Interfacial friction and substrate deformation mediate long-range signal propagation in tissues.

Diffusive force propagation Elasticity theory Elasticity-friction coupling Extracellular matrix Tissue layer Tissue-substrate interaction

Journal

Biomechanics and modeling in mechanobiology
ISSN: 1617-7940
Titre abrégé: Biomech Model Mechanobiol
Pays: Germany
ID NLM: 101135325

Informations de publication

Date de publication:
Oct 2022
Historique:
received: 25 03 2022
accepted: 22 06 2022
pubmed: 4 9 2022
medline: 4 11 2022
entrez: 3 9 2022
Statut: ppublish

Résumé

Tissue layers can generally slide at the interface, accompanied by the dissipation due to friction. Nevertheless, it remains elusive how force could propagate in a tissue with such interfacial friction. Here, we elaborate the force dynamics in a prototypical multilayer system in which an epithelial monolayer was cultivated upon an elastic substrate in contact with a hard surface, and discover a novel mechanism of pronounced force propagation over a long distance due to interfacial dynamics between substrate layers. We derived an analytical model for the dynamics of the elastic substrate under the shear stress provided by the cell layer at the surface boundary and the friction at bottom. The model reveals that sliding between substrate layers leads to an expanding stretch regime from a shear regime of substrate deformation in time and space. The regime boundary propagating diffusively with a speed depending on the stiffness, thickness, and slipperiness of the substrate, is a robust nature of a deformed elastic sheet with interfacial friction. These results shed new light on force propagation in tissues and our model could serve as a basis for studies of such propagation in a more complex tissue environment.

Identifiants

pubmed: 36057053
doi: 10.1007/s10237-022-01603-3
pii: 10.1007/s10237-022-01603-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1511-1530

Subventions

Organisme : Ministry of Education - Singapore
ID : MOE2015-T2-1-116
Organisme : Ministry of Education - Singapore
ID : MOE2020-T2-2-033

