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Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells

Department of Pathology & Laboratory Medicine, Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA

^* Author for correspondence (e-mail: yurchenc{at}umdnj.edu )

Accepted 28 November 2001

Laminins are important for Schwann cell basement membrane assembly and axonal function. In this study, we found that exogenous laminin-1, like neuromuscular laminins-2/4, formed two distinct extracellular matrices on Schwann cell surfaces, each facilitated by laminin polymerization. Assembly of one, a densely-distributed reticular matrix, was accompanied by a redistribution of cell-surface dystroglycan and cytoskeletal utrophin into matrix-receptor-cytoskeletal complexes. The other, a fibrillar matrix, accumulated in separate zones associated with pre-existing ß1-integrin arrays. The laminin-1 fragment E3 (LG-modules 4-5), which binds dystroglycan and heparin, inhibited reticular-matrix formation. By contrast, ß1-integrin blocking antibody (Ha2/5) prevented fibrillar assembly. Ultrastructural analysis revealed that laminin treatment induced the formation of a linear electron-dense extracellular matrix (lamina densa) separated from plasma membrane by a narrow lucent zone (lamina lucida). This structure was considerably reduced with non-polymerizing laminin, fully blocked by E3, and unaffected by Ha2/5. Although it formed in the absence of type IV collagen, it was nonetheless able to incorporate this collagen. Finally, cell competency to bind laminin and form a basement membrane was passage-dependent. We postulate that laminin induces the assembly of a basement membrane on competent cell surfaces probably mediated by anchorage through LG 4-5. Upon binding, laminin interacts with dystroglycan, mobilizes utrophin, and assembles a `nascent' basement membrane, independent of integrin, that is completed by incorporation of type IV collagen. However, the fibrillar ß1-integrin dependent matrix is unlikely to be precursor to basement membrane.

Key words: Schwann cell, Laminin, Collagen, Integrin, Dystroglycan, Utrophin

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