Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing

Nature Communications

Volumn 6, Issue , 2015, Pages

  Gupta, Mukund ^a   Sarangi, Bibhu Ranjan ^b   Deschamps, Joran ^b,g   Nematbakhsh, Yasaman ^c,d   Callan Jones, Andrew ^e   Margadant, Felix ^a   Mège, René Marc ^b   Lim, Chwee Teck ^a,c,d   Voituriez, Raphaël ^f   Ladoux, Benoît ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b INSTITUT JACQUES MONOD   (France)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e UNIVERSITÉ PARIS DIDEROT   (France)

^f CNRS   (France)

^g EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; CELLS AND CELL COMPONENTS; ENVIRONMENTAL STRESS; LABORATORY METHOD; PROTEIN; RHEOLOGY; RIGIDITY; SHAPE; STIFFNESS; SUBSTRATE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CYTOSKELETON; EXTRACELLULAR MATRIX; FLOW KINETICS; IN VITRO STUDY; LIQUID CRYSTAL; NONHUMAN; RAT; RIGIDITY; ANIMAL; ATOMIC FORCE MICROSCOPY; BIOLOGICAL MODEL; BIOMECHANICS; CYTOLOGY; FEEDER CELL; FIBROBLAST; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES;

ACTIN; BACTERIAL PROTEIN; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ACTINS; ANIMALS; BACTERIAL PROTEINS; BIOMECHANICAL PHENOMENA; CYTOSKELETON; FEEDER CELLS; FIBROBLASTS; LUMINESCENT PROTEINS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; RATS; RHEOLOGY;

EID: 84933050468     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8525     Document Type: Article

References (49)

