Abstract

Cells sense biophysical cues in the micro-environment and respond to the cues biochemically and biophysically. Proper responses from cells are critical to maintain the homeostasis in the body. Abnormal biophysical cues will cause pathological development in the cells; pathological or aging cells, on the other hand, can alter their micro-environment to become abnormal. In this minireview, we discuss four important biophysical cues of the micro-environment—stiffness, curvature, extracellular matrix (ECM) architecture and viscosity—in terms of their roles in health, aging, and diseases.

References

1.
Leight
,
J. L.
,
Drain
,
A. P.
, and
Weaver
,
V. M.
,
2017
, “
Extracellular Matrix Remodeling and Stiffening Modulate Tumor Phenotype and Treatment Response
,”
Annu. Rev. Cancer Biol.
,
1
(
1
), pp.
313
334
.10.1146/annurev-cancerbio-050216-034431
2.
Ng
,
M. R.
, and
Brugge
,
J. S.
,
2009
, “
A Stiff Blow From the Stroma: Collagen Crosslinking Drives Tumor Progression
,”
Cancer Cell
,
16
(
6
), pp.
455
457
.10.1016/j.ccr.2009.11.013
3.
Netti
,
P. A.
,
Roberge
,
S.
,
Boucher
,
Y.
,
Baxter
,
L. T.
, and
Jain
,
R. K.
,
1996
, “
Effect of Transvascular Fluid Exchange on Pressure-Flow Relationship in Tumors: A Proposed Mechanism for Tumor Blood Flow Heterogeneity
,”
Microvasc. Res.
,
52
(
1
), pp.
27
46
.10.1006/mvre.1996.0041
4.
Jain
,
R. K.
,
Martin
,
J. D.
, and
Stylianopoulos
,
T.
,
2014
, “
The Role of Mechanical Forces in Tumor Growth and Therapy
,”
Annu. Rev. Biomed. Eng.
,
16
(
1
), pp.
321
346
.10.1146/annurev-bioeng-071813-105259
5.
Taufalele
,
P. V.
,
VanderBurgh
,
J. A.
,
Muñoz
,
A.
,
Zanotelli
,
M. R.
, and
Reinhart-King
,
C. A.
,
2019
, “
Fiber Alignment Drives Changes in Architectural and Mechanical Features in Collagen Matrices
,”
PLoS One
,
14
(
5
), p.
e0216537
.10.1371/journal.pone.0216537
6.
Goetz
,
J. G.
,
Minguet
,
S.
,
Navarro-Lérida
,
I.
,
Lazcano
,
J. J.
,
Samaniego
,
R.
,
Calvo
,
E.
,
Tello
,
M.
,
Osteso-Ibáñez
,
T.
,
Pellinen
,
T.
,
Echarri
,
A.
,
Cerezo
,
A.
,
Klein-Szanto
,
A. J. P.
,
Garcia
,
R.
,
Keely
,
P. J.
,
Sánchez-Mateos
,
P.
,
Cukierman
,
E.
, and
Del Pozo
,
M. A.
,
2011
, “
Biomechanical Remodeling of the Microenvironment by Stromal Caveolin-1 Favors Tumor Invasion and Metastasis
,”
Cell
,
146
(
1
), pp.
148
163
.10.1016/j.cell.2011.05.040
7.
Erdogan
,
B.
,
Ao
,
M.
,
White
,
L. M.
,
Means
,
A. L.
,
Brewer
,
B. M.
,
Yang
,
L.
,
Washington
,
M. K.
,
Shi
,
C.
,
Franco
,
O. E.
,
Weaver
,
A. M.
,
Hayward
,
S. W.
,
Li
,
D.
, and
Webb
,
D. J.
,
2017
, “
Cancer-Associated Fibroblasts Promote Directional Cancer Cell Migration by Aligning Fibronectin
,”
J. Cell Biol.
,
216
(
11
), pp.
3799
3816
.10.1083/jcb.201704053
8.
Lee
,
J.
,
Nishikawa
,
R. M.
,
Reiser
,
I.
,
Boone
,
J. M.
, and
Lindfors
,
K. K.
,
2015
, “
Local Curvature Analysis for Classifying Breast Tumors: Preliminary Analysis in Dedicated Breast CT
,”
Med. Phys.
,
42
(
9
), pp.
5479
5489
.10.1118/1.4928479
9.
Handorf
,
A. M.
,
Zhou
,
Y.
,
Halanski
,
M. A.
, and
Li
,
W.-J.
,
2015
, “
Tissue Stiffness Dictates Development, Homeostasis, and Disease Progression
,”
Organogenesis
,
11
(
1
), pp.
1
15
.10.1080/15476278.2015.1019687
10.
Baiocchini
,
A.
,
Montaldo
,
C.
,
Conigliaro
,
A.
,
Grimaldi
,
A.
,
Correani
,
V.
,
Mura
,
F.
,
Ciccosanti
,
F.
,
Rotiroti
,
N.
,
Brenna
,
A.
,
Montalbano
,
M.
,
D'Offizi
,
G.
,
Capobianchi
,
M. R.
,
Alessandro
,
R.
,
Piacentini
,
M.
,
Schininà
,
M. E.
,
Maras
,
B.
,
Del Nonno
,
F.
,
Tripodi
,
M.
, and
Mancone
,
C.
,
2016
, “
Extracellular Matrix Molecular Remodeling in Human Liver Fibrosis Evolution
,”
PLoS One
,
11
(
3
), p.
e0151736
.10.1371/journal.pone.0151736
11.
Levental
,
K. R.
,
Yu
,
H.
,
Kass
,
L.
,
Lakins
,
J. N.
,
Egeblad
,
M.
,
Erler
,
J. T.
,
Fong
,
S. F. T.
,
Csiszar
,
K.
,
Giaccia
,
A.
,
Weninger
,
W.
,
Yamauchi
,
M.
,
Gasser
,
D. L.
, and
Weaver
,
V. M.
,
2009
, “
Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling
,”
Cell
,
139
(
5
), pp.
891
906
.10.1016/j.cell.2009.10.027
12.
Chen
,
G.
,
Xia
,
B.
,
Fu
,
Q.
,
Huang
,
X.
,
Wang
,
F.
,
Chen
,
Z.
, and
Lv
,
Y.
,
2019
, “
Matrix Mechanics as Regulatory Factors and Therapeutic Targets in Hepatic Fibrosis
,”
Int. J. Biol. Sci.
,
15
(
12
), pp.
2509
2521
.10.7150/ijbs.37500
13.
Jung
,
W.-H.
,
Elawad
,
K.
,
Kang
,
S. H.
, and
Chen
,
Y.
,
2019
, “
Cell–Cell Adhesion and Myosin Activity Regulate Cortical Actin Assembly in Mammary Gland Epithelium on Concaved Surface
,”
Cells
,
8
(
8
), p.
813
.10.3390/cells8080813
14.
Tilbury
,
K.
,
Hocker
,
J.
,
Wen
,
B. L.
,
Sandbo
,
N.
,
Singh
,
V.
, and
Campagnola
,
P. J.
,
2014
, “
Second Harmonic Generation Microscopy Analysis of Extracellular Matrix Changes in Human Idiopathic Pulmonary Fibrosis
,”
J. Biomed. Opt.
,
19
(
8
), p.
086014
.10.1117/1.JBO.19.8.086014
15.
Sicard
,
D.
,
Fredenburgh
,
L. E.
, and
Tschumperlin
,
D. J.
,
2017
, “
Measured Pulmonary Arterial Tissue Stiffness is Highly Sensitive to AFM Indenter Dimensions
,”
J. Mech. Behav. Biomed. Mater
,
2017
, pp.
118
127
.10.1016/j.jmbbm.2017.05.039
16.
Engler
,
A. J.
,
Griffin
,
M. A.
,
Sen
,
S.
,
Bönnemann
,
C. G.
,
Sweeney
,
H. L.
, and
Discher
,
D. E.
,
2004
, “
Myotubes Differentiate Optimally on Substrates With Tissue-Like Stiffness: Pathological Implications for Soft or Stiff Microenvironments
,”
J. Cell Biol.
,
166
(
6
), pp.
877
887
.10.1083/jcb.200405004
17.
Jaiswal
,
D.
,
Cowley
,
N.
,
Bian
,
Z.
,
Zheng
,
G.
,
Claffey
,
K. P.
, and
Hoshino
,
K.
,
2017
, “
Stiffness Analysis of 3D Spheroids Using Microtweezers
,”
PLoS One
,
12
(
11
), p.
e0188346
.10.1371/journal.pone.0188346
18.
Park
,
S.
,
Lui
,
C.
,
Jung
,
W. H.
,
Maity
,
D.
,
Ong
,
C. S.
,
Bush
,
J.
,
Maruthamuthu
,
V.
,
Hibino
,
N.
, and
Chen
,
Y.
,
2018
, “
Mechanical Characterization of HiPSC-Derived Cardiac Tissues for Quality Control
,”
Adv. Biosyst.
,
2
(
12
), p.
1800251
.10.1002/adbi.201800251
19.
Ueki
,
Y.
,
Sakamoto
,
N.
, and
Sato
,
M.
,
2010
, “
Direct Measurement of Shear Strain in Adherent Vascular Endothelial Cells Exposed to Fluid Shear Stress
,”
Biochem. Biophys. Res. Commun.
,
394
(
1
), pp.
94
99
.10.1016/j.bbrc.2010.02.115
20.
Park
,
S.
,
Joo
,
Y. K.
, and
Chen
,
Y.
,
2019
, “
Versatile and High-Throughput Force Measurement Platform for Dorsal Cell Mechanics
,”
Sci. Rep.
,
9
, p.
13286
.10.1038/s41598-019-49592-1
21.
McKee
,
C. T.
,
Last
,
J. A.
,
Russell
,
P.
, and
Murphy
,
C. J.
,
2011
, “
Indentation Versus Tensile Measurements of Young's Modulus for Soft Biological Tissues
,”
Tissue Eng. Part B Rev.
,
17
(
3
), pp.
155
164
.10.1089/ten.teb.2010.0520
22.
Park
,
S.
,
Tao
,
J.
,
Sun
,
L.
,
Fan
,
C.-M.
, and
Chen
,
Y.
,
2019
, “
An Economic, Modular, and Portable Skin Viscoelasticity Measurement Device for In Situ Longitudinal Studies
,”
Molecules
,
24
(
5
), p.
907
.10.3390/molecules24050907
23.
Klatt
,
D.
,
Hamhaber
,
U.
,
Asbach
,
P.
,
Braun
,
J.
, and
Sack
,
I.
,
2007
, “
Noninvasive Assessment of the Rheological Behavior of Human Organs Using Multifrequency MR Elastography: A Study of Brain and Liver Viscoelasticity
,”
Phys. Med. Biol.
,
52
(
24
), pp.
7281
7294
.10.1088/0031-9155/52/24/006
24.
Park
,
S.
, and
Chen
,
Y.
,
2019
,
Mechanics of Biological Systems
,
Morgan & Claypool Publishers
, Williston, ND.
25.
Rubenstein
,
D.
,
Yin
,
W.
, and
Frame
,
M. D.
,
2012
,
Biofluid Mechanics
,
Elsevier
, Amsterdam, The Netherlands.
26.
Quemada
,
D.
,
1993
, “
A Non-Linear Maxwell Model of Biofluids: Application to Normal Blood
,”
Biorheology
,
30
(
3–4
), pp.
253
265
.10.3233/BIR-1993-303-410
27.
Gupta
,
S.
,
Wang
,
W. S.
, and
Vanapalli
,
S. A.
,
2016
, “
Microfluidic Viscometers for Shear Rheology of Complex Fluids and Biofluids
,”
Biomicrofluidics
,
10
(
4
), p.
043402
.10.1063/1.4955123
28.
Statsenko
,
A.
,
Inami
,
W.
, and
Kawata
,
Y.
,
2017
, “
Measurement of Viscosity of Liquids Using Optical Tweezers
,”
Opt. Commun.
,
402
, pp.
9
13
.10.1016/j.optcom.2017.05.034
29.
Tassieri
,
M.
,
Del Giudice
,
F.
