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Laminins, tenascin and type VII collagen in colorectal mucosa

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Summary

The distribution of different laminin polypeptides, type VII collagen and tenascin has been studied in adult and foetal colorectal mucosa by using the indirect immunofluorescence technique. Immunoreactivity for laminin α1 chain was located to basement membranes of epithelia, muscularis mucosae, and blood vessels, respectively in different segments of adult colon and rectum. Laminin β1 and γ1 chains were additionally expressed in lamina propria. Laminin α2 chain was also found in lamina propria around the pericyptal fibrollasts. Immunoreactivity for laminin β2 chain was restricted to basement membranes in the muscularis mucosae and arteries. Laminin α3 and β3 chains, suggestive for laminin-5, were confined especially to surface epithelial basement membranes. Immunoreactivity for type VII collagen was confined to basement membrane of surface epithelium in a punctate manner, while that for tenascin was seen slightly more broadly in the basement membrane zone and also in the muscular layer. The distribution of laminin chains in 16-week-foetal colon mostly resembled that of corresponding adult tissue, although immunoreactivities for laminin α2 and β2 chains were lacking. Type VII collagen and the high molecular weight isoform of tenascin also absent from the foetal colon. The results show that the basement membrane of the surface epithelium of colon and rectum express the components of epithelial adhesion complex, laminin-5 (α3-β3-γ2) and type VII collagen, resembling in this respect small intestine and stomach while laminin-2 (α2-β1-γ1) appears to be associated with pericryptal fibroblasts, and laminin-1 (α1-β1-γ1) widely in most basement membranes.

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References

  • Adams, J. C. &Watt, F. M. (1993) Regulation of development and differentiation by the extracellular matrix.Development 117, 1183–98.

    CAS  PubMed  Google Scholar 

  • Aufderheide, E. &Ekblom, P. (1988) Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions.J. Cell Biol. 107, 2341–9.

    Article  CAS  PubMed  Google Scholar 

  • Balza, E., Siri, A., Ponassi, M., Caocci, F., Linnala, A. A., Virtanen, I. &Zardi, I. (1993) Production and characterization of monoclonal antibodies specific for different epitopes of human tenascin.FEBS Lett. 332, 39–43.

    Article  CAS  PubMed  Google Scholar 

  • Beaulieu, J.-F. (1992) Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine.J. Cell Sci. 102, 427–36.

    CAS  PubMed  Google Scholar 

  • Beaulieu, J.-F. &Vachon, P. H. (1994) Reciprocal expression of laminin A-chain isoforms along the crypt-villus axis in the human small intestine.Gastroenterology 106, 829–39.

    CAS  PubMed  Google Scholar 

  • Beaulieu, J.-F., Jutras, S., Kusakabe, M. &Perreault, N. (1993) Expression of tenascin in the developing human small intestine.Biochem. Biophys. Res. Commun. 192, 1086–92.

    Article  CAS  PubMed  Google Scholar 

  • Burgeson, R. E., Chiquet, M., Deutzmann, R., Ekblom, P., Engel, J., Kleinman, H., Martin, G. R., Meneguzzi, G., Paulsson, M., Sanes, J., Timpl, R., Tryggvason, K., Yamada, Y. &Yurchenco, P. D. (1994) A new nomenclature for the laminins.Matrix Biol. 14, 209–11.

    Article  CAS  PubMed  Google Scholar 

  • Chiquet-Ehrismann, R. (1995) Tenascins, a growing family of extracellular matrix proteins.Experientia 51, 853–62.

    Article  CAS  PubMed  Google Scholar 

  • Desloges, N., Simoneau, A., Jutras, S. &Beaulieau, J.-F. (1994) Tenascin may not be required for intestinal villus development (Int. J. Dev. Biol. 38, 737–9.

    CAS  PubMed  Google Scholar 

  • Dieckgraefe, B. K., Santoro, S. A. &Alpers, D. H. (1996) Immunolocalization of α-integrin subunits and extracellular matrix components during human colonic organogenesis.Gastroenterology 110, 58–71.

