Skip to main content
Log in

Differential expression of laminin chains in the human major salivary gland

  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Abstract

Laminin represents a macromolecule family. The heterotrimeric isoforms of laminin can be determined by immunohistochemical demonstration of the single chains. The laminin chain heterogeneity of the basement membrane in adult human major salivary glands was evaluated in relation to cellular differentiation of the epithelia and the stromal compartment. Monoclonal antibodies to the laminin alpha1, alpha3 (BM165) chains and epiligrin reacted with the basement membranes of serous and mucous acini and of intercalated, striated and excretory ducts. As evidenced by a double-labelling technique, the alpha2 chain showed a spatial association with the myoepithelium of the acini, whereas the ductal basement membranes containing no myoepithelial cells were negative. Almost exclusively, beta1 chain was detected in acinar basement membrane, beta2 chain whereas in ductal basement membrane. gamma2 chain is a unique chain belonging to the laminin-5 isoform. It was restricted to the ductal basement membrane. alpha1, alpha2, beta1, beta2 and gamma1 chains were detected in nerves of salivary tissue and alpha1, alpha3, beta1, beta2 and gamma1 chains and epiligrin in blood vessels. Our results indicate that the acinar ductal unit contains basement membranes with different isoforms, which relate to cell differentiation and cell function. © 1998 Chapman & Hall

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aberdam, D., Aguzzi, A., Baudoin, C., Galliano, M.F., Ortonne, J.P. & Meneguzzi, G. (1994) Developmental expression of nicein adhesion protein (laminin-5) subunits suggest multiple morphogenic roles. Cell Adhes. Commun. 2, 115-29.

    Google Scholar 

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

    Google Scholar 

  • Airenne, T., Haakana, H., Sainio, K., Kallunki, T., Kallunki, P., Sariola, H. & Tryggvason, K. (1996) Structure of the human laminin γ2 chain gene (LAMC2): alternative splicing with different tissue distribution of two transcripts. Genomics 32, 54-64.

    Google Scholar 

  • Altraja, A., Laitinen, A., Virtanen, I., Kampe, M., Simonsson, B.G., Karlsson, S.E., Hakansson, L., Venge, P., Sillastu, H. & Laitinen, L.A. (1996) Expression of laminins in the airways in various types of asthmatic patients: a morphometric study. Am. J. Respir. Cell Mol. Biol. 15, 482-8.

    Google Scholar 

  • Baker, S.E., Hopkinson, S.B., Fitchmun, M., Andreason, G.L., Frasier, F., Plopper, G., Quaranta, V. & Jones, J.C.R. (1996) Laminin-5 and hemidesmosomes: role of the α3 chain subunit in hemidesmosome stability and assembly. J. Cell Sci. 109, 2509-20.

    Google Scholar 

  • Berndt, A., Kosmehl, H., Mandel, U., Gabler, U., Luo, X., Celeda, D., Zardi, L. & Katenkamp, D. (1995) TGFβ and bFGF synthesis and localization in Dupuytren's disease (nodular palmar fibromatosis) relative to cellular activity, myofibroblast phenotype and oncofetal variants of fibronectin. Histochem. J. 27, 1014-20.

    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.

    Google Scholar 

  • Carter, W.G., Ryan, M.C. & Gahr, P. J. (1991) Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell 65, 599-610.

    Google Scholar 

  • Caselitz, J., Schmitt, P., Seifert, G., Wustrow, J. & Schuppan, D. (1988) Basal membrane associated substances in human salivary glands and salivary gland tumours. Path. Res. Pract. 183, 386-94.

    Google Scholar 

  • Champliaud, M.F., Lunstrum, G.P., Rousselle, P., Nishiyama, T., Keene, D.R. & Burgeson, R.E. (1996) Human amnion contains a novel laminin variant, laminin 7, which like laminin 6, covalently associates with laminin 5 to promote stable epithelial-stromal attachment. J. Cell Biol. 132, 1189-98.

    Google Scholar 

  • Durbeej, M., Fecker, L., Hjalt, T., Zhang, H.Y., Salmi-Virta, K., Klein, G., Timpl, R., Sorokin, L., Ebendal, T., Ekblom, P. & Ekblom, M. (1996) Expression of laminin α1, α5 and β2 chains during embryogenesis of the kidney and vasculature. Matrix Biol. 15, 397-413.

