Abstract
Conversion of the nephrogenic mesenchyme into epithelial tubules requires an inductive stimulus from the ureter bud. Here we show with immunofluorescence techniques that the undifferentiated mesenchyme before induction expresses uniformly type I and type III collagens. Induction both in vivo and in vitro leads to a loss of these proteins and to the appearance of basement membrane components including type IV collagen. This change correlates both spatially and temporally with the determination of the mesenchyme and precedes and morphological events. During morphogenesis, type IV collagen concentrates at the borders of the developing tubular structures where, by electron microscopy, a thin, often discontinuous basal lamina was seen to cover the first pretubular cell aggregates. Subsequently, the differentiating tubules were surrounded by a well-developed basal lamina. No loss of the interstitial collagens was seen in the metanephric mesenchyme when brought into contact with noninducing tissues or when cultured alone. Similar observations were made with nonnephrogenic mesenchyme (salivary, lung) when exposed to various heterotypic tissues known to induce tubules in the nephrogenic mesenchyme. The sequential shift in the composition of the extracellular matrix from an interstitial, mesenchymal type to a differentiated, epithelial type is so far the first detectable response of the nephrogenic mesenchyme to the tubule- inducing signal.
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Selected References
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- Adamson E. D., Ayers S. E. The localization and synthesis of some collagen types in developing mouse embryos. Cell. 1979 Apr;16(4):953–965. doi: 10.1016/0092-8674(79)90110-7. [DOI] [PubMed] [Google Scholar]
- Bornstein P., Sage H. Structurally distinct collagen types. Annu Rev Biochem. 1980;49:957–1003. doi: 10.1146/annurev.bi.49.070180.004521. [DOI] [PubMed] [Google Scholar]
- Conrad G. W., Dessau W., von der Mark K. Synthesis of type III collagen by fibroblasts from the embryonic chick cornea. J Cell Biol. 1980 Mar;84(3):501–512. doi: 10.1083/jcb.84.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeLellis R. A., Sternberger L. A., Mann R. B., Banks P. M., Nakane P. K. Immunoperoxidase technics in diagnostic pathology. Report of a workshop sponsored by the National Cancer Institute. Am J Clin Pathol. 1979 May;71(5):483–488. doi: 10.1093/ajcp/71.5.483. [DOI] [PubMed] [Google Scholar]
- 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]
- Ekblom P., Miettinen A., Saxén L. Induction of brush border antigens of the proximal tubule in the developing kidney. Dev Biol. 1980 Feb;74(2):263–274. doi: 10.1016/0012-1606(80)90429-7. [DOI] [PubMed] [Google Scholar]
- GROBSTEIN C. Morphogenetic interaction between embryonic mouse tissues separated by a membrane filter. Nature. 1953 Nov 7;172(4384):869–870. doi: 10.1038/172869a0. [DOI] [PubMed] [Google Scholar]
- Grobstein C. Mechanisms of organogenetic tissue interaction. Natl Cancer Inst Monogr. 1967 Sep;26:279–299. [PubMed] [Google Scholar]
- Johnson-Muller B., Gross J. Regulation of corneal collagenase production: epithelial-stromal cell interactions. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4417–4421. doi: 10.1073/pnas.75.9.4417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lehtonen E. Epithelio-mesenchymal interface during mouse kidney tubule induction in vivo. J Embryol Exp Morphol. 1975 Dec;34(3):695–705. [PubMed] [Google Scholar]
- Leivo I., Vaheri A., Timpl R., Wartiovaara J. Appearance and distribution of collagens and laminin in the early mouse embryo. Dev Biol. 1980 Apr;76(1):100–114. doi: 10.1016/0012-1606(80)90365-6. [DOI] [PubMed] [Google Scholar]
- Linsenmayer T. F., Toole B. P., Trelstad R. L. Temporal and spatial transitions in collagen types during embryonic chick limb development. Dev Biol. 1973 Dec;35(2):232–239. doi: 10.1016/0012-1606(73)90020-1. [DOI] [PubMed] [Google Scholar]
