A contractile actomyosin network linked to adherens junctions by Canoe/afadin helps drive convergent extension

Integrating individual cell movements to create tissue-level shape change is essential to building an animal. We explored mechanisms of adherens junction (AJ):cytoskeleton linkage and roles of the linkage regulator Canoe/afadin during Drosophila germband extension (GBE), a convergent-extension proce...

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Bibliographic Details
Published in:Molecular biology of the cell 2011-07, Vol.22 (14), p.2491-2508
Main Authors: Sawyer, Jessica K, Choi, Wangsun, Jung, Kuo-Chen, He, Li, Harris, Nathan J, Peifer, Mark
Format: Article
Language:English
Subjects:
Actomyosin - genetics
Actomyosin - metabolism
Actomyosin - physiology
Adherens Junctions - genetics
Adherens Junctions - metabolism
Adherens Junctions - physiology
Animals
Cell Movement - genetics
Cell Movement - physiology
Cell Polarity - genetics
Cell Polarity - physiology
Cell Shape - genetics
Cell Shape - physiology
Cytoskeleton - genetics
Cytoskeleton - physiology
Drosophila melanogaster - genetics
Drosophila melanogaster - physiology
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Drosophila Proteins - physiology
Gastrulation - genetics
Mesoderm - growth & development
Morphogenesis - genetics
Morphogenesis - physiology
Mutation
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Summary:Integrating individual cell movements to create tissue-level shape change is essential to building an animal. We explored mechanisms of adherens junction (AJ):cytoskeleton linkage and roles of the linkage regulator Canoe/afadin during Drosophila germband extension (GBE), a convergent-extension process elongating the body axis. We found surprising parallels between GBE and a quite different morphogenetic movement, mesoderm apical constriction. Germband cells have an apical actomyosin network undergoing cyclical contractions. These coincide with a novel cell shape change--cell extension along the anterior-posterior (AP) axis. In Canoe's absence, GBE is disrupted. The apical actomyosin network detaches from AJs at AP cell borders, reducing coordination of actomyosin contractility and cell shape change. Normal GBE requires planar polarization of AJs and the cytoskeleton. Canoe loss subtly enhances AJ planar polarity and dramatically increases planar polarity of the apical polarity proteins Bazooka/Par3 and atypical protein kinase C. Changes in Bazooka localization parallel retraction of the actomyosin network. Globally reducing AJ function does not mimic Canoe loss, but many effects are replicated by global actin disruption. Strong dose-sensitive genetic interactions between canoe and bazooka are consistent with them affecting a common process. We propose a model in which an actomyosin network linked at AP AJs by Canoe and coupled to apical polarity proteins regulates convergent extension.
ISSN:1059-1524
1939-4586
DOI:10.1091/mbc.e11-05-0411