A FAK-Cas-Rac-lamellipodin signaling module transduces extracellular matrix stiffness into mechanosensitive cell cycling

Science Signaling

Volumn 7, Issue 330, 2014, Pages

  Bae, Yong Ho ^a   Mui, Keeley L ^a   Hsu, Bernadette Y ^a   Liu, Shu Lin ^a   Cretu, Alexandra ^a   Razinia, Ziba ^a   Xu, Tina ^a   Puré, Ellen ^b   Assoian, Richard K ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CELL CYCLE PROTEIN; CYCLIN D1; FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATASE; RAC PROTEIN; CARRIER PROTEIN; CRK ASSOCIATED SUBSTRATE PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CELL FUNCTION; CELL MIGRATION; CYTOSKELETON; EMBRYO; EXTRACELLULAR MATRIX; LAMELLIPODIUM; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RIGIDITY; ANIMAL; CELL CYCLE; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; CELL CYCLE; CRK-ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION PROTEIN-TYROSINE KINASES; MECHANOTRANSDUCTION, CELLULAR; MICE; SIGNAL TRANSDUCTION;

EID: 84903168767     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004838     Document Type: Article

References (71)

1. R. J. Pelham Jr., Y.-L. Wang, Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. U.S.A. 94, 13661-13665 (1997).
2. M. Paszek, V. Weaver, The tension mounts: Mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia 9, 325-342 (2004).
3. A. J. Engler, S. Sen, H. L. Sweeney, D. E. Discher, Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
4. P. P. Provenzano, D. R. Inman, K. W. Eliceiri, P. J. Keely, Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28, 4326-4343 (2009).
5. D. Kothapalli, S.-L. Liu, Y. H. Bae, J. Monslow, T. Xu, E. A. Hawthorne, F. J. Byfield, P. Castagnino, S. Rao, D. J. Rader, E. Puré, M. C. Phillips, S. Lund-Katz, P. A. Janmey, R. K. Assoian, Cardiovascular protection by ApoE and ApoE-HDL linked to suppression of ECM gene expression and arterial stiffening. Cell Rep. 2, 1259-1271 (2012).
6. J. Schrader, T. T. Gordon-Walker, R. L. Aucott, M. van Deemter, A. Quaas, S. Walsh, D. Benten, S. J. Forbes, R. G.Wells, J. P. Iredale, Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53, 1192-1205 (2011).
7. M. J. Paszek, N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, V. M.Weaver, Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 (2005).
8. K. A. Owen, M. Y. Abshire, R. W. Tilghman, J. E. Casanova, A. H. Bouton, FAK regulates intestinal epithelial cell survival and proliferation during mucosal wound healing. PLOS One 6, e23123 (2011).
9. D. T. Butcher, T. Alliston, V. M. Weaver, A tense situation: Forcing tumour progression. Nat. Rev. Cancer 9, 108-122 (2009).
10. 1 function. Science 323, 642-644 (2009).
11. T. Yeung, P. C. Georges, L. A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W. Ming, V. Weaver, P. A. Janmey, Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34 (2005).
12. K. Burridge, E. S. Wittchen, The tension mounts: Stress fibers as force-generating mechanotransducers. J. Cell Biol. 200, 9-19 (2013).
13. E. A. Klein, L. Yin, D. Kothapalli, P. Castagnino, F. J. Byfield, T. Xu, I. Levental, E. Hawthorne, P. A. Janmey, R. K. Assoian, Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr. Biol. 19, 1511-1518 (2009).
14. S. K. Sastry, K. Burridge, Focal adhesions: A nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell Res. 261, 25-36 (2000).
15. D. W. Dumbauld, T. T. Lee, A. Singh, J. Scrimgeour, C. A. Gersbach, E. A. Zamir, J. Fu, C. S. Chen, J. E. Curtis, S. W. Craig, A. J. García, How vinculin regulates force transmission. Proc. Natl. Acad. Sci. U.S.A. 110, 9788-9793 (2013).
