Calcium waves facilitate and coordinate the contraction of endfeet actin stress fibers in Drosophila interommatidial cells

Development. 2021 Nov 15;148(22):dev199700. doi: 10.1242/dev.199700. Epub 2021 Nov 30.

Abstract

Actomyosin contraction shapes the Drosophila eye's panoramic view. The convex curvature of the retinal epithelium, organized in ∼800 close-packed ommatidia, depends upon a fourfold condensation of the retinal floor mediated by contraction of actin stress fibers in the endfeet of interommatidial cells (IOCs). How these tensile forces are coordinated is not known. Here, we discover a previously unobserved phenomenon: Ca2+ waves regularly propagate across the IOC network in pupal and adult eyes. Genetic evidence demonstrates that IOC waves are independent of phototransduction, but require the inositol 1,4,5-triphosphate receptor (IP3R), suggesting that these waves are mediated by Ca2+ releases from endoplasmic reticulum stores. Removal of IP3R disrupts stress fibers in IOC endfeet and increases the basal retinal surface by ∼40%, linking IOC waves to facilitation of stress fiber contraction and floor morphogenesis. Furthermore, IP3R loss disrupts the organization of a collagen IV network underneath the IOC endfeet, implicating the extracellular matrix and its interaction with stress fibers in eye morphogenesis. We propose that coordinated cytosolic Ca2+ increases in IOC waves promote stress fiber contractions, ensuring an organized application of the planar tensile forces that condense the retinal floor. This article has an associated 'The people behind the papers' interview.

Keywords: Drosophila; Actomyosin contraction; Calcium waves; Eye.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / genetics
  • Actins / genetics*
  • Actins / metabolism
  • Actomyosin / genetics
  • Actomyosin / metabolism
  • Animals
  • Calcium / metabolism*
  • Calcium Signaling / genetics
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Endoplasmic Reticulum / genetics
  • Morphogenesis / genetics*
  • Pupa
  • Retina / growth & development
  • Retina / metabolism
  • Stress Fibers / genetics*

Substances

  • Actins
  • Actomyosin
  • Calcium