Advertisement

Cell and Tissue Biology

, Volume 2, Issue 5, pp 472–480 | Cite as

Interaction of signal cascades induced by cAMP and prolactin in bovine oocyte-cumulus complexes

  • I. Yu. Lebedeva
  • G. N. Singina
  • N. A. Volkova
  • A. N. Mormishev
  • A. K. Golubev
  • N. A. Zinovieva
Article

Abstract

Prolactin (PRL) is one of the pituitary hormones that participate in controlling mammalian folliculo-and oogenesis. In the present study, the combined action of PRL (50 ng/ml) and dibutyryl cAMP (dbcAMP, 1 mM) on oocyte maturation and the morphologic-functional state of the surrounding cumulus cells was investigated in vitro. It has been shown that PRL completely suppresses the inhibitory effect of dbcAMP on meiosis reinitiation and completion of the oocyte nuclear maturation. Moreover, PRL partly inhibited the dbcAMP-induced cumulus expansion, although it produced an opposite effect in the control medium. In the presence of PRL, the inhibitory effect of dbcAMP on the proliferative activity of cumulus cells, as well as on the PRL-induced suppression of destructive processes in these cells, was revealed. In cumulus cells, the mRNA expression of the long PRL receptor isoform was established by the RT-PCR method. The obtained data indicate an interaction of signal cascades induced by PRL and cAMP in the bovine oocyte-cumulus complexes, with the coupling site of these cascades in oocytes seeming to differ from that in cumulus cells.

