Abstract

The interruption of cellular interactions in biological processes such as migration, differentiation, proliferation, and wound healing could lead to conditions such as fibrosis, muscular dystrophy, brain tumors, and cancer. The role of microstructural and mechanical properties of the surrounding fibrous extracellular matrix has been highlighted in facilitating cellular communications and long-range transmission of displacements and stresses. However, the role of prestress, which is commonly seen in biological materials, is largely overlooked. The primary objective of the present study is to address this existing gap by investigating the influence of prestress on the displacement propagation caused by a local contractile domain inside discrete fibrous media. In this regard, we first generate 2D random fiber networks with an average network connectivity of less than the isostatic threshold. We create a prestressed state in these networks by applying both compressive/tensile uniaxial and biaxial deformation. Then, we numerically characterize prestress effects on the displacement propagation caused by the local contractile deformation. In comparison with displacement transmission in random fiber networks under tensile prestress, the numerical simulations show that the displacement propagation due to a local contraction is more pronounced in networks with compressive prestress. The numerical findings are discussed in terms of prestress effects on microstructural and mechanical properties of random fiber networks.

References

1.
Chaudhuri
,
O.
,
Cooper-White
,
J.
,
Janmey
,
P. A.
,
Mooney
,
D. J.
, and
Shenoy
,
V. B.
,
2020
, “
Effects of Extracellular Matrix Viscoelasticity on Cellular Behaviour
,”
Nature
,
584
(
7822
), pp.
535
546
.
2.
Loebel
,
C.
,
Mauck
,
R. L.
, and
Burdick
,
J. A.
,
2019
, “
Local Nascent Protein Deposition and Remodelling Guide Mesenchymal Stromal Cell Mechanosensing and Fate in Three-Dimensional Hydrogels
,”
Nat. Mater.
,
18
(
8
), pp.
883
891
.
3.
Schmidt
,
S.
, and
Friedl
,
P.
,
2010
, “
Interstitial Cell Migration: Integrin-Dependent and Alternative Adhesion Mechanisms
,”
Cell Tissue Res.
,
339
(
1
), pp.
83
92
.
4.
Madri
,
J. A.
, and
Pratt
,
B. M.
,
1986
, “
Endothelial Cell-Matrix Interactions: In Vitro Models of Angiogenesis
,”
J Histochem Cytochem.
,
34
(
1
), pp.
85
91
.
5.
Goody
,
M. F.
, and
Henry
,
C. A.
,
2010
, “
Dynamic Interactions Between Cells and Their Extracellular Matrix Mediate Embryonic Development
,”
Mol. Reprod. Dev.
,
77
(
6
), pp.
475
488
.
6.
Frisch
,
S.
, and
Francis
,
H.
,
1994
, “
Disruption of Epithelial Cell-Matrix Interactions Induces Apoptosis
,”
J. Cell Biol.
,
124
(
4
), pp.
619
626
.
7.
Hegedüs
,
B.
,
Marga
,
F.
,
Jakab
,
K.
,
Sharpe-Timms
,
K. L.
, and
Forgacs
,
G.
,
2006
, “
The Interplay of Cell-Cell and Cell-Matrix Interactions in the Invasive Properties of Brain Tumors
,”
Biophys. J.
,
91
(
7
), pp.
2708
2716
.
8.
Carmignac
,
V.
, and
Durbeej
,
M.
,
2012
, “
Cell-Matrix Interactions in Muscle Disease
,”
J. Pathol.
,
226
(
2
), pp.
200
218
.
9.
Koorman
,
T.
,
Jansen
,
K. A.
,
Khalil
,
A.
,
Haughton
,
P. D.
,
Visser
,
D.
,
Rätze
,
M. A. K.
,
Haakma
,
W. E.
, et al
,
2022
, “
Spatial Collagen Stiffening Promotes Collective Breast Cancer Cell Invasion by Reinforcing Extracellular Matrix Alignment
,”
Oncogene
,
41
(
17
), pp.
2458
2469
.
10.
Doyle
,
A. D.
,
Nazari
,
S. S.
, and
Yamada
,
K. M.
,
2022
, “
Cell-Extracellular Matrix Dynamics
,”
Phys. Biol.
,
19
(
2
), p.
021002
.
11.
Guo
,
C.-L.
,
Ouyang
,
M.
,
Yu
,
J.-Y.
,
Maslov
,
J.
,
Price
,
A.
, and
Shen
,
C.-Y.
,
2012
, “
Long-Range Mechanical Force Enables Self-Assembly of Epithelial Tubular Patterns
,”
PNAS
,
109
(
15
), pp.
5576
5582
.
12.
Pakshir
,
P.
,
Alizadehgiashi
,
M.
,
Wong
,
B.
,
Coelho
,
N. M.
,
Chen
,
X.
,
Gong
,
Z.
,
Shenoy
,
V. B.
,
McCulloch
,
C. A.
, and
Hinz
,
B.
,
2019
, “
Dynamic Fibroblast Contractions Attract Remote Macrophages in Fibrillar Collagen Matrix
,”
Nat. Commun.
