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Survivin is a critical regulator of spindle organization and chromosome segregation during rat oocyte meiotic maturation

Published online by Cambridge University Press:  04 October 2010

Ke Wang ,
Guang-Jian Jiang ,
Liang Wei ,
Xing-Wei Liang ,
De-Qiang Miao ,
Shao-Chen Sun ,
Lei Guo ,
Zhen-Bo Wang  and
Sheng-Sheng Lu
Ke Wang
Affiliation:
Department of Biochemistry and Molecular Biology, North China Coal Medical University, Tangshan 063000, China.
Guang-Jian Jiang*
Affiliation:
Department of Biochemistry and Molecular Biology, North China Coal Medical University, Tangshan 063000, China. Department of Biochemistry and Molecular Biology, North China Coal Medical University, Tangshan 063000, China.
Liang Wei
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
Xing-Wei Liang
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
De-Qiang Miao
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
Shao-Chen Sun
Affiliation:
Animal Reproduction Institute, Guangxi Key Laboratory of Subtropical Bioresource Conservation and Utilization, Guangxi University, Nanning, China.
Lei Guo
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
Zhen-Bo Wang
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
Sheng-Sheng Lu
Affiliation:
Animal Reproduction Institute, Guangxi Key Laboratory of Subtropical Bioresource Conservation and Utilization, Guangxi University, Nanning, China.
*
All correspondence to: Guang-Jian Jiang, Department of Biochemistry and Molecular Biology, North China Coal Medical University, Tangshan 063000, China. e-mail: [email protected]
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Summary

Survivin is a novel member of the inhibitor of apoptosis gene family that bear baculoviral IAP repeats (BIRs), whose physiological roles in regulating meiotic cell cycle need to be determined. Confocal microscopy was employed to observe the localization of survivin in rat oocytes. At the germinal vesicle (GV) stage, survivin was mainly concentrated in the GV. At the prometaphase I (pro-MI) and metaphase I (MI) stage, survivin was mainly localized at the kinetochores, with a light staining detected on the chromosomes. After transition to anaphase I or telophase I stage, survivin migrated to the midbody, and signals on the kinetochores and chromosomes disappeared. At metaphase II (MII) stage, survivin became mainly localized at the kinetochores again. Microinjection of oocytes with anti-survivin antibodies at the beginning of the meiosis, thus blocking the normal function of survivin, resulted in abnormal spindle assembly, chromosome segregation and first polar body emission. These results suggest that survivin is involved in regulating the meiotic cell cycle in rat oocytes.

Keywords

MeiosisMicrotubulesOocyteSpindleSurvivin
Type
Research Article
Information
Zygote , Volume 19 , Issue 4 , November 2011 , pp. 307 - 313
Copyright
Copyright © Cambridge University Press 2010

