Emergence of Spatial Scales and Macroscopic Tissue Dynamics in Active Epithelial Monolayers

Selvamani P.a· Chelakkot R.b· Nandi A.b· Inamdar M.M.c

Author affiliations

aCenter for Research in Nanotechnology and Science, Indian Institute of Technology Bombay, Mumbai, India
bDepartment of Physics, Indian Institute of Technology Bombay, Mumbai, India
cDepartment of Civil Engineering, Indian Institute of Technology Bombay, Mumbai, India

Log in to MyKarger to check if you already have access to this content.

Buy FullText & PDF Unlimited re-access via MyKarger Unrestricted printing, no saving restrictions for personal use
read more

CHF 38.00 *
EUR 35.00 *
USD 39.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.

Save over 20% compared to the individual article price.

Learn more

Rent via DeepDyve Unlimited fulltext viewing of this article Organize, annotate and mark up articles Printing and downloading restrictions apply

Start free trial

Subscribe Access to all articles of the subscribed year(s) guaranteed for 5 years Unlimited re-access via Subscriber Login or MyKarger Unrestricted printing, no saving restrictions for personal use read more

Subcription rates

Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview

Abstract of Research Article

Received: June 05, 2022
Accepted: November 22, 2022
Published online: April 12, 2023

Number of Print Pages: 14
Number of Figures: 6
Number of Tables: 1

ISSN: 1422-6405 (Print)
eISSN: 1422-6421 (Online)

For additional information: https://www.karger.com/CTO

Abstract

Migrating cells in tissues are often known to exhibit collective swirling movements. In this paper, we develop an active vertex model with polarity dynamics based on contact inhibition of locomotion (CIL). We show that under this dynamics, the cells form steady-state vortices in velocity, polarity, and cell stress with length scales that depend on polarity alignment rate (ζ), self-motility (v0), and cell-cell bond tension (λ). When the ratio λ/v0 becomes larger, the tissue reaches a near jamming state because of the inability of the cells to exchange their neighbors, and the length scale associated with tissue kinematics increases. A deeper examination of this jammed state provides insights into the mechanism of sustained swirl formation under CIL rule that is governed by the feedback between cell polarities and deformations. To gain additional understanding of how active forcing governed by CIL dynamics leads to large-scale tissue dynamics, we systematically coarse-grain cell stress, polarity, and motility and show that the tissue remains polar even on larger length scales. Overall, we explore the origin of swirling patterns during collective cell migration and obtain a connection between cell-level dynamics and large-scale cellular flow patterns observed in epithelial monolayers.

