Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa

PLoS Pathogens

Volumn 4, Issue 5, 2008, Pages

  Mendes, Antonio M ^a   Schlegelmilch, Timm ^a   Cohuet, Anna ^b   Awono Ambene, Parfait ^c   De Iorio, Maria ^a   Fontenille, Didier ^b   Morlais, Isabelle ^c   Christophides, George K ^a   Kafatos, Fotis C ^a   Vlachou, Dina ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^c Laboratoire de Recherche sur le Paludisme Yaounde   (Cameroon)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; LIPID TRANSFER PROTEIN; PROTEIN APOII I; PROTEIN WASP; APOLIPOPROTEIN A1; APOLIPOPROTEIN A2; PROTOZOAL DNA; WISKOTT ALDRICH SYNDROME PROTEIN;

AFRICA; ANOPHELES GAMBIAE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; EVOLUTION; GENE SILENCING; GENETIC TRANSCRIPTION; HEMOLYMPH; HOST PARASITE INTERACTION; MALARIA; MOSQUITO; NONHUMAN; OOCYST; PARASITE DEVELOPMENT; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; REGULATOR GENE; ANIMAL; BLOOD; CHILD; DIGESTIVE SYSTEM; DISEASE CARRIER; DISEASE TRANSMISSION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; HUMAN; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PRESCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM;

ANOPHELES GAMBIAE; PLASMODIUM FALCIPARUM; RODENTIA;

ANIMALS; ANOPHELES GAMBIAE; APOLIPOPROTEIN A-I; APOLIPOPROTEIN A-II; CHILD; CHILD, PRESCHOOL; DIGESTIVE SYSTEM; DISEASE VECTORS; DNA, PROTOZOAN; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC PREDISPOSITION TO DISEASE; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA, FALCIPARUM; OOCYSTS; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; TRANSCRIPTION, GENETIC; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 44649094083     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000069     Document Type: Article

References (53)

1. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670.
2. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52. doi:10.1371/journal.ppat.0020052.
3. 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.
4. Osta MA, Christophides GK, Kafatos FC (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030-2032.
5. Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC (2005) Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 15: 1185-1195.
6. Volz J, Muller HM, Zdanowicz A, Kafatos FC, Osta MA (2006) A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell Microbiol 8: 1392-1405.
7. Sinden RE, Alavi Y, Raine JD (2004) Mosquito-malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness. Insect Biochem Mol Biol 34: 625-629.
8. Lambrechts L, Halbert J, Durand P, Gouagna LC, Koella JC (2005) Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar J 4: 3.
9. Menge DM, Zhong D, Guda T, Gouagna L, Githure J, et al. (2006) Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya. Genetics 173: 235-241.
10. Vernick KD, Oduol F, Lazzaro BP, Glazebrook J, Xu J, et al. (2005) Molecular genetics of mosquito resistance to malaria parasites. Curr Top Microbiol Immunol 295: 383-415.
11. Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, et al. (1986) Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234: 607-610.
12. Cohuet A, Osta MA, Morlais I, Awono-Ambene PH, Michel K, et al. (2006) Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep 7: 1285-1289.
13. Koella JC, Boete 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.
14. Riehle MM, Markianos K, Niare O, Xu J, Li J, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577-579.
15. 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.
16. Baton LA, Ranford-Cartwright LC (2005) How do malaria ookinetes cross the mosquito midgut wall? Trends Parasitol 21: 22-28.
17. Vlachou D, Kafatos FC (2005) The complex interplay between mosquito positive and negative regulators of Plasmodium development. Curr Opin Microbiol 8: 415-421.
18. Meister S, Kanzok SM, Zheng XL, Luna C, Li TR, et al. (2005) Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 102: 11420-11425.
19. Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, et al. (2002) Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci U S A 99: 8814-8819.
20. Weers PM, Ryan RO (2006) Apolipophorin III: role model apolipoprotein. Insect Biochem Mol Biol 36: 231-240.
21. Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, et al. (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.
22. Arias L, Bejarana EE, Marquez E, Moncada J, Velez I, Uribe S (2005) Mitochondrial DNA divergence between wild and laboratory populations of Anopheles albimanus Wiedemann (Diptera: Culicidae). Neotropical Entomology 34: 499-506.
23. Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, et al. (1997) Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science 276: 425-428.
24. Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, et al. (2002) Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep 3: 852-856.
25. Marinotti O, Capurro Mde L, Nirmala X, Calvo E, James AA (2006) Structure and expression of the lipophorin-encoding gene of the malaria vector, Anopheles gambiae. Comp Biochem Physiol B Biochem Mol Biol 144: 101-109.
26. Tahar R, Boudin C, Thiery 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.
27. Atella GC, Silva-Neto MA, Golodne DM, Arefin S, Shahabuddin M (2006) Anopheles gambiae lipophorin: