J. Cell Biol.
© The Rockefeller University Press
0021-9525/97/05/685/17 $2.00
Volume 137, Number 3, May 5, 1997 685-701

The Laminin  Chains: Expression, Developmental Transitions, and Chromosomal Locations of 1-5, Identification of Heterotrimeric Laminins 8-11, and Cloning of a Novel 3 Isoform

Jeffrey H. Miner,^* Bruce L. Patton,^* Stephen I. Lentz,^§ Debra J. Gilbert, William D. Snider,^§ Nancy A. Jenkins, Neal G. Copeland, and Joshua R. Sanes^*

^* Department of Anatomy and Neurobiology,  Department of Internal Medicine (Renal Division), ^§ Department of Neurology, Washington University School of Medicine, St. Louis, Missouri, 63110; and  Mammalian Genetics Laboratory, ABL-Basic Research Program, National Cancer Institute-Frederick Cancer Research and Development Center, Frederick, Maryland 21702

Laminin trimers composed of , , and  chains are major components of basal laminae (BLs) throughout the body. To date, three  chains (1-3) have been shown to assemble into at least seven heterotrimers (called laminins 1-7). Genes encoding two additional  chains (4 and 5) have been cloned, but little is known about their expression, and their protein products have not been identified. Here we generated antisera to recombinant 4 and 5 and used them to identify authentic proteins in tissue extracts. Immunoprecipitation and immunoblotting showed that 4 and 5 assemble into four novel laminin heterotrimers (laminins 8-11: 411, 421, 511, and 521, respectively). Using a panel of nucleotide and antibody probes, we surveyed the expression of 1-5 in murine tissues. All five chains were expressed in both embryos and adults, but each was distributed in a distinct pattern at both RNA and protein levels. Overall, 4 and 5 exhibited the broadest patterns of expression, while expression of 1 was the most restricted. Immunohistochemical analysis of kidney, lung, and heart showed that the  chains were confined to extracellular matrix and, with few exceptions, to BLs. All developing and adult BLs examined contained at least one  chain, all  chains were present in multiple BLs, and some BLs contained two or three  chains. Detailed analysis of developing kidney revealed that some individual BLs, including those of the tubule and glomerulus, changed in laminin chain composition as they matured, expressing up to three different  chains and two different  chains in an elaborate and dynamic progression. Interspecific backcross mapping of the five  chain genes revealed that they are distributed on four mouse chromosomes. Finally, we identified a novel full-length 3 isoform encoded by the Lama3 gene, which was previously believed to encode only truncated chains. Together, these results reveal remarkable diversity in BL composition and complexity in BL development.

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• Gonzales, M., Weksler, B., Tsuruta, D., Goldman, R. D., Yoon, K. J., Hopkinson, S. B., Flitney, F. W., Jones, J. C. R. (2001). Structure and Function of a Vimentin-associated Matrix Adhesion in Endothelial Cells. Mol. Biol. Cell 12: 85-100 [Abstract] [Full Text]  
• Siler, U., Seiffert, M., Puch, S., Richards, A., Torok-Storb, B., Muller, C. A., Sorokin, L., Klein, G. (2000). Characterization and functional analysis of laminin isoforms in human bone marrow. Blood 96: 4194-4203 [Abstract] [Full Text]  
• Fischer, E., Mougenot, B., Callard, P., Ronco, P., Rossert, J. (2000). Abnormal expression of glomerular basement membrane laminins in membranous glomerulonephritis. Nephrol Dial Transplant 15: 1956-1964 [Abstract] [Full Text]  
• Pierce, R. A., Griffin, G. L., Miner, J. H., Senior, R. M. (2000). Expression Patterns of Laminin alpha 1 and alpha 5 in Human Lung during Development. Am. J. Respir. Cell Mol. Bio. 23: 742-747 [Abstract] [Full Text]  
• Pedraza, C., Geberhiwot, T., Ingerpuu, S., Assefa, D., Wondimu, Z., Kortesmaa, J., Tryggvason, K., Virtanen, I., Patarroyo, M. (2000). Monocytic Cells Synthesize, Adhere to, and Migrate on Laminin-8 ({alpha}4{beta}1{gamma}1). J. Immunol. 165: 5831-5838 [Abstract] [Full Text]  
• Cosgrove, D., Rodgers, K., Meehan, D., Miller, C., Bovard, K., Gilroy, A., Gardner, H., Kotelianski, V., Gotwals, P., Amatucci, A., Kalluri, R. (2000). Integrin {alpha}1{beta}1 and Transforming Growth Factor-{beta}1 Play Distinct Roles in Alport Glomerular Pathogenesis and Serve as Dual Targets for Metabolic Therapy. Am. J. Pathol. 157: 1649-1659 [Abstract] [Full Text]  
• Erickson, A. C., Couchman, J. R. (2000). Still More Complexity in Mammalian Basement Membranes. J. Histochem. Cytochem. 48: 1291-1306 [Abstract] [Full Text]  
• Libby, R. T., Champliaud, M.-F., Claudepierre, T., Xu, Y., Gibbons, E. P., Koch, M., Burgeson, R. E., Hunter, D. D., Brunken, W. J. (2000). Laminin Expression in Adult and Developing Retinae: Evidence of Two Novel CNS Laminins. J. Neurosci. 20: 6517-6528 [Abstract] [Full Text]  
• Andrews, K. L., Betsuyaku, T., Rogers, S., Shipley, J. M., Senior, R. M., Miner, J. H. (2000). Gelatinase B (MMP-9) Is Not Essential in the Normal Kidney and Does Not Influence Progression of Renal Disease in a Mouse Model of Alport Syndrome. Am. J. Pathol. 157: 303-311 [Abstract] [Full Text]  
• Orian-Rousseau, V, Aberdam, D, Rousselle, P, Messent, A, Gavrilovic, J, Meneguzzi, G, Kedinger, M, Simon-Assmann, P (2000). Human colonic cancer cells synthesize and adhere to laminin-5. Their adhesion to laminin-5 involves multiple receptors among which is integrin alpha2beta1. J. Cell Sci. 111: 1993-2004 [Abstract]  
• Kortesmaa, J., Yurchenco, P., Tryggvason, K. (2000). Recombinant Laminin-8 (alpha 4beta 1gamma 1). PRODUCTION, PURIFICATION, AND INTERACTIONS WITH INTEGRINS. J. Biol. Chem. 275: 14853-14859 [Abstract] [Full Text]  
• Nielsen, P. K., Gho, Y. S., Hoffman, M. P., Watanabe, H., Makino, M., Nomizu, M., Yamada, Y. (2000). Identification of a Major Heparin and Cell Binding Site in the LG4 Module of the Laminin alpha 5 Chain. J. Biol. Chem. 275: 14517-14523 [Abstract] [Full Text]  
• Piras, G., El Kharroubi, A., Kozlov, S., Escalante-Alcalde, D., Hernandez, L., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Stewart, C. L. (2000). Zac1 (Lot1), a Potential Tumor Suppressor Gene, and the Gene for varepsilon -Sarcoglycan Are Maternally Imprinted Genes: Identification by a Subtractive Screen of Novel Uniparental Fibroblast Lines. Mol. Cell. Biol. 20: 3308-3315 [Abstract] [Full Text]  
• Oliviero, P., Chassagne, C., Salichon, N., Corbier, A., Hamon, G., Marotte, F., Charlemagne, D., Rappaport, L., Samuel, J.-L. (2000). Expression of laminin {alpha}2 chain during normal and pathological growth of myocardium in rat and human. Cardiovasc Res 46: 346-355 [Abstract] [Full Text]  
• Sunderland, W. J., Son, Y.-J., Miner, J. H., Sanes, J. R., Carlson, S. S. (2000). The Presynaptic Calcium Channel Is Part of a Transmembrane Complex Linking a Synaptic Laminin (alpha 4beta 2gamma 1) with Non-Erythroid Spectrin. J. Neurosci. 20: 1009-1019 [Abstract] [Full Text]  
• Son, Y.-J., Scranton, T. W., Sunderland, W. J., Baek, S. J., Miner, J. H., Sanes, J. R., Carlson, S. S. (2000). The Synaptic Vesicle Protein SV2 Is Complexed with an alpha 5-Containing Laminin on the Nerve Terminal Surface. J. Biol. Chem. 275: 451-460 [Abstract] [Full Text]  
• Furuyama, A, Mochitate, K (2000). Assembly of the exogenous extracellular matrix during basement membrane formation by alveolar epithelial cells in vitro. J. Cell Sci. 113: 859-868 [Abstract]  
• Kikkawa, Y, Sanzen, N, Fujiwara, H, Sonnenberg, A, Sekiguchi, K (2000). Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J. Cell Sci. 113: 869-876 [Abstract]  
• Relan, N. K., Yang, Y., Beqaj, S., Miner, J. H., Schuger, L. (1999). Cell Elongation Induces Laminin {alpha}2 Chain Expression in Mouse Embryonic Mesenchymal Cells: Role in Visceral Myogenesis. JCB 147: 1341-1350 [Abstract] [Full Text]  
• Skyldberg, B., Salo, S., Eriksson, E., Aspenblad, U., Moberger, B., Tryggvason, K., Auer, G. (1999). Laminin-5 as a Marker of Invasiveness in Cervical Lesions. JNCI J Natl Cancer Inst 91: 1882-1887 [Abstract] [Full Text]  

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