,
Robertson
,
E. J.
,
Jain
,
N.
,
Fries
,
B.
,
Wilson
,
R.
,
Glidle
,
A.
,
Greco
,
F.
,
Netti
,
P. A.
,
Maffettone
,
P. L.
,
Bicanic
,
T.
, and
Cooper
,
J. M.
,
2015
, “
Microrheology With Optical Tweezers: Measuring the Relative Viscosity of Solutions ‘at a Glance
,”
Sci. Rep.
,
5
(
1
), p.
8831
.10.1038/srep08831
30.
Zhang
,
Y.
,
Wu
,
X.
,
Wang
,
Y.
,
Zhu
,
S.
,
Gao
,
B. Z.
, and
Yuan
,
X. C.
,
2014
, “
Measurement of the Microscopic Viscosities of Microfluids With a Dynamic Optical Tweezers System
,”
Laser Phys.
,
24
(
6
), p.
065601
.10.1088/1054-660X/24/6/065601
31.
Rich
,
J. P.
,
Lammerding
,
J.
,
McKinley
,
G. H.
, and
Doyle
,
P. S.
,
2011
, “
Nonlinear Microrheology of an Aging, Yield Stress Fluid Using Magnetic Tweezers
,”
Soft Matter
,
7
(
21
), pp.
9933
9943
.10.1039/c1sm05843f
32.
Gosse
,
C.
, and
Croquette
,
V.
,
2002
, “
Magnetic Tweezers: Micromanipulation and Force Measurement at the Molecular Level
,”
Biophys. J.
,
82
(
6
), pp.
3314
3329
.10.1016/S0006-3495(02)75672-5
33.
Fereidouni
,
F.
,
Todd
,
A.
,
Li
,
Y.
,
Chang
,
C.-W.
,
Luong
,
K.
,
Rosenberg
,
A.
,
Lee
,
Y.-J.
,
Chan
,
J. W.
,
Borowsky
,
A.
,
Matsukuma
,
K.
,
Jen
,
K.-Y.
, and
Levenson
,
R.
,
2019
, “
Dual-Mode Emission and Transmission Microscopy for Virtual Histochemistry Using Hematoxylin- and Eosin-Stained Tissue Sections
,”
Biomed. Opt. Express
,
10
(
12
), p.
6516
.10.1364/BOE.10.006516
34.
Leonard
,
A. K.
,
Loughran
,
E. A.
,
Klymenko
,
Y.
,
Liu
,
Y.
,
Kim
,
O.
,
Asem
,
M.
,
McAbee
,
K.
,
Ravosa
,
M. J.
, and
Stack
,
M. S.
,
2018
, “
Methods for the Visualization and Analysis of Extracellular Matrix Protein Structure and Degradation
,”
Methods Cell Biol.
,
143
, pp.
79
95
.10.1016/bs.mcb.2017.08.005
35.
Vader
,
D.
,
Kabla
,
A.
,
Weitz
,
D.
, and
Mahadevan
,
L.
,
2009
, “
Strain-Induced Alignment in Collagen Gels
,”
PLoS One
,
4
(
6
), p.
e5902
.10.1371/journal.pone.0005902
36.
Guilbert
,
M.
,
Roig
,
B.
,
Terryn
,
C.
,
Garnotel
,
R.
,
Jeannesson
,
P.
,
Sockalingum
,
G. D.
,
Manfait
,
M.
,
Perraut
,
F.
,
Dinten
,
J. M.
,
Koenig
,
A.
, and
Piot
,
O.
,
2016
, “
Highlighting the Impact of Aging on Type I Collagen: Label-Free Investigation Using Confocal Reflectance Microscopy and Diffuse Reflectance Spectroscopy in 3D Matrix Model
,”
Oncotarget
,
7
(
8
), pp.
8546
8555
.10.18632/oncotarget.7385
37.
Jung
,
W. H.
,
Yam
,
N.
,
Chen
,
C. C.
,
Elawad
,
K.
,
Hu
,
B.
, and
Chen
,
Y.
,
2020
, “
Force-Dependent Extracellular Matrix Remodeling by Early-Stage Cancer Cells Alters Diffusion and Induces Carcinoma-Associated Fibroblasts
,”
Biomaterials
,
234
, p.
119756
.10.1016/j.biomaterials.2020.119756
38.
Chen
,
X.
,
Nadiarynkh
,
O.
,
Plotnikov
,
S.
, and
Campagnola
,
P. J.
,
2012
, “
Second Harmonic Generation Microscopy for Quantitative Analysis of Collagen Fibrillar Structure
,”
Nat. Protoc.
,
7
(
4
), pp.
654
669
.10.1038/nprot.2012.009
39.
Raub
,
C. B.
,
Putnam
,
A. J.
,
Tromberg
,
B. J.
, and
George
,
S. C.
,
2010
, “
Predicting Bulk Mechanical Properties of Cellularized Collagen Gels Using Multiphoton Microscopy
,”
Acta Biomater.
,
6
(
12
), pp.
4657
4665
.10.1016/j.actbio.2010.07.004
40.
Provenzano
,
P. P.
,
Eliceiri
,
K. W.
,
Campbell
,
J. M.
,
Inman
,
D. R.
,
White
,
J. G.
, and
Keely
,
P. J.
,
2006
, “
Collagen Reorganization at the Tumor-Stromal Interface Facilitates Local Invasion
,”
BMC Med.
,
4
(
1
), p.
38
.10.1186/1741-7015-4-38
41.
Dempsey
,
W. P.
,
Fraser
,
S. E.
, and
Pantazis
,
P.
,
2012
, “
SHG Nanoprobes: Advancing Harmonic Imaging in Biology
,”
Bioessays
,
34
(
5
), pp.
351
360
.10.1002/bies.201100106
42.
Gjorevski
,
N.
, and
Nelson
,
C. M.
,
2012
, “
Mapping of Mechanical Strains and Stresses Around Quiescent Engineered Three-Dimensional Epithelial Tissues
,”
Biophys. J.
,
103
(
1
), pp.
152
162
.10.1016/j.bpj.2012.05.048
43.
Tarle
,
V.
,
Ravasio
,
A.
,
Hakim
,
V.
, and
Gov
,
N. S.
,
2015
, “
Modeling the Finger Instability in an Expanding Cell Monolayer
,”
Integr. Biol.
,
7
(
10
), pp.
1218
1227
.10.1039/C5IB00092K
44.
Xi
,
W.
,
Sonam
,
S.
,
Beng Saw
,
T.
,
Ladoux
,
B.
, and
Teck Lim
,
C.
,
2017
, “
Emergent Patterns of Collective Cell Migration Under Tubular Confinement
,”
Nat. Commun.
,
8
(
1
), p.
1517
.10.1038/s41467-017-01390-x
45.
Charrier
,
E. E.
,
Pogoda
,
K.
,
Wells
,
R. G.
, and
Janmey
,
P. A.
,
2018
, “
Control of Cell Morphology and Differentiation by Substrates With Independently Tunable Elasticity and Viscous Dissipation
,”
Nat. Commun.
,
9
(
1
), p.
449
.10.1038/s41467-018-02906-9
46.
Chaudhuri
,
O.
,
Gu
,
L.
,
Klumpers
,
D.
,
Darnell
,
M.
,
Bencherif
,
S. A.
,
Weaver
,
J. C.
,
Huebsch
,
N.
,
Lee
,
H.-P.
,
Lippens
,
E.
,
Duda
,
G. N.
, and
Mooney
,
D. J.
,
2016
, “
Hydrogels With Tunable Stress Relaxation Regulate Stem Cell Fate and Activity
,”
Nat. Mater.
,
15
(
3
), pp.
326
–3
34
.10.1038/nmat4489
47.
Gong
,
Z.
,
Szczesny
,
S. E.
,
Caliari
,
S. R.
,
Charrier
,
E. E.
,
Chaudhuri
,
O.
,
Cao
,
X.
,
Lin
,
Y.
,
Mauck
,
R. L.
,
Janmey
,
P. A.
,
Burdick
,
J. A.
, and
Shenoy
,
V. B.
,
2018
, “
Matching Material and Cellular Timescales Maximizes Cell Spreading on Viscoelastic Substrates
,”
Proc. Natl. Acad. Sci. U. S. A.
,
115
(
12
), pp.
E2686
E2695
.10.1073/pnas.1716620115
48.
Hall
,
M. S.
,
Alisafaei
,
F.
,
Ban
,
E.
,
Feng
,
X.
,
Hui
,
C. Y.
,
Shenoy
,
V. B.
, and
Wu
,
M.
,
2016
, “
Fibrous Nonlinear Elasticity Enables Positive Mechanical Feedback Between Cells and ECMs
,”
Proc. Natl. Acad. Sci. U. S. A.
,
113
(
49
), p.
201613058
.10.1073/pnas.1613058113
49.
Emon
,
B.
,
Bauer
,
J.
,
Jain
,
Y.
,
Jung
,
B.
, and
Saif
,
T.
,
2018
, “
Biophysics of Tumor Microenvironment and Cancer Metastasis—A Mini Review
,”
Comput. Struct. Biotechnol. J.
,
16
, pp.
279
287
.10.1016/j.csbj.2018.07.003
50.
Liu
,
Z.
,
Lee
,
S. J.
,
Park
,
S.
,
Konstantopoulos
,
K.
,
Glunde
,
K.
,
Chen
,
Y.
, and
Barman
,
I.
,
2020
, “
Cancer Cells Display Increased Migration and Deformability in Pace With Metastatic Progression
,”
Faseb J.
,
34
(
7
), pp.
9307
9315
. 10.1096/fj.202000101RR
51.
Buchsbaum
,
R. J.
, and
Oh
,
S. Y.
,
2016
, “
Breast Cancer-Associated Fibroblasts: Where We Are and Where We Need to Go
,”
Cancers (Basel
),
8
(
2
), p.
19
.10.3390/cancers8020019
52.
Gascard
,
P.
, and
Tlsty
,
T. D.
,
2016
, “
Carcinoma-Associated Fibroblasts: Orchestrating the Composition of Malignancy
,”
Genes Dev.
,
30
(
9
), pp.
1002
1019
.10.1101/gad.279737.116
53.
Grasset
,
E. M.
,
Bertero
,
T.
,
Bozec
,
A.
,
Friard
,
J.
,
Bourget
,
I.
,
Pisano
,
S.
,
Lecacheur
,
M.
,
Maiel
,
M.
,
Bailleux
,
C.
,
Emelyanov
,
A.
,
Ilie
,
M.
,
Hofman
,
P.
,
Meneguzzi
,
G.
,
Duranton
,
C.
,
Bulavin
,
D. V.
, and
Gaggioli
,
C.
,
2018
, “
Matrix Stiffening and EGFR Cooperate to Promote the Collective Invasion of Cancer Cells
,”
Cancer Res.
,
78
(
18
), pp.
5229
5242
.10.1158/0008-5472.CAN-18-0601
54.
Jung
,
W.-H.
,
Yam
,
N.
,
Chen
,
C.-C.
,
Elawad
,
K.
,
Hu
,
B.
, and
Chen
,
Y.
,
2020
, “
Force-Dependent Extracellular Matrix Remodeling by Early-Stage Cancer Cells Alters Diffusion and Induces Carcinoma-Associated Fibroblasts
,”
Biomaterials
,
234
, p.
119756
.
55.
Park
,
S.
,
Shi
,
Y.
,
Kim
,
B. C.
,
Jo
,
M. H.
,
Cruz
,
L. O.
,
Gou
,
Z.
,
Ha
,
T.
,
Lu
,
L.-F.
,
Reich
,
D. H.
, and
Chen
,
Y.
,
2020
, “
Force-Dependent Trans-Endocytosis by Breast Cancer Cells Depletes Costimulatory Receptor CD80 and Attenuates T Cell Activation
,”
Biosens. Bioelectron.
,
165
, p.
112389
.10.1016/j.bios.2020.112389
56.
Hadden
,
W. J.
,
Young
,
J. L.
,
Holle
,
A. W.
,
McFetridge
,
M. L.
,
Kim
,
D. Y.
,
Wijesinghe
,
P.
,
Taylor-Weiner
,
H.
,
Wen
,
J. H.
,
Lee
,
A. R.
,
Bieback
,
K.
,
Vo
,
B. N.
,
Sampson
,
D. D.
,
Kennedy
,
B. F.
,
Spatz
,
J. P.
,
Engler
,
A. J.
, and
Cho
,
Y. S.
,
2017
, “
Stem Cell Migration and Mechanotransduction on Linear Stiffness Gradient Hydrogels
,”
Proc. Natl. Acad. Sci. U. S. A.
,
114
(
22
), pp.
5647
5652
.10.1073/pnas.1618239114
57.
González-Cruz
,
R. D.
,
Fonseca
,
V. C.
, and
Darling
,
E. M.
,
2012
, “
Cellular Mechanical Properties Reflect the Differentiation Potential of Adipose-Derived Mesenchymal Stem Cells
,”
Proc. Natl. Acad. Sci. U. S. A.
,
109
(
24
), p.
E1523
.10.1073/pnas.1120349109
58.
Dobrokhotov
,
O.
,
Samsonov
,
M.
,
Sokabe
,
M.
, and
Hirata
,
H.
,
2018
, “
Mechanoregulation and Pathology of Yap/TAZ Via Hippo and Non-Hippo Mechanisms
,”
Clin. Transl. Med.
,
7
(
1
), p. 23.10.1186/s40169-018-0202-9
59.
McEvoy
,
E.
,
Deshpande
,
V. S.
, and
McGarry
,
P.
,
2017
, “
Free Energy Analysis of Cell Spreading
,”
J. Mech. Behav. Biomed. Mater.
,
74
, pp.
283
295
.10.1016/j.jmbbm.2017.06.006
60.
McEvoy
,
E.
,
Shishvan
,
S. S.
,
Deshpande
,
V. S.
, and
McGarry
,
J. P.
,
2018
, “
Thermodynamic Modeling of the Statistics of Cell Spreading on Ligand-Coated Elastic Substrates
,”
Biophys. J.
, 115(12), pp.
2451
2460
.10.1016/j.bpj.2018.11.007
61.
Park
,
S.
,
Seawright
,
A.
,
Park
,
S.
,
Craig Dutton
,
J.
,
Grinnell
,
F.
, and
Han
,
B.
,
2015
, “
Preservation of Tissue Microstructure and Functionality During Freezing by Modulation of Cytoskeletal Structure
,”
J. Mech. Behav. Biomed. Mater.
,
45
, pp.
32
44
.10.1016/j.jmbbm.2015.01.014
62.
Wells
,
R. G.
,
2008
, “
The Role of Matrix Stiffness in Regulating Cell Behavior
,”
Hepatology
,
47
(
4
), pp.
1394
1400
.10.1002/hep.22193
63.
Engler
,
A. J.
,
Sen
,
S.
,
Sweeney
,
H. L.
, and
Discher
,
D. E.
,
2006
, “
Matrix Elasticity Directs Stem Cell Lineage Specification
,”
Cell
,
126
(
4
), pp.
677
89
.10.1016/j.cell.2006.06.044
64.
Lv
,
H.
,
Li
,
L.
,
Sun
,
M.
,
Zhang
,
Y.
,
Chen
,
L.
,
Rong
,
Y.
, and
Li
,
Y.
,
2015
, “
Mechanism of Regulation of Stem Cell Differentiation by Matrix Stiffness
,”
Stem Cell Res. Ther.
, 6(1), p.
103
.10.1186/s13287-015-0083-4
65.
Bangasser
,
B. L.
,
Shamsan
,
G. A.
,
Chan
,
C. E.
,
Opoku
,
K. N.
,
Tüzel
,
E.
,
Schlichtmann
,
B. W.
,
Kasim
,
J. A.
,
Fuller
,
B. J.
,
McCullough
,
B. R.
,
Rosenfeld
,
S. S.
, and
Odde
,
D. J.
,
2017
, “
Shifting the Optimal Stiffness for Cell Migration
,”
Nat. Commun.
, 8, p.
15313
.10.1038/ncomms15313
66.
Gkretsi
,
V.
, and
Stylianopoulos
,
T.
,
2018
, “
Cell Adhesion and Matrix Stiffness: Coordinating Cancer Cell Invasion and Metastasis
,”
Front. Oncol.
,
8
, p. 145.10.3389/fonc.2018.00145
67.
Lange
,
J. R.
, and
Fabry
,
B.
,
2013
, “
Cell and Tissue Mechanics in Cell Migration
,”
Exp. Cell Res.
, 319(16), pp.
2418
2423
.10.1016/j.yexcr.2013.04.023
68.
Dong
,
Y.
,
Zheng
,
Q.
,
Wang
,
Z.
,
Lin
,
X.
,
You
,
Y.
,
Wu
,
S.
,
Wang
,
Y.
,
Hu
,
C.
,
Xie
,
X.
,
Chen
,
J.
,
Gao
,
D.
,
Zhao
,
Y.
,
Wu
,
W.
,
Liu
,
Y.
,
Ren
,
Z.
,
Chen
,
R.
, and
Cui
,
J.
,
2019
, “
Higher Matrix Stiffness as an Independent Initiator Triggers Epithelial-Mesenchymal Transition and Facilitates HCC Metastasis
,”
J. Hematol. Oncol.,
12, p.
112
.10.1186/s13045-019-0795-5
69.
Wang
,
T.
,
Hamilla
,
S.
,
Cam
,
M.
,
Aranda-Espinoza
,
H.
, and
Mili
,
S.
,
2017
, “
Extracellular Matrix Stiffness and Cell Contractility Control RNA Localization to Promote Cell Migration
,”
Nat. Commun.
, 8, p.
896
.10.1038/s41467-017-00884-y
70.
Liu
,
Y.-J.
,
Le Berre
,
M.
,
Lautenschlaeger
,
F.
,
Maiuri
,
P.
,
Callan-Jones
,
A.
,
Heuzé
,
M.
,
Takaki
,
T.
,
Voituriez
,
R.
, and
Piel
,
M.
,
2015
, “
Confinement and Low Adhesion Induce Fast Amoeboid Migration of Slow Mesenchymal Cells
,”
Cell
,
160
(
4
), pp.
659
672
.10.1016/j.cell.2015.01.007
71.
Vargas
,
P.
,
Barbier
,
L.
,
Sáez
,
P. J.
, and
Piel
,
M.
,
2017
, “
Mechanisms for Fast Cell Migration in Complex Environments
,”
Curr. Opin. Cell Biol.
,
48
, pp.
72
78
.10.1016/j.ceb.2017.04.007
72.
Elosegui-Artola
,
A.
,
Trepat
,
X.
, and
Roca-Cusachs
,
P.
,
2018
, “
Control of Mechanotransduction by Molecular Clutch Dynamics
,”
Trends Cell Biol.
, 28(5), pp.
356
367
.10.1016/j.tcb.2018.01.008
73.
Marshall
,
B. T.
,
Long
,
M.
,
Piper
,
J. W.
,
Yago
,
T.
,
McEver
,
R. P.
, and
Zhu
,
C.
,
2003
, “
Direct Observation of Catch Bonds Involving Cell-Adhesion Molecules
,”
Nature
,
423
(
6936
), pp.
190
193
.10.1038/nature01605
74.
Oakes
,
P. W.
,
Bidone
,
T. C.
,
Beckham
,
Y.
,
Skeeters
,
A. V.
,
Ramirez-San Juan
,
G. R.
,
Winter
,
S. P.
,
Voth
,
G. A.
, and
Gardel
,
M. L.
,
2018
, “
Lamellipodium is a Myosin-Independent Mechanosensor
,”
Proc. Natl. Acad. Sci.
,
115
(
11
), pp.
2646
2651
.10.1073/pnas.1715869115
75.
Kanchanawong
,
P.
,
Shtengel
,
G.
,
Pasapera
,
A. M.
,
Ramko
,
E. B.
,
Davidson
,
M. W.
,
Hess
,
H. F.
, and
Waterman
,
C. M.
,
2010
, “
Nanoscale Architecture of Integrin-Based Cell Adhesions
,”
Nature
,
468
(
7323
), pp.
580
584
.10.1038/nature09621
76.
Chen
,
Y.
,
Pasapera
,
A. M.
,
Koretsky
,
A. P.
, and
Waterman
,
C. M.
,
2013
, “
Orientation-Specific Responses to Sustained Uniaxial Stretching in Focal Adhesion Growth and Turnover
,”
Proc. Natl. Acad. Sci. U. S. A.
,
110
(
26
), pp.
E2352
–E23
61
.10.1073/pnas.1221637110
77.
Liu
,
Y.
,
Dai
,
Q.
, and
You
,
Z.
,
2009
, “
Viscoelastic Model for Discrete Element Simulation of Asphalt Mixtures
,”
J. Eng. Mech.
,
135
(
4
), pp.
324
333
.10.1061/(ASCE)0733-9399(2009)135:4(324)
78.
Nicolas
,
A.
,
Besser
,
A.
, and
Safran
,
S. A.
,
2008
, “
Dynamics of Cellular Focal Adhesions on Deformable Substrates: Consequences for Cell Force Microscopy
,”
Biophys. J.
,
95
(
2
), pp.
527
539
.10.1529/biophysj.107.127399
79.
Wan
,
X.
,
O'Quinn
,
R. P.
,
Pierce
,
H. L.
,
Joglekar
,
A. P.
,
Gall
,
W. E.
,
DeLuca
,
J. G.
,
Carroll
,
C. W.
,
Liu
,
S.-T.
,
Yen
,
T. J.
,
McEwen
,
B. F.
,
Stukenberg
,
P. T.
,
Desai
,
A.
, and
Salmon
,
E. D.
,
2009
, “
Protein Architecture of the Human Kinetochore Microtubule Attachment Site
,”
Cell
,
137
(
4
), pp.
672
684
.10.1016/j.cell.2009.03.035
80.
Dmitrieff
,
S.
,
Alsina
,
A.
,
Mathur
,
A.
, and
Nédélec
,
F. J.
,
2017
, “
Balance of Microtubule Stiffness and Cortical Tension Determines the Size of Blood Cells With Marginal Band Across Species
,”
Proc. Natl. Acad. Sci. U. S. A.
,
114
(
17
), pp.
4418
4423
.10.1073/pnas.1618041114
81.
Watanabe
,
T.
,
Noritake
,
J.
, and
Kaibuchi
,
K.
,
2005
, “
Regulation of Microtubules in Cell Migration
,”
Trends Cell Biol.
,
15
(
2
), pp.
76
83
.10.1016/j.tcb.2004.12.006
82.
Lo
,
C.-M.
,
Wang
,
H.-B.
,
Dembo
,
M.
, and
Wang
,
Y.
,
2000
, “
Cell Movement is Guided by the Rigidity of the Substrate
,”
Biophys. J.
,
79
(
1
), pp.
144
152
.10.1016/S0006-3495(00)76279-5
83.
Raab
,
M.
,
Swift
,
J.
,
P. Dingal
,
P. C. D.
,
Shah
,
P.
,
Shin
,
J.-W.
, and
Discher
,
D. E.
,
2012
, “
Crawling From Soft to Stiff Matrix Polarizes the Cytoskeleton and Phosphoregulates Myosin—II Heavy Chain
,”
J. Cell Biol.
,
199
(
4
), pp.
669
683
.10.1083/jcb.201205056
84.
Sunyer
,
R.
,
Conte
,
V.
,
Escribano
,
J.
,
Elosegui-Artola
,
A.
,
Labernadie
,
A.
,
Valon
,
L.
,
Navajas
,
D.
,
García-Aznar
,
J. M.
,
Muñoz
,
J. J.
,
Roca-Cusachs
,
P.
,
Trepat
,
X.
,
Garcia-Aznar
,
J. M.
,
Munoz
,
J. J.
,
Roca-Cusachs
,
P.
, and
Trepat
,
X.
,
2016
, “
Collective Cell Durotaxis Emerges From Long-Range Intercellular Force Transmission
,”
Science
,
353
(
6304
), pp.
1157
1161
.10.1126/science.aaf7119
85.
Shenoy
,
V. B.
,
Wang
,
H.
, and
Wang
,
X.
