Pulsed Contractions of an Actin-Myosin Network Drive Apical Constriction

Nature. 2009 Jan 22;457(7228):495-9. doi: 10.1038/nature07522. Epub 2008 Nov 23.

Abstract

Apical constriction facilitates epithelial sheet bending and invagination during morphogenesis. Apical constriction is conventionally thought to be driven by the continuous purse-string-like contraction of a circumferential actin and non-muscle myosin-II (myosin) belt underlying adherens junctions. However, it is unclear whether other force-generating mechanisms can drive this process. Here we show, with the use of real-time imaging and quantitative image analysis of Drosophila gastrulation, that the apical constriction of ventral furrow cells is pulsed. Repeated constrictions, which are asynchronous between neighbouring cells, are interrupted by pauses in which the constricted state of the cell apex is maintained. In contrast to the purse-string model, constriction pulses are powered by actin-myosin network contractions that occur at the medial apical cortex and pull discrete adherens junction sites inwards. The transcription factors Twist and Snail differentially regulate pulsed constriction. Expression of snail initiates actin-myosin network contractions, whereas expression of twist stabilizes the constricted state of the cell apex. Our results suggest a new model for apical constriction in which a cortical actin-myosin cytoskeleton functions as a developmentally controlled subcellular ratchet to reduce apical area incrementally.

Publication types

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

MeSH terms

  • Actins / chemistry
  • Actins / metabolism*
  • Adherens Junctions / chemistry
  • Adherens Junctions / metabolism
  • Animals
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Gastrulation*
  • Gene Expression Regulation, Developmental
  • Myosin Type II / chemistry
  • Myosin Type II / metabolism*
  • Periodicity
  • Snail Family Transcription Factors
  • Transcription Factors / metabolism
  • Twist-Related Protein 1 / metabolism

Substances

  • Actins
  • Drosophila Proteins
  • Snail Family Transcription Factors
  • Transcription Factors
  • Twi protein, Drosophila
  • Twist-Related Protein 1
  • sna protein, Drosophila
  • Myosin Type II