Integrin cytoplasmic domains mediate inside-out signal transduction

doi:10.1083/jcb.124.6.1047

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Integrin cytoplasmic domains mediate inside-out signal transduction

TE O'Toole, Y Katagiri, RJ Faull, K Peter, R Tamura, V Quaranta, JC Loftus, SJ Shattil and MH Ginsberg
Department of Vascular Biology, Scripps Research Institute, La Jolla, California 92037.

We analyzed the binding of fibronectin to integrin alpha 5 beta 1 in various cells; in some cells fibronectin bound with low affinity (e.g., K562 cells) whereas in others (e.g., CHO), it bound with high affinity (Kd approximately 100 nM) in an energy-dependent manner. We constructed chimeras of the extracellular and transmembrane domains of alpha IIb beta 3 joined to the cytoplasmic domains of alpha 5 beta 1. The affinity state of these chimeras was assessed by binding of fibrinogen or the monoclonal antibody, PAC1. The cytoplasmic domains of alpha 5 beta 1 conferred an energy-dependent high affinity state on alpha IIb beta 3 in CHO but not K562 cells. Three additional alpha cytoplasmic domains (alpha 2, alpha 6A, alpha 6B) conferred PAC1 binding in CHO cells, while three others (alpha M, alpha L, alpha v) did not. In the high affinity alpha chimeras, cotransfection with a truncated (beta 3 delta 724) or mutated (beta 3(S752-->P)) beta 3 subunit abolished high affinity binding. Thus, both cytoplasmic domains are required for energy-dependent, cell type-specific affinity modulation. In addition, mutations that disrupted a highly conserved alpha subunit GFFKR motif, resulted in high affinity binding of ligands to alpha IIb beta 3. In contrast to the chimeras, the high affinity state of these mutants was independent of cellular metabolism, cell type, and the bulk of the beta subunit cytoplasmic domain. Thus, integrin cytoplasmic domains mediate inside-out signaling. Furthermore, the highly conserved GFFKR motif of the alpha subunit cytoplasmic domain maintains the default low affinity state.
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Katagiri, K., Hattori, M., Minato, N., Irie, S.-k., Takatsu, K., Kinashi, T. (2000). Rap1 Is a Potent Activation Signal for Leukocyte Function-Associated Antigen 1 Distinct from Protein Kinase C and Phosphatidylinositol-3-OH Kinase. Mol. Cell. Biol. 20: 1956-1969 [Abstract] [Full Text]
Jung, S. M., Moroi, M. (2000). Signal-transducing Mechanisms Involved in Activation of the Platelet Collagen Receptor Integrin alpha 2beta 1. J. Biol. Chem. 275: 8016-8026 [Abstract] [Full Text]
Zent, R., Fenczik, C. A., Calderwood, D. A., Liu, S., Dellos, M., Ginsberg, M. H. (2000). Class- and Splice Variant-specific Association of CD98 with Integrin beta Cytoplasmic Domains. J. Biol. Chem. 275: 5059-5064 [Abstract] [Full Text]
Duncan, M. K., Cvekl, A., Li, X., Piatigorsky, J. (2000). Truncated Forms of Pax-6 Disrupt Lens Morphology in Transgenic Mice. IOVS 41: 464-473 [Abstract] [Full Text]
Leitinger, B., Hogg, N. (2000). Effects of I Domain Deletion on the Function of the beta 2 Integrin Lymphocyte Function-associated Antigen-1. Mol. Biol. Cell 11: 677-690 [Abstract] [Full Text]
Liu, S, Calderwood, D., Ginsberg, M. (2000). Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113: 3563-3571 [Abstract]
Hadari, Y., Arbel-Goren, R, Levy, Y, Amsterdam, A, Alon, R, Zakut, R, Zick, Y (2000). Galectin-8 binding to integrins inhibits cell adhesion and induces apoptosis. J. Cell Sci. 113: 2385-2397 [Abstract]
Martin-Bermudo, M. (2000). Integrins modulate the Egfr signaling pathway to regulate tendon cell differentiation in the Drosophila embryo. Development 127: 2607-2615 [Abstract]
Klass, C., Couchman, J., Woods, A (2000). Control of extracellular matrix assembly by syndecan-2 proteoglycan. J. Cell Sci. 113: 493-506 [Abstract]
Shiraga, M., Ritchie, A., Aidoudi, S., Baron, V., Wilcox, D., White, G., Ybarrondo, B., Murphy, G., Leavitt, A., Shattil, S. (1999). Primary Megakaryocytes Reveal a Role for Transcription Factor Nf-E2 in Integrin {alpha}iib{beta}3 Signaling. JCB 147: 1419-1430 [Abstract] [Full Text]
Armulik, A., Nilsson, I., von Heijne, G., Johansson, S. (1999). Determination of the Border between the Transmembrane and Cytoplasmic Domains of Human Integrin Subunits. J. Biol. Chem. 274: 37030-37034 [Abstract] [Full Text]
Tang, S., Gao, Y., Ware, J. A. (1999). Enhancement of Endothelial Cell Migration and in Vitro Tube Formation by Tap20, a Novel {beta}5 Integrin-Modulating, Pkc{theta}-Dependent Protein. JCB 147: 1073-1084 [Abstract] [Full Text]
Phan, C., McMahon, A. W., Nelson, R. C., Elliott, J. F., Murray, A. G. (1999). Activated Lymphocytes Promote Endothelial Cell Detachment from Matrix: A Role for Modulation of Endothelial Cell {beta}1 Integrin Affinity. J. Immunol. 163: 4557-4563 [Abstract] [Full Text]