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Curr Biol. 2017 Aug 7;27(15):2260-2270.e5. doi: 10.1016/j.cub.2017.06.038. Epub 2017 Jul 20.

An Actomyosin-Arf-GEF Negative Feedback Loop for Tissue Elongation under Stress.

Author information

1
Department of Cell & Systems Biology, University of Toronto, 25 Harbord Street, Toronto, ON M5S 3G5, Canada.
2
Institute of Biomaterials and Biomedical Engineering, University of Toronto, 164 College Street, Toronto, ON M5S 3G9, Canada; Ted Rogers Centre for Heart Research, University of Toronto, 661 University Avenue, Toronto, ON M5G 1M1, Canada.
3
Department of Cell & Systems Biology, University of Toronto, 25 Harbord Street, Toronto, ON M5S 3G5, Canada; Institute of Biomaterials and Biomedical Engineering, University of Toronto, 164 College Street, Toronto, ON M5S 3G9, Canada; Ted Rogers Centre for Heart Research, University of Toronto, 661 University Avenue, Toronto, ON M5G 1M1, Canada; Developmental and Stem Cell Biology Program, The Hospital for Sick Children, 686 Bay Street, Toronto, ON M5G 1X8, Canada.
4
Department of Cell & Systems Biology, University of Toronto, 25 Harbord Street, Toronto, ON M5S 3G5, Canada. Electronic address: tony.harris@utoronto.ca.

Abstract

In response to a pulling force, a material can elongate, hold fast, or fracture. During animal development, multi-cellular contraction of one region often stretches neighboring tissue. Such local contraction occurs by induced actomyosin activity, but molecular mechanisms are unknown for regulating the physical properties of connected tissue for elongation under stress. We show that cytohesins, and their Arf small G protein guanine nucleotide exchange activity, are required for tissues to elongate under stress during both Drosophila dorsal closure (DC) and zebrafish epiboly. In Drosophila, protein localization, laser ablation, and genetic interaction studies indicate that the cytohesin Steppke reduces tissue tension by inhibiting actomyosin activity at adherens junctions. Without Steppke, embryogenesis fails, with epidermal distortions and tears resulting from myosin misregulation. Remarkably, actomyosin network assembly is necessary and sufficient for local Steppke accumulation, where live imaging shows Steppke recruitment within minutes. This rapid negative feedback loop provides a molecular mechanism for attenuating the main tension generator of animal tissues. Such attenuation relaxes tissues and allows orderly elongation under stress.

KEYWORDS:

Arf small G protein; Drosophila; actomyosin; cytohesin; dorsal closure; epiboly; morphogenesis; negative feedback; tissue relaxation; zebrafish

PMID:
28736167
DOI:
10.1016/j.cub.2017.06.038
[Indexed for MEDLINE]
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