J. Cell Biol., Volume 143, Number 6, December 14, 1998 1635-1646

AIR-2: An Aurora/Ipl1-related Protein Kinase Associated with Chromosomes and Midbody Microtubules Is Required for Polar Body Extrusion and Cytokinesis in Caenorhabditis elegans Embryos

Jill M. Schumacher,^* Andy Golden, and Peter J. Donovan^*

^* Cell Biology of Development and Differentiation Group and  Developmental Signal Transduction Group, ABL-Basic Research Program, NCI-Frederick Cancer Research and Development Center, Frederick, Maryland 21702

An emerging family of kinases related to the Drosophila Aurora and budding yeast Ipl1 proteins has been implicated in chromosome segregation and mitotic spindle formation in a number of organisms. Unlike other Aurora/Ipl1-related kinases, the Caenorhabditis elegans orthologue, AIR-2, is associated with meiotic and mitotic chromosomes. AIR-2 is initially localized to the chromosomes of the most mature prophase I-arrested oocyte residing next to the spermatheca. This localization is dependent on the presence of sperm in the spermatheca. After fertilization, AIR-2 remains associated with chromosomes during each meiotic division. However, during both meiotic anaphases, AIR-2 is present between the separating chromosomes. AIR-2 also remains associated with both extruded polar bodies. In the embryo, AIR-2 is found on metaphase chromosomes, moves to midbody microtubules at anaphase, and then persists at the cytokinesis remnant. Disruption of AIR-2 expression by RNA- mediated interference produces entire broods of one-cell embryos that have executed multiple cell cycles in the complete absence of cytokinesis. The embryos accumulate large amounts of DNA and microtubule asters. Polar bodies are not extruded, but remain in the embryo where they continue to replicate. The cytokinesis defect appears to be late in the cell cycle because transient cleavage furrows initiate at the proper location, but regress before the division is complete. Additionally, staining with a marker of midbody microtubules revealed that at least some of the components of the midbody are not well localized in the absence of AIR-2 activity. Our results suggest that during each meiotic and mitotic division, AIR-2 may coordinate the congression of metaphase chromosomes with the subsequent events of polar body extrusion and cytokinesis.

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

This article has been cited by other articles:

• Govindan, J. A., Nadarajan, S., Kim, S., Starich, T. A., Greenstein, D. (2009). Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans. Development 136: 2211-2221 [Abstract] [Full Text]  
• Martinez-Perez, E., Schvarzstein, M., Barroso, C., Lightfoot, J., Dernburg, A. F., Villeneuve, A. M. (2008). Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 22: 2886-2901 [Abstract] [Full Text]  
• Fu, D.-H., Jiang, W., Zheng, J.-T., Zhao, G.-Y., Li, Y., Yi, H., Li, Z.-R., Jiang, J.-D., Yang, K.-Q., Wang, Y., Si, S.-Y. (2008). Jadomycin B, an Aurora-B kinase inhibitor discovered through virtual screening. Molecular Cancer Therapeutics 7: 2386-2393 [Abstract] [Full Text]  
