Summary
Urogenital morphogenesis and cytodifferentiation are presented in the context of the epithelial-stromal interaction. The essential role of stroma in these processes is reviewed.
Similar content being viewed by others
References
Spemann, H. 1939.Embryonic Development and Induction. Yale University Press, New Haven.
Grobstein, C. 1967. Mechanisms of organogenetic tissue interactions. Nat. Cancer Inst. Monogr. 26: 279–299.
Saxen, L. 1977. Directive versus permissive induction: A working hypothesis. In: J. W. Lash, and M. M. Burger (Eds.),Cell and Tissue Interactions. Raven Press, New York, pp. 1–10.
Saxen, L. 1977. Morphogenetic tissue interactions: An introduction. In: M. Karkinen-Jaaskelainen, and L. Saxen (Eds.),Cell Interactions in Differentiation. Academic Press, New York, pp. 145–152.
Saxen, L., M. Karkinen-Jaaskelainen, E. Lehtonen, S. Nordling, and J. Wartiovaara. 1976. Inductive tissue interactions. In: G. Poste, and G. L. Nicolson (Eds.),The Cell Surface in Animal Embryogenesis and Development. North-Holland Publishing Co., New York, pp. 331–408.
Kratochwil, K. 1972. Tissue interactions during embryonic development: General properties. In: D. Tarin (Ed.),Tissue Interactions in Carcinogenesis. Academic Press, New York, pp. 1–47.
Kollar, E. J. 1972. The development of the integument: Spatial, temporal, and phylogenetic factors. Am. Zool. 12: 125–135.
Pictet, R. L., S. Filosa, P. Phelps, and W. J. Rutter. 1975. Control of DNA synthesis in the embryonic pancreas: Interaction of the mesenchymal factor and cyclic AMP. In: H. C. Slavkin, and R. C. Greulich (Eds.),Extracellular Matrix Influences on Gene Expression. Academic Press, New York, pp. 531–540.
Baumann, K. R., and H. L. Hosick. 1979. Replication of mouse mammary tumor cells in monolayer cultures stimulated with embryo extract. Exp. Cell Biol., in press.
Cunha, G. R. 1972. Support of normal salivary gland morphogenesis by mesenchyme derived from accessory sexual glands of embryonic mice. Anat. Rec. 173: 205–212.
Lawson, K. A. 1972. The role of mesenchyme in the morphogenesis and functional differentiation of rat salivary epithelium. J. Embryol. Exp. Morphol. 27: 497–513.
Kollar, E. J., and G. R. Baird. 1970. Tissue interaction in embryonic mouse tooth germs. II. The inductive role of the dental papilla. J. Embryol. Exp. Morphol. 24: 173–186.
Cunha, G. R. 1976. Epithelial-stromal interactions in development of the urogenital tract. Int. Rev. Cytol. 47: 137–194.
Cunha, G. R. 1970. Epithelio-mesenchymal interaction in the develo** accessory sexual glands of the mouse embryo (abstr.). Anat. Rec. 166: 295.
Cunha, G. R. 1972. Epithelio-mesenchymal interactions in primordial gland structures which become responsive to androgenic stimulation. Anat. Rec. 172: 179–196.
Cunha, G. R. 1975. The age-dependent loss in responsiveness of vagina in forming prostate as a function of the epithelial-stromal interaction (abstr.). Anat. Rec. 181: 340.
Cunha, G. R. 1975. Age-dependent loss of sensitivity of female urogenital sinus to androgenic conditions as a function of the epithelial-stromal interaction in mice. Endocrinology 95: 665–673.
Cunha, G. R., and B. Lung. 1978. Age-dependent factors governing androgen-responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice (abstr.). Anat. Rec. 190: 373–374.
Cunha, G. R., and B. Lung. 1978. The possible influence of temporal factors in androgenic responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice. J. Exp. Zool. 205: 181–204.
Cunha, G. R. 1972. Tissue interactions between epithelium and mesenchyme of urogenital and integumental origin. Anat. Rec. 172: 529–542.
Lung, B., G. R. Cunha, and B. A. Reese. Heterotypic differentiation of mouse urinary bladder epithelium: Prostatic induction by urogenital sinus mesenchyme. Manuscript in preparation.
Weniger, J.-P., and A. Zeis. 1972. Sur la secretion precoce de testosterone par le testicule embryonaire de souris. C. R. Acad. Sci. 275: 1431–1433.
