Central Spindle. J. Biol. Chem. 283: 28392-28400 [Abstract] [Full Text]  
  • Sourirajan, A., Lichten, M. (2008). Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev. 22: 2627-2632 [Abstract] [Full Text]  
  • Umeyama, T., Wang, C. C. (2008). Polo-Like Kinase Is Expressed in S/G2/M Phase and Associated with the Flagellum Attachment Zone in both Procyclic and Bloodstream Forms of Trypanosoma brucei. Eukaryot Cell 7: 1582-1590 [Abstract] [Full Text]  
  • Seeburg, D. P., Sheng, M. (2008). Activity-Induced Polo-Like Kinase 2 Is Required for Homeostatic Plasticity of Hippocampal Neurons during Epileptiform Activity. J. Neurosci. 28: 6583-6591 [Abstract] [Full Text]  
  • Park, C. J., Park, J.-E., Karpova, T. S., Soung, N.-K., Yu, L.-R., Song, S., Lee, K. H., Xia, X., Kang, E., Dabanoglu, I., Oh, D.-Y., Zhang, J. Y., Kang, Y. H., Wincovitch, S., Huffaker, T. C., Veenstra, T. D., McNally, J. G., Lee, K. S. (2008). Requirement for the Budding Yeast Polo Kinase Cdc5 in Proper Microtubule Growth and Dynamics. Eukaryot Cell 7: 444-453 [Abstract] [Full Text]  
  • Haarer, B. K., Helfant, A. H., Nelson, S. A., Cooper, J. A., Amberg, D. C. (2007). Stable Preanaphase Spindle Positioning Requires Bud6p and an Apparent Interaction between the Spindle Pole Bodies and the Neck. Eukaryot Cell 6: 797-807 [Abstract] [Full Text]  
  • Rubenstein, E. M., Schmidt, M. C. (2007). Mechanisms Regulating the Protein Kinases of Saccharomyces cerevisiae. Eukaryot Cell 6: 571-583 [Full Text]  
  • Kumar, P., Wang, C. C. (2006). Dissociation of Cytokinesis Initiation from Mitotic Control in a Eukaryote. Eukaryot Cell 5: 92-102 [Abstract] [Full Text]  
  • Guan, R., Tapang, P., Leverson, J. D., Albert, D., Giranda, V. L., Luo, Y. (2005). Small Interfering RNA-Mediated Polo-Like Kinase 1 Depletion Preferentially Reduces the Survival of p53-Defective, Oncogenic Transformed Cells and Inhibits Tumor Growth in Animals. Cancer Res. 65: 2698-2704 [Abstract] [Full Text]  
  • van de Weerdt, B. C. M., van Vugt, M. A. T. M., Lindon, C., Kauw, J. J. W., Rozendaal, M. J., Klompmaker, R., Wolthuis, R. M. F., Medema, R. H. (2005). Uncoupling Anaphase-Promoting Complex/Cyclosome Activity from Spindle Assembly Checkpoint Control by Deregulating Polo-Like Kinase 1. Mol. Cell. Biol. 25: 2031-2044 [Abstract] [Full Text]  
  • Rapley, J., Baxter, J. E., Blot, J., Wattam, S. L., Casenghi, M., Meraldi, P., Nigg, E. A., Fry, A. M. (2005). Coordinate Regulation of the Mother Centriole Component Nlp by Nek2 and Plk1 Protein Kinases. Mol. Cell. Biol. 25: 1309-1324 [Abstract] [Full Text]  
  • Park, J.-E., Park, C. J., Sakchaisri, K., Karpova, T., Asano, S., McNally, J., Sunwoo, Y., Leem, S.-H., Lee, K. S. (2004). Novel Functional Dissection of the Localization-Specific Roles of Budding Yeast Polo Kinase Cdc5p. Mol. Cell. Biol. 24: 9873-9886 [Abstract] [Full Text]  
