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Protein kinase implication in prolactin signaling in bovine oocyte-cumulus complexes

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Abstract

The mechanisms of prolactin signal transduction in generative and somatic cells of mammalian ovarian follicles are poorly understood. In this work, participation of tyrosine kinases and protein kinase C in mediation of the previously revealed modulating effects of prolactin on the nuclear maturation of bovine oocytes and the morphologic and functional state of surrounding cumulus cells in vitro has been investigated. It was found that a tyrosine kinase inhibitor genistein suppresses the stimulating action of prolactin on the completion of oocyte nuclear maturation and cumulus expansion, whereas a protein kinase C inhibitor calpostin C does not affect the hormonal effect. Furthermore, both genistein and calpostin C inhibited the inducing influence of prolactin on the proliferative activity of cumulus cells. At the same time, the retarding action of prolactin on destructive processes in cumulus cells was blocked only in the presence of calpostin C. These results show that the stimulating influence of prolactin on oocyte nuclear maturation accompanied by cumulus expansion is achieved with participation of tyrosine kinases, whereas the modulating action of the hormone on the functional state of cumulus cells depends on activation both of tyrosine kinases and protein kinase C.

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References

  • Bachelot, A., and Binart, N., Reproductive Role of Prolactin, Reproduction, 2007, vol. 133, pp. 361–369.

    Article  PubMed  CAS  Google Scholar 

  • Bartke, A., Role of Growth Hormone and Prolactin in the Control of Reproduction: What Are We Learning from Transgenic and Knock-out Animals? Steroids, 1999, vol. 64, pp. 598–604.

    Article  PubMed  CAS  Google Scholar 

  • Besterman, B., and Schultz, R.M., Regulation of Mouse Preimplantation Development: Inhibitory Effect of Genistein, an Inhibitor of Tyrosine Protein Phosphorylation, on Cleavage of One-Cell Embryos, J. Exp. Zool., 1990, vol. 256, pp. 44–53.

    Article  PubMed  CAS  Google Scholar 

  • Bole-Feysot, C., Goffin, V., Edery, M., Binart, N., and Kelly, P.A., Prolactin (PRL) and Its Receptor: Actions, Signal Transduction Pathways and Phenotypes Observed in PRL Receptor Knockout Mice, Endocr. Rev., 1998, vol. 19, pp. 225–268.

    Article  PubMed  CAS  Google Scholar 

  • Calder, M.D., Caveney, A.N., Westhusin, M.H., and Watson, A.J., Cyclooxygenase-2 and Prostaglandin E2 Receptor Messenger RNAs are Affected by Bovine Oocyte Maturation Time and Cumulus-Oocyte Complex Quality, and PGE2 Induces Moderate Expansion of the Bovine Cumulus in vitro, Biol. Reprod., 2001, vol. 65, pp. 135–140.

    Article  PubMed  CAS  Google Scholar 

  • Chan, W.H., Impact of Genistein on Maturation of Mouse Oocytes, Fertilization, and Fetal Development, Reprod. Toxicol., 2009, vol. 28, pp. 52–58.

    Article  PubMed  CAS  Google Scholar 

  • Ciereszko, R., Opalka, M., Kamisnka, B., Górska, T., and Dusza, L., Prolactin Signalling in Porcine Theca Cells: the Involvement of Protein Kinases and Phosphatases, Reprod. Fertil. Dev., 2003, vol. 15, pp. 27–35.

    Article  PubMed  CAS  Google Scholar 

  • Ciereszko, R., Opalka, M., Kaminska, B., Wojtczak, M., Okrasa, S., and Dusza, L., Luteotrophic Action of Prolactin during the Early Luteal Phase in Pigs: The Involvement of Protein Kinases and Phosphatases, Reprod. Biol., 2001, vol. 1, pp. 62–83.

    PubMed  CAS  Google Scholar 

  • Ciereszko, R.E., Petroff, B.K., Ottobre, A.C., Guan, Z., Stokes, B.T., and Ottobre, J.S., Assessment of the Mechanism by Which Prolactin Stimulates Progesterone Production by Early Corpora Lutea of Pigs, J. Endocrinol., 1998, vol. 159, pp. 201–209.

