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Overexpression of the Focal Adhesion Kinase (p125^FAK) in Invasive Human Tumors¹

Departments of Surgery [L. V. O., L. X., R. J. C., T. M. W., W. G. C.], Medicine [E. T. L.], Pathology [G. A. D.], Curriculum in Genetics and Molecular Biology [R. J. C., E. T. L.], and The Lineberger Comprehensive Cancer Center [L. V. O., L. X., R. J. C., T. M. W., E. T. L., W. G. C.], University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina 27599, and Research Triangle Institute, Research Triangle Park, North Carolina 27709 [L. K.]

The focal adhesion kinase (FAK) gene encodes a tyrosine kinase (p125^FAK) thought to be involved in signal transduction pathways used in cell adhesion, motility, and anchorage-independent growth. Because alterations in these cellular processes occur in tumor invasion and metastasis, we studied the protein expression of FAK in a variety of human tumors and found that in the 119 samples studied, increased levels of p125^FAK correlated with the invasive potential of a tumor. By comparing FAK expression in tumors with normal tissue from the same patient, we found that p125^FAK was significantly elevated in 17 (100%) of 17 invasive and metastatic colonic lesions and in 22 (88%) of 25 invasive and metastatic breast tumors. Additional studies of FAK expression in 13 high grade sarcomas showed high levels in all samples compared to benign, noninvasive mesenchymal specimens. Furthermore, FAK protein levels were elevated in preinvasive lesions, such as large (>2 cm) colonic villous adenomas, whereas noninvasive, yet hypercellular, neoplastic tissues such as parathyroid and hepatocellular adenomas did not overexpress FAK. These data provide evidence that both epithelial and mesenchymal tumor progression are accompanied by increased p125^FAK expression and suggest that the level of FAK expression might be a marker for the invasive potential of a tumor.

¹ This study was supported by NIH Grants CA09688, CA01625, and CA58233-01 Specialized Program of Research Excellence in breast cancer.

² Recipient of the George H. A. Clowes, Jr., Memorial Research Career Development Award from the American College of Surgeons.

³ To whom requests for reprints should be addressed, at Department of Surgery, 3010 Old Clinic Building, CB #7210, University of North Carolina, Chapel Hill, North Carolina 27599.

Received 3/21/95. Accepted 5/19/95.

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				W. G. Cance, J. E. Harris, M. V. Iacocca, E. Roche, X. Yang, J. Chang, S. Simkins, and L. Xu Immunohistochemical Analyses of Focal Adhesion Kinase Expression in Benign and Malignant Human Breast and Colon Tissues: Correlation with Preinvasive and Invasive Phenotypes Clin. Cancer Res., June 1, 2000; 6(6): 2417 - 2423. [Abstract] [Full Text]

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				B. M. FREY, B. F. X. REBER, B. S. VISHWANATH, G. ESCHER, and F. J. FREY Annexin I modulates cell functions by controlling intracellular calcium release FASEB J, December 1, 1999; 13(15): 2235 - 2245. [Abstract] [Full Text]

				M. Tamura, J. Gu, H. Tran, and K. M. Yamada PTEN Gene and Integrin Signaling in Cancer J Natl Cancer Inst, November 3, 1999; 91(21): 1820 - 1828. [Abstract] [Full Text] [PDF]

				M. W. Renshaw, L. S. Price, and M. A. Schwartz Focal Adhesion Kinase Mediates the Integrin Signaling Requirement for Growth Factor Activation of Map Kinase J. Cell Biol., November 1, 1999; 147(3): 611 - 618. [Abstract] [Full Text] [PDF]

				N. D. Zantek, M. Azimi, M. Fedor-Chaiken, B. Wang, R. Brackenbury, and M. S. Kinch E-Cadherin Regulates the Function of the EphA2 Receptor Tyrosine Kinase Cell Growth Differ., September 1, 1999; 10(9): 629 - 638. [Abstract] [Full Text]

				D. C. Han and J.-L. Guan Association of Focal Adhesion Kinase with Grb7 and Its Role in Cell Migration J. Biol. Chem., August 20, 1999; 274(34): 24425 - 24430. [Abstract] [Full Text] [PDF]

				M. Tamura, J. Gu, E. H. J. Danen, T. Takino, S. Miyamoto, and K. M. Yamada PTEN Interactions with Focal Adhesion Kinase and Suppression of the Extracellular Matrix-dependent Phosphatidylinositol 3-Kinase/Akt Cell Survival Pathway J. Biol. Chem., July 16, 1999; 274(29): 20693 - 20703. [Abstract] [Full Text] [PDF]