,
2016
, “
A Chemo-Mechanical Free-Energy-Based Approach to Model Durotaxis and Extracellular Stiffness-Dependent Contraction and Polarization of Cells
,”
Interface Focus
,
6
(
1
), p.
20150067
.10.1098/rsfs.2015.0067
86.
Choi
,
Y. S.
,
Vincent
,
L. G.
,
Lee
,
A. R.
,
Kretchmer
,
K. C.
,
Chirasatitsin
,
S.
,
Dobke
,
M. K.
, and
Engler
,
A. J.
,
2012
, “
The Alignment and Fusion Assembly of Adipose-Derived Stem Cells on Mechanically Patterned Matrices
,”
Biomaterials
,
33
(
29
), pp.
6943
6951
.10.1016/j.biomaterials.2012.06.057
87.
Mandeville
,
J. T. H.
,
Lawson
,
M. A.
, and
Maxfield
,
F. R.
,
1997
, “
Dynamic Imaging of Neutrophil Migration in Three Dimensions: Mechanical Interactions Between Cells and Matrix
,”
J. Leukoc. Biol.
, 61(2), pp.
188
200
.10.1002/jlb.61.2.188
88.
Paszek
,
M. J.
,
Zahir
,
N.
,
Johnson
,
K. R.
,
Lakins
,
J. N.
,
Rozenberg
,
G. I.
,
Gefen
,
A.
,
Reinhart-King
,
C. A.
,
Margulies
,
S. S.
,
Dembo
,
M.
,
Boettiger
,
D.
,
Hammer
,
D. A.
, and
Weaver
,
V. M.
,
2005
, “
Tensional Homeostasis and the Malignant Phenotype
,”
Cancer Cell
,
8
(
3
), pp.
241
254
.10.1016/j.ccr.2005.08.010
89.
Guo
,
W. H.
,
Frey
,
M. T.
,
Burnham
,
N. A.
, and
Wang
,
Y. L.
,
2006
, “
Substrate Rigidity Regulates the Formation and Maintenance of Tissues
,”
Biophys. J.
, 90(6), pp.
2213
2220
.10.1529/biophysj.105.070144
90.
Plotnikov
,
S. V.
,
Pasapera
,
A. M.
,
Sabass
,
B.
, and
Waterman
,
C. M.
,
2012
, “
Force Fluctuations Within Focal Adhesions Mediate ECM-Rigidity Sensing to Guide Directed Cell Migration
,”
Cell
,
151
(
7
), pp.
1513
1527
.10.1016/j.cell.2012.11.034
91.
Flanagan
,
L. A.
,
Ju
,
Y.
,
El
,
Marg
,
B.
,
Osterfield
,
M.
, and
Janmey
,
P. A.
,
2002
, “
Neurite Branching on Deformable Substrates
,”
Neuroreport.
, 13(18), pp.
2411
2415
.10.1097/01.wnr.0000048003.96487.97
92.
Forte
,
G.
,
Pagliari
,
S.
,
Ebara
,
M.
,
Uto
,
K.
,
Van Tam
,
J. K.
,
Romanazzo
,
S.
,
Escobedo-Lucea
,
C.
,
Romano
,
E.
,
Di Nardo
,
P.
,
Traversa
,
E.
, and
Aoyagi
,
T.
,
2012
, “
Substrate Stiffness Modulates Gene Expression and Phenotype in Neonatal Cardiomyocytes In Vitro
,”
Tissue Eng. Part A
, 18(17-18), pp.
1837
1848
.
93.
Xia
,
T.
,
Zhao
,
R.
,
Feng
,
F.
,
Song
,
Y.
,
Zhang
,
Y.
,
Dong
,
L.
,
Lv
,
Y.
, and
Yang
,
L.
,
2018
, “
Gene Expression Profiling of Human Hepatocytes Grown on Differing Substrate Stiffness
,”
Biotechnol. Lett.
,
40
(
5
), pp.
809
818
.10.1007/s10529-018-2536-1
94.
Yu
,
C. K.
,
Xu
,
T.
,
Assoian
,
R. K.
, and
Rader
,
D. J.
,
2018
, “
Mining the Stiffness-Sensitive Transcriptome in Human Vascular Smooth Muscle Cells Identifies Long Noncoding RNA Stiffness Regulators
,”
Arterioscler. Thromb. Vasc. Biol.
, 38(1), pp.
164
173
.
95.
Werfel
,
J.
,
Krause
,
S.
,
Bischof
,
A. G.
,
Mannix
,
R. J.
,
Tobin
,
H.
,
Bar-Yam
,
Y.
,
Bellin
,
R. M.
, and
Ingber
,
D. E.
,
2013
, “
How Changes in Extracellular Matrix Mechanics and Gene Expression Variability Might Combine to Drive Cancer Progression
,”
PLoS One
,
8
(
10
), p.
e76122
.10.1371/journal.pone.0076122
96.
Dupont
,
S.
,
Morsut
,
L.
,
Aragona
,
M.
,
Enzo
,
E.
,
Giulitti
,
S.
,
Cordenonsi
,
M.
,
Zanconato
,
F.
,
Le Digabel
,
J.
,
Forcato
,
M.
,
Bicciato
,
S.
,
Elvassore
,
N.
, and
Piccolo
,
S.
,
2011
, “
Role of Yap/TAZ in Mechanotransduction
,”
Nature
,
474
(
7350
), pp.
179
183
.10.1038/nature10137
97.
Aragona
,
M.
,
Panciera
,
T.
,
Manfrin
,
A.
,
Giulitti
,
S.
,
Michielin
,
F.
,
Elvassore
,
N.
,
Dupont
,
S.
, and
Piccolo
,
S.
,
2013
, “
A Mechanical Checkpoint Controls Multicellular Growth Through Yap/TAZ Regulation by Actin-Processing Factors
,”
Cell
,
154
(
5
), pp.
1047
1059
.10.1016/j.cell.2013.07.042
98.
Dong
,
J.
,
Feldmann
,
G.
,
Huang
,
J.
,
Wu
,
S.
,
Zhang
,
N.
,
Comerford
,
S. A.
,
Gayyed
,
M. F.
,
Anders
,
R. A.
,
Maitra
,
A.
, and
Pan
,
D.
,
2007
, “
Elucidation of a Universal Size-Control Mechanism in Drosophila and Mammals
,”
Cell
,
130
(
6
), pp.
1120
1133
.10.1016/j.cell.2007.07.019
99.
Huang
,
J.
,
Wu
,
S.
,
Barrera
,
J.
,
Matthews
,
K.
, and
Pan
,
D.
,
2005
, “
The Hippo Signaling Pathway Coordinately Regulates Cell Proliferation and Apoptosis by Inactivating Yorkie, the Drosophila Homolog of Yap
,”
Cell
,
122
(
3
), pp.
421
434
.10.1016/j.cell.2005.06.007
100.
Olivier
,
M.
,
Hollstein
,
M.
, and
Hainaut
,
P.
,
2010
, “
TP53 Mutations in Human Cancers: Origins, Consequences, and Clinical Use
,”
Cold Spring Harb. Perspect. Biol.
,
2
(
1
), p.
a001008
.10.1101/cshperspect.a001008
101.
Girardini
,
J. E.
,
Napoli
,
M.
,
Piazza
,
S.
,
Rustighi
,
A.
,
Marotta
,
C.
,
Radaelli
,
E.
,
Capaci
,
V.
,
Jordan
,
L.
,
Quinlan
,
P.
,
Thompson
,
A.
,
Mano
,
M.
,
Rosato
,
A.
,
Crook
,
T.
,
Scanziani
,
E.
,
Means
,
A. R.
,
Lozano
,
G.
,
Schneider
,
C.
, and
Del Sal
,
G.
,
2011
, “
A Pin1/Mutant P53 Axis Promotes Aggressiveness in Breast Cancer
,”
Cancer Cell
,
20
(
1
), pp.
79
91
.10.1016/j.ccr.2011.06.004
102.
Di Minin
,
G.
,
Bellazzo
,
A.
,
Dal Ferro
,
M.
,
Chiaruttini
,
G.
,
Nuzzo
,
S.
,
Bicciato
,
S.
,
Piazza
,
S.
,
Rami
,
D.
,
Bulla
,
R.
,
Sommaggio
,
R.
,
Rosato
,
A.
,
Del Sal
,
G.
, and
Collavin
,
L.
,
2014
, “
Mutant P53 Reprograms TNF Signaling in Cancer Cells Through Interaction With the Tumor Suppressor DAB2IP
,”
Mol. Cell
,
56
(
5
), pp.
617
629
.10.1016/j.molcel.2014.10.013
103.
Bae
,
Y.-H.
,
Shin
,
J.-M.
,
Park
,
H.-J.
,
Jang
,
H.-O.
,
Bae
,
M.-K.
, and
Bae
,
S.-K.
,
2014
, “
Gain-of-Function Mutant P53-R280K Mediates Survival of Breast Cancer Cells
,”
Genes Genomics
,
36
(
2
), pp.
171
178
.10.1007/s13258-013-0154-9
104.
Weissmueller
,
S.
,
Manchado
,
E.
,
Saborowski
,
M.
,
Morris
,
J. P.
, IV
,
Wagenblast
,
E.
,
Davis
,
C. A.
,
Moon
,
S. H.
,
Pfister
,
N. T.
,
Tschaharganeh
,
D. F.
,
Kitzing
,
T.
,
Aust
,
D.
,
Markert
,
E. K.
,
Wu
,
J.
,
Grimmond
,
S. M.
,
Pilarsky
,
C.
,
Prives
,
C.
,
Biankin
,
A. V.
, and
Lowe
,
S. W.
,
2014
, “
Mutant P53 Drives Pancreatic Cancer Metastasis Through Cell-Autonomous PDGF Receptor β Signaling
,”
Cell
,
157
(
2
), pp.
382
394
.10.1016/j.cell.2014.01.066
105.
Zerp
,
S. F.
,
Elsas
,
A. V.
,
Peltenburg
,
L. T. C.
, and
Schrier
,
P. I.
,
1999
, “
P53 Mutations in Human Cutaneous Melanoma Correlate With Sun Exposure but Are Not Always Involved in Melanomagenesis
,”
Br. J. Cancer
,
79
(
5–6
), pp.
921
926
.10.1038/sj.bjc.6690147
106.
Ingallina
,
E.
,
Sorrentino
,
G.
,
Bertolio
,
R.
,
Lisek
,
K.
,
Zannini
,
A.
,
Azzolin
,
L.
,
Severino
,
L. U.
,
Scaini
,
D.
,
Mano
,
M.
,
Mantovani
,
F.
,
Rosato
,
A.
,
Bicciato
,
S.
,
Piccolo
,
S.
, and
Del Sal
,
G.
,
2018
, “
Mechanical Cues Control Mutant P53 Stability Through a Mevalonate-RhoA Axis
,”
Nat. Cell Biol.
,
20
(
1
), pp.
28
35
.10.1038/s41556-017-0009-8
107.
Pitolli
,
C.
,
Wang
,
Y.
,
Mancini
,
M.
,
Shi
,
Y.
,
Melino
,
G.
, and
Amelio
,
I.
,
2019
, “
Do Mutations Turn P53 Into an Oncogene?
,”
Int. J. Mol. Sci.
, 20(24), p.
6241
.10.3390/ijms20246241
108.
Elsheikh
,
A.
,
Geraghty
,
B.
,
Rama
,
P.
,
Campanelli
,
M.
, and
Meek
,
K. M.
,
2010
, “
Characterization of Age-Related Variation in Corneal Biomechanical Properties
,”
J. R. Soc. Interface
,
7
(
51
), pp.
1475
1485
.10.1098/rsif.2010.0108
109.
Cartwright
,
N. E. K.
,
Tyrer
,
J. R.
, and
Marshall
,
J.
,
2011
, “
Age-Related Differences in the Elasticity of the Human Cornea
,”
Investig. Ophthalmol. Vis. Sci.
,
52
(
7
), pp.
4324
4329
.10.1167/iovs.09-4798
110.
Sicard
,
D.