Forsberg, J.-G. 1973. Cervicovaginal epithelium: Its origin and development. Am. J. Obstet. Gynecol. 115: 1025–1043.
Cunha, G. R. 1975. The dual origin of vaginal epithelium. Am. J. Anat. 143: 387–392.
Cunha, G. R. 1976. Stromal induction and specification of uterine and vaginal morphogenesis in neonatal mice (abstr.). Anat. Rec. 184: 386.
Cunha, G. R. 1976. Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Müllerian ducts and urogenital sinus during development of the uterus and vagina in mice. J. Exp. Zool. 196: 361–370.
Wartiovaara, J., S. Nordling, E. Lehtonen, and L. Saxen. 1974. Transfilter induction of kidney tubules: Correlation with cytoplasmic penetration into nucleopore filters. J. Embryol. Exp. Morphol. 31: 667–682.
Slavkin, H. C., G. N. Trump, A. Brownell, and N. Sorgente. 1977. Epithelial-mesenchymal specificity. In: J. W. Lash, and M. M. Burger (Eds.),Cell and Tissue Interactions. Raven Press, New York, pp. 29–46.
Thesleff, I. 1977. Tissue interactions in tooth developmentin vitro. In: M. Karinen-Jaaskelainen, and L. Saxen (Eds.),Cell Interactions in Development. Academic Press, New York, pp. 191–209.
Thesleff, I., E. Lehtonen, J. Wartiovaara, and L. Saxen. 1977. Interference of tooth differentiation with interposed filters. Dev. Biol. 58: 197–203.
Saxen, L., and J. Kohonen. 1969. Inductive tissue interactions in vertebrate morphogenesis. Int. Rev. Exp. Pathol. 69: 57–128.
Grobstein, C. 1955. Tissue interaction in the morphogenesis of mouse embryonic rudimentsin vitro. In: D. Rudnick (Ed.),Aspects of Synthesis and Order in Growth. Princeton University Press, Princeton, N.J., pp. 233–256.
Bernfield, M. R., R. H. Cohn, and S. D. Banerjee. 1973. Glycosaminoglycans and epithelial organ formation. Am. Zool. 13: 1067–1083.
Hay, E. D.. 1977. Cell-matrix interaction in embryonic induction. In: B. R. Brinkley, and K. R. Porter (Eds.),International Cell Biology. Rockefeller University Press, New York, pp. 50–60.
Cunha, G. R., and A. K. Lee. 1977. Ultrastructural aspects of vaginal differentiation in untreated and estradiol-treated neonatal mice (abstr.). J. Electron Microsc. 26: 170.
Cunha, G. R., A. K. Lee, and B. Lung. 1978. Electron microscopic observations of vaginal development in untreated and neonatally-estrogenized BALB/c Crgl mice. Am. J. Anat. 152: 343–381.
Takasugi, N., and Y. Kamishima. 1973. Development of vaginal epithelium showing irreversible proliferation and cornification in neonatally estrogenized mice: An electron microscope study. Dev. Growth Differ. 15: 127–140.
Forsberg, J.-G., and A. Abro. 1971. Ultrastructural differences between the sinus and the müllerian epithelium of the mouse vaginal anlage. Z. Anat. Entwicklungsgesch. 135: 67–75.
Forsberg, J.-G., and A. Abro. 1973. Ultrastructural studies on cell degeneration in the mouse utero-vaginal anlage. Acta Anat. 83: 353–367.
Juillard, M. T. 1972. Ultrastructure de l'epithelium vaginal de la souris au cours de la differenciation. Arch. Anat. Microsc. Morphol. Exp. 61: 33–46.
Meier, S., and E. D. Hay. 1975. Control of corneal differentiationin vitro by extracellular matrix In: H. C. Slavkin, and R. C. Greulich (Eds.)Extracellular Matrix Influences on Gene Expression Academic Press, New York, pp. 185–196.
Cunha, G. R., B. Lung, E. Starkey, and A. K. Lee. 1978. Uptake of basal laminar material by vaginal epithelial cells, manuscript in preparation.
Billingham, R. E., and W. K. Silvers 1968. Dermoepidermal interactions and epithelial specificity. In: R. Fleischmajer, and R. E. Billingham (Eds.),Epithelial-Mesenchymal Interactions. Williams and Wilkins, Baltimore, pp. 252–266.
Van Scott, E. J., and R. P. Reinertson. 1961. The modulating influence of stromal environment on epithelial cells studied in human autotransplants. J. Invest. Dermatol. 36: 109–131.
