Skip to main content Accessibility help
×
Home

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

  • Ke Wang (a1), Guang-Jian Jiang (a2) (a1), Liang Wei (a3), Xing-Wei Liang (a3), De-Qiang Miao (a3), Shao-Chen Sun (a4), Lei Guo (a3), Zhen-Bo Wang (a3) and Sheng-Sheng Lu (a4)...

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.

Copyright

Corresponding author

All correspondence to: Guang-Jian Jiang, Department of Biochemistry and Molecular Biology, North China Coal Medical University, Tangshan 063000, China. e-mail: guangjianjiang@sina.com

References

Hide All
Adams, R.R., Carmena, M. & Earnshaw, W.C. (2001). Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol. 11, 4954.
Ambrosini, G., Adida, C. & Altieri, D.C. (1997). A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med. 3, 917–21.
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.
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.
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.
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.
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, 292301.
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.
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.
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, 798812.
Keefer, C.L. & Schuetz, A.W. (1982). Spontaneous activation of ovulated rat oocytes during in vitro culture. J. Exp. Zool. 224, 371–7.
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.
Kotwaliwale, C. & Biggins, S. (2006). Microtubule capture: a concerted effort. Cell 127, 1105–8.
Lens, S.M. & Medema, R.H. (2003). The survivin/aurora B complex: its role in coordinating tension and attachment. Cell Cycle 2, 507–10.
Lens, S.M., Vader, G. & Medema, R.H. (2006). The case for survivin as mitotic regulator. Curr. Opin. Cell Biol. 18, 616–22.
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.
Ruchaud, S., Carmena, M. & Earnshaw, W.C. (2007). Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell. Biol. 8, 798812.
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.
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.
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.
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.
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.
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.
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, 8592.
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.
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.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed