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J. Biol. Chem., Vol. 279, Issue 10, 9490-9496, March 5, 2004

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A Role for Apical Membrane Antigen 1 during Invasion of Hepatocytes by Plasmodium falciparum Sporozoites^*

From the ^aINSERM U511, Immunobiologie Cellulaire et Moléculaire des Infections Parasitaires, Centre Hospitalo-Universitaire Pitié-Salpêtrière, Université Pierre et Marie Curie, 75013 Paris, France, ^cINSERM U268, Institut André-Lwoff, Université Paris XI, Hôpital Paul-Brousse, 94807 Villejuif, France, ^dMolecular Immunology, Swiss Tropical Institute, CH-4002 Basel, Switzerland, the ^eService de Chirurgie Digestive, Hépato-Bilio-Pancréatique et Transplantation Hépatique, Hôpital Pitié-Salpêtrière, 75013 Paris, France, the ^fMalaria Program, Naval Medical Research Center, Silver Spring, Massachusetts 20910, the ^gBiomedical Primate Research Centre, Department of Parasitology, 2280 GH Rijswijk, The Netherlands, the ^hDepartment of Medical Microbiology, University Medical Centre St. Radboud, 6500 HB Nijmegen, The Netherlands, the ⁱDivision of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA, United Kingdom, and the ^jDepartment of Biochemistry and Cooperative Research Centre for Vaccine Technology, La Trobe University, Victoria 3086, Australia

Plasmodium sporozoites are transmitted through the bite of infected mosquitoes and invade hepatocytes as a first and obligatory step of the parasite life cycle in man. Hepatocyte invasion involves proteins secreted from parasite vesicles called micronemes, the most characterized being the thrombospondin-related adhesive protein (TRAP). Here we investigated the expression and function of another microneme protein recently identified in Plasmodium falciparum sporozoites, apical membrane antigen 1 (AMA-1). P. falciparum AMA-1 is expressed in sporozoites and is lost after invasion of hepatocytes, and anti-AMA-1 antibodies inhibit sporozoite invasion, suggesting that the protein is involved during invasion of hepatocytes. As observed with TRAP, AMA-1 is initially mostly sequestered within the sporozoite. Upon microneme exocytosis, AMA-1 and TRAP relocate to the sporozoite surface, where they are proteolytically cleaved, resulting in the shedding of soluble fragments. A subset of serine protease inhibitors blocks the processing and shedding of both AMA-1 and TRAP and inhibits sporozoite infectivity, suggesting that interfering with sporozoite proteolytic processing may constitute a valuable strategy to prevent hepatocyte infection.

Received for publication, October 15, 2003 , and in revised form, December 6, 2003.

^* 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.

^b To whom correspondence should be addressed: INSERM U511, Faculté de Médecine Pitié-Salpêtrière, 91 Blvd. de l'Hôpital, 75013 Paris, France. Tel.: 33-1-40-77-97-36; Fax: 33-1-45-83-88-58; E-mail: silvie{at}ext.jussieu.fr.

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