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References

Adams, R.R., Carmena, M. & Earnshaw, W.C. (2001). Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol. 11, 49–54.CrossRefGoogle ScholarPubMed
Ambrosini, G., Adida, C. & Altieri, D.C. (1997). A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med. 3, 917–21.CrossRefGoogle ScholarPubMed
Chen, J., Wu, W., Tahir, S.K., Kroeger, P.E., Rosenberg, S.H., Cowsert, L.M., Bennett, F., Krajewski, S., Krajewska, M., Welsh, K., Reed, J.C. & Ng, S.C. (2000). Down-regulation of survivin by antisense oligonucleotides increases apoptosis, inhibits cytokinesis and anchorage-independent growth. Neoplasia 2, 235–41.CrossRefGoogle ScholarPubMed
Crook, N.E., Clem, R.J. & Miller, L.K. (1993). An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67, 2168–74.CrossRefGoogle ScholarPubMed
DeLuca, J.G., Dong, Y., Hergert, P., Strauss, J., Hickey, J.M., Salmon, E.D. & McEwen, B.F. (2005). Hec1 and nuf2 are core components of the kinetochore outer plate essential for organizing microtubule attachment sites. Mol. Biol. Cell 16, 519–31.CrossRefGoogle ScholarPubMed
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
Fraser, A.G., James, C., Evan, G.I. & Hengartner, M.O. (1999). Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr. Biol. 9, 292–301.CrossRefGoogle Scholar
Fukuda, S. & Pelus, L.M. (2001). Regulation of the inhibitor-of-apoptosis family member survivin in normal cord blood and bone marrow CD34+ cells by hematopoietic growth factors: implication of survivin expression in normal hematopoiesis. Blood 98, 2091–100.CrossRefGoogle ScholarPubMed
Hinds, M.G., Norton, R.S., Vaux, D.L. & Day, C.L. (1999). Solution structure of a baculoviral inhibitor of apoptosis (IAP) repeat. Nat. Struct. Biol. 6, 648–51.Google ScholarPubMed
Kaitna, S., Pasierbek, P., Jantsch, M., Loidl, J. & Glotzer, M. (2002). The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr. Biol. 12, 798–812.CrossRefGoogle ScholarPubMed
Keefer, C.L. & Schuetz, A.W. (1982). Spontaneous activation of ovulated rat oocytes during in vitro culture. J. Exp. Zool. 224, 371–7.CrossRefGoogle ScholarPubMed
Kobayashi, K., Hatano, M., Otaki, M., Ogasawara, T. & Tokuhisa, T. (1999). Expression of a murine homologue of the inhibitor of apoptosis protein is related to cell proliferation. Proc. Natl. Acad. Sci. USA 96, 1457–62.CrossRefGoogle ScholarPubMed
Kotwaliwale, C. & Biggins, S. (2006). Microtubule capture: a concerted effort. Cell 127, 1105–8.CrossRefGoogle ScholarPubMed
Lens, S.M. & Medema, R.H. (2003). The survivin/aurora B complex: its role in coordinating tension and attachment. Cell Cycle 2, 507–10.CrossRefGoogle ScholarPubMed
Lens, S.M., Vader, G. & Medema, R.H. (2006). The case for survivin as mitotic regulator. Curr. Opin. Cell Biol. 18, 616–22.CrossRefGoogle ScholarPubMed
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. J. Cell Biol. 157, 219–29.CrossRefGoogle ScholarPubMed
Ruchaud, S., Carmena, M. & Earnshaw, W.C. (2007). Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell. Biol. 8, 798–812.CrossRefGoogle ScholarPubMed
Speliotes, E.K., Uren, A., Vaux, D. & Horvitz, H.R. (2000). The survivin-like C. elegans BIR-1 protein acts with the aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone. Mol. Cell. 6, 211–23.CrossRefGoogle ScholarPubMed
Sun, S.C., Wei, L., Li, M., Lin, S.L., Xu, B.Z., Liang, X.W., Kim, N.H., Schatten, H., Lu, S.S. & Sun, Q.Y. (2009). Perturbation of survivin expression affects chromosome alignment and spindle checkpoint in mouse oocyte meiotic maturation. Cell Cycle 8, 3365–72.CrossRefGoogle ScholarPubMed
Suzuki, A., Hayashida, M., Ito, T., Kawano, H., Nakano, T., Miura, M., Akahane, K. & Shiraki, K. (2000). Survivin initiates cell cycle entry by the competitive interaction with Cdk4/p16(INK4a) and Cdk2/cyclin E complex activation. Oncogene 19, 3225–34.CrossRefGoogle ScholarPubMed
Tanaka, K., Iwamoto, S., Gon, G., Nohara, T., Iwamoto, M. & Tanigawa, N. (2000). Expression of survivin and its relationship to loss of apoptosis in breast carcinomas. Clin. Cancer Res. 6, 127–34.Google ScholarPubMed
Uren, A.G., Coulson, E.J. & Vaux, D.L. (1998). Conservation of baculovirus inhibitor of apoptosis repeat proteins (BIRPs) in viruses, nematodes, vertebrates and yeasts. Trends Biochem. Sci. 23, 159–62.CrossRefGoogle ScholarPubMed
Uren, A.G., Wong, L., Pakusch, M., Fowler, K.J., Burrows, F.J., Vaux, D.L. & Choo, K.H. (2000). Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr. Biol. 10, 1319–28.CrossRefGoogle ScholarPubMed
Vader, G., Kauw, J.J., Medema, R.H. & Lens, S.M. (2006). Survivin mediates targeting of the chromosomal passenger complex to the centromere and midbody. EMBO Rep. 7, 85–92.CrossRefGoogle Scholar
Wang, Y., Toppari, J., Parvinen, M. & Kallio, M. J. (2006). Inhibition of aurora kinases perturbs chromosome alignment and spindle checkpoint signaling in rat spermatocytes. Exp. Cell Res. 312, 3459–70.CrossRefGoogle ScholarPubMed
Yoon, H.J. & Carbon, J. (1999). Participation of Bir1p, a member of the inhibitor of apoptosis family, in yeast chromosome segregation events. Proc. Natl. Acad. Sci. USA 96, 13208–13.CrossRefGoogle ScholarPubMed