The plasma membrane flattens out to fuel cell-surface growth during Drosophila cellularization

Dev Cell. 2013 Dec 23;27(6):648-55. doi: 10.1016/j.devcel.2013.11.006. Epub 2013 Dec 5.

Abstract

Cell-shape change demands cell-surface growth, but how growth is fueled and choreographed is still debated. Here we use cellularization, the first complete cytokinetic event in Drosophila embryos, to show that cleavage furrow ingression is kinetically coupled to the loss of surface microvilli. We modulate furrow kinetics with RNAi against the Rho1-GTPase regulator slam and show that furrow ingression controls the rate of microvillar depletion. Finally, we directly track the microvillar membrane and see it move along the cell surface and into ingressing furrows, independent of endocytosis. Together, our results demonstrate that the kinetics of the ingressing furrow regulate the utilization of a microvillar membrane reservoir. Because membranes of the furrow and microvilli are contiguous, we suggest that ingression drives unfolding of the microvilli and incorporation of microvillar membrane into the furrow. We conclude that plasma membrane folding/unfolding can contribute to the cell-shape changes that promote embryonic morphogenesis.

Publication types

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

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Animals
  • Cell Membrane / metabolism*
  • Cell Membrane / ultrastructure
  • Cell Membrane Structures / metabolism
  • Cytokinesis
  • Drosophila / embryology*
  • Drosophila / metabolism*
  • Drosophila / ultrastructure
  • Drosophila Proteins / antagonists & inhibitors
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Embryo, Nonmammalian / cytology*
  • Embryo, Nonmammalian / metabolism
  • Embryo, Nonmammalian / ultrastructure
  • Embryonic Development
  • Endocytosis
  • Fluorescence
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Microscopy, Electron, Scanning
  • Microvilli / metabolism*
  • Morphogenesis / physiology*
  • RNA, Small Interfering / genetics
  • Time-Lapse Imaging

Substances

  • Drosophila Proteins
  • Intracellular Signaling Peptides and Proteins
  • RNA, Small Interfering
  • Slam protein, Drosophila