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Aurora kinase A is essential for correct chromosome segregation in mouse zygote

Published online by Cambridge University Press:  15 July 2015

Veronika Kovarikova ,
Jan Burkus ,
Pavol Rehak ,
Adela Brzakova ,
Petr Solc  and
Vladimir Baran
Veronika Kovarikova
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, Kosice, Slovakia.
Jan Burkus
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, Kosice, Slovakia.
Pavol Rehak
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, Kosice, Slovakia.
Adela Brzakova
Affiliation:
Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Libechov, Czech Republic.
Petr Solc
Affiliation:
Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Libechov, Czech Republic.
Vladimir Baran*
Affiliation:
Institute of Animal Physiology, Slovak Academy of Sciences, Soltesovej 4, 040 01 Kosice, Slovakia.
*
All correspondence to: Vladimir Baran. Institute of Animal Physiology, Slovak Academy of Sciences, Soltesovej 4, 040 01 Kosice, Slovakia. E-mail: baran@saske.sk
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Summary

Aurora-A kinase (AURKA), a member of the serine/threonine protein kinase family, is involved in multiple steps of mitotic progression. It regulates centrosome maturation, mitotic spindle formation, and cytokinesis. While studied extensively in somatic cells, little information is known about AURKA in the early cleavage mouse embryo with respect to acentrosomal spindle assembly. In vitro experiments in which AURKA was inactivated with specific inhibitor MLN8237 during the early stages of embryogenesis documented gradual arrest in the cleavage ability of the mouse embryo. In the AURKA-inhibited 1-cell embryos, spindle formation and anaphase onset were delayed and chromosome segregation was defective. AURKA inhibition increased apoptosis during early embryonic development. In conclusion these data suggest that AURKA is essential for the correct chromosome segregation in the first mitosis as a prerequisite for normal later development after first cleavage.

Keywords

ApoptosisAurora AMLN8237Mouse zygoteSpindle
Type
Research Article
Information
Zygote , Volume 24 , Issue 3 , June 2016 , pp. 326 - 337
Copyright
Copyright © Cambridge University Press 2015 

