Riaz, Maryam
Versaevel, Marie
Mohammed, Danahe
Glinel, Karine
[UCL]
Gabriele, Sylvain
Despite the importance of matrix rigidity on cell functions, many aspects of the mechanosensing process in highly migratory cells remain elusive. Here, we studied the migration of highly motile keratocytes on culture substrates with similar biochemical properties and rigidities spanning the range between soft tissues (~kPa) and stiff culture substrates (~GPa). We show that morphology, polarization and persistence of motile keratocytes are regulated by the matrix stiffness over seven orders of magnitude, without changing the cell spreading area. Increasing the matrix rigidity leads to more F-actin in the lamellipodia and to the formation of mature contractile actomyosin fibers that control the cell rear retraction. Keratocytes remain rounded and form nascent adhesions on compliant substrates, whereas large and uniformly distributed focal adhesions are formed on fan-shaped keratocytes migrating on rigid surfaces. By combining poly-L-lysine, fibronectin and vitronectin coatings with selective blocking of αvβ3 or α5β1 integrins, we show that αVβ3 integrins permit the spreading of keratocytes but are not sufficient for polarization and rigidity sensing that require the engagement of α5β1 integrins. Our study demonstrates a matrix rigidity-dependent regulation of the directional persistence in motile keratocytes and refines the role of αvβ3 and α5β1 integrins in the molecular clutch model.
- Lauffenburger Douglas A, Horwitz Alan F, Cell Migration: A Physically Integrated Molecular Process, 10.1016/s0092-8674(00)81280-5
- Reffay M., Parrini M. C., Cochet-Escartin O., Ladoux B., Buguin A., Coscoy S., Amblard F., Camonis J., Silberzan P., Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells, 10.1038/ncb2917
- Friedl Peter, Gilmour Darren, Collective cell migration in morphogenesis, regeneration and cancer, 10.1038/nrm2720
- Roca-Cusachs Pere, Sunyer Raimon, Trepat Xavier, Mechanical guidance of cell migration: lessons from chemotaxis, 10.1016/j.ceb.2013.04.010
- Plotnikov Sergey V., Pasapera Ana M., Sabass Benedikt, Waterman Clare M., Force Fluctuations within Focal Adhesions Mediate ECM-Rigidity Sensing to Guide Directed Cell Migration, 10.1016/j.cell.2012.11.034
- Charras Guillaume, Sahai Erik, Physical influences of the extracellular environment on cell migration, 10.1038/nrm3897
- Cooper M. S., Motility of cultured fish epidermal cells in the presence and absence of direct current electric fields, 10.1083/jcb.102.4.1384
- Discher D. E., Tissue Cells Feel and Respond to the Stiffness of Their Substrate, 10.1126/science.1116995
- Lo Chun-Min, Wang Hong-Bei, Dembo Micah, Wang Yu-li, Cell Movement Is Guided by the Rigidity of the Substrate, 10.1016/s0006-3495(00)76279-5
- Gu Yun, Ji Yawei, Zhao Yahong, Liu Yan, Ding Fei, Gu Xiaosong, Yang Yumin, The influence of substrate stiffness on the behavior and functions of Schwann cells in culture, 10.1016/j.biomaterials.2012.06.006
- Guo Wei-hui, Frey Margo T., Burnham Nancy A., Wang Yu-li, Substrate Rigidity Regulates the Formation and Maintenance of Tissues, 10.1529/biophysj.105.070144
- Gupta Gaorav P., Massagué Joan, Cancer Metastasis: Building a Framework, 10.1016/j.cell.2006.11.001
- Gardel Margaret L., Schneider Ian C., Aratyn-Schaus, Yvonne, Waterman Clare M., Mechanical Integration of Actin and Adhesion Dynamics in Cell Migration, 10.1146/annurev.cellbio.011209.122036
- Wang N., Tolic-Norrelykke I. M., Chen J., Mijailovich S. M., Butler J. P., Fredberg J. J., Stamenovic D., Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells, 10.1152/ajpcell.00269.2001
- Ingber D. E., Tensegrity II. How structural networks influence cellular information processing networks, 10.1242/jcs.00360
- Bangasser Benjamin L., Rosenfeld Steven S., Odde David J., Determinants of Maximal Force Transmission in a Motor-Clutch Model of Cell Traction in a Compliant Microenvironment, 10.1016/j.bpj.2013.06.027
- Hynes Richard O., Integrins, 10.1016/s0092-8674(02)00971-6
- Morgan Mark R., Byron Adam, Humphries Martin J., Bass Mark D., Giving off mixed signals-Distinct functions of α5β1and αvβ3integrins in regulating cell behaviour, 10.1002/iub.200
- Fath, K. R., Edgell, C. J. & Burridge, K. The distribution of distinct integrins in focal contacts is determined by the substratum composition. J. Cell Sci. 92, 67–75 (1989).
