Skip to main content
Log in

The influence of ovarian steroids on ovine endometrial glycosaminoglycans

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

The ovine endometrium is subjected to cyclic oscillations of estrogen and progesterone in preparation for implantation. One response to fluctuating hormonal levels is the degree of hydration of the tissue, suggesting cyclical alterations in glycosaminoglycan/proteoglycan content. The aim of the present study was to quantitate and characterize glycosaminoglycans in the ovine endometrium during estrogen and progesterone dominant stages. Endogenous endometrial glycosaminoglycan content was determined by chemical analysis and characterized by enzyme specific or chemical degradation. [35S]-sulphate and [3H]-glucosamine labeled proteoglycans/glycosaminoglycans were extracted by cell lysis or with 4M guanidine-HCl. Extracts were purified by anion exchange and gel chromatography and characterized as above. Estrogen and progesterone dominant endometrium contained 3.2 ± 0.1 and 2.1 ± 0.1 mg endogenous glycosaminoglycan/g dehydrated tissue, respectively. Characterization of endogenous glycosaminoglycan showed chondroitin sulphate and hyaluronan contributing over 80%. The major difference between hormonal dominant tissue was a higher estrogenic hyaluronan percentage and a higher progestational keratan sulphate percentage (p < 0.001). Estrogen dominant tissue incorporated 1.6–1.9 fold more radiolabeled proteoglycans/glycosaminoglycans (p < 0.001). Analysis of newly synthesized proteoglycans/glycosaminoglycans revealed a heparan/chondroitin sulphate ratio of 1:2.2–2.5. Keratan sulphate was not detected. Estrogenic hyaluronan was 1.6 fold greater in [3H]-labeled tissue. Analysis of labeled proteoglycans/glycosaminoglycans revealed two size classes with apparent molecular weights >2.0 × 106 and 0.8–1.1 × 105 and a charge class eluting between 0.1–0.5 M NaCl. The greater glycosaminoglycan content (particularly hyaluronan) and synthesis in estrogen dominant tissue supports a role for steroid hormones in endometrial glycosaminoglycan/proteoglycan regulation and consequent tissue hydration. It also suggests a role for these macromolecules in endometrial function and possibly the implantation process. Published in 2003.

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

References

  1. Farach MC, Tang JP, Decker GL, Carson DD, Heparin/heparan sulphate is involved in attachment and spreading of mouse embryos in vitro, Deve Biol 123, 401–10 (1987).

    Google Scholar 

  2. Weigel PH, Frost SJ, McGary CT, LeBoeuf RD, The role of hyaluronic acid in inflammation and wound healing, Int J Tissue React 10, 355–65 (1988).

    Google Scholar 

  3. Wight TN, Kinsella MG, Qwarnstrom EE, The role of proteoglycans in cell adhesion, migration and proliferation, Curr Opin Cell Biol 4, 793–801 (1992).

    Google Scholar 

  4. Scott JE, Haigh M, Proteoglycan-type I collagen fibril interactions in bone and non-calcifying connective tissues, Biosci Rep 5, 71–81 (1985).

    Google Scholar 

  5. Laurent TC, Fraser JR, The properties and turnover of hyaluronan, Ciba Found Symp 124, 9–29 (1986).

    Google Scholar 

  6. Cidadao AJ, Thorsteinsdottir S, David-Ferreira JF, Immunocytochemical study of tissue distribution and hormonal control of chondroitin-, dermatan-and keratan sulfates from rodent uterus, Eur J Cell Biol 52, 105–16 (1990).

    Google Scholar 

  7. Casida LE, McKenzie FF, The oestrous cycle of the ewe; histology of the genital tract, Agricultural Experiment Station Research Bulletin 170, 4–28 (1932).

    Google Scholar 

  8. Fosang AJ, Handley CJ, Santer V, Lowther DA, Thorburn GD, Pregnancy-related changes in the connective tissue of the ovine cervix, Biol Reprod 30, 1223–35 (1984).

    Google Scholar 

  9. Granstrom L, Ekman G, Ulmsten U, Malmstrom A, Changes in the connective tissue of corpus and cervix uteri during ripening and labour in term pregnancy, Br J Obstet Gynaecol 96, 1198–202 (1989).

    Google Scholar 

  10. Kobayashi H, Sun GW, Tanaka Y, Kondo T, Terao T, Serum hyaluronic acid levels during pregnancy and labor, Obstet Gynecol 93, 480–4 (1999).

    Google Scholar 

  11. Norman M, Ekman G, Ulmsten U, Barchan K, Malmstrom A, Proteoglycan metabolism in the connective tissue of pregnant and non-pregnant human cervix.Anin vitro study, Biochem J 275(Pt 2), 515–20 (1991).

    Google Scholar 

  12. Osmers R, Rath W, Pflanz MA, Kuhn W, Stuhlsatz HW, Szeverenyi M, Glycosaminoglycans in cervical connective tissue during pregnancy and parturition, Obstet Gynecol 81, 88–92 (1993).

    Google Scholar 

  13. Wu WX, Zhang Q, Unno N, Derks JB, Nathanielsz PW, Characterization of decorin mRNA in pregnant intrauterine tissues of the ewe and regulation by steroids, Am J Physiol Cell Physiol 278, C199–C206 (2000).

