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. 1987 Jul 1;105(1):599–608. doi: 10.1083/jcb.105.1.599

Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme

PMCID: PMC2114901  PMID: 2440899

Abstract

Tenascin, a mesenchymal extracellular matrix glycoprotein, has been implicated in epithelial-mesenchymal interactions during fetal development (Chiquet-Ehrismann, R., E. J. Mackie, C. A. Pearson, T. Sakakura, 1986, Cell, 47:131-139). We have now investigated the expression of tenascin during embryonic development of the mouse kidney. In this system, mesenchymal cells convert into epithelial cells as a result of a tissue interaction. By immunofluorescence, tenascin could not be found in the mesenchyme until kidney tubule epithelial began to form. It then became detectable around condensates and s- shaped bodies, the early stages of tubulogenesis. In an in vitro culture system, tenascin expression by the mesenchyme is tightly coupled to the de novo formation of epithelial, and does not occur if tubulogenesis is suppressed. The results strongly suggest that the formation of the new epithelium stimulates the expression of tenascin in the nearby mesenchyme. During postnatal development, the expression of tenascin decreases and the spatial distribution changes. In kidneys from adult mice, no tenascin can be found in the cortex, but interspersed patches of staining are visible in the medullary stroma. The results strongly support the view that tenascin is involved in epithelial-mesenchymal interactions. It could therefore be crucial for embryonic development.

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Selected References

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  1. Bourdon M. A., Wikstrand C. J., Furthmayr H., Matthews T. J., Bigner D. D. Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res. 1983 Jun;43(6):2796–2805. [PubMed] [Google Scholar]
  2. Brûlet P., Babinet C., Kemler R., Jacob F. Monoclonal antibodies against trophectoderm-specific markers during mouse blastocyst formation. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4113–4117. doi: 10.1073/pnas.77.7.4113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
  4. Chiquet M., Fambrough D. M. Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol. 1984 Jun;98(6):1926–1936. doi: 10.1083/jcb.98.6.1926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chiquet M., Fambrough D. M. Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol. 1984 Jun;98(6):1937–1946. doi: 10.1083/jcb.98.6.1937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooke P. S., Uchima F. D., Fujii D. K., Bern H. A., Cunha G. R. Restoration of normal morphology and estrogen responsiveness in cultured vaginal and uterine epithelia transplanted with stroma. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2109–2113. doi: 10.1073/pnas.83.7.2109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crossin K. L., Hoffman S., Grumet M., Thiery J. P., Edelman G. M. Site-restricted expression of cytotactin during development of the chicken embryo. J Cell Biol. 1986 May;102(5):1917–1930. doi: 10.1083/jcb.102.5.1917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cunha G. R. Epithelio-mesenchymal interactions in primordial gland structures which become responsive to androgenic stimulation. Anat Rec. 1972 Feb;172(2):179–195. doi: 10.1002/ar.1091720206. [DOI] [PubMed] [Google Scholar]
  9. Ekblom P., Alitalo K., Vaheri A., Timpl R., Saxén L. Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis. Proc Natl Acad Sci U S A. 1980 Jan;77(1):485–489. doi: 10.1073/pnas.77.1.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol. 1981 Oct;91(1):1–10. doi: 10.1083/jcb.91.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ekblom P., Lehtonen E., Saxén L., Timpl R. Shift in collagen type as an early response to induction of the metanephric mesenchyme. J Cell Biol. 1981 May;89(2):276–283. doi: 10.1083/jcb.89.2.276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ekblom P., Nordling S., Saxén L. Inhibition of kidney tubule induction by charged polymers. Cell Differ. 1978 Dec;7(6):345–353. doi: 10.1016/0045-6039(78)90035-0. [DOI] [PubMed] [Google Scholar]
  13. Ekblom P., Thesleff I., Miettinen A., Saxén L. Organogenesis in a defined medium supplemented with transferrin. Cell Differ. 1981 Nov;10(5):281–288. doi: 10.1016/0045-6039(81)90010-5. [DOI] [PubMed] [Google Scholar]
  14. Enat R., Jefferson D. M., Ruiz-Opazo N., Gatmaitan Z., Leinwand L. A., Reid L. M. Hepatocyte proliferation in vitro: its dependence on the use of serum-free hormonally defined medium and substrata of extracellular matrix. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1411–1415. doi: 10.1073/pnas.81.5.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Erickson H. P., Inglesias J. L. A six-armed oligomer isolated from cell surface fibronectin preparations. Nature. 1984 Sep 20;311(5983):267–269. doi: 10.1038/311267a0. [DOI] [PubMed] [Google Scholar]
  16. GROBSTEIN C. Trans-filter induction of tubules in mouse metanephrogenic mesenchyme. Exp Cell Res. 1956 Apr;10(2):424–440. doi: 10.1016/0014-4827(56)90016-7. [DOI] [PubMed] [Google Scholar]
  17. Grobstein C. Mechanisms of organogenetic tissue interaction. Natl Cancer Inst Monogr. 1967 Sep;26:279–299. [PubMed] [Google Scholar]
  18. Grumet M., Hoffman S., Crossin K. L., Edelman G. M. Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8075–8079. doi: 10.1073/pnas.82.23.8075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hadley M. A., Byers S. W., Suárez-Quian C. A., Kleinman H. K., Dym M. Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation, and germ cell development in vitro. J Cell Biol. 1985 Oct;101(4):1511–1522. doi: 10.1083/jcb.101.4.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hall H. G., Farson D. A., Bissell M. J. Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4672–4676. doi: 10.1073/pnas.79.15.4672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kratochwil K., Dziadek M., Löhler J., Harbers K., Jaenisch R. Normal epithelial branching morphogenesis in the absence of collagen I. Dev Biol. 1986 Oct;117(2):596–606. doi: 10.1016/0012-1606(86)90328-3. [DOI] [PubMed] [Google Scholar]
  22. Kratochwil K., Schwartz P. Tissue interaction in androgen response of embryonic mammary rudiment of mouse: identification of target tissue for testosterone. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4041–4044. doi: 10.1073/pnas.73.11.4041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 1985 Jul 11;316(6024):146–148. doi: 10.1038/316146a0. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Li M. L., Aggeler J., Farson D. A., Hatier C., Hassell J., Bissell M. J. Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc Natl Acad Sci U S A. 1987 Jan;84(1):136–140. doi: 10.1073/pnas.84.1.136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. POTTER E. L. DEVELOPMENT OF THE HUMAN GLOMERULUS. Arch Pathol. 1965 Sep;80:241–255. [PubMed] [Google Scholar]
  27. Richter A., Sanford K. K., Evans V. J. Influence of oxygen and culture media on plating efficiency of some mammalian tissue cells. J Natl Cancer Inst. 1972 Dec;49(6):1705–1712. doi: 10.1093/jnci/49.6.1705. [DOI] [PubMed] [Google Scholar]
  28. Saxén L., Koskimies O., Lahti A., Miettinen H., Rapola J., Wartiovaara J. Differentiation of kidney mesenchyme in an experimental model system. Adv Morphog. 1968;7:251–293. doi: 10.1016/b978-1-4831-9954-2.50011-2. [DOI] [PubMed] [Google Scholar]
  29. Thiery J. P., Duband J. L., Tucker G. C. Cell migration in the vertebrate embryo: role of cell adhesion and tissue environment in pattern formation. Annu Rev Cell Biol. 1985;1:91–113. doi: 10.1146/annurev.cb.01.110185.000515. [DOI] [PubMed] [Google Scholar]
  30. Thorogood P., Bee J., von der Mark K. Transient expression of collagen type II at epitheliomesenchymal interfaces during morphogenesis of the cartilaginous neurocranium. Dev Biol. 1986 Aug;116(2):497–509. doi: 10.1016/0012-1606(86)90150-8. [DOI] [PubMed] [Google Scholar]
  31. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vaughan L., Huber S., Chiquet M., Winterhalter K. H. A major, six-armed glycoprotein from embryonic cartilage. EMBO J. 1987 Feb;6(2):349–353. doi: 10.1002/j.1460-2075.1987.tb04761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vestweber D., Kemler R., Ekblom P. Cell-adhesion molecule uvomorulin during kidney development. Dev Biol. 1985 Nov;112(1):213–221. doi: 10.1016/0012-1606(85)90135-6. [DOI] [PubMed] [Google Scholar]

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