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J. Biol. Chem., Vol. 280, Issue 48, 40169-40176, December 2, 2005

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Distinct Protein Classes Including Novel Merozoite Surface Antigens in Raft-like Membranes of Plasmodium falciparum^*

Paul R. Sanders¶1, Paul R. Gilson, Greg T. Cantin||, Doron C. Greenbaum2, Thomas Nebl, Daniel J. Carucci**, Malcolm J. McConville3, Louis Schofield3, Anthony N. Hodder, John R. Yates, III||, and Brendan S. Crabb34

From the The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC 3050 Australia, The Co-operative Research Centre for Vaccine Technology, Australia and the ^¶Department of Medical Biology, The University of Melbourne, VIC 3010 Australia, the ^||Department of Cell Biology, The Scripps Research Institute, La, Jolla, California 92037, ^**The Foundation for the National Institutes of Health, Bethesda, Maryland 20814, and the Department of Biochemistry and Molecular Biology, The University of Melbourne, VIC 3050 Australia

Glycosylphosphatidylinositol (GPI)-anchored proteins coat the surface of extracellular Plasmodium falciparum merozoites, of which several are highly validated candidates for inclusion in a blood-stage malaria vaccine. Here we determined the proteome of gradient-purified detergent-resistant membranes of mature blood-stage parasites and found that these membranes are greatly enriched in GPI-anchored proteins and their putative interacting partners. Also prominent in detergent-resistant membranes are apical organelle (rhoptry), multimembrane-spanning, and proteins destined for export into the host erythrocyte cytosol. Four new GPI-anchored proteins were identified, and a number of other novel proteins that are predicted to localize to the merozoite surface and/or apical organelles were detected. Three of the putative surface proteins possessed six-cysteine (Cys₆) motifs, a distinct fold found in adhesive surface proteins expressed in other life stages. All three Cys₆ proteins, termed Pf12, Pf38, and Pf41, were validated as merozoite surface antigens recognized strongly by antibodies present in naturally infected individuals. In addition to the merozoite surface, Pf38 was particularly prominent in the secretory apical organelles. A different cysteine-rich putative GPI-anchored protein, Pf92, was also localized to the merozoite surface. This insight into merozoite surfaces provides new opportunities for understanding both erythrocyte invasion and anti-parasite immunity.

Received for publication, September 1, 2005 , and in revised form, September 29, 2005.

^* This work was supported by the National Health and Medical Research Council of Australia. 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.

The on-line version of this article (available at http://www.jbc.org) contains two supplemental figures and two supplemental tables.

¹ Recipient of an Australian Postgraduate Research Award

² Recipient of a Human Frontiers long-term fellowship.

³ International Research Scholars of the Howard Hughes Medical Institute.

⁴ To whom correspondence should be addressed: The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, VIC 3050, Australia. Tel.: 61-3-9345-2555; Fax: 61-3-9347-0852; E-mail: crabb{at}wehi.edu.au.

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