Pulsed contractions of an actin-myosin network drive apical constriction.
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.
Martin
Adam C
AC
Howard Hughes Medical Institute, Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.
Kaschube
Matthias
M
Wieschaus
Eric F
EF
D000199:Actins / Q000737:chemistry / Q000378:metabolism*; D022005:Adherens Junctions / Q000737:chemistry / Q000378:metabolism; D000818:Animals; D029721:Drosophila Proteins / Q000378:metabolism; D004331:Drosophila melanogaster / Q000166:cytology* / Q000196:embryology* / Q000235:genetics; D054262:Gastrulation; D018507:Gene Expression Regulation, Developmental; D024462:Myosin Type II / Q000737:chemistry / Q000378:metabolism*; D010507:Periodicity; D000071250:Snail Family Transcription Factors; D014157:Transcription Factors / Q000378:metabolism; D051879:Twist-Related Protein 1 / Q000378:metabolism
D000199:Actins; D029721:Drosophila Proteins; D000071250:Snail Family Transcription Factors; D014157:Transcription Factors; C497753:Twi protein, Drosophila; D051879:Twist-Related Protein 1; C000604451:sna protein, Drosophila; D024462:Myosin Type II