Briggamen, R. A., and C. E. Wheeler. 1968. Epidermal-dermal interactions in adult human skin: Role of dermis in epidermal maintenance. J. Invest. Dermatol. 51: 454–465.
Redler, P., and E. S. Lustig. 1968. Differences in the growth-promoting effect of normal and peritumoral dermis on epidermisin vitro. Dev. Biol. 17: 679–691.
Cohen, J. 1969. Dermis, epidermis and dermal papillae interacting. In: W. Montagna, and R. L. Dobson (Eds.),Advances in Biology of Skin and Hair Growth. Vol. 9. Pergamon Press, New York, pp. 1–18.
Friedenwald, J. S. 1951. Growth pressure and metaplasia of conjunctival and corneal epithelium. Doc. Ophthalmol. 5: 184–192.
Karring, T., N. P. Lang, and H. Loe. 1975. The role of gingival connective tissue in determining epithelial differentiation. J. Periodontal Res. 10: 1–11.
Lasfargues, E. Y. 1957. Cultivation and behaviorin vitro of the normal mammary epithelium of the adult mouse. II. Observations on the secretory activity. Exp. Cell Res. 13: 553–562.
Sakakura, T., Y. Nishizuka, and C. J. Dawe. 1979. Capacity of adult mammary fat pad to interact morphogenetically with embryonic mammary epithelium. J. Nat'l. Cancer Instit., submitted for publication.
Franks, L. M., P. N. Riddle, A. W. Carbonelli, and G. O. Gey. 1970. A comparative study of the ultrastructure and lack of growth capacity of adult human prostate epithelium mechanically separated from its stroma. J. Pathol. 100: 113–119.
Saxen, L., and S. Toivonen. 1962.Primary Embryonic Induction. Prentice-Hall, Inc., Englewood Cliffs, N.J.
Saxen, L., and J. Rapola 1969.Congenital Defects. Holt, Rinehart and Winston, Inc., New York.
Liao, S., S. Fang, J. L. Tymoczko, and T. Liang. 1974. Androgen receptors, antiandrogens, and uptake and retention of androgens in male sex accessory organs. In: D. Brandes (Ed.),Male Accessory Sex Organs. Structure and Function in Mammals. Academic Press. New York, 237–265.
Liao, S. 1976. Receptors and the mechanism of action of androgen. In: J. R. Pasqualini (Ed.),Receptors and Mechanism of Actions of Steroid Hormones Marcel Dekker, Inc., New York, pp. 159–214.
Mainwaring, W. I. P. 1977.The Mechanism of Action of Androgens. Springer-Verlag, New York. 1–173.
Drews, U., S. R. Blecher, D. A. Owen, and S. Ohno. 1974. Genetically directed preferential X-activation seen in mice. Cell 1: 3–8.
Ohno, S. 1977. Testosterone and cellular response. In: R. J. Blandau, and D. Bergsma (Eds.),Morphogenesis and Malformation of the Genital System. A. R. Liss, Inc. New York, pp. 99–108.
Kratochwil, K., and P. Schwartz 1976 Tissue interaction in androgen response of embryonic mammary rudiment of mouse: Identification of target tissue for testosterone. Proc. Nat. Acad. Sci. U.S.A. 73: 4041–4044.
Drews, U., and U. Drews 1977. Regression of mouse mammary gland anlagen in recombinants of Tfm and wild-type tissues: Testosterone acts via the mesenchyme. Cell 10: 401–404.
Allen, E., F. L. Hisaw, and W. U. Gardner 1939. The endocrine functions of the ovaries. In: E. Allen (Ed.)Sex and Internal Secretions. Williams and Wilkins Co., Baltimore, pp. 452–629.
Takasugi, N., T. Kimura, and T. Mori. 1970. Irreversible changes in mouse vaginal epithelium induced by early postnatal treatment with steroid hormones.Symposium of the Czechoslovak Academy of Sciences, Liblice. Academa Publishing House of the Czechoslovak Academy of Sciences, Prague, pp. 229–251.
Takasugi, N. 1976. Cytological basis for permanent vaginal changes in mice treated neonatally with steroid hormones. Int. Rev. Cytol. 44: 193–224.
Takasugi, N., and H. A. Bern. 1964. Tissue changes in mice with persistent vaginal cornification induced by early postnatal treatment with estrogen. J. Nat. Cancer Inst. 33: 855–865.
