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Actin dynamics drive cell-like membrane deformation

Nature Physics volume 15, pages 602–609 (2019)Cite this article

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Abstract

Cell membrane deformations are crucial for proper cell function. Specialized protein assemblies initiate inward or outward membrane deformations that the cell uses respectively to uptake external substances or probe the environment. The assembly and dynamics of the actin cytoskeleton are involved in this process, although their detailed role remains controversial. We show here that a dynamic, branched actin network is sufficient to initiate both inward and outward membrane deformation. The polymerization of a dense actin network at the membrane of liposomes produces inward membrane bending at low tension, while outward deformations are robustly generated regardless of tension. Our results shed light on the mechanism cells use to internalize material, both in mammalian cells, where actin polymerization forces are required when membrane tension is increased, and in yeast, where those forces are necessary to overcome the opposing turgor pressure. By combining experimental observations with physical modelling, we propose a mechanism that explains how membrane tension and the architecture of the actin network regulate cell-like membrane deformations.

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Fig. 1: Experimental system and observations.
Fig. 2: Actin incorporation during tube formation.
Fig. 3: Tube length compared to network thickness.
Fig. 4: Actin incorporation in spikes.
Fig. 5: Model for spike initiation and tube formation.
Fig. 6: Dependence of membrane deformations on membrane tension and actin network mesh size.

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Data availability

The data that support the plots within this paper and other findings of this study are available from the corresponding author upon request.

Change history

  • 26 April 2019

    In the Supplementary Information initially published online for this Article, Supplementary Figs. 1, 2, 4, 5, 8–11 were corrupted; these have now been corrected.

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Acknowledgements

We acknowledge A. Kawska at IlluScientia.com for the figures. We thank J. Pernier for suggesting the excess profiling experiment for loosening the actin network. This work was supported by the French Agence Nationale pour la Recherche (ANR), grants ANR 09BLAN0283 and ANR 12BSV5001401, by Fondation pour la Recherche Médicale, grant DEQ20120323737, by the LabEx CelTisPhyBio postdoctoral fellowship (M.L.), no. ANR-10-LBX-0038 part of the IDEX PSL NANR- 10-IDEX-0001-02 PSL, by Marie Curie Integration Grant PCIG12-GA-2012-334053, ‘Investissements d’Avenir’ LabEx PALM (ANR-10-LABX-0039-PALM), ANR grant ANR-15-CE13-0004-03 and ERC Starting Grant 677532. Our groups belong to the CNRS consortium CellTiss. This work was supported by grants from the French National Research Agency through the ‘Investments for the Future’ (France-BioImaging, ANR-10-INSB-04), the PICT-IBiSA Institut Curie (Paris, France).

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Author notes

  1. These authors contributed equally: Camille Simon, Rémy Kusters, Valentina Caorsi.

  2. These authors jointly supervised this work: Pierre Sens, Cécile Sykes.

Authors and Affiliations

  1. Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168, Paris, France

    Camille Simon, Rémy Kusters, Valentina Caorsi, Antoine Allard, Majdouline Abou-Ghali, John Manzi, Aurélie Di Cicco, Daniel Lévy, Jean-François Joanny, Julie Plastino, Pierre Sens & Cécile Sykes

  2. Sorbonne Universités, UPMC Univ. Paris 06, Paris, France

    Camille Simon, Rémy Kusters, Valentina Caorsi, Antoine Allard, Majdouline Abou-Ghali, John Manzi, Aurélie Di Cicco, Daniel Lévy, Jean-François Joanny, Julie Plastino, Pierre Sens & Cécile Sykes

  3. LAMBE, Université Evry, CNRS, CEA, Université Paris-Saclay, Evry, France

    Antoine Allard & Clément Campillo

  4. LPTMS, CNRS, Univ. Paris-Sud, Université Paris-Saclay, Orsay, France

    Martin Lenz

  5. ESPCI-Paris, Paris, France

    Jean-François Joanny

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Contributions

C.S., R.K. and V.C. have equal contributions. C.S. and V.C. performed experiments and analysed data. R.K. performed the development of theoretical models. A.A. M.A.-G., J.M., A.D.C., D.L., C.C. and J.P. contributed to experimental data; M.L. and J.-F.J. contributed to the development of the model; P.S. and C.S. designed the research. All authors contributed to writing the paper.

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Correspondence to Pierre Sens or Cécile Sykes.

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Journal peer review information: Nature Physics thanks Allen Liu and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Simon, C., Kusters, R., Caorsi, V. et al. Actin dynamics drive cell-like membrane deformation. Nat. Phys. 15, 602–609 (2019). https://doi.org/10.1038/s41567-019-0464-1

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