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Clathrin Heavy Chain 1 is Required for Spindle Assembly and Chromosome Congression in Mouse Oocytes

Published online by Cambridge University Press:  02 July 2013

Jie Zhao
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Lu Wang
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Hong-Xia Zhou
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Li Liu
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Angeleem Lu
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Guang-Peng Li
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Heide Schatten
Affiliation:
Department of Veterinary Pathobiology, University of Missouri, Columbia, MO 65211, USA
Cheng-Guang Liang
Affiliation:
The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot, Inner Mongolia 010070, People's Republic of China
Corresponding
E-mail address:

Abstract

Clathrin heavy chain 1 (CLTC) has been considered a “moonlighting protein” which acts in membrane trafficking during interphase and in stabilizing spindle fibers during mitosis. However, its roles in meiosis, especially in mammalian oocyte maturation, remain unclear. This study investigated CLTC expression and function in spindle formation and chromosome congression during mouse oocyte meiotic maturation. Our results showed that the expression level of CLTC increased after germinal vesicle breakdown (GVBD) and peaked in the M phase. Immunostaining results showed CLTC distribution throughout the cytoplasm in a cell cycle-dependent manner. Appearance and disappearance of CLTC along with β-tubulin (TUBB) could be observed during spindle dynamic changes. To explore the relationship between CLTC and microtubule dynamics, oocytes at metaphase were treated with taxol or nocodazole. CLTC colocalized with TUBB at the enlarged spindle and with cytoplasmic asters after taxol treatment; it disassembled and distributed into the cytoplasm along with TUBB after nocodazole treatment. Disruption of CLTC function using stealth siRNA caused a decreased first polar body extrusion rate and extensive spindle formation and chromosome congression defects. Taken together, these results show that CLTC plays an important role in spindle assembly and chromosome congression through a microtubule correlation mechanism during mouse oocyte maturation.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2013 

