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Originally published In Press as doi:10.1074/jbc.M413541200 on December 28, 2004

J. Biol. Chem., Vol. 280, Issue 9, 8606-8616, March 4, 2005
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Induction of Proinflammatory Responses in Macrophages by the Glycosylphosphatidylinositols of Plasmodium falciparum

CELL SIGNALING RECEPTORS, GLYCOSYLPHOSPHATIDYLINOSITOL (GPI) STRUCTURAL REQUIREMENT, AND REGULATION OF GPI ACTIVITY*

Gowdahalli Krishnegowda{ddagger}§, Adeline M. Hajjar§¶||, Jianzhong Zhu{ddagger}§, Erika J. Douglass¶, Satoshi Uematsu**, Shizuo Akira**, Amina S. Woods{ddagger}{ddagger}, and D. Channe Gowda{ddagger}§§

From the {ddagger}Department of Biochemistry and Molecular Biology, Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033-0850, Department of Immunology, University of Washington, Seattle, Washington 98195, **Department of Host Defense, Research Institutes for Microbial Diseases, Osaka University, Osaka 565-0871, Japan, and {ddagger}{ddagger}NIDA, National Institutes of Health, Baltimore, Maryland 21224

The glycosylphosphatidylinositol (GPI) anchors of Plasmodium falciparum have been proposed to be the major factors that contribute to malaria pathogenesis through their ability to induce proinflammatory responses. In this study we identified the receptors for P. falciparum GPI-induced cell signaling that leads to proinflammatory responses and studied the GPI structure-activity relationship. The data show that GPI signaling is mediated mainly through recognition by TLR2 and to a lesser extent by TLR4. The activity of sn-2-lyso-GPIs is comparable with that of the intact GPIs, whereas the activity of Man3-GPIs is about 80% that of the intact GPIs. The GPIs with three (intact GPIs and Man3-GPIs) and two fatty acids (sn-2-lyso-GPIs) appear to differ considerably in the requirement of the auxiliary receptor, TLR1 or TLR6, for recognition by TLR2. The former are preferentially recognized by TLR2/TLR1, whereas the latter are favored by TLR2/TLR6. However, the signaling pathways initiated by all three GPI types are similar, involving the MyD88-dependent activation of extracellular signal-regulated kinase, c-Jun N-terminal kinase, and p38 and NF-{kappa}B-signaling pathways. The signaling molecules of these pathways differentially contribute to the production of various cytokines and nitric oxide (Zhu, J., Krishnegowda, G., and Gowda, D. C. (2004) J. Biol. Chem. 280, 8617-8627). Our data also show that GPIs are degraded by the macrophage surface phospholipases predominantly into inactive species, indicating that the host can regulate GPI activity at least in part by this mechanism. These results imply that macrophage surface phospholipases play important roles in the GPI-induced innate immune responses and malaria pathogenesis.

Received for publication, December 2, 2004 , and in revised form, December 17, 2004.

* This study was supported by National Institutes of Health Grants AI41139 (to D. C. G.) and HL69503 (to A. M. H.). 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.

§ These authors contributed equally.

|| To whom correspondence may be addressed: Dept. of Immunology, Box 357650, University of Washington, Seattle, WA 98195. Tel.: 206-221-2817; E-mail: hajjar{at}u.washington.edu.

§§ To whom correspondence may be addressed: Dept. of Biochemistry and Molecular Biology, Pennsylvania State University College of Medicine, 500 University Dr., Hershey, PA. Tel.: 717-531-0992; Fax: 717-531-7072; E-mail: gowda{at}psu.edu.


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