Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-24T17:26:47.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of age, GV transfer and modified nucleocytoplasmic ratio on PKCα in mouse oocytes and early embryos

Published online by Cambridge University Press:  14 January 2011

Long-Bo Cui ,
Zhen-Jun Zhao ,
Xue-Ying Zhou ,
Qian Li ,
Xiu-Ying Huang  and
Fang-Zhen Sun
Long-Bo Cui*
Affiliation:
Department of Biology, Yantai University, Yantai 264005, P. R. China.
Zhen-Jun Zhao
Affiliation:
Department of Biology, Yantai University, Yantai 264005, P. R. China.
Xue-Ying Zhou
Affiliation:
Department of Biology, Yantai University, Yantai 264005, P. R. China.
Qian Li
Affiliation:
Department of Biology, Yantai University, Yantai 264005, P. R. China.
Xiu-Ying Huang
Affiliation:
Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P. R. China.
Fang-Zhen Sun
Affiliation:
Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P. R. China.
*
All correspondence to: Long-Bo Cui, Department of Biology, Yantai University, Yantai 264005, P. R. China. Tel: +86 535 6903162. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Protein kinase C (PKC) is a family of Ser/Thr protein kinases that can be activated by Ca2+, phospholipid and diacylglycerol. There is evidence that PKC plays key roles in the meiotic maturation and activation of mammalian oocytes. The present study aimed to monitor the effect of age, germinal vesicle (GV) transfer and modified nucleoplasmic ratio on the subcellular distribution profile of PKCα, an important isozyme of PKC, in mouse oocytes undergoing meiotic maturation and following egg activation. Germinal vesicle oocytes were collected from 6–8-week-old and 12-month-old mice. Germinal vesicle-reconstructed oocytes and GV oocytes with one-half or one-third of the original oocyte volume were created using micromanipulation and electrofusion. The subcellular localization of PKCα was detected by immunocytochemistry and laser confocal microscopy. Our study showed that PKCα had a similar location pattern in oocytes and early embryos from young and old mice. PKCα was localized evenly in ooplasm, with weak staining in GV at the GV stage, and present in the entire meiosis II (MII) spindle at the MII stage. In pronuclear and 2-cell embryos, PKCα was concentrated in the nucleus except for the nucleolus. After the GV oocytes were reconstructed, the resultant MII oocytes and embryos showed a similar distribution of PKCα between reconstructed and unreconstructed controls. After one-half or two-thirds of the cytoplasm was removed from the GV oocytes, PKCα still had a similar location pattern in MII oocytes and early embryos from the GV oocytes with modified nucleoplasmic ratio. Our study showed that age, GV transfer and modified nucleocytoplasmic ratio does not affect distribution of PKCα during mouse oocyte maturation, activation, and early embryonic mitosis.

Keywords

ageembryogerminal vesicleoocytePKCα
Type
Research Article
Information
Zygote , Volume 20 , Issue 1 , February 2012 , pp. 87 - 95
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Avazeri, N., Courtot, A-M. & Lefevre, B. (2004). Regulation of spontaneous meiosis resumption in mouse oocytes by various conventional PKC isozymes depends on cellular compartmentalization. J. Cell Sci. 117, 4969–78.CrossRefGoogle ScholarPubMed
Battaglia, D.E., Goodwin, P., Klein, N.A. & Soules, M.R. (1996). Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 11, 2217–22.CrossRefGoogle ScholarPubMed
Battaini, F. & Pascale, A. (2005). Protein kinase C signal transduction regulation in physiological and pathological aging. Ann. NY Acad. Sci. 1057, 177–92.CrossRefGoogle ScholarPubMed
