The WAVE Regulatory Complex and Branched F-Actin Counterbalance Contractile Force to Control Cell Shape and Packing in the Drosophila Eye

Dev Cell. 2018 Feb 26;44(4):471-483.e4. doi: 10.1016/j.devcel.2017.12.025. Epub 2018 Jan 27.

Abstract

Contractile forces eliminate cell contacts in many morphogenetic processes. However, mechanisms that balance contractile forces to promote subtler remodeling remain unknown. To address this gap, we investigated remodeling of Drosophila eye lattice cells (LCs), which preserve cell contacts as they narrow to form the edges of a multicellular hexagonal lattice. We found that during narrowing, LC-LC contacts dynamically constrict and expand. Similar to other systems, actomyosin-based contractile forces promote pulses of constriction. Conversely, we found that WAVE-dependent branched F-actin accumulates at LC-LC contacts during expansion and functions to expand the cell apical area, promote shape changes, and prevent elimination of LC-LC contacts. Finally, we found that small Rho GTPases regulate the balance of contractile and protrusive dynamics. These data suggest a mechanism by which WAVE regulatory complex-based F-actin dynamics antagonize contractile forces to regulate cell shape and tissue topology during remodeling and thus contribute to the robustness and precision of the process.

Keywords: Abi; Arp2/3 complex; PI(3,4,5)P3; SCAR; WAVE regulatory complex; actomyosin contractility; branched F-actin; cell shape change; epithelial morphogenesis; small Rho GTPases.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Actins / metabolism*
  • Actomyosin / metabolism
  • Animals
  • Cell Shape
  • Cells, Cultured
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / growth & development*
  • Drosophila melanogaster / metabolism
  • Epithelium / growth & development
  • Epithelium / metabolism
  • Eye / cytology*
  • Eye / metabolism
  • Female
  • Male
  • Morphogenesis / physiology*
  • Muscle Contraction / physiology
  • Wiskott-Aldrich Syndrome Protein Family / metabolism*
  • rho GTP-Binding Proteins / metabolism

Substances

  • Actins
  • Drosophila Proteins
  • Wiskott-Aldrich Syndrome Protein Family
  • Actomyosin
  • rho GTP-Binding Proteins