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Originally published In Press as doi:10.1074/jbc.M302907200 on April 10, 2003

J. Biol. Chem., Vol. 278, Issue 25, 22657-22663, June 20, 2003
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SHIP-2 Inositol Phosphatase Is Inducibly Expressed in Human Monocytes and Serves to Regulate Fc{gamma} Receptor-mediated Signaling*

Ruma A. Pengal {ddagger} §, Latha P. Ganesan § ¶, Huiqing Fang ¶, Clay B. Marsh ¶, Clark L. Anderson ¶ and Susheela Tridandapani ¶ ||

From the {ddagger}Molecular, Cellular, and Developmental Biology Program and the Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, Dorothy M. Davis Heart and Lung Institute, James Cancer Hospital and Comprehensive Cancer Center, Ohio State University, Columbus, Ohio 43210

SHIP-2, a recently identified inositol 5'-phosphatase, shares high level homology with SHIP-1. Although the role of SHIP-1 has been extensively studied, the role of SHIP-2 in myeloid cell functions is not known. Here, we have analyzed the expression patterns, molecular mechanism of activation, and function of SHIP-2 in human myeloid cell Fc{gamma} receptor (Fc{gamma}R) signaling. We report that SHIP-2 is expressed in transformed myeloid cells and in primary macrophages, but not in peripheral blood monocytes. Treatment of peripheral blood monocytes with bacterial lipopolysaccharide induced expression of SHIP-2 in a dose-dependent manner. Fc{gamma}RIIa clustering in THP-1 cells induced SHIP-2 tyrosine phosphorylation, suggesting a role for SHIP-2 in modulating Fc{gamma}R-mediated function. Consistent with this notion, overexpression of wild-type SHIP-2 (but not catalytically deficient SHIP-2) in THP-1 cells almost completely abrogated NF{kappa}B-mediated gene transcription in response to Fc{gamma}RIIa clustering. Furthermore, Fc{gamma}RIIa-induced Akt activation was blocked by wild-type SHIP-2, but not by a catalytically deficient mutant of SHIP-2. Additional experiments analyzing the molecular mechanism of SHIP-2 induction by Fc{gamma}RIIa revealed that SHIP-2 associated with the phosphorylated Fc{gamma}RIIa immunoreceptor tyrosine-based activation motif via the SHIP-2 SH2 domain. Thus, an SH2 domain mutant of SHIP-2 failed to associate with Fc{gamma}RIIa or to become tyrosine-phosphorylated upon Fc{gamma}RIIa clustering. Finally, we also demonstrate that SHIP-2 phosphorylation was induced by Fc{gamma}RI clustering in THP-1 cells. These findings unravel a novel level of regulation of Fc{gamma}R-mediated activation of human myeloid cells by the expression and function of the inositol phosphatase SHIP-2.


Received for publication, March 21, 2003 , and in revised form, April 8, 2003.

* This work was supported by National Institutes of Health Grants P30 CA16058, HL63800, and P01 CA095426. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Both authors contributed equally to this work.

|| Fellow of the Leukemia and Lymphoma Society. To whom correspondence should be addressed: Dept. of Internal Medicine, Ohio State University, Rm. 405B HLRI, 473 W. 12th Ave., Columbus, OH 43210. Tel.: 614-247-6768; Fax: 614-688-4662; E-mail: tridandapani.2{at}osu.edu.


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