    Article  PubMed  CAS  Google Scholar 

  • Doppler, W., Regulation of Gene Expression by Prolactin, in Reviews of Physiology, Biochemistry and Pharmacology, Berlin: Springer-Verlag, 1994, vol. 124, pp. 93–130.

    Google Scholar 

  • Downs, S.M., Cottom, J., and Hunzicker-Dunn, M., Protein Kinase C and Meiotic Regulation in Isolated Mouse Oocytes, Mol. Reprod. Dev., 2001, vol. 58, pp. 101–115.

    Article  PubMed  CAS  Google Scholar 

  • Fresno Vara, J.A., Cáceres, M.A., Silva, A., and Martin-Pérez, J., Src Family Kinases are Required for Prolactin Induction of Cell Proliferation, Mol. Biol. Cell., 2001, vol. 12, pp. 2171–2183.

    PubMed  CAS  Google Scholar 

  • Gilchrist, R.B., Ritter, L.J., and Armstrong, D.T., Oocyte-Somatic Cell Interactions during Follicular Development in Mammals, Anim. Reprod. Sci., 2004, vol. 82–83, pp. 431–446.

    Article  PubMed  Google Scholar 

  • Gregoraszczuk, E., Słomczyńska, M., and Stokłosowa, S., Effect of Genistein, Tyrphostin and Herbimycin on Prolactin-Stimulated Progesterone Production by Porcine Theca and Luteal Cells, J. Physiol. Pharmacol., 1999, vol. 50, pp. 477–484.

    PubMed  CAS  Google Scholar 

  • Homa, S.T., Neomycin, an Inhibitor of Phosphoinositide Hydrolysis, Inhibits the Resumption of Bovine Oocyte Spontaneous Meiotic Maturation, J. Exp. Zool., 1991, vol. 258, pp. 95–103.

    Article  PubMed  CAS  Google Scholar 

  • Jacquet, P., de Saint-Georges, L., Barrio, S., and Baugnet-Mahieu, L., Morphological Effects of Caffeine, Okadaic Acid and Genistein in One-Cell Mouse Embryos Blocked in G2 by X-Irradiation, Int. J. Radiat. Biol., 1995, vol. 67, pp. 347–358.

    Article  PubMed  CAS  Google Scholar 

  • Jolly, P.D., Smith, P.R., Heath, D.A., Hudson, N.L., Lun, S., Still, L.A., Watts, C.H., and McNatty, K.P., Morphological Evidence of Apoptosis and the Prevalence of Apoptotic Versus Mitotic Cells in the Membrana Granulosa of Ovarian Follicles during Spontaneous and Induced Atresia in Ewes, Biol. Reprod., 1997, vol. 56, pp. 837–846.

    Article  PubMed  CAS  Google Scholar 

  • Kiapekou, E., Loutradis, D., Patsoula, E., Koussidis, G.A., Minas, V., Bletsa, R., Antsaklis, A., Michalas, S., and Makrigiannakis, A., Prolactin Receptor mRNA Expression in Oocytes and Preimplantation Mouse Embryos, Reprod. Biomed. Online, 2005, vol. 10, pp. 339–346.

    Article  PubMed  CAS  Google Scholar 

  • Kiapekou, E., Zapanti, E., Mastorakos, G., Beretsos, P., Bletsa, R., Drakakis, P., Loutradis, D., and Antsaklis, A., Effect of Prolactin in the Absence of hCG on Maturation, Fertilization, and Embryonic Development of in vitro Matured Mouse Oocytes, Ann. N. Y. Acad. Sci., 2006, vol. 1092, pp. 450–459.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J.H., Han, J.S., and Yoon, Y.D., Biochemical and Morphological Identification of Ceramide-Induced Cell Cycle Arrest and Apoptosis in Cultured Granulosa Cells, Tissue Cell, 1999, vol. 31, pp. 531–539.

    Article  PubMed  CAS  Google Scholar 

  • Kotok, T., Bogorad, R.L., Smirnov, A.N., Turovetskii, V.M., and Smirnova, O.V., The Effect of Periovulatory Imbalance of Prolactin on the Expression of Prolactin Receptors in Rat Ovary Cells, Russ. J. Dev. Biol., 2000, vol. 31, no. 2, pp. 117–123.

