Laminin α subunits and their role in C. elegans development

Cheng Chen Huang, David H. Hall, Edward M. Hedgecock, Gautam Kao, Vassiliki Karantza, Bruce E. Vogel, Harald Hutter, Andrew D. Chisholm, Peter D. Yurchenco, William G. Wadsworth

Research output: Contribution to journalArticle

97 Scopus citations

Abstract

Laminins are heterotrimeric (α/β/γ) glycoproteins that form a major polymer within basement membranes. Different α, β and γ subunits can assemble into various laminin isoforms that have different, but often overlapping, distributions and functions. In this study, we examine the contributions of the laminin α subunits to the development of C. elegans. There are two α, one β and one γ laminin subunit, suggesting two laminin isoforms that differ by their α subunit assemble in C. elegans. We find that near the end of gastrulation and before other basement membrane components are detected, the α subunits are secreted between primary tissue layers and become distributed in different patterns to the surfaces of cells. Mutations in either α subunit gene cause missing or disrupted extracellular matrix where the protein normally localizes. Cell-cell adhesions are abnormal: in some cases essential cell-cell adhesions are lacking, while in other cases, cells inappropriately adhere to and invade neighboring tissues. Using electron microscopy, we observe adhesion complexes at improper cell surfaces and disoriented cytoskeletal filaments. Cells throughout the animal show defective differentiation, proliferation or migration, suggesting a general disruption of cell-cell signaling. The results suggest a receptor-mediated process localizes each secreted laminin to exposed cell surfaces and that laminin is crucial for organizing extracellular matrix, receptor and intracellular proteins at those surfaces. We propose this supramolecular architecture regulates adhesions and signaling between adjacent tissue.

Original languageEnglish (US)
Pages (from-to)3343-3358
Number of pages16
JournalDevelopment
Volume130
Issue number14
DOIs
StatePublished - Jul 2003

Keywords

  • Basement membranes
  • C. elegans
  • Cell adhesion
  • Cell migration
  • Cell polarity
  • Cell-cell signaling
  • Differentiation
  • Extracellular matrix
  • Laminin

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

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  • Cite this

    Huang, C. C., Hall, D. H., Hedgecock, E. M., Kao, G., Karantza, V., Vogel, B. E., Hutter, H., Chisholm, A. D., Yurchenco, P. D., & Wadsworth, W. G. (2003). Laminin α subunits and their role in C. elegans development. Development, 130(14), 3343-3358. https://doi.org/10.1242/dev.00481