© 2023 S. Karger AG, Basel

References Alert R, Trepat X. Physical models of collective cell migration. Annu Rev Condens Matter Phys. 2020;11(1):77–101. Alert R, Blanch-Mercader C, Casademunt J. Active fingering instability in tissue spreading. Phys Rev Lett. 2019;122(8):088104. Angelini TE, Hannezo E, Trepat X, Fredberg JJ, Weitz DA. Cell migration driven by cooperative substrate deformation patterns. Phys Rev Lett. 2010 Apr;104(16):168104. Banerjee S, Utuje KJC, Marchetti MC. Propagating stress waves during epithelial expansion. Phys Rev Lett. 2015;114(22):228101. Barton DL, Henkes S, Weijer CJ, Sknepnek R. Active vertex model for cell-resolution description of epithelial tissue mechanics. PLoS Comput Biol. 2017;13(6):e1005569. Bi D, Lopez JH, Schwarz JM, Manning ML. A density-independent rigidity transition in biological tissues. Nat Phys. 2015;11(12):1074–9. Bi D, Yang X, Marchetti MC, Manning ML. Motility-driven glass and jamming transitions in biological tissues. Phys Rev X. 2016 Apr;6(2):021011. Blanch-Mercader C, Yashunsky V, Garcia S, Duclos G, Giomi L, Silberzan P. Turbulent dynamics of epithelial cell cultures. Phys Rev Lett. 2018 May;120(20):208101. Collinet C, Lecuit T. Programmed and self-organized flow of information during morphogenesis. Nat Rev Mol Cell Biol. 2021;22(4):245–65. Comelles J, Ss S, Lu L, Le Maout E, Anvitha S, Salbreux G, et al. Epithelial colonies in vitro elongate through collective effects. Elife. 2021 Jan;10:e57730. Duclut C, Paijmans J, Inamdar MM, Modes CD, Jülicher F. Active T1 transitions in cellular networks. Eur Phys J E Soft Matter. 2022;45(3):29. Duclut C, Paijmans J, Inamdar MM, Modes CD, Jülicher F. Nonlinear rheology of cellular networks. Cells Dev. 2021;168:203746. Eaton S, Jülicher F. Cell flow and tissue polarity patterns. Curr Opin Genet Dev. 2011;21(6):747–52. Etournay R, Popović M, Merkel M, Nandi A, Blasse C, Aigouy B, et al. Interplay of cell dynamics and epithelial tension during morphogenesis of the drosophila pupal wing. Elife. 2015;4:e07090. Fang C, Yao J, Zhang Y, Lin Y. Active chemo-mechanical feedbacks dictate the collective migration of cells on patterned surfaces. Biophys J. 2022;121(7):1266–75. Farhadifar R, Röper JC, Aigouy B, Eaton S, Jülicher F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol. 2007;17(24):2095–104. Fletcher AG, Osborne JM, Maini PK, Gavaghan DJ. Implementing vertex dynamics models of cell populations in biology within a consistent computational framework. Prog Biophys Mol Biol. 2013;113(2):299–326. Fletcher AG, Osterfield M, Baker RE, Shvartsman SY. Vertex models of epithelial morphogenesis. Biophys J. 2014;106(11):2291–304. Friedl P, Hegerfeldt Y, Tusch M. Collective cell migration in morphogenesis and cancer. Int J Dev Biol. 2004;48(5–6):441–9. Friedl P, Locker J, Sahai E, Segall JE. Classifying collective cancer cell invasion. Nat Cell Biol. 2012;14(8):777–83. Giomi L. Geometry and topology of turbulence in active nematics. Phys Rev X. 2015;5(3):031003. Giomi L, Kos Ž, Ravnik M, Sengupta A. Cross-talk between topological defects in different fields revealed by nematic microfluidics. Proc Natl Acad Sci U S A. 2017;114(29):E5771–7. Guillot C, Lecuit T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science. 2013;340(6137):1185–9. Guirao B, Rigaud SU, Bosveld F, Bailles A, López-Gay J, Ishihara S, et al. Unified quantitative characterization of epithelial tissue development. Elife. 2015;4:e08519. Hakim V, Silberzan P. Collective cell migration: a physics perspective. Rep Prog Phys. 2017 Apr;80(7):076601. Heisenberg C-P, Bellaïche Y. Forces in tissue morphogenesis and patterning. Cell. 2013;153(5):948–62. Henkes S, Kostanjevec K, Collinson JM, Sknepnek R, Bertin E. Dense active matter model of motion patterns in confluent cell monolayers. Nat Commun. 2020 Mar;11(1):1405. Ladoux B, Mège R-M. Mechanobiology of collective cell behaviours. Nat Rev Mol Cell Biol. 2017;18(12):743–57. Lee P, Wolgemuth CW. Crawling cells can close wounds without purse strings or signaling. PLoS Comput Biol. 2011;7(3):e1002007. Lin S-Z, Merkel M, Rupprecht J-F. Implementation of cellular bulk stresses in vertex models of biological tissues. Eur Phys J E Soft Matter. 