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References

Asteriti, I.A., di Cesare, E., de Mattia, F., Hilsenstain, V., Neumann, B., Cundari, E., Lavia, P. & Guarguaglini, G. (2014). The Aurora-A inhibitor MLN8237 affects multiple mitotic processes and induces dose-dependent mitotic abnormalities and aneuploidy. Oncotarget 5, 6229–43.CrossRefGoogle ScholarPubMed
Baran, V., Solc, P., Kovarikova, V., Rehak, P., Sutovsky, P. (2013). Polo-like kinase 1 is essential for the first mitotic division in mouse embryo. Mol. Reprod. Dev. 80, 522–34.CrossRefGoogle ScholarPubMed
Barr, A.R. & Gergely, F. (2007). Aurora-A: the marker and breaker of spindle poles. J. Cell Sci. 120, 2987–96.CrossRefGoogle Scholar
Bruinsma, W., Macurek, L., Freire, R., Lindquist, A. & Medena, R.H. (2014). Bora and Aurora-A continue to activate PLK1 in mitosis. J. Cell Sci. 127, 801–11.Google ScholarPubMed
Cazales, M., Schmitt, E., Montembault, E., Dozier, C., Prigent, C. & Ducommun, B. (2005). CDC25B phosphorylation by Aurora-A occurs at the G2/M transition and is inhibited by DNA damage. Cell Cycle 9, 1233–8.CrossRefGoogle Scholar
Courtois, A., Schuh, M., Ellenberg, J. & Hiiragi, T. (2012). The translation from meiotic to mitotic spindle assembly is gradual during early mammalian development. J. Cell Biol. 198, 357–70.CrossRefGoogle Scholar
Cowley, D.O., Rivera-Pérez, J.A., Schliekelman, M., He, Y.J., Oliver, T.G., Lu, L., O'Quinn, R., Salmon, E.D., Magnuson, T. & Van Dyke, T. (2009) Aurora-A kinase is essential for bipolar spindle formation and early development. Mol. Cell Biol. 4, 1059–71.CrossRefGoogle Scholar
De Luca, M., Lavia, P. & Guarguaglini, G. (2006). A functional interplay between Aurora-A, PLK1 and TPX2 at spindle poles: PLK1 control centrosomal localization of Aurora-A and TPX2 spindle association. Cell Cycle 5, 296–303.CrossRefGoogle ScholarPubMed
Hadjantonakis, A.K. & Papaioannou, V. (2004) Dynamic in vivo imaging and cell tracking sing a histone fluorescent protein fusion in mice. BMC Biotechnol. 4, 33.CrossRefGoogle Scholar
Hannak, E., Kirkham, M., Hymann, A.A. & Oegema, K. (2011). Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans . J. Cell Biol. 155, 1109–16.CrossRefGoogle Scholar
Hirota, T., Kunitoku, N., Sasayama, T., Marumoto, T., Zhang, D., Nitta, M., Hatakeyama, K. & Saya, H. (2003). Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114, 585–98.CrossRefGoogle Scholar
Iannuccelli, E., Mompart, F., Gellin, J., Lahbib-Mansais, Y., Yerle, M. & Boudier, T. (2010). NEMO: a tool for analyzing gene and chromosome territory distribution from 3D-FISH experiments. Bioinformatics 26, 696–7.CrossRefGoogle Scholar
Kelly, K.R., Ecsedy, J., Medina, E., Mahalingam, D., Padmanabhan, S., Nawrocki, S.T., Giles, F.J. & Carew, J.S. (2011). The novel Aurora A kinase inhibitor MLN8237 is active in resistant chronic myeloid leukaemia and significantly increases the efficacy of nilotinib. J. Cell. Mol. Med. 15, 2057–70.CrossRefGoogle ScholarPubMed
Kitajima, T.S., Ohsugi, M. & Ellenberg, J. (2011). Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146, 568–81.CrossRefGoogle ScholarPubMed
Khodjakov, A. & Rieder, C.L. (1999). The sudden recruitment of γ-tubulin to the centrosomes at the onset of mitosis Exchange throughout the cell cycle, do not require microtubules. J. Cell Biol. 146, 585–96.CrossRefGoogle Scholar
Kufer, T.A., Silje, H.H., Korner, R., Gruss, O.J., Meraldi, P. & Nigg, E.A. (2002). Human TPX2 is required for targeting Aurora-A kinase to the spindle. J. Cell Biol. 158, 617–23.CrossRefGoogle ScholarPubMed
Lens, S.M.A., Voest, E.E. & Medena, R.H. (2010). Shared and separate functions of Polo-like kinases and Aurora kinases in cancer. Nature Rev. 10, 825–41.Google ScholarPubMed
Lu, L.Y., Wood, J.L, Ye, L., Minter-Dykhouse, K., Sauders, T.L., Yu, X. & Chen, J. (2008). Aurora-A is essential for early embryonic development and tumor suppression. J. Biol. Chem. 283, 31785–90.CrossRefGoogle ScholarPubMed
Macurek, L., Linquist, A., Lim, D., Lampson, M.A., Klompmaker, R., Freire, R., Clouin, C., Taylor, S.S., Yaffe, M.B. & Medena, R.H. (2008). Polo-like kinase-1 is activated by Aurora A to promote checkpoint recovery. Nature 455, 119–23.CrossRefGoogle Scholar
Manandhar, G., Schatten, H. & Sutovsky, P. (2005). Centrosome reduction during gametogenesis and its significance. Biol. Reprod. 72, 2–13.CrossRefGoogle ScholarPubMed
Manfredi, M.G., Ecsedy, J.A., Meetze, K.A., Blanai, S.K., Burenkova, O., Chen, W., Galvin, K.M., Hoar, K.M., Huck, J.J., LeRoy, P.J., Ray, E.T., Sells, T.B. et al. (2007). Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase. Proc. Natl. Acad. Sci. USA 104, 4106–11.CrossRefGoogle ScholarPubMed
Manfredi, M.G., Ecsedy, J.A., Chakravarty, A., Silverman, I., Zhang, M., Hoar, K.M., Stroud, S.G., Chen, W., Shide, V., et al. (2011). Characterization of Alisertib (MLN 8237), an investigational small-molecule inhibitor of Aurora-A kinase using novel in vivo pharmacodynamic assays. Clin. Cancer Res. 17, 7614–24.CrossRefGoogle ScholarPubMed
Marumoto, T., Honda, S., Hara, T., Nitta, M., Hirota, T., Kohmura, E. & Saya, H. (2003). Aurora-A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J. Biol. Chem. 278, 51786–95.CrossRefGoogle ScholarPubMed