    Article  CAS  PubMed  Google Scholar 

  • Engvall, E., Davis, G. E., Dickerson, K., Ruoslahti, E., Varon, S. &Manthorpe, M. (1986) Mapping of domains in human laminin using monoclonal antibodies: localization of the neurite-promoting site.J. Cell Biol. 103, 2457–65.

    Article  CAS  PubMed  Google Scholar 

  • Erickson, H. P. (1993) Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions.Current. Op. Cell Biol. 5, 869–76.

    CAS  Google Scholar 

  • Gerecke, D. R., Cordon, M. K., Wagman, D. W., Champliaud, M. F. &Burgeson, R. E. (1994) Hemidesmosomes, anchoring filaments, and anchoring fibrils: components of a unique attachment complex. InExtracellular Matrix Assembly and Structure (edited byYurchenco, P. D., Birk, D. E. &Mecham, R. P. pp. 417–39. San Diego: Academic Press.

    Google Scholar 

  • Glukhova, M., Koteliansky, V., Fondacci, C., Marotte, F. &Rappaport, L. (1993) Laminin variants and integrin laminin receptors in developing and adult human smooth muscle.Dev. Biol. 157, 437–47.

    Article  CAS  PubMed  Google Scholar 

  • Hauptmann, S., Zardi, L., Siri, A., Carnemolla, B., Borsi, L., Castellucci, M., Klosterhalfen, B., Hartung, P., Weis, J., Stöcker, G., Haubeck, H.-D. &Kirkpatrick, C. J. (1995) Extracellular matrix proteins in colorectal carcinomas. Expression of tenascin and fibronectin isoforms.Lab. Invest. 73, 172–82.

    CAS  PubMed  Google Scholar 

  • Howeedy, A. A., Virtanen, I., Laitinen, L., Gould, N. S., Koukoulis, G. K. &Gould, V. E. (1990) Differential distribution of tenascin in the normal, hyperplastic, and neoplastic breast.Lab. Invest. 63, 798–806.

    CAS  PubMed  Google Scholar 

  • Hunter, D. D., Shah, V., Merlie, J. P. &Sanes, J. R. (1989) A lamininlike adhesive protein concentrated in the synaptic cleft of the neuromuscular junction.Nature,338, 229–34.

    Article  CAS  PubMed  Google Scholar 

  • Iivanainen, A., Sainio, K., Sariola, H. &Tryggvason, K. (1995) Primary structure and expression of a novel human laminin α 4 chain.FEBS Lett. 365, 183–8.

    Article  CAS  PubMed  Google Scholar 

  • Ikeda, Y., Mori, M., Kajiyama, K., Haraguchi, Y., Sasaki, O. &Sugimachi, K. (1995) Immunohistochemical expression of tenascin in normal stomach tissue, gastric carcinomas and gastric carcinoma in lymph nodes.Br. J. Cancer 72, 189–92.

    CAS  PubMed  Google Scholar 

  • Johnson, F. P. (1913) The development of the mucous membrane of the large intestine and vermiform process in the human embryo.Am. J. Anat.,14, 187–233.

    Google Scholar 

  • Jones, J. C. R., Asmuth, J., Baker S. E., Langhofer, M., Roth, S. I. &Hopkinson, S. B. (1994) Hemidesmosomes: extracellular matrix/intermediate filament connectors.Exp. Cell. Res. 213, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Koukoulis, G. K., Gould, V. E., Bhattacharyya, A., Gould, J. E., Howeedy, A. A. &Virtanen, I. (1991) Perspectives in pathology. Tenascin in normal, reactive, hyperplastic, and neoplastic tissues.Hum. Pathol. 22, 636–43.

    Article  CAS  PubMed  Google Scholar 

  • Leigh, I. M., Purkis, P. E. &Bruckner-Tuderman, L. (1987) LH7.2 Monoclonal antibody detects type VII collagen in the sublamina densa zone of ectodermally-derived epithelia, including skin.Epithelia 1, 17–29.