    Article  CAS  Google Scholar 

  • Kubiak, J.Z., Yes Fyn Can: Individual or Team Player in SFKs? Cell Cycle, 2010, vol. 9, pp. 1460–1461.

    Article  PubMed  CAS  Google Scholar 

  • Kuz’mina, T.I., Lebedeva, I.Yu., Torner, H., and Alm, H., Effects of Prolactin in Different Culture Systems on the Maturation of Bovine Oocytes and Their Capacity for Subsequent Development, Russ. J. Dev. Biol., 2001, vol. 32, no. 2, pp. 112–118.

    Article  Google Scholar 

  • Lakin, G.F., Biometriya (Biometry), Moscow: Vysshaya Shkola, 1990.

    Google Scholar 

  • Lebedeva, I., Vejlsted, M., Volkova, N., Singina, G., and Schmidt, M., The Direct and Cumulus-Mediated Effects of Prolactin on Bovine Oocytes, Reprod. Fertil. Dev., 2009a, vol. 21, pp. 222 abstr.

  • Lebedeva, I.Yu., Kibardina, T.V., and Kuz’mina, T.I., Participation of Granulosa Cells in Mediation of Prolactin and Somatotropin Action on Bovine Oocyte-Cumulus Complexes in vitro, Tsitologiia, 2005, vol. 47, no. 10, pp. 882–888.

    PubMed  CAS  Google Scholar 

  • Lebedeva, I.Yu., Lebedev, V.A., and Kuz’mina, T.I., Characterization of Somatotropin- and Prolactin-Binding Sites on Bovine Granulosa Cells Using Homologous Hormones, Biochemistry (Mosc.), 2001, vol. 66, no. 9, pp. 967–972.

    Article  CAS  Google Scholar 

  • Lebedeva, I.Yu., Singina, G.N., Ernst, L.K., and Golubev, A.K., Realization Pathways of Prolactin Modulating Influence on the cAMP-Dependent Mechanism of Meiosis Regulation in Bovine Oocytes, Tsitologiia, 2009b, vol. 51, no. 7, pp. 559–564.

    PubMed  CAS  Google Scholar 

  • Lebedeva, I.Yu., Singina, G.N., Volkova, N.A., Mormyshev, A.N., Golubev, A.K., and Zinovieva, N.A., Interaction of Signal Cascades Induced by cAMP and Prolactin in Bovine Oocyte-Cumulus Complexes, Tsitologiia, 2008, vol. 50, no. 8, pp. 734–742.

    PubMed  CAS  Google Scholar 

  • Levi, M., and Shalgi, R., The Role of Fyn Kinase in the Release from Metaphase in Mammalian Oocytes, Mol. Cell. Endocrinol., 2010, vol. 314, pp. 228–233.

    Article  PubMed  CAS  Google Scholar 

  • McGinnis, L.K., Kinsey, W.H., and Albertini, D.F., Functions of Fyn Kinase in the Completion of Meiosis in Mouse Oocytes, Dev. Biol., 2009, vol. 327, pp. 280–287.

    Article  PubMed  CAS  Google Scholar 

  • Mehlmann, L.M., Stops and Starts in Mammalian Oocytes: Recent Advances in Understanding the Regulation of Meiotic Arrest and Oocyte Maturation, Reproduction, 2005, vol. 130, pp. 791–799.

    Article  PubMed  CAS  Google Scholar 

  • Mendoza, C., Cremades, N., Ruiz-Requena, E., Martinez, F., Ortega, E., Bernabeu, S., and Tesarik, J., Relationship between Fertilization Results after Intracytoplasmic Sperm Injection, Intrafollicular Steroid, Pituitary Hormone and Cytokine Concentrations, Hum. Reprod., 1999, vol. 14, pp. 628–635.

    Article  PubMed  CAS  Google Scholar 

  • Picazo, R.A., Garcia, Ruiz, J.P., Santiago Moreno, J., Gonzalez de, Bulnes, A., Munoz, J., Silvan, G., Lorenzo, P.L., and Illera, J.C., Cellular Localization and Changes in Expression of Prolactin Receptor Isoforms in Sheep Ovary throughout the Estrous Cycle, Reproduction, 2004, vol. 128, pp. 545–553.