Meraldi, P. & Nigg, E.A. (2002). The centrosome cycle. FEBS Lett. 521, 9–13.CrossRefGoogle ScholarPubMed
Michaelis, M., Selt, F., Rothweiler, F., Löschmann, N., Nüsse, B., Dirks, W.G., Zehner, R. & Cinatl, J. Jr. (2014). Aurora kinases as targets in drug-resistant neuroblastoma cells. PLoS One 9, e108758.CrossRefGoogle ScholarPubMed
Moser, J.J., Fritzler, M.J., Ou, Y. & Rattner, J.B. (2010). The PCM-basal body/primary cilium coalition. Semin. Cell Dev. Biol. 21, 148–55.CrossRefGoogle ScholarPubMed
Musacchio, A. & Salmon, ED. (2007) The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell. Biol. 5, 379–93.CrossRefGoogle Scholar
Qi, W., Cooke, L.S., Liu, X., Rimsza, L., Roe, D.J., Manziolli, A., Persky, D.O., Miller, T.P. & Mahadevan, D. (2011). Aurora inhibitor MLN8237 in combination with docetaxel enhances apoptosis and anti-tumor activity in mantle cell lymphoma. Biochem. Pharmacol. 81, 881–90.CrossRefGoogle ScholarPubMed
Saskova, A., Solc, P., Baran, V., Kubelka, V., Schultz, R.M. & Motlik, J. (2008). Aurora A controls meiosis I progression in mouse oocytes. Cell Cycle 7, 2368–76.CrossRefGoogle Scholar
Schindelin, J., Aranda-Carreras, I., Frise, E., Kaying, V., Longair, M., Pietzsch, T., Preibisch, S., Ruenden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D., Hartenstein, D.J., Eliceri, V., Tomancak, P. & Cardona, A. (2012). FiJi An open-source platform for biological-image analysis. Nat. Methods 9, 676–82.CrossRefGoogle ScholarPubMed
Schatten, G., Simerly, C. & Schatten, H. (1985). Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated mobility during mammalian fertilization. Proc. Natl. Acad. Sci. USA 82, 4152–6.CrossRefGoogle Scholar
Schatten, H. & Sun, Q-Y. (2009). The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol. Hum. Reprod. 15, 531–36.CrossRefGoogle ScholarPubMed
Schatten, H., Schatten, G., Mazia, D., Balczon, R. & Simerly, C. (1986). Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc. Natl. Acad. Sci. USA 83, 105–9.CrossRefGoogle ScholarPubMed
Schatten, H. & Sun, Q-Y. (2010). The role of centrosomes in fertilization, cell division and establishment of asymmetry during embryo development. Semin. Cell Dev. Biol. 21, 174–84.CrossRefGoogle ScholarPubMed
Schuh, M. & Ellenberg, J. (2007). Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130, 484–98.CrossRefGoogle ScholarPubMed
Seki, A., Coppinger, J.A., Jang, C.Y., Yates, J.R. & Fang, G. (2008). Bora and the kinase Aurora A cooperatively activate the kinase PLK1 and control mitotic entry. Science 320, 1655–8.CrossRefGoogle ScholarPubMed
Sikora-Polaczek, M., Hupalowka, A., Polanski, Z., Kubiak, J.Z. & Ciemerych, M.A. (2006). The first mitosis of the mouse embryo is prolonged by transitional metaphase arrest. Biol. Reprod. 74, 734–43.CrossRefGoogle ScholarPubMed
Solc, P., Saskova, A., Baran, V., Kubelka, M., Schultz, R.M. & Motlik, J. (2008). CDC25A phosphatase controls meiosis I progression in mouse oocytes. Dev. Biol. 317, 260–9.CrossRefGoogle ScholarPubMed
Solc, P., Baran, V., Mayer, A., Bohmova, T., Havlova-Panenkova, G., Saskova, A., Schultz, R.M. & Motlik, J. (2012). Aurora kinase A drives MTOC biogenesis but does not trigger resumption of meiosis in mouse oocytes maturated in vivo . Biol. Reprod. 87, 1–12.CrossRefGoogle Scholar
Solc, P., Kitajima, T.S., Yoshida, S., Brzakova, A., Kaido, M., Baran, V., Mayer, A., Samalova, P., Motlik, J. & Ellenberg, J. (2015). Multiple requirements of PLK1 during mouse oocyte maturation. PLoS One 10, e0116783.CrossRefGoogle ScholarPubMed
Sutovsky, P. & Schatten, G. (2000). Paternal contribution to the mammalian zygote fertilization after sperm-egg fusion. Int. Rev. Cytol. 195, 1–65.Google Scholar
Van Horn, R.D., Chu, S., Fan, L., Yin, T., Du, J., Beckmann, R., Mader, M., Zhu, G., Toth, J., Blanchard, K. & Ye, X.S. (2010). Cdk1 activity is required for mitotic activation of Aurora A during G2/M transition of human cells. J. Biol. Chem. 285, 21849–57.CrossRefGoogle Scholar
Wei, Y., Multi, S., Yang, C.R., Ma, J., Zhang, Q.H., Wang, Z.B., Li, M., Wei, L., Ge, Z.J., Zhang, C.H., Ouyang, Y.C., Hou, Y., Shatten, H. & Yuang, Q. (2011). Spindle assembly checkpoint regulates mitotic cell cycle progression during preimplantation embryo development. PLoS One 6, e21557.CrossRefGoogle ScholarPubMed
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 egg, and early embryos. Biol. Reprod. 70, 1392–9.CrossRefGoogle ScholarPubMed
Yoon, Y., Cowley, D., Gallant, J., Jones, S., van Dyke, T. & Rivera-Pérez, J.A. (2012). Conditional Aurora-A deficiency differentially affects early mouse embryo patterning. Dev. Biol. 371, 77–85.CrossRefGoogle ScholarPubMed
Zhou, N., Singh, K., Mir, M.C., Parker, Y., Lindner, D., Dreicer, R., Ecsedy, J.A., Zhang, Z., Teh, B.T., Almasan, A. & Hansel, D.E. (2013). The investigational Aurora kinase A inhibitor MLN8237 induces defects in cell viability and cell-cycle progression in malignant bladder cancer cells in vitro and in vivo . Clin. Cancer Res. 19, 1717–28.CrossRefGoogle ScholarPubMed
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