Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors

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Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors

S Miyamoto, H Teramoto, JS Gutkind and KM Yamada
Laboratory of Developmental Biology, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland 20892-4370, USA.

Integrins mediate cell adhesion, migration, and a variety of signal transduction events. These integrin actions can overlap or even synergize with those of growth factors. We examined for mechanisms of collaboration or synergy between integrins and growth factors involving MAP kinases, which regulate many cellular functions. In cooperation with integrins, the growth factors EGF, PDGF-BB, and basic FGF each produced a marked, transient activation of the ERK (extracellular signal-regulated kinase) class of MAP kinase, but only if the integrins were both aggregated and occupied by ligand. Transmembrane accumulation of total tyrosine-phosphorylated proteins, as well as nonsynergistic MAP kinase activation, could be induced by simple integrin aggregation, whereas enhanced transient accumulation of the EGF-receptor substrate eps8 required integrin aggregation and occupancy, as well as EGF treatment. Each type of growth factor receptor was itself induced to aggregate transiently by integrin ligand-coated beads in a process requiring both aggregation and occupancy of integrin receptors, but not the presence of growth factor ligand. Synergism was also observed between integrins and growth factors for triggering tyrosine phosphorylation of EGF, PDGF, and FGF receptors. This collaborative response also required both integrin aggregation and occupancy. These studies identify mechanisms in the signal transduction response to integrins and growth factors that require various combinations of integrin aggregation and ligands for integrin or growth factor receptors, providing opportunities for collaboration between these major regulatory systems.
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Liou, H.-H., Lin, W., Liou, H.-C., Huang, T.-F., Fu, W.-M. (2001). Modulation of Protein Kinase A Activation by Fibronectin Matrix Proteins at Developing Neuromuscular Synapses in Xenopuslaevis Cell Cultures. Mol. Pharmacol. 60: 348-354 [Abstract] [Full Text]
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]
Stockton, R. A., Jacobson, B. S. (2001). Modulation of Cell-Substrate Adhesion by Arachidonic Acid: Lipoxygenase Regulates Cell Spreading and ERK1/2-inducible Cyclooxygenase Regulates Cell Migration in NIH-3T3 Fibroblasts. Mol. Biol. Cell 12: 1937-1956 [Abstract] [Full Text]
PONCE, M. L., NOMIZU, M., KLEINMAN, H. K. (2001). An angiogenic laminin site and its antagonist bind through the {alpha}v{beta}3 and {alpha}5{beta}1 integrins. FASEB J. 15: 1389-1397 [Abstract] [Full Text]
Alt, A., Ohba, M., Li, L., Gartsbein, M., Belanger, A., Denning, Mitchell. F., Kuroki, T., Yuspa, S. H., Tennenbaum, T. (2001). Protein Kinase C{{delta}}-mediated Phosphorylation of {{alpha}}6{beta}4 Is Associated with Reduced Integrin Localization to the Hemidesmosome and Decreased Keratinocyte Attachment. Cancer Res. 61: 4591-4598 [Abstract] [Full Text]
Li, X., Chen, Y., Scheele, S., Arman, E., Haffner-Krausz, R., Ekblom, P., Lonai, P. (2001). Fibroblast Growth Factor Signaling and Basement Membrane Assembly Are Connected during Epithelial Morphogenesis of the Embryoid Body. JCB 153: 811-822 [Abstract] [Full Text]
Hintermann, E., Bilban, M., Sharabi, A., Quaranta, V. (2001). Inhibitory Role of {alpha}6{beta}4-Associated Erbb-2 and Phosphoinositide 3-Kinase in Keratinocyte Haptotactic Migration Dependent on {alpha}3{beta}1 Integrin. JCB 153: 465-478 [Abstract] [Full Text]
Aplin, A. E., Stewart, S. A., Assoian, R. K., Juliano, R.L. (2001). Integrin-Mediated Adhesion Regulates ERK Nuclear Translocation and Phosphorylation of Elk-1. JCB 153: 273-282 [Abstract] [Full Text]
Kapur, R., Cooper, R., Zhang, L., Williams, D. A. (2001). Cross-talk between {alpha}4{beta}1/{alpha}5{beta}1 and c-Kit results in opposing effect on growth and survival of hematopoietic cells via the activation of focal adhesion kinase, mitogen-activated protein kinase, and Akt signaling pathways. Blood 97: 1975-1981 [Abstract] [Full Text]
Brock, R., Jovin, T. M. (2001). Heterogeneity of signal transduction at the subcellular level: microsphere-based focal EGF receptor activation and stimulation of Shc translocation. J. Cell Sci. 114: 2437-2447 [Abstract] [Full Text]
Bai, J, Chiu, W, Wang, J, Tzeng, T, Perrimon, N, Hsu, J (2001). The cell adhesion molecule Echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway. Development 128: 591-601 [Abstract]
Miyamoto, T., Arai, F., Ohneda, O., Takagi, K., Anderson, D. M., Suda, T. (2000). An adherent condition is required for formation of multinuclear osteoclasts in the presence of macrophage colony-stimulating factor and receptor activator of nuclear factor kappa B ligand. Blood 96: 4335-4343 [Abstract] [Full Text]
WILKINSON, M. G., MILLAR, J. B. A. (2000). Control of the eukaryotic cell cycle by MAP kinase signaling pathways. FASEB J. 14: 2147-2157 [Abstract] [Full Text]
Wang, H.-B., Dembo, M., Wang, Y.-L. (2000). Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am. J. Physiol. Cell Physiol. 279: C1345-C1350 [Abstract] [Full Text]
Hornberger, L. K., Singhroy, S., Cavalle-Garrido, T., Tsang, W., Keeley, F., Rabinovitch, M. (2000). Synthesis of Extracellular Matrix and Adhesion Through {beta}1 Integrins Are Critical for Fetal Ventricular Myocyte Proliferation. Circ. Res. 87: 508-515 [Abstract] [Full Text]
Greenwood, J. A., Theibert, A. B., Prestwich, G. D., Murphy-Ullrich, J. E. (2000). Restructuring of Focal Adhesion Plaques by Pi 3-Kinase: Regulation by Ptdins (3,4,5-P)3 Binding to {alpha}-Actinin. JCB 150: 627-642 [Abstract] [Full Text]
Kuwada, S. K., Li, X. (2000). Integrin alpha 5/beta 1 Mediates Fibronectin-dependent Epithelial Cell Proliferation through Epidermal Growth Factor Receptor Activation. Mol. Biol. Cell 11: 2485-2496 [Abstract] [Full Text]