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PLK1 regulates spindle formation kinetics and APC/C activation in mouse zygote

Published online by Cambridge University Press:  15 July 2015

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

Polo-like kinase 1 (PLK1) is involved in essential events of cell cycle including mitosis in which it participates in centrosomal microtubule nucleation, spindle bipolarity establishment and cytokinesis. Although PLK1 function has been studied in cycling cancer cells, only limited data are known about its role in the first mitosis of mammalian zygotes. During the 1-cell stage of mouse embryo development, the acentriolar spindle is formed and the shift from acentriolar to centrosomal spindle formation progresses gradually throughout the preimplantation stage, thus providing a unique possibility to study acentriolar spindle formation. We have shown previously that PLK1 activity is not essential for entry into first mitosis, but is required for correct spindle formation and anaphase onset in 1-cell mouse embryos. In the present study, we extend this knowledge by employing quantitative confocal live cell imaging to determine spindle formation kinetics in the absence of PLK1 activity and answer the question whether metaphase arrest at PLK1-inhibited embryos is associated with low anaphase-promoting complex/cyclosome (APC/C) activity and consequently high securin level. We have shown that inhibition of PLK1 activity induces a delay in onset of acentriolar spindle formation during first mitosis. Although these PLK1-inhibited 1-cell embryos were finally able to form a bipolar spindle, not all chromosomes were aligned at the metaphase equator. PLK1-inhibited embryos were arrested in metaphase without any sign of APC/C activation with high securin levels. Our results document that PLK1 controls the onset of spindle assembly and spindle formation, and is essential for APC/C activation before anaphase onset in mouse zygotes.

Keywords

APC/CBI2536Live cell imagingMouse zygotePLK1SecurinSpindle assembly
Type
Research Article
Information
Zygote , Volume 24 , Issue 3 , June 2016 , pp. 338 - 345
Copyright
Copyright © Cambridge University Press 2015 

