Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics

Journal of Cell Biology

Volumn 176, Issue 5, 2007, Pages 667-680

  Schober, Markus ^a   Raghavan, Srikala ^a,c   Nikolova, Maria ^a   Polak, Lisa ^a   Pasolli, H Amalia ^a   Beggs, Hilary E ^b   Reichardt, Louis F ^b   Fuchs, Elaine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA1 INTEGRIN; FOCAL ADHESION KINASE; MYOSIN LIGHT CHAIN KINASE; PROTEIN TYROSINE KINASE; RHO FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSKELETON; KERATINOCYTE; MEMBRANE FORMATION; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL DETECTION;

ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CELL SHAPE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; FOCAL ADHESION KINASE 2; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GTPASE-ACTIVATING PROTEINS; KERATINOCYTES; MICE; MICROFILAMENTS; MICROTUBULES; PHOSPHORYLATION; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 33847413148     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200608010     Document Type: Article

References (75)

1. Arthur, W.T., and K. Burridge. 2001. RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell. 12:2711-2720.
2. Arthur, W.T., L.A. Petch, and K. Burridge. 2000. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10:719-722.
3. Astier, A., H. Avraham, S.N. Manie, J. Groopman, T. Canty, S. Avraham, and A.S. Freedman. 1997. The related adhesion focal tyrosine kinase is tyrosine-phosphorylated after beta1-integrin stimulation in B cells and binds to p130cas. J. Biol. Chem. 272:228-232.
4. Avizienyte, E., A.W. Wyke, R.J. Jones, G.W. McLean, M.A. Westhoff, V.G. Brunton, and M.C. Frame. 2002. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat. Cell Biol. 4:632-638.
5. Beggs, H.E., D. Schahin-Reed, K. Zang, S. Goebbels, K.A. Nave, J. Gorski, K.R. Jones, D. Sretavan, and L.F. Reichardt. 2003. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron. 40:501-514.
6. Bershadsky, A., A. Chausovsky, E. Becker, A. Lyubimova, and B. Geiger. 1996. Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr. Biol. 6:1279-1289.
7. Bhatt, A., I. Kaverina, C. Otey, and A. Huttenlocher. 2002. Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115:3415-3425.
8. Billuart, P., C.G. Winter, A. Maresh, X. Zhao, and L. Luo. 2001. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell. 107:195-207.
9. Brakebusch, C., R. Grose, F. Quondamatteo, A. Ramirez, J.L. Jorcano, A. Pirro, M. Svensson, R. Herken, T. Sasaki, R. Timpl, et al. 2000. Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J. 19:3990-4003.
10. Braren, R., H. Hu, Y.H. Kim, H.E. Beggs, L.F. Reichardt, and R. Wang. 2006. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol. 172:151-162.
11. Brouns, M.R., S.F. Matheson, and J. Settleman. 2001. p190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat. Cell Biol. 3:361-367.
12. Brown, M.C., L.A. Cary, J.S. Jamieson, J.A. Cooper, and C.E. Turner. 2005. Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol. Biol. Cell. 16:4316-4328.
13. Chen, L.M., D. Bailey, and C. Fernandez-Valle. 2000. Association of beta 1 integrin with focal adhesion kinase and paxillin in differentiating Schwann cells. J. Neurosci. 20:3776-3784.
14. Chrzanowska-Wodnicka, M., and K. Burridge. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133:1403-1415.
15. DiPersio, C.M., K.M. Hodivala-Dilke, R. Jaenisch, J.A. Kreidberg, and R.O. Hynes. 1997. α3β1 integrin is required for normal development of the epidermal basement membrane. J. Cell Biol. 137:729-742.
16. Dowling, J., Q.C. Yu, and E. Fuchs. 1996. β4 integrin is required for hemi-desmosome formation, cell adhesion and cell survival. J. Cell Biol. 134:559-572.
17. Dumenil, G., P. Sansonetti, and G. Tran Van Nhieu. 2000. Src tyrosine kinase activity down-regulates Rho-dependent responses during Shigella entry into epithelial cells and stress fibre formation. J. Cell Sci. 113:71-80.
18. Essayem, S., B. Kovacic-Milivojevic, C. Baumbusch, S. McDonagh, G. Dolganov, K. Howerton, N. Larocque, T. Mauro, A. Ramirez, D.M. Ramos, et al. 2006. Hair cycle and wound healing in mice with a keratinocyte-restricted deletion of FAK. Oncogene. 25:1081-1089.
19. Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature. 420:629-635.
20. Ezratty, E.J., M.A. Partridge, and G.G. Gundersen. 2005. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7:581-590.
