Advertisement

Endocrine

, Volume 3, Issue 9, pp 667–676 | Cite as

Tissue specific and cyclic expression of insulin-like growth factor binding proteins-1,-2,-3,-4,-5,-6 in the rat oviduct

  • Gregory F. Erickson
  • Michael R. Girvigian
  • Ali R. Sadighian
  • Akira Nakatani
  • Nicholas Ling
  • Shunichi Shimasaki
Papers

Abstract

Although much is known about the expression insulin-like growth factors (IGF) and their receptors in the murine oviduct, significantly less is known about the expression of IGF binding proteins (IGFBPs). To fill this gap in our knowledge, we identified and characterized the tissue specific expression of IGFBP-1 to-6 in rat oviducts over the estrous cycle byin situ hybridization and immunocytochemistry. Tissues were analysed on proestrus (P1000 h, P2000 h), estrus (E0200, E1000 h), and diestrus I and II (DI 1100 h, DII 1100 h). IGFBP-1 was undetectable in the oviduct over the cycle. IGFBP-2 was selectively expressed in the luminal epithelium. The mRNA levels were high between P2000 h and E1000 h but low or undetectable thereafter. Immunoreactive IGFBP-2 was strong to very strong in these cells over most of the cycle. IGFBP-3 mRNA was undetectable in the oviduct; however, strong hybridization and immunoreactive signals were present in the mesosalpinx and mesotubarium, particularly at DI and DII. IGFBP-4 mRNA was not detected in the oviduct. In contrast, immunoreactive IGFBP-4 was observed in the luminal epithelium and the intensity was very strong after ovulation (E1000 h, DI and DII). IGFBP-5 and-6 mRNAs were selectively expressed in circular smooth muscle cells. Hybridization signals were evident over the cycle, but were greatest at estrus. By comparison, IGFBP-5 and-6 proteins were essentially undetectable in these cells except at DII 1100 h when immunostaining was moderate to high. Luminal epithelial cells were weakly positive for IGFBP-5 and-6. However, intense immunostaining was associated with the ciliated border and the luminal fluid juxtaposed to these cells during the cycle. The oocyte-cumulus complexes were immunostained intensely for IGFBP-2,-4,-5 and-6, but their mRNAs were undetectable. The signals were strongest in degenerating cumulus cells suggesting a potential role for these IGFBPs in cumulus apoptosis. These results demonstrate that the estrous cycle is accompanied by major changes in the pattern of expression of IGFBP-2,-4,-5 and-6 in the rat oviduct. We therefore conclude that the regulated production of these particular IGFBPs may be functionally important in modulating IGF activities in the oviduct, oocyte cumulus complexes, and perhaps the preimplantation embryo as well.

