Fibrin Networks Support Recurring Mechanical Loads by Adapting their Structure across Multiple Scales.
Tissues and cells sustain recurring mechanical loads that span a wide range of loading amplitudes and timescales as a consequence of exposure to blood flow, muscle activity, and external impact. Both tissues and cells derive their mechanical strength from fibrous protein scaffolds, which typically have a complex hierarchical structure. In this study, we focus on a prototypical hierarchical biomaterial, fibrin, which is one of the most resilient naturally occurring biopolymers and forms the structural scaffold of blood clots. We show how fibrous networks composed of fibrin utilize irreversible changes in their hierarchical structure at different scales to maintain reversible stress stiffening up to large strains. To trace the origin of this paradoxical resilience, we systematically tuned the microstructural parameters of fibrin and used a combination of optical tweezers and fluorescence microscopy to measure the interactions of single fibrin fibers for the first time, to our knowledge. We demonstrate that fibrin networks adapt to moderate strains by remodeling at the network scale through the spontaneous formation of new bonds between fibers, whereas they adapt to high strains by plastic remodeling of the fibers themselves. This multiscale adaptation mechanism endows fibrin gels with the remarkable ability to sustain recurring loads due to shear flows and wound stretching. Our findings therefore reveal a microscopic mechanism by which tissues and cells can balance elastic nonlinearity and plasticity, and thus can provide microstructural insights into cell-driven remodeling of tissues.
Department of Systems Biophysics, FOM Institute AMOLF, Amsterdam, The Netherlands; Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, The Netherlands; Institute for Complex Molecular Systems, Eindhoven University of Technology, Eindhoven, The Netherlands.
Nicholas A
NA
Kurniawan
Department of Systems Biophysics, FOM Institute AMOLF, Amsterdam, The Netherlands.
Bart E
BE
Vos
Department of Physics and Astronomy, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Andreas
A
Biebricher
Department of Physics and Astronomy, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Gijs J L
GJ
Wuite
Department of Physics and Astronomy, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Erwin J G
EJ
Peterman
Department of Systems Biophysics, FOM Institute AMOLF, Amsterdam, The Netherlands. Electronic address: g.koenderink@amolf.nl.
Gijsje H
GH
Koenderink
D004548:Elasticity; D005337:Fibrin / Q000737:chemistry* / Q000378:metabolism; D006801:Humans; D008856:Microscopy, Fluorescence; D052898:Optical Tweezers; D012212:Rheology; D013314:Stress, Mechanical
D005337:Fibrin