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Journal of Cell Science, Vol 112, Issue 16 2677-2691, Copyright © 1999 by Company of Biologists
JOURNAL ARTICLES |
DJ Sieg, CR Hauck and DD Schlaepfer
The Scripps Research Institute, Department of Immunology, IMM26, La Jolla, CA 92037, USA.
FAK localizes to sites of transmembrane integrin receptor clustering and facilitates intracellular signaling events. FAK-null (FAK-) fibroblasts exhibit a rounded morphology, defects in cell migration, and an elevated number of cell-substratum contact sites. Here we show that stable re-expression of epitope-tagged FAK reversed the morphological defects of the FAK- cells through the dynamic regulation of actin structures and focal contact sites in fibronectin (FN) stimulated cells. FAK re-expressing fibroblasts (clones DA2 and DP3) exhibit a characteristic fibrillar shape and display indistinguishable FN receptor-stimulated migration properties compared to normal fibroblasts. Expression of various FAK mutants in the FAK- cells showed that FAK kinase activity, the Tyr-397/SH2 domain binding site, and the first proline-rich SH3 binding region in the FAK C-terminal domain were individually needed to promote full FAK-mediated FAK- cell migration to FN whereas direct paxillin binding to FAK was not required. Expression of the FAK Phe-397 mutant did not promote FAK- cell migration and overexpression of p50(csk) in DA2 cells inhibited migration to FN suggesting that Src-family PTKs play important roles in FAK-mediated motility events. Expression of the FAK C-terminal domain, FRNK, promoted FAK dephosphorylation at Tyr-397 and potently blocked FAK-mediated cell migration. This dominant-negative effect of FRNK was reversed by a point mutation (Leu-1034 to Ser) which prevented FRNK localization to focal contact sites. Our results show that FAK functions as a key regulator of fibronectin receptor stimulated cell migration events through the recruitment of both SH2 and SH3 domain-containing signaling proteins to sites of integrin receptor clustering.
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K. Moissoglu and I. H. Gelman v-Src Rescues Actin-based Cytoskeletal Architecture and Cell Motility and Induces Enhanced Anchorage Independence during Oncogenic Transformation of Focal Adhesion Kinase-null Fibroblasts J. Biol. Chem., November 28, 2003; 278(48): 47946 - 47959. [Abstract] [Full Text] [PDF]
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G. S. Goldberg, D. B. Alexander, P. Pellicena, Z.-Y. Zhang, H. Tsuda, and W. T. Miller Src Phosphorylates Cas on Tyrosine 253 to Promote Migration of Transformed Cells J. Biol. Chem., November 21, 2003; 278(47): 46533 - 46540. [Abstract] [Full Text] [PDF]
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Q. Ding, J. Stewart Jr., M. A. Olman, M. R. Klobe, and C. L. Gladson The Pattern of Enhancement of Src Kinase Activity on Platelet-derived Growth Factor Stimulation of Glioblastoma Cells Is Affected by the Integrin Engaged J. Biol. Chem., October 10, 2003; 278(41): 39882 - 39891. [Abstract] [Full Text] [PDF]
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 O. I. Stenina, S. Y. Desai, I. Krukovets, K. Kight, D. Janigro, E. J. Topol, and E. F. Plow Thrombospondin-4 and Its Variants: Expression and Differential Effects on Endothelial Cells Circulation, September 23, 2003; 108(12): 1514 - 1519. [Abstract] [Full Text] [PDF]
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M. Okigaki, C. Davis, M. Falasca, S. Harroch, D. P. Felsenfeld, M. P. Sheetz, and J. Schlessinger Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration PNAS, September 16, 2003; 100(19): 10740 - 10745. [Abstract] [Full Text] [PDF]
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Y. A. Abassi, M. Rehn, N. Ekman, K. Alitalo, and K. Vuori p130Cas Couples the Tyrosine Kinase Bmx/Etk with Regulation of the Actin Cytoskeleton and Cell Migration J. Biol. Chem., September 12, 2003; 278(37): 35636 - 35643. [Abstract] [Full Text] [PDF]