21. Fincham, V.J., A. Chudleigh, and M.C. Frame. 1999. Regulation of p190 Rho-GAP by v-Src is linked to cytoskeletal disruption during transformation. J. Cell Sci. 112:947-956.
22. Frost, J.A., A. Khokhlatchev, S. Stippec, M.A. White, and M.H. Cobb. 1998. Differential effects of PAK1-activating mutations reveal activity-dependent and -independent effects on cytoskeletal regulation. J. Biol. Chem. 273:28191-28198.
23. Fuchs, E., and S. Raghavan. 2002. Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 3:199-209.
24. Fuchs, E., J. Dowling, J. Segre, S.H. Lo, and Q.C. Yu. 1997. Integrators of epidermal growth and differentiation: distinct functions for beta 1 and beta 4 integrins. Curr. Opin. Genet. Dev. 7:672-682.
25. Georges-Labouesse, E., N. Messaddeq, G. Yehia, L. Cadalbert, A. Dierich, and M. Le Meur. 1996. Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat. Genet. 13:370-373.
26. Giancotti, F.G., and G. Tarone. 2003. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu. Rev. Cell Dev. Biol. 19:173-206.
27. Gismondi, A., L. Bisogno, F. Mainiero, G. Palmieri, M. Piccoli, L. Frati, and A. Santoni. 1997. Proline-rich tyrosine kinase-2 activation by beta 1 integrin fibronectin receptor cross-linking and association with paxillin in human natural killer cells. J. Immunol. 159:4729-4736.
28. Grabbe, C., C.G. Zervas, T. Hunter, N.H. Brown, and R.H. Palmer. 2004. Focal adhesion kinase is not required for integrin function or viability in Drosophila. Development. 131:5795-5805.
29. Grose, R., C. Hutter, W. Bloch, I. Thorey, F.M. Watt, R. Fassler, C. Brakebusch, and S. Werner. 2002. A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development. 129:2303-2315.
30. Gupton, S.L., and C.M. Waterman-Storer. 2006. Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell. 125:1361-1374.
31. Hannigan, G.E., C. Leung-Hagesteijn, L. Fitz-Gibbon, M.G. Coppolino, G. Radeva, J. Filmus, J.C. Bell, and S. Dedhar. 1996. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature. 379:91-96.
32. Hannigan, G., A.A. Troussard, and S. Dedhar. 2005. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat. Rev. Cancer. 5:51-63.
33. Holinstat, M., N. Knezevic, M. Broman, A.M. Samarel, A.B. Malik, and D. Mehta. 2006. Suppression of RhoA activity by focal adhesion kinase-induced activation of p190RhoGAP: role in regulation of endothelial permeability. J. Biol. Chem. 281:2296-2305.
34. Hsia, D.A., S.K. Mitra, C.R. Hauck, D.N. Streblow, J.A. Nelson, D. Ilic, S. Huang, E. Li, G.R. Nemerow, J. Leng, et al. 2003. Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 160:753-767.
35. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687.
36. Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 377:539-544.
37. Janes, S.M., and F.M. Watt. 2006. New roles for integrins in squamous-cell carcinoma. Nat. Rev. Cancer. 6:175-183.
38. Kaverina, I., K. Rottner, and J.V. Small. 1998. Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 142:181-190.
39. Kaverina, I., O. Krylyshkina, and J.V. Small. 1999. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146:1033-1044.
40. Kaverina, I., O. Krylyshkina, and J.V. Small. 2002. Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34:746-761.
41. Kodama, A., I. Karakesisoglou, E. Wong, A. Vaezi, and E. Fuchs. 2003. ACF7: an essential integrator of microtubule dynamics. Cell. 115:343-354.
42. Legate, K.R., E. Montanez, O. Kudlacek, and R. Fassler. 2006. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7:20-31.
43. Manser, E., H.Y. Huang, T.H. Loo, X.Q. Chen, J.M. Dong, T. Leung, and L. Lim. 1997. Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17:1129-1143.
44. Manser, E., T.H. Loo, C.G. Koh, Z.S. Zhao, X.Q. Chen, L. Tan, I. Tan, T. Leung, and L. Lim. 1998. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell. 1:183-192.
45. Matsumura, F. 2005. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15:371-377.
46. McLean, G.W., K. Brown, M.I. Arbuckle, A.W. Wyke, T. Pikkarainen, E. Ruoslahti, and M.C. Frame. 2001. Decreased focal adhesion kinase suppresses papilloma formation during experimental mouse skin carcinogenesis. Cancer Res. 61:8385-8389.
47. McLean, G.W., N.H. Komiyama, B. Serrels, H. Asano, L. Reynolds, F. Conti, K. Hodivala-Dilke, D. Metzger, P. Chambon, S.G. Grant, and M.C. Frame. 2004. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev. 18:2998-3003.
48. McLean, G.W., N.O. Carragher, E. Avizienyte, J. Evans, V.G. Brunton, and M.C. Frame. 2005. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat. Rev. Cancer. 5:505-515.
