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Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity
Abstract
Cell function depends on tissue rigidity, which cells probe by applying and transmitting forces to their extracellular matrix, and then transducing them into biochemical signals. Here we show that in response to matrix rigidity and density, force transmission and transduction are explained by the mechanical properties of the actin-talin-integrin-fibronectin clutch. We demonstrate that force transmission is regulated by a dynamic clutch mechanism, which unveils its fundamental biphasic force/rigidity relationship on talin depletion. Force transduction is triggered by talin unfolding above a stiffness threshold. Below this threshold, integrins unbind and release force before talin can unfold. Above the threshold, talin unfolds and binds to vinculin, leading to adhesion growth and YAP nuclear translocation. Matrix density, myosin contractility, integrin ligation and talin mechanical stability differently and nonlinearly regulate both force transmission and the transduction threshold. In all cases, coupling of talin unfolding dynamics to a theoretical clutch model quantitatively predicts cell response.
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“However, beyond acting as a physical barrier, ECM stiffness also triggers mechanotransduction pathways that profoundly influence tumor cell behavior [91,92]. Mechanical cues generated by a stiffened matrix are sensed through integrin-based focal adhesions and transmitted via cytoskeletal tension to activate intracellular signaling cascades, including Yes-associated protein/Transcriptional coactiv”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [93]
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“Previous work has focused mainly on the recruitment of new linkages, especially integrins and cadherins (41, 52).”
Chen, Y.-Q., Wu, M.-C., Wei, M., Kuo, J.-C., Yu, H., & Chiou, A. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.101058 · Cited by 18
“The translocation of YAP into the nucleus stands as a critical factor in the promotion of osteogenesis [39], and this translocation is facilitated by biomechanical cues, such as substrate stiffness, cell spreading area, shear stress, and traction force [38,40,41].”
BackgroundNagasato, A. I., Yamashita, H., Matsuo, M., Ueda, K., & Kioka, N. (2017) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2017.1289074 · Cited by 19
Navarro-Hernández, I. C., López‐Ortega, O., Acevedo‐Ochoa, E., Cervantes‐Díaz, R., Romero‐Ramírez, S., Sosa‐Hernández, V. A., Meza-Sánchez, D. E., Juárez‐Vega, G., Pérez‐Martínez, C. A., Chávez‐Munguía, B., et al. (2020) · FEBS Journal · doi:10.1111/febs.15216 · Cited by 17
Missirlis, D., Baños, M., Lussier, F., & Spatz, J. P. (2022) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c17901 · Cited by 19
The 2016 John J. Abel Award Lecture: Targeting the Mechanical Microenvironment in Cancer
Majeski, H. E., & Yang, J. (2016) · Molecular Pharmacology · doi:10.1124/mol.116.106765 · Cited by 19
Wang, Y.-T., Wang, N., Yang, Y., Chen, Y., & Zhang, Z. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01713-1 · Cited by 20
The Forces behind Directed Cell Migration
Fortunato, I. C., & Sunyer, R. (2022) · Biophysica · doi:10.3390/biophysica2040046 · Cited by 18
Mechanoresponse of Curved Epithelial Monolayers Lining Bowl‐Shaped 3D Microwells
Luciano, M., Versaevel, M., Kalukula, Y., & Gabriele, S. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202203377 · Cited by 18
Mittal, N., Michels, E. B., Massey, A. E., Qiu, Y., Royer, S. P., Smith, B. R., Cartagena‐Rivera, A. X., & Han, S. J. (2024) · Communications Materials · doi:10.1038/s43246-024-00444-0 · Cited by 17
“This stiffness-dependent traction trend is consistent with data from previous studies 14 – 16, 21 , To test whether the stiffness-dependent differential traction still exists in the absence of myosin-II activity, we treated the cells with 20 µM of blebbistatin (BBS), a myosin ATPase inhibitor 46,47…”
InfluentialCellular stiffness sensing through talin 1 in tissue mechanical homeostasis
Chanduri, M. V. L., Kumar, A., Weiss, D., Emuna, N., Barsukov, I., Shi, M., Tanaka, K., Wang, X., Datye, A., Kanyo, J. E., et al. (2024) · Science Advances · doi:10.1126/sciadv.adi6286 · Cited by 18
“Deletion of talin or segments of the rod domain alters cellular mechanoresponses ( 25 – 27 ).”
BackgroundMechanotransduction in Coronary Vein Graft Disease
Ruiter, M. S., & Pesce, M. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00020 · Cited by 18
“On the other hand, very recent findings suggest that force generation by docking stress fibres to focal adhesion contacts and translation of this tension to nuclear deformation and opening of the nuclear pores promote YAP nuclear translocation, thus connecting directly mechanosensing and YAPdependent transcriptional c…”
BackgroundMechanical characterization of single cells based on microfluidic techniques
Huang, J., Lin, F., & Xiong, C. (2019) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2019.07.015 · Cited by 18
Fascin1 empowers YAP mechanotransduction and promotes cholangiocarcinoma development
Pocaterra, A., Scattolin, G., Romani, P., Ament, C. E., Ribback, S., Chen, X., Evert, M., Calvisi, D. F., & Dupont, S. (2021) · Communications Biology · doi:10.1038/s42003-021-02286-9 · Cited by 19
Wang, D., Liu, B., Xiong, T., Yu, W., & She, Q. (2020) · BMC Cardiovascular Disorders · doi:10.1186/s12872-020-01701-z · Cited by 17
“an organ that is continuously subjected to mechanical force under basic conditions and must adapt to mechanical changes under physiological pressure or pathological conditions [34, 35].”