				M. Oktay, K. K. Wary, M. Dans, R. B. Birge, and F. G. Giancotti Integrin-mediated Activation of Focal Adhesion Kinase Is Required for Signaling to Jun NH2-terminal Kinase and Progression through the G1 Phase of the Cell Cycle J. Cell Biol., June 28, 1999; 145(7): 1461 - 1470. [Abstract] [Full Text] [PDF]

				D. Sieg, C. Hauck, and D. Schlaepfer Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration J. Cell Sci., January 8, 1999; 112(16): 2677 - 2691. [Abstract] [PDF]

				M. Tamura, J. Gu, T. Takino, and K. M. Yamada Tumor Suppressor PTEN Inhibition of Cell Invasion, Migration, and Growth: Differential Involvement of Focal Adhesion Kinase and p130Cas Cancer Res., January 1, 1999; 59(2): 442 - 449. [Abstract] [Full Text] [PDF]

				H.-C. Chen, P.-C. Chan, M.-J. Tang, C.-H. Cheng, and T.-J. Chang Tyrosine Phosphorylation of Focal Adhesion Kinase Stimulated by Hepatocyte Growth Factor Leads to Mitogen-activated Protein Kinase Activation J. Biol. Chem., October 2, 1998; 273(40): 25777 - 25782. [Abstract] [Full Text] [PDF]

				A. Casamassima and E. Rozengurt Insulin-like Growth Factor I Stimulates Tyrosine Phosphorylation of p130Cas, Focal Adhesion Kinase, and Paxillin. ROLE OF PHOSPHATIDYLINOSITOL 3'-KINASE AND FORMATION OF A p130Cas·Crk COMPLEX J. Biol. Chem., October 2, 1998; 273(40): 26149 - 26156. [Abstract] [Full Text] [PDF]

				D.-H. Yu, C.-K. Qu, O. Henegariu, X. Lu, and G.-S. Feng Protein-tyrosine Phosphatase Shp-2 Regulates Cell Spreading, Migration, and Focal Adhesion J. Biol. Chem., August 14, 1998; 273(33): 21125 - 21131. [Abstract] [Full Text] [PDF]

				F. G. Gervais, N. A. Thornberry, S. C. Ruffolo, D. W. Nicholson, and S. Roy Caspases Cleave Focal Adhesion Kinase during Apoptosis to Generate a FRNK-like Polypeptide J. Biol. Chem., July 3, 1998; 273(27): 17102 - 17108. [Abstract] [Full Text] [PDF]

				L.-P. Wen, J. A. Fahrni, S. Troie, J.-L. Guan, K. Orth, and G. D. Rosen Cleavage of Focal Adhesion Kinase by Caspases during Apoptosis J. Biol. Chem., October 10, 1997; 272(41): 26056 - 26061. [Abstract] [Full Text] [PDF]

				D. D. Schlaepfer and T. Hunter Focal Adhesion Kinase Overexpression Enhances Ras-dependent Integrin Signaling to ERK2/Mitogen-activated Protein Kinase through Interactions with and Activation of c-Src J. Biol. Chem., May 16, 1997; 272(20): 13189 - 13195. [Abstract] [Full Text] [PDF]

				P. S. Leventhal, E. A. Shelden, B. Kim, and E. L. Feldman Tyrosine Phosphorylation of Paxillin and Focal Adhesion Kinase during Insulin-like Growth Factor-I-stimulated Lamellipodial Advance J. Biol. Chem., February 21, 1997; 272(8): 5214 - 5218. [Abstract] [Full Text] [PDF]

				D Ilic, C. Damsky, and T Yamamoto Focal adhesion kinase: at the crossroads of signal transduction J. Cell Sci., January 2, 1997; 110(4): 401 - 407. [Abstract] [PDF]

				L. Cary, J. Chang, and J. Guan Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn J. Cell Sci., January 7, 1996; 109(7): 1787 - 1794. [Abstract] [PDF]

				E. P. Salazar and E. Rozengurt Src Family Kinases Are Required for Integrin-mediated but Not for G Protein-coupled Receptor Stimulation of Focal Adhesion Kinase Autophosphorylation at Tyr-397 J. Biol. Chem., May 18, 2001; 276(21): 17788 - 17795. [Abstract] [Full Text] [PDF]

				L.-H. Xu, X. Yang, C. A. Bradham, D. A. Brenner, A. S. Baldwin Jr., R. J. Craven, and W. G. Cance The Focal Adhesion Kinase Suppresses Transformation-associated, Anchorage-independent Apoptosis in Human Breast Cancer Cells. INVOLVEMENT OF DEATH RECEPTOR-RELATED SIGNALING PATHWAYS J. Biol. Chem., September 22, 2000; 275(39): 30597 - 30604. [Abstract] [Full Text] [PDF]