Skip to main content
Log in

Realization pathways of prolactin modulating effect on the cAMP-dependent mechanism of meiosis regulation in bovine oocytes

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

Cyclic AMP is one of the key regulators of mammalian meiosis. In the present work, realization pathways of the previously revealed modulating effect of prolactin (PRL) on the cAMP-dependent mechanism of meiosis regulation in bovine oocytes were studied. A comparative investigation of individual and combined effects of PRL (50 ng/ml) and an activator of adenylate cyclase forskolin (FK, 20 µM) on the meiotic reinitiation and completion of nuclear maturation in cumulus-surrounded and cumulus-free oocytes was performed. It has been shown that the pattern of the effects of PRL on the meiotic resumption in oocytes devoid of cumulus cells depends on the presence of FK in the culture medium. Furthermore, the realization of this effect is not associated with the activation of cytoplasmic isoforms of protein kinase C. It has also been found that PRL inhibits the retarding action of FK on the completion of oocyte nuclear maturation both in the presence and absence of cumulus cells. These findings suggest that PRL may modulate the functioning of the cAMP-dependent mechanism of meiosis regulation by the direct action on bovine oocytes, with realization of this action being independent of the metabolic coupling of oocytes with cumulus cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

DO:

denuded oocytes (oocytes free of cumulus cells)

Dp:

diplotene

MII:

metaphase II

OCC:

oocyte-cumulus complexes

PRL:

prolactin

TI:

telophase I

FK:

forskolin

References

  • Aktas, H., Wheeler, M.B., Rosenkrans, C.F.Jr., First, N.L., and Leibfried-Rutledge, M.L., Maintenance of Bovine Oocytes in Prophase of Meiosis I by High [cAMP]i. J. Reprod. Fertil., 1995, vol. 105, pp. 227–235.

    PubMed  CAS  Google Scholar 

  • Avazeri, N., Courtot, A.M., and Lefevre, B., Regulation of Spontaneous Meiosis Resumption in Mouse Oocytes by Various Conventional PKC Isozymes Depends on Cellular Compartmentalization, J. Cell Sci., 2004, vol. 117, pp. 4969–4978.

    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 

  • Bilodeau-Goeseels, S., Sasseville, M., Guillemette, C., and Richard, F.J., Effects of Adenosine Monophosphate-Activated Kinase Activators on Bovine Oocyte Nuclear Maturation in Vitro, Mol. Reprod. Dev., 2007, vol. 74, pp. 1021–1034.

    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 

  • Bos, J.L., Epac: A New cAMP Target and New Avenues in cAMP Research, Nat. Rev. Mol. Cell Biol., 2003, vol. 4, pp. 733–738.

    Article  PubMed  CAS  Google Scholar 

  • Chang, S.P., Ng, H.T., Lan, T.L., Chao, H.T., Wei, T.C., Yang, T.S., and Ou Yang, X.R., Transient Hyperprolactinemia in Gonadotropin-Stimulated Cycles for in Vitro Fertilization and Its Effect on Conception, Chung Hua I Hsueh Chin Taipei, 1993, vol. 51, pp. 401–406.

    CAS  Google Scholar 

  • Conti, M., Andersen, C.B., Richard, F., Mehats, C., Chun, S.Y., Horner, K., Jin, C., and Tsafriri, A., Role of Cyclic Nucleotide Signaling in Oocyte Maturation, Mol. Cell Endocrinol., 2002, vol. 187, pp. 153–159.

    Article  PubMed  CAS  Google Scholar 

  • Downs, S.M., Cotton, 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 

  • Dusza, L. and Tilton, J.E., Role of Prolactin in the Regulation of Ovarian Function in Pigs, J. Reprod. Fert., 1990, vol. 40,Suppl, pp. 33–45.

    CAS  Google Scholar 

  • Fan, H.Y., Li, M.Y., Tong, C., Chen, D.Y., Xia, G.L., Song, X.F., Schatten, H., and Sun, Q.Y., Inhibitory Effects of cAMP and Protein Kinase C on Meiotic Maturation and MAP Kinase Phosphorylation in Porcine Oocytes, Mol. Reprod. Dev., 2002, vol. 63, pp. 480–487.

    Article  PubMed  CAS  Google Scholar 

  • Hinrichs, K., Manipulation of Oocyte Maturation in Vitro, Arch. Anim. Breed., 1996, vol. 39, Special issue, pp. 43–50.

    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 

  • Jinno, M., Katsumata, Y., Hoshiai, T., Nakamura, Y., Matsumoto, K., and Yoshimura, Y., A Therapeutic Role of Prolactin Supplementation in Ovarian Stimulation for in Vitro Fertilization: The Bromocriptine-Rebound Method, J. Clin. Endocrinol. Metab., 1997, vol. 82, pp. 3603–3611.

    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 

  • Kotok, T., Bogorad, R.L., Smirnov, A.N., Turovetskii, V.M., Smirnova, O.V., The Effect of Periovulatory Imbalance of Prolactin on the Expression of Prolactin Receptors in Rat Ovary Cells, Ontogenez, 2000, vol. 31, no. 2, pp. 144–151.