• Yamamoto, T. M., Lewellyn, A. L., Maller, J. L. (2008). Regulation of the Aurora B Chromosome Passenger Protein Complex during Oocyte Maturation in Xenopus laevis. Mol. Cell. Biol. 28: 4196-4203 [Abstract] [Full Text]  
• Riefler, G. M., Dent, S. Y. R., Schumacher, J. M. (2008). Tousled-mediated Activation of Aurora B Kinase Does Not Require Tousled Kinase Activity in Vivo. J. Biol. Chem. 283: 12763-12768 [Abstract] [Full Text]  
• Li, H., Chen, Q., Kaller, M., Nellen, W., Graf, R., De Lozanne, A. (2008). Dictyostelium Aurora Kinase Has Properties of both Aurora A and Aurora B Kinases. Eukaryot Cell 7: 894-905 [Abstract] [Full Text]  
• Sun, L., Hodeify, R., Haun, S., Charlesworth, A., MacNicol, A. M., Ponnappan, S., Ponnappan, U., Prigent, C., Machaca, K. (2008). Ca2+ Homeostasis Regulates Xenopus Oocyte Maturation. Biol. Reprod. 78: 726-735 [Abstract] [Full Text]  
• Lee, M.-H., Ohmachi, M., Arur, S., Nayak, S., Francis, R., Church, D., Lambie, E., Schedl, T. (2007). Multiple Functions and Dynamic Activation of MPK-1 Extracellular Signal-Regulated Kinase Signaling in Caenorhabditis elegans Germline Development. Genetics 177: 2039-2062 [Abstract] [Full Text]  
• Verbrugghe, K. J. C., White, J. G. (2007). Cortical centralspindlin and G{alpha} have parallel roles in furrow initiation in early C. elegans embryos. J. Cell Sci. 120: 1772-1778 [Abstract] [Full Text]  
• Sakita-Suto, S., Kanda, A., Suzuki, F., Sato, S., Takata, T., Tatsuka, M. (2007). Aurora-B Regulates RNA Methyltransferase NSUN2. Mol. Biol. Cell 18: 1107-1117 [Abstract] [Full Text]  
• Fu, J., Bian, M., Jiang, Q., Zhang, C. (2007). Roles of Aurora Kinases in Mitosis and Tumorigenesis. Mol Cancer Res 5: 1-10 [Abstract] [Full Text]  
• Li, Z., Wang, C. C. (2006). Changing Roles of Aurora-B Kinase in Two Life Cycle Stages of Trypanosoma brucei.. Eukaryot Cell 5: 1026-1035 [Abstract] [Full Text]  
• Klein, U. R., Nigg, E. A., Gruneberg, U. (2006). Centromere Targeting of the Chromosomal Passenger Complex Requires a Ternary Subcomplex of Borealin, Survivin, and the N-Terminal Domain of INCENP. Mol. Biol. Cell 17: 2547-2558 [Abstract] [Full Text]  
• Chang, C.-J., Goulding, S., Adams, R. R., Earnshaw, W. C., Carmena, M. (2006). Drosophila Incenp is required for cytokinesis and asymmetric cell division during development of the nervous system. J. Cell Sci. 119: 1144-1153 [Abstract] [Full Text]  
• Burrows, A. E., Sceurman, B. K., Kosinski, M. E., Richie, C. T., Sadler, P. L., Schumacher, J. M., Golden, A. (2006). The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133: 697-709 [Abstract] [Full Text]  
• Stewart, S., Fang, G. (2005). Destruction Box-Dependent Degradation of Aurora B Is Mediated by the Anaphase-Promoting Complex/Cyclosome and Cdh1. Cancer Res. 65: 8730-8735 [Abstract] [Full Text]  
• Pielak, R. M., Hawkins, C., Pyie, A., Bautista, J., Lee, K.-G., Cohen, W. D. (2005). Polar Body Formation in Spisula Oocytes: Function of the Peripheral Aster. Biol. Bull. 209: 21-30 [Abstract] [Full Text]  
• Gatt, M. K., Savoian, M. S., Riparbelli, M. G., Massarelli, C., Callaini, G., Glover, D. M. (2005). Klp67A destabilises pre-anaphase microtubules but subsequently is required to stabilise the central spindle. J. Cell Sci. 118: 2671-2682 [Abstract] [Full Text]  