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Aoki K, Kondo Y, Naoki H et al (2017) Propagating wave of erk activation orients collective cell migration. Dev Cell 43(3):305-317.e5
Asano S, Ito S, Morosawa M et al (2018) Cyclic stretch enhances reorientation and differentiation of 3-d culture model of human airway smooth muscle. Biochem Biophys Reports 16:32–38
Barnett CH, Cobbold A (1962) Lubrication within living joints. J Bone and Joint Surg British 44(3):662–674
doi: 10.1302/0301-620X.44B3.662
Bertet C, Sulak L, Lecuit T (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429(6992):667–671. https://doi.org/10.1038/nature02590
doi: 10.1038/nature02590
Blanch-Mercader C, Casademunt J (2017) Hydrodynamic instabilities, waves and turbulence in spreading epithelia. Soft Matter 13(38):6913–6928
doi: 10.1039/C7SM01128H
Boocock D, Hino N, Ruzickova N et al (2021) Theory of mechanochemical patterning and optimal migration in cell monolayers. Nat Phys 17(2):267–274
doi: 10.1038/s41567-020-01037-7
Burla F, Mulla Y, Vos BE et al (2019) From mechanical resilience to active material properties in biopolymer networks. Nat Rev Phys 1(4):249–263
doi: 10.1038/s42254-019-0036-4
Buxboim A, Ivanovska IL, Discher DE (2010) Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells “feel” outside and in? J Cell Sci 123(3), 297–308. https://doi.org/10.1242/jcs.041186,
Chaudhuri O, Cooper-White J, Janmey PA et al (2020) Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature 584(7822):535–546
doi: 10.1038/s41586-020-2612-2
Cui Y, Hameed FM, Yang B et al (2015) Cyclic stretching of soft substrates induces spreading and growth. Nat Commun 6(1):6333. https://doi.org/10.1038/ncomms7333
doi: 10.1038/ncomms7333
De R, Safran SA (2008) Dynamical theory of active cellular response to external stress. Phys Rev E 78(031):923. https://doi.org/10.1103/PhysRevE.78.031923
doi: 10.1103/PhysRevE.78.031923
De R, Zemel A, Safran SA (2007) Dynamics of cell orientation. Nat Phys 3(9):655–659. https://doi.org/10.1038/nphys680
doi: 10.1038/nphys680
De Gennes P (1976) Dynamics of entangled polymer solutions.i. the rouse model. Macromolecules 9(4):587
Deforet M, Hakim V, Yevick H et al (2014) Emergence of collective modes and tri-dimensional structures from epithelial confinement. Nat Commun 5(1):1–9
doi: 10.1038/ncomms4747
Dupont S, Morsut L, Aragona M et al (2011) Role of yap/taz in mechanotransduction. Nature 474(7350):179–183
doi: 10.1038/nature10137
Fukuyama T, Ebata H, Kondo Y, et al (2020) Why epithelial cells collectively move against a traveling signal wave, https://arxiv.org/abs/2008.12955”, preprint
Gudipaty SA, Lindblom J, Loftus PD et al (2017) Mechanical stretch triggers rapid epithelial cell division through piezo1. Nature 543(7643):118–121. https://doi.org/10.1038/nature21407
doi: 10.1038/nature21407
Heisenberg CP, Bellaïche Y (2013) Forces in tissue morphogenesis and patterning. Cell 153(5):948–962. https://doi.org/10.1016/j.cell.2013.05.008
doi: 10.1016/j.cell.2013.05.008
Hino N, Rossetti L, Marín-Llauradó A et al (2020) Erk-mediated mechanochemical waves direct collective cell polarization. Dev Cell 53(6):646-660.e8
Hoffman BD, Grashoff C, Schwartz MA (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475(7356):316–323. https://doi.org/10.1038/nature10316
doi: 10.1038/nature10316
Iwadate Y, Okimura C, Sato K et al (2013) Myosin-ii-mediated directional migration of dictyostelium cells in response to cyclic stretching of substratum. Biophys J 104(4):748–758. https://doi.org/10.1016/j.bpj.2013.01.005
doi: 10.1016/j.bpj.2013.01.005
Katta J, Jin Z, Ingham E et al (2008) Biotribology of articular cartilage-a review of the recent advances. Med eng & phys 30(10):1349–1363
doi: 10.1016/j.medengphy.2008.09.004
Kawaue T, Yow I, Le AP et al (2021). Mechanics defines the spatial pattern of compensatory proliferation. https://doi.org/10.1101/2021.07.04.451019
doi: 10.1101/2021.07.04.451019
Khalilgharibi N, Fouchard J, Asadipour N et al (2019) Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex. Nat Phys 15:839–847. https://doi.org/10.1038/s41567-019-0516-6
doi: 10.1038/s41567-019-0516-6
Kocgozlu L, Saw TB, Le AP et al (2016) Epithelial cell packing induces distinct modes of cell extrusions. Current Biol 26(21):2942–2950. https://doi.org/10.1016/j.cub.2016.08.057
doi: 10.1016/j.cub.2016.08.057
Kruse K, Joanny J, Jülicher F et al (2006) Contractility and retrograde flow in lamellipodium motion. Phys Biol 3(2):130
doi: 10.1088/1478-3975/3/2/005
Leong MC, Nai MH, Cheong FC et al (2015) Viscoelastic effects of silicone gels at the micro-and nanoscale. Procedia IUTAM 12:20–30
doi: 10.1016/j.piutam.2014.12.004
Levine AJ, MacKintosh F (2009) The mechanics and fluctuation spectrum of active gels. J Phys Chem B 113(12):3820–3830
doi: 10.1021/jp808192w
Liu Z, Tan JL, Cohen DM, et al. (2010) Mechanical tugging force regulates the size of cell-cell junctions. Proceedings of the National Academy of Sciences 107(22), 9944–9949. doi: https://doi.org/10.1073/pnas.0914547107
Lu P, Weaver VM, Werb Z (2012) The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 196(4):395–406
doi: 10.1083/jcb.201102147
Maloney JM, Walton EB, Bruce CM, et al (2008) Influence of finite thickness and stiffness on cellular adhesion-induced deformation of compliant substrata. Phys Review E 78(4):041,923
Marchetti MC, Joanny JF, Ramaswamy S et al (2013) Hydrodynamics of soft active matter. Rev Mod Phys 85:1143–1189. https://doi.org/10.1103/RevModPhys.85.1143
doi: 10.1103/RevModPhys.85.1143
Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457(7228):495–499. https://doi.org/10.1038/nature07522
doi: 10.1038/nature07522
Maruthamuthu V, Sabass B, Schwarz US, et al. (2011) Cell-ecm traction force modulates endogenous tension at cell-cell contacts. Proceedings of the National Academy of Sciences 108(12), 4708–4713. doi: 10.1073/pnas.1011123108
Merkel R, Kirchgeßner N, Cesa CM et al (2007) Cell force microscopy on elastic layers of finite thickness. Biophys J 93(9):3314–3323. https://doi.org/10.1529/biophysj.107.111328
doi: 10.1529/biophysj.107.111328
Merkher Y, Sivan S, Etsion I et al (2006) A rational human joint friction test using a human cartilage-on-cartilage arrangement. Tribol Lett 22(1):29–36
doi: 10.1007/s11249-006-9069-9
Nardone G, Oliver-De La Cruz J, Vrbsky J et al (2017) Yap regulates cell mechanics by controlling focal adhesion assembly. Nat Commun 8(1):1–13
doi: 10.1038/ncomms15321
Panzetta V, Fusco S, Netti PA (2019) Cell mechanosensing is regulated by substrate strain energy rather than stiffness. Proceedings of the National Academy of Sciences 116(44):22,004–22,013
Ranft J, Prost J, Jülicher F et al (2012) Tissue dynamics with permeation. Eur Phys J E 35(6):1–13
doi: 10.1140/epje/i2012-12046-5
Roca-Cusachs P, Conte V, Trepat X (2017) Quantifying forces in cell biology. Nat Cell Biol 19(7):742–751
doi: 10.1038/ncb3564
Sen S, Engler AJ, Discher DE (2009) Matrix strains induced by cells: Computing how far cells can feel. Cell Mol Bioeng 2(1):39–48. https://doi.org/10.1007/s12195-009-0052-z
doi: 10.1007/s12195-009-0052-z
Serra-Picamal X, Conte V, Vincent R et al (2012) Mechanical waves during tissue expansion. Nat Phys 8(8):628–634
doi: 10.1038/nphys2355
Shacham S, Castel D, Gefen A (2010) Measurements of the static friction coefficient between bone and muscle tissues. J Biomech Eng 132(084):502
Steinwachs J, Metzner C, Skodzek K et al (2016) Three-dimensional force microscopy of cells in biopolymer networks. Nat Methods 13(2):171–176. https://doi.org/10.1038/nmeth.3685
doi: 10.1038/nmeth.3685
Tambe DT, Corey Hardin C, Angelini TE et al (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10(6):469–475. https://doi.org/10.1038/nmat3025
doi: 10.1038/nmat3025
Tanaka T, Fillmore DJ (1979) Kinetics of swelling of gels. J Chem Phys 70(3):1214–1218
doi: 10.1063/1.437602
Tawada K, Sekimoto K (1991) Protein friction exerted by motor enzymes through a weak-binding interaction. J Theor Biol 150(2):193–200
doi: 10.1016/S0022-5193(05)80331-5
Tawada K, Sekimoto K (1991) Protein friction exerted by motor enzymes through a weak-binding interaction. J Theoretical Biol 150(2):193–200. https://doi.org/10.1016/S0022-5193(05)80331-5
doi: 10.1016/S0022-5193(05)80331-5
Teng X, Toyama Y (2011) Apoptotic force: Active mechanical function of cell death during morphogenesis. Development, Growth & Differentiation 53(2), 269–276. doi: https://doi.org/10.1111/j.1440-169X.2011.01251.x
Teng X, Qin L, Borgne RL et al (2017) Remodeling of adhesion and modulation of mechanical tensile forces during apoptosis in drosophila epithelium. Development 144(1):95–105. https://doi.org/10.1242/dev.139865
doi: 10.1242/dev.139865
Toyama Y, Peralta XG, Wells AR, et al. (2008) Apoptotic force and tissue dynamics during drosophila embryogenesis. Science 321(5896), 1683–1686. doi: https://doi.org/10.1126/science.1157052
Trepat X, Wasserman MR, Angelini TE et al (2009) Physical forces during collective cell migration. Nat Phys 5(6):426–430. https://doi.org/10.1038/nphys1269
doi: 10.1038/nphys1269
Uroz M, Wistorf S, Serra-Picamal X et al (2018) Regulation of cell cycle progression by cell-cell and cell-matrix forces. Nat Cell Biol 20(6):646–654. https://doi.org/10.1038/s41556-018-0107-2
doi: 10.1038/s41556-018-0107-2
Wang N, Tolic-Nørrelykke IM, Chen J, et al (2002) Cell prestress. i. stiffness and prestress are closely associated in adherent contractile cells. Am J Physio-Cell Physiol 282(3):C606–C616
Zhou Z, Jin Z (2015) Biotribology: recent progresses and future perspectives. Biosurf biotribol 1(1):3–24
doi: 10.1016/j.bsbt.2015.03.001