    PubMed  CAS  Google Scholar 

  • Kuzmina, T.I., Lebedeva, I.Yu., Torner, Kh., Alm, Kh., Effects of Prolactin in Different Culture Systems on the Maturation of Bovine Oocytes and Their Capacity for Subsequent Development, Ontogenez, 2001, vol. 32, no. 2, pp. 140–147.

    CAS  Google Scholar 

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

    Google Scholar 

  • Lebedeva, I.Yu., Kibardina, T.V., Kuzmina, 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., Singina, G.N., Volkova, N.A., Mormyshev, A.N., Golubev, A.K., and Zinoveva, 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 

  • Lebedeva, I.Yu., Skotti, O.S., and Kuz'mina, T.I., Prolactin Modulation of Theophylline Inhibitory Action on Maturation of Bovine Oocyte-Cumulus Complexes in Vitro, Tsitologiia, 2006, vol. 48, no. 12, pp. 1010–1015.

    PubMed  CAS  Google Scholar 

  • Lu, Z., Xia, G., and Zhang, J., Protein Kinase C, Rather than Protein Kinase A Is Involved in Follicle-Stimulating Hormone-Mediated Meiotic Resumption of Mouse Cumulus Cell-Enclosed Oocytes in Hypoxanthine-Supplemented Medium, Mol. Cell Endocrinol., 2001, vol. 182, pp. 225–232.

    Article  PubMed  CAS  Google Scholar 

  • Mattioli, M., Transduction Mechanisms for Gonadotropin-Induced Oocyte Maturation, Zygote, 1994, vol. 2, pp. 347–349.

    Article  PubMed  CAS  Google Scholar 

  • Mayes, M.A. and Sirard, M.A., Effect of Type 3 and Type 4 Phosphodiesterase Inhibitors on the Maintenance of Bovine Oocytes in Meiotic Arrest, Biol. Reprod., 2002, vol. 66, pp. 180–184.

    Article  PubMed  CAS  Google Scholar 

  • Mendes, M.C., Ferriani, R.A., Sals, M.M., Moura, M.D., Carrara, H.H., and de Sa, M.F., Effect of Transitory Hyperprolactinemia on in Vitro Fertilization of Human Oocytes, J. Reprod. Med., 2001, vol. 46, pp. 444–450.

    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 

  • Raymond, D.R., Wilson, L.S., Carter, R.L., and Maurice, D.H., Numerous Distinct PKA-, or EPAC-Based, Signalling Complexes Allow Selective Phosphodiesterase 3 and Phosphodiesterase 4 Coordination of Cell Adhesion, Cell Signal., 2007, vol. 19, pp. 2507–2518.

    Article  PubMed  CAS  Google Scholar 

  • Richard, F.J., Fortier, M.A., and Sirard, M.A., Role of the Cyclic Adenosine Monophosphate-Dependent Protein Kinase in the Control of Meiotic Resumption in Bovine Oocytes Cultured with Thecal Cell Monolayers, Biol. Reprod., 1997, vol. 56, pp. 1363–1369.

    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 

  • Sirard, M.A. and First, N.L., In Vitro Inhibition of Oocyte Nuclear Maturation in the Bovine, Biol. Reprod., 1988, vol. 39, pp. 229–234.

    Article  PubMed  CAS  Google Scholar 

  • Thomas, R.E., Armstrong, D.T., and Gilchrist, R.B., Differential Effects of Specific Phosphodiesterase Isoenzyme Inhibitors on Bovine Oocyte Meiotic Maturation, Dev. Biol., 2002, vol. 244, pp. 215–225.

    Article  PubMed  CAS  Google Scholar 

  • Wise, T. and Maurer, R.R., Follicular Development, Oocyte Viability and Recovery 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, Dom. Anim. Endocrinol., 1994, vol. 11, pp. 35–58.

    Article  CAS  Google Scholar 

  • Wu, X.Q., Zhang, X., Li, X.H., Cheng, H.H., Kuai, Y.R., Wang, S., and Guo, Y.L., Translocation of Classical PKC and Cortical Granule Exocytosis of Human Oocyte in Germinal Vesicle and Metaphase II Stage, Acta Pharmacol., 2006, vol. 27, pp. 1353–1358.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. Yu. Lebedeva.

Additional information

Original Russian Text © I.Yu. Lebedeva, G.N. Singina, L.K. Ernst, A.K. Golubev, 2009, published in Tsitologiya, Vol. 51, No. 7, 2009, pp. 559–564.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lebedeva, I.Y., Singina, G.N., Ernst, L.K. et al. Realization pathways of prolactin modulating effect on the cAMP-dependent mechanism of meiosis regulation in bovine oocytes. Cell Tiss. Biol. 3, 438–444 (2009). https://doi.org/10.1134/S1990519X0905006X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X0905006X

Key words

Navigation