,
Haak
,
A. J.
,
Choi
,
K. M.
,
Craig
,
A. R.
,
Fredenburgh
,
L. E.
, and
Tschumperlin
,
D. J.
,
2018
, “
Aging and Anatomical Variations in Lung Tissue Stiffness
,”
Am. J. Physiol. Lung Cell. Mol. Physiol.
, 314(6), pp. L946–L955.10.1152/ajplung.00415.2017
111.
Kalra
,
A.
, and
Lowe
,
A.
,
2016
, “
An Overview of Factors Affecting the Skins Youngs Modulus
,”
J. Aging Sci.
, 4(2), p.
1000156
.https://www.longdom.org/open-access/an-overview-of-factors-affecting-the-skins-youngs-modulus-2329-8847-1000156.pdf
112.
Liu
,
B.
,
McNally
,
S.
,
Kilpatrick
,
J. I.
,
Jarvis
,
S. P.
, and
O'Brien
,
C. J.
,
2018
, “
Aging and Ocular Tissue Stiffness in Glaucoma
,”
Surv. Ophthalmol.
, 63(1), pp.
56
74
.10.1016/j.survophthal.2017.06.007
113.
Park
,
S.
,
2016
, “
Fluid-Structure Interaction Analysis for Drug Transport in a Curved Stenotic Right Coronary Artery
,”
J. Biosci. Med.
,
4
(
5
), pp.
105
115
.10.1002/cnm.1231
114.
Palombo
,
C.
, and
Kozakova
,
M.
,
2016
, “
Arterial Stiffness, Atherosclerosis and Cardiovascular Risk: Pathophysiologic Mechanisms and Emerging Clinical Indications
,”
Vascul. Pharmacol.
,
77
, pp.
1
7
.10.1016/j.vph.2015.11.083
115.
Lampi
,
M. C.
, and
Reinhart-King
,
C. A.
,
2018
, “
Targeting Extracellular Matrix Stiffness to Attenuate Disease: From Molecular Mechanisms to Clinical Trials
,”
Sci. Transl. Med.
,
10
(
422
), p.
eaao0475
10.1126/scitranslmed.aao0475
116.
Tuttolomondo
,
A.
,
Di Raimondo
,
D.
,
Di Sciacca
,
R.
,
Pecoraro
,
R.
,
Arnao
,
V.
,
Buttà
,
C.
,
Licata
,
G.
, and
Pinto
,
A.
,
2012
, “
Arterial Stiffness and Ischemic Stroke in Subjects With and Without Metabolic Syndrome
,”
Atherosclerosis
,
225
(
1
), pp.
216
219
.10.1016/j.atherosclerosis.2012.08.027
117.
Gray
,
C.
,
Goodman
,
P.
,
Badger
,
S. A.
,
O'Malley
,
M. K.
,
O'Donohoe
,
M. K.
, and
McDonnell
,
C. O.
,
2016
, “
Endovascular Aneurysm Repair Increases Aortic Arterial Stiffness When Compared to Open Repair of Abdominal Aortic Aneurysms
,”
Vasc. Endovascular Surg.
, 50(5), pp.
317
320
.10.1177/1538574416647503
118.
Eble
,
J. A.
, and
Niland
,
S.
,
2019
, “
The Extracellular Matrix in Tumor Progression and Metastasis
,”
Clin. Exp. Metastasis
, 36, pp.
171
198
.
119.
Lynch
,
B.
,
Bonod-Bidaud
,
C.
,
Ducourthial
,
G.
,
Affagard
,
J. S.
,
Bancelin
,
S.
,
Psilodimitrakopoulos
,
S.
,
Ruggiero
,
F.
,
Allain
,
J. M.
, and
Schanne-Klein
,
M. C.
,
2017
, “
How Aging Impacts Skin Biomechanics: A Multiscale Study in Mice
,”
Sci. Rep.
, 7, p.
13750
.10.1038/s41598-017-13150-4
120.
Diridollou
,
S.
,
Vabre
,
V.
,
Berson
,
M.
,
Vaillant
,
L.
,
Black
,
D.
,
Lagarde
,
J. M.
,
Grégoire
,
J. M.
,
Gall
,
Y.
, and
Patat
,
F.
,
2001
, “
Skin Ageing: Changes of Physical Properties of Human Skin In Vivo
,”
Int. J. Cosmet. Sci.
, 23(6), pp.
353
362
.10.1046/j.0412-5463.2001.00105.x
121.
Pawlaczyk
,
M.
,
Lelonkiewicz
,
M.
, and
Wieczorowski
,
M.
,
2013
, “
Age-Dependent Biomechanical Properties of the Skin
,”
Postep. Dermatologii i Alergol.
, 30(5), pp.
302
306
.10.5114/pdia.2013.38359
122.
Barnes
,
J. M.
,
Przybyla
,
L.
, and
Weaver
,
V. M.
,
2017
, “
Tissue Mechanics Regulate Brain Development, Homeostasis and Disease
,”
J. Cell Sci.
,
130
(
1
), pp.
71
82
.10.1242/jcs.191742
123.
Northcott
,
J. M.
,
Dean
,
I. S.
,
Mouw
,
J. K.
, and
Weaver
,
V. M.
,
2018
, “
Feeling Stress: The Mechanics of Cancer Progression and Aggression,” Front
,”
Cell Dev. Biol.
,
6
, p.
17
.10.3389/fcell.2018.00017
124.
Sprenger
,
C. C.
,
Plymate
,
S. R.
, and
Reed
,
M. J.
,
2010
, “
Aging-Related Alterations in the Extracellular Matrix Modulate the Microenvironment and Influence Tumor Progression
,”
Int. J. Cancer
,
127
(
12
), pp.
2739
2748
.10.1002/ijc.25615
125.
Zhao
,
M.
,
Liu
,
H.
,
Tang
,
Y.
,
Meng
,
X.
,
Yu
,
J.
,
Wang
,
Q.
,
Zhou
,
Q.
,
Leng
,
S. X.
, and
Zhang
,
H.
,
2017
, “
Clinicopathologic Features and Prognostic Factors for Patients With Colorectal Cancer Who Are 75 Years and Older
,”
Oncotarget
,
8
(
45
), pp.
80002
80011
.10.18632/oncotarget.20656
126.
Shin
,
J.-W.
, and
Mooney
,
D. J.
,
2016
, “
Extracellular Matrix Stiffness Causes Systematic Variations in Proliferation and Chemosensitivity in Myeloid Leukemias
,”
Proc. Natl. Acad. Sci.
,
113
(
43
), pp.
12126
12131
.10.1073/pnas.1611338113
127.
Flemming
,
R. G.
,
Murphy
,
C. J.
,
Abrams
,
G. A.
,
Goodman
,
S. L.
, and
Nealey
,
P. F.
,
1999
, “
Effects of Synthetic Micro- and Nano-Structured Surfaces on Cell Behavior
,”
Biomaterials
,
20
(
6
), pp.
573
588
.10.1016/S0142-9612(98)00209-9
128.
Yim
,
E. K. F.
,
Reano
,
R. M.
,
Pang
,
S. W.
,
Yee
,
A. F.
,
Chen
,
C. S.
, and
Leong
,
K. W.
,
2005
, “
Nanopattern-Induced Changes in Morphology and Motility of Smooth Muscle Cells
,”
Biomaterials
,
26
(
26
), pp.
5405
5413
.10.1016/j.biomaterials.2005.01.058
129.
Capozza
,
R.
,
Caprettini
,
V.
,
Gonano
,
C. A.
,
Bosca
,
A.
,
Moia
,
F.
,
Santoro
,
F.
, and
De Angelis
,
F.
,
2018
, “
Cell Membrane Disruption by Vertical Micro-/Nanopillars: Role of Membrane Bending and Traction Forces
,”
ACS Appl. Mater. Interfaces
,
10
(
34
), pp.
29107
29114
.10.1021/acsami.8b08218
130.
Antonny
,
B.
,
2011
, “
Mechanisms of Membrane Curvature Sensing
,”
Annu. Rev. Biochem.
,
80
(
1
), pp.
101
123
.10.1146/annurev-biochem-052809-155121
131.
McMahon
,
H. T.
, and
Gallop
,
J. L.
,
2005
, “
Membrane Curvature and Mechanisms of Dynamic Cell Membrane Remodelling
,”
Nature
,
438
(
7068
), pp.
590
596
.10.1038/nature04396
132.
Peter
,
B. J.
,
Kent
,
H. M.
,
Mills
,
I. G.
,
Vallis
,
Y.
,
Butler
,
P. J. G.
,
Evans
,
P. R.
, and
McMahon
,
H. T.
,
2004
, “
BAR Domains as Sensors of Membrane Curvature: The Amphiphysin BAR Structure
,”
Science
,
303
(
5657
), pp.
495
499
.10.1126/science.1092586
133.
Fritz
,
R. D.
,
Menshykau
,
D.
,
Martin
,
K.
,
Reimann
,
A.
,
Pontelli
,
V.
, and
Pertz
,
O.
,
2015
, “
SrGAP2-Dependent Integration of Membrane Geometry and Slit-Robo-Repulsive Cues Regulates Fibroblast Contact Inhibition of Locomotion
,”
Dev. Cell
,
35
(
1
), pp.
78
92
.10.1016/j.devcel.2015.09.002
134.
Galic
,
M.
,
Tsai
,
F. C.
,
Collins
,
S. R.
,
Matis
,
M.
,
Bandara
,
S.
, and
Meyer
,
T.
,
2014
, “
Dynamic Recruitment of the Curvature-Sensitive Protein ArhGAP44 to Nanoscale Membrane Deformations Limits Exploratory Filopodia Initiation in Neurons
,”
Elife
,
3
, p.
e03116
.10.7554/eLife.03116
135.
Kim
,
S. H.
,
Chi
,
M.
,
Yi
,
B.
,
Kim
,
S. H.
,
Oh
,
S.
,
Kim
,
Y.
,
Park
,
S.
, and
Sung
,
J. H.
,
2014
, “
Three-Dimensional Intestinal Villi Epithelium Enhances Protection of Human Intestinal Cells From Bacterial Infection by Inducing Mucin Expression
,”
Integr. Biol.
,
6
(
12
), pp.
1122
1131
.10.1039/c4ib00157e
136.
Lee
,
J.
,
Abdeen
,
A. A.
,
Wycislo
,
K. L.
,
Fan
,
T. M.
, and
Kilian
,
K. A.
,
2016
, “
Interfacial Geometry Dictates Cancer Cell Tumorigenicity
,”
Nat. Mater.
,
15
(
8
), pp.
856
–8
62
.10.1038/nmat4610
137.
Boghaert
,
E.
,
Gleghorn
,
J. P.
,
Lee
,
K.
,
Gjorevski
,
N.
,
Radisky
,
D. C.
, and
Nelson
,
C. M.
,
2012
, “
Host Epithelial Geometry Regulates Breast Cancer Cell Invasiveness
,”
Proc. Natl. Acad. Sci.
,
109
(
48
), pp.
19632
19637
.10.1073/pnas.1118872109
138.
Maechler
,
F. A.
,
Allier
,
C.
,
Roux
,
A.
, and
Tomba
,
C.
,
2019
, “
Curvature-Dependent Constraints Drive Remodeling of Epithelia
,”
J. Cell Sci.
,
132
(
4
), pp. jcs222372.10.1242/jcs.222372
139.
Yevick
,
H. G.
,
Duclos
,
G.
,
Bonnet
,
I.
, and
Silberzan
,
P.
,
2015
, “
Architecture and Migration of an Epithelium on a Cylindrical Wire
,”
Proc. Natl. Acad. Sci. U. S. A.
,
112
(
19
), pp.
5944
5949
.10.1073/pnas.1418857112
140.
Bade
,
N. D.
,
Kamien
,
R. D.
,
Assoian
,
R. K.
, and
Stebe
,
K. J.
,
2017
, “
Curvature and Rho Activation Differentially Control the Alignment of Cells and Stress Fibers
,”
Sci. Adv.
,
3
(
9
), p.
e1700150
.10.1126/sciadv.1700150
141.
Werner
,
M.
,
Blanquer
,
S. B. G.
,
Haimi
,
S. P.
,
Korus
,
G.