Takasugi, N. 1972. Carcinogenesis by vaginal transplants from ovariectomized, neonatally estrogenized mice into ovariectomized normal hosts. Gann 63: 73–77.
Kimura, R., and S. Nandi 1967. Nature of induced persistent vaginal cornification in mice. IV. Changes in the vaginal epithelium of old mice treated neonatally with estradiol or testosterone. J. Nat. Cancer Inst. 39: 75–93.
Forsberg, J.-G. 1972. Estrogen, vaginal cancer, and vaginal development. Am. J. Obstet. Gynecol. 113: 83–87.
Forsberg, J.-G. 1975 Late effects in vaginal and cervical epithelia after injections of diethylstilbestrol into neonatal mice. Am. J. Obstet. Gynecol. 121: 101–104.
Bern, H. A., L. A. Jones, T. Mori, and P. N. Young. 1975. Exposure of neonatal mice to steroids: Long-term effects on the mammary gland and other reproductive structures. Steroid biochem. 6: 673–676.
Cunha, G. R., B. Lung, and K. Kato 1977. Role of the epithelial-stromal interaction during the development and expression of ovary-independent vaginal hyperplasia. Dev. Biol. 56: 52–67.
Hodges, G. M., R. M. Hicks, and G. D. Spacey. Epithelial-stromal interactions in normal and chemical carcinogen-treated adult bladder. Cancer Res. 37: 3720–3730.
Bern, H. A. The neonatal mouse—tumorigenesis after short-term exposure to hormones and its possible relevance to human syndromes. In:Procedures on the Symposium on Endocrine-Induced Neoplasia, in press.
Takasugi, N. 1971. Morphogenesis of estrogen-independent proliferation and cornification of the vaginal epithelium in neonatally estrogenized mice. Proc. Jpn. Acad. 47: 193–198.
Shirahama, T., and A. S. Cohen. 1970. The association of hemidesmosome-like plaque and dense coating with the pinocytic uptake of heterologous fibrillar protein (amyloid) by macrophages. J. Ultrastruct. Res. 33: 587–597.
Laguens, R. 1972. Subepithelial fibrils associated with the basement membrane of human cervical epithelium. J. Ultrastruct. Res. 41: 202–208.
Krawczyk, W. S., and G. F. Wilgram 1973. Hemidesmosomes and desmosome morphogenesis during epidermal wound healing. J. Ultrastruct. Res. 45: 93–101.
Beerens, E. G. J., J. W. Slot, and J. C. van der Leun. 1975. Rapid regeneration of the dermal-epidermal junction after partial separation by vacuum: An electron microscopic study. J. Invest. Dermatol. 65: 513–521.
Christophers, E., and H. H. Wolff. 1975. Differential formation of desmosomes and hemidesmosomes in epidermal cell cultures treated with retinoic acid. Nature 256: 209–210.
Cunha, G. R., and A. K. Lee 1978. The possible role of hemidesmosomes in neonatally estrogen-induced selection of a permanently altered abnormal vaginal epithelium. J. Exp. Zool. 203: 361–370.
Burgos, M. H., and G. B. Wislocki 1958. The cyclical changes in the mucosa of the guinea pig's uterus, cervix and vagina and in the sexual skin, investigated by the electron microscope. Endocrinology 63: 106–121.
Cooper, R. A., R. D. Cardiff, and S. R. Wellings. 1967. Ultrastructure of vaginal keratinization in estrogen treated immature BALB/c, CRGL mice. Z. Zellforsch. Mikrosk. Anat. 77: 377–403.
Parakkal, P. F., and A. T. Gregoire. 1972. Differentiation of vaginal epithelium in the normal and hormone-treated rhesus monkey. Physiol. Reprod. 6: 117–130.
Schuchner, E. G., A. Foix, C. A. Borenstein, and C. Marchese. 1974. Electron microscopy of human vaginal epithelium under normal and experimental conditions. J. Reprod. Fertil. 36: 231–233.
Cutler, L. S., and A. P. Chaudhry 1973. Intercellular contacts at the epithelial-mesenchymal interface during the prenatal development of the rat submandibular gland. Dev. Biol. 33: 229–240.
Cutler, L. S. 1977. Intercellular contacts at the epithelial-mesenchymal interface of the develo** rat submandibular glandin vitro. J. Embryol. Exp. Morphol. 39: 71–77.