Key words

prolactin cAMP oocytes cumulus cells in vitro maturation meiosis 

Abbreviations

dbcAMP

dibutyryl derivative of cAMP

Dp

diplotene

MII

metaphase II

OCC

oocyte-cumulus complexes

RT-PCR

reverse transcription coupled with polymerase chain reaction

PRL

prolactin

TI

telophase I

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Armstrong, D.T., Xia, P., de Gannes, G., Tekpetey, F.R., and Khamsi, F., Differential Effects of Insulin-like Growth Factor-I and Follicle-Stimulating Hormone on Proliferation and Differentiation of Bovine Cumulus Cells and Granulosa Cells, Biol. Reprod. 1996, vol. 54, pp. 331–338.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. Bilodeau-Goeseels, S., Effects of Phosphodiesterase Inhibitors on Spontaneous Nuclear Maturation and cAMP Concentrations in Bovine Oocytes, Theriogenology, 2003, vol. 60, pp. 1679–1690.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. Buccione, R., Vanderhyden, B.C., Caron, P.J., and Eppig, J.J., FSH-Induced Expansion of the Mouse Cumulus Oophorus in Vitro Is Dependent upon a Specific Factor(s) Secreted by the Oocyte, Dev. Biol., 1990, vol. 138, pp. 16–25.PubMedCrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. Degen, J.L., Neubauer, M.G., Degen, S.J.F., Seyfried, C.E., and Morris, D.R., Regulation of Protein Synthesis in Mitogen-Activated Bovine Lymphocytes. Analysis of Actin-Specific and Total mRNA Accumulation and Utilization, J. Biol. Chem., 1983, vol. 258, pp. 12153–12162.PubMedGoogle Scholar
  9. Demura, R., Suzuki, T., Komatsu, H., Jibiki, K., Odagiri, E., Demura, H., and Shizume, K., Prolactin Interacts with Gonadotropin through a Suppression of cAMP Production Probably as a LH-Sensitive Adenylate Cyclase Inhibitor, Endocrinol. Jpn., 1986, vol. 33, pp. 29–35.PubMedGoogle Scholar
  10. Gilchrist, R.B., Ritter, L.J., and Armstrong, D.T., Oocyte-Somatic Cell Interactions during Follicular Development in Mammals, Anim. Reprod. Sci., 2004, vols. 82–83, pp. 431–446.PubMedCrossRefGoogle Scholar
  11. Gitay-Goren, H., Lindenbaum, E.S., and Kraiem, Z., Prolactin Inhibits hCG-Stimulated Steroidogenesis and cAMP Accumulation, Possibly by Increasing Phosphodiesterase Activity, in Rat Granulosa Cell Cultures, Mol. Cell Endocrinol., 1989, vol. 61, pp. 69–76.PubMedCrossRefGoogle Scholar
  12. Goffin, V., Binart, N., Touraine, P., and Kelly, P.A., Prolactin: The New Biology of an Old Hormone, Annu. Rev. Physiol., 2002, vol. 64, pp. 47–67.PubMedCrossRefGoogle Scholar
  13. Ikeda, S., Imai, H., and Yamada, M., Apoptosis in Cumulus Cells during in Vitro Maturation of Bovine Cumulus-Enclosed Oocytes, Reproduction, 2003, vol. 125, pp. 369–376.PubMedCrossRefGoogle Scholar
  14. Jabbour, H.N., and Kelly, P.A., Prolactin Receptor Subtypes: A Possible Mode of Tissue Specific Regulation of Prolactin Function, Rev. Reprod., 1997, vol. 2, pp. 14–18.PubMedCrossRefGoogle Scholar
  15. 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.PubMedCrossRefGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. Krasnow, J.S., Hickey, G.L., and Richards, J.S., Regulation of Aromatase Messenger RNA and Estradiol Biosynthesis in Rat Ovarian Granulosa and Luteal Cells by Prolactin, Mol. Endocrinol., 1990, vol. 4, pp. 13–21.PubMedCrossRefGoogle Scholar
  18. Kuzmina, 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, Ontogenez, 2001, vol. 32, no. 2, pp. 140–147.Google Scholar
  19. Lakin, G.F., Biometriya (Biometry), Moscow: Vysshaya Shkola, 1990.Google Scholar
  20. Lebedeva, I.Yu., Kibardina, T.V., and Kuzmina, T.I., Participation of Granulosa Cells in Mediation of Prolactin and Somatotropin Action on Bovine Oocyte-Cumulus Complexes in Vitro, Tsitologiya, 2005, vol. 47, no. 10, pp. 882–888.Google Scholar
  21. Lebedeva, I.Yu., Kuzmina, T.I., and Goilo, T.A., The Influence of Prolactin on DNA Synthesis in Cultured Cow Granulosa Cells, Tsitologiya, 1995, vol. 37, no. 3, pp. 220–226.Google Scholar
  22. Lebedeva, I.Yu., Kuzmina, T.I., Kibardina, T.V., Shokin, O.V., Schneider, F., Alm, H., and Torner, H., The Influence of Somatotropin, Prolactin, and Insulin on Granulosa Cells from Bovine Atretic Follicles, Ross. Fiziol. Zh. im. I.M. Sechenova, 2004, vol. 90, no. 10, pp. 1281–1288.PubMedGoogle Scholar
  23. Lebedeva, I.Yu., Lebedev, V.A., and Kuzmina, T.I., Characterization of Somatotropin-and Prolactin-Binding Sites on Bovine Granulosa Cells Using Homologous Hormones, Biokhimiya, 2001, vol. 66, no. 9, pp. 1188–1194.Google Scholar
  24. Lebedeva, I.Yu., Skotti, O.S., and Kuzmina, T.I., Prolactin Modulation of Theophylline Inhibitory Action on Maturation of Bovine Oocyte-Cumulus Complexes in Vitro, Tsitologiya, 2006, vol. 48, no. 12, pp. 1010–1015.Google Scholar
  25. Luciano, A.M., Modina, S., Vassena, R., Milanesi, E., Lauria, A., and Gandolfi, F., Role of Intracellular Cyclic Adenosine 3′,5′-Monophosphate Concentration and Oocyte-Cumulus Cells Communications on the Acquisition of the Developmental Competence during in Vitro Maturation of Bovine Oocyte, Biol. Reprod., 2004, vol. 70, pp. 465–472.PubMedCrossRefGoogle Scholar
  26. Markström, E., Svensson, E.C., Shao, R., Svanberg, B., and Billig, H., Survival Factors Regulating Ovarian Apoptosis-Dependence on Follicle Differentiation, Reproduction, 2002, vol. 123, pp. 23–30.PubMedCrossRefGoogle Scholar
  27. Mattioli, M., Transduction Mechanisms for Gonadotropin-Induced Oocyte Maturation, Zygote, 1994, vol. 2, pp. 347–349.PubMedCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. Schuetz, A.W., Whittingham, D.G., and Snowden, R., Alterations in the Cell Cycle of Mouse Cumulus Granulosa Cells during Expansion and Mucification in Vivo and in Vitro, Reprod. Fertil. Dev., 1996, vol. 8, pp. 935–943.PubMedCrossRefGoogle Scholar
  32. Schuler, L.A., Nagel, R.J., Gao, J., Horseman, N.D., and Kessler, M.A., Prolactin Receptor Heterogeneity in Bovine Fetal and Maternal Tissues, Endocrinology, 1997, vol. 138, pp. 3187–3194.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. Sirard, M.A., Resumption of Meiosis: Mechanism Involved in Meiotic Progression and Its Relation with Developmental Competence, Theriogenology, 2001, vol. 55, pp. 1241–1254.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. Torner, H., Brüssow, K.P., Alm, H., Ratky, J., Pöhland, R., Tuchscherer, A., and Kanitz, W., Mitochondrial Aggregation Patterns and Activity in Porcine Oocytes and Apoptosis in Surrounding Cumulus Cells Depends on the Stage of Preovulatory Maturation, Theriogenology, 2004, vol. 61, pp. 1675–1689.PubMedCrossRefGoogle Scholar
  37. Vanderhyden, B.C., Species Differences in the Regulation of Cumulus Expansion by an Oocyte-Secreted Factor (s), J. Reprod. Fertil., 1993, vol. 98, pp. 219–227.PubMedCrossRefGoogle Scholar
  38. Vlahos, N.P., Bugg, E.M., Shamblott, M.J., Phelps, J.Y., Gearhart, J.D., and Zacur, H.A., Prolactin Receptor Gene Expression and Immunolocalization of the Prolactin Receptor in Human Luteinized Granulosa Cells, Mol. Hum. Reprod., 2001, vol. 7, pp. 1033–1038.PubMedCrossRefGoogle Scholar
  39. Zhang, M., Tao, Y., Zhou, B., Xie, H., Wang, F., Lei, L., Huo, L., Sun, Q., and Xia, G., Atrial Natriuretic Peptide Inhibits the Actions of FSH and Forskolin in Meiotic Maturation of Pig Oocytes via Different Signalling Pathways, J. Mol. Endocrinol., 2005, vol. 34, pp. 459–472.PubMedCrossRefGoogle Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  • I. Yu. Lebedeva
    • 1
    • 2
  • G. N. Singina
    • 1
  • N. A. Volkova
    • 1
  • A. N. Mormishev
    • 1
  • A. K. Golubev
    • 2
  • N. A. Zinovieva
    • 1
  1. 1.All-Russian State Research Institute of Animal BreedingPodolsk, Moscow oblastRussia
  2. 2.Department of Animal Genetics, Breeding, and BiotechnologySt. Petersburg State Agrarian UniversitySt. Petersburg, PushkinRussia

Personalised recommendations