,
Dunlop
,
J. W. C.
,
Duda
,
G. N.
,
Grijpma
,
D. W.
, and
Petersen
,
A.
,
2017
, “
Surface Curvature Differentially Regulates Stem Cell Migration and Differentiation Via Altered Attachment Morphology and Nuclear Deformation
,”
Adv. Sci.
,
4
(
2
), p.
1600347
.10.1002/advs.201600347
142.
Pieuchot
,
L.
,
Marteau
,
J.
,
Guignandon
,
A.
,
Dos Santos
,
T.
,
Brigaud
,
I.
,
Chauvy
,
P. F.
,
Cloatre
,
T.
,
Ponche
,
A.
,
Petithory
,
T.
,
Rougerie
,
P.
,
Vassaux
,
M.
,
Milan
,
J. L.
,
Tusamda Wakhloo
,
N.
,
Spangenberg
,
A.
,
Bigerelle
,
M.
, and
Anselme
,
K.
,
2018
, “
Curvotaxis Directs Cell Migration Through Cell-Scale Curvature Landscapes
,”
Nat. Commun.
,
9
(
1
), p.
3995
.10.1038/s41467-018-06494-6
143.
Ravasio
,
A.
,
Le
,
A. P.
,
Saw
,
T. B.
,
Tarle
,
V.
,
Ong
,
H. T.
,
Bertocchi
,
C.
,
Mège
,
R.-M.
,
Lim
,
C. T.
,
Gov
,
N. S.
, and
Ladoux
,
B.
,
2015
, “
Regulation of Epithelial Cell Organization by Tuning Cell–Substrate Adhesion
,”
Integr. Biol.
,
7
(
10
), pp.
1228
1241
.10.1039/C5IB00196J
144.
Maruthamuthu
,
V.
,
Sabass
,
B.
,
Schwarz
,
U. S.
, and
Gardel
,
M. L.
,
2011
, “
Cell-ECM Traction Force Modulates Endogenous Tension at Cell-Cell Contacts
,”
Proc. Natl. Acad. Sci.
,
108
(
12
), pp.
4708
4713
.10.1073/pnas.1011123108
145.
Sim
,
J. Y.
,
Moeller
,
J.
,
Hart
,
K. C.
,
Ramallo
,
D.
,
Vogel
,
V.
,
Dunn
,
A. R.
,
Nelson
,
W. J.
, and
Pruitt
,
B. L.
,
2015
, “
Spatial Distribution of Cell–Cell and Cell–ECM Adhesions Regulates Force Balance While Main-Taining E-Cadherin Molecular Tension in Cell Pairs
,”
Mol. Biol. Cell
,
26
(
13
), pp.
2456
2465
.10.1091/mbc.E14-12-1618
146.
Ng
,
M. R. O.
,
Besser
,
A.
,
Brugge
,
J. S.
, and
Danuser
,
G.
,
2014
, “
Mapping the Dynamics of Force Transduction at Cell-Cell Junctions of Epithelial Clusters
,”
Elife
,
3
, p.
e03282
.10.7554/eLife.03282
147.
Broaders
,
K. E.
,
Cerchiari
,
A. E.
, and
Gartner
,
Z. J.
,
2015
, “
Coupling Between Apical Tension and Basal Adhesion Allow Epithelia to Collectively Sense and Respond to Substrate Topography Over Long Distances
,”
Integr. Biol.
,
7
(
12
), pp.
1611
1621
.10.1039/C5IB00240K
148.
Pitaktong
,
I.
,
Lui
,
C.
,
Lowenthal
,
J.
,
Mattson
,
G.
,
Jung
,
W. H.
,
Bai
,
Y.
,
Yeung
,
E.
,
Ong
,
C. S.
,
Chen
,
Y.
,
Gerecht
,
S.
, and
Hibino
,
N.
,
2020
, “
Early Vascular Cells Improve Microvascularization Within 3D Cardiac Spheroids
,”
Tissue Eng. Part C Methods
,
26
(
2
), pp.
80
90
.10.1089/ten.tec.2019.0228
149.
Boudou
,
T.
,
Legant
,
W. R.
,
Mu
,
A.
,
Borochin
,
M. A.
,
Thavandiran
,
N.
,
Radisic
,
M.
,
Zandstra
,
P. W.
,
Epstein
,
J. A.
,
Margulies
,
K. B.
, and
Chen
,
C. S.
,
2012
, “
A Microfabricated Platform to Measure and Manipulate the Mechanics of Engineered Cardiac Microtissues
,”
Tissue Eng. Part A
,
18
(
9–10
), pp.
910
919
.10.1089/ten.tea.2011.0341
150.
Chen
,
P.-Y.
,
Yang
,
K.-C.
,
Wu
,
C.-C.
,
Yu
,
J.-H.
,
Lin
,
F.-H.
, and
Sun
,
J.-S.
,
2014
, “
Fabrication of Large Perfusable Macroporous Cell-Laden Hydrogel Scaffolds Using Microbial Transglutaminase
,”
Acta Biomater.
,
10
(
2
), pp.
912
920
.10.1016/j.actbio.2013.11.009
151.
Davidson
,
C. D.
,
Wang
,
W. Y.
,
Zaimi
,
I.
,
Jayco
,
D. K. P.
, and
Baker
,
B. M.
,
2019
, “
Cell Force-Mediated Matrix Reorganization Underlies Multicellular Network Assembly
,”
Sci. Rep.
,
9
(
1
), p.
12
.10.1038/s41598-018-37044-1
152.
Balkwill
,
F. R.
,
Capasso
,
M.
, and
Hagemann
,
T.
,
2012
, “
The Tumor Microenvironment at a Glance
,”
J. Cell Sci.
,
125
(
23
), pp.
5591
5596
.10.1242/jcs.116392
153.
Kalluri
,
R.
, and
Zeisberg
,
M.
,
2006
, “
Fibroblasts in Cancer
,”
Nat. Rev. Cancer
,
6
(
5
), pp.
392
401
.10.1038/nrc1877
154.
Folkman
,
J.
,
2002
, “
Role of Angiogenesis in Tumor Growth and Metastasis
,”
Semin. Oncol.
,
29
(
6Q
), pp.
15
18
.10.1053/sonc.2002.37263
155.
Orimo
,
A.
,
Gupta
,
P. B.
,
Sgroi
,
D. C.
,
Arenzana-Seisdedos
,
F.
,
Delaunay
,
T.
,
Naeem
,
R.
,
Carey
,
V. J.
,
Richardson
,
A. L.
, and
Weinberg
,
R. A.
,
2005
, “
Stromal Fibroblasts Present in Invasive Human Breast Carcinomas Promote Tumor Growth and Angiogenesis Through Elevated SDF-1/CXCL12 Secretion
,”
Cell
,
121
(
3
), pp.
335
348
.10.1016/j.cell.2005.02.034
156.
Olumi
,
A. F.
,
Grossfeld
,
G. D.
,
Hayward
,
S. W.
,
Carroll
,
P. R.
,
Tlsty
,
T. D.
, and
Cunha
,
G. R.
,
1999
, “
Carcinoma-Associated Fibroblasts Direct Tumor Progression of Initiated Human Prostatic Epithelium
,”
Cancer Res.
,
59
(
19
), pp.
5002
5011
.10.1186/bcr138
157.
Nieman
,
K. M.
,
Kenny
,
H. A.
,
Penicka
,
C. V.
,
Ladanyi
,
A.
,
Buell-Gutbrod
,
R.
,
Zillhardt
,
M. R.
,
Romero
,
I. L.
,
Carey
,
M. S.
,
Mills
,
G. B.
,
Hotamisligil
,
G. S.
,
Yamada
,
S. D.
,
Peter
,
M. E.
,
Gwin
,
K.
, and
Lengyel
,
E.
,
2011
, “
Adipocytes Promote Ovarian Cancer Metastasis and Provide Energy for Rapid Tumor Growth
,”
Nat. Med.
,
17
(
11
), pp.
1498
1503
.10.1038/nm.2492
158.
Hanahan
,
D.
, and
Weinberg
,
R. A.
,
2011
, “
Hallmarks of Cancer: The Next Generation
,”
Cell
,
144
(
5
), pp.
646
674
.10.1016/j.cell.2011.02.013
159.
Frantz
,
C.
,
Stewart
,
K. M.
, and
Weaver
,
V. M.
,
2010
, “
The Extracellular Matrix at a Glance
,”
J. Cell Sci.
,
123
(
24
), pp.
4195
4200
.10.1242/jcs.023820
160.
Guo
,
Y. P.
,
Martin
,
L. J.
,
Hanna
,
W.
,
Banerjee
,
D.
,
Miller
,
N.
,
Fishell
,
E.
,
Khokha
,
R.
, and
Boyd
,
N. F.
,
2001
, “
Growth Factors and Stromal Matrix Proteins Associated With Mammographic Densities
,”
Cancer Epidemiol. Biomarkers Prev.
,
10
(
3
), pp.
243
248
.https://pubmed.ncbi.nlm.nih.gov/11303594/#:~:text=Abstract,breast%20tissue%20with%20mammographic%20densities
161.
Boyd
,
N. F.
,
Martin
,
L. J.
,
Stone
,
J.
,
Greenberg
,
C.
,
Minkin
,
S.
, and
Yaffe
,
M. J.
,
2001
, “
Mammographic Densities as a Marker of Human Breast Cancer Risk and Their Use in Chemoprevention
,”
Curr. Oncol. Rep.
,
3
(
4
), pp.
314
321
.10.1007/s11912-001-0083-7
162.
Haeger
,
A.
,
Krause
,
M.
,
Wolf
,
K.
, and
Friedl
,
P.
,
2014
, “
Cell Jamming: Collective Invasion of Mesenchymal Tumor Cells Imposed by Tissue Confinement
,”
Biochim. Biophys. Acta
,
1840
(
8
), pp.
2386
2395
.10.1016/j.bbagen.2014.03.020
163.
Arnold
,
S. A.
,
Rivera
,
L. B.
,
Miller
,
A. F.
,
Carbon
,
J. G.
,
Dineen
,
S. P.
,
Xie
,
Y.
,
Castrillon
,
D. H.
,
Sage
,
E. H.
,
Puolakkainen
,
P.
,
Bradshaw
,
A. D.
, and
Brekken
,
R. A.
,
2010
, “
Lack of Host SPARC Enhances Vascular Function and Tumor Spread in an Orthotopic Murine Model of Pancreatic Carcinoma
,”
DMM Dis. Model. Mech.
,
3
(
1–2
), pp.
57
72
.10.1242/dmm.003228
164.
Gilkes
,
D. M.
,
Bajpai
,
S.
,
Wong
,
C. C.
,
Chaturvedi
,
P.
,
Hubbi
,
M. E.
,
Wirtz
,
D.
, and
Semenza
,
G. L.
,
2013
, “
Procollagen Lysyl Hydroxylase 2 is Essential for Hypoxia-Induced Breast Cancer Metastasis
,”
Mol. Cancer Res.
,
11
(
5
), pp.
456
466
.10.1158/1541-7786.MCR-12-0629
165.
Spill
,
F.
,
Reynolds
,
D. S.
,
Kamm
,
R. D.
, and
Zaman
,
M. H.
,
2016
, “
Impact of the Physical Microenvironment on Tumor Progression and Metastasis
,”
Curr. Opin. Biotechnol.
,
40
, pp.
41
48
.10.1016/j.copbio.2016.02.007
166.
Erler
,
J. T.
,
Bennewith
,
K. L.
,
Nicolau
,
M.
,
Dornhöfer
,
N.
,
Kong
,
C.
,
Le
,
Q. T.
,
Chi
,
J. T. A.
,
Jeffrey
,
S. S.
, and
Giaccia
,
A. J.
,
2006
, “
Lysyl Oxidase is Essential for Hypoxia-Induced Metastasis
,”
Nature
,
440
(
7088
), pp.
1222
1226
.10.1038/nature04695
167.
Xiong
,
G.
,
Deng
,
L.
,
Zhu
,
J.
,
Rychahou
,
P. G.
, and
Xu
,
R.
,
2014
, “
Prolyl-4-Hydroxylase α Subunit 2 Promotes Breast Cancer Progression and Metastasis by Regulating Collagen Deposition
,”
BMC Cancer
,
14
(
1
), p.