    Google Scholar 

  • Durham, P.L. & Snyder, J.M. (1996) Regulation of the β2 subunit chain of laminin in developing rabbit fetal lung tissue. Differentiation 60, 229-43.

    Google Scholar 

  • Engvall, E. (1993) Laminin variants: why, where and when? Kidney Int. 43, 2-6.

    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: localisation of the neurite-promoting site. J. Cell Biol. 103, 2457-65.

    Google Scholar 

  • Engvall, E., Earwicker, D., Haaparanta, T., Ruoslahti, E. & Sanes, J.R. (1990) Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul. 1, 731-40.

    Google Scholar 

  • Franchi, A., Santoro, R., Paglierani, M. & Bondi, R. (1994) Immunolocalization of α2, α5 and α6 integrin subunits in salivary tissue and adenomas of the parotid gland. J. Oral. Pathol. Med. 23, 457-60.

    Google Scholar 

  • Galliano, M.-F., Aberdam, D., Aguzzi, A., Ortonne, J.-P. & Meneguzzi, G. (1995) Cloning and complete primary structure of the mouse laminin α3 chain. J. Biol. Chem. 270, 21820-6.

    Google Scholar 

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

    Google Scholar 

  • Gustmann, C., Altmannsberger, M., Osborn, M., Griesser, H. & Feller, A.C. (1991) Cytokeratin expression and vimentin content in large cell anaplastic lymphomas and other non-Hodgkin's lymphoma. Am. J. Pathol. 138, 1413-22.

    Google Scholar 

  • Hewitt, R.E., Powe, D.G., Morrell, K., Balley, E., Leach, I.H., Ellis, I.O. & Turner, D.R. (1997) Laminin and collagen IV subunit distribution in normal and neoplastic tissues of colorectum and breast. Br. J. Cancer 75, 221-9.

    Google Scholar 

  • Hsi, B.-L. & Yeh, C.-J.G. (1986) Monoclonal antibodies to human amnion. J. Reprod. Immunol. 9, 11-21.

    Google Scholar 

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

    Google Scholar 

  • Jucker, M., Tian, M. & Ingram, D.K. (1996) Laminins in the adult and aged brain. Mol. Chem. Neuropathol. 28, 209-18.

    Google Scholar 

  • Kadoya, Y., Kadoya, K., Durbeej, M., Holmvall, K., Sorokin, L. & Ekblom, P. (1995) Antibodies against domain E3 of laminin-1 and integrin α6 subunit perturb branching epithelial morphogenesis of sub-mandibular gland, but by different modes. J. Cell Biol. 129, 521-34.

    Google Scholar 

  • Kosmehl, H., Berndt, A., Katenkamp, D., Mandel, U., Bohle, R., Gabler, U. & Celeda, D. (1995) Differential expression of fibronectin splice variants, oncofetal glycosylated fibronectin and laminin isoforms in nodular palmar fibromatosis. Pathol. Res. Pract. 191, 1105-13.

    Google Scholar 

  • Kosmehl, H., Berndt, A. & Katenkamp, D. (1996) Molecular variants of fibronectin and laminin: structure, physiological occurrence and histopathological aspects. Virchows Arch. 429, 311-22.

    Google Scholar 

  • Libby, R.T., Hunter, D.D. & Brunken, W. J. (1996) Developmental expression of laminin beta 2 in rat retina. Further support for a role in rod morphogenesis. Invest. Ophthalmol. Vis. Sci. 37, 1651-61.

    Google Scholar 

  • Lohi, J., Leivo, I., Tani, T., Kiviluoto, T., Kiviaakso, E., Burgeson, R.E. & Virtanen, I. (1996) Laminins, tenascin and type VII collagen in colorectal mucosa. Histochem. J. 28, 431-40.

    Google Scholar 

  • Malandrini, A., Villanova, M., Sabatelli, P., Squarzoni, S., Six, J., Toti, P., Guazzi, G.C. & Maraldi, M.N. (1997) Localization of laminin α2 chain in normal human skeletal muscle and peripheral nerve: an ultrastructural immunolabeling study. Acta Neuropathol. 93, 166-72.

    Google Scholar 

  • Marinkovich, M.P., Verrando, P., Keene, D.R., Meneguzzi, G., Lunstrum, G.P., Ortonne, J.P. & Burgeson, R.E. (1993) Basement membrane proteins kalinin and nicein are structurally and immunologically identical. Lab. Invest. 69, 295-9.