  • Liu, X., Zhou, T., Kuriyama, R., Erikson, R. L. (2004). Molecular interactions of Polo-like-kinase 1 with the mitotic kinesin-like protein CHO1/MKLP-1. J. Cell Sci. 117: 3233-3246 [Abstract] [Full Text]  
  • Ando, K., Ozaki, T., Yamamoto, H., Furuya, K., Hosoda, M., Hayashi, S., Fukuzawa, M., Nakagawara, A. (2004). Polo-like Kinase 1 (Plk1) Inhibits p53 Function by Physical Interaction and Phosphorylation. J. Biol. Chem. 279: 25549-25561 [Abstract] [Full Text]  
  • Liu, J., Lewellyn, A. L., Chen, L. G., Maller, J. L. (2004). The Polo Box Is Required for Multiple Functions of Plx1 in Mitosis. J. Biol. Chem. 279: 21367-21373 [Abstract] [Full Text]  
  • Park, C. J., Song, S., Giddings, T. H. Jr., Ro, H.-S., Sakchaisri, K., Park, J.-E., Seong, Y.-S., Winey, M., Lee, K. S. (2004). Requirement for Bbp1p in the Proper Mitotic Functions of Cdc5p in Saccharomyces cerevisiae. Mol. Biol. Cell 15: 1711-1723 [Abstract] [Full Text]  
  • Sakchaisri, K., Asano, S., Yu, L.-R., Shulewitz, M. J., Park, C. J., Park, J.-E., Cho, Y.-W., Veenstra, T. D., Thorner, J., Lee, K. S. (2004). Coupling morphogenesis to mitotic entry. Proc. Natl. Acad. Sci. USA 101: 4124-4129 [Abstract] [Full Text]  
  • Blank, M., Mandel, M., Keisari, Y., Meruelo, D., Lavie, G. (2003). Enhanced Ubiquitinylation of Heat Shock Protein 90 as a Potential Mechanism for Mitotic Cell Death in Cancer Cells Induced with Hypericin. Cancer Res. 63: 8241-8247 [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]  
  • Bachewich, C., Thomas, D. Y., Whiteway, M. (2003). Depletion of a Polo-like Kinase in Candida albicans Activates Cyclase-dependent Hyphal-like Growth. Mol. Biol. Cell 14: 2163-2180 [Abstract] [Full Text]  
  • Reynolds, N., Ohkura, H. (2003). Polo boxes form a single functional domain that mediates interactions with multiple proteins in fission yeast polo kinase. J. Cell Sci. 116: 1377-1387 [Abstract] [Full Text]  
  • Lee, P. R., Song, S., Ro, H.-S., Park, C. J., Lippincott, J., Li, R., Pringle, J. R., De Virgilio, C., Longtine, M. S., Lee, K. S. (2002). Bni5p, a Septin-Interacting Protein, Is Required for Normal Septin Function and Cytokinesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 6906-6920 [Abstract] [Full Text]  
  • McMillan, J. N., Theesfeld, C. L., Harrison, J. C., Bardes, E. S. G., Lew, D. J. (2002). Determinants of Swe1p Degradation in Saccharomyces cerevisiae. Mol. Biol. Cell 13: 3560-3575 [Abstract] [Full Text]  
  • Yarm, F. R. (2002). Plk Phosphorylation Regulates the Microtubule-Stabilizing Protein TCTP. Mol. Cell. Biol. 22: 6209-6221 [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]  
  • Seong, Y.-S., Kamijo, K., Lee, J.-S., Fernandez, E., Kuriyama, R., Miki, T., Lee, K. S. (2002). A Spindle Checkpoint Arrest and a Cytokinesis Failure by the Dominant-negative Polo-box Domain of Plk1 in U-2 OS Cells. J. Biol. Chem. 277: 32282-32293 [Abstract] [Full Text]  
  • Kaiser, B. K., Zimmerman, Z. A., Charbonneau, H., Jackson, P. K. (2002). Disruption of Centrosome Structure, Chromosome Segregation, and Cytokinesis by Misexpression of Human Cdc14A Phosphatase. Mol. Biol. Cell 13: 2289-2300 [Abstract] [Full Text]  
