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J. Biol. Chem., Vol. 279, Issue 6, 4648-4656, February 6, 2004

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Characterization of a Membrane-associated Rhoptry Protein of Plasmodium falciparum^*

Agnieszka E. Topolska, Angela Lidgett, Dirk Truman, Hisashi Fujioka¶, and Ross L. Coppel||

From the Department of Microbiology, Monash University, Wellington Road, Clayton 3800, Victoria, Australia and the ^¶Institute of Pathology, Case Western Reserve University, Cleveland, Ohio 44106

Invasive forms of apicomplexan parasites contain secretory organelles called rhoptries that are essential for entry into host cells. We present a detailed characterization of an unusual rhoptry protein of the human malaria parasite Plasmodium falciparum, the rhoptry-associated membrane antigen (RAMA) that appears to have roles in both rhoptry biogenesis and host cell invasion. RAMA is synthesized as a 170-kDa protein in early trophozoites, several hours before rhoptry formation and is transiently localized within the endoplasmic reticulum and Golgi within lipid-rich microdomains. Regions of the Golgi membrane containing RAMA bud to form vesicles that later mature into rhoptries in a process that is inhibitable by brefeldin A. Other rhoptry proteins such as RhopH3 and RAP1 are found in close apposition with RAMA suggesting direct protein-protein interactions. We suggest that RAMA is involved in trafficking of these proteins into rhoptries. In rhoptries, RAMA is proteolytically processed to give a 60-kDa form that is anchored in the inner face of the rhoptry membrane by means of the glycosylphosphatidylinositol anchor. The p60 RAMA form is discharged from the rhoptries of free merozoites and binds to the red blood cell membrane by its most C-terminal region. In early ring stages RAMA is found in association with the parasitophorous vacuole.

Received for publication, July 21, 2003 , and in revised form, November 7, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY324391.

^* This work was supported in part by the National Institutes of Health Grant DK-32094, the Howard Hughes Medical Institute International Scholars Program, and 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.

Recipient of the Monash Graduate Scholarship.

^|| To whom correspondence should be addressed: Dept. of Microbiology, P. O. Box 53, Monash University, Clayton 3800, Victoria, Australia. Tel.: 61-3-9905-4822; Fax: 61-3-9905-9772; E-mail: ross.coppel{at}med.monash.edu.au.

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