Skip to main content
Log in

Ultrastructural changes in the rat endometrium during the normal estrous cycle

Interactions between epithelial cells, stromal cells, macrophages and eosinophils

  • Published:
Medical Electron Microscopy Aims and scope Submit manuscript

Abstract

Dynamic changes in the endometrial stroma during the following 5 stages of the estrous cycle in normal rats were examined by transmission electron microscopy. Diestrus: Macrophages migrated into the endometrial stroma from blood vessels. Proestrus: Eosinophils migrated into the endometrial stroma from blood vessels. They possessed specific crystalloid granules and small granules. Estrus: The endometrial stroma was swollen and stromal cells degenerated. Eosinophils contained a few or no crystalloid granules, while the number of small granules increased. Metestrus-1: Epithelial projections protruded through the basal lamina and established focal adhesions to stromal cells. Stromal cells also adhered to one another. Metestrus-2: Most eosinophils were engulfed by macrophages. In this report, we discuss the interaction of epithelial cells with endometrial stromal cells during the normal estrous cycle.

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Igarashi, T., Sato, S., Aihara, K. andAraki, T.: The ultrastructure of the rat endometrium. Appearance of giant lysosomes in estrus.J. Clin. Electron Microsc. 25, 179–189 (1992).

    Google Scholar 

  2. Igarashi, T., Sato, S., Aihara, K. andAraki, T.: The ultrastructure of the rat endometrium II. Changes of the epithelial cell of endometrium during the normal sexual cycle.J. Clin. Electron Microsc. 26, 77–88 (1993).

    Google Scholar 

  3. Allen, W.M.: Cyclical alterations of the endometrium of the rat during the normal cycle, pseudopregnancy, and pregnancy. II. Production of deciduomata during pregnancy.Anat. Rec. 48, 65–103 (1931).

    Article  Google Scholar 

  4. Gansler, H.: Über ringkernige Gewebsleukocyten im Genitaltrakt der Ratte und ihren Zusammenhang mit weiblichen Sexualhormonen.Virchows Arch. Pathol. Anat. 325, 235–244 (1954).

    Google Scholar 

  5. Rytömaa, T.: Organ distribution and histochemical properties of eosinophil glanulocytes in rat.Acta Pathol. Microbiol. Scand. Suppl. 140, 1–118 (1960).

    Google Scholar 

  6. Bassett, E.G.: Infiltration of eosinophils into the modified connective tissue of estrous and pregnant animals.Nature,194, 1259–1261 (1962).

    Google Scholar 

  7. Ross, R. andKlebanoff, S.J.: The eosinophilic leukocyte. Fine structure studies of changes in the uterus during the estrous cycle.J. Exp. Med. 124, 653–659 (1966).

    Article  CAS  PubMed  Google Scholar 

  8. Sugiura, Y. andMizuhira, V.: Strong affinity of estradiol and its ligands for eosinophilic leukocytes in the rat and mouse uteri during the estrous cycle.Acta Histochem. Cytochem. 17, 665–680 (1984).

    CAS  Google Scholar 

  9. Bjersing, L. andBorglin, N.E.: Effect of hormones on incidence of uterine eosinophilia in rats.Acta Pathol. Microbiol. Scand. 60, 27–35 (1964).

    CAS  PubMed  Google Scholar 

  10. Tachi, C., Tachi, S., Knysznski, A. andLindner, H.R.: Possible involvement of macrophages in embryo-maternal relationships during ovum implantation in the rat.J. Exp. Zool. 217, 81–92 (1981).

    Article  CAS  PubMed  Google Scholar 

  11. Namimatsu, S.: Periodic acid thiosemicarbazide gelatin methenamine silver (PATSC-GMS) staining for transmission electron microscopy.J. Submicrosc. Cytol. Pathol. 24, 19–28 (1992).

    CAS  PubMed  Google Scholar 

  12. Wang, J.M., Griffin, J.D., Rambaldi, A., Chen, Z.G. andMantovani, A.: Induction of monocyte migration by recombinant macrophage colony stimulating factor.J. Immunol. 141, 575–579 (1988).

    CAS  PubMed  Google Scholar 

  13. Pierce, J.H., DiMarco, E., Cox, G.W., Lombardi, D., Ruggiero, M., Varesio, L., Wang, L.M., Choudhury, G.G., Sakaguchi, A.Y., DiFiore, P.P. andAaronson, S.A.: Macrophage colony stimulating factor (CSF-1) induces pro-liferation, chemotaxis, and reversible monocytic differentiation in myeloid progenitor cells transfected with the humanc-fms/CSF-1 receptor cDNA.Proc. Natl. Acad. Sci. 87, 5613–5617 (1990).

    CAS  PubMed  Google Scholar 

  14. Pollard, J.W., Bartocci, A., Arcecci, R., Olofsky, A., Ladner, M.B. andStanley, E.R.: Apparent role of macrophage growth factor in placental development.Nature,330, 484–486 (1987).

    Article  CAS  PubMed  Google Scholar 

  15. Arceci, R.J., Shanahan, F., Stanley, E.R. andPollard, J.W.: Temporal expression and location of colony stimulating factor 1 (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1-regulated placental development.Proc. Natl. Acad. Sci. 86, 8818–8822 (1989).