16. B. Fabry, A. H. Klemm, S. Kienle, T. E. Schäffer, W. H. Goldmann, Focal adhesion kinase stabilizes the cytoskeleton. Biophys. J. 101, 2131-2138 (2011).
17. Y. Sawada, M. Tamada, B. J. Dubin-Thaler, O. Cherniavskaya, R. Sakai, S. Tanaka, M. P. Sheetz, Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127, 1015-1026 (2006).
18. C. Grashoff, B. D. Hoffman, M. D. Brenner, R. Zhou, M. Parsons, M. T. Yang, M. A. McLean, S. G. Sligar, C. S. Chen, T. Ha, M. A. Schwartz, Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010).
19. A. Kostic, M. P. Sheetz, Fibronectin rigidity response through Fyn and p130Cas recruitment to the leading edge. Mol. Biol. Cell 17, 2684-2695 (2006).
20. S. V. Plotnikov, A. M. Pasapera, B. Sabass, C. M. Waterman, Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513-1527 (2012).
21. B. D. Hoffman, C. Grashoff, M. A. Schwartz, Dynamic molecular processes mediate cellular mechanotransduction. Nature 475, 316-323 (2011).
22. A. M. Pasapera, I. C. Schneider, E. Rericha, D. D. Schlaepfer, C. M. Waterman, Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188, 877-890 (2010).
23. P. M. Fonseca, N.-Y. Shin, J. Brábek, L. Ryzhova, J. Wu, S. K. Hanks, Regulation and localization of CAS substrate domain tyrosine phosphorylation. Cell. Signal. 16, 621-629 (2004).
24. P. J. Ruest, N.-Y. Shin, T. R. Polte, X. Zhang, S. K. Hanks, Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21, 7641-7652 (2001).
25. P. Defilippi, P. Di Stefano, S. Cabodi, p130Cas: A versatile scaffold in signaling networks. Trends Cell Biol. 16, 257-263 (2006).
26. C. E. Turner, Paxillin and focal adhesion signalling. Nat. Cell Biol. 2, E231-E236 (2000).
27. FAK accompanies cell adhesion to extracellular matrix: A role in cytoskeletal assembly. J. Cell Biol. 119, 893-903 (1992).
28. M. C. Subauste, O. Pertz, E. D. Adamson, C. E. Turner, S. Junger, K. M. Hahn, Vinculin modulation of paxillin-FAK interactions regulates ERK to control survival and motility. J. Cell Biol. 165, 371-381 (2004).
29. C. Ballestrem, N. Erez, J. Kirchner, Z. Kam, A. Bershadsky, B. Geiger, Molecular mapping of tyrosine-phosphorylated proteins in focal adhesions using fluorescence resonance energy transfer. J. Cell Sci. 119, 866-875 (2006).
30. R. Janoštiak, O. Tolde, Z. Brùhová, M. Novotný, S. K. Hanks, D. Rösel, J. Brábek, Tyrosine phosphorylation within the SH3 domain regulates CAS subcellular localization, cell migration, and invasiveness. Mol. Biol. Cell 22, 4256-4267 (2011).
31. S. K. Mitra, D. D. Schlaepfer, Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516-523 (2006).
32. M. D. Schaller, J. D. Hildebrand, J. D. Shannon, J. W. Fox, R. R. Vines, J. T. Parsons, Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14, 1680-1688 (1994).
33. L. Kjøller, A. Hall, Rac mediates cytoskeletal rearrangements and increased cell motility induced by urokinase-type plasminogen activator receptor binding to vitronectin. J. Cell Biol. 152, 1145-1158 (2001).
