Drosophila vinculin is more harmful when hyperactive than absent, and can circumvent integrin to form adhesion complexes

J Cell Sci. 2016 Dec 1;129(23):4354-4365. doi: 10.1242/jcs.189878. Epub 2016 Oct 13.

Abstract

Vinculin is a highly conserved protein involved in cell adhesion and mechanotransduction, and both gain and loss of its activity causes defective cell behaviour. Here, we examine how altering vinculin activity perturbs integrin function within the context of Drosophila development. Whereas loss of vinculin produced relatively minor phenotypes, gain of vinculin activity, through a loss of head-tail autoinhibition, caused lethality. The minimal domain capable of inducing lethality is the talin-binding D1 domain, and this appears to require talin-binding activity, as lethality was suppressed by competition with single vinculin-binding sites from talin. Activated Drosophila vinculin triggered the formation of cytoplasmic adhesion complexes through the rod of talin, but independently of integrin. These complexes contain a subset of adhesion proteins but no longer link the membrane to actin. The negative effects of hyperactive vinculin were segregated into morphogenetic defects caused by its whole head domain and lethality caused by its D1 domain. These findings demonstrate the crucial importance of the tight control of the activity of vinculin.

Keywords: Adhesion; Drosophila; Integrin; Protein complex; Rhea; Talin; Vinculin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Adhesion
  • Cytoplasm / metabolism
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / metabolism*
  • Embryo, Nonmammalian / metabolism
  • Integrins / metabolism*
  • Models, Biological
  • Muscles / embryology
  • Muscles / metabolism
  • Protein Aggregates
  • Protein Binding
  • Protein Domains
  • Vinculin / chemistry
  • Vinculin / metabolism*

Substances

  • Integrins
  • Protein Aggregates
  • Vinculin