Saxen, L. 1975. Transmission and spread of kidney tubule induction. In: H. C. Slavkin, and R. C. Greulich (Eds.),Extracellular Matrix Influences in Gene Expression. Academic Press, New York, pp. 523–530.
Mathan, M., J. A. Hermos, and J. S. Trier. 1972. Structural features of the epithelio-mesenchymal interface of rat duodenal mucosa during development. J. Cell Biol. 52: 577–588.
Bluemink, J. G., P. Van Maruik, and K. A. Lawson. 1976. Intimate cell contacts at the epithelial/mesenchymal interface in embryonic mouse lung. J. Ultrastruct. Res. 55: 257–270.
Bernfield, M. R., and N. K. Wessells. 1970. Intra- and extracellular control of epithelial morphogenesis. Dev. Biol. Suppl. 4: 195–249.
Manasek, F. J. 1975. The extracellular matrix: A dynamic component of the develo** embryo. Curr. Top. Dev. Biol. 10: 35–102.
Hay, E. D. 1977. Interactions between the cell surface and extracellular matrix in corneal development. In: J. W. Lash, and M. M. Burger (Eds.),Cell and Tissue Interactions. Raven Press, New York, pp. 115–138.
Gross, J. 1976. Aspects of the animal collagenase. In: G. Ramachandran, and A. H. Reddi (Eds.),Biochemistry of Collagen. Plenum Press, New York, pp. 275–317.
Lung, B., and G. R. Cunha. 1979. Development of seminal vesicles and coagulating glands in neonatal mice. I. The morphogenetic effects of various hormonal conditions. Anat. Rec., submitted for publication.
Cunha, G. R., and B. Lung. 1977. The effect of various hormonal conditions on the morphogenesis of the seminal vesicles (SV) and coagulating glands (CG) of neonatal mice (abstr.). Anat. Rec. 187: 561.
Cunha, G. R., and B. Lung. 1979. Development of seminal vesicles and coagulating glands in neonatal mice. II. Histochemical and autoradiographic localization of glycosaminoglycans. Anat. Rec., submitted for publication.
Bernfield, M. R., and S. D. Banerjee. 1972. Acid mucopolysaccharide (glycosaminoglycan) at the epithelial mesenchymal interface of mouse embryo salivary glands. J. Cell Biol. 52: 664–673.
Bernfield, M. R., S. D. Banerjee, and R. H. Cohn. 1972. Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein (proteoglycan) at the epithelial surface. J. Cell Biol. 52: 674–689.
Cohn, R. H., S. D. Banerjee, and M. R. Bernfield. 1977. Basal lamina of embryonic salivary epithelia: Nature of the glycosaminoglycans and organization of extracellular materials. J. Cell Biol. 73: 464–478.
Banerjee, S. D., R. H. Cohn, and M. R. Bernfield. 1977. Basal lamina of embryonic salivary epithelia: Production by the epithelium and role in maintaining lobular morphology. J. Cell Biol. 73: 445–463.
Franks, L. M., and A. A. Barton. 1960 The effects of testosterone on the ultrastructure of the mouse prostatein vivo and in organ cultures. Exp. Cell Res. 19: 35–50.
Sengel, P. 1976.Morphogenesis of Skin. Cambridge University Press, New York, pp. 85–138.
Cooper, M., and H. Pinkus. 1977. Intrauterine transplantation of rat basal cell carcinoma as a model for reconversion of malignant to benign growth. Cancer Res. 37: 2544–2552.
McNeal, J. E. 1978. Origin and evolution of benign prostatic enlargement. Invest. Urol. 15: 340–345.
Stumpf, W. E., and M. Sar. 1976. Autoradiographic localization of estrogen, androgen, progestin, and glucocorticosteroid in “target tissues” and “non-target tissues”. In: J. R. Pasqualini (Ed.),Receptors and Mechanism of Action of Steroid Hormones Marcel Dekker, Inc., New York, pp. 41–84.
Author information
Authors and Affiliations
Additional information
The study was supported in part by Grant No. PDT-8 from the American Cancer Society, and Contract Grants N01-CP-55649 and N01-CP-75875 from the National Cancer Institute.
Rights and permissions
About this article
Cite this article
Cunha, G.R., Lung, B. The importance of stroma in morphogenesis and functional activity of urogenital epithelium. In Vitro 15, 50–71 (1979). https://doi.org/10.1007/BF02627079
Issue Date:
DOI: https://doi.org/10.1007/BF02627079