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Originally published In Press as doi:10.1074/jbc.M003518200 on October 2, 2000

J. Biol. Chem., Vol. 275, Issue 48, 37357-37364, December 1, 2000
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Molecular Basis of the Recruitment of the SH2 Domain-containing Inositol 5-Phosphatases SHIP1 and SHIP2 by Fcgamma RIIB*

Pierre BruhnsDagger §, Frédéric Vély, Odile MalbecDagger , Wolf H. FridmanDagger , Eric Vivier, and Marc DaëronDagger ||

From the Dagger  Laboratoire d'Immunologie Cellulaire et Clinique, INSERM U255, Institut Curie, 75005 Paris, France and the  Centre d'Immunologie INSERM-CNRS de Marseille-Luminy, 13288 Marseille, France

Fcgamma RIIB are single-chain low affinity receptors for IgG that negatively regulate immunoreceptor tyrosine-based activation motif-dependent cell activation. They bear one immunoreceptor tyrosine-based inhibition motif (ITIM) that becomes tyrosyl-phosphorylated upon coaggregation of Fcgamma RIIB with immunoreceptor tyrosine-based activation motif-bearing receptors and that recruits SH2 domain-containing inositol 5-phosphatases (SHIPs) in vivo. Synthetic Fcgamma RIIB ITIM phosphopeptides, however, also bind SH2 domain-containing protein-tyrosine phosphatases (SHPs) in vitro. To identify SHIP-binding sites, we exchanged residues between the Fcgamma RIIB ITIM and the N-terminal ITIM of a killer cell Ig-like receptor that does not bind SHIPs. Loss of function and gain of function substitutions identified the Y+2 leucine, in the Fcgamma RIIB ITIM, as determining the binding of both SHIP1 and SHIP2, but not the binding of SHP-1 or SHP-2. Conversely, the Y-2 isoleucine that determines the in vitro binding of SHP-1 and SHP-2 affected neither the binding nor the recruitment of SHIP1 or SHIP2. One hydrophobic residue, in the ITIM of Fcgamma RIIB therefore determines the affinity for SHIPs. This residue is symmetrical to the hydrophobic residue that determines the affinity of all ITIMs for SHPs. It defines a SHIP-binding site, distinct from a SHP-binding site, that enables Fcgamma RIIB to recruit SHIP1 and SHIP2 and that is preferentially used in vivo.

* This work was supported by the Institut National de la Santé et de la Recherche Médicale, the Association pour la Recherche sur le Cancer, and the Institut Curie.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Recipient of a fellowship from the Association pour la Recherche sur le Cancer.

|| To whom correspondence should be addressed: Lab. d'Immunologie Cellulaire et Clinique, INSERM U255, Institut Curie, 26 rue d'Ulm, 75005 Paris, France. E-mail: Marc.Daeron@curie.fr.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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