    CAS  PubMed  Google Scholar 

  16. Regenstreif, L.J. andRossant, J.: Expression of thec-fms protooncogene and of the cytokine CSF-1, during mouse embryogenesis.Dev. Biol. 133, 284–294 (1989).

    Article  CAS  PubMed  Google Scholar 

  17. Wood, G.W., De Mamata, Sanford, T. andChoudhuri, R.: Macrophage colony stimulating factor controls macrophage recruitment to the cycling mouse uterus.Dev. Biol. 152, 336–343 (1992).

    Article  CAS  PubMed  Google Scholar 

  18. Frank, J.S., Langer, G.A., Nudd, L.M. andSeraydarian, K.: The myocardial cell surface, its histochemistry, and the effect of sialic acid and calcium removal on its structure and cellular ionic exchange.Circ. Res. 41, 702–714 (1977).

    CAS  PubMed  Google Scholar 

  19. Kellokumpu-Lehtinen, P., Santti, R. andPelliniemi, L.J.: Correlation of early cytodifferentiation of the human fetal prostate, and Leidig cells.Anat. Rec. 196, 263–273 (1980).

    Article  CAS  PubMed  Google Scholar 

  20. Bluemink, J.G., Van Mauri, P. andLawson, K.A.: Intimate cell contacts at the epithelial/mesenchymal interface in embryonic mouse lung.J. Ultrastruct. Res. 55, 257–270 (1976).

    Article  CAS  PubMed  Google Scholar 

  21. Adamson, I.Y.R. andKing, G.M.: Epithelial-mesenchymal interactions in postnatal rat lung growth.Exp. Lung Res.,8, 261–274 (1985).

    CAS  PubMed  Google Scholar 

  22. Cutler, L.S. andChaudhry, A.P.: Intercellular contacts at the epithelial-mesenchymal interface during the prenatal development of the submandibular gland.Dev. Biol. 33, 229–240 (1973).

    Article  CAS  PubMed  Google Scholar 

  23. Spooner, B.S.: Microfilaments, cell shape changes and morphogenesis of salivary epithelium.Ann. Zool. 13, 1007–1022 (1973).

    Google Scholar 

  24. Rifkind, R.A., Chui, D. andEpler, H.: Ultrastructural study of early morphogenetic events during the establishment of fetal hepatic erythropoiesis.J. Cell Biol. 40, 343–365 (1969).

    Article  CAS  PubMed  Google Scholar 

  25. Mauger, A., Demarchez, M. andSengel, P.: Role of extracellular matrix and of dermal-epidermal junction architecture in skin development. In: Martrices and Cell Differentiation (Kamt, R.B. and Hinchliffe, J.R. ed.), p. 115–128, Liss, New York, 1984.

    Google Scholar 

  26. Slavkin, H.C., Snead, M.L., Zeichner-David, M., Jaskoll, T.F. andSmith, B.T.: Concepts of epithelial-mesenchymal interactions during development: tooth and lung organogenesis.J. Cell Biochem. 26, 117–125 (1984).

    Article  CAS  PubMed  Google Scholar 

  27. Roberts, D.K., Walker, N.J. andLavia, L.A.: Ultrastructural evidence of stromal/epithelial interactions in the human endometrial cycle.Am. J. Obstet. Gynecol. 158, 854–861 (1988).

    CAS  PubMed  Google Scholar 

  28. Lavia, L.A. andLarson, B.A.: Rat endometrial stromal-epithelial response to estrogen infusion.Steroids,56, 123–130 (1991).

    Article  CAS  PubMed  Google Scholar 

  29. Parmley, R.T. andSpicer, S.S.: Cytochemical and ultrastructural identification of a small type glanule in human late eosinophils.Lab. Invest. 30, 557–567 (1974).

    CAS  PubMed  Google Scholar 

  30. Gleich, G.J. andAdolphson, C.R.: The eosinophilic leukocyte: structure and function.Adv. Immunol. 39, 177–253 (1986).

    CAS  PubMed  Google Scholar 

  31. Ackerman, S.J.: “Activated” eosinophils as proinflammatory cells in allergic diseases: biochemistry and functions of eosinophil proteins. In: Immunopharmacology Reviews of the 5th Symposium, Eosinophil in Pathology of Allergy (Makino, S. ed.), p. 3–17, D.M.W. Japan, Tokyo, 1987.

    Google Scholar 

  32. Lindsay, A.D., Malcolm, S., Andrew, L.M. andColin, J.S.: Eosinophilia in transgenic mice expressing interleukin 5.J. Exp. Med. 172, 1425–1431 (1990).

    Google Scholar 

  33. Okuda, M., Yen, C., Okubo, K., Fooanant, S. andPawankar, R.: Cellular elements in the nasal epithelium, especially nasal intraepithelial lymphocytes. In: Immunobiology in Otology, Rhinology and Laryngology (Makabe, B.F., Veldman, J.E. andMogi, G. ed.), Proceedings of the Third International Academic Conference on Immunobiology in Otology, Rhinology and Laryngology, p. 185–193, Kugler, Coronado, 1992.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Igarashi, T., Sato, S., Aihara, K. et al. Ultrastructural changes in the rat endometrium during the normal estrous cycle. Med Electron Microsc 28, 200–209 (1995). https://doi.org/10.1007/BF02347964

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02347964

Key words

Navigation