Auteurs

Yuting Lou (Y)

Mechanobiology Institute, National University Singapore, queenstown, 100190, Singapore. chelinqueen@hotmail.com.

Takumi Kawaue (T)

Mechanobiology Institute, National University Singapore, queenstown, 100190, Singapore.

Ivan Yow (I)

Mechanobiology Institute, National University Singapore, queenstown, 100190, Singapore.

Yusuke Toyama (Y)

Mechanobiology Institute, National University Singapore, queenstown, 100190, Singapore.

Jacques Prost (J)

Mechanobiology Institute, National University Singapore, queenstown, 100190, Singapore.
Laboratoire Physico Chimie Curie, Institut Curie, Paris Science et Lettres Research University, CNRS UMR168, Paris, 75005, France.

Tetsuya Hiraiwa (T)

Mechanobiology Institute, National University Singapore, queenstown, 100190, Singapore. mbithi@nus.edu.sg.

Articles similaires

Calcium Carbonate Sand Powders Construction Materials Materials Testing

Strain learning in protein-based mechanical metamaterials.

Naroa Sadaba, Eva Sanchez-Rexach, Curt Waltmann et al.
1.00
Serum Albumin, Bovine Stress, Mechanical Animals Polymers Materials Testing

Emergent behaviors of buckling-driven elasto-active structures.

Yuchen Xi, Tom Marzin, Richard B Huang et al.
1.00
Elasticity Robotics Animals Movement
Humans Finite Element Analysis Malocclusion, Angle Class II Biomechanical Phenomena Male

Classifications MeSH