Matrix stiffness reverses the effect of actomyosin tension on cell proliferation

Journal of Cell Science

Volumn 125, Issue 24, 2012, Pages 5974-5983

  Mih, Justin D ^a   Marinkovic, Aleksandar ^a   Liu, Fei ^a   Sharif, Asma S ^a   Tschumperlin, Daniel J ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Actomyosin tension; Cell proliferation; Matrix stiffness

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; AMIDE; BLEBBISTATIN; CANTHARIDIN; FUSED HETEROCYCLIC RINGS; PYRIDINE DERIVATIVE;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL GROWTH; CELL PROLIFERATION; CELL TYPE; CELLULAR PARAMETERS; ENZYME INHIBITION; EXTRACELLULAR MATRIX; GENE SILENCING; HUMAN; MATRIX STIFFNESS; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; 3T3 CELL LINE; ACTIN FILAMENT; ANIMAL; CELL ADHESION; CYTOLOGY; DOG; DRUG EFFECTS; FIBROBLAST; MDCK CELL LINE; MESENCHYMAL STROMA CELL; METABOLISM; MOUSE; PHYSIOLOGY; RAT; TUMOR CELL LINE;

ACTIN CYTOSKELETON; ACTOMYOSIN; AMIDES; ANIMALS; CANTHARIDIN; CELL ADHESION; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; DOGS; EXTRACELLULAR MATRIX; FIBROBLASTS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MESENCHYMAL STROMAL CELLS; MICE; NIH 3T3 CELLS; PYRIDINES; RATS;

EID: 84875580590     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.108886     Document Type: Article

References (55)

1. Aratyn-Schaus, Y. and Gardel, M. L. (2010). Transient frictional slip between integrin and the ECM in focal adhesions under myosin II tension. Curr. Biol. 20, 1145-1153.
2. Assoian, R. K. and Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends Cell Biol. 18, 347-352.
3. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., Mahalu, D., Safran, S., Bershadsky, A., Addadi, L. et al. (2001). Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472.
4. Butcher, D. T., Alliston, T. and Weaver, V. M. (2009). A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122.
5. Butler, J. P., Tolić-Nørrelykke, I. M., Fabry, B. and Fredberg, J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282, C595-C605.
6. Cai, Y., Biais, N., Giannone, G., Tanase, M., Jiang, G., Hofman, J. M., Wiggins, C. H., Silberzan, P., Buguin, A., Ladoux, B. et al. (2006). Nonmuscle myosin IIAdependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91, 3907-3920.
7. Califano, J. P. and Reinhart-King, C. A. (2010). Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell Mol. Bioeng. 3, 68-75.
8. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. and Ingber, D. E. (1997). Geometric control of cell life and death. Science 276, 1425-1428.
9. Chicurel, M. E., Chen, C. S. and Ingber, D. E. (1998). Cellular control lies in the balance of forces. Curr. Opin. Cell Biol. 10, 232-239.
10. Chowdhury, F., Li, Y., Poh, Y. C., Yokohama-Tamaki, T., Wang, N. and Tanaka, T. S. (2010). Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS ONE 5, e15655.
11. Discher, D. E., Janmey, P. and Wang, Y. L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143.
12. Dugina, V., Fontao, L., Chaponnier, C., Vasiliev, J. and Gabbiani, G. (2001). Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. J. Cell Sci. 114, 3285-3296.
13. Folkman, J. and Moscona, A. (1978). Role of cell shape in growth control. Nature 273, 345-349.
14. Fringer, J. and Grinnell, F. (2001). Fibroblast quiescence in floating or released collagen matrices: contribution of the ERK signaling pathway and actin cytoskeletal organization. J. Biol. Chem. 276, 31047-31052.
15. Fu, J., Wang, Y. K., Yang, M. T., Desai, R. A., Yu, X., Liu, Z. and Chen, C. S. (2010). Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods 7, 733-736.
16. Galbraith, C. G., Yamada, K. M. and Sheetz, M. P. (2002). The relationship between force and focal complex development. J. Cell Biol. 159, 695-705.
17. Geiger, B., Spatz, J. P. and Bershadsky, A. D. (2009). Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33.
18. Georges, P. C. and Janmey, P. A. (2005). Cell type-specific response to growth on soft materials. J. Appl. Physiol. 98, 1547-1553.
19. Ghosh, K., Pan, Z., Guan, E., Ge, S., Liu, Y., Nakamura, T., Ren, X. D., Rafailovich, M. and Clark, R. A. (2007). Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials 28, 671-679.
20. Grinnell, F., Ho, C. H., Tamariz, E., Lee, D. J. and Skuta, G. (2003). Dendritic fibroblasts in three-dimensional collagen matrices. Mol. Biol. Cell 14, 384-395.
21. Guilak, F., Cohen, D. M., Estes, B. T., Gimble, J. M., Liedtke, W. and Chen, C. S. (2009). Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17-26.
22. 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, 2213-2220.
23. Hotulainen, P. and Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173, 383-394.
24. Huang, S., Chen, C. S. and Ingber, D. E. (1998). Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol. Biol. Cell 9, 3179-3193.
25. Huang, S. and Ingber, D. E. (1999). The structural and mechanical complexity of cellgrowth control. Nat. Cell Biol. 1, E131-E138.
26. Klein, E. A., Yin, L., Kothapalli, D., Castagnino, P., Byfield, F. J., Xu, T., Levental, I., Hawthorne, E., Janmey, P. A. and Assoian, R. K. (2009). Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr. Biol. 19, 1511-1518.
27. Knapp, J., Bokník, P., Huke, S., Lüss, H., Müller, F. U., Müller, T., Nacke, P., Schmitz, W., Vahlensieck, U. and Neumann, J. (1998). The mechanism of action of cantharidin in smooth muscle. Br. J. Pharmacol. 123, 911-919.
28. Kong, H. J., Polte, T. R., Alsberg, E. and Mooney, D. J. (2005). FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc. Natl. Acad. Sci. USA 102, 4300-4305.
29. Kuo, J. C., Han, X., Hsiao, C. T., Yates, J. R., 3rd and Waterman, C. M. (2011). Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for b-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13, 383-393.
30. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W. et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
31. Liu, F., Mih, J. D., Shea, B. S., Kho, A. T., Sharif, A. S., Tager, A. M. and Tschumperlin, D. J. (2010). Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J. Cell Biol. 190, 693-706.
32. Lo, C. M., Wang, H. B., Dembo, M. and Wang, Y. L. (2000). Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152.
33. Mammoto, A., Huang, S., Moore, K., Oh, P. and Ingber, D. E. (2004). Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. J. Biol. Chem. 279, 26323-26330.
34. Mammoto, A. and Ingber, D. E. (2009). Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 21, 864-870.
35. Marinković, A., Mih, J. D., Park, J. A., Liu, F. and Tschumperlin, D. J. (2012). Improved throughput traction microscopy reveals pivotal role for matrix stiffness in fibroblast contractility and TGF-β responsiveness. Am. J. Physiol. Lung Cell. Mol. Physiol. 303, L169-L180.
36. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. and Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495.
37. Mih, J. D., Sharif, A. S., Liu, F., Marinkovic, A., Symer, M. M. and Tschumperlin, D. J. (2011). A multiwell platform for studying stiffness-dependent cell biology. PLoS ONE 6, e19929.
38. Moore, S. W., Roca-Cusachs, P. and Sheetz, M. P. (2010). Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev. Cell 19, 194-206.
39. Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A. and Horwitz, A. F. (1997). Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385, 537-540.
40. Pasapera, A. M., Schneider, I. C., Rericha, E., Schlaepfer, D. D. and Waterman, C. M. (2010). Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188, 877-890.
41. 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. et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254.
42. 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, 1195-1205.
43. Rhee, S., Jiang, H., Ho, C. H. and Grinnell, F. (2007). Microtubule function in fibroblast spreading is modulated according to the tension state of cell-matrix interactions. Proc. Natl. Acad. Sci. USA 104, 5425-5430.
44. Roca-Cusachs, P., Alcaraz, J., Sunyer, R., Samitier, J., Farré, R. and Navajas, D. (2008). Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation. Biophys. J. 94, 4984-4995.
45. Saez, A., Buguin, A., Silberzan, P. and Ladoux, B. (2005). Is the mechanical activity of epithelial cells controlled by deformations or forces. Biophys. J. 89, L52-L54.
46. Shin, J. W., Swift, J., Spinler, K. R. and Discher, D. E. (2011). Myosin-II inhibition and soft 2D matrix maximize multinucleation and cellular projections typical of platelet-producing megakaryocytes. Proc. Natl. Acad. Sci. USA 108, 11458-11463.
47. Solon, J., Levental, I., Sengupta, K., Georges, P. C. and Janmey, P. A. (2007). Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93, 4453-4461.
48. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R. and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299, 1743-1747.
49. Tilghman, R. W., Cowan, C. R., Mih, J. D., Koryakina, Y., Gioeli, D., Slack-Davis, J. K., Blackman, B. R., Tschumperlin, D. J. and Parsons, J. T. (2010). Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS ONE 5, e12905.
50. Tolić-Nørrelykke, I. M. and Wang, N. (2005). Traction in smooth muscle cells varies with cell spreading. J. Biomech. 38, 1405-1412.
51. Tolić-Nørrelykke, I. M., Butler, J. P., Chen, J. and Wang, N. (2002). Spatial and temporal traction response in human airway smooth muscle cells. Am. J. Physiol., Cell Physiol. 283. doi: 10.1152/ajpcell.00169.2002
52. Ulrich, T. A., de Juan Pardo, E. M. and Kumar, S. (2009). The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 69, 4167-4174.
53. Wang, N., Ostuni, E., Whitesides, G. M. and Ingber, D. E. (2002). Micropatterning tractional forces in living cells. Cell Motil. Cytoskeleton 52, 97-106.
54. Wozniak, M. A. and Chen, C. S. (2009). Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell Biol. 10, 34-43.
55. Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J. and Keely, P. J. (2003). ROCKgenerated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163, 583-595.