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References

Baran, V., Solc, P., Kovarikova, V., Rehak, P. & Sutovsky, P. (2013). Polo-like kinase 1 is essential for the first mitotic division in the mouse embryo. Mol. Reprod. Dev. 80, 522–34.CrossRefGoogle ScholarPubMed
Brennan, I.M., Peters, U., Kapoor, T.M. & Straight, A.F. (2007). Polo-like kinase controls vertebrate spindle elongation and cytokinesis. PLoS One 2, e409.CrossRefGoogle ScholarPubMed
Burkard, M.E., Randall, C.L., Larochelle, S., Zhang, C., Shokat, K.M., Fisher, R.P. & Jallepalli, P.V. (2007). Chemical genetics reveals the requirement for Polo-like kinase 1 activity in positioning RhoA and triggering cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 104, 4383–8.Google Scholar
Courtois, A., Schuh, M., Ellenberg, J. & Hiiragi, T. (2012). The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J. Cell. Biol. 198, 357–70.Google Scholar
Fan, H.Y., Tong, C., Teng, C.B., Lian, L., Li, S.W., Yang, Z.M., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2003). Characterization of polo-like kinase-1 in rat oocytes and early embryos implies its functional roles in the regulation of meiotic maturation, fertilization, and cleavage. Mol. Reprod. Dev. 65, 318–29.CrossRefGoogle ScholarPubMed
Foley, E.A. & Kapoor, T.M. (2013). Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14, 25–37.Google Scholar
Golan, A., Yudkovsky, Y. & Hershko, A. (2002). The cyclin-ubiquitin ligase activity of cyclosome/APC is jointly activated by protein kinases Cdk1-cyclin B and Plk. J. Biol. Chem. 277, 15552–7.CrossRefGoogle ScholarPubMed
Hanisch, A., Wehner, A., Nigg, E.A. & Sillje, H.H.W. (2006). Different PLK1 function show distinct dependencies on polo-box domain-mediated targeting. Mol. Biol. Cell 17, 448–59.Google Scholar
Hansen, D.V., Loktev, A.V., Ban, K.H. & Jackson, P.K. (2004). Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering CFbetaTrCP-dependent destruction of the APC Inhibitor Emi1. Mol. Biol. Cell 15, 5623–34.Google Scholar
Herbert, M., Levasseur, M., Homer, H., Yallop, K., Murdoch, A. & McDougall, A. (2003). Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat. Cell Biol. 5, 1023–5.Google Scholar
Howe, K. & FitzHarris, G. (2013). Recent insights into spindle function in mammalian oocytes and early embryos. Biol. Reprod. 89, 1–9.CrossRefGoogle ScholarPubMed
Kotani, S., Tugendreich, S., Fuji, M., Jorgensen, P.M., Watanabe, N., et al. (1998). PKA and MPF-activated polo-like kinase regulate anaphase-promoting complex activity and mitosis progression. Mol. Cell 1, 371–80.Google Scholar
Kraft, C., Herzog, F., Gieffers, C., Mechler, K., Hagting, A. et al. (2003). Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22, 6598–609.Google Scholar
Kudo, N.R., Anger, M., Peters, A.H., Stemmann, O., Theussl, H.C., Helmhart, W., Kudo, H., Heyting, C. & Nasmyth, K. (2009). Role of cleavage by separase of the Rec8 kleisin subunit of cohesin during mammalian meiosis I. J. Cell Sci. 122, 2686–98.Google Scholar
Lee, K. & Rhee, K. (2011). Plk1 phosphorylation of pericentrin initiates centrosome maturation at the onset of mitosis. J. Cell Biol. 195, 1093–101.Google Scholar
Lenart, P., Petronczki, M., Steegmaier, M., Di Fiore, B., Lipp, J.J., Hoffmann, M., Rettig, W.J., Kraut, N. & Peters, J.M. (2007). The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr. Biol. 17, 304–15.Google Scholar
Manandhar, G., Schatten, H. & Sutovsky, P. (2005). Centrosome reduction during gametogenesis and its significance. Biol. Reprod. 72, 2–13.Google Scholar
Meraldi, P. & Nigg, E.A. (2002). The centrosome cycle. FEBS Lett. 521, 9–13.Google Scholar
Moshe, Y., Boulaire, J., Pagano, M. & Hershko, A. (2004). Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome. Proc. Natl. Acad. Sci. USA 101, 7937–42.Google Scholar
Musacchio, A. & Salmon, E.D. (2007). The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379–93.Google Scholar
Sanhaji, M., Ritter, A., Belsham, H.R., Friel, C.T., Roth, S., Louwen, F. & Yuan, J. (2014). Polo-like kinase 1 regulates the stability of the mitotic centromere-associated kinesin in mitosis. Oncotarget 5, 3130–44.Google Scholar
Santamaria, A., Neef, R., Eberspacher, U., Eis, K., Husemann, M., Mumberg, D., Prechtl, S., Schulze, V., Siemeister, G., Wortmann, L., Barr, F.A. & Nigg, E.A. (2007). Use of the novel Plk1 inhibitor ZK thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis. Mol. Biol. Cell 18, 4024–36.CrossRefGoogle ScholarPubMed
Scutt, P.J., Chu, M.L., Sloane, D.A., Cherry, M., Bignell, C.R., Williams, D.H. & Eyers, P.A. (2009). Discovery and exploitation of inhibitor-resistant aurora and polo kinase mutants for the analysis of mitotic networks. J. Biol. Chem. 284, 15880–93.Google Scholar
Schatten, G., Simerly, C. & Schatten, H. (1985). Microtubule configuration 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, 531–6.CrossRefGoogle ScholarPubMed
Schindelin, J., Arganda-Carreras, I., Frise, E, Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C. Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–82.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.Google Scholar
Solc, P., Saskova, A., Baran, V., Kubelka, M., Schultz, R.M. & Motlik, J. (2008). CDC25A phosphatase control meiosis I progression in mouse oocytes. Dev. Biol. 317, 260–9.Google 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.Google Scholar
Steegmaier, M., Hoffmann, M., Baum, A., Lenart, P., Petronczki, M., Krssak, M., Gurtler, U., Garin-Chesa, P., Lieb, S., Quant, J., Grauert, M., Adolf, G.R., Kraut, N., Peters, J.M. & Rettig, W. (2007). BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo . Curr. Biol. 17, 316–22.Google Scholar
Sumara, I., Gimenez-Abian, J.F., Gerlich, D., Hirota, T., Kraft, C., de la Torre, C., Ellenberg, J. & Peters, J.M. (2004). Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr. Biol. 14, 1712–22.Google Scholar
Tong, C., Fan, H.Y., Li, S.W., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2002). Polo like kinase-1 is a pivotal regulator of microtubule assembly during mouse oocyte meiotic maturation, fertilization, and early embryonic mitosis. Biol. Reprod. 67, 546–54.Google 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.Google Scholar
Vanderheyden, V., Wakai, T., Bultynck, G., De Smedt, H., Parys, J.B. & Fissiore, R.A. (2009). Regulation of inositol 1,4,5-trisphosphate receptor type 1 function during oocyte maturation by MPM-2 phosphorylation. Cell Calcium 46, 56–64.Google Scholar
van Vugt, M.A., van de Weerdt, B.C., Vaderm, G., Janssen, H., Calafat, J., Klompmaker, R., Wolthuis, R.M. & Medema, R.H. (2004). Polo-like kinase-1 is required for bipolar spindle formation but is dispensable for anaphase promoting complex/Cdc20 activation and initiation of cytokinesis. J. Biol. Chem. 279, 36841–54.CrossRefGoogle ScholarPubMed
Zhang, Z., Su, W.H., Feng, C., Yu, D.H., Cui, C., Xu, X.Y. & Yu, B.Z. (2007). Polo like kinase 1 may regulate G2/M transition of mouse fertilized eggs by means of inhibiting the phosphorylation of Tyr 15 of Cdc2. Mol. Reprod. Dev. 74, 1247–54.Google Scholar
Zhao, Y., Ai, J., Zhang, H. & Zhu, G. (2010). Polo-like kinase-1 regulates first cleavage of 1-cell embryos in culture during assisted reproduction. Saudi Med. J. 31, 247–52.Google Scholar
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