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Mechanical waves during tissue expansion

Nature Physics volume 8, pages 628–634 (2012)Cite this article

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Abstract

The processes by which an organism develops its shape and heals wounds involve expansion of a monolayer sheet of cells. The mechanism underpinning this epithelial expansion remains obscure, despite the fact that its failure is known to contribute to several diseases, including carcinomas, which account for about 90% of all human cancers. Here, using the micropatterned epithelial monolayer as a model system, we report the discovery of a mechanical wave that propagates slowly to span the monolayer, traverses intercellular junctions in a cooperative manner and builds up differentials of mechanical stress. Essential features of this wave generation and propagation are captured by a minimal model based on sequential fronts of cytoskeletal reinforcement and fluidization. These findings establish a mechanism of long-range cell guidance, symmetry breaking and pattern formation during monolayer expansion.

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Figure 1: Experimental model.
Figure 2: Maps of cell velocity, cell substrate tractions and monolayer stresses.
Figure 3: Dynamic behaviour of a cell sheet expanding nearly symmetrically.
Figure 4: Essential features of wave generation and propagation are captured by a minimal model based on sequential fronts of cytoskeletal reinforcement and fluidization.

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Acknowledgements

We thank M. Bintanel for technical assistance, S. Garcia and A. Carreras for help with polyacrylamide gels and micropatterning, the Nanotechnology Platform from Barcelona Science Park, J. J. Munoz for help with the numerical implementation of the model, and P. Roca-Cusachs, D.G. Miguez, D. Navajas, R. Farre and J. Alcaraz for discussions. This research was supported by the Spanish Ministry for Science and Innovation (BFU2009-07595 and FPU fellowship XS), the European Research Council (Grant Agreement 242993) and the National Institutes of Health (R01HL102373, R01HL107561).

Author information

Author notes

  1. Xavier Serra-Picamal and Vito Conte: These authors contributed equally to this work

Authors and Affiliations

  1. Institute for Bioengineering of Catalonia, Barcelona 08028, Spain

    Xavier Serra-Picamal, Vito Conte, Romaric Vincent, Ester Anon, Elsa Bazellieres & Xavier Trepat

  2. Facultat de Medicina, Universitat de Barcelona, and Ciber Enfermedades Respiratorias, Barcelona 08036, Spain

    Xavier Serra-Picamal & Xavier Trepat

  3. Laboratoire Matière et Systèmes Complexes (MSC), Université Paris Diderot, and Unité Mixte de Recherche 7057 CNRS, Paris, F-75205 Paris Cedex 13, France

    Ester Anon

  4. School of Public Health, Harvard University, Boston, Massachusetts 02115, USA

    Dhananjay T. Tambe, James P. Butler & Jeffrey J. Fredberg

  5. Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA

    James P. Butler

  6. Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona 08010, Spain

    Xavier Trepat

Authors
  1. Xavier Serra-Picamal
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Contributions

X.S-P. and X.T. designed experiments; X.S-P. performed all experiments. E.B. and X.S-P. performed gene expression experiments; X.S-P., R.V., V.C. and X.T. analysed data; D.T.T. contributed software; V.C. built the computer model and performed simulations; X.S-P., V.C., J.J.F. and X.T. wrote the manuscript; all authors discussed and interpreted results and commented on the manuscript; X.T. supervised the project.

Corresponding author

Correspondence to Xavier Trepat.

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The authors declare no competing financial interests.

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Serra-Picamal, X., Conte, V., Vincent, R. et al. Mechanical waves during tissue expansion. Nature Phys 8, 628–634 (2012). https://doi.org/10.1038/nphys2355

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