Involvement of the "I" domain of LFA-1 in selective binding to ligands ICAM-1 and ICAM-3

doi:10.1083/jcb.126.2.529

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Involvement of the "I" domain of LFA-1 in selective binding to ligands ICAM-1 and ICAM-3

RC Landis, A McDowall, CL Holness, AJ Littler, DL Simmons and N Hogg
Leukocyte Adhesion Laboratory, Imperial Cancer Research Fund, London, United Kingdom.

To analyze the binding requirements of LFA-1 for its two most homologous ligands, ICAM-1 and ICAM-3, we compared the effects of various LFA-1 activation regimes and a panel of anti-LFA-1 mAbs in T cell binding assays to ICAM-1 or ICAM-3 coated on plastic. These studies demonstrated that T cell binding to ICAM-3 was inducible both from the exterior of the cell by Mn2+ and from the interior by an agonist of the "inside-out" signaling pathway. T cells bound both ICAM ligands with comparable avidity. A screen of 29 anti-LFA-1 mAbs led to the identification of two mAbs specific for the alpha subunit of LFA-1 which selectively blocked adhesion of T cells to ICAM-3 but not ICAM-1. These two mAbs, YTH81.5 and 122.2A5, exhibited identical blocking properties in a more defined adhesion assay using LFA-1 transfected COS cells binding to immobilized ligand. Blocking was not due to a steric interference between anti-LFA-1 mAbs and N-linked carbohydrate residues present on ICAM-3 but not ICAM-1. The epitopes of mAbs YTH81.5 and 122.2A5 were shown to map to the I domain of the LFA-1 alpha subunit. A third I domain mAb, MEM-83, has been previously reported to uniquely activate LFA-1 to bind ICAM-1 (Landis, R. C., R. I. Bennett, and N. Hogg. 1993. J. Cell Biol. 120:1519-1527). We now show that mAb MEM-83 is not able to stimulate binding of T cells to ICAM-3 over a wide concentration range. Failure to induce ICAM-3 binding by mAb MEM-83 was not due to a blockade of the ICAM-3 binding site on LFA-1. This study has demonstrated that two sets of functionally distinct mAbs recognizing epitopes in the I domain of LFA-1 are able to exert differential effects on the binding of LFA-1 to its ligands ICAM-1, and ICAM-3. These results suggest for the first time that LFA-1 is capable of binding these two highly homologous ligands in a selective manner and that the I domain plays a role in this process.
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Pozo, M. A. d., Cabanas, C., Montoya, M. C., Ager, A., Sanchez-Mateos, P., Sanchez-Madrid, F. (1997). ICAMs Redistributed by Chemokines to Cellular Uropods as a Mechanism for Recruitment of T Lymphocytes. JCB 137: 493-508 [Abstract] [Full Text]
Dickeson, S. K., Walsh, J. J., Santoro, S. A. (1997). Contributions of the I and EF Hand Domains to the Divalent Cation-dependent Collagen Binding Activity of the alpha 2beta 1 Integrin. J. Biol. Chem. 272: 7661-7668 [Abstract] [Full Text]
Mizuno, T., Yoshihara, Y., Inazawa, J., Kagamiyama, H., Mori, K. (1997). cDNA Cloning and Chromosomal Localization of the Human Telencephalin and Its Distinctive Interaction with Lymphocyte Function-associated Antigen-1. J. Biol. Chem. 272: 1156-1163 [Abstract] [Full Text]
Klickstein, L. B., York, M. R., Fougerolles, A. R.d., Springer, T. A. (1996). Localization of the Binding Site on Intercellular Adhesion Molecule-3 (ICAM-3) for Lymphocyte Function-associated Antigen 1(LFA-1). J. Biol. Chem. 271: 23920-23927 [Abstract] [Full Text]
Binnerts, M. E., van Kooyk, Y., Edwards, C. P., Champe, M., Presta, L., Bodary, S. C., Figdor, C. G., Berman, P. W. (1996). Antibodies That Selectively Inhibit Leukocyte Function-associated Antigen 1 Binding to Intercellular Adhesion Molecule-3 Recognize a Unique Epitope within the CD11a I Domain. J. Biol. Chem. 271: 9962-9968 [Abstract] [Full Text]
Buckley, C., Doyonnas, R, Newton, J., Blystone, S., Brown, E., Watt, S., Simmons, D. (1996). Identification of alpha v beta 3 as a heterotypic ligand for CD31/PECAM-1. J. Cell Sci. 109: 437-445 [Abstract]
Garnotel, R., Monboisse, J.-C., Randoux, A., Haye, B., Borel, J. P. (1995). The Binding of Type I Collagen to Lymphocyte Function-associated Antigen (LFA) 1 Integrin Triggers the Respiratory Burst of Human Polymorphonuclear Neutrophils. J. Biol. Chem. 270: 27495-27503 [Abstract] [Full Text]
Huang, C., Springer, T. A. (1995). A Binding Interface on the I Domain of Lymphocyte Function-associated Antigen-1 (LFA-1) Required for Specific Interaction with Intercellular Adhesion Molecule 1 (ICAM-1). J. Biol. Chem. 270: 19008-19016 [Abstract] [Full Text]
Edwards, C. P., Champe, M., Gonzalez, T., Wessinger, M. E., Spencer, S. A., Presta, L. G., Berman, P. W., Bodary, S. C. (1995). Identification of Amino Acids in the CD11a I-domain Important for Binding of the Leukocyte Function-associated Antigen-1 (LFA-1) to Intercellular Adhesion Molecule-1 (ICAM-1). J. Biol. Chem. 270: 12635-12640 [Abstract] [Full Text]
Holness, C. L., Bates, P. A., Littler, A. J., Buckley, C. D., McDowall, A., Bossy, D., Hogg, N., Simmons, D. L. (1995). Analysis of the Binding Site on Intercellular Adhesion Molecule 3 for the Leukocyte Integrin Lymphocyte Function-associated Antigen 1. J. Biol. Chem. 270: 877-884 [Abstract] [Full Text]