• Yan, X., Cao, L., Li, Q., Wu, Y., Zhang, H., Saiyin, H., Liu, X., Zhang, X., Shi, Q., Yu, L. (2005). Aurora C is directly associated with Survivin and required for cytokinesis. GENES CELLS 10: 617-626 [Abstract] [Full Text]  
• D'Avino, P. P., Savoian, M. S., Glover, D. M. (2005). Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J. Cell Sci. 118: 1549-1558 [Abstract] [Full Text]  
• Glotzer, M. (2005). The Molecular Requirements for Cytokinesis. Science 307: 1735-1739 [Abstract] [Full Text]  
• Gadea, B. B., Ruderman, J. V. (2005). Aurora Kinase Inhibitor ZM447439 Blocks Chromosome-induced Spindle Assembly, the Completion of Chromosome Condensation, and the Establishment of the Spindle Integrity Checkpoint in Xenopus Egg Extracts. Mol. Biol. Cell 16: 1305-1318 [Abstract] [Full Text]  
• Nabeshima, K., Villeneuve, A. M., Colaiacovo, M. P. (2005). Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. JCB 168: 683-689 [Abstract] [Full Text]  
• Bishop, J. D., Han, Z., Schumacher, J. M. (2005). The Caenorhabditis elegans Aurora B Kinase AIR-2 Phosphorylates and Is Required for the Localization of a BimC Kinesin to Meiotic and Mitotic Spindles. Mol. Biol. Cell 16: 742-756 [Abstract] [Full Text]  
• Scrittori, L., Skoufias, D. A., Hans, F., Gerson, V., Sassone-Corsi, P., Dimitrov, S., Margolis, R. L. (2005). A Small C-Terminal Sequence of Aurora B Is Responsible for Localization and Function. Mol. Biol. Cell 16: 292-305 [Abstract] [Full Text]  
• Kachur, T., Ao, W., Berger, J., Pilgrim, D. (2004). Maternal UNC-45 is involved in cytokinesis and colocalizes with non-muscle myosin in the early Caenorhabditis elegans embryo. J. Cell Sci. 117: 5313-5321 [Abstract] [Full Text]  
• Gruneberg, U., Neef, R., Honda, R., Nigg, E. A., Barr, F. A. (2004). Relocation of Aurora B from centromeres to the central spindle at the metaphase to anaphase transition requires MKlp2. JCB 166: 167-172 [Abstract] [Full Text]  
• Yao, L.-J., Zhong, Z.-S., Zhang, L.-S., Chen, D.-Y., Schatten, H., Sun, Q.-Y. (2004). Aurora-A Is a Critical Regulator of Microtubule Assembly and Nuclear Activity in Mouse Oocytes, Fertilized Eggs, and Early Embryos. Biol. Reprod. 70: 1392-1399 [Abstract] [Full Text]  
• Alsop, G. B., Zhang, D. (2004). Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes. J. Cell Sci. 117: 1591-1602 [Abstract] [Full Text]  
• Glotzer, M. (2004). Cleavage furrow positioning. JCB 164: 347-351 [Abstract] [Full Text]  
• Tien, A.-C., Lin, M.-H., Su, L.-J., Hong, Y.-R., Cheng, T.-S., Lee, Y.-C. G., Lin, W.-J., Still, I. H., Huang, C.-Y. F. (2004). Identification of the Substrates and Interaction Proteins of Aurora Kinases from a Protein-Protein Interaction Model. Mol. Cell. Proteomics 3: 93-104 [Abstract] [Full Text]  
• Saint, R., Somers, W. G. (2003). Animal cell division: a fellowship of the double ring?. J. Cell Sci. 116: 4277-4281 [Abstract] [Full Text]  
• Prigent, C., Dimitrov, S. (2003). Phosphorylation of serine 10 in histone H3, what for?. J. Cell Sci. 116: 3677-3685 [Abstract] [Full Text]  
• Neef, R., Preisinger, C., Sutcliffe, J., Kopajtich, R., Nigg, E. A., Mayer, T. U., Barr, F. A. (2003). Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. JCB 162: 863-876 [Abstract] [Full Text]  