2022;45(1):4. Lin S-Z, Ye S, Xu G-K, Li B, Feng X-Q. Dynamic migration modes of collective cells. Biophys J. 2018;115(9):1826–35. Malinverno C, Corallino S, Giavazzi F, Bergert M, Li Q, Leoni M, et al. Endocytic reawakening of motility in jammed epithelia. Nat Mater. 2017 May;16(5):587–96. Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J, Rao M, et al. Hydrodynamics of soft active matter. Rev Mod Phys. 2013;85(3):1143–89. Mirams GR, Arthurs CJ, Bernabeu MO, Bordas R, Cooper J, Corrias A, et al. Chaste: an open source C++ library for computational physiology and biology. PLoS Comput Biol. 2013;9(3):e1002970. Mitchel JA, Das A, O’Sullivan MJ, Stancil IT, DeCamp SJ, Koehler S, et al. In primary airway epithelial cells, the unjamming transition is distinct from the epithelial-to-mesenchymal transition. Nat Commun. 2020;11(1):5053–14. Mueller R, Yeomans JM, Doostmohammadi A. Emergence of active nematic behavior in monolayers of isotropic cells. Phys Rev Lett. 2019;122(4):048004. Notbohm J, Banerjee S, Utuje KJC, Gweon B, Jang H, Park Y, et al. Cellular contraction and polarization drive collective cellular motion. Biophys J. 2016;110(12):2729–38. Petitjean L, Reffay M, Grasland-Mongrain E, Poujade M, Ladoux B, Buguin A, et al. Velocity fields in a collectively migrating epithelium. Biophys J. 2010 May;98(9):1790–800. Peyret G, Mueller R, d’Alessandro J, Begnaud S, Marcq P, Mège R-M, et al. Sustained oscillations of epithelial cell sheets. Biophys J. 2019 Aug;117(3):464–78. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, Ladoux B, et al. Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci U S A. 2007 Oct;104(41):15988–93. Recho P, Hallou A, Hannezo E. Theory of mechanochemical patterning in biphasic biological tissues. Proc Natl Acad Sci U S A. 2019;116(12):5344–9. Sepúlveda N, Petitjean L, Cochet O, Grasland-Mongrain E, Silberzan P, Hakim V. Collective cell motion in an epithelial sheet can be quantitatively described by a stochastic interacting particle model. PLoS Comput Biol. 2013 Mar;9(3):e1002944. Soumya SS, Gupta A, Cugno A, Deseri L, Dayal K, Das D, et al. Coherent motion of monolayer sheets under confinement and its pathological implications. PLoS Comput Biol. 2015;11(12):e1004670. Staple DB, Farhadifar R, Röper JC, Aigouy B, Eaton S, Jülicher F. Mechanics and remodelling of cell packings in epithelia. Eur Phys J E Soft Matter. 2010;33(2):117–27. Sussman DM. cellGPU: massively parallel simulations of dynamic vertex models. Comput Phys Commun. 2017;219:400–6. Tambe DT, Hardin CC, Angelini TE, Rajendran K, Park CY, Serra-Picamal X, et al. Collective cell guidance by cooperative intercellular forces. Nat Mater. 2011;10(6):469–75. Tetley RJ, Staddon MF, Heller D, Hoppe A, Banerjee S, Mao Y. Tissue fluidity promotes epithelial wound healing. Nat Phys. 2019;15(11):1195–203. Trepat X, Fredberg JJ. Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol. 2011;21(11):638–46. Trepat X, Sahai E. Mesoscale physical principles of collective cell organization. Nat Phys. 2018;14(7):671–82. Vedula SRK, Leong MC, Lai TL, Hersen P, Kabla AJ, Lim CT, et al. Emerging modes of collective cell migration induced by geometrical constraints. Proc Natl Acad Sci U S A. 2012;109(32):12974–9. Vishwakarma M, Di Russo J, Probst D, Schwarz US, Das T, Spatz JP. Mechanical interactions among followers determine the emergence of leaders in migrating epithelial cell collectives. Nat Commun. 2018;9(1):3469–12. Yabunaka S, Marcq P. Emergence of epithelial cell density waves. Soft Matter. 2017;13(39):7046–52. Zimmermann J, Camley BA, Rappel W-J, Levine H. Contact inhibition of locomotion determines cell–cell and cell–substrate forces in tissues. Proc Natl Acad Sci U S A. 2016;113(10):2660–5. Article / Publication Details

First-Page Preview

Abstract of Research Article

Received: June 05, 2022
Accepted: November 22, 2022
Published online: April 12, 2023

Number of Print Pages: 14
Number of Figures: 6
Number of Tables: 1

ISSN: 1422-6405 (Print)
eISSN: 1422-6421 (Online)

For additional information: https://www.karger.com/CTO

Copyright / Drug Dosage / Disclaimer Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

留言 (0)

沒有登入
gif