34. L. Van Aelst, C. D'Souza-Schorey, Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322 (1997).
35. A. J. Ridley, A. Hall, The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399 (1992).
36. C. D. Nobes, A. Hall, Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62 (1995).
37. A. Hall, Rho GTPases and the actin cytoskeleton. Science 279, 509-514 (1998).
38. S. M. Schoenwaelder, K. Burridge, Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 11, 274-286 (1999).
39. S. Y. Cho, R. L. Klemke, Purification of pseudopodia from polarized cells reveals redistribution and activation of Rac through assembly of a CAS/Crk scaffold. J. Cell Biol. 156, 725-736 (2002).
40. E. Kiyokawa, Y. Hashimoto, S. Kobayashi, H. Sugimura, T. Kurata, M. Matsuda, Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12, 3331-3336 (1998).
41. D. A. Hsia, S. K. Mitra, C. R. Hauck, D. N. Streblow, J. A. Nelson, D. Ilic, S. Huang, E. Li, G. R. Nemerow, J. Leng, K. S. R. Spencer, D. A. Cheresh, D. D. Schlaepfer, Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 160, 753-767 (2003).
42. E. A. Klein, L. E. Campbell, D. Kothapalli, A. K. Fournier, R. K. Assoian, Joint requirement for Rac and ERK activities underlies the mid-G1 phase induction of cyclin d1 and S phase entry in both epithelial and mesenchymal cells. J. Biol. Chem. 283, 30911-30918 (2008).
43. R. K. Assoian, M. A. Schwartz, Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11, 48-53 (2001).
44. D. Joyce, B. Bouzahzah, M. Fu, C. Albanese, M. D'Amico, J. Steer, J. U. Klein, R. J. Lee, J. E. Segall, J. K. Westwick, C. J. Der, R. G. Pestell, Integration of Rac-dependent regulation of cyclin D1 transcription through a nuclear factor-kB-dependent pathway. J. Biol. Chem. 274, 25245-25249 (1999).
45. M. R. Bubb, I. Spector, B. B. Beyer, K. M. Fosen, Effects of jasplakinolide on the kinetics of actin polymerization: An explanation for certain in vivo observations. J. Biol. Chem. 275, 5163-5170 (2000).
46. J. Thyberg, K. Blomgren, J. Roy, P. K. Tran, U. Hedin, Phenotypic modulation of smooth muscle cells after arterial injury is associated with changes in the distribution of laminin and fibronectin. J. Histochem. Cytochem. 45, 837-846 (1997).
47. J. Thyberg, U. Hedin, M. Sjölund, L. Palmberg, B. A. Bottger, Regulation of differentiated properties and proliferation of arterial smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 10, 966-990 (1990).
48. M. Krause, J. D. Leslie, M. Stewart, E. M. Lafuente, F. Valderrama, R. Jagannathan, G. A. Strasser, D. A. Rubinson, H. Liu, M. Way, M. B. Yaffe, V. A. Boussiotis, F. B. Gertler, Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571-583 (2004).
49. M. Krause, E. W. Dent, J. E. Bear, J. J. Loureiro, F. B. Gertler, Ena/VASP proteins: Regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541-564 (2003).
50. Y. H. Bae, Z. Ding, L. Zou, A. Wells, F. Gertler, P. Roy, Loss of profilin-1 expression enhances breast cancer cell motility by Ena/VASP proteins. J. Cell. Physiol. 219, 354-364 (2009).
51. A.-L. Law, A. Vehlow, M. Kotini, L. Dodgson, D. Soong, E. Theveneau, C. Bodo, E. Taylor, C. Navarro, U. Perera, M. Michael, G. A. Dunn, D. Bennett, R. Mayor, M. Krause, Lamellipodin and the Scar/WAVE complex cooperate to promote cell migration in vivo. J. Cell Biol. 203, 673-689 (2013).
52. R. H. Insall, L. M. Machesky, Actin dynamics at the leading edge: From simple machinery to complex networks. Dev. Cell 17, 310-322 (2009).
53. K. G. Campellone, M. D. Welch, A nucleator arms race: Cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251 (2010).