49. Miranti, C.K., and J.S. Brugge. 2002. Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4:E83-E90.
50. Nayal, A., D.J. Webb, C.M. Brown, E.M. Schaefer, M. Vicente-Manzanares, and A.R. Horwitz. 2006. Paxillin phosphorylation at Ser273 localizes a GIT1-PIX-PAK complex and regulates adhesion and protrusion dynamics. J. Cell Biol. 173:587-589.
51. Owens, D.M., S. Broad, X. Yan, S.A. Benitah, and F.M. Watt. 2005. Suprabasal alpha 5 beta1 integrin expression stimulates formation of epidermal squamous cell carcinomas without disrupting TGFbeta signaling or inducing spindle cell tumors. Mol. Carcinog. 44:60-66.
52. Raghavan, S., C. Bauer, G. Mundschau, Q. Li, and E. Fuchs. 2000. Conditional ablation of β1 integrin in skin: severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell Biol. 150:1149-1160.
53. Raghavan, S., A. Vaezi, and E. Fuchs. 2003. A role for alphabeta1 integrins in focal adhesion function and polarized cytoskeletal dynamics. Dev. Cell. 5:415-427.
54. Ren, X.D., W.B. Kiosses, D.J. Sieg, C.A. Otey, D.D. Schlaepfer, and M.A. Schwartz. 2000. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113:3673-3678.
55. Rheinwald, J.G., and H. Green. 1977. Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature. 265:421-424.
56. Rodriguez, O.C., A.W. Schaefer, C.A. Mandato, P. Forscher, W.M. Bement, and C.M. Waterman-Storer. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5:599-609.
57. Sanders, L.C., F. Matsumura, G.M. Bokoch, and P. de Lanerolle. 1999. Inhibition of myosin light chain kinase by p21-activated kinase. Science. 283:2083-2085.
58. Schaller, M.D., J.D. Hildebrand, J.D. Shannon, J.W. Fox, R.R. Vines, and J.T. Parsons. 1994. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14:1680-1688.
59. Schaller, M.D., C.A. Otey, J.D. Hildebrand, and J.T. Parsons. 1995. Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domains. J. Cell Biol. 130:1181-1187.
60. Schwartz, M.A., and M.H. Ginsberg. 2002. Networks and crosstalk: integrin signalling spreads. Nat. Cell Biol. 4:E65-E68.
61. Shen, T.L., A.Y. Park, A. Alcaraz, X. Peng, I. Jang, P. Koni, R.A. Flavell, H. Gu, and J.L. Guan. 2005. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 169:941-952.
62. Small, J.V., B. Geiger, I. Kaverina, and A. Bershadsky. 2002. How do microtubules guide migrating cells? Nat. Rev. Mol. Cell Biol. 3:957-964.
63. Tilghman, R.W., J.K. Slack-Davis, N. Sergina, K.H. Martin, M. Iwanicki, E.D. Hershey, H.E. Beggs, L.F. Reichardt, and J.T. Parsons. 2005. Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J. Cell Sci. 118:2613-2623.
64. Tukey, J.W. 1977. Exploratory Data Analysis. Addison-Wesley, Reading, MA. 688 pp.
65. Turner, C.E., M.C. Brown, J.A. Perrotta, M.C. Riedy, S.N. Nikolopoulos, A.R. McDonald, S. Bagrodia, S. Thomas, and P.S. Leventhal. 1999. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell Biol. 145:851-863.
66. Vaezi, A., C. Bauer, V. Vasioukhin, and E. Fuchs. 2002. Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. Dev. Cell. 3:367-381.
67. van der Neut, R., P. Krimpenfort, J. Calafat, C.M. Niessen, and A. Sonnenberg. 1996. Epithelial detachment due to absence of hemidesmosomes in integrin beta 4 null mice. Nat. Genet. 13:366-369.
68. Vasioukhin, V., L. Degenstein, B. Wise, and E. Fuchs. 1999. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl. Acad. Sci. USA. 96:8551-8556.
69. Watt, F.M. 2002. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21:3919-3926.
70. Webb, D.J., K. Donais, L.A. Whitmore, S.M. Thomas, C.E. Turner, J.T. Parsons, and A.F. Horwitz. 2004. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6:154-161.
71. West, K.A., H. Zhang, M.C. Brown, S.N. Nikolopoulos, M.C. Riedy, A.F. Horwitz, and C.E. Turner. 2001. The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL). J. Cell Biol. 154:161-176.
72. Wilhelmsen, K., S.H. Litjens, and A. Sonnenberg. 2006. Multiple functions of the integrin alpha6beta4 in epidermal homeostasis and tumorigenesis. Mol. Cell. Biol. 26:2877-2886.
73. Wu, X., B. Gan, Y. Yoo, and J.L. Guan. 2005. FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev. Cell. 9:185-196.
74. Yano, H., Y. Mazaki, K. Kurokawa, S.K. Hanks, M. Matsuda, and H. Sabe. 2004. Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J. Cell Biol. 166:283-295.
75. Zhao, Z.S., E. Manser, T.H. Loo, and L. Lim. 2000. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20:6354-6363.