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© The Rockefeller University Press, 0021-9525/1998//547 $5.00
The Journal of Cell Biology, Volume 143, Number 2, , 1998 547-560

Extracellular Matrix Survival Signals Transduced by Focal Adhesion Kinase Suppress p53-mediated Apoptosis

Duko Ili^*, Eduardo A.C. Almeida^*, David D. Schlaepfer, Paul Dazin, Shinichi Aizawa^||, and Caroline H. Damsky^*

^* Departments of Stomatology and Anatomy, Howard Hughes Medical Institute, University of California San Francisco, San Francisco, California 94143-0512; The Scripps Research Institute, Department of Immunology, La Jolla, California 92037; and ^|| Department of Morphogenesis, Institute of Molecular Embryology and Genetics, Kumamoto University School of Medicine, Kumamoto 860, Japan

In many malignant cells, both the anchorage requirement for survival and the function of the p53 tumor suppressor gene are subverted. These effects are consistent with the hypothesis that survival signals from extracellular matrix (ECM) suppress a p53-regulated cell death pathway. We report that survival signals from fibronectin are transduced by the focal adhesion kinase (FAK). If FAK or the correct ECM is absent, cells enter apoptosis through a p53-dependent pathway activated by protein kinase C / and cytosolic phospholipase A₂. This pathway is suppressible by dominant-negative p53 and Bcl2 but not CrmA. Upon inactivation of p53, cells survive even if they lack matrix signals or FAK. This is the first report that p53 monitors survival signals from ECM/FAK in anchorage- dependent cells.

Key Words: fibronectin • survival • FAK • p53 • apoptosis

Abbreviations used in this paper: cPLA₂, cytosolic phospholipase A₂; DiI-Ac-LDL, DiI-labeled acetylated low-density lipoprotein; E, embryonic day; EB, embryoid bodies; ECM, extracellular matrix; ES, embryoid stem cells; FAK, focal adhesion kinase; FAT, focal adhesion targeting; FRNK, FAK-related nonkinase; GFP, green fluorescent protein; GSE, genetic suppressor element; HA, hemagglutinin; PECAM-1, platelet–endothelial cell adhesion molecule; PI3K, phosphatidylinositol-3'-kinase; PKC, protein kinase C; PLC-, phospholipase C-; pmT, polyoma middle T; RSF, rabbit synovial fibroblasts; TNF-, tumor necrosis factor-; TUNEL, terminal deoxynucleotidyl transferase (TdT)-mediated dUTP nick end labeling.

Duko Ili and Eduardo A.C. Almeida contributed equally to this work.

Address all correspondence to Caroline H. Damsky, Ph.D, University of California San Francisco, 513 Parnassus Avenue, HSW-604, San Francisco, CA 94143-0512. Tel.: (415) 476-8922. Fax: (415) 502-7338. E-mail: damsky{at}cgl.ucsf.edu