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References

Booth, D.G., Hood, F.E., Prior, I.A. & Royle, S.J. (2011). A TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J 30(5), 906919.CrossRefGoogle ScholarPubMed
Calarco, P.G. (2000). Centrosome precursors in the acentriolar mouse oocyte. Microsc Res Tech 49(5), 428434.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Calarco, P.G. (2005). The role of microfilaments in early meiotic maturation of mouse oocytes. Microsc Microanal 11(2), 146153.CrossRefGoogle ScholarPubMed
Eichenlaub-Ritter, U. & Boll, I. (1989). Age-related non-disjunction, spindle formation and progression through maturation of mammalian oocytes. Prog Clin Biol Res 318, 259269.Google ScholarPubMed
Fielding, A.B. & Royle, S.J. (2013). Mitotic inhibition of clathrin-mediated endocytosis. Cell Mol Life Sci, doi:10.1007/s00018-1250-8.CrossRefGoogle ScholarPubMed
Fotin, A., Cheng, Y., Sliz, P., Grigorieff, N., Harrison, S.C., Kirchhausen, T. & Walz, T. (2004). Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432(7017), 573579.CrossRefGoogle ScholarPubMed
Fu, W., Tao, W., Zheng, P., Fu, J., Bian, M., Jiang, Q., Clarke, P.R. & Zhang, C. (2010). Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J Cell Sci 123(Pt 21), 36453651.CrossRefGoogle ScholarPubMed
Gergely, F., Draviam, V.M. & Raff, J.W. (2003). The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17(3), 336341.CrossRefGoogle ScholarPubMed
Han, Z., Liang, C.G., Cheng, Y., Duan, X., Zhong, Z., Potireddy, S., Moncada, C., Merali, S. & Latham, K.E. (2010). Oocyte spindle proteomics analysis leading to rescue of chromosome congression defects in cloned embryos. J Proteome Res 9(11), 60256032.CrossRefGoogle ScholarPubMed
Hassold, T. & Hunt, P. (2001). To err (meiotically) is human: The genesis of human aneuploidy. Nat Rev Genet 2(4), 280291.CrossRefGoogle Scholar
Holmfeldt, P., Stenmark, S. & Gullberg, M. (2004). Differential functional interplay of TOGp/XMAP215 and the KinI kinesin MCAK during interphase and mitosis. EMBO J 23(3), 627637.CrossRefGoogle ScholarPubMed
Holzenspies, J.J., Roelen, B.A., Colenbrander, B., Romijn, R.A., Hemrika, W., Stoorvogel, W. & van Haeften, T. (2010). Clathrin is essential for meiotic spindle function in oocytes. Reproduction 140(2), 223233.CrossRefGoogle ScholarPubMed
Hood, F.E. & Royle, S.J. (2009). Functional equivalence of the clathrin heavy chains CHC17 and CHC22 in endocytosis and mitosis. J Cell Sci 122(Pt 13), 21852190.CrossRefGoogle ScholarPubMed
Hubner, N.C., Bird, A.W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A. & Mann, M. (2010). Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189(4), 739754.CrossRefGoogle ScholarPubMed
Kaksonen, M., Toret, C.P. & Drubin, D.G. (2005). A modular design for the clathrin-and actin-mediated endocytosis machinery. Cell 123(2), 305320.CrossRefGoogle Scholar
Kirchhausen, T. (2000). Clathrin. Annu Rev Biochem 69, 699727.CrossRefGoogle ScholarPubMed
Kirchhausen, T. & Harrison, S.C. (1981). Protein organization in clathrin trimers. Cell 23(3), 755761.CrossRefGoogle ScholarPubMed
Lin, C.H., Hu, C.K. & Shih, H.M. (2010). Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J Cell Biol 189(7), 10971105.CrossRefGoogle ScholarPubMed
Maddox, A.S., Azoury, J. & Dumont, J. (2012). Polar body cytokinesis. Cytoskeleton (Hoboken) 69(11), 855868.CrossRefGoogle ScholarPubMed
Maro, B., Johnson, M.H., Pickering, S.J. & Louvard, D. (1985). Changes in the distribution of membranous organelles during mouse early development. J Embryol Exp Morphol 90, 287309.Google ScholarPubMed
Medendorp, K., Vreede, L., van Groningen, J.J., Hetterschijt, L., Brugmans, L., Jansen, P.A., van den Hurk, W.H., de Bruijn, D.R. & van Kessel, A.G. (2010). The mitotic arrest deficient protein MAD2B interacts with the clathrin light chain A during mitosis. PLoS One 5(11), e15128. CrossRefGoogle ScholarPubMed
Musacchio, A. & Salmon, E.D. (2007). The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8(5), 379393.CrossRefGoogle ScholarPubMed
Nezi, L. & Musacchio, A. (2009). Sister chromatid tension and the spindle assembly checkpoint. Curr Opin Cell Biol 21(6), 785795.CrossRefGoogle ScholarPubMed
O'Connell, C.B. & Khodjakov, A.L. (2007). Cooperative mechanisms of mitotic spindle formation. J Cell Sci 120(Pt 10), 17171722.CrossRefGoogle ScholarPubMed
Okamoto, C.T., McKinney, J. & Jeng, Y.Y. (2000). Clathrin in mitotic spindles. Am J Physiol Cell Physiol 279(2), C369C374.CrossRefGoogle ScholarPubMed
Pearse, B.M. (1975). Coated vesicles from pig brain: Purification and biochemical characterization. J Mol Biol 97(1), 9398.CrossRefGoogle ScholarPubMed
Royle, S.J. (2006). The cellular functions of clathrin. Cell Mol Life Sci 63(16), 18231832.CrossRefGoogle ScholarPubMed
Royle, S.J. (2012). The role of clathrin in mitotic spindle organisation. J Cell Sci 125(Pt 1), 1928.CrossRefGoogle ScholarPubMed
Royle, S.J., Bright, N.A. & Lagnado, L. (2005). Clathrin is required for the function of the mitotic spindle. Nature 434(7037), 11521157.CrossRefGoogle ScholarPubMed
Royle, S.J. & Lagnado, L. (2006). Trimerisation is important for the function of clathrin at the mitotic spindle. J Cell Sci 119(Pt 19), 40714078.CrossRefGoogle ScholarPubMed
Schiff, P.B., Fant, J. & Horwitz, S.B. (1979). Promotion of microtubule assembly in vitro by taxol. Nature 277(5698), 665667.CrossRefGoogle ScholarPubMed
Schiff, P.B. & Horwitz, S.B. (1980). Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci USA 77(3), 15611565.CrossRefGoogle ScholarPubMed
Ungewickell, E.J. & Hinrichsen, L. (2007). Endocytosis: Clathrin-mediated membrane budding. Curr Opin Cell Biol 19(4), 417425.CrossRefGoogle ScholarPubMed
Warren, G. (1993). Membrane partitioning during cell division. Annu Rev Biochem 62, 323348.CrossRefGoogle ScholarPubMed
Weitzel, D.H. & Vandre, D.D. (2000). Differential spindle assembly checkpoint response in human lung adenocarcinoma cells. Cell Tissue Res 300(1), 5765.CrossRefGoogle ScholarPubMed
Xiong, B., Li, S., Ai, J.S., Yin, S., Ouyang, Y.C., Sun, S.C., Chen, D.Y. & Sun, Q.Y. (2008). BRCA1 is required for meiotic spindle assembly and spindle assembly checkpoint activation in mouse oocytes. Biol Reprod 79(4), 718726.CrossRefGoogle ScholarPubMed
Yamauchi, T., Ishidao, T., Nomura, T., Shinagawa, T., Tanaka, Y., Yonemura, S. & Ishii, S. (2008). A B-Myb complex containing clathrin and filamin is required for mitotic spindle function. EMBO J 27(13), 18521862.CrossRefGoogle ScholarPubMed
Yin, S., Sun, X.F., Schatten, H. & Sun, Q.Y. (2008). Molecular insights into mechanisms regulating faithful chromosome separation in female meiosis. Cell Cycle 7(19), 29973005.CrossRefGoogle ScholarPubMed
Yu, L.Z., Xiong, B., Gao, W.X., Wang, C.M., Zhong, Z.S., Huo, L.J., Wang, Q., Hou, Y., Liu, K., Liu, X.J., Schatten, H., Chen, D.Y. & Sun, Q.Y. (2007). MEK1/2 regulates microtubule organization, spindle pole tethering and asymmetric division during mouse oocyte meiotic maturation. Cell Cycle 6(3), 330338.CrossRefGoogle ScholarPubMed
Zhu, J., Qi, S.T., Wang, Y.P., Wang, Z.B., Ouyang, Y.C., Hou, Y., Schatten, H. & Sun, Q.Y. (2011). Septin1 is required for spindle assembly and chromosome congression in mouse oocytes. Dev Dyn 240(10), 22812289.CrossRefGoogle ScholarPubMed

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