,
10
(
1
), p.
1850
.
13.
Storm
,
C.
,
Pastore
,
J. J.
,
MacKintosh
,
F. C.
,
Lubensky
,
T. C.
, and
Janmey
,
P. A.
,
2005
, “
Nonlinear Elasticity in Biological Gels
,”
Nature
,
435
(
7039
), pp.
191
194
.
14.
Rens
,
R.
,
Vahabi
,
M.
,
Licup
,
A. J.
,
MacKintosh
,
F. C.
, and
Sharma
,
A.
,
2016
, “
Nonlinear Mechanics of Athermal Branched Biopolymer Networks
,”
J. Phys. Chem. B
,
120
(
26
), pp.
5831
5841
.
15.
Hatami-Marbini
,
H.
, and
Rohanifar
,
M.
,
2021
, “
Nonlinear Mechanical Properties of Prestressed Branched Fibrous Networks
,”
Biophys. J.
,
120
(
3
), pp.
527
538
.
16.
Fomovsky
,
G. M.
,
Thomopoulos
,
S.
, and
Holmes
,
J. W.
,
2010
, “
Contribution of Extracellular Matrix to the Mechanical Properties of the Heart
,”
J. Mol. Cell. Cardiol.
,
48
(
3
), pp.
490
496
.
17.
Destrade
,
M.
,
Liu
,
Y.
,
Murphy
,
J. G.
, and
Kassab
,
G. S.
,
2012
, “
Uniform Transmural Strain in Pre-Stressed Arteries Occurs at Physiological Pressure
,”
J. Theor. Biol.
,
303
, pp.
93
97
.
18.
Wang
,
P.
,
Zhang
,
Q.
,
Fang
,
X.
,
Lin
,
F.
, and
Huang
,
J.
,
2021
, “
Mechanical Regulation of Cell Volume in 3D Extracellular Matrices
,”
Extreme Mech. Lett.
,
49
, p.
101498
.
19.
Cavalcante
,
F. S. A.
,
Ito
,
S.
,
Brewer
,
K.
,
Sakai
,
H.
,
Alencar
,
A. M.
,
Almeida
,
M. P.
,
Andrade
,
J. S.
,
Majumdar
,
A.
,
Ingenito
,
E. P.
, and
Suki
,
B.
,
2005
, “
Mechanical Interactions Between Collagen and Proteoglycans: Implications for the Stability of Lung Tissue
,”
J. Appl. Physiol.
,
98
(
2
), pp.
672
679
.
20.
Knudsen
,
L.
, and
Ochs
,
M.
,
2018
, “
The Micromechanics of Lung Alveoli: Structure and Function of Surfactant and Tissue Components
,”
Histochem. Cell Biol.
,
150
(
6
), pp.
661
676
.
21.
Erlich
,
A.
,
Étienne
,
J.
,
Fouchard
,
J.
, and
Wyatt
,
T.
,
2022
, “
How Dynamic Prestress Governs the Shape of Living Systems, From the Subcellular to Tissue Scale
,”
Interface Focus
,
12
(
6
), p.
20220038
.
22.
Humphries
,
D. L.
,
Grogan
,
J. A.
, and
Gaffney
,
E. A.
,
2017
, “
Mechanical Cell–Cell Communication in Fibrous Networks: The Importance of Network Geometry
,”
Bull. Math. Biol.
,
79
(
3
), pp.
498
524
.
23.
Hatami-Marbini
,
H.
,
Etebu
,
E.
, and
Rahimi
,
A.
,
2013
, “
Swelling Pressure and Hydration Behavior of Porcine Corneal Stroma
,”
Curr. Eye Res.
,
38
(
11
), pp.
1124
1132
.
24.
Saraswathibhatla
,
A.
,
Indana
,
D.
, and
Chaudhuri
,
O.
,
2023
, “
Cell–Extracellular Matrix Mechanotransduction in 3D
,”
Nat. Rev. Mol. Cell Biol.
,
24
(
7
), pp.
495
516
.
25.
Hatami-Marbini
,
H.
, and
Rohanifar
,
M.
,
2021
, “
Mechanical Response of Composite Fiber Networks Subjected to Local Contractile Deformation
,”
Int. J. Solids Struct.
,
228
, p.
111045
.
26.
Sopher
,
R. S.
,
Goren
,
S.
,
Koren
,
Y.
,
Tchaicheeyan
,
O.
, and
Lesman
,
A.
,
2023
, “
Intercellular Mechanical Signalling in a 3D Nonlinear Fibrous Network Model
,”
Mech. Mater.
,
184
, p.
104739
.
27.
Liu
,
J.
,
Wang
,
M.
,
Xue
,
C.
,
Wang
,
H.
, and
Wang
,
H.
,
2024
, “
Ultra-Long-Range Force Transmission in Fiber Networks Enabled by Multiaxial Mechanical Coupling
,”
Int. J. Solids Struct.
,
291
, p.
112698
.
28.
Abhilash
,
A. S.
,
Baker
,
B. M.
,
Trappmann
,
B.
