Drosophilalaminins act as key regulators of basement membrane assembly and morphogenesis

Author:

Urbano Jose M.1,Torgler Catherine N.12,Molnar Cristina3,Tepass Ulrich4,López-Varea Ana3,Brown Nicholas H.2,de Celis Jose F.3,Martín-Bermudo Maria D.1

Affiliation:

1. Centro Andaluz de Biología de Desarrollo (CABD), Univ. Pablo de Olavide-CSIC, Ctra. Utrera Km. 1, 41013 Sevilla, Spain

2. The Gurdon Institute and Department of Physiology, Development & Neuroscience, University of Cambridge, Tennis Court Road, Cambridge CB2 1QN, UK

3. Centro de Biología Molecular ‘Severo Ochoa’, CSIC and Universidad Autónoma de Madrid, Cantoblanco, Madrid 28049, Spain

4. Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada

Abstract

Laminins are heterotrimeric molecules found in all basement membranes. In mammals, they have been involved in diverse developmental processes, from gastrulation to tissue maintenance. The Drosophila genome encodes two laminin α chains, one β and one Γ, which form two distinct laminin trimers. So far, only mutations affecting one or other trimer have been analysed. In order to study embryonic development in the complete absence of laminins, we mutated the gene encoding the sole laminin β chain in Drosophila, LanB1, so that no trimers can be made. We show that LanB1 mutant embryos develop until the end of embryogenesis. Electron microscopy analysis of mutant embryos reveals that the basement membranes are absent and the remaining extracellular material appears disorganised and diffuse. Accordingly, abnormal accumulation of major basement membrane components, such as Collagen IV and Perlecan, is observed in mutant tissues. In addition, we show that elimination of LanB1 prevents the normal morphogenesis of most organs and tissues, including the gut, trachea, muscles and nervous system. In spite of the above structural roles for laminins, our results unravel novel functions in cell adhesion, migration and rearrangement. We propose that while an early function of laminins in gastrulation is not conserved in Drosophila and mammals, their function in basement membrane assembly and organogenesis seems to be maintained throughout evolution.

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

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