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• Ilic, D., Genbacev, O., Jin, F., Caceres, E., Almeida, E. A. C., Bellingard-Dubouchaud, V., Schaefer, E. M., Damsky, C. H., Fisher, S. J. (2001). Plasma Membrane-Associated pY397FAK Is a Marker of Cytotrophoblast Invasion in Vivo and in Vitro. Am. J. Pathol. 159: 93-108 [Abstract] [Full Text]  
• Schneider, G.B., Zaharias, R., Stanford, C. (2001). Osteoblast Integrin Adhesion and Signaling Regulate Mineralization. JDR 80: 1540-1544 [Abstract]  
• Zachary, I. (2001). Signaling mechanisms mediating vascular protective actions of vascular endothelial growth factor. Am. J. Physiol. Cell Physiol. 280: C1375-C1386 [Abstract] [Full Text]  
• Weinberg, J. M., Venkatachalam, M. A., Roeser, N. F., Senter, R. A., Nissim, I. (2001). Energetic Determinants of Tyrosine Phosphorylation of Focal Adhesion Proteins during Hypoxia/Reoxygenation of Kidney Proximal Tubules. Am. J. Pathol. 158: 2153-2164 [Abstract] [Full Text]  
• DeRoock, I. B., Pennington, M. E., Sroka, T. C., Lam, K. S., Bowden, G. T., Bair, E. L., Cress, A. E. (2001). Synthetic Peptides Inhibit Adhesion of Human Tumor Cells to Extracellular Matrix Proteins. Cancer Res. 61: 3308-3313 [Abstract] [Full Text]  
• White, S. R., Williams, P., Wojcik, K. R., Sun, S., Hiemstra, P. S., Rabe, K. F., Dorscheid, D. R. (2001). Initiation of Apoptosis by Actin Cytoskeletal Derangement in Human Airway Epithelial Cells. Am. J. Respir. Cell Mol. Bio. 24: 282-294 [Abstract] [Full Text]  
• Grossmann, J., Walther, K., Artinger, M., Kiessling, S., Schölmerich, J. (2001). Apoptotic Signaling during Initiation of Detachment-induced Apoptosis ("Anoikis") of Primary Human Intestinal Epithelial Cells. Cell Growth Differ. 12: 147-155 [Abstract] [Full Text]  
• Zachary, I., Gliki, G. (2001). Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res 49: 568-581 [Abstract] [Full Text]  
• Aoudjit, F., Vuori, K. (2001). Matrix Attachment Regulates FAS-Induced Apoptosis in Endothelial Cells: A Role for C-Flip and Implications for Anoikis. JCB 152: 633-644 [Abstract] [Full Text]  
• Harrington, E. O., Smeglin, A., Newton, J., Ballard, G., Rounds, S. (2001). Protein tyrosine phosphatase-dependent proteolysis of focal adhesion complexes in endothelial cell apoptosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L342-L353 [Abstract] [Full Text]  
• Weyant, M. J., Carothers, A. M., Dannenberg, A. J., Bertagnolli, M. M. (2001). (+)-Catechin Inhibits Intestinal Tumor Formation and Suppresses Focal Adhesion Kinase Activation in the Min/+ Mouse. Cancer Res. 61: 118-125 [Abstract] [Full Text]  
• Jones, C. B., McIntosh, J., Huang, H., Graytock, A., Hoyt, D. G. (2001). Regulation of Bleomycin-Induced DNA Breakage and Chromatin Structure in Lung Endothelial Cells by Integrins and Poly(ADP-Ribose) Polymerase. Mol. Pharmacol. 59: 69-75 [Abstract] [Full Text]  
• Komarova, S. V., Ataullakhanov, F. I., Globus, R. K. (2000). Bioenergetics and mitochondrial transmembrane potential during differentiation of cultured osteoblasts. Am. J. Physiol. Cell Physiol. 279: C1220-C1229 [Abstract] [Full Text]  
• Cummings, B. S., McHowat, J., Schnellmann, R. G. (2000). Phospholipase A2s in Cell Injury and Death. J. Pharmacol. Exp. Ther. 294: 793-799 [Abstract] [Full Text]  
• Fincham, V. J., Brunton, V. G., Frame, M. C. (2000). The SH3 Domain Directs Acto-Myosin-Dependent Targeting of v-Src to Focal Adhesions via Phosphatidylinositol 3-Kinase. Mol. Cell. Biol. 20: 6518-6536 [Abstract] [Full Text]  
• Fornaro, M., Steger, C. A., Bennett, A. M., Wu, J. J., Languino, L. R. (2000). Differential Role of beta 1C and beta 1A Integrin Cytoplasmic Variants in Modulating Focal Adhesion Kinase, Protein Kinase B/AKT, and Ras/Mitogen-activated Protein Kinase Pathways. Mol. Biol. Cell 11: 2235-2249 [Abstract] [Full Text]  
• Zachary, I., Mathur, A., Yla-Herttuala, S., Martin, J. (2000). Vascular Protection : A Novel Nonangiogenic Cardiovascular Role for Vascular Endothelial Growth Factor. Arterioscler. Thromb. Vasc. Bio. 20: 1512-1520 [Abstract] [Full Text]  

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