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M. Funakoshi-Tago, Y. Sonoda, S. Tanaka, K. Hashimoto, K. Tago, S.-i. Tominaga, and T. Kasahara Tumor Necrosis Factor-induced Nuclear Factor {kappa}B Activation Is Impaired in Focal Adhesion Kinase-deficient Fibroblasts J. Biol. Chem., August 1, 2003; 278(31): 29359 - 29365. [Abstract] [Full Text] [PDF]
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J. Zhai, H. Lin, Z. Nie, J. Wu, R. Canete-Soler, W. W. Schlaepfer, and D. D. Schlaepfer Direct Interaction of Focal Adhesion Kinase with p190RhoGEF J. Biol. Chem., June 27, 2003; 278(27): 24865 - 24873. [Abstract] [Full Text] [PDF]
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D. M. Rose, S. Liu, D. G. Woodside, J. Han, D. D. Schlaepfer, and M. H. Ginsberg Paxillin Binding to the {alpha}4 Integrin Subunit Stimulates LFA-1 (Integrin {alpha}L{beta}2)-Dependent T Cell Migration by Augmenting the Activation of Focal Adhesion Kinase/Proline-Rich Tyrosine Kinase-2 J. Immunol., June 15, 2003; 170(12): 5912 - 5918. [Abstract] [Full Text] [PDF]
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H. Haskell, M. Natarajan, T. P. Hecker, Q. Ding, J. Stewart Jr., J. R. Grammer, and C. L. Gladson Focal Adhesion Kinase Is Expressed in the Angiogenic Blood Vessels of Malignant Astrocytic Tumors in Vivo and Promotes Capillary Tube Formation of Brain Microvascular Endothelial Cells Clin. Cancer Res., June 1, 2003; 9(6): 2157 - 2165. [Abstract] [Full Text] [PDF]
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D. M. McKean, L. Sisbarro, D. Ilic, N. Kaplan-Alburquerque, R. Nemenoff, M. Weiser-Evans, M. J. Kern, and P. L. Jones FAK induces expression of Prx1 to promote tenascin-C-dependent fibroblast migration J. Cell Biol., April 28, 2003; 161(2): 393 - 402. [Abstract] [Full Text] [PDF]
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L. Li, D. L. Guris, M. Okura, and A. Imamoto Translocation of CrkL to Focal Adhesions Mediates Integrin-Induced Migration Downstream of Src Family Kinases Mol. Cell. Biol., April 15, 2003; 23(8): 2883 - 2892. [Abstract] [Full Text] [PDF]
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J. T. Parsons Focal adhesion kinase: the first ten years J. Cell Sci., April 15, 2003; 116(8): 1409 - 1416. [Abstract] [Full Text] [PDF]
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Q. G. Medley, E. G. Buchbinder, K. Tachibana, H. Ngo, C. Serra-Pages, and M. Streuli Signaling between Focal Adhesion Kinase and Trio J. Biol. Chem., April 4, 2003; 278(15): 13265 - 13270. [Abstract] [Full Text] [PDF]
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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, et al. Differential regulation of cell motility and invasion by FAK J. Cell Biol., March 3, 2003; 160(5): 753 - 767. [Abstract] [Full Text] [PDF]
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C. A. Lipinski, N. L. Tran, C. Bay, J. Kloss, W. S. McDonough, C. Beaudry, M. E. Berens, and J. C. Loftus Differential Role of Proline-Rich Tyrosine Kinase 2 and Focal Adhesion Kinase in Determining Glioblastoma Migration and Proliferation Mol. Cancer Res., March 1, 2003; 1(5): 323 - 332. [Abstract] [Full Text] [PDF]
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L. Kwong, M. A. Wozniak, A. S. Collins, S. D. Wilson, and P. J. Keely R-Ras Promotes Focal Adhesion Formation through Focal Adhesion Kinase and p130Cas by a Novel Mechanism That Differs from Integrins Mol. Cell. Biol., February 1, 2003; 23(3): 933 - 949. [Abstract] [Full Text]
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E. A. Cox, D. Bennin, A. T. Doan, T. O'Toole, and A. Huttenlocher RACK1 Regulates Integrin-mediated Adhesion, Protrusion, and Chemotactic Cell Migration via Its Src-binding Site Mol. Biol. Cell, February 1, 2003; 14(2): 658 - 669. [Abstract] [Full Text] [PDF]
