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
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.
Adams, J.C. & Watt, F.M. (1993) Regulation of development and differentiation by the extracellular matrix. Development 117, 1183-98.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Engvall, E. (1993) Laminin variants: why, where and when? Kidney Int. 43, 2-6.
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.
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.
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.
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.
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.
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.
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.
Hsi, B.-L. & Yeh, C.-J.G. (1986) Monoclonal antibodies to human amnion. J. Reprod. Immunol. 9, 11-21.
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.
Jucker, M., Tian, M. & Ingram, D.K. (1996) Laminins in the adult and aged brain. Mol. Chem. Neuropathol. 28, 209-18.
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.
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.
Kosmehl, H., Berndt, A. & Katenkamp, D. (1996) Molecular variants of fibronectin and laminin: structure, physiological occurrence and histopathological aspects. Virchows Arch. 429, 311-22.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Simon-Assmann, P. & Kedinger, M. (1993) Heterotypic cellular cooperation in gut morphogenesis and differentiation. Semin. Cell Biol. 4, 221-30.
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.
Simon-Assmann, P., Kedinger, M., de Arcangelis, A., Rousseau, V. & Simo, P. (1995) Extracellular matrix components in intestinal development. Experimentia 51, 883-900
Skalova, A., & Leivo, I. (1992) Basement membrane proteins in salivary gland tumours. Virchows Arch. A. Pathol. Anat. 420, 425-34.
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.
Timpl, R. & Brown, J.C. (1994) The laminins. Matrix Biol. 14, 275-81.
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.
Tsukada, T. (1987a) HHF35, a muscle-actin-specific monoclonal antibody: I. Immunocytochemical and biochemical characterization. Am. J. Pathol. 126, 51.
Tsukada, T. (1987b) HHF35, a muscle-actin-specific monoclonal antibody: II. Reactivity in normal reactive, and neoplastic human tissues. Am. J. Pathol. 127, 389.
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.
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.
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.
Virtanen, I., Laitinen, L. & Korhonen, M. (1995b) Differential expression of laminin polypeptides in developing and adult human kidney. J. Histochem. Cytochem. 43, 621-8.
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.
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.
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.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Rights 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
Issue Date:
DOI: https://doi.org/10.1023/A:1003226931910