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PMID: 2461951 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions.

The Journal of cell biology ·Vol. 107 ·No. 6 Pt 1 ·1988-12-00 ·Pages 2341-9

Aufderheide E, Ekblom P

Abstract

Tenascin, an extracellular matrix protein, is expressed in the mesenchyme around growing epithelia in the embryo. We therefore investigated whether epithelial cells can stimulate expression of tenascin in embryonic mesenchyme. Mesenchyme from the presumptive small intestine was used because it is known that reciprocal epithelial-mesenchymal interactions are important for gut morphogenesis. Rat monoclonal antibodies against mouse tenascin were raised and were found to react specifically with mouse tenascin in ELISA. In supernatants of cultured fibroblasts, the antibodies precipitated two peptides of Mr 260 and 210 kD. One of the antibodies also reacted with these tenascin chains in immunoblots of tissue extracts. We found that tenascin was absent during early stages of gut development, at stages when the mesenchyme is already in contact with the stratified epithelium of the endoderm. Rather, it appeared in the mesenchyme when the homogenous endodermal epithelium differentiated into the heterogenous absorptive epithelium. Tenascin remained present in the stroma of the adult gut, close to the migration pathways of the continuously renewing epithelium. When first detected during intestinal differentiation, the 210-kD component was predominant but at birth the relative amount of the 260-kD component had increased. The expression data suggested that the appearance of tenascin in the mesenchyme was dependent on the presence of epithelium. To test this, isolated gut mesenchymes from 13-d-old mouse embryos were cultured for 24 h either alone or together with epithelial and nonepithelial cells. Whereas mesenchyme cultured alone or in the presence of nonepithelial B16-F1 melanoma cells produced only trace amounts of tenascin, expression was strongly stimulated by the epithelial cell line, Madin-Darby canine kidney (MDCK). We propose that growing and differentiating epithelia produce locally active factors which stimulate synthesis of tenascin in the surrounding mesenchyme.