• Carvalho, A., Carmena, M., Sambade, C., Earnshaw, W. C., Wheatley, S. P. (2003). Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J. Cell Sci. 116: 2987-2998 [Abstract] [Full Text]  
• Warner, S. L., Bearss, D. J., Han, H., Von Hoff, D. D. (2003). Targeting Aurora-2 Kinase in Cancer. Molecular Cancer Therapeutics 2: 589-595 [Abstract] [Full Text]  
• Ono, K., Parast, M., Alberico, C., Benian, G. M., Ono, S. (2003). Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J. Cell Sci. 116: 2073-2085 [Abstract] [Full Text]  
• Romano, A., Guse, A., Krascenicova, I., Schnabel, H., Schnabel, R., Glotzer, M. (2003). CSC-1: a subunit of the aurora b kinase complex that binds to the survivin-like protein BIR-1 and the incenp-like protein ICP-1. JCB 161: 229-236 [Abstract] [Full Text]  
• Kawajiri, A., Yasui, Y., Goto, H., Tatsuka, M., Takahashi, M., Nagata, K.-i., Inagaki, M. (2003). Functional Significance of the Specific Sites Phosphorylated in Desmin at Cleavage Furrow: Aurora-B May Phosphorylate and Regulate Type III Intermediate Filaments during Cytokinesis Coordinatedly with Rho-kinase. Mol. Biol. Cell 14: 1489-1500 [Abstract] [Full Text]  
• Parra, M. T., Viera, A., Gomez, R., Page, J., Carmena, M., Earnshaw, W. C., Rufas, J. S., Suja, J. A. (2003). Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis. J. Cell Sci. 116: 961-974 [Abstract] [Full Text]  
• Ma, C., Cummings, C., Liu, X. J. (2003). Biphasic Activation of Aurora-A Kinase during the Meiosis I- Meiosis II Transition in Xenopus Oocytes. Mol. Cell. Biol. 23: 1703-1716 [Abstract] [Full Text]  
• Goto, H., Yasui, Y., Kawajiri, A., Nigg, E. A., Terada, Y., Tatsuka, M., Nagata, K.-i., Inagaki, M. (2003). Aurora-B Regulates the Cleavage Furrow-specific Vimentin Phosphorylation in the Cytokinetic Process. J. Biol. Chem. 278: 8526-8530 [Abstract] [Full Text]  
• Buvelot, S., Tatsutani, S. Y., Vermaak, D., Biggins, S. (2003). The budding yeast Ipl1/Aurora protein kinase regulates mitotic spindle disassembly. JCB 160: 329-339 [Abstract] [Full Text]  
• Castro, A., Mandart, E., Lorca, T., Galas, S. (2003). Involvement of Aurora A Kinase during Meiosis I-II Transition in Xenopus Oocytes. J. Biol. Chem. 278: 2236-2241 [Abstract] [Full Text]  
• Kuwabara, P. E. (2003). The multifaceted C. elegans major sperm protein: an ephrin signaling antagonist in oocyte maturation. Genes Dev. 17: 155-161 [Full Text]  
• Chen, J., Jin, S., Tahir, S. K., Zhang, H., Liu, X., Sarthy, A. V., McGonigal, T. P., Liu, Z., Rosenberg, S. H., Ng, S.-C. (2003). Survivin Enhances Aurora-B Kinase Activity and Localizes Aurora-B in Human Cells. J. Biol. Chem. 278: 486-490 [Abstract] [Full Text]  
• Cheetham, G. M. T., Knegtel, R. M. A., Coll, J. T., Renwick, S. B., Swenson, L., Weber, P., Lippke, J. A., Austen, D. A. (2002). Crystal Structure of Aurora-2, an Oncogenic Serine/Threonine Kinase. J. Biol. Chem. 277: 42419-42422 [Abstract] [Full Text]  
• Murata-Hori, M., Wang, Y.-l. (2002). Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. JCB 159: 45-53 [Abstract] [Full Text]  
