Medical Electron Microscopy

, Volume 28, Issue 3–4, pp 200–209 | Cite as

Ultrastructural changes in the rat endometrium during the normal estrous cycle

Interactions between epithelial cells, stromal cells, macrophages and eosinophils
  • Toshio Igarashi
  • Shigeru Sato
  • Kaoru Aihara
  • Tsutomu Araki


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.

Key words

Ultrastructure Rat Endometrium Eosmophil Macrophage 


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  1. 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. 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. 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).CrossRefGoogle Scholar
  4. 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. 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. 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. 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).CrossRefPubMedGoogle Scholar
  8. 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).Google Scholar
  9. 9).
    Bjersing, L. andBorglin, N.E.: Effect of hormones on incidence of uterine eosinophilia in rats.Acta Pathol. Microbiol. Scand. 60, 27–35 (1964).PubMedGoogle Scholar
  10. 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).CrossRefPubMedGoogle Scholar
  11. 11).
    Namimatsu, S.: Periodic acid thiosemicarbazide gelatin methenamine silver (PATSC-GMS) staining for transmission electron microscopy.J. Submicrosc. Cytol. Pathol. 24, 19–28 (1992).PubMedGoogle Scholar
  12. 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).PubMedGoogle Scholar
  13. 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).PubMedGoogle Scholar
  14. 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).CrossRefPubMedGoogle Scholar
  15. 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).PubMedGoogle Scholar
  16. 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).CrossRefPubMedGoogle Scholar
  17. 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).CrossRefPubMedGoogle Scholar
  18. 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).PubMedGoogle Scholar
  19. 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).CrossRefPubMedGoogle Scholar
  20. 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).CrossRefPubMedGoogle Scholar
  21. 21).
    Adamson, I.Y.R. andKing, G.M.: Epithelial-mesenchymal interactions in postnatal rat lung growth.Exp. Lung Res.,8, 261–274 (1985).PubMedGoogle Scholar
  22. 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).CrossRefPubMedGoogle Scholar
  23. 23).
    Spooner, B.S.: Microfilaments, cell shape changes and morphogenesis of salivary epithelium.Ann. Zool. 13, 1007–1022 (1973).Google Scholar
  24. 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).CrossRefPubMedGoogle Scholar
  25. 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. 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).CrossRefPubMedGoogle Scholar
  27. 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).PubMedGoogle Scholar
  28. 28).
    Lavia, L.A. andLarson, B.A.: Rat endometrial stromal-epithelial response to estrogen infusion.Steroids,56, 123–130 (1991).CrossRefPubMedGoogle Scholar
  29. 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).PubMedGoogle Scholar
  30. 30).
    Gleich, G.J. andAdolphson, C.R.: The eosinophilic leukocyte: structure and function.Adv. Immunol. 39, 177–253 (1986).PubMedGoogle Scholar
  31. 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. 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. 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

Copyright information

© The Clinical Electron Microscopy Society of Japan 1995

Authors and Affiliations

  • Toshio Igarashi
    • 1
  • Shigeru Sato
    • 2
  • Kaoru Aihara
    • 2
  • Tsutomu Araki
    • 1
  1. 1.Department of Obstetrics and GynecologyNippon Medical SchoolTokyoJapan
  2. 2.Central Institute for Electron Microscopic ResearchNippon Medical SchoolTokyoJapan

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