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Distinct RhoGEFs Activate Apical and Junctional 1 Actomyosin Contractility Under Control of G Proteins During Epithelial Morphogenesis

54 Pages Posted: 2 Apr 2019 Publication Status: Review Complete

See all articles by Alain Garcia De Las Bayonas

Alain Garcia De Las Bayonas

Aix-Marseille University - Turing Center for Living Systems

Jean-Marc Philippe

Aix-Marseille University - Turing Center for Living Systems

Annemarie C. Lellouch

Aix-Marseille University - Turing Center for Living Systems

Thomas Lecuit

Aix-Marseille University - Turing Center for Living Systems; Université Paris I Panthéon-Sorbonne - College of France

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Abstract

Small RhoGTPases direct cell shape changes and movements during tissue morphogenesis. Their activities are tightly regulated in space and time to specify the desired pattern of actomyosin contractility that supports tissue morphogenesis. This is expected to stem from polarized surface stimuli and from polarized signaling processing inside cells. We examined this general problem in the context of cell intercalation that drives extension of the Drosophila ectoderm. In the ectoderm, G protein coupled receptors (GPCRs) and their downstream heterotrimeric G proteins (Gα and Gβγ) activate Rho1 both medial-apically, where it exhibits pulsed dynamics, and at junctions, where its activity is planar polarized. However, the mechanisms responsible for polarizing Rho1 activity are unclear. We report that distinct guanine exchange factors (GEFs) activate Rho1 in these two cellular compartments. RhoGEF2 acts uniquely to activate medial-apical Rho1 but is recruited both medial-apically and at junctions by Gα12/13-GTP, also called Concertina (Cta) in Drosophila. On the other hand, p114RhoGEF/Wireless (Wrl), a newly characterized RhoGEF, is required for cell intercalation in the extending ectoderm where it activates Rho1 specifically at junctions. Its localization is restricted to adherens junctions and is under Gβ13F/Gγ1 control. Furthermore, Gβ13F/Gγ1 activates junctional Rho1 and exerts quantitative control over planar polarization of Rho1. Finally, we found that p114RhoGEF/Wireless is absent in the mesoderm, arguing for a tissue specific control over junctional Rho1 activity. These results shed light on the mechanisms of polarization of Rho1 activity in different cellular compartments and reveal that distinct GEFs are sensitive tuning parameters of cell contractility in remodeling epithelia.

Keywords: Tissue morphogenesis, epithelium, Rho1 signaling, RhoGEF, Cell polarity, Actomyosin, Heterotrimeric G proteins, Cell intercalation

Suggested Citation

Bayonas, Alain Garcia De Las and Philippe, Jean-Marc and Lellouch, Annemarie C. and Lecuit, Thomas, Distinct RhoGEFs Activate Apical and Junctional 1 Actomyosin Contractility Under Control of G Proteins During Epithelial Morphogenesis (April 1, 2019). Available at SSRN: https://ssrn.com/abstract=3363748 or http://dx.doi.org/10.2139/ssrn.3363748
This version of the paper has not been formally peer reviewed.

Alain Garcia De Las Bayonas (Contact Author)

Aix-Marseille University - Turing Center for Living Systems

3 Avenue Robert Schuman
Aix-en-Provence, 13628
France

Jean-Marc Philippe

Aix-Marseille University - Turing Center for Living Systems

3 Avenue Robert Schuman
Aix-en-Provence, 13628
France

Annemarie C. Lellouch

Aix-Marseille University - Turing Center for Living Systems

3 Avenue Robert Schuman
Aix-en-Provence, 13628
France

Thomas Lecuit

Aix-Marseille University - Turing Center for Living Systems ( email )

3 Avenue Robert Schuman
Aix-en-Provence, 13628
France

Université Paris I Panthéon-Sorbonne - College of France ( email )

11, place Marcelin Berthelot
75231 Paris Cedex 05
France

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