• Ota, T., Suto, S., Katayama, H., Han, Z.-B., Suzuki, F., Maeda, M., Tanino, M., Terada, Y., Tatsuka, M. (2002). Increased Mitotic Phosphorylation of Histone H3 Attributable to AIM-1/Aurora-B Overexpression Contributes to Chromosome Number Instability. Cancer Res. 62: 5168-5177 [Abstract] [Full Text]  
• Gruneberg, U., Glotzer, M., Gartner, A., Nigg, E. A. (2002). The CeCDC-14 phosphatase is required for cytokinesis in the Caenorhabditis elegans embryo. JCB 158: 901-914 [Abstract] [Full Text]  
• Bolton, M. A., Lan, W., Powers, S. E., McCleland, M. L., Kuang, J., Stukenberg, P. T. (2002). Aurora B Kinase Exists in a Complex with Survivin and INCENP and Its Kinase Activity Is Stimulated by Survivin Binding and Phosphorylation. Mol. Biol. Cell 13: 3064-3077 [Abstract] [Full Text]  
• Bishop, J. D., Schumacher, J. M. (2002). Phosphorylation of the Carboxyl Terminus of Inner Centromere Protein (INCENP) by the Aurora B Kinase Stimulates Aurora B Kinase Activity. J. Biol. Chem. 277: 27577-27580 [Abstract] [Full Text]  
• Guertin, D. A., Trautmann, S., McCollum, D. (2002). Cytokinesis in Eukaryotes. Microbiol. Mol. Biol. Rev. 66: 155-178 [Abstract] [Full Text]  
• Rogers, E., Bishop, J. D., Waddle, J. A., Schumacher, J. M., Lin, R. (2002). The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. JCB 157: 219-229 [Abstract] [Full Text]  
• Hagstrom, K. A., Holmes, V. F., Cozzarelli, N. R., Meyer, B. J. (2002). C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 16: 729-742 [Abstract] [Full Text]  
• Tanaka, M., Ueda, A., Kanamori, H., Ideguchi, H., Yang, J., Kitajima, S., Ishigatsubo, Y. (2002). Cell-cycle-dependent Regulation of Human aurora A Transcription Is Mediated by Periodic Repression of E4TF1. J. Biol. Chem. 277: 10719-10726 [Abstract] [Full Text]  
• Petersen, J., Paris, J., Willer, M., Philippe, M., Hagan, I. M. (2002). The S. pombe aurora-related kinase Ark1 associates with mitotic structures in a stage dependent manner and is required for chromosome segregation. J. Cell Sci. 114: 4371-4384 [Abstract] [Full Text]  
• Kuriyama, R., Gustus, C., Terada, Y., Uetake, Y., Matuliene, J. (2002). CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis. JCB 156: 783-790 [Abstract] [Full Text]  
• Crosio, C., Fimia, G. M., Loury, R., Kimura, M., Okano, Y., Zhou, H., Sen, S., Allis, C. D., Sassone-Corsi, P. (2002). Mitotic Phosphorylation of Histone H3: Spatio-Temporal Regulation by Mammalian Aurora Kinases. Mol. Cell. Biol. 22: 874-885 [Abstract] [Full Text]  
• Dernburg, A. F. (2001). Here, There, and Everywhere: Kinetochore Function on Holocentric Chromosomes. JCB 153: F33-F38 [Abstract] [Full Text]  
• Adams, R. R., Maiato, H., Earnshaw, W. C., Carmena, M. (2001). Essential Roles of Drosophila Inner Centromere Protein (INCENP) and Aurora B in Histone H3 Phosphorylation, Metaphase Chromosome Alignment, Kinetochore Disjunction, and Chromosome Segregation. JCB 153: 865-880 [Abstract] [Full Text]  
• Giet, R., Glover, D. M. (2001). Drosophila Aurora B Kinase Is Required for Histone H3 Phosphorylation and Condensin Recruitment during Chromosome Condensation and to Organize the Central Spindle during Cytokinesis. JCB 152: 669-682 [Abstract] [Full Text]  
