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GE Plopper, HP McNamee, LE Dike, K Bojanowski and DE Ingber
Department of Surgery, Children's Hospital, Boston, Massachusetts 02115, USA.
Extracellular matrix controls capillary endothelial cell sensitivity to soluble mitogens by binding integrin receptors and thereby activating a chemical signaling response that rapidly integrates with growth factor- induced signaling mechanisms. Here we report that in addition to integrins, growth factor receptors and multiple molecules that transduce signals conveyed by both types of receptors are immobilized on the cytoskeleton (CSK) and spatially integrated within the focal adhesion complex (FAC) at the site of integrin binding. FACs were rapidly induced in round cells and physically isolated from the remainder of the CSK after detergent-extraction using magnetic microbeads coated with fibronectin or a synthetic RGD-containing peptide. Immunofluorescence microscopy revealed that multiple signaling molecules (e.g., pp60c-src, pp125FAK, phosphatidylinositol-3-kinase, phospholipase C-gamma, and Na+/H+ antiporter) involved in both integrin and growth factor receptor signaling pathways became associated with the CSK framework of the FAC within 15 min after binding to beads coated with integrin ligands. Recruitment of tyrosine kinases to the FAC was also accompanied by a local increase in tyrosine phosphorylation, as indicated by enhanced phosphotyrosine staining at the site of integrin binding. In contrast, neither recruitment of signaling molecules nor increased phosphotyrosine staining was observed when cells bound to beads coated with a control ligand (acetylated low density lipoprotein) that ligates transmembrane scavenger receptors, but does not induce FAC formation. Western blot analysis confirmed that FACs isolated using RGD-beads were enriched for pp60c-src, pp125FAK, phospholipase C-gamma, and the Na+/H+ antiporter when compared with intact CSK or basal cell surface preparations that retained lipid bilayer. Isolated FACs were also greatly enriched for the high affinity fibroblast growth factor receptor flg. Most importantly, isolated FACs continued to exhibit multiple chemical signaling activities in vitro, including protein tyrosine kinase activities (pp60c-src and pp125FAK) as well as the ability to undergo multiple sequential steps in the inositol lipid synthesis cascade. These data suggest that many of the chemical signaling events that are induced by integrins and growth factor receptors in capillary cells may effectively function in a "solid-state" on insoluble CSK scaffolds within the FAC and that the FAC may represent a major site for signal integration between these two regulatory pathways. Future investigations into the biochemical and biophysical basis of signal transduction may be facilitated by this method, which results in isolation of FACs that retain the CSK framework as well as multiple associated chemical signaling activities.
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S. J. Reshkin, A. Bellizzi, V. Albarani, L. Guerra, M. Tommasino, A. Paradiso, and V. Casavola Phosphoinositide 3-Kinase Is Involved in the Tumor-specific Activation of Human Breast Cancer Cell Na+/H+ Exchange, Motility, and Invasion Induced by Serum Deprivation J. Biol. Chem., February 25, 2000; 275(8): 5361 - 5369. [Abstract] [Full Text] [PDF]
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I. N. Rich, D. Worthington-White, O. A. Garden, and P. Musk Apoptosis of leukemic cells accompanies reduction in intracellular pH after targeted inhibition of the Na+/H+ exchanger Blood, February 15, 2000; 95(4): 1427 - 1434. [Abstract] [Full Text] [PDF]
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A. Asthagiri, C. Reinhart, A. Horwitz, and D. Lauffenburger The role of transient ERK2 signals in fibronectin- and insulin-mediated DNA synthesis J. Cell Sci., January 12, 2000; 113(24): 4499 - 4510. [Abstract] [PDF]
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L Yan, M. Moses, S Huang, and D. Ingber Adhesion-dependent control of matrix metalloproteinase-2 activation in human capillary endothelial cells J. Cell Sci., January 11, 2000; 113(22): 3979 - 3987. [Abstract] [PDF]
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M. Duncan, Z Kozmik, K Cveklova, J Piatigorsky, and A Cvekl Overexpression of PAX6(5a) in lens fiber cells results in cataract and upregulation of (alpha)5(beta)1 integrin expression J. Cell Sci., January 9, 2000; 113(18): 3173 - 3185. [Abstract] [PDF]
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M. Akamatsu, S.-i. Aota, A. Suwa, K. Ueda, T. Amachi, K. M. Yamada, S. K. Akiyama, and N. Kioka Vinexin Forms a Signaling Complex with Sos and Modulates Epidermal Growth Factor-induced c-Jun N-terminal Kinase/Stress-activated Protein Kinase Activities J. Biol. Chem., December 10, 1999; 274(50): 35933 - 35937. [Abstract] [Full Text] [PDF]
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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]
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 G. J. Mizejewski Role of Integrins in Cancer: Survey of Expression Patterns Experimental Biology and Medicine, November 1, 1999; 222(2): 124 - 138. [Abstract] [Full Text]
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A. R. Asthagiri, C. M. Nelson, A. F. Horwitz, and D. A. Lauffenburger Quantitative Relationship among Integrin-Ligand Binding, Adhesion, and Signaling via Focal Adhesion Kinase and Extracellular Signal-regulated Kinase 2 J. Biol. Chem., September 17, 1999; 274(38): 27119 - 27127. [Abstract] [Full Text] [PDF]
