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Marco Colonna^*, Francisco Navarro, Teresa Bellón, Manuel Llano, Pilar García, Jacqueline Samaridis^*, Lena Angman^*, Marina Cella^*, and Miguel López-Botet

From the ^* Basel Institute for Immunology, Basel CH-4005, Switzerland; and Hospital Universitario de la Princesa, 28006 Madrid, Spain

Natural killer (NK) cell–mediated lysis is negatively regulated by killer cell inhibitory receptors specific for major histocompatibility complex (MHC) class I molecules. In this study, we characterize a novel inhibitory MHC class I receptor of the immunoglobulin-superfamily, expressed not only by subsets of NK and T cells, but also by B cells, monocytes, macrophages, and dendritic cells. This receptor, called Ig-like transcript (ILT)2, binds MHC class I molecules and delivers a negative signal that inhibits killing by NK and T cells, as well as Ca²⁺ mobilization in B cells and myelomonocytic cells triggered through the B cell antigen receptor and human histocompatibility leukocyte antigens (HLA)–DR, respectively. In addition, myelomonocytic cells express receptors homologous to ILT2, which are characterized by extensive polymorphism and might recognize distinct HLA class I molecules. These results suggest that diverse leukocyte lineages have adopted recognition of self–MHC class I molecules as a common strategy to control cellular activation during an immune response.

The Basel Institute for Immunology was founded and is supported by Hoffmann-La Roche Ltd., Basel, Switzerland. The work at Hospital de la Princesa is supported by grants SAF96/0335 (Plan Nacional I+D) and PL950062 (European Commission). M. Llano is the recipient of a fellowship from the Fundacion Rich.

¹ Abbreviations used in this paper: DC, dendritic cell; ILT, Ig-like transcript; ITIM, immunoreceptor tyrosine-based inhibitory motifs; KIR, killer cell inhibitory receptor; RBL, rat basophilic leukemia; rADCC, reverse antibody-dependent cell-mediated cytoxicity; SF, superfamily; TSST, toxic shock syndrome toxin.