MeSH Terms
Animals Antibodies, Monoclonal/immunology Antibody Specificity Blotting, Western Cell Adhesion Embryonic Induction Epithelium/physiology Fibronectins/physiology Fluorescent Antibody Technique Intestines/embryology Mesoderm/physiology Mice Molecular Weight Precipitin Tests Proteins/physiology Tenascin
Chemicals
Antibodies, Monoclonal Fibronectins Proteins Tenascin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Aufderheide E
Friederich-Miescher-Laboratorium der Max-Planck-Gesellschaft, Tübingen, Federal Republic of Germany.
Ekblom P
References (41)
41 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. Structural features of the epithelio-mesenchymal interface of rat duodenal mucosa during development.
    J Cell Biol. 1972 Mar;52(3):577-88 PMID: 5009520
  3. Metastasis results from preexisting variant cells within a malignant tumor.
    Science. 1977 Aug 26;197(4306):893-5 PMID: 887927
  4. 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):4350-4 PMID: 388439
  5. Specificity of tissue interaction and origin of mesenchymal cells in the androgen response of the embryonic mammary gland.
    Cell. 1980 Feb;19(2):465-71 PMID: 7357614
  6. 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):485-9 PMID: 6987652
  7. Enzyme immunoassay ELISA and EMIT.
    Methods Enzymol. 1980;70(A):419-39 PMID: 6999296
  8. Monoclonal antibodies against trophectoderm-specific markers during mouse blastocyst formation.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):4113-7 PMID: 6933460
  9. Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody.
    Cancer Res. 1983 Jun;43(6):2796-805 PMID: 6342760
  10. Dual origin of glomerular basement membrane.
    Dev Biol. 1984 Jan;101(1):86-96 PMID: 6420214
  11. Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis.
    J Cell Biol. 1984 Jun;98(6):1926-36 PMID: 6725406
  12. Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits.
    J Cell Biol. 1984 Jun;98(6):1937-46 PMID: 6202699
  13. A six-armed oligomer isolated from cell surface fibronectin preparations.
    Nature. 1984 Sep 20-26;311(5983):267-9 PMID: 6482952
  14. Role of muscle fibroblasts in the deposition of type-IV collagen in the basal lamina of myotubes.
    Differentiation. 1984;28(2):164-72 PMID: 6396135
  15. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family.
    Nature. 1985 Jul 11-17;316(6024):146-8 PMID: 2409452
  16. Immunochemical and biochemical characterization of a glioma-associated extracellular matrix glycoprotein.
    J Cell Biochem. 1985;28(3):183-95 PMID: 4066774
  17. 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):8075-9 PMID: 2415980
  18. Site-restricted expression of cytotactin during development of the chicken embryo.
    J Cell Biol. 1986 May;102(5):1917-30 PMID: 2422181
  19. Epithelial-mesenchymal interactions control basement membrane production and differentiation in cultured and transplanted mouse keratinocytes.
    Cell Tissue Res. 1986;244(2):413-29 PMID: 2424607
  20. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis.
    Cell. 1986 Oct 10;47(1):131-9 PMID: 2428505
  21. Mesenchyme-dependent differentiation of epithelial progenitor cells in the gut.
    J Pediatr Gastroenterol Nutr. 1987 Jan-Feb;6(1):14-23 PMID: 3540259
  22. Molecular biology of fibronectin.
    Annu Rev Cell Biol. 1985;1:67-90 PMID: 3916323
  23. Cell-matrix interactions and cell adhesion during development.
    Annu Rev Cell Biol. 1986;2:27-47 PMID: 3548769
  24. Cell adhesion molecules in the regulation of animal form and tissue pattern.
    Annu Rev Cell Biol. 1986;2:81-116 PMID: 3548776
  25. Importance of a fibroblastic support for in vitro differentiation of intestinal endodermal cells and for their response to glucocorticoids.
    Cell Differ. 1987 Mar;20(2-3):171-82 PMID: 3552252
  26. Tenascin is a stromal marker for epithelial malignancy in the mammary gland.
    Proc Natl Acad Sci U S A. 1987 Jul;84(13):4621-5 PMID: 2440026
  27. Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme.
    J Cell Biol. 1987 Jul;105(1):599-608 PMID: 2440899
  28. Biology of mammary fat pad in fetal mouse: capacity to support development of various fetal epithelia in vivo.
    Development. 1987 Jul;100(3):421-30 PMID: 3308404
  29. Hexabrachion proteins in embryonic chicken tissues and human tumors.
    J Cell Biol. 1987 Sep;105(3):1387-94 PMID: 3654758
  30. Characterization of the cell adhesion molecules L1, N-CAM and J1 in the mouse intestine.
    EMBO J. 1987 Sep;6(9):2581-6 PMID: 3315649
  31. Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):7977-81 PMID: 2446315
  32. Laminin and other basement membrane components.
    Annu Rev Cell Biol. 1987;3:57-85 PMID: 3318883
  33. Intestinal cells produce basement membrane proteins in vitro.
    Gut. 1987;28 Suppl:143-51 PMID: 3692300
  34. Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2569-79 PMID: 2447094
  35. Molecular forms, binding functions, and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules.
    J Cell Biol. 1988 Feb;106(2):519-32 PMID: 2448317
  36. A cDNA clone for cytotactin contains sequences similar to epidermal growth factor-like repeats and segments of fibronectin and fibrinogen.
    Proc Natl Acad Sci U S A. 1988 Apr;85(7):2186-90 PMID: 2451243
  37. Tenascin interferes with fibronectin action.
    Cell. 1988 May 6;53(3):383-90 PMID: 2452695
  38. Antibodies to cell surface ganglioside GD3 perturb inductive epithelial-mesenchymal interactions.
    Cell. 1988 Jul 15;54(2):235-45 PMID: 3292056
  39. The distribution of tenascin coincides with pathways of neural crest cell migration.
    Development. 1988 Jan;102(1):237-50 PMID: 2458221
  40. Role of laminin A chain in the development of epithelial cell polarity.
    Cell. 1988 Oct 21;55(2):331-41 PMID: 3048705
  41. Epithelial-mesenchymal interactions in the production of basement membrane components in the gut.
    Development. 1988 Feb;102(2):339-47 PMID: 17061377
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1988-12-00
Pages
2341-9
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2115636
Subset
IM
Corrections
ErratumIn
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