Cited by 3,941Cellular Mechanics and InteractionsCell Adhesion Molecules ResearchProtein Kinase Regulation and GTPase Signaling

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Tensional homeostasis and the malignant phenotype

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Paszek, Matthew J., Zahir, Nastaran, Johnson, Kandice R., Lakins, Johnathon N., Rozenberg, Gabriela I., Gefen, Amit, Reinhart-King, Cynthia A., Margulies, Susan S., Dembo, Micah, Boettiger, David, Hammer, Daniel A., Weaver, Valerie M.·2005·Cancer Cell

DOI 10.1016/j.ccr.2005.08.010

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Abstract

Tumors are stiffer than normal tissue, and tumors have altered integrins. Because integrins are mechanotransducers that regulate cell fate, we asked whether tissue stiffness could promote malignant behavior by modulating integrins. We found that tumors are rigid because they have a stiff stroma and elevated Rho-dependent cytoskeletal tension that drives focal adhesions, disrupts adherens junctions, perturbs tissue polarity, enhances growth, and hinders lumen formation. Matrix stiffness perturbs epithelial morphogenesis by clustering integrins to enhance ERK activation and increase ROCK-generated contractility and focal adhesions. Contractile, EGF-transformed epithelia with elevated ERK and Rho activity could be phenotypically reverted to tissues lacking focal adhesions if Rho-generated contractility or ERK activity was decreased. Thus, ERK and Rho constitute part of an integrated mechanoregulatory circuit linking matrix stiffness to cytoskeletal tension through integrins to regulate tissue phenotype.

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Crossref · 10.1016/j.ccr.2005.08.010

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Self-citation
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A multiscale dynamic model of cell–substrate interfaces
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Background
Multiscale elasticity mapping of biological samples in 3D at optical resolution
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Membrane tension-mediated stiff and soft tumor subtypes closely associated with prognosis for prostate cancer patients
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An extracellular matrix stiffness-induced breast cancer cell transcriptome resembles the transition from ductal carcinoma in situ (DCIS) to invasive ductal carcinoma (IDC)
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“Malignant cells proliferate and migrate faster in such mechanical environment (64, 65).”
Background
A Bloody Conspiracy— Blood Vessels and Immune Cells in the Tumor Microenvironment
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Mechanical Properties of the Extracellular Environment of Human Brain Cells Drive the Effectiveness of Drugs in Fighting Central Nervous System Cancers
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Increased matrix stiffness suppresses ATP-induced sustained Ca2+ influx in MDA-MB-231 breast cancer cells
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Spatial-Temporal Patterns and Inflammatory Factors of Bone Matrix Remodeling
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In situ evaluation of spatiotemporal distribution of doxorubicin from Drug-eluting Beads in a tissue mimicking phantom.
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Material properties of disulfide-crosslinked hyaluronic acid hydrogels influence prostate cancer cell growth and metabolism
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Background
Computational 4D-OCM for label-free imaging of collective cell invasion and force-mediated deformations in collagen
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Nanomedicines Reshape the Tumor Microenvironment: Multidimensional Strategies from Modulating “Barriers” to Metabolic Intervention
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ECM Mechanics Control Jamming-to-Unjamming Transition of Cancer Cells
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Novel FRET‐Based Biosensors for Real‐Time Monitoring of Estrogen Receptor Dimerization and Translocation Dynamics in Living Cells
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Breast Tumor Cell Survival and Morphology in a Brain‐like Extracellular Matrix Depends on Matrix Composition and Mechanical Properties
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Improving regulatory T cell production through mechanosensing
Shi, L., Lim, J. Y., & Kam, L. C. (2024) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.37702 · Cited by 15
An injectable CS-hydrogel incorporating TPGS for cartilage repair
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Rho activation drives luminal collapse and eversion in epithelial acini
Narayanan, V., Purkayastha, P., Yu, B., Pendyala, K., Chukkapalli, S. S., Cabe, J. I., Dickinson, R., Conway, D. E., & Lele, T. (2022) · bioRxiv · doi:10.1101/2022.07.06.499064 · Cited by 9
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Avoiding tensional equilibrium in cells migrating on a matrix with cell-scale stiffness-heterogeneity
Ebata, H., & Kidoaki, S. (2020) · bioRxiv · doi:10.1101/2020.10.15.342006 · Cited by 9
Constructing a Biomaterial to Simulate Extracellular Drug Transport in Solid Tumors.
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Oncogenetic engagement with mechanosensing
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Fully-automatic deep learning-based analysis for determination of the invasiveness of breast cancer cells in an acoustic trap
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Focal adhesion displacement magnitude is a unifying feature of tensional homeostasis.
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Authors: 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., & Weaver, V. M.
Affiliations: University of Pennsylvania (US)
Tel Aviv University (IL)
Boston University (US)
Corresponding author: Weaver, Valerie M.
ORCID: Paszek, Matthew J.
Zahir, Nastaran
Lakins, Johnathon N.
Gefen, Amit
Margulies, Susan S.
Boettiger, David
Hammer, Daniel A.
Weaver, Valerie M.
Venue: Cancer Cell
Publisher: Elsevier BV
Published: 2005-09
Volume: 8
Issue: 3
Pages: 241-254
ISSN: 1535-6108 (ISSN-L)
DOI: 10.1016/j.ccr.2005.08.010
OpenAlex: W2099052265
Cited by: 3,941
References: 0
Citations by year: 2026: 142 · 2025: 165 · 2024: 155 · 2023: 172 · 2022: 193 · 2021: 221 · 2020: 273 · 2019: 217 · 2018: 262 · 2017: 256 · 2016: 239 · 2015: 249 · 2014: 225 · 2013: 237 · 2012: 183
FWCI: 33.71
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3367 d)
Locations: Cancer Cell (publishedVersion)
PubMed (publishedVersion)
Funders: Ministerio de Economía y Competitividad
National Heart, Lung, and Blood Institute (R01HL057204, HL-57204, HL64388-01A1, T32HL007954, T32HL00795404)
National Cancer Institute (R01CA078731, CA078731)
National Institute of General Medical Sciences (R01GM057388, GM57388)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Keywords: tumor stiffness, extracellular matrix stiffness, integrins, mechanotransduction, cytoskeletal tension, Rho GTPase signaling, ERK activation, focal adhesions, adherens junctions, tissue polarity, epithelial morphogenesis, tumor stroma, contractility, malignant phenotype
MeSH terms: Animals, Cytoskeleton, Homeostasis, Neoplasms, Phenotype, Stress, Mechanical, 3T3 Cells, Stromal Cells, Cell Line, Tumor, Cell Shape, Mice

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Tensional homeostasis and the malignant phenotype

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