    Google Scholar 

  14. Yanagishita M, Proteoglycans and hyaluronan in female reproductive organs. In Proteoglycans, edited by Jolles P (Birkhauser Vertag Basel, Switzerland, 1994).

    Google Scholar 

  15. Stephens CA, Anastassiadis PA, Comparative distribution of glycosaminoglycans and proteoglycans in the reproductive tissues of the female fowl, Comp Biochem Physiol B 84, 29–35 (1986).

    Google Scholar 

  16. Potter SW, Morris JE, Changes in histochemical distribution of cell surface heparan sulfate proteoglycan in mouse uterus during the estrous cycle and early pregnancy, Anat Rec 234, 383–90 (1992).

    Google Scholar 

  17. Carson DD, Tang JP, Julian J, Glasser SR, Vectorial secretion of proteoglycans by polarized rat uterine epithelial cells, J Cell Biol 107, 2425–35 (1988).

    Google Scholar 

  18. Jacobs AL, Carson DD, Proteoglycan synthesis and metabolism by mouse uterine stroma cultured in vitro, J Biol Chem 266, 15464–73 (1991).

    Google Scholar 

  19. Carson DD, Dutt A, Tang JP, Glycoconjugate synthesis during early pregnancy: Hyaluronate synthesis and function, Deve Biol 120, 228–35 (1987).

    Google Scholar 

  20. Brown JJG, Papaioannou VE, Extracellular matrix remodelling at implantation: Role of hyaluronan. In Molecular and Cellular Aspects of Periimplantation Processes, edited by Dey SK (Springer-Verlag, New York, 1995), p. 125.

    Google Scholar 

  21. Greiss FC, Jr, Wagner WD, Glycosaminoglycans: Their distribution and potential vasoactive action in the nonpregnant and pregnant ovine uterus, Am J Obstet Gynecol 145, 1041–8 (1983).

    Google Scholar 

  22. Kim YJ, Sah RL, Doong JY, Grodzinsky AJ, Fluorometric assay of DNA in cartilage explants using Hoechst 33258, Anal Biochem 174, 168–76 (1988).

    Google Scholar 

  23. Bitter T, Muir H, A modified uronic acid carbazole reaction, Anal Biochem 4, 330–4 (1962).

    Google Scholar 

  24. Goldberg RL, Kolibas LM, An improved method for determining proteoglycans synthesized by chondrocytes in culture, Connect Tissue Res 24, 265–75 (1990).

    Google Scholar 

  25. Robinson HC, Lindahl U, Effect of cycloheximide, beta-Dxylosides and beta-D-galactosides on heparin biosynthesis in mouse mastocytoma, Biochem J 194, 575–86 (1981).

    Google Scholar 

  26. Boutin EL, Sanderson RD, Bernfield M, Cunha GR, Epithelialmesenchymal interactions in uterus and vagina alter the expression of the cell surface proteoglycan, syndecan, Deve Biol 148, 63–74 (1991).

    Google Scholar 

  27. Nicollier M, Beck L, Mahfoudi A, Coosemans V, Adessi GL, Effect of progesterone on hydrophobic cell-associated proteoglycans bound to cholesterol sulfate in glandular epithelial cells of guineapig endometrium, Biochim Biophys Acta 1220, 125–31 (1994).

    Google Scholar 

  28. Smith RA, Seif MW, Rogers AW, Li TC, Dockery P, Cooke ID, Aplin JD, The endometrial cycle: The expression of a secretory component correlated with the luteinizing hormone peak, Hum Reprod 4, 236–42 (1989).

    Google Scholar 

  29. Wewer UM, Damjanov A, Weiss J, Liotta LA, Damjanov I, Mouse endometrial stromal cells produce basement-membrane components, Differentiation 32, 49–58 (1986).

    Google Scholar 

  30. Uldbjerg N, Malmstrom A, Ekman G, Sheehan J, Ulmsten U, Wingerup L, Isolation and characterization of dermatan sulphate proteoglycan from human uterine cervix, Biochem J 209, 497–503 (1983).

    Google Scholar 

  31. Tanaka K, Nakamura T, Ikeya H, Higuchi T, Tanaka A, Morikawa A, Saito Y, Takagaki K, Endo M, Hyaluronate depolymerization activity induced by progesterone in cultured fibroblasts derived from human uterine cervix, FEBS Lett 347, 95–8 (1994).

    Google Scholar 

  32. Tanaka K, Nakamura T, Takagaki K, Funahashi M, Saito Y, Endo M, Regulation of hyaluronate metabolism by progesterone in cultured fibroblasts from the human uterine cervix, FEBS Lett 402, 223–6 (1997).

    Google Scholar 

  33. Johnson ML, Redmer DA, Reynolds LP, Effects of ovarian steroids on uterine growth, morphology, and cell proliferation in ovariectomized, steroid-treated ewes, Biol Reprod 57, 588–96 (1997).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marianne Tellbach.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tellbach, M., Salamonsen, L.A. & Van Damme, MP. The influence of ovarian steroids on ovine endometrial glycosaminoglycans. Glycoconj J 19, 385–394 (2002). https://doi.org/10.1023/B:GLYC.0000004010.24877.2f

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:GLYC.0000004010.24877.2f

Navigation