    Google Scholar 

  • Leivo, I. &Engvall, E. (1988) Merosin, a protein specific for basement membranes of Schwann cells, stratified muscle, and trophoplast, is expressed late in nerve and muscle development.Proc. Natl Acad. Sci. USA 85, 1544–8.

    CAS  PubMed  Google Scholar 

  • Leivo, I., Tani, T., Laitinen, L., Bruns, R., Kivilaakso, E., Lehto, V.-P., Burgeson, R. & Virtanen, I. (1996) Anchoring complex components laminin-5 and type VII collagen in the intestine: association with migrating and differentiating enterocytes.J. Histochem. Cytochem. (in press).

  • Liesi, P., Dahl, D. &Vaheri, A. (1983) Laminin is produced by early rat astrocytes in primary culture.J. Cell Biol. 96, 920–4.

    Article  CAS  PubMed  Google Scholar 

  • Lunstrum, G. P., Kuo, H. J., Rosenbaum L. M., Keene, D. R., Glanville, R. W. Sakai, L. Y. &Burgeson, R. E. (1987) Anchoring fibrils contain the carboxy-terminal globular domain of the type VII procollagen, but lack the amino-terminal globular domain.J. Biol. Chem. 262, 13706–12.

    CAS  PubMed  Google Scholar 

  • Mackie, E. J. (1994) Tenascin in connective tissue development and pathogenesis.Persp. Dev. Neurobiol. 2, 125–32.

    CAS  Google Scholar 

  • Marinkovich, M. P., Lunstrum, G. P. &Burgeson, R. E. (1992) The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor.J. Biol. Chem. 267, 17900–6.

    CAS  PubMed  Google Scholar 

  • Merker, H. J. (1994) Morphology of the basement membrane.Microscopy Res. Technique 28, 95–124.

    CAS  Google Scholar 

  • Miner, J. H., Lewis, M. R. &Sanes, J. R. (1995). Molecular cloning of a novel laminin chain, α 5, and widespread expression in adult mouse tissues.J. Biol. Chem. 270, 28523–6.

    CAS  PubMed  Google Scholar 

  • Perreault, N., Vachon, P. H. &Beaulieu, J.-F. (1995) Appearance and distribution of laminin A chain isoforms and integrin α2, α3, α6, β1, and β4 subunits in the developing human small intestinal mucosa.Anal. Rec. 242, 242–50.

    CAS  Google Scholar 

  • Probstmeier, R., Martini, R. &Schachner, M. (1990) Expression of J1/tenascin in the crypt-villus unit of adult mouse small intestine: implications for its role in epithelial cell shedding.Development.109, 313–21.

    CAS  PubMed  Google Scholar 

  • Richards, A. J., Al-Imara, L., Carter, N. P., Lloyd, J. C., Leversha, M. A. &Pope, F. M. (1994) Localization of the gene (LAMA4) to chromosome 6q21 and isolation of a partial cDNA encoding a variant laminin A chain.Genomics,22, 237–9.

    Article  CAS  PubMed  Google Scholar 

  • Riedl, S. E., Faissner, A., Schlag, P., Von Herbay, A., Koretz, K. &Moller, P. (1992) Altered content and distribution of tenascin in colitis, colon adenoma, and colorectal carcinoma.Gastroenterology 103, 400–6.

    CAS  PubMed  Google Scholar 

  • Rousselle, P., Lunstrum, G. P., Keene, D. R. &Burgeson, R. E. (1991) Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filament.J. Cell Biol. 114, 567–76.

    Article  CAS  PubMed  Google Scholar 

  • Ryan, M. C., Tizard, R., Vandevanter, D. R. &Carter, W. C. (1994) Cloning of the Lam A3 gene encoding the α3 chain of the adhesive ligand epiligrin.J. Biol. Chem. 269, 22779–87.

    CAS  PubMed  Google Scholar 

  • Sakai, L. Y., Keene, D. R., Morris, N. P. &Burgeson, R. E. (1986) Type VII collagen is a major structural component of anchoring fibrils.J. Cell Biol. 103, 1577–86.