- Desgrosellier Jay S., Cheresh David A., Integrins in cancer: biological implications and therapeutic opportunities, 10.1038/nrc2748
- Danen Erik H.J., van Rheenen Jacco, Franken Willeke, Huveneers Stephan, Sonneveld Petra, Jalink Kees, Sonnenberg Arnoud, Integrins control motile strategy through a Rho–cofilin pathway, 10.1083/jcb.200412081
- Missirlis Dimitris, Haraszti Tamás, Scheele Catharina v. C., Wiegand Tina, Diaz Carolina, Neubauer Stefanie, Rechenmacher Florian, Kessler Horst, Spatz Joachim P., Substrate engagement of integrins α5β1 and αvβ3 is necessary, but not sufficient, for high directional persistence in migration on fibronectin, 10.1038/srep23258
- Rafelski Susanne M., Theriot Julie A., Crawling Toward a Unified Model of Cell Motility: Spatial and Temporal Regulation of Actin Dynamics, 10.1146/annurev.biochem.73.011303.073844
- Le Clainche C., Carlier M.-F., Regulation of Actin Assembly Associated With Protrusion and Adhesion in Cell Migration, 10.1152/physrev.00021.2007
- Keren Kinneret, Cell motility: the integrating role of the plasma membrane, 10.1007/s00249-011-0741-0
- Ikoma Toshiyuki, Kobayashi Hisatoshi, Tanaka Junzo, Walsh Dominic, Mann Stephen, Microstructure, mechanical, and biomimetic properties of fish scales from Pagrus major, 10.1016/s1047-8477(03)00053-4
- Grevesse Thomas, Versaevel Marie, Circelli Géraldine, Desprez Sylvain, Gabriele Sylvain, A simple route to functionalize polyacrylamide hydrogels for the independent tuning of mechanotransduction cues, 10.1039/c2lc41168g
- Versaevel Marie, Grevesse Thomas, Riaz Maryam, Lantoine Joséphine, Gabriele Sylvain, Micropatterning Hydroxy-PAAm Hydrogels and Sylgard 184 Silicone Elastomers with Tunable Elastic Moduli, Methods in Cell Biology (2014) ISBN:9780128002810 p.33-48, 10.1016/b978-0-12-800281-0.00003-8
- Grevesse Thomas, Dabiri Borna E., Parker Kevin Kit, Gabriele Sylvain, Opposite rheological properties of neuronal microcompartments predict axonal vulnerability in brain injury, 10.1038/srep09475
- Lantoine Joséphine, Grevesse Thomas, Villers Agnès, Delhaye Geoffrey, Mestdagh Camille, Versaevel Marie, Mohammed Danahe, Bruyère Céline, Alaimo Laura, Lacour Stéphanie P., Ris Laurence, Gabriele Sylvain, Matrix stiffness modulates formation and activity of neuronal networks of controlled architectures, 10.1016/j.biomaterials.2016.02.041
- Trappmann Britta, Gautrot Julien E., Connelly John T., Strange Daniel G. T., Li Yuan, Oyen Michelle L., Cohen Stuart Martien A., Boehm Heike, Li Bojun, Vogel Viola, Spatz Joachim P., Watt Fiona M., Huck Wilhelm T. S., Extracellular-matrix tethering regulates stem-cell fate, 10.1038/nmat3339
- Wen Jessica H., Vincent Ludovic G., Fuhrmann Alexander, Choi Yu Suk, Hribar Kolin C., Taylor-Weiner Hermes, Chen Shaochen, Engler Adam J., Interplay of matrix stiffness and protein tethering in stem cell differentiation, 10.1038/nmat4051
