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Stress management in composite biopolymer networks

Nature Physics volume 15, pages 549–553 (2019)Cite this article

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Abstract

Living tissues show an extraordinary adaptiveness to strain, which is crucial for their proper biological functioning1,2. The physical origin of this mechanical behaviour has been widely investigated using reconstituted networks of collagen fibres, the principal load-bearing component of tissues3,4,5. However, collagen fibres in tissues are embedded in a soft hydrated polysaccharide matrix, which generates substantial internal stresses, and the effect of this on tissue mechanics is unknown6,7,8. Here, by combining mechanical measurements and computer simulations, we show that networks composed of collagen fibres and a hyaluronan matrix exhibit synergistic mechanics characterized by an enhanced stiffness and delayed strain stiffening. We demonstrate that the polysaccharide matrix has a dual effect on the composite response involving both internal stress and elastic reinforcement. Our findings elucidate how tissues can tune their strain-sensitivity over a wide range and provide a novel design principle for synthetic materials with programmable mechanical properties.

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Fig. 1: Composite collagen–hyaluronan networks as a minimal tissue-mimetic model system.
Fig. 2: Hyaluronan gel prestresses the collagen network during gelation.
Fig. 3: Computational modelling of two-component networks reveals that the composite mechanics depends on a balance between collagen bending and hyaluronan contraction.
Fig. 4: The mechanical response of composite networks can be mapped onto an effective single-component model.

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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 authors upon reasonable request.

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Acknowledgements

The authors thank F. C. MacKintosh (Rice University, Texas), E. Pelan (University of Birmingham), K. Jansen (UMC, Utrecht) and S. Stoyanov (Unilever B.V., the Netherlands) for many useful discussions, A. Sharma (Leibniz Institute for Polymer Research, Dresden) for the MatLab script for determining the bending rigidity of collagen fibres from rheology data, D. Nedrelow (University of Minnesota) for suggestions regarding the sample preparation, K. Miura (EMBL, Heidelberg, Germany) for the Temporal Colour Code ImageJ plugin and J. T. B. Overvelde (AMOLF, Amsterdam) for a critical reading of the manuscript. The work of F.B. and G.H.K. is part of the Industrial Partnership Programme Hybrid Soft Materials, which is carried out under an agreement between Unilever Research and Development B.V. and the Netherlands Organisation for Scientific Research (NWO). The work of J.T., S.D. and J.v.d.G. is part of the SOFTBREAK project funded by the European Research Council (ERC Consolidator Grant).

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Author notes

  1. These authors contributed equally: Federica Burla, Justin Tauber.

Authors and Affiliations

  1. AMOLF, Department of Living Matter, Biological Soft Matter group, Amsterdam, The Netherlands

    Federica Burla & Gijsje H. Koenderink

  2. Physical Chemistry and Soft Matter, Wageningen University & Research, Wageningen, The Netherlands

    Justin Tauber, Simone Dussi & Jasper van der Gucht

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  1. Federica Burla
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  5. Gijsje H. Koenderink
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Contributions

F.B. and G.H.K designed the experiments. F.B. performed and analysed the experiments under the supervision of G.H.K. J.T. and S.D. designed, performed and analysed the simulations under the supervision of J.v.d.G. All authors interpreted and discussed the results and co-wrote the paper.

Corresponding authors

Correspondence to Simone Dussi or Gijsje H. Koenderink.

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Journal peer review information: Nature Physics thanks Wouter Ellenbroek, Spencer Lake and Tom Shearer for their contribution to the peer review of this work.

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Supplementary Figures 1–20 and Supplementary References 1–7.

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Burla, F., Tauber, J., Dussi, S. et al. Stress management in composite biopolymer networks. Nat. Phys. 15, 549–553 (2019). https://doi.org/10.1038/s41567-019-0443-6

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