,
Chen
,
C. S.
, and
Shenoy
,
V. B.
,
2014
, “
Remodeling of Fibrous Extracellular Matrices by Contractile Cells: Predictions From Discrete Fiber Network Simulations
,”
Biophys. J.
,
107
(
8
), pp.
1829
1840
.
29.
Sopher
,
R. S.
,
Tokash
,
H.
,
Natan
,
S.
,
Sharabi
,
M.
,
Shelah
,
O.
,
Tchaicheeyan
,
O.
, and
Lesman
,
A.
,
2018
, “
Nonlinear Elasticity of the ECM Fibers Facilitates Efficient Intercellular Communication
,”
Biophys. J.
,
115
(
7
), pp.
1357
1370
.
30.
Notbohm
,
J.
,
Lesman
,
A.
,
Rosakis
,
P.
,
Tirrell
,
D. A.
, and
Ravichandran
,
G.
,
2015
, “
Microbuckling of Fibrin Provides a Mechanism for Cell Mechanosensing
,”
J. R. Soc. Interface
,
12
(
108
), p.
20150320
.
31.
Licup
,
A. J.
,
Münster
,
S.
,
Sharma
,
A.
,
Sheinman
,
M.
,
Jawerth
,
L. M.
,
Fabry
,
B.
,
Weitz
,
D. A.
, and
MacKintosh
,
F. C.
,
2015
, “
Stress Controls the Mechanics of Collagen Networks
,”
Proc. Natl. Acad. Sci. U. S. A.
,
112
(
31
), pp.
9573
9578
.
32.
Hatami-Marbini
,
H.
, and
Picu
,
R.
,
2008
, “
Scaling of Nonaffine Deformation in Random Semiflexible Fiber Networks
,”
Phys. Rev. E
,
77
(
6
), p.
062103
.
33.
Vahabi
,
M.
,
Sharma
,
A.
,
Licup
,
A. J.
,
Oosten
,
A. S. G.
,
Galie
,
P. A.
,
Janmey
,
P. A.
, and
MacKintosh
,
F. C.
,
2016
, “
Elasticity of Fibrous Networks Under Uniaxial Prestress
,”
Soft Matter
,
12
(
22
), pp.
5050
5060
.
34.
Steinwachs
,
J.
,
Metzner
,
C.
,
Skodzek
,
K.
,
Lang
,
N.
,
Thievessen
,
I.
,
Mark
,
C.
,
Münster
,
S.
,
Aifantis
,
K. E.
, and
Fabry
,
B.
,
2016
, “
Three-Dimensional Force Microscopy of Cells in Biopolymer Networks
,”
Nat. Methods
,
13
(
2
), pp.
171
176
.
35.
Hatami-Marbini
,
H.
, and
Rohanifar
,
M.
,
2020
, “
Mechanical Properties of Subisostatic Random Networks Composed of Nonlinear Fibers
,”
Soft Matter
,
16
(
30
), pp.
7156
7164
.
36.
Goren
,
S.
,
Koren
,
Y.
,
Xu
,
X.
, and
Lesman
,
A.
,
2020
, “
Elastic Anisotropy Governs the Range of Cell-Induced Displacements
,”
Biophys. J.
,
118
(
5
), pp.
1152
1164
.
37.
Shahsavari
,
A. S.
, and
Picu
,
R. C.
,
2013
, “
Size Effect on Mechanical Behavior of Random Fiber Networks
,”
Int. J. Solids Struct.
,
50
(
20
), pp.
3332
3338
.
38.
Rosakis
,
P.
,
Notbohm
,
J.
, and
Ravichandran
,
G.
,
2015
, “
A Model for Compression-Weakening Materials and the Elastic Fields due to Contractile Cells
,”
J. Mech. Phys. Solids
,
85
, pp.
16
32
.
39.
Mann
,
A.
,
Sopher
,
R. S.
,
Goren
,
S.
,
Shelah
,
O.
,
Tchaicheeyan
,
O.
, and
Lesman
,
A.
,
2019
, “
Force Chains in Cell–Cell Mechanical Communication
,”
J. R. Soc. Interface
,
16
(
159
), p.
20190348
.
40.
Grimmer
,
P.
, and
Notbohm
,
J.
,
2018
, “
Displacement Propagation in Fibrous Networks Due to Local Contraction
,”
ASME J. Biomech. Eng.
,
140
(
4
), p.
041011
.
41.
Hatami-Marbini
,
H.
,
2016
, “
Nonaffine Behavior of Three-Dimensional Semiflexible Polymer Networks
,”
Phys. Rev. E
,
93
(
4
), p.
042503
.
42.
Hatami-Marbini
,
H.
,
2018
, “
Simulation of the Mechanical Behavior of Random Fiber Networks With Different Microstructure
,”
Eur. Phys. J. E
,
41
(
5
), p.
65
.
43.
Hatami-Marbini
,
H.
, and
Rohanifar
,
M.
,
2019
, “
Stiffness of bi-Modulus Hexagonal and Diamond Honeycombs
,”
J. Mech. Sci. Technol.
,
33
(
4
), pp.
1703
1709
.
You do not currently have access to this content.