BackgroundComputational models of migration modes improve our understanding of metastasis
Shatkin, G., Yeoman, B. M., Birmingham, K. G., Katira, P., & Engler, A. J. (2020) · APL Bioengineering · doi:10.1063/5.0023748 · Cited by 17
Biosensors for Studies on Adhesion-Mediated Cellular Responses to Their Microenvironment
Saffioti, N. A., Cavalcanti‐Adam, E. A., & Pallarola, D. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.597950 · Cited by 18
Ting, M. S., Vella, J., Raos, B. J., Narasimhan, B. N., Svirskis, D. M., Travaš‐Sejdić, J., & Malmström, J. (2021) · Biomaterials Advances · doi:10.1016/j.msec.2021.112559 · Cited by 17
Optimal cell traction forces in a generalized motor-clutch model
Alonso‐Matilla, R., Provenzano, P. P., & Odde, D. J. (2023) · Biophysical Journal · doi:10.1016/j.bpj.2023.07.012 · Cited by 17
“Together, these studies suggest the existence of an optimal substrate stiffness for maximal traction force, as observed experimentally (12,14).”
InfluentialCharbonier, F. W., Zhu, J., Slyman, R., Allan, C., & Chaudhuri, O. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2417290122 · Cited by 17
Mechanical Effect on Gene Transfection Based on Dielectric Elastomer Actuator
Gao, C., Li, Z., Zou, J., Cheng, J. Q., Jiang, K., Liu, C., Gu, G., Tao, W., & Song, J. (2020) · ACS Applied Bio Materials · doi:10.1021/acsabm.9b01199 · Cited by 16
Cinar, B., Al‐Mathkour, M. M., Khan, S. A., & Moreno, C. S. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.013794 · Cited by 17
“In addition to the covalent modification, a mechanical force could also increase YAP1 nuclear import (14, 17).”
BackgroundVargas, D. A., Gonçalves, I. G., Heck, T., Smeets, B., Lafuente-Gracia, L., Ramón, H., & Oosterwyck, H. V. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00459 · Cited by 17
“With talin silenced, cells are not able to exert high tractions (Elosegui-Artola et al., 2016).”
BackgroundA mechanogenetic role for the actomyosin complex in branching morphogenesis of epithelial organs
Kim, J. M., Jo, Y., Jung, J. W., & Park, K. (2021) · Development · doi:10.1242/dev.190785 · Cited by 15
PIEZO1 Affects Cell Growth and Migration via Microfilament-Mediated YAP trans-Latitudinal Regulation
Duan, J., Li, H., Zhang, J., Xu, H., Gao, J., Cai, M., Pan, Y., Shi, Y. C., & Wang, H. (2024) · Analytical Chemistry · doi:10.1021/acs.analchem.4c03420 · Cited by 17
Yousfi, Y. E., Fernández-Farrán, F. J., Oliver, F. J., López‐Rivas, A., & Yerbes, R. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02335-w · Cited by 17
“Hydrogels were prepared as previously described [41].”
Liu, P., Wang, Q., Dai, X., Pei, L., Wang, J., Zhao, W., Johnson, H. E., Yao, M., & Efremov, A. K. (2025) · Nature Physics · doi:10.1038/s41567-025-02964-z · Cited by 16
“This monophasic behaviour is consistent with the behaviour of wild-type (WT) fibroblast cells observed in experiments 13 .”
InfluentialStiffness of the extracellular matrix regulates differentiation into beige adipocytes
Takata, K., Goto, T., Kuroda, M., Kimura, Y., Harada, I., Ueda, K., Kawada, T., & Kioka, N. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.08.032 · Cited by 16
Metadata
- Authors
- Elosegui-Artola, A., Oria, R., Chen, Y., Kosmalska, A., Pérez-González, C., Castro, N., Zhu, C., Trepat, X., & Roca-Cusachs, P.
- Affiliations
- Institute for Bioengineering of Catalonia (ES)
- Georgia Institute of Technology (US)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- Venue
- Nature Cell Biology
- Published
- 2016-04-11
- Volume
- 18
- Issue
- 5
- Pages
- 540-548
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- OpenAlex
- W2327893020
- Cited by
- 858
- References
- 57
- Citations by year
- 2026: 72 · 2025: 101 · 2024: 87 · 2023: 93 · 2022: 103 · 2021: 93 · 2020: 96 · 2019: 71 · 2018: 67 · 2017: 60 · 2016: 15
- FWCI
- 48.78
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI044902)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Force Microscopy Techniques and Applications
- Keywords
- molecular clutch, matrix rigidity, force transmission, mechanotransduction, vinculin, YAP nuclear translocation, cell adhesion, extracellular matrix stiffness, myosin contractility, actin cytoskeleton, fibronectin
- MeSH terms
- YAP-Signaling Proteins, Animals, Biomechanical Phenomena, Cell Adhesion, Cell Nucleus, Cytoskeleton, Extracellular Matrix, Fibronectins, Phosphoproteins, Phosphorylation, Protein Binding, Integrins, Vinculin, Talin, Cell Cycle Proteins, Protein Transport, Stress Fibers, Mechanotransduction, Cellular, Adaptor Proteins, Signal Transducing, Mice, Focal Adhesion Protein-Tyrosine Kinases
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