    Google Scholar 

  • Matsui, C., Nelson, C.F., Hernandez, G.T., Herron, G.S., Bauer, E.A. & Hoeffler, W.K. (1995) γ2 chain of laminin-5 is recognised by monoclonal antibody GB3. J. Invest. Dermatol. 105, 648-52.

    Google Scholar 

  • Miner, J.H. & Sanes, J.R. (1994) Collagen IV α3, α4 and α5 chains in rodent basal laminae: sequence, distribution, association with laminins and developmental switches. J. Cell Biol. 127, 879-91.

    Google Scholar 

  • Miner, J.H., Patton, B.L., Lentz, S. I., Gilbert, D. J., Snider, W.D., Jenkins, N.A., Copeland, N.G. & Sanes, J. (1997) The laminin α chains: expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J. Cell Biol. 137(3), 685-701.

    Google Scholar 

  • Naiem, M., Gerdes, J., Abdulaziz, Z., Sunderland, C.A., Allington, M. J. & Stein, H. (1982) The value of immunohistological screening in the production of monoclonal antibodies. J. Immunol. Methods 50, 145-60.

    Google Scholar 

  • Natali, P.G., Nicotra, M.R., Bigotti, A. & Demartino, C. (1992) Localization of the α6 and β4 integrin subunits in normal human non-lymphoid tissues. J. Cell Sci. 103, 1243-7.

    Google Scholar 

  • Pellerin, S., Keramidas, M., Chambaz, E.M. & Feige, J.-J. (1997) Expression of laminin and its possible role in adrenal cortex homeostasis. Endocrinology 138, 1321-7.

    Google Scholar 

  • Richards, A., Al-Imara, L. & Pope, F.M. (1996) The complete cDNA sequence of laminin α4 and its relationship to other human laminin α chains. Eur. J. Biochem. 238, 813-21.

    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 Laminin chains in the human salivary glands 87 component of anchoring filaments. J. Cell Biol. 114, 567-76.

    Google Scholar 

  • Ryan, M., Tizard, R., Vandevanter, D. & Carter, W.G. (1994) Cloning of the LAMA3 gene encoding the α3 chain of the adhesive ligand epiligrin. J. Biol. Chem. 269, 22779-87.

    Google Scholar 

  • Ryan, M.C., Christiano, A.M., Engvall, E., Wewer, U., Miner, J.H., Sanes, J.R. & Burgeson, R.E. (1996) The functions of laminins: lessons from in vivo studies. Matrix Biol. 15, 369-81.

    Google Scholar 

  • Saku, T., Cheng, J., Okabe, H., Koyama, Z. (1990) Immunolocalization of basement membrane molecules in the stroma of salivary gland pleomorphic adenoma. J. Oral. Pathol. Med. 19, 208-14.

    Google Scholar 

  • Sanes, J.R., Engvall, E., Butkowski, R. & Hunter, D.D. (1990) Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J. Cell Biol. 111, 1685-99.

    Google Scholar 

  • Sephel, G.C., Kennedy, R. & Kudravi, S. (1996) Expression of capillary basement membrane components during sequential phases of wound angiogenesis. Matrix Biol. 15, 263-79.

    Google Scholar 

  • Simo, P., Bouziges, F., Lissitzky, J.-C., Sorokin, L., Kedinger, M. & Simon-Assmann, P. (1992) Dual and asynchronous deposition of laminin chains at the epithelial-mesenchymal interface in the gut. Gastroenterology 102, 1835-45.

    Google Scholar 

  • Simon-Assmann, P. & Kedinger, M. (1993) Heterotypic cellular cooperation in gut morphogenesis and differentiation. Semin. Cell Biol. 4, 221-30.

    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.

    Google Scholar 

  • Simon-Assmann, P., Kedinger, M., de Arcangelis, A., Rousseau, V. & Simo, P. (1995) Extracellular matrix components in intestinal development. Experimentia 51, 883-900

    Google Scholar 

  • Skalova, A., & Leivo, I. (1992) Basement membrane proteins in salivary gland tumours. Virchows Arch. A. Pathol. Anat. 420, 425-34.

    Google Scholar 

  • Sunardhi-Widyaputra, S. & van Damme, B. (1994) Distribution of the VLA family of integrins in normal salivary gland and in pleomorphic adenoma. Pathol. Res. Pract. 190, 600-8.