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L. Zeng, X. Si, W.-P. Yu, H. T. Le, K. P. Ng, R. M.H. Teng, K. Ryan, D. Z.-M. Wang, S. Ponniah, and C. J. Pallen PTP{alpha} regulates integrin-stimulated FAK autophosphorylation and cytoskeletal rearrangement in cell spreading and migration J. Cell Biol., January 2, 2003; 160(1): 137 - 146. [Abstract] [Full Text] [PDF]
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S. Mochizuki, B. Brassart, and A. Hinek Signaling Pathways Transduced through the Elastin Receptor Facilitate Proliferation of Arterial Smooth Muscle Cells J. Biol. Chem., November 15, 2002; 277(47): 44854 - 44863. [Abstract] [Full Text] [PDF]
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V. Golubovskaya, L. Beviglia, L.-H. Xu, H. S. Earp III, R. Craven, and W. Cance Dual Inhibition of Focal Adhesion Kinase and Epidermal Growth Factor Receptor Pathways Cooperatively Induces Death Receptor-mediated Apoptosis in Human Breast Cancer Cells J. Biol. Chem., October 4, 2002; 277(41): 38978 - 38987. [Abstract] [Full Text] [PDF]
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S. Wagner, T. A. Flood, P. O'Reilly, K. Hume, and L. A. Sabourin Association of the Ste20-like Kinase (SLK) with the Microtubule. ROLE IN Rac1-MEDIATED REGULATION OF ACTIN DYNAMICS DURING CELL ADHESION AND SPREADING J. Biol. Chem., September 27, 2002; 277(40): 37685 - 37692. [Abstract] [Full Text] [PDF]
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S. Abbi, H. Ueda, C. Zheng, L. A. Cooper, J. Zhao, R. Christopher, and J.-L. Guan Regulation of Focal Adhesion Kinase by a Novel Protein Inhibitor FIP200 Mol. Biol. Cell, September 1, 2002; 13(9): 3178 - 3191. [Abstract] [Full Text] [PDF]
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S. A. Wilcox-Adelman, F. Denhez, and P. F. Goetinck Syndecan-4 Modulates Focal Adhesion Kinase Phosphorylation J. Biol. Chem., August 30, 2002; 277(36): 32970 - 32977. [Abstract] [Full Text] [PDF]
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G. Giannone, P. Ronde, M. Gaire, J. Haiech, and K. Takeda Calcium Oscillations Trigger Focal Adhesion Disassembly in Human U87 Astrocytoma Cells J. Biol. Chem., July 12, 2002; 277(29): 26364 - 26371. [Abstract] [Full Text] [PDF]
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Y.-P. Jin, R. P. Singh, Z.-Y. Du, A. K. Rajasekaran, E. Rozengurt, and E. F. Reed Ligation of HLA Class I Molecules on Endothelial Cells Induces Phosphorylation of Src, Paxillin, and Focal Adhesion Kinase in an Actin-Dependent Manner J. Immunol., June 1, 2002; 168(11): 5415 - 5423. [Abstract] [Full Text] [PDF]
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L. A. Cary, R. A. Klinghoffer, C. Sachsenmaier, and J. A. Cooper Src Catalytic but Not Scaffolding Function Is Needed for Integrin-Regulated Tyrosine Phosphorylation, Cell Migration, and Cell Spreading Mol. Cell. Biol., April 15, 2002; 22(8): 2427 - 2440. [Abstract] [Full Text] [PDF]
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G. Schratt, U. Philippar, J. Berger, H. Schwarz, O. Heidenreich, and A. Nordheim Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells J. Cell Biol., February 18, 2002; 156(4): 737 - 750. [Abstract] [Full Text] [PDF]
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A. Bhatt, I. Kaverina, C. Otey, and A. Huttenlocher Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain J. Cell Sci., January 9, 2002; 115(17): 3415 - 3425. [Abstract] [Full Text] [PDF]
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P. J. Bruce-Staskal, C. L. Weidow, J. J. Gibson, and A. H. Bouton Cas, Fak and Pyk2 function in diverse signaling cascades to promote Yersinia uptake J. Cell Sci., January 7, 2002; 115(13): 2689 - 2700. [Abstract] [Full Text] [PDF]
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