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Modular activation of Rho1 by GPCR signalling imparts polarized myosin II activation during morphogenesis

Nature Cell Biology volume 18, pages 261–270 (2016)Cite this article

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Abstract

Polarized cell shape changes during tissue morphogenesis arise by controlling the subcellular distribution of myosin II. For instance, during Drosophila melanogaster gastrulation, apical constriction and cell intercalation are mediated by medial–apical myosin II pulses that power deformations, and polarized accumulation of myosin II that stabilizes these deformations. It remains unclear how tissue-specific factors control different patterns of myosin II activation and the ratchet-like myosin II dynamics. Here we report the function of a common pathway comprising the heterotrimeric G proteins Gα12/13, Gβ13F and Gγ1 in activating and polarizing myosin II during Drosophila gastrulation. Gα12/13 and the Gβ13F/γ1 complex constitute distinct signalling modules, which regulate myosin II dynamics medial–apically and/or junctionally in a tissue-dependent manner. We identify a ubiquitously expressed GPCR called Smog required for cell intercalation and apical constriction. Smog functions with other GPCRs to quantitatively control G proteins, resulting in stepwise activation of myosin II and irreversible cell shape changes. We propose that GPCR and G proteins constitute a general pathway for controlling actomyosin contractility in epithelia and that the activity of this pathway is polarized by tissue-specific regulators.

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Figure 1: Heterotrimeric G proteins control MyoII dynamics in the mesoderm and ectoderm.
Figure 2: RhoGEF2 is required for apical–medial MyoII in the ectoderm and acts downstream of Gα12/13.
Figure 3: The ubiquitously expressed GPCR Smog and G proteins are required for both mesoderm constriction and ectoderm elongation.
Figure 4: The Fog ligand requires at least two GPCRs, Smog and Mist, for apical MyoII accumulation in the mesoderm.
Figure 5: Smog is required in the ectoderm for MyoII distribution and contributes to Fog signalling.
Figure 6: Smog controls Rok and Rho1 distribution in the ectoderm and mild inhibition of Rok mimics the effects of smog or mist knockdown in the mesoderm.

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Acknowledgements

We are grateful to K. Zinn (Caltech, USA), N. Fuse (Kyoto, Japan), J. Knoblich (IMBA, Austria), M. Leptin (Cologne, Germany), A. Martin (MIT, USA), V. Mirouse (Clermont, USA), E. Wieschaus (Princeton, USA), J. Zallen (Sloan-Kettering, USA), the Drosophila Genetic Resource Center and the Bloomington Stock Center for the gift of flies. A. Ratnaparkhi (IISER, India) provided plasmids. We thank D. Coiffier for the in situ hybridization shown in Supplementary Fig. 3e. This work benefited greatly from the stimulating discussions in the Lecuit and Lenne laboratories and from the Labex INFORM ((ANR-11-LABX-0054) under the A∗MIDEX program (ANR-11-IDEX-0001-02)). This work was financially supported by the ERC (Biomecamorph no. 323027), the ANR Archiplast (Programme Blanc) and the CNRS (S.K. and T.L.). A.M. was supported by the Ministère de l’Education nationale and the Association pour la Recherche contre le Cancer (ARC). This work was performed using the France-BioImaging infrastructure supported by the Agence Nationale de la Recherche (ANR-10-INSB-04-01, call ‘Investissements d’Avenir’).

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  1. Stephen Kerridge and Akankshi Munjal: These authors contributed equally to this work.

Authors and Affiliations

  1. Aix Marseille Université, CNRS, IBDM UMR7288, 13009 Marseille, France

    Stephen Kerridge, Akankshi Munjal, Jean-Marc Philippe, Ankita Jha, Alain Garcia de las Bayonas, Andrew J. Saurin & Thomas Lecuit

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Contributions

S.K. and T.L. planned the project. S.K., A.M. and T.L. analysed the data. S.K. discovered smog and performed the experiments shown in Figs 1, 3–5 and Supplementary Figs 1, and 3 and 4. A.M. carried out the experiments in Figs 4–6 and the quantifications of Figs 1 and 4–6. A.G.d.l.B. performed the experiments in Fig. 2 and Supplementary Fig. 2. A.J. carried out the experiments and quantifications in Supplementary Figs 4 and 5. J.-M.P. made the constructs, cloning and molecular characterization of smog. A.J.S. provided unpublished materials and technical expertise for the S2 cell experiments (Supplementary Fig. 4). S.K., A.M. and T.L. wrote the paper. All authors commented on the manuscript.

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Correspondence to Stephen Kerridge or Thomas Lecuit.

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Integrated supplementary information

Supplementary Figure 2 Gβ13F is required for apical MyoII accumulation.

MyoII in control and Gβ13F mutant mesoderm (a) and ectoderm (b). Scale bars 10 μm (a) and 5 μm (b).

Supplementary Figure 3 RhoGEF affects elongation.