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• Shiroishi, M., Tsumoto, K., Amano, K., Shirakihara, Y., Colonna, M., Braud, V. M., Allan, D. S. J., Makadzange, A., Rowland-Jones, S., Willcox, B., Jones, E. Y., van der Merwe, P. A., Kumagai, I., Maenaka, K. (2003). Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc. Natl. Acad. Sci. USA 100: 8856-8861 [Abstract] [Full Text]  
• Achdout, H., Arnon, T. I., Markel, G., Gonen-Gross, T., Katz, G., Lieberman, N., Gazit, R., Joseph, A., Kedar, E., Mandelboim, O. (2003). Enhanced Recognition of Human NK Receptors After Influenza Virus Infection. J. Immunol. 171: 915-923 [Abstract] [Full Text]  
• Stewart, C. A., van Bergen, J., Trowsdale, J. (2003). Different and Divergent Regulation of the KIR2DL4 and KIR3DL1 Promoters. J. Immunol. 170: 6073-6081 [Abstract] [Full Text]  
• Urdahl, K. B., Liggitt, D., Bevan, M. J. (2003). CD8+ T Cells Accumulate in the Lungs of Mycobacterium tuberculosis-Infected Kb-/-Db-/- Mice, But Provide Minimal Protection. J. Immunol. 170: 1987-1994 [Abstract] [Full Text]  
• Borges, L., Kubin, M., Kuhlman, T. (2003). LIR9, an immunoglobulin-superfamily-activating receptor, is expressed as a transmembrane and as a secreted molecule. Blood 101: 1484-1486 [Abstract] [Full Text]  
• Moreau, P., Mouillot, G., Rousseau, P., Marcou, C., Dausset, J., Carosella, E. D. (2003). HLA-G gene repression is reversed by demethylation. Proc. Natl. Acad. Sci. USA 100: 1191-1196 [Abstract] [Full Text]  
• Ibrahim, E. C., Allory, Y., Commo, F., Gattegno, B., Callard, P., Paul, P. (2003). Altered Pattern of Major Histocompatibility Complex Expression in Renal Carcinoma: Tumor-Specific Expression of the Nonclassical Human Leukocyte Antigen-G Molecule Is Restricted to Clear Cell Carcinoma While Up-Regulation of Other Major Histocompatibility Complex Antigens Is Primarily Distributed in All Subtypes of Renal Carcinoma. Am. J. Pathol. 162: 501-508 [Abstract] [Full Text]  
• Radaev, S., Kattah, M., Zou, Z., Colonna, M., Sun, P. D. (2002). Making Sense of the Diverse Ligand Recognition by NKG2D. J. Immunol. 169: 6279-6285 [Abstract] [Full Text]  
• Feldhahn, N., Schwering, I., Lee, S., Wartenberg, M., Klein, F., Wang, H., Zhou, G., Wang, S. M., Rowley, J. D., Hescheler, J., Kronke, M., Rajewsky, K., Kuppers, R., Muschen, M. (2002). Silencing of B Cell Receptor Signals in Human Naive B Cells. JEM 196: 1291-1305 [Abstract] [Full Text]  
• Chwae, Y.-J., Chang, M. J., Park, S. M., Yoon, H., Park, H.-J., Kim, S. J., Kim, J. (2002). Molecular Mechanism of the Activation-Induced Cell Death Inhibition Mediated by a p70 Inhibitory Killer Cell Ig-Like Receptor in Jurkat T Cells. J. Immunol. 169: 3726-3735 [Abstract] [Full Text]  
• Guerra, N., Michel, F., Gati, A., Gaudin, C., Mishal, Z., Escudier, B., Acuto, O., Chouaib, S., Caignard, A. (2002). Engagement of the inhibitory receptor CD158a interrupts TCR signaling, preventing dynamic membrane reorganization in CTL/tumor cell interaction. Blood 100: 2874-2881 [Abstract] [Full Text]  
• Farag, S. S., Fehniger, T. A., Ruggeri, L., Velardi, A., Caligiuri, M. A. (2002). Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood 100: 1935-1947 [Abstract] [Full Text]  
• Nikolova, M., Musette, P., Bagot, M., Boumsell, L., Bensussan, A. (2002). Engagement of ILT2/CD85j in Sezary syndrome cells inhibits their CD3/TCR signaling. Blood 100: 1019-1025 [Abstract] [Full Text]  
• Dulphy, N., Rabian, C., Douay, C., Flinois, O., Laoussadi, S., Kuipers, J., Tamouza, R., Charron, D., Toubert, A. (2002). Functional modulation of expanded CD8+ synovial fluid T cells by NK cell receptor expression in HLA-B27-associated reactive arthritis. Int Immunol 14: 471-479 [Abstract] [Full Text]  
• Miller, I., Hatzivassiliou, G., Cattoretti, G., Mendelsohn, C., Dalla-Favera, R. (2002). IRTAs: a new family of immunoglobulinlike receptors differentially expressed in B cells. Blood 99: 2662-2669 [Abstract] [Full Text]  
• Bellon, T., Kitzig, F., Sayos, J., Lopez-Botet, M. (2002). Mutational Analysis of Immunoreceptor Tyrosine-Based Inhibition Motifs of the Ig-Like Transcript 2 (CD85j) Leukocyte Receptor. J. Immunol. 168: 3351-3359 [Abstract] [Full Text]  
• Markel, G., Lieberman, N., Katz, G., Arnon, T. I., Lotem, M., Drize, O., Blumberg, R. S., Bar-Haim, E., Mader, R., Eisenbach, L., Mandelboim, O. (2002). CD66a Interactions Between Human Melanoma and NK Cells: A Novel Class I MHC-Independent Inhibitory Mechanism of Cytotoxicity. J. Immunol. 168: 2803-2810 [Abstract] [Full Text]  
• Rieger, L., Hofmeister, V., Probe, C., Dietl, J., Weiss, E.H., Steck, T., Kammerer, U. (2002). Th1- and Th2-like cytokine production by first trimester decidual large granular lymphocytes is influenced by HLA-G and HLA-E. Mol Hum Reprod 8: 255-261 [Abstract] [Full Text]  
• Tedla, N., Gibson, K., McNeil, H. P., Cosman, D., Borges, L., Arm, J. P. (2002). The Co-Expression of Activating and Inhibitory Leukocyte Immunoglobulin-Like Receptors in Rheumatoid Synovium. Am. J. Pathol. 160: 425-431 [Abstract] [Full Text]  
• Urosevic, M., Willers, J., Mueller, B., Kempf, W., Burg, G., Dummer, R. (2002). HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood 99: 609-617 [Abstract] [Full Text]  
• Kim, N., Takami, M., Rho, J., Josien, R., Choi, Y. (2002). A Novel Member of the Leukocyte Receptor Complex Regulates Osteoclast Differentiation. JEM 195: 201-209 [Abstract] [Full Text]  
• Saverino, D., Merlo, A., Bruno, S., Pistoia, V., Grossi, C. E., Ciccone, E. (2002). Dual Effect of CD85/Leukocyte Ig-Like Receptor-1/Ig-Like Transcript 2 and CD152 (CTLA-4) on Cytokine Production by Antigen-Stimulated Human T Cells. J. Immunol. 168: 207-215 [Abstract] [Full Text]  
• Hurks, H. M. H., Valter, M. M., Wilson, L., Hilgert, I., van den Elsen, P. J., Jager, M. J. (2001). Uveal Melanoma: No Expression of HLA-G. IOVS 42: 3081-3084 [Abstract] [Full Text]  

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