54. Y. Chen, A. M. Pasapera, A. P. Koretsky, C. M. Waterman, Orientation-specific responses to sustained uniaxial stretching in focal adhesion growth and turnover. Proc. Natl. Acad. Sci. U.S.A. 110, E2352-E2361 (2013).
55. J. D. Hildebrand, J. M. Taylor, J. T. Parsons, An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol. Cell. Biol. 16, 3169-3178 (1996).
56. B. Cen, A. Selvaraj, R. C. Burgess, J. K. Hitzler, Z. Ma, S. W. Morris, R. Prywes, Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol. Cell. Biol. 23, 6597-6608 (2003).
57. F. Miralles, G. Posern, A.-I. Zaromytidou, R. Treisman, Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342 (2003).
58. C. Baarlink, H. Wang, R. Grosse, Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 340, 864-867 (2013).
59. S. Medjkane, C. Perez-Sanchez, C. Gaggioli, E. Sahai, R. Treisman, Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol. 11, 257-268 (2009).
60. E. Lyulcheva, E. Taylor, M. Michael, A. Vehlow, S. Tan, A. Fletcher, M. Krause, D. Bennett, Drosophila pico and its mammalian ortholog lamellipodin activate serum response factor and promote cell proliferation. Dev. Cell 15, 680-690 (2008).
61. S. Dupont, L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, N. Elvassore, S. Piccolo, Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011).
62. M. Aragona, T. Panciera, A. Manfrin, S. Giulitti, F. Michielin, N. Elvassore, S. Dupont, S. Piccolo, A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059 (2013).
63. E. A. Klein, Y. Yung, P. Castagnino, D. Kothapalli, R. K. Assoian, in Methods in Enzymology, A. C. David, Ed. (Academic Press, New York, 2007), vol. 426, pp. 155-175.
64. C. A. Cuff, D. Kothapalli, I. Azonobi, S. Chun, Y. Zhang, R. Belkin, C. Yeh, A. Secreto, R. K. Assoian, D. J. Rader, E. Puré, The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation. J. Clin. Invest. 108, 1031-1040 (2001).
65. J. K. Slack-Davis, K. H. Martin, R. W. Tilghman, M. Iwanicki, E. J. Ung, C. Autry, M. J. Luzzio, B. Cooper, J. C. Kath, W. G. Roberts, J. T. Parsons, Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem. 282, 14845-14852 (2007).
66. Y. Gao, J. B. Dickerson, F. Guo, J. Zheng, Y. Zheng, Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. U.S.A. 101, 7618-7623 (2004).
67. A. Cretu, P. Castagnino, R. Assoian, Studying the effects of matrix stiffness on cellular function using acrylamide-based hydrogels. J. Vis. Exp. e2089 (2010).
68. J. Domke, M. Radmacher, Measuring the elastic properties of thin polymer films with the atomic force microscope. Langmuir 14, 3320-3325 (1998).
69. A. Wirth, Z. Benyó, M. Lukasova, B. Leutgeb, N. Wettschureck, S. Gorbey, P. Orsy, B. Horváth, C. Maser-Gluth, E. Greiner, B. Lemmer, G. Schütz, J. S. Gutkind, S. Offermanns, G12-G13-LARG-mediated signaling in vascular smooth muscle is required for saltinduced hypertension. Nat. Med. 14, 64-68 (2008).
70. D. Kothapalli, L. Zhao, E. A. Hawthorne, Y. Cheng, E. Lee, E. Puré, R. K. Assoian, Hyaluronan and CD44 antagonize mitogen-dependent cyclin D1 expression in mesenchymal cells. J. Cell Biol. 176, 535-544 (2007).
71. P. Castagnino, D. Kothapalli, E. A. Hawthorne, S.-L. Liu, T. Xu, S. Rao, Y. Yung, R. K. Assoian, miR-221/222 compensates for Skp2-mediated p27 degradation and is a primary target of cell cycle regulation by prostacyclin and cAMP. PLOS One 8, e56140 (2013).