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J. Biol. Chem., Vol. 282, Issue 35, 25376-25384, August 31, 2007

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Mosquito Heparan Sulfate and Its Potential Role in Malaria Infection and Transmission^*

Photini Sinnis, Alida Coppi, Toshihiko Toida, Hidenao Toyoda, Akiko Kinoshita-Toyoda, Jin Xie^¶, Melissa M. Kemp^¶, and Robert J. Linhardt^¶1

From the Department of Medical Parasitology, New York University School of Medicine, New York, New York 10010, the Graduate School of Pharmaceutical Sciences, Chiba University, 1-33, Yayoi, Inage-ku, Chiba 263-8522, Japan, and the ^¶Center for Biocatalysis and Interdisciplinary Studies and Departments of Chemistry, Biology, and Chemical Engineering, Rensselaer Polytechnic Institute, Troy, New York, 12180

Heparan sulfate has been isolated for the first time from the mosquito Anopheles stephensi, a known vector for Plasmodium parasites, the causative agents of malaria. Chondroitin sulfate, but not dermatan sulfate or hyaluronan, was also present in the mosquito. The glycosaminoglycans were isolated, from salivary glands and midguts of the mosquito in quantities sufficient for disaccharide microanalysis. Both of these organs are invaded at different stages of the Plasmodium life cycle. Mosquito heparan sulfate was found to contain the critical trisulfated disaccharide sequence, 4)-D-GlcNS6S(1 4)--L-IdoA2S(1, that is commonly found in human liver heparan sulfate, which serves as the receptor for apolipoprotein E and is also believed to be responsible for binding to the circumsporozoite protein found on the surface of the Plasmodium sporozoite. The heparan sulfate isolated from the whole mosquito binds to circumsporozoite protein, suggesting a role within the mosquito for infection and transmission of the Plasmodium parasite.

Received for publication, June 7, 2007

^* This work was supported in part by National Institutes of Health Grants HL62244, HL52622, and GM38060 (to R. J. L.) and AI056840 (to P. S.). 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.

¹ To whom correspondence should be addressed. Tel.: 518-276-3404; Fax: 518-276-3405; E-mail: linhar{at}rpi.edu.

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