Embryos showing elongation defects in mutant RhoGEF2 and RNAi compared to controls (a). Arrow heads point to the dorsal edge of posterior midgut at indicated times and red lines highlight the extent of elongation at indicated time. Note the folds in ectoderm (white arrows) (b) MyoII::GFP levels in controls and RhoGEF2 over-expression (c) MyoII::GFP levels in Gα12/13QL303 plus RhoGEF4 RNAi (right panel compared to Gα12/13QL303 (left) and Gα12/13QL303 plus rhoGEF2 RNAi (middle). Scale bars 100 μm (a) and 5 μm (b).

Supplementary Figure 4 Smog gene structure, knock out and RNAi probe.

(a) CG31660 gene structure encoding for Smog. Red boxes: coding exons, blue boxes: 5′ and3′ non coding exons. The predicted 7 pass transmembrane regions are depicted above. Smog disrupting dsRNA probe below in brown. The deleted portion of the knockout of smog between red lines. (b) Real time QPCR using gDNA showing that smog knock out lacks the WT locus (see Materials and Methods); n = 3 independent experiments. (c) RT-QPCR showing the specific absence of mRNAs transcribed from the smog knock out. (see Materials and Methods); n = 3 independent experiments. Error bars are Standard Error of Mean.

Supplementary Figure 5 Fog induces endocytosis of Smog and is immobilized on heterologous cells expressing Smog::GFP.

(a) partial rescue of the smog− elongation phenotype by sqh-driven production of Smog and Smog::GFP. (b) Functional Smog::GFP is detected at the surface of epithelial cells: top orthogonal view lower panels single planes (c) Smog::GFP is also detected in intracellular organelles in mesoderm cells (left top, arrowheads). Loss of zygotic Fog reduces Smog::GFP positive organelles in mesoderm cells (top right) prior to constriction (d) Smog::GFP (green) is detected together with extracellular-injected dextran (magenta) at the surface and in intracellular organelles in the ectoderm during intercalation (top panel). Overexpression of Fog increases intracellular Smog::GFP positive organelles (bottom panel, quantified in (g) where n = number of embryos and ∗∗∗∗∗ is p < 0.000005). Vesicle sizes are often larger in cells over-expressing Fog (d enlarged in right panels). (e) Fog (red) is immobilised on the surface of S2 cells expressing Smog::GFP (green); quantified in (f) n = 68 (GFP positive) and 95 (GFP negative) cells. Error bars are Standard Error of Mean. Scale bars 5 μm.

Supplementary Figure 6 Smog is required for apical accumulation of Rok and Rho1 in the mesoderm.

Ubi-Rok::GFP (a) and Rho biosensor::GFP distribution in mesoderm cells at indicated times in control and smog mutants. Scale bars 5 μm.

Supplementary Figure 7 Models for modular and quantitative control of MyoII activation.

Localised inputs derive from striped ectoderm (orange) and ventral mesoderm (purple) expressed transcription factors in blastoderm embryos (top). Mesoderm and endoderm patterning relies on Fog and possibly other ligands signalling via multiple, localised (e.g. Mist) or ubiquitous (e.g. Smog) GPCRs, which relay information to G proteins α,β andγ. T48 and Tolls are single pass transmembrane proteins.

Supplementary Table 1 Summary of genotypes employed.
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Supplementary information

Supplementary Information

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Developing mesoderm in control and Gγ1 mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green); Scale = 5 μm. (MOV 1663 kb)

Developing mesoderm in control and Gα12/13 mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green); Scale = 5 μm. (MOV 4069 kb)

Developing mesoderm in control and Gαβ13F mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green); Scale = 5 μm. (MOV 8753 kb)

Developing ectoderm in control and Gγ1 mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green) on left and MyoII::Cherry on right; Scale = 5 μm. (MOV 12798 kb)

Developing ectoderm in control and Gα12/13 mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green) on left and MyoII::Cherry on right; Scale = 5 μm. (MOV 5888 kb)

Developing ectoderm in control and Gβ13F mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green) on left and MyoII::Cherry on right; Scale = 5 μm. (MOV 8642 kb)

Developing mesoderm in control, smog RNAi, mist RNAi and smog + mist double RNAi embryos.

MyoII::Cherry (magenta) and E-cadherin::GFP (green); Scale = 5 μm. (MOV 19912 kb)

Developing mesoderm in control, fog RNAi, mist + fog RNAi and smog + fog double RNAi embryos.

MyoII::Cherry (magenta) and E-cadherin::GFP (green); Scale = 5 μm. (MOV 17525 kb)

Developing ectoderm in control and smog− mutant.

MyoII::Cherry (magenta) and E-cadherin::GFP (green) on left and MyoII::Cherry on right; Scale = 5 μm. (MOV 5392 kb)

Developing mesoderm in control, H1152 5 mM and H1152 10 mM injected embryos.

MyoII::Cherry (green) and E-cadherin::GFP (purple); Scale = 5 μm. (MOV 8636 kb)

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Kerridge, S., Munjal, A., Philippe, JM. et al. Modular activation of Rho1 by GPCR signalling imparts polarized myosin II activation during morphogenesis. Nat Cell Biol 18, 261–270 (2016). https://doi.org/10.1038/ncb3302

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