- Keren Kinneret, Pincus Zachary, Allen Greg M., Barnhart Erin L., Marriott Gerard, Mogilner Alex, Theriot Julie A., Mechanism of shape determination in motile cells, 10.1038/nature06952
- Barnhart Erin L., Lee Kun-Chun, Keren Kinneret, Mogilner Alex, Theriot Julie A., An Adhesion-Dependent Switch between Mechanisms That Determine Motile Cell Shape, 10.1371/journal.pbio.1001059
- Prager-Khoutorsky Masha, Lichtenstein Alexandra, Krishnan Ramaswamy, Rajendran Kavitha, Mayo Avi, Kam Zvi, Geiger Benjamin, Bershadsky Alexander D., Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing, 10.1038/ncb2370
- Solon Jérôme, Levental Ilya, Sengupta Kheya, Georges Penelope C., Janmey Paul A., Fibroblast Adaptation and Stiffness Matching to Soft Elastic Substrates, 10.1529/biophysj.106.101386
- Stokes, C. L., Lauffenburger, D. A. & Williams, S. K. Migration of individual microvessel endothelial cells: stochastic model and parameter measurement. J. Cell Sci. 99, 419–430 (1991).
- Zhu Jiangtao, Wong Hoi Man, Yeung Kelvin Wai Kwok, Tjong Sie Chin, Spark Plasma Sintered Hydroxyapatite/Graphite Nanosheet and Hydroxyapatite/Multiwalled Carbon Nanotube Composites: Mechanical and in Vitro Cellular Properties, 10.1002/adem.201000300
- Versaevel Marie, Braquenier Jean-Baptiste, Riaz Maryam, Grevesse Thomas, Lantoine Joséphine, Gabriele Sylvain, Super-resolution microscopy reveals LINC complex recruitment at nuclear indentation sites, 10.1038/srep07362
- Pollard Thomas D, Borisy Gary G, Cellular Motility Driven by Assembly and Disassembly of Actin Filaments, 10.1016/s0092-8674(03)00120-x
- Mseka Tayamika, Cramer Louise P., Actin Depolymerization-Based Force Retracts the Cell Rear in Polarizing and Migrating Cells, 10.1016/j.cub.2011.11.006
- Alexandrova Antonina Y., Arnold Katya, Schaub Sébastien, Vasiliev Jury M., Meister Jean-Jacques, Bershadsky Alexander D., Verkhovsky Alexander B., Comparative Dynamics of Retrograde Actin Flow and Focal Adhesions: Formation of Nascent Adhesions Triggers Transition from Fast to Slow Flow, 10.1371/journal.pone.0003234
- Palecek Sean P., Loftus Joseph C., Ginsberg Mark H., Lauffenburger Douglas A., Horwitz Alan F., Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness, 10.1038/385537a0
- Yam Patricia T., Wilson Cyrus A., Ji Lin, Hebert Benedict, Barnhart Erin L., Dye Natalie A., Wiseman Paul W., Danuser Gaudenz, Theriot Julie A., Actin–myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility, 10.1083/jcb.200706012
- Fournier Maxime F., Sauser Roger, Ambrosi Davide, Meister Jean-Jacques, Verkhovsky Alexander B., Force transmission in migrating cells, 10.1083/jcb.200906139
- Parsons J. Thomas, Horwitz Alan Rick, Schwartz Martin A., Cell adhesion: integrating cytoskeletal dynamics and cellular tension, 10.1038/nrm2957