Keywords

IGFBPs oviduct ratin situ hybridization immunocytochemistry 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bicsak, T., Shimonaka, M., Malkowski, M. & Ling, N. (1990).Endocrinology,126, 2184–2189.PubMedGoogle Scholar
  2. Brown, A., Chiariotti L., Orlowski, C., Tornell, J. & Billig, H. (1989).J. Biol. Chem. 264, 5148–5154.PubMedGoogle Scholar
  3. Carlsson, B., Hillensjo, T., Nilsson, A.et al. (1993).Endocrinology,133, 2031–2039.PubMedCrossRefGoogle Scholar
  4. Dey, S.K. & Paria, B.C. (1993). In:Preimplantation Embryo Development. Bavister, B.D. (ed.). Springer-Verlag: New York. pp. 264–275.Google Scholar
  5. Erickson, G.F., Nakatani, A., Ling, N. & Shimasaki, S. (1992a).Endocrinology,130, 625–636.PubMedCrossRefGoogle Scholar
  6. Erickson, G.F., Nakatani, A., Ling, N. & Shimasaki, S. (1992b).Endocrinology,130, 1867–1878.PubMedCrossRefGoogle Scholar
  7. Erickson, G., Nakatini, A., Liu, X-J., Shimasaki, S. & Ling, N. (1994a). In:Molecular Biology of the Female Reproductive System. Findlay, J. (ed.). Academic Press: London. pp. 101–127.Google Scholar
  8. Erickson, G.F., Li, D., Sadrkhanloo, R., Liu, X.-J., Shimasaki, S. & Ling, N. (1994b).Endocrinology,134: 1365–1372.PubMedCrossRefGoogle Scholar
  9. Erickson, G.F., Li, D., Shimasaki, S., Ling, N. & Magoffin, D. (1995).Endocrine,3, 525–531.CrossRefGoogle Scholar
  10. Ewton, D.Z. & Florini, J.R. (1981).Dev. Biol.,86, 31–39.PubMedCrossRefGoogle Scholar
  11. Forcelledo, M., Cerda, M. & Croxatto, H. (1986).Endocrinology,119, 1189–1193.PubMedGoogle Scholar
  12. Fuentealba, B., Nieto, M. & Croxatto, H. (1987).Biol. Reprod.,38, 63–69.CrossRefGoogle Scholar
  13. Girvigian, M., Nakatani, A., Ling, N., Shimasaki, S. & Erickson, G. (1994).Biol. Reproduc.,51, 296–302.CrossRefGoogle Scholar
  14. Giudice, L., Dsupin, B., Irwin, J. & Eckert, R. (1992).Fertil. Steril.,57, 294–301.PubMedGoogle Scholar
  15. Hahnel, A. & Schultz, G. (1994).Endocrinology,134, 1956–1959.PubMedCrossRefGoogle Scholar
  16. Harvey, M. & Kaye, P. (1991).Mol. Reproduc. Devel.,29, 253–258.CrossRefGoogle Scholar
  17. Jones, J.I. & Clemmons, D.R. (1995).Endocr. Rev. 16, 3–34.PubMedCrossRefGoogle Scholar
  18. Liu, X.-J., Malkowski, M., Guo, Y.-L., Erickson, G.F., Shimasaki, S. & Ling, N. (1993).Endocrinology,132, 1172–1183.Google Scholar
  19. Michels, K., Lee, W.-H., Seltzer, A., Saavedra, J. & Bondy, C. (1993).Endocrinology,132, 23–29.PubMedCrossRefGoogle Scholar
  20. Murphy, L., Seneviratne, C., Ballejo, G., Croze, F. & Kennedy, T. (1990).Mol. Endocrinol.,4, 329–336.PubMedCrossRefGoogle Scholar
  21. Murphy, L.J. & Barron, D.J. (1993).Molec. Reprod. Devel.,35, 376–381.CrossRefGoogle Scholar
  22. Nakatani, A., Shimasaki, S., Erickson, G.F. & Ling, N. (1991).Endocrinology,129, 1521–1529.PubMedCrossRefGoogle Scholar
  23. Ooi, G., Orlowski, C., Brown, S., Becker, R., Unterman, T. & Rechler, M. (1990).Mol. Endocrinol.,4, 321–328.PubMedGoogle Scholar
  24. Rechler, M. (1993).Vitam. Horm.,47, 1–114.PubMedGoogle Scholar
  25. Ricciarelli, E., Hernandez, E., Hurwitz, A., Kokia, E., Rosenfeld, R., Schwander, J. & Adashi, E. (1991).Endocrinology,129, 2266–2268.PubMedGoogle Scholar
  26. Salamonsen, L. & Nancarrow, C. (1994). In:Molecular Biology of the Female Reproductive System. Findlay, J. (ed) Academic Press, London, pp. 289–328.Google Scholar
  27. Schultz, G.A., Hahnel, A., Arcellana-Panlilio, M., Loang, L., Gouban, S., Watson, A. & Harvey, M. (1993).Molec. Reprod. Dev.,35, 414–420.PubMedCrossRefGoogle Scholar
  28. Shimasaki, S., Koba, A., Mercado, M. & Ling, N. (1989).Biochem. Biophys. Res. Comm.,165, 907–912.PubMedCrossRefGoogle Scholar
  29. Shimasaki, S., Uchiyama, F., Shimonaka, M. & Ling, N. (1990).Molec. Endocrin.,4, 1451–1458.Google Scholar
  30. Shimasaki, S., Shimonaka, M., Zhang, H.-P. & Ling, N. (1991a).J. Biol. Chem.,266, 10646–10653.PubMedGoogle Scholar
  31. Shimasaki, S., Gao, L., Shimonaka, M., Shimonaka, M. & Ling, N. (1991b).Molec. Endocrin.,5, 938–948.Google Scholar
  32. Shimasaki, S. & Ling, N. (1991).Prog. Growth Factor Res.,3, 248–266.CrossRefGoogle Scholar
  33. Silverman, L.A., Cheng, Z.Q., Hsiao, D. & Rosenthal, S.M. (1995).Endocrinology,136, 720–726.PubMedCrossRefGoogle Scholar
  34. Simmons, D., Arriza, J. & Swanson, L. (1989).J. Histotechnol.,12, 169–181.Google Scholar
  35. Smith, M., Freeman, M. & Neill, J. (1975).Endocrinology,96, 219–225.PubMedGoogle Scholar
  36. Stumpf, W. (1969).Endocrinology,85, 31–37.PubMedGoogle Scholar
  37. Zhang, X., Kidder, G., Watson, A., Schultz, G. & Armstrong, P. (1994).J. Reproduc. Fertil.,100, 375–380.CrossRefGoogle Scholar

Copyright information

© Stockton Press 1995

Authors and Affiliations

  • Gregory F. Erickson
    • 1
  • Michael R. Girvigian
    • 1
  • Ali R. Sadighian
    • 1
  • Akira Nakatani
    • 2
  • Nicholas Ling
    • 3
  • Shunichi Shimasaki
    • 4
  1. 1.Department of Reproductive MedicineUniversity of California, San DiegoLa JollaUSA
  2. 2.Department of PathologyNagasaki University School of MedicineNagasakiJapan
  3. 3.Neurocrine Biosciences, Inc.San DiegoUSA
  4. 4.The Scripps Research InstituteLa JollaUSA

Personalised recommendations