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

Maria V. Tsiper, Peter D. Yurchenco

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71 Scopus citations

Abstract

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 β1-integrin arrays. The laminin-1 fragment E3 (LG-modules 4-5), which binds dystroglycan and heparin, inhibited reticular-matrix formation. By contrast, β1-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 β1-integrin dependent matrix is unlikely to be precursor to basement membrane.

Original languageEnglish (US)
Pages (from-to)1005-1015
Number of pages11
JournalJournal of cell science
Volume115
Issue number5
StatePublished - Mar 1 2002

All Science Journal Classification (ASJC) codes

  • Cell Biology

Keywords

  • Collagen
  • Dystroglycan
  • Integrin
  • Laminin
  • Schwann cell
  • Utrophin

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