- Pelham R. J., Wang Y.-l., Cell locomotion and focal adhesions are regulated by substrate flexibility, 10.1073/pnas.94.25.13661
- Riveline Daniel, Zamir Eli, Balaban Nathalie Q., Schwarz Ulrich S., Ishizaki Toshimasa, Narumiya Shuh, Kam Zvi, Geiger Benjamin, Bershadsky Alexander D., Focal Contacts as Mechanosensors : Externally Applied Local Mechanical Force Induces Growth of Focal Contacts by an Mdia1-Dependent and Rock-Independent Mechanism, 10.1083/jcb.153.6.1175
- Cox Elisabeth A., Huttenlocher Anna, Regulation of integrin-mediated adhesion during cell migration, 10.1002/(sici)1097-0029(19981201)43:5<412::aid-jemt7>3.0.co;2-f
- Heidemann Steven R., Buxbaum Robert E., Cell Crawling: First the Motor, Now the Transmission, 10.1083/jcb.141.1.1
- Chan C. E., Odde D. J., Traction Dynamics of Filopodia on Compliant Substrates, 10.1126/science.1163595
- Moore Simon W., Roca-Cusachs Pere, Sheetz Michael P., Stretchy Proteins on Stretchy Substrates: The Important Elements of Integrin-Mediated Rigidity Sensing, 10.1016/j.devcel.2010.07.018
- Roca-Cusachs P., del Rio A., Puklin-Faucher E., Gauthier N. C., Biais N., Sheetz M. P., Integrin-dependent force transmission to the extracellular matrix by -actinin triggers adhesion maturation, 10.1073/pnas.1220723110
- Shafaq-Zadah Massiullah, Gomes-Santos Carina S., Bardin Sabine, Maiuri Paolo, Maurin Mathieu, Iranzo Julian, Gautreau Alexis, Lamaze Christophe, Caswell Patrick, Goud Bruno, Johannes Ludger, Persistent cell migration and adhesion rely on retrograde transport of β1 integrin, 10.1038/ncb3287
- Roca-Cusachs P., Gauthier N. C., del Rio A., Sheetz M. P., Clustering of 5 1 integrins determines adhesion strength whereas v 3 and talin enable mechanotransduction, 10.1073/pnas.0902818106
- Jiang Xue, Georges Penelope C., Li Baogang, Du Yangzhou, Kutzing Melinda K., Previtera Michelle L., Langrana Noshir A., Firestein Bonnie L., Cell Growth in Response to Mechanical Stiffness is Affected by Neuron- Astroglia Interactions, 10.2174/1874082000701010007
- Versaevel Marie, Riaz Maryam, Grevesse Thomas, Gabriele Sylvain, Cell confinement: putting the squeeze on the nucleus, 10.1039/c3sm00147d
- Lin Grace L., Cohen Daniel M., Desai Ravi A., Breckenridge Mark T., Gao Lin, Humphries Martin J., Chen Christopher S., Activation of beta 1 but not beta 3 integrin increases cell traction forces, 10.1016/j.febslet.2013.01.068
- Lieber Arnon D., Yehudai-Resheff Shlomit, Barnhart Erin L., Theriot Julie A., Keren Kinneret, Membrane Tension in Rapidly Moving Cells Is Determined by Cytoskeletal Forces, 10.1016/j.cub.2013.05.063
Bibliographic reference |
Riaz, Maryam ; Versaevel, Marie ; Mohammed, Danahe ; Glinel, Karine ; Gabriele, Sylvain. Persistence of fan-shaped keratocytes is a matrix-rigidity-dependent mechanism that requires α5β1 integrin engagement. In: Scientific Reports, Vol. 6, p. 34141 (2016) |
Permanent URL |
http://hdl.handle.net/2078.1/179062 |