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M. A. Skinner and A. G. Wildeman beta 1 Integrin Binds the 16-kDa Subunit of Vacuolar H+-ATPase at a Site Important for Human Papillomavirus E5 and Platelet-derived Growth Factor Signaling J. Biol. Chem., August 13, 1999; 274(33): 23119 - 23127. [Abstract] [Full Text] [PDF]
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X. Zhang, A. Chattopadhyay, Q.-s. Ji, J. D. Owen, P. J. Ruest, G. Carpenter, and S. K. Hanks Focal adhesion kinase promotes phospholipase C-gamma 1 activity PNAS, August 3, 1999; 96(16): 9021 - 9026. [Abstract] [Full Text] [PDF]
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M. Fluck, J. A. Carson, S. E. Gordon, A. Ziemiecki, and F. W. Booth Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle Am J Physiol Cell Physiol, July 1, 1999; 277(1): C152 - C162. [Abstract] [Full Text] [PDF]
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K.-D. Chen, Y.-S. Li, M. Kim, S. Li, S. Yuan, S. Chien, and J. Y-J. Shyy Mechanotransduction in Response to Shear Stress. ROLES OF RECEPTOR TYROSINE KINASES, INTEGRINS, AND Shc J. Biol. Chem., June 25, 1999; 274(26): 18393 - 18400. [Abstract] [Full Text] [PDF]
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M. S. Goligorsky, H. Abedi, E. Noiri, A. Takhtajan, S. Lense, V. Romanov, and I. Zachary Nitric oxide modulation of focal adhesions in endothelial cells Am J Physiol Cell Physiol, June 1, 1999; 276(6): C1271 - C1281. [Abstract] [Full Text] [PDF]
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A. Sahni, L. A. Sporn, and C. W. Francis Potentiation of Endothelial Cell Proliferation by Fibrin(ogen)-bound Fibroblast Growth Factor-2 J. Biol. Chem., May 21, 1999; 274(21): 14936 - 14941. [Abstract] [Full Text] [PDF]
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C. K. Miranti, S. Ohno, and J. S. Brugge Protein Kinase C Regulates Integrin-induced Activation of the Extracellular Regulated Kinase Pathway Upstream of Shc J. Biol. Chem., April 9, 1999; 274(15): 10571 - 10581. [Abstract] [Full Text] [PDF]
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N. Farrelly, Y.-J. Lee, J. Oliver, C. Dive, and C. H. Streuli Extracellular Matrix Regulates Apoptosis in Mammary Epithelium through a Control on Insulin Signaling J. Cell Biol., March 22, 1999; 144(6): 1337 - 1348. [Abstract] [Full Text] [PDF]
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S. K. Sastry, M. Lakonishok, S. Wu, T. Q. Truong, A. Huttenlocher, C. E. Turner, and A. F. Horwitz Quantitative Changes in Integrin and Focal Adhesion Signaling Regulate Myoblast Cell Cycle Withdrawal J. Cell Biol., March 22, 1999; 144(6): 1295 - 1309. [Abstract] [Full Text] [PDF]
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M. D. Martin-Bermudo and N. H. Brown Uncoupling integrin adhesion and signaling: the beta PS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo Genes & Dev., March 15, 1999; 13(6): 729 - 739. [Abstract] [Full Text]
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Y. Tu, F. Li, S. Goicoechea, and C. Wu The LIM-Only Protein PINCH Directly Interacts with Integrin-Linked Kinase and Is Recruited to Integrin-Rich Sites in Spreading Cells Mol. Cell. Biol., March 1, 1999; 19(3): 2425 - 2434. [Abstract] [Full Text] [PDF]
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Y. Tu, F. Li, and C. Wu Nck-2, a Novel Src Homology2/3-containing Adaptor Protein That Interacts with the LIM-only Protein PINCH and Components of Growth Factor Receptor Kinase-signaling Pathways Mol. Biol. Cell, December 1, 1998; 9(12): 3367 - 3382. [Abstract] [Full Text]
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D. Ilic, E. A.C. Almeida, D. D. Schlaepfer, P. Dazin, S. Aizawa, and C. H. Damsky Extracellular Matrix Survival Signals Transduced by Focal Adhesion Kinase Suppress p53-mediated Apoptosis J. Cell Biol., October 19, 1998; 143(2): 547 - 560. [Abstract] [Full Text] [PDF]
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S. Y Low and P. M Taylor Integrin and cytoskeletal involvement in signalling cell volume changes to glutamine transport in rat skeletal muscle J. Physiol., October 15, 1998; 512(2): 481 - 485. [Abstract] [Full Text] [PDF]
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X. Wu, J. E. Mogford, S. H. Platts, G. E. Davis, G. A. Meininger, and M. J. Davis Modulation of Calcium Current in Arteriolar Smooth Muscle by {alpha}v{beta}3 and {alpha}5{beta}1 Integrin Ligands J. Cell Biol., October 5, 1998; 143(1): 241 - 252. [Abstract] [Full Text] [PDF]
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B. Zheng and D. R. Clemmons Blocking ligand occupancy of the alpha Vbeta 3 integrin inhibits insulin-like growth factor I signaling in vascular smooth muscle cells PNAS, September 15, 1998; 95(19): 11217 - 11222. [Abstract] [Full Text] [PDF]
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T. Tominaga and D. L. Barber Na-H Exchange Acts Downstream of RhoA to Regulate Integrin-induced Cell Adhesion and Spreading Mol. Biol. Cell, August 1, 1998; 9(8): 2287 - 2303. [Abstract] [Full Text]
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M. C. Brown, J. A. Perrotta, and C. E. Turner Serine and Threonine Phosphorylation of the Paxillin LIM Domains Regulates Paxillin Focal Adhesion Localization and Cell Adhesion to Fibronectin Mol. Biol. Cell, July 1, 1998; 9(7): 1803 - 1816. [Abstract] [Full Text]
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