Battistella-Patterson, A.S., Fultz, M.E., Li, C., Geng, W., Norton, M. & Wright, G.L. (2000). PKCα translocation is microtubule-dependent in passaged smooth muscle cells. Acta Physiol. Scand. 170, 87–97CrossRefGoogle ScholarPubMed
Carbone, M.C. & Tatone, C. (2009). Alterations in the protein kinase C signaling activated by a parthenogenetic agent in oocytes from reproductively old mice. Mol. Reprod. Dev. 76, 122–31.CrossRefGoogle ScholarPubMed
Chen, D., Purohit, A., Halilovic, E., Doxsey, S.J. & Newton, A.C. (2004). Centrosomal anchoring of protein kinase C beta II by pericentrin controls microtubule organization, spindle function, and cytokinesis. J. Biol. Chem. 279, 4829–39.CrossRefGoogle ScholarPubMed
Corsini, E., Racchi, M., Sinforiani, E., Lucchi, L., Viviani, B., Rovati, G.E., Govoni, S., Galli, C.L. & Marinovich, M. (2005). Age-related decline in RACK-1 expression in human leukocytes is correlated to plasma levels of dehydroepiandrosterone. J. Leukoc. Biol. 77, 247–56.CrossRefGoogle ScholarPubMed
Cui, L.B., Huang, X-Y. & Sun, F-Z. (2005a). Transfer of germinal vesicle to ooplasm of young mice could not rescue ageing-associated chromosome misalignment in meiosis of oocytes from aged mice. Hum. Reprod. 20, 1624–31.CrossRefGoogle Scholar
Cui, L.B., Huang, X-Y. & Sun, F-Z. (2005b). Nucleocytoplasmic ratio of fully grown germinal vesicle oocytes is essential for mouse meiotic chromosome segregation and alignment, spindle shape and early embryonic development. Hum. Reprod. 20, 2946–53.CrossRefGoogle ScholarPubMed
Dehghani, H. & Hahnel, A.C. (2005). Expression profile of protein kinase C isozymes in preimplantation mouse development. Reproduction 130, 441–51.CrossRefGoogle ScholarPubMed
Downs, S.M., Cottom, J. & Hunzicker-Dunn, M. (2001). Protein kinase C and meiotic regulation in isolated mouse oocytes. Mol. Reprod. Dev. 58, 101–15.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Fan, H.Y., Tong, C., Li, M.Y., Lian, L., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2002). Translocation of the classic protein kinase C isoforms in porcine oocytes: implications of protein kinase C involvement in the regulation of nuclear activity and cortical granule exocytosis. Exp. Cell Res. 277, 183–91.CrossRefGoogle ScholarPubMed
Fan, H.Y., Tong, C., Li, M.Y., Chen, D.Y. & Sun, Q.Y. (2003) Roles of protein kinase C in mouse oocyte maturation and fertilization in vitro. Acta Biolog. Exp. Sin. 36, 37–42.Google ScholarPubMed
Fulka, J. Jr, First, N.L. & Moor, R.M. (1998). Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Mol. Hum. Reprod. 4, 41–9.CrossRefGoogle ScholarPubMed
Gangeswaran, R. & Jones, K.T. (1997). Unique protein kinase C profile in mouse oocytes: lack of calcium-dependent conventional isoforms suggested by rtPCR and western blotting. FEBS Lett. 412, 309–12.CrossRefGoogle ScholarPubMed
Garcia, M.M., Edwards, R., Brennan, G.B. & Harlan, R.E. (2000). Deafferentation-induced changes in protein kinase C expression in the rat cochlear nucleus. Hear Res. 147, 113–24.CrossRefGoogle ScholarPubMed
Halet, G. (2004). PKC signaling at fertilization in mammalian eggs. Biochim. Biophys. Acta 1742, 185–9.CrossRefGoogle ScholarPubMed
Halet, G., Tunwell, R., Parkinson, S.J. & Carroll, J. (2004). Conventional PKCs regulate the temporal pattern of Ca2+ oscillations at fertilization in mouse eggs. J. Cell Biol. 164, 1033–44.CrossRefGoogle ScholarPubMed
Hassold, T. & Chiu, D. (1985). Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy. Hum. Genet. 70, 11–7.CrossRefGoogle ScholarPubMed
Hug, H. & Sarre, T.F. (1993). Protein kinase C isozymes: divergence in signal transduction? Biochem. J. 291, 329–43.CrossRefGoogle ScholarPubMed