    CAS  PubMed  Google Scholar 

  • Sakai, T., Kawakatsu, H., Hirota, N., Yokoyama, T., Sakakura, T. &Saito, M. (1993) Specific expression of tenascin in human colonic neoplasms.Br. J. Cancer 67, 1058–64.

    CAS  PubMed  Google Scholar 

  • Shamsuddin, A. M., Phelps, P. C. &Trump, B. F. (1982) Human large intestinal epithelium: light microscopy, histochemistry, and ultrastructure.Hum. Pathol. 13, 790–803.

    CAS  PubMed  Google Scholar 

  • Simon-Assmann, P., Duclos, B., Orian-Rousseau, V., Arnold, C., Mathelin, C., Engvall, E. &Kedinger, M. (1994) Differential expression of laminin isoforms and α6-β4 integrin subunits in the developing human and mouse intestine.Dev. Dynam. 201, 71–85.

    CAS  Google Scholar 

  • Simon-Assmann, P., Kedinger, M., De Archangelis, A., Rousseau, V. &Simo, P. (1995) Extracellular matrix components in intestinal development.Experientia 51, 883–900.

    Article  CAS  PubMed  Google Scholar 

  • Siri, A., Carnemolla, B., Saginati, M., Leprini, A., Casari, G., Barelle, F. &Zardi, L. (1991) Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies.Nucleic Acids Res. 19, 523–31.

    Google Scholar 

  • Tiitta, O., Sipponen, P., Gould, V. &Virtanen, I. (1994) Tenascin expression in inflammatory, dysplastic and neoplastic lesions of the human stomach.Virchows Arch. 425, 369–74.

    Article  CAS  PubMed  Google Scholar 

  • Timpl, R. &Brown, J. C. (1994) The laminins.Matrix Biol. 14, 275–81.

    Article  CAS  PubMed  Google Scholar 

  • Traber, P. G. &Wu, G. D. (1995) Intestinal development and differentiation. InGastrointestinal Cancers: Biology Diagnosis and Therapy (edited byRustgi, A. K.) pp. 21–43. Philadelphia: Lippincott-Raven.

    Google Scholar 

  • Vachon, P. H., Durand, J. &Beaulieu, J.-F. (1993) Basement membrane formation and re-distribution of the β1 integrins in human intestinal co-culture systems.Anat. Rec. 236, 567–76.

    Google Scholar 

  • Valentich, J. D. &Powell, D. W. (1994) Intestinal subepithelial myofibroblasts and mucosal immunophysiology.Cur. Op. Gastroenterol. 10, 645–51.

    Google Scholar 

  • Virtanen, I., Tani, T., Bäck, N., Häppölä, O., Laitinen, L., Kiviluoto, T., Salo, J., Burgeson, R. E., Lehto, V.-P. &Kivilaakso, E. (1995) Differential expression of laminin chains and their integrin receptors in human gastric mucosa.Am. J. Pathol. 147, 1123–32.

    CAS  PubMed  Google Scholar 

  • Vuolteenaho, R., Nissinen, M., Sainio, K., Byers, M., Eddy, R., Hirvonen, H., Shows, T. B., Sariola, H., Engvall, F. &Tryggvason, K. (1994) Human laminin M chain (Merosin): complete primary structure, chromosomal assignment, and expression of the M and A chain in human fetal tissues.J. Cell Biol. 124, 381–94.

    Article  CAS  PubMed  Google Scholar 

  • Wetzels, R. H. W., Robben, H. C. M., Leigh, I. M., Schaafsma, H. E., Vooijs, G. P. &Ramaekers, F. C. S. (1991) Distribution patterns of type VII collagen in normal and malignant human tissues.Am. J. Pathol. 139, 451–9.

    CAS  PubMed  Google Scholar 

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Lohi, J., Leivo, I., Tani, T. et al. Laminins, tenascin and type VII collagen in colorectal mucosa. Histochem J 28, 431–440 (1996). https://doi.org/10.1007/BF02331434

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