1
.10.1186/1471-2407-14-1
168.
Wozniak
,
M. A.
,
Desai
,
R.
,
Solski
,
P. A.
,
Der
,
C. J.
, and
Keely
,
P. J.
,
2003
, “
ROCK-Generated Contractility Regulates Breast Epithelial Cell Differentiation in Response to the Physical Properties of a Three-Dimensional Collagen Matrix
,”
J. Cell Biol.
,
163
(
3
), pp.
583
595
.10.1083/jcb.200305010
169.
Provenzano
,
P. P.
, and
Keely
,
P. J.
,
2011
, “
Mechanical Signaling Through the Cytoskeleton Regulates Cell Proliferation by Coordinated Focal Adhesion and Rho GTPase Signaling
,”
J. Cell Sci.
,
124
(
8
), pp.
1195
1205
.10.1242/jcs.067009
170.
Ford
,
A. J.
, and
Rajagopalan
,
P.
,
2018
, “
Extracellular Matrix Remodeling in 3D: Implications in Tissue Homeostasis and Disease Progression
,”
Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol.
,
10
(
4
), p.
e1503
.10.1002/wnan.1503
171.
Schedin
,
P.
, and
Keely
,
P. J.
,
2011
, “
Mammary Gland ECM Remodeling, Stiffness, and Mechanosignaling in Normal Development and Tumor Progression
,”
Cold Spring Harb. Perspect. Biol.
,
3
(
1
), p.
a003228
.10.1101/cshperspect.a003228
172.
Öhlund
,
D.
,
Elyada
,
E.
, and
Tuveson
,
D.
,
2014
, “
Fibroblast Heterogeneity in the Cancer Wound
,”
J. Exp. Med.
,
211
(
8
), pp.
1503
1523
.10.1084/jem.20140692
173.
Leung
,
C. S.
,
Yeung
,
T. L.
,
Yip
,
K. P.
,
Wong
,
K. K.
,
Ho
,
S. Y.
,
Mangala
,
L. S.
,
Sood
,
A. K.
,
Lopez-Berestein
,
G.
,
Sheng
,
J.
,
Wong
,
S. T. C.
,
Birrer
,
M. J.
, and
Mok
,
S. C.
,
2017
, “
Cancer-Associated Fibroblasts Regulate Endothelial Adhesion Protein LPP to Promote Ovarian Cancer Chemoresistance
,”
J. Clin. Invest.
,
128
(
2
), pp.
589
606
.10.1172/JCI95200
174.
Liu
,
T.
,
Zhou
,
L.
,
Li
,
D.
,
Andl
,
T.
, and
Zhang
,
Y.
,
2019
, “
Cancer-Associated Fibroblasts Build and Secure the Tumor Microenvironment
,” Front
Cell Dev. Biol.
,
7
, p.
60
.10.3389/fcell.2019.00060
175.
Donnarumma
,
E.
,
Fiore
,
D.
,
Nappa
,
M.
,
Roscigno
,
G.
,
Adamo
,
A.
,
Iaboni
,
M.
,
Russo
,
V.
,
Affinito
,
A.
,
Puoti
,
I.
,
Quintavalle
,
C.
,
Rienzo
,
A.
,
Piscuoglio
,
S.
,
Thomas
,
R.
, and
Condorelli
,
G.
,
2017
, “
Cancer-Associated Fibroblasts Release Exosomal MicroRNAs That Dictate an Aggressive Phenotype in Breast Cancer
,”
Oncotarget
,
8
(
12
), pp.
19592
19608
.10.18632/oncotarget.14752
176.
Osuala
,
K. O.
,
Sameni
,
M.
,
Shah
,
S.
,
Aggarwal
,
N.
,
Simonait
,
M. L.
,
Franco
,
O. E.
,
Hong
,
Y.
,
Hayward
,
S. W.
,
Behbod
,
F.
,
Mattingly
,
R. R.
, and
Sloane
,
B. F.
,
2015
, “
Il-6 Signaling Between Ductal Carcinoma In Situ Cells and Carcinoma-Associated Fibroblasts Mediates Tumor Cell Growth and Migration
,”
BMC Cancer
,
15
(
1
), p.
584
.10.1186/s12885-015-1576-3
177.
Tao
,
L.
,
Huang
,
G.
,
Song
,
H.
,
Chen
,
Y.
, and
Chen
,
L.
,
2017
, “
Cancer Associated Fibroblasts: An Essential Role in the Tumor Microenvironment
,”
Oncol. Lett.
,
14
(
3
), pp.
2611
2620
.10.3892/ol.2017.6497
178.
Jang
,
I.
, and
Beningo
,
K. A.
,
2019
, “
Integrins, CAFs and Mechanical Forces in the Progression of Cancer
,”
Cancers (Basel)
,
11
(
5
), p.
721
.10.3390/cancers11050721
179.
Attieh
,
Y.
,
Clark
,
A. G.
,
Grass
,
C.
,
Richon
,
S.
,
Pocard
,
M.
,
Mariani
,
P.
,
Elkhatib
,
N.
,
Betz
,
T.
,
Gurchenkov
,
B.
, and
Vignjevic
,
D. M.
,
2017
, “
Cancer-Associated Fibroblasts Lead Tumor Invasion Through Integrin-Β3-Dependent Fibronectin Assembly
,”
J. Cell Biol.
,
216
(
11
), pp.
3509
3520
.10.1083/jcb.201702033
180.
Glentis
,
A.
,
Oertle
,
P.
,
Mariani
,
P.
,
Chikina
,
A.
,
El Marjou
,
F.
,
Attieh
,
Y.
,
Zaccarini
,
F.
,
Lae
,
M.
,
Loew
,
D.
,
Dingli
,
F.
,
Sirven
,
P.
,
Schoumacher
,
M.
,
Gurchenkov
,
B. G.
,
Plodinec
,
M.
, and
Vignjevic
,
D. M.
,
2017
, “
Cancer-Associated Fibroblasts Induce Metalloprotease-Independent Cancer Cell Invasion of the Basement Membrane
,”
Nat. Commun.
,
8
(
1
), p.
924
.10.1038/s41467-017-00985-8
181.
Karnoub
,
A. E.
,
Dash
,
A. B.
,
Vo
,
A. P.
,
Sullivan
,
A.
,
Brooks
,
M. W.
,
Bell
,
G. W.
,
Richardson
,
A. L.
,
Polyak
,
K.
,
Tubo
,
R.
, and
Weinberg
,
R. A.
,
2007
, “
Mesenchymal Stem Cells Within Tumour Stroma Promote Breast Cancer Metastasis
,”
Nature
,
449
(
7162
), pp.
557
563
.10.1038/nature06188
182.
Ying
,
L.
,
Zhu
,
Z.
,
Xu
,
Z.
,
He
,
T.
,
Li
,
E.
,
Guo
,
Z.
,
Liu
,
F.
,
Jiang
,
C.
, and
Wang
,
Q.
,
2015
, “
Cancer Associated Fibroblast-Derived Hepatocyte Growth Factor Inhibits the Paclitaxel-Induced Apoptosis of Lung Cancer A549 Cells by Up-Regulating the PI3K/Akt and GRP78 Signaling on a Microfluidic Platform
,”
PLoS One
,
10
(
6
), p.
e0129593
.10.1371/journal.pone.0129593
183.
Labernadie
,
A.
,
2017
, “
A Mechanically Active Heterotypic E-Cadherin/N-Cadherin Adhesion Enables Fibroblasts To
,”
Nat. Cell Biol.
,
19
, pp.
224
237
.10.1038/ncb3478
184.
Paulsson
,
J.
, and
Micke
,
P.
,
2014
, “
Prognostic Relevance of Cancer-Associated Fibroblasts in Human Cancer
,”
Semin. Cancer Biol.
,
25
, pp.
61
68
.10.1016/j.semcancer.2014.02.006
185.
Shiao
,
S. L.
,
Chu
,
G. C. Y.
, and
Chung
,
L. W. K.
,
2016
, “
Regulation of Prostate Cancer Progression by the Tumor Microenvironment
,”
Cancer Lett.
,
380
(
1
), pp.
340
348
.10.1016/j.canlet.2015.12.022
186.
Houthuijzen
,
J. M.
, and
Jonkers
,
J.
,
2018
, “
Cancer-Associated Fibroblasts as Key Regulators of the Breast Cancer Tumor Microenvironment
,”
Cancer Metastasis Rev.
,
37
(
4
), pp.
577
597
.10.1007/s10555-018-9768-3
187.
Bray
,
F.
,
Ferlay
,
J.
,
Soerjomataram
,
I.
,
Siegel
,
R. L.
,
Torre
,
L. A.
, and
Jemal
,
A.
,
2018
, “
Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries
,”
CA Cancer J. Clin
,.,
68
(
6
), pp.
394
424
.10.3322/caac.21492
188.
Erez
,
N.
,
Truitt
,
M.
,
Olson
,
P.
, and
Hanahan
,
D.
,
2010
, “
Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-ΚB-Dependent Manner
,”
Cancer Cell
,
17
(
2
), pp.
135
147
.10.1016/j.ccr.2009.12.041
189.
Borges
,
F. T.
,
Melo
,
S. A.
,
Özdemir
,
B. C.
,
Kato
,
N.
,
Revuelta
,
I.
,
Miller
,
C. A.
,
Gattone
,
V. H.
,
LeBleu
,
V. S.
, and
Kalluri
,
R.
,
2013
, “
TGF-β1–Containing Exosomes From Injured Epithelial Cells Activate Fibroblasts to Initiate Tissue Regenerative Responses and Fibrosis
,”
J. Am. Soc. Nephrol.
,
24
(
3
), pp.
385
392
.10.1681/ASN.2012101031
190.
Chiba
,
M.
,
Kimura
,
M.
, and
Asari
,
S.
,
2012
, “
Exosomes Secreted From Human Colorectal Cancer Cell Lines Contain MRNAs, MicroRNAs and Natural Antisense RNAs, That Can Transfer Into the Human Hepatoma HepG2 and Lung Cancer A549 Cell Lines
,”
Oncol. Rep.
,
28
(
5
), pp.
1551
1558
.10.3892/or.2012.1967
191.
Valadi
,
H.
,
Ekström
,
K.
,
Bossios
,
A.
,
Sjöstrand
,
M.
,
Lee
,
J. J.
, and
Lötvall
,
J. O.
,
2007
, “
Exosome-Mediated Transfer of MRNAs and MicroRNAs is a Novel Mechanism of Genetic Exchange Between Cells
,”
Nat. Cell Biol.
,
9
(
6
), pp.
654
659
.10.1038/ncb1596
192.
Jotzu
,
C.
,
Alt
,
E.
,
Welte
,
G.
,
Li
,
J.
,
Hennessy
,
B. T.
,
Devarajan
,
E.
,
Krishnappa
,
S.
,
Pinilla
,
S.
,
Droll
,
L.
, and
Song
,
Y.-H.
,
2010
, “
Adipose Tissue-Derived Stem Cells Differentiate Into Carcinoma-Associated Fibroblast-Like Cells Under the Influence of Tumor-Derived Factors
,”
Anal. Cell. Pathol.
,
33
(
2
), pp.
61
79
.10.1155/2010/695162
193.
Xiao
,
L.
,
Kim
,
D. J.
,
Davis
,
C. L.
,
McCann
,
J. V.
,
Dunleavey
,
J. M.
,
Vanderlinden
,
A. K.
,
Xu
,
N.
,
Pattenden
,
S. G.
,
Frye
,
S. V.
,
Xu
,
X.
,
Onaitis
,
M.
,
Monaghan-Benson
,
E.
,
Burridge
,
K.
, and
Dudley
,
A. C.
,
2015
, “
Tumor Endothelial Cells With Distinct Patterns of TGFβ-Driven Endothelial-to-Mesenchymal Transition
,”
Cancer Res.
,
75
(
7
), pp.
1244
1254
.10.1158/0008-5472.CAN-14-1616
194.
Rizki
,
A.
,
Weaver
,
V. M.
,
Lee
,
S.-Y.