1. Lo, C. M., Wang, H. B., Dembo, M., Wang, Y. L. & Wang, Y. L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152 (2000).
2. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
3. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and rhoa regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004).
4. Ulrich, T. A., de Juan Pardo, E. M. & Kumar, S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 69, 4167-4174 (2009).
5. Discher, D. E., Janmey, P. & Wang, Y. L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143 (2005).
6. Wozniak, M. A. & Chen, C. S. Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell Biol. 10, 34-43 (2009).
7. Jaalouk, D. E. & Lammerding, J. Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 10, 63-73 (2009).
8. Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 (2005).
9. Ladoux, B. & Nicolas, A. Physically based principles of cell adhesion mechanosensitivity in tissues. Rep. Prog. Phys. 75, 116601 (2012).
10. Balaban, N. Q. et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472 (2001).
11. Plotnikov, S. V., Pasapera, A. M., Sabass, B. & Waterman, C. M. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513-1527 (2012).
12. Hayakawa, K., Tatsumi, H. & Sokabe, M. Actin stress fibers transmit and focus force to activate mechanosensitive channels. J. Cell Sci. 121, 496-503 (2008).
13. Mitrossilis, D. et al. Single-cell response to stiffness exhibits muscle-like behavior. Proc. Natl Acad. Sci. USA 106, 18243-18248 (2009).
14. Colombelli, J. et al. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122, 1665-1679 (2009).
15. Hayakawa, K., Tatsumi, H. & Sokabe, M. Actin filaments function as a tension sensor by tension-dependent binding of cofilin to the filament. J. Cell Biol. 195, 721-727 (2011).
16. del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
17. Elosegui-Artola, A. et al. Rigidity sensing and adaptation through regulation of integrin types. Nat. Mater. 13, 631-637 (2014).
18. Plotnikov, S. V. & Waterman, C. M. Guiding cell migration by tugging. Curr. Opin. Cell Biol. 25, 619-626 (2013).
19. Stricker, J., Aratyn-Schaus, Y., Oakes, P. W. & Gardel, M. L. Spatiotemporal constraints on the force-dependent growth of focal adhesions. Biophys. J. 100, 2883-2893 (2011).
20. Trichet, L. et al. Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness. Proc. Natl Acad. Sci. USA 109, 6933-6938 (2012).
21. Walcott, S. & Sun, S. X. A mechanical model of actin stress fiber formation and substrate elasticity sensing in adherent cells. Proc. Natl Acad. Sci. USA 107, 7757-7762 (2010).
22. Kumar, S. et al. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys. J. 90, 3762-3773 (2006).
23. Wang, N., Tytell, J. D. & Ingber, D. E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82 (2009).
24. Schwarz, U. S. & Safran, S. A. Physics of adherent cells. Rev. Mod. Phys. 85, 1327-1381 (2013).
25. Prager-Khoutorsky, M. et al. Fibroblast polarization is a matrix-rigiditydependent process controlled by focal adhesion mechanosensing. Nat. Cell Biol. 13, 1457-1465 (2011).
26. Zemel, A., Rehfeldt, F., Brown, A. E., Discher, D. E. & Safran, S. A. Optimal matrix rigidity for stress fiber polarization in stem cells. Nat. Phys. 6, 468-473 (2010).
27. Friedrich, B. M. & Safran, S. A. Nematic order by elastic interactions and cellular rigidity sensing. Europhys. Lett. 93, 28007 (2011).
28. Solon, J., Levental, I., Sengupta, K., Georges, P. C. & Janmey, P. A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93, 4453-4461 (2007).
29. Pelham, R. J. & Wang, Y-l. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13661-13665 (1997).
30. Ghibaudo, M. et al. Traction forces and rigidity sensing regulate cell functions. Soft Matter 4, 1836-1843 (2008).
31. Lubensky, T. C., Mukhopadhyay, R., Radzihovsky, L. & Xing, X. Symmetries and elasticity of nematic gels. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 66, 011702 (2002).
32. Marchetti, M. et al. Hydrodynamics of soft active matter. Rev. Mod. Phys. 85, 1143 (2013).
33. Chaikin, P. M. & Lubensky, T. C. Principles of Condensed Matter Physics vol. 1 (Cambridge Univ. Press, 2000).
34. Engler, A. J. et al. Myotubes differentiate optimally on substrates with tissuelike stiffness pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887 (2004).
35. Kruse, K., Joanny, J., Jülicher, F., Prost, J. & Sekimoto, K. Asters, vortices, and rotating spirals in active gels of polar filaments. Phys. Rev. Lett. 92, 078101 (2004).
36. Kruse, K., Joanny, J. F., Julicher, F., Prost, J. & Sekimoto, K. Generic theory of active polar gels: a paradigm for cytoskeletal dynamics. Eur. Phys. J. E 16, 5-16 (2005).
37. Julicher, F., Kruse, K., Prost, J. & Joanny, J.-F. Active behavior of the cytoskeleton. Phys. Rep. 449, 3-28 (2007).
38. Salbreux, G., Prost, J. & Joanny, J. F. Hydrodynamics of cellular cortical flows and the formation of contractile rings. Phys. Rev. Lett. 103, 058102 (2009).
39. de Gennes, P. D. & Prost, J. The Physics of Liquid Crystals (Oxford Univ. Press, 1995).
40. Voituriez, R., Joanny, J.-F. & Prost, J. Spontaneous flow transition in active polar gels. Europhys. Lett. 70, 404 (2005).
41. Stolz, M. et al. Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nat. Nanotechnol. 4, 186-192 (2009).
42. Yeung, T. et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34 (2005).
43. Riveline, D. et al. Focal contacts as mechanosensors externally applied local mechanical force induces growth of focal contacts by an mdia1-dependent and rock-independent mechanism. J. Cell Biol. 153, 1175-1186 (2001).
44. Heil, P. & Spatz, J. P. Lateral shear forces applied to cells with single elastic micropillars to influence focal adhesion dynamics. J. Phys. Condens. Matter 22, 194108 (2010).
45. Medeiros, N. A., Burnette, D. T. & Forscher, P. Myosin ii functions in actinbundle turnover in neuronal growth cones. Nat. Cell Biol. 8, 216-226 (2006).
46. Plestant, C. et al. Adhesive interactions of n-cadherin limit the recruitment of microtubules to cell-cell contacts through organization of actomyosin. J. Cell Sci. 127, 1660-1671 (2014).
47. Ladoux, B. et al. Strength dependence of cadherin-mediated adhesions. Biophys. J. 98, 534-542 (2010).
48. Tse, J. R. & Engler, A. J. Preparation of hydrogel substrates with tunable mechanical properties. Curr. Protoc. Cell Biol. 10, 10-16 (2010).
49. Yi, J., Wu, X. S., Crites, T. & Hammer, J. A. Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells. Mol. Biol. Cell 23, 834-852 (2012).