Kárníková, L., Urban, F., Moor, R. & Fulka, J. Jr. (1998). Mouse oocyte maturation: the effect of modified nucleocytoplasmic ratio. Reprod. Nutr. Dev. 38, 665–70.CrossRefGoogle ScholarPubMed
Knopf, J.L., Lee, M.H., Sultzman, L.A., Kriz, R.W., Loomis, C.R., Hewick, R.M. & Bell, R.M. (1986). Cloning and expression of multiple protein kinase C cDNAs. Cell 46, 491–502.CrossRefGoogle ScholarPubMed
Luria, A., Tennenbaum, T., Sun, Q.Y., Rubinstein, S. & Breitbart, H. (2000). Differential localization of conventional protein kinase C isoforms during mouse oocyte development. Biol. Reprod. 62, 1564–70.CrossRefGoogle ScholarPubMed
Osada, S., Mizuno, K., Saido, T.C., Akita, Y., Suzuki, K., Kuroki, T. & Ohno, S. (1990). A phorbol ester receptor/protein kinase, nPKC eta, a new member of the protein kinase C family predominantly expressed in lung and skin. J. Biol. Chem. 265, 22434–40.CrossRefGoogle ScholarPubMed
Page Baluch, D., Koeneman, B.A., Hatch, K.R., McGaughey, R.W. & Capco, D.G. (2004). PKC isotypes in postactivated and fertilized mouse eggs: association with the meiotic spindle. Dev. Biol. 274, 45–55.CrossRefGoogle Scholar
Palermo, G.D., Takeuchi, T. & Rosenwaks, Z. (2002). Technical approaches to correction of oocyte aneuploidy. Hum. Reprod. 17, 2165–73.CrossRefGoogle ScholarPubMed
Pauken, C.M. & Capco, D.G. (2000). The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development. Dev. Biol. 223, 411–21.CrossRefGoogle ScholarPubMed
Quan, H-M., Fan, H-Y., Meng, X-Q., Huo, L-J., Chen, D-Y., Schatten, H., Yang, P-M. & Sun, Q-Y. (2003). Effect of protein kinase C activation on mouse oocyte meiotic maturation, fertilization and early embryo development. Zygote 11, 329–37.CrossRefGoogle Scholar
Raz, T., Eliyahu, E., Yesodi, V. & Shalgi, R. (1998). Profile of protein kinase C isozymes and their possible role in mammalian egg activation. FEBS Lett. 431, 415–8.CrossRefGoogle ScholarPubMed
Selbie, L.A., Schmitz-Peiffer, C., Sheng, Y. & Biden, T. J. (1993). Molecular cloning and characterization of PKC2, an atypical isoform of protein kinase C derived from insulin-secreting cells. J. Biol. Chem. 268, 24296–302.CrossRefGoogle Scholar
Sun, F.Z. & Moor, R.M. (1991). Nuclear–cytoplasmic interactions during ovine oocyte maturation. Development 111, 171–80.CrossRefGoogle ScholarPubMed
Takeuchi, T., Ergün, B., Huang, T.H., Rosenwaks, Z. & Palermo, G.D. (1999). A reliable technique of nuclear transplantation for immature mammalian oocytes. Hum. Reprod. 14, 1312–7.CrossRefGoogle ScholarPubMed
Tang, T.S., Dong, J.B., Huang, X.Y. & Sun, F.Z. (2000). Ca2+ oscillations induced by a cytosolic sperm protein factor are mediated by a maternal machinery that functions only once in mammalian eggs. Development 127, 1141–50.CrossRefGoogle ScholarPubMed
Viveiros, M.M., Hirao, Y. & Eppig, J.J. (2001). Evidence that protein kinase C (PKC) participates in the meiosis I to meiosis II transition in mouse oocytes. Dev. Biol. 235, 330–42.CrossRefGoogle ScholarPubMed
Viveiros, M.M., O'Brien, M. & Eppig, J.J. (2004). Protein kinase C activity regulates the onset of anaphase I in mouse oocytes. Biol. Reprod. 77, 1525–32.CrossRefGoogle Scholar
Wagner, L.M. & Takemoto, D.J. (2001). Protein kinase C α and γ in N/N 1003A rabbit lens epithelial cell differentiation. Mol. Vis. 7, 57–62.Google Scholar
Wu, X.Q., Zhang, X., Li, X.H., Cheng, H.H., Kuai, Y.R., Wang, S. & Guo, Y.L. (2006). Translocation of classical PKC and cortical granule exocytosis of human oocyte in germinal vesicle and metaphase II stage. Acta Pharmacol. Sin, 27, 1353–8.CrossRefGoogle ScholarPubMed
Zhang, J., Wang, C.W., Krey, L., Liu, H., Meng, L., Blaszczyk, A., Adler, A. & Grifo, J. (1999). In vitro maturation of human preovulatory oocytes reconstructed by germinal vesicle transfer. Fertil. Steril. 71, 726–31.CrossRefGoogle ScholarPubMed