  • Guertin, D. A., Trautmann, S., McCollum, D. (2002). Cytokinesis in Eukaryotes. Microbiol. Mol. Biol. Rev. 66: 155-178 [Abstract] [Full Text]  
  • Wang, Q., Xie, S., Chen, J., Fukasawa, K., Naik, U., Traganos, F., Darzynkiewicz, Z., Jhanwar-Uniyal, M., Dai, W. (2002). Cell Cycle Arrest and Apoptosis Induced by Human Polo-Like Kinase 3 Is Mediated through Perturbation of Microtubule Integrity. Mol. Cell. Biol. 22: 3450-3459 [Abstract] [Full Text]  
  • Ro, H.-S., Song, S., Lee, K. S. (2002). Bfa1 can regulate Tem1 function independently of Bub2 in the mitotic exit network of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99: 5436-5441 [Abstract] [Full Text]  
  • Lee, S. E., Jensen, S., Frenz, L. M., Johnson, A. L., Fesquet, D., Johnston, L. H. (2002). The Bub2-dependent mitotic pathway in yeast acts every cell cycle and regulates cytokinesis. J. Cell Sci. 114: 2345-2354 [Abstract] [Full Text]  
  • Gale, C., Gerami-Nejad, M., McClellan, M., Vandoninck, S., Longtine, M. S., Berman, J. (2001). Candida albicans Int1p Interacts with the Septin Ring in Yeast and Hyphal Cells. Mol. Biol. Cell 12: 3538-3549 [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]  
  • Bartholomew, C. R., Woo, S. H., Chung, Y. S., Jones, C., Hardy, C. F. J. (2001). Cdc5 Interacts with the Wee1 Kinase in Budding Yeast. Mol. Cell. Biol. 21: 4949-4959 [Abstract] [Full Text]  
  • Mah, A. S., Jang, J., Deshaies, R. J. (2001). Protein kinase Cdc15 activates the Dbf2-Mob1 kinase complex. Proc. Natl. Acad. Sci. USA 10.1073/pnas.141098998v1 [Abstract] [Full Text]  
  • Cid, V. J., Shulewitz, M. J., McDonald, K. L., Thorner, J. (2001). Dynamic Localization of the Swe1 Regulator Hsl7 During the Saccharomyces cerevisiae Cell Cycle. Mol. Biol. Cell 12: 1645-1669 [Abstract] [Full Text]  
  • Asakawa, K., Yoshida, S., Otake, F., Toh-e, A. (2001). A Novel Functional Domain of Cdc15 Kinase Is Required for Its Interaction With Tem1 GTPase in Saccharomyces cerevisiae. Genetics 157: 1437-1450 [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]  
  • Jensen, S., Segal, M., Clarke, D. J., Reed, S. I. (2001). A Novel Role of the Budding Yeast Separin Esp1 in Anaphase Spindle Elongation: Evidence That Proper Spindle Association of Esp1 Is Regulated by Pds1. JCB 152: 27-40 [Abstract] [Full Text]  
  • Giet, R., Prigent, C. (2001). The non-catalytic domain of the Xenopus laevis auroraA kinase localises the protein to the centrosome. J. Cell Sci. 114: 2095-2104 [Abstract] [Full Text]  
  • Balasubramanian, M., McCollum, D, Surana, U (2000). Tying the knot: linking cytokinesis to the nuclear cycle. J. Cell Sci. 113: 1503-1513 [Abstract]  
  • Mah, A. S., Jang, J., Deshaies, R. J. (2001). Protein kinase Cdc15 activates the Dbf2-Mob1 kinase complex. Proc. Natl. Acad. Sci. USA 98: 7325-7330 [Abstract] [Full Text]