    Google Scholar 

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

    Google Scholar 

  • Toida, M., Takeuchi, J. & Hara, K. (1984) Histochemical studies of intercellular components of salivary gland tumors with special reference of glycosaminoglycan, laminin and vascular elements. Virchows Arch. 403, 15-26.

    Google Scholar 

  • Tsukada, T. (1987a) HHF35, a muscle-actin-specific monoclonal antibody: I. Immunocytochemical and biochemical characterization. Am. J. Pathol. 126, 51.

    Google Scholar 

  • Tsukada, T. (1987b) HHF35, a muscle-actin-specific monoclonal antibody: II. Reactivity in normal reactive, and neoplastic human tissues. Am. J. Pathol. 127, 389.

    Google Scholar 

  • Uitto, J., Pulkkinen, L., & Christiano, A.M. (1994) Molecular basis of the dystrophic and junctional forms of epidermolysis bullosa: mutations in the type VII collagen and kalinin (laminin 5) genes. J. Invest. Dermatol. 103, 39-46.

    Google Scholar 

  • Villanova, M., Malandrini, A., Toti, P., Salvestroni, R., Six, J., Martin, J. J. & Guazzi, G.C. (1996) Localization of merosin in the normal human brain: implications for congenital muscular dystrophy with merosin deficiency. J. Submicrosc. Cytol. Pathol. 28, 1-4.

    Google Scholar 

  • Virtanen, I., Tani, T., BÄck, N., HÄppÖ l Ö, O., Laiti-Nen, L., Kiviluoto, T., Salo, J., Burgeson, R.E., Lehto, V.P. & Kivilaakso, E. (1995a) Differential expression of laminin chains and their integrin receptors in the human gastric mucosa. Am. J. Pathol. 147, 1123-32.

    Google Scholar 

  • Virtanen, I., Laitinen, L. & Korhonen, M. (1995b) Differential expression of laminin polypeptides in developing and adult human kidney. J. Histochem. Cytochem. 43, 621-8.

    Google Scholar 

  • Virtanen, I., Laitinen, A., Tani, T., PÄÄkkÖ, P., Laiti-Nen, L. A., Burgeson, R.E. & Lehto, V.-P. (1996a) Differential expression of laminins and their integrin receptors in developing and adult human lung. Am. J. Respir. Cell. Mol. Biol. 15, 184-96.

    Google Scholar 

  • Virtanen, I., Lohni, J., Tani, T., Sariola, H., Burgeson, E.B. & Lehto, V.-P. (1996b) Laminin chains in the basement membranes of human thymus. Histochem. J. 28, 643-50.

    Google Scholar 

  • Vuolteenaho, R., Nissinen, M., Sainio, K., Byers, M., Eddy, R., Hirvonen, H., Shows, T.B., Sariola, H., Engvall, E. & 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.

    Google Scholar 

  • Wayner, E.A., Gil, S.G., Murphy, G.F., Mark, S.W. & Carter W.G. (1993) Epiligrin, a component of epithelial basement membranes is an adhesive ligand for α3β1 positive T lymphocytes. J. Cell Biol. 121, 1141-52.

    Google Scholar 

  • Wewer, U.M., Albrechtsen, R., Manthorpe, M., Varon, S., Engvall, E. & Ruoslahti, E. (1983) Human laminin isolated in a nearly intact, biologically active form from placenta by limited proteolysis. J. Biol. Chem. 258, 12654-60.

    Google Scholar 

  • Wewer, U.M., Wagner, E., Hoffstrom, B.G., Meyernielsen, B., Lan, F., Engvall, E. & Albrechtsen, R. (1994) Selective assembly of laminin variants by human carcinoma cells. Lab. Invest. 71, 719-30.

    Google Scholar 

  • Xia, Y., Gil, S.G. & Carter, W.G. (1996) Anchorage mediated by integrin α6β4 to laminin 5 (epiligrin) regulates tyrosine phosphorylation of a membraneassociated 80-kD protein. J. Cell Biol. 132, 727-40.

    Google Scholar 

  • Yeh, C.-J.G., Hsi, B.-L. & Ettore, F. (1986) Normal epithelial antigens recognised by GB3 and GB5 are diminished in intraductal and lost in infiltrating human breast carcinomas. Breast Cancer Res. Treat. 8, 117-23.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Strassburger, S., Berndt, A., Hyckel, P. et al. Differential expression of laminin chains in the human major salivary gland. Histochem J 30, 81–88 (1998). https://doi.org/10.1023/A:1003226931910

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003226931910

Keywords

Navigation