• Kawasaki, A., Matsumura, I., Miyagawa, J.-i., Ezoe, S., Tanaka, H., Terada, Y., Tatsuka, M., Machii, T., Miyazaki, H., Furukawa, Y., Kanakura, Y. (2001). Downregulation of an AIM-1 Kinase Couples with Megakaryocytic Polyploidization of Human Hematopoietic Cells. JCB 152: 275-288 [Abstract] [Full Text]  
• Golden, A., Sadler, P. L., Wallenfang, M. R., Schumacher, J. M., Hamill, D. R., Bates, G., Bowerman, B., Seydoux, G., Shakes, D. C. (2000). Metaphase to Anaphase (mat) Transition-defective Mutants in Caenorhabditis elegans. JCB 151: 1469-1482 [Abstract] [Full Text]  
• Jantsch-Plunger, V., Gonczy, P., Romano, A., Schnabel, H., Hamill, D., Schnabel, R., Hyman, A. A., Glotzer, M. (2000). CYK-4: A Rho Family GTPase Activating Protein (GAP) Required for Central Spindle Formation and Cytokinesis. JCB 149: 1391-1404 [Abstract] [Full Text]  
• Frank-Vaillant, M, Haccard, O, Thibier, C, Ozon, R, Arlot-Bonnemains, Y, Prigent, C, Jessus, C (2000). Progesterone regulates the accumulation and the activation of Eg2 kinase in Xenopus oocytes. J. Cell Sci. 113: 1127-1138 [Abstract]  
• Shelton, C. A., Carter, J. C., Ellis, G. C., Bowerman, B. (1999). The Nonmuscle Myosin Regulatory Light Chain Gene mlc-4 Is Required for Cytokinesis, Anterior-Posterior Polarity, and Body Morphology during Caenorhabditis elegans Embryogenesis. JCB 146: 439-452 [Abstract] [Full Text]  
• Kim, J.-h., Kang, J.-s., Chan, C. S.M. (1999). Sli15 Associates with the Ipl1 Protein Kinase to Promote Proper Chromosome Segregation in Saccharomyces cerevisiae. JCB 145: 1381-1394 [Abstract] [Full Text]  
• Giet, R, Prigent, C (1999). Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases. J. Cell Sci. 112: 3591-3601 [Abstract]  
• Pan, J., Snell, W. J. (2000). Regulated Targeting of a Protein Kinase into an Intact Flagellum. AN AURORA/Ipl1p-LIKE PROTEIN KINASE TRANSLOCATES FROM THE CELL BODY INTO THE FLAGELLA DURING GAMETE ACTIVATION IN CHLAMYDOMONAS. J. Biol. Chem. 275: 24106-24114 [Abstract] [Full Text]  
• Murnion, M. E., Adams, R. R., Callister, D. M., Allis, C. D., Earnshaw, W. C., Swedlow, J. R. (2001). Chromatin-associated Protein Phosphatase 1 Regulates Aurora-B and Histone H3 Phosphorylation. J. Biol. Chem. 276: 26656-26665 [Abstract] [Full Text]  
• Zeitlin, S. G., Shelby, R. D., Sullivan, K. F. (2001). CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. JCB 155: 1147-1158 [Abstract] [Full Text]  
• Kuriyama, R., Gustus, C., Terada, Y., Uetake, Y., Matuliene, J. (2002). CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis. JCB 156: 783-790 [Abstract] [Full Text]  
• Rogers, E., Bishop, J. D., Waddle, J. A., Schumacher, J. M., Lin, R. (2002). The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. JCB 157: 219-229 [Abstract] [Full Text]  
• Leverson, J. D., Huang, H.-k., Forsburg, S. L., Hunter, T. (2002). The Schizosaccharomyces pombe Aurora-related Kinase Ark1 Interacts with the Inner Centromere Protein Pic1 and Mediates Chromosome Segregation and Cytokinesis. Mol. Biol. Cell 13: 1132-1143 [Abstract] [Full Text]  
• Murata-Hori, M., Tatsuka, M., Wang, Y.-L. (2002). Probing the Dynamics and Functions of Aurora B Kinase in Living Cells during Mitosis and Cytokinesis. Mol. Biol. Cell 13: 1099-1108 [Abstract] [Full Text]  

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