Volume 76, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


Melanization is an immune response of mosquitoes that could potentially limit development. That mosquitoes rarely melanize in natural populations might result from immuno-suppression by the parasite, as has been observed in mosquitoes infected by . We tested this possibility in mosquitoes infected by 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 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– interactions.


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  1. Christophides GK, 2005. Transgenic mosquitoes and malaria transmission. Cell Microbiol 7 : 325–333.
  2. Richman A, Kafatos FC, 1996. Immunity to eukaryotic parasites in vector insects. Curr Opin Immunol 8 : 14–19.
  3. Tahar R, Boudin C, Thiéry I, Bourgouin C, 2002. Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J 21 : 6673–6680.
  4. Michel K, Kafatos FC, 2005. Mosquito immunity against Plasmodium. Insect Biochem Mol Biol 35 : 677–689.
  5. Gouagna LC, Mulder B, Noubissi E, Tchuinkam T, Verhave JP, Boudin C, 1998. The early sporogonic cycle of Plasmodium falciparum in laboratory-infected Anopheles gambiae: An estimation of parasite efficacy. Trop Med Int Health 3 : 21–28.
  6. Vaughan JA, Noden BH, Beier JC, 1992. Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. J Parasitol 78 : 716–724.
  7. Christensen BM, Li J, Chen CC, Nappi AJ, 2005. Melanization immune responses in mosquito vectors. Trends Parasitol 21 : 192–199.
  8. Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC, Gwadz RW, 1986. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234 : 607–610.
  9. Paskewitz SM, Brown MR, Lea AO, Collins FH, 1988. Ultra-structure of the encapsulation of Plasmodium cynomolgi (B strain) on the midgut of a refractory strain of Anopheles gambiae. J Parasitol 74 : 432–439.
  10. Osta MA, Christophides GK, Kafatos FC, 2004. Effects of mosquito genes on Plasmodium development. Science 303 : 2030–2032.
  11. Michel K, Budd A, Pinto S, Gibson TJ, Kafatos FC, 2005. Anopheles gambiae SRPN2 facilitates midgut invasion by the malaria parasite Plasmodium berghei. EMBO Rep 6 : 891–897.
  12. Volz J, Osta MA, Kafatos FC, Muller HM, 2005. The roles of two clip domain serine proteases in innate immune responses of the malaria vector Anopheles gambiae. J Biol Chem 280 : 40161–40168.
  13. Abraham EG, Pinto SB, Ghosh A, Vanlandingham DL, Budd A, Higgs S, Kafatos FC, Jacobs-Lorena M, Michel K, 2005. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci USA 102 : 16327–16332.
  14. Schwartz A, Koella JC, 2002. Melanization of Plasmodium falciparum and C-25 sephadex beads by field-caught Anopheles gambiae (Diptera: Culicidae) from southern Tanzania. J Med Entomol 39 : 84–88.
  15. Adini A, Warburg A, 1999. Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins. Parasitology 119 : 331–336.
  16. Li X, Webb BA, 1994. Apparent functional role for a cysteine-rich polydnavirus protein in suppression of the insect cellular immune response. J Virol 68 : 7482–7489.
  17. Rosqvist R, Forsberg A, Rimpilainen M, Bergman T, Wolf-Watz H, 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol 4 : 657–667.
  18. Rosqvist R, Forsberg A, Wolf-Watz H, 1991. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun 59 : 4562–4569.
  19. Bouarab K, Melton R, Peart J, Baulcombe D, Osbourn A, 2002. A saponin-detoxifying enzyme mediates suppression of plant defences. Nature 418 : 889–892.
  20. Lindmark H, Johansson KC, Stoven S, Hultmark D, Engstrom Y, Soderhall K, 2001. Enteric bacteria counteract lipopolysaccharide induction of antimicrobial peptide genes. J Immunol 167 : 6920–6923.
  21. Boëte C, Paul RE, Koella JC, 2002. Reduced efficacy of the immune melanization response in mosquitoes infected by malaria parasites. Parasitology 125 : 93–98.
  22. Boëte C, Paul RE, Koella JC, 2004. Direct and indirect immunosuppression by a malaria parasite in its mosquito vector. Proc R Soc Lond B Biol Sci 271 : 1611–1615.
  23. Boëte C, 2005. Malaria parasites in mosquitoes: Laboratory models, evolutionary temptation and the real world. Trends Parasitol 21 : 445–447.
  24. Paskewitz S, Riehle MA, 1994. Response of Plasmodium refractory and susceptible strains of Anopheles gambiae to inoculated Sephadex beads. Dev Comp Immunol 18 : 369–375.
  25. Lensen AH, Van Gemert GJ, Bolmer MG, Meis JF, Kaslow D, Meuwissen JH, Ponnudurai T, 1992. Transmission blocking antibody of the Plasmodium falciparum zygote/ookinete surface protein Pfs25 also influences sporozoite development. Parasite Immunol 14 : 471–479.
  26. Vermeulen AN, van Deursen J, Brakenhoff RH, Lensen TH, Ponnudurai T, Meuwissen JH, 1986. Characterization of Plasmodium falciparum sexual stage antigens and their biosynthesis in synchronised gametocyte cultures. Mol Biochem Parasitol 20 : 155–163.
  27. Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, Carnevale P, Meuwissen JH, Robert V, 1993. Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: Factors influencing the infectivity to mosquitoes. Trop Med Parasitol 44 : 271–276.
  28. Koella JC, Lyimo EO, 1996. Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). J Med Entomol 33 : 261–264.
  29. Rigaud T, Moret Y, 2003. Differential phenoloxidase activity between native and invasive gammarids infected by local acan-thocephalans: Differential immunosuppression? Parasitology 127 : 571–577.
  30. Koella JC, Boëte C, 2003. A model for the coevolution of immunity and immune evasion in vector-borne diseases with implications for the epidemiology of malaria. Am Nat 161 : 698–707.
  31. Cotter SC, Kruuk LE, Wilson K, 2004. Costs of resistance: Genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17 : 421–429.
  32. Riehle MM, Markianos K, Niare O, Xu J, Li J, Toure AM, Podiougou B, Oduol F, Diawara S, Diallo M, Coulibaly B, Ouatara A, Kruglyak L, Traore SF, Vernick KD, 2006. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312 : 577–579.
  33. Lambrechts L, Vulule JM, Koella JC, 2004. Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambiae. Evolution Int J Org Evolution 58 : 2377–2381.
  34. Baton LA, Ranford-Cartwright LC, 2005. How do malaria ookinetes cross the mosquito midgut wall? Trends Parasitol 21 : 22–28.
  35. Moret Y, Siva-Jothy MT, 2003. Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 270 : 2475–2480.
  36. Luckhart S, Vodovotz Y, Cui L, Rosenberg R, 1998. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci USA 95 : 5700–5705.
  37. Zambrano-Villa S, Rosales-Borjas D, Carrero JC, Ortiz-Ortiz L, 2002. How protozoan parasites evade the immune response. Trends Parasitol 18 : 272–278.
  38. Warr E, Lambrechts L, Koella JC, Bourgouin C, Dimopoulos G, 2006. Anopheles gambiae immune responses to Sephadex beads: Involvement of anti-Plasmodium factors in regulating melanization. Insect Biochem Mol Biol 36 : 769–778.
  39. Aguilar R, Dong Y, Warr E, Dimopoulos G, 2005. Anopheles infection responses; laboratory models versus field malaria transmission systems. Acta Trop 95 : 285–291.

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  • Received : 13 Sep 2006
  • Accepted : 18 Nov 2006

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