- Liotta L. A., Abe S., Robey P. G., Martin G. R. Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor. Proc Natl Acad Sci U S A. 1979 May;76(5):2268–2272. doi: 10.1073/pnas.76.5.2268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayne R., Vail M. S., Mayne P. M., Miller E. J. Changes in type of collagen synthesized as clones of chick chondrocytes grow and eventually lose division capacity. Proc Natl Acad Sci U S A. 1976 May;73(5):1674–1678. doi: 10.1073/pnas.73.5.1674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nowack H., Gay S., Wick G., Becker U., Timpl R. Preparation and use in immunohistology of antibodies specific for type I and type III collagen and procollagen. J Immunol Methods. 1976;12(1-2):117–124. doi: 10.1016/0022-1759(76)90101-0. [DOI] [PubMed] [Google Scholar]
- Saxen L., Lehtonen E., Karkinen-Jäskeläinen M., Nordling S., Wartiovaara J. Are morphogenetic tissue interactions mediated by transmissible signal substances or through cell contacts? Nature. 1976 Feb 26;259(5545):662–663. doi: 10.1038/259662a0. [DOI] [PubMed] [Google Scholar]
- Saxén L. Failure to demonstrate tubule induction in a heterologous mesenchyme. Dev Biol. 1970 Dec;23(4):511–523. doi: 10.1016/0012-1606(70)90137-5. [DOI] [PubMed] [Google Scholar]
- 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]
- Saxén L., Lehtonen E. Transfilter induction of kidney tubules as a function of the extent and duration of intercellular contacts. J Embryol Exp Morphol. 1978 Oct;47:97–109. [PubMed] [Google Scholar]
- Saxén L., Saksela E. Transmission and spread of embryonic induction. II. Exclusion of an assimilatory transmission mechanism in kidney tubule induction. Exp Cell Res. 1971 Jun;66(2):369–377. doi: 10.1016/0014-4827(71)90690-2. [DOI] [PubMed] [Google Scholar]
- Thesleff I., Stenman S., Vaheri A., Timpl R. Changes in the matrix proteins, fibronectin and collagen, during differentiation of mouse tooth germ. Dev Biol. 1979 May;70(1):116–126. doi: 10.1016/0012-1606(79)90011-3. [DOI] [PubMed] [Google Scholar]
- Timpl R., Glanville R. W., Wick G., Martin G. R. Immunochemical study on basement membrane (type IV) collagens. Immunology. 1979 Sep;38(1):109–116. [PMC free article] [PubMed] [Google Scholar]
- Timpl R., Rohde H., Robey P. G., Rennard S. I., Foidart J. M., Martin G. R. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed] [Google Scholar]
- Timpl R., Wick G., Gay S. Antibodies to distinct types of collagens and procollagens and their application in immunohistology. J Immunol Methods. 1977;18(1-2):165–182. doi: 10.1016/0022-1759(77)90168-5. [DOI] [PubMed] [Google Scholar]
- Unsworth B., Grobstein C. Induction of kidney tubules in mouse metanephrogenic mesenchyme by various embryonic mesenchymal tissues. Dev Biol. 1970 Apr;21(4):547–556. doi: 10.1016/0012-1606(70)90077-1. [DOI] [PubMed] [Google Scholar]
- Vainio T., Jainchill J., Clement K., Saxén L. Studies on kidney tubulogenesis. VI. Survival and nucleic acid metabolism of differentiating mouse metanephrogenic mesenchyme in vitro. J Cell Physiol. 1965 Dec;66(3):311–317. doi: 10.1002/jcp.1030660308. [DOI] [PubMed] [Google Scholar]
- Vracko R. Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structure. Am J Pathol. 1974 Nov;77(2):314–346. [PMC free article] [PubMed] [Google Scholar]
- Wartiovaara J., Nordling S., Lehtonen E., Saxén L. Transfilter induction of kidney tubles: correlation with cytoplasmic penetration into nucleopore filters. J Embryol Exp Morphol. 1974 Jun;31(3):667–682. [PubMed] [Google Scholar]
- von der Mark K., von der Mark H. Immunological and biochemical studies of collagen type transition during in vitro chrondrogenesis of chick limb mesodermal cells. J Cell Biol. 1977 Jun;73(3):736–747. doi: 10.1083/jcb.73.3.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