    Article  PubMed  CAS  Google Scholar 

  • Shimada, M., and Terada, T., Roles of cAMP in Regulation of Both MAP Kinase and p34 (cdc2) Kinase Activity during Meiotic Progression, Especially beyond the MI Stage, Mol. Reprod. Dev., 2002, vol. 62, pp. 124–131.

    Article  PubMed  CAS  Google Scholar 

  • Sun, Q.Y., Miao, Y.L., and Schatten, H., Towards a New Understanding on the Regulation of Mammalian Oocyte Meiosis Resumption, Cell Cycle, 2009, vol. 8, pp. 2741–2747.

    Article  PubMed  CAS  Google Scholar 

  • Talmor-Cohen, A., Tomashov-Matar, R., Eliyahu, E., Shapiro, R., and Shalgi, R., Are Src Family Kinases Involved in Cell Cycle Resumption in Rat Eggs?, Reproduction, 2004, vol. 127, pp. 455–463.

    Article  PubMed  CAS  Google Scholar 

  • Tatemoto, H., and Terada, T., Activation of p34(cdc2) Kinase Around the Meiotic Resumption in Bovine Oocytes Cultured in vitro, Theriogenology, 1996, vol. 45, pp. 427–437.

    Article  PubMed  CAS  Google Scholar 

  • Torner, H., Kubelka, M., Heleil, B., Tomek, W., Alm, H., Kuzmina, T., and Guiard, V., Dynamics of Meiosis and Protein Kinase Activities in Bovine Oocytes Correlated to Prolactin Treatment and Follicle Size, Theriogenology, 2001, vol. 55, pp. 885–899.

    Article  PubMed  CAS  Google Scholar 

  • Villanueva, L.A., Méndez, I., Ampuero, S., and Larrea, F., The Prolactin Inhibition of Follicle-Stimulating Hormone-Induced Aromatase Activity in Cultured Rat Granulosa Cells Is in Part Tyrosine Kinase and Protein Kinase-C Dependent, Mol. Hum. Reprod., 1996, vol. 2, pp. 725–731.

    Article  PubMed  CAS  Google Scholar 

  • Vodkova, Z., Rajmon, R., Petr, J., Klabanová, P., and Jilek, F., Effects of Genistein and Genistin on in vitro Maturation of Pig Oocytes, Czech. J. Anim. Sci., 2008, vol. 53, pp. 1–8.

    CAS  Google Scholar 

  • Wise, T., Suss, U., Stranzinger, G., Wuthrich, K., and Maurer, R.R., Cumulus and Oocyte Maturation and in vitro and in vivo Fertilization of Oocytes in Relation to Follicular Steroids, Prolactin, and Glycosaminoglycans throughout the Estrous Period in Superovulated Heifers with a Normal LH Surge, no Detectable LH Surge, and Progestin Inhibition of LH Surge, Domest. Anim. Endocrin., 1994, vol. 11, pp. 59–86.

    Article  CAS  Google Scholar 

  • Yoshimura, Y., Nakamura, Y., Yamada, H., Ando, M., Ubukata, Y., Oda, T., and Suzuki, M., Possible Contribution of Prolactin in the Process of Ovulation and Oocyte Maturation, Horm. Res., 1991, vol. 35,suppl. 1, pp. 22–32.

    Article  PubMed  CAS  Google Scholar 

  • Zhuang, S., Lynch, M.C., and Kochevar, I.E., Activation of Protein Kinase C is Required for Protection of Cells Against Apoptosis Induced by Singlet Oxygen, FEBS Lett., 1998, vol. 437, pp. 158–162.

    Article  PubMed  CAS  Google Scholar 

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Lebedeva, I.Y., Singina, G.N., Taradajnic, T.E. et al. Protein kinase implication in prolactin signaling in bovine oocyte-cumulus complexes. Cell Tiss. Biol. 5, 560–567 (2011). https://doi.org/10.1134/S1990519X11060071

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