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Nucleation geometry governs ordered actin networks structures

Nature Materials volume 9, pages 827–832 (2010)Cite this article

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Abstract

Actin filaments constitute one of the main components of cell cytoskeleton. Assembled into bundles in filopodia or in stress fibres, they play a pivotal role in eukaryotes during cell morphogenesis, adhesion and motility. The bundle emergence has been extensively related to specific actin regulators1,2,3 in vivo4,5,6,7. Such dynamic modulation was also highlighted by biochemical reconstitution of the actin-network assembly, in bulk solution or with biomimetic devices8,9,10,11,12,13,14,15,16,17,18. However, the question of how geometrical boundaries, such as those encountered in cells, affect the dynamic formation of highly ordered actin structures remains poorly studied14,19. Here we demonstrate that the nucleation geometry in itself can be the principal determinant of actin-network architecture. We developed a micropatterning method that enables the spatial control of actin nucleation sites for in vitro assays. Shape, orientation and distance between nucleation regions control filament orientation and length, filament–filament interactions and filopodium-like bundle formation. Modelling of filament growth and interactions demonstrates that basic mechanical and probabilistic laws govern actin assembly in higher-order structures.

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Figure 1: Geometrical control of actin nucleation and growth.
Figure 2: Filament length controls their ability to cross dense actin networks.
Figure 3: Orientation of nucleation regions controls bundle formation.
Figure 4: Intrinsic properties and collective assembly of actin filaments regulate parallel-bundle formation.

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Acknowledgements

We are grateful to C. J. Staiger, J. Plastino and D. Pellman for critical reading of the manuscript and suggestions. This work was supported by grants from Agence National pour la Recherche to L.B. (ANR-06-PCV1-0022 and ANR-08-BLAN-0012) and M.T. (ANR-08-JC-0103 and ANR-PCV08-322457); A-C.R. is supported by an IRTELIS fellowship from CEA.

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Authors and Affiliations

  1. Institut de Recherches en Technologies et Sciences pour le Vivant, iRTSV, Laboratoire de Physiologie Cellulaire et Végétale, CNRS/CEA/INRA/UJF, Grenoble, 38054, France

    Anne-Cécile Reymann, Jean-Louis Martiel, Théo Cambier, Laurent Blanchoin, Rajaa Boujemaa-Paterski & Manuel Théry

  2. Laboratoire Techniques de l’Ingénierie Médicale et de la Complexité, CNRS/UJF, Pavillon Taillefer Faculté de Médecine, La Tronche, 38706, France

    Jean-Louis Martiel

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  1. Anne-Cécile Reymann
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  2. Jean-Louis Martiel
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Contributions

A-C.R. and T.C. carried out the experiments. J-L.M. carried out the physical modelling. L.B., R.B-P. and M.T. directed the project and wrote the manuscript.

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Correspondence to Rajaa Boujemaa-Paterski or Manuel Théry.

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The authors declare no competing financial interests.

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Reymann, AC., Martiel, JL., Cambier, T. et al. Nucleation geometry governs ordered actin networks structures. Nature Mater 9, 827–832 (2010). https://doi.org/10.1038/nmat2855

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