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EFFECT OF INFECTION BY PLASMODIUM FALCIPARUM ON THE MELANIZATION IMMUNE RESPONSE OF ANOPHELES GAMBIAE

Melanization is an immune response of mosquitoes that could potentially limit Plasmodium development. That mosquitoes rarely melanize Plasmodium falciparum in natural populations might result from immuno-suppression by the parasite, as has been observed in Aedes aegypti mosquitoes infected by Plasmodium gallinaceum. We tested this possibility in Anopheles gambiae mosquitoes infected by P. falciparum by comparing the ability to melanize a Sephadex bead of infected mosquitoes, of mosquitoes that had fed on infectious blood without becoming infected, and of control mosquitoes fed on uninfected blood. Rather than being immuno-suppressed, infected mosquitoes tended to have a stronger melanization response than mosquitoes in which the infection failed and than control mosquitoes, possibly because of immune activation after previous exposure to invading parasites. This finding suggests that P. falciparum relies on immune evasion rather than immuno-suppression to avoid being melanized and confirms that natural malaria transmission systems differ from laboratory models of mosquito–Plasmodium interactions.

Received September 13, 2006. Accepted for publication November 18, 2006.

Acknowledgments: We thank the inhabitants of Mfou for cooperation and Engelbert Manga, Constance Efemba, and Emmanuel Bozewan for kind support during the fieldwork in Mfou. The authors thank Isaac Tchikangwa for rearing mosquitoes, Rose Nyambam and Sylvie Kemleu-Zebaze for assistance in the screening of gametocyte carriers, Kristin Michel for help during the fieldwork and for the images of beads, Isabelle Thiéry for providing cultured P. falciparum gametocytes, and an anonymous reviewer for helpful comments on an earlier version of the manuscript.

Financial support: This study was supported by the VIHPAL Program of the French Ministry of Research.

^* Address correspondence to Louis Lambrechts, Department of Entomology, University of California, One Shields Ave., Davis, CA 95616. E-mail: llambrechts{at}ucdavis.edu

Authors’ addresses: Louis Lambrechts and Jacob C. Koella, Laboratoire de Parasitologie Evolutive, Unité Mixte de Recherche 7103, Centre National de la Recherche Scientifique-Université Pierre et Marie Curie, Case Courrier 237, 7 quai St Bernard, 75252 Paris Cedex 05, France, Telephone: 33144275204, Fax: 33144273516. Present address of Louis Lambrechts, Department of Entomology, University of California, One Shields Ave., Davis, CA 95616, Telephone: 5307520565, Fax: 5307521537. Present address of Jacob C. Koella, Division of Biology, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK, Telephone: 442075942254. Louis Lambrechts, Jean-Claude Jacques, and Catherine Bourgouin, Centre de Production et d’Infection des Anophèles, Institut Pasteur, 28 rue du Dr Roux, 75724 Paris Cedex 15, France, Telephone: 33144389577, Fax: 33140613089. Isabelle Morlais, Parfait H. Awono-Ambene, and Frédéric Simard, Laboratoire de Recherche sur le Paludisme, Institut de Recherche pour le Développement-Organisation de Coordination pour la Lutte contre les Endémies en Afrique Centrale, BP 288, Yaoundé, Cameroon, Telephone: 2372232232/9932111, Fax: 2372230061/2201854. Isabelle Morlais, Anna Cohuet, and Frédéric Simard, Unité de Caractérisation et Contrôle des Populations de Vecteurs, Institut de Recherche pour le Développement, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France, Telephone: 33467041924, Fax: 33467542044. Catherine Bourgouin, Unité de Biologie et Génétique du Paludisme, Institut Pasteur, 28 rue du Dr Roux, 75724 Paris Cedex 15, France, Telephone: 33145688224, Fax: 33140613089.

Reprints requests: Louis Lambrechts, Department of Entomology, University of California, One Shields Ave., Davis, CA 95616. E-mail: llambrechts{at}ucdavis.edu.