,
Rozenberg
,
G. I.
,
Chin
,
K.
,
Myers
,
C. A.
,
Bascom
,
J. L.
,
Mott
,
J. D.
,
Semeiks
,
J. R.
,
Grate
,
L. R.
,
Mian
,
I. S.
,
Borowsky
,
A. D.
,
Jensen
,
R. A.
,
Idowu
,
M. O.
,
Chen
,
F.
,
Chen
,
D. J.
,
Petersen
,
O. W.
,
Gray
,
J. W.
, and
Bissell
,
M. J.
,
2008
, “
A Human Breast Cell Model of Preinvasive to Invasive Transition
,”
Cancer Res.
,
68
(
5
), pp.
1378
1387
.10.1158/0008-5472.CAN-07-2225
195.
Ma
,
X.-J.
,
Dahiya
,
S.
,
Richardson
,
E.
,
Erlander
,
M.
, and
Sgroi
,
D. C.
,
2009
, “
Gene Expression Profiling of the Tumor Microenvironment During Breast Cancer Progression
,”
Breast Cancer Res.
,
11
(
1
), p.
R7
.10.1186/bcr2222
196.
Stylianopoulos
,
T.
,
Diop-Frimpong
,
B.
,
Munn
,
L. L.
, and
Jain
,
R. K.
,
2010
, “
Diffusion Anisotropy in Collagen Gels and Tumors: The Effect of Fiber Network Orientation
,”
Biophys. J.
,
99
(
10
), pp.
3119
3128
.10.1016/j.bpj.2010.08.065
197.
Gomez
,
D.
,
Natan
,
S.
,
Shokef
,
Y.
, and
Lesman
,
A.
,
2019
, “
Mechanical Interaction Between Cells Facilitates Molecular Transport
,”
Adv. Biosyst.
,
3
(
12
), p.
1900192
.10.1002/adbi.201900192
198.
Wang
,
H.
,
Abhilash
,
A. S.
,
Chen
,
C. S.
,
Wells
,
R. G.
, and
Shenoy
,
V. B.
,
2014
, “
Long-Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers
,”
Biophys. J.
,
107
(
11
), pp.
2592
2603
.10.1016/j.bpj.2014.09.044
199.
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
,”
Proc. Natl. Acad. Sci. U. S. A.
,
109
(
15
), pp.
5576
5582
.10.1073/pnas.1114781109
200.
Calvo
,
F.
,
Ege
,
N.
,
Grande-Garcia
,
A.
,
Hooper
,
S.
,
Jenkins
,
R. P.
,
Chaudhry
,
S. I.
,
Harrington
,
K.
,
Williamson
,
P.
,
Moeendarbary
,
E.
,
Charras
,
G.
, and
Sahai
,
E.
,
2013
, “
Mechanotransduction and Yap-Dependent Matrix Remodelling is Required for the Generation and Maintenance of Cancer-Associated Fibroblasts
,”
Nat. Cell Biol.
,
15
(
6
), pp.
637
–6
46
.10.1038/ncb2756
201.
Liu
,
F.
,
Lagares
,
D.
,
Choi
,
K. M.
,
Stopfer
,
L.
,
Marinković
,
A.
,
Vrbanac
,
V.
,
Probst
,
C. K.
,
Hiemer
,
S. E.
,
Sisson
,
T. H.
,
Horowitz
,
J. C.
,
Rosas
,
I. O.
,
Fredenburgh
,
L. E.
,
Feghali-Bostwick
,
C.
,
Varelas
,
X.
,
Tager
,
A. M.
, and
Tschumperlin
,
D. J.
,
2015
, “
Mechanosignaling Through Yap and TAZ Drives Fibroblast Activation and Fibrosis
,”
Am. J. Physiol. Lung Cell. Mol. Physiol.
,
308
(
4
), pp.
L344
L357
.10.1152/ajplung.00300.2014
202.
Lai
,
S. K.
,
Wang
,
Y. Y.
,
Wirtz
,
D.
, and
Hanes
,
J.
,
2009
, “
Micro- and Macrorheology of Mucus
,”
Adv. Drug Deliv. Rev.
,
61
(
2
), pp.
86
100
.10.1016/j.addr.2008.09.012
203.
Verdier
,
C.
,
Etienne
,
J.
,
Duperray
,
A.
, and
Preziosi
,
L.
,
2009
, “
Review: Rheological Properties of Biological Materials
,”
C. R. Phys.
,
10
(
8
), pp.
790
811
.10.1016/j.crhy.2009.10.003
204.
Galabert
,
C.
,
Jacquot
,
J.
,
Zahm
,
J. M.
, and
Puchelle
,
E.
,
1987
, “
Relationships Between the Lipid Content and the Rheological Properties of Airway Secretions in Cystic Fibrosis
,”
Clin. Chim. Acta
,
164
(
2
), pp.
139
149
.10.1016/0009-8981(87)90065-9
205.
Fahy
,
J. V.
, and
Dickey
,
B. F.
,
2010
, “
Medical Progress: Airway Mucus Function and Dysfunction
,”
N. Engl. J. Med.
,
363
(
23
), pp.
2233
2247
.10.1056/NEJMra0910061
206.
Drenos
,
F.
,
Miller
,
G. J.
, and
Humphries
,
S. E.
,
2007
, “
Increase of Plasma Fibrinogen Levels and Variability With Age in a Sample of Middle Aged Healthy Men
,”
Ann. Hum. Genet.
,
71
(
1
), pp.
43
53
.10.1111/j.1469-1809.2006.00302.x
207.
Simmonds
,
M. J.
,
Meiselman
,
H. J.
, and
Baskurt
,
O. K.
,
2013
, “
Blood Rheology and Aging
,”
J. Geriatr. Cardiol.
,
10
(
3
), pp.
291
301
.10.3969/j.issn.1671-5411.2013.03.010
208.
Pisetsky
,
D. S.
,
2011
, “
Pus: The Rodney Dangerfield of Immunology
,”
Arthritis Res. Ther.
,
13
(
5
), p.
131
.10.1186/ar3477
209.
Kufe
,
D. W.
,
2009
, “
Mucins in Cancer: Function, Prognosis and Therapy
,”
Nat. Rev. Cancer
,
9
(
12
), pp.
874
885
.10.1038/nrc2761
210.
Rachagani
,
S.
,
Torres
,
M. P.
,
Moniaux
,
N.
, and
Batra
,
S. K.
,
2009
, “
Current Status of Mucins in the Diagnosis and Therapy of Cancer
,”
BioFactors
,
35
(
6
), pp.
509
527
.10.1002/biof.64
211.
Hollingsworth
,
M. A.
, and
Swanson
,
B. J.
,
2004
, “
Mucins in Cancer: Protection and Control of the Cell Surface
,”
Nat. Rev. Cancer
,
4
(
1
), pp.
45
60
.10.1038/nrc1251
212.
Requena
,
S.
,
Ponomarchuk
,
O.
,
Castillo
,
M.
,
Rebik
,
J.
,
Brochiero
,
E.
,
Borejdo
,
J.
,
Gryczynski
,
I.
,
Dzyuba
,
S. V.
,
Gryczynski
,
Z.
,
Grygorczyk
,
R.
, and
Fudala
,
R.
,
2017
, “
Imaging Viscosity of Intragranular Mucin Matrix in Cystic Fibrosis Cells
,”
Sci. Rep.
,
7
(
1
), p.
16761
.10.1038/s41598-017-17037-2
213.
Shimolina
,
L. E.
,
Izquierdo
,
M. A.
,
López-Duarte
,
I.
,
Bull
,
J. A.
,
Shirmanova
,
M. V.
,
Klapshina
,
L. G.
,
Zagaynova
,
E. V.
, and
Kuimova
,
M. K.
,
2017
, “
Imaging Tumor Microscopic Viscosity In Vivo Using Molecular Rotors
,”
Sci. Rep.
,
7
(
1
), p.
41097
.10.1038/srep41097
214.
Pal
,
M.
,
Dasgupta
,
D.
,
Somalwar
,
N.
,
Vr
,
R.
,
Tiwari
,
M.
,
Pally
,
D.
,
Narayana
,
S. M.
,
Katke
,
A.
,
Rs
,
J.
,
Bhat
,
R.
,
Saini
,
D. K.
, and
Ghosh
,
A.
,
2020
, “
Helical Nanobots as Mechanical Probes of Intra- and Extracellular Environments
,”
J. Phys. Condens. Matter
, 32, p.
224001
.10.1088/1361-648X/ab6f89
215.
Jee
,
A.-Y.
,
Curtis-Fisk
,
J. L.
, and
Granick
,
S.
,
2014
, “
Nanoparticle Diffusion in Methycellulose Thermoreversible Association Polymer
,”
Macromolecules
, 47(16), pp.
5793
5797
.10.1021/ma501331z
216.
Folger
,
R.
,
Weiss
,
L.
,
Glaves
,
D.
,
Subjeck
,
J. R.
, and
Harlos
,
J. P.
,
1978
, “
Translational Movements of Macrophages Through Media of Different Viscosities
,”
J. Cell Sci.
,
31
, pp.
245
–2
57
.https://pubmed.ncbi.nlm.nih.gov/670322/
217.
Matsui
,
H.
,
Verghese
,
M. W.
,
Kesimer
,
M.
,
Schwab
,
U. E.
,
Randell
,
S. H.
,
Sheehan
,
J. K.
,
Grubb
,
B. R.
, and
Boucher
,
R. C.
,
2005
, “
Reduced Three-Dimensional Motility in Dehydrated Airway Mucus Prevents Neutrophil Capture and Killing Bacteria on Airway Epithelial Surfaces
,”
J. Immunol.
,
175
(
2
), pp.
1090
1099
.10.4049/jimmunol.175.2.1090
218.
Gonzalez-Molina
,
J.
,
Zhang
,
X.
,
Borghesan
,
M.
,
Mendonça da Silva
,
J.
,
Awan
,
M.
,
Fuller
,
B.
,
Gavara
,
N.
, and
Selden
,
C.
,
2018
, “
Extracellular Fluid Viscosity Enhances Liver Cancer Cell Mechanosensing and Migration
,”
Biomaterials
,
177
, pp.
113
124
.10.1016/j.biomaterials.2018.05.058
219.
Gonzalez-Molina
,
J.
,
Mendonça da Silva
,
J.
,
Fuller
,
B.
, and
Selden
,
C.
,
2019
, “
The Extracellular Fluid Macromolecular Composition Differentially Affects Cell-Substrate Adhesion and Cell Morphology
,”
Sci. Rep.
,
9
(
1
), p.
8505
.10.1038/s41598-019-44960-3
220.
Pittman
,
M.
,
Li
,
K.
, and
Chen
,
Y.
,
2020
, “
Elevated Extracellular Fluid Viscosity Stimulates Migration of Metastatic Cancer Cells
,”
Biophys. J.
,
118
(
3
), p.
602a
.10.1016/j.bpj.2019.11.3252
221.
Mai
,
M. H.
, and
Camley
,
B. A.
,
2020
, “
Hydrodynamic Effects on the Motility of Crawling Eukaryotic Cells
,”
Soft Matter
,
16
(
5
), pp.
1349
1358
.10.1039/C9SM01797F
222.
Kobylkevich
,
B. M.
,
Sarkar
,
A.
,
Carlberg
,
B. R.
,
Huang
,
L.
,
Ranjit
,
S.
,
Graham
,
D. M.
, and
Messerli
,
M. A.
,
2018
, “
Reversing the Direction of Galvanotaxis With Controlled Increases in Boundary Layer Viscosity
,”
Phys. Biol.
,
15
(
3
), p.
036005
.10.1088/1478-3975/aaad91
223.
Levental
,
K. R.
,
Yu
,
H.
,
Kass
,
L.
,
Lakins
,
J. N.
,
Egeblad
,
M.
,
Erler
,
J. T.
,
Fong
,
S. F. T.
,
Csiszar
,
K.
,
Giaccia
,
A.
,
Weninger
,
W.
,
Yamauchi
,
M.
,
Gasser
,
D. L.
, and
Weaver
,
V. M.
,
2009
, “
Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling
,”
Cell
,
139
(
5
), pp.
891
906
.
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