Biomechanical Feedback Strengthens Jammed Cellular Packings
Abstract
Growth in confined spaces can drive cellular populations through a jamming transition from a fluidlike state to a solidlike state. Experiments have found that jammed budding yeast populations can build up extreme compressive pressures (over 1 MPa), which in turn feed back onto cellular physiology by slowing or even stalling cell growth. Using numerical simulations, we investigate how this feedback impacts the mechanical properties of model jammed cell populations. In this work, we find that feedback directs growth toward poorly coordinated regions, resulting in an excess number of cell-cell contacts that rigidify cell packings. Cell packings possess anomalously large shear and bulk moduli that depend sensitively on the strength of feedback. These results demonstrate that mechanical feedback on the single-cell level is a simple mechanism by which living systems may tune their population-level mechanical properties.
- Authors:
-
- Univ. of California, Berkeley, CA (United States). Dept. of Physics and Integrative Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
- Sponsoring Org.:
- USDOE Office of Science (SC); Simons Foundation; National Science Foundation (NSF); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH)
- OSTI Identifier:
- 1527126
- Alternate Identifier(s):
- OSTI ID: 1515111
- Grant/Contract Number:
- AC02-05CH11231; 327934; 1555330; R01GM115851
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Physical Review Letters
- Additional Journal Information:
- Journal Volume: 122; Journal Issue: 20; Journal ID: ISSN 0031-9007
- Publisher:
- American Physical Society (APS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 75 CONDENSED MATTER PHYSICS, SUPERCONDUCTIVITY AND SUPERFLUIDITY
Citation Formats
Gniewek, Pawel, Schreck, Carl F., and Hallatschek, Oskar. Biomechanical Feedback Strengthens Jammed Cellular Packings. United States: N. p., 2019.
Web. doi:10.1103/PhysRevLett.122.208102.
Gniewek, Pawel, Schreck, Carl F., & Hallatschek, Oskar. Biomechanical Feedback Strengthens Jammed Cellular Packings. United States. https://doi.org/10.1103/PhysRevLett.122.208102
Gniewek, Pawel, Schreck, Carl F., and Hallatschek, Oskar. Wed .
"Biomechanical Feedback Strengthens Jammed Cellular Packings". United States. https://doi.org/10.1103/PhysRevLett.122.208102. https://www.osti.gov/servlets/purl/1527126.
@article{osti_1527126,
title = {Biomechanical Feedback Strengthens Jammed Cellular Packings},
author = {Gniewek, Pawel and Schreck, Carl F. and Hallatschek, Oskar},
abstractNote = {Growth in confined spaces can drive cellular populations through a jamming transition from a fluidlike state to a solidlike state. Experiments have found that jammed budding yeast populations can build up extreme compressive pressures (over 1 MPa), which in turn feed back onto cellular physiology by slowing or even stalling cell growth. Using numerical simulations, we investigate how this feedback impacts the mechanical properties of model jammed cell populations. In this work, we find that feedback directs growth toward poorly coordinated regions, resulting in an excess number of cell-cell contacts that rigidify cell packings. Cell packings possess anomalously large shear and bulk moduli that depend sensitively on the strength of feedback. These results demonstrate that mechanical feedback on the single-cell level is a simple mechanism by which living systems may tune their population-level mechanical properties.},
doi = {10.1103/PhysRevLett.122.208102},
journal = {Physical Review Letters},
number = 20,
volume = 122,
place = {United States},
year = {2019},
month = {5}
}
Works referenced in this record:
Random Packings of Frictionless Particles
journal, January 2002
- O'Hern, Corey S.; Langer, Stephen A.; Liu, Andrea J.
- Physical Review Letters, Vol. 88, Issue 7
A comparison of jamming behavior in systems composed of dimer- and ellipse-shaped particles
journal, January 2010
- Schreck, Carl F.; Xu, Ning; O'Hern, Corey S.
- Soft Matter, Vol. 6, Issue 13
Constraints and vibrations in static packings of ellipsoidal particles
journal, June 2012
- Schreck, Carl F.; Mailman, Mitch; Chakraborty, Bulbul
- Physical Review E, Vol. 85, Issue 6
Jamming at zero temperature and zero applied stress: The epitome of disorder
journal, July 2003
- O’Hern, Corey S.; Silbert, Leonardo E.; Liu, Andrea J.
- Physical Review E, Vol. 68, Issue 1
Active Vertex Model for cell-resolution description of epithelial tissue mechanics
journal, June 2017
- Barton, Daniel L.; Henkes, Silke; Weijer, Cornelis J.
- PLOS Computational Biology, Vol. 13, Issue 6
Biofilm Dispersal: Mechanisms, Clinical Implications, and Potential Therapeutic Uses
journal, February 2010
- Kaplan, J. B.
- Journal of Dental Research, Vol. 89, Issue 3
Vibrations and Diverging Length Scales Near the Unjamming Transition
journal, August 2005
- Silbert, Leonardo E.; Liu, Andrea J.; Nagel, Sidney R.
- Physical Review Letters, Vol. 95, Issue 9
Active jamming: Self-propelled soft particles at high density
journal, October 2011
- Henkes, Silke; Fily, Yaouen; Marchetti, M. Cristina
- Physical Review E, Vol. 84, Issue 4
Contact force measurements and stress-induced anisotropy in granular materials
journal, June 2005
- Majmudar, T. S.; Behringer, R. P.
- Nature, Vol. 435, Issue 7045
The Effects of Stochasticity at the Single-Cell Level and Cell Size Control on the Population Growth
journal, October 2017
- Lin, Jie; Amir, Ariel
- Cell Systems, Vol. 5, Issue 4
Random packings of spheres and spherocylinders simulated by mechanical contraction
journal, May 2003
- Williams, S. R.; Philipse, A. P.
- Physical Review E, Vol. 67, Issue 5
Geometric origin of excess low-frequency vibrational modes in weakly connected amorphous solids
journal, November 2005
- Wyart, M.; Nagel, S. R.; Witten, T. A.
- Europhysics Letters (EPL), Vol. 72, Issue 3
On the rigidity of amorphous solids
journal, January 2005
- Wyart, M.
- Annales de Physique, Vol. 30, Issue 3
Underconstrained jammed packings of nonspherical hard particles: Ellipses and ellipsoids
journal, May 2007
- Donev, Aleksandar; Connelly, Robert; Stillinger, Frank H.
- Physical Review E, Vol. 75, Issue 5
The statistical physics of active matter: From self-catalytic colloids to living cells
journal, August 2018
- Fodor, Étienne; Cristina Marchetti, M.
- Physica A: Statistical Mechanics and its Applications, Vol. 504
Amorphous solids: their structure, lattice dynamics and elasticity
journal, March 1998
- Alexander, Shlomo
- Physics Reports, Vol. 296, Issue 2-4
The Mechanics and Statistics of Active Matter
journal, August 2010
- Ramaswamy, Sriram
- Annual Review of Condensed Matter Physics, Vol. 1, Issue 1
Jamming in Systems Composed of Frictionless Ellipse-Shaped Particles
journal, June 2009
- Mailman, Mitch; Schreck, Carl F.; O’Hern, Corey S.
- Physical Review Letters, Vol. 102, Issue 25
Flocking transitions in confluent tissues
journal, January 2018
- Giavazzi, Fabio; Paoluzzi, Matteo; Macchi, Marta
- Soft Matter, Vol. 14, Issue 18
A density-independent rigidity transition in biological tissues
journal, September 2015
- Bi, Dapeng; Lopez, J. H.; Schwarz, J. M.
- Nature Physics, Vol. 11, Issue 12
Critical jamming of frictional grains in the generalized isostaticity picture
journal, April 2010
- Henkes, S.; van Hecke, M.; van Saarloos, W.
- EPL (Europhysics Letters), Vol. 90, Issue 1
Structural signatures of the unjamming transition at zero temperature
journal, April 2006
- Silbert, Leonardo E.; Liu, Andrea J.; Nagel, Sidney R.
- Physical Review E, Vol. 73, Issue 4
Hypostatic jammed packings of frictionless nonspherical particles
journal, January 2018
- VanderWerf, Kyle; Jin, Weiwei; Shattuck, Mark D.
- Physical Review E, Vol. 97, Issue 1
Force mobilization and generalized isostaticity in jammed packings of frictional grains
journal, January 2007
- Shundyak, Kostya; van Hecke, Martin; van Saarloos, Wim
- Physical Review E, Vol. 75, Issue 1
Protocol dependence of the jamming transition
journal, January 2016
- Bertrand, Thibault; Behringer, Robert P.; Chakraborty, Bulbul
- Physical Review E, Vol. 93, Issue 1
Motility-Driven Glass and Jamming Transitions in Biological Tissues
journal, April 2016
- Bi, Dapeng; Yang, Xingbo; Marchetti, M. Cristina
- Physical Review X, Vol. 6, Issue 2
Jamming by shear
journal, December 2011
- Bi, Dapeng; Zhang, Jie; Chakraborty, Bulbul
- Nature, Vol. 480, Issue 7377
Flexible Microfluidic Device for Mechanical Property Characterization of Soft Viscoelastic Solids Such as Bacterial Biofilms
journal, July 2009
- Hohne, Danial N.; Younger, John G.; Solomon, Michael J.
- Langmuir, Vol. 25, Issue 13
Nonlinear Rheology in a Model Biological Tissue
journal, April 2017
- Matoz-Fernandez, D. A.; Agoritsas, Elisabeth; Barrat, Jean-Louis
- Physical Review Letters, Vol. 118, Issue 15
Self-induced mechanical stress can trigger biofilm formation in uropathogenic Escherichia coli
journal, October 2018
- Chu, Eric K.; Kilic, Onur; Cho, Hojung
- Nature Communications, Vol. 9, Issue 1
Viscoelastic Properties of a Mixed Culture Biofilm from Rheometer Creep Analysis
journal, October 2003
- Towler, Brett W.; Rupp, Cory J.; Cunningham, Al B.
- Biofouling, Vol. 19, Issue 5
SCWISh network is essential for survival under mechanical pressure
journal, November 2017
- Delarue, Morgan; Poterewicz, Gregory; Hoxha, Ori
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 51
Sensitivity of Granular Force Chain Orientation to Disorder-Induced Metastable Relaxation
journal, March 2016
- Iikawa, N.; Bandi, M. M.; Katsuragi, H.
- Physical Review Letters, Vol. 116, Issue 12
Self-driven jamming in growing microbial populations
journal, May 2016
- Delarue, Morgan; Hartung, Jörn; Schreck, Carl
- Nature Physics, Vol. 12, Issue 8
Soft-Sphere Packings at Finite Pressure but Unstable to Shear
journal, August 2012
- Dagois-Bohy, Simon; Tighe, Brian P.; Simon, Johannes
- Physical Review Letters, Vol. 109, Issue 9
Critical Scaling of Shear Viscosity at the Jamming Transition
journal, October 2007
- Olsson, Peter; Teitel, S.
- Physical Review Letters, Vol. 99, Issue 17
Jamming is not just cool any more
journal, November 1998
- Liu, Andrea J.; Nagel, Sidney R.
- Nature, Vol. 396, Issue 6706
The effects of molecular noise and size control on variability in the budding yeast cell cycle
journal, August 2007
- Talia, Stefano Di; Skotheim, Jan M.; Bean, James M.
- Nature, Vol. 448, Issue 7156
Finite-Size Scaling at the Jamming Transition
journal, August 2012
- Goodrich, Carl P.; Liu, Andrea J.; Nagel, Sidney R.
- Physical Review Letters, Vol. 109, Issue 9
Cellular packing, mechanical stress and the evolution of multicellularity
journal, November 2017
- Jacobeen, Shane; Pentz, Jennifer T.; Graba, Elyes C.
- Nature Physics, Vol. 14, Issue 3
Fluidization of tissues by cell division and apoptosis
journal, November 2010
- Ranft, J.; Basan, M.; Elgeti, J.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 49
Geometry, packing, and evolutionary paths to increased multicellular size
journal, May 2018
- Jacobeen, Shane; Graba, Elyes C.; Brandys, Colin G.
- Physical Review E, Vol. 97, Issue 5
Critical Scaling in Linear Response of Frictionless Granular Packings near Jamming
journal, December 2006
- Ellenbroek, Wouter G.; Somfai, Ellák; van Hecke, Martin
- Physical Review Letters, Vol. 97, Issue 25
Jamming Transition as Probed by Quasistatic Shear Flow
journal, May 2009
- Heussinger, Claus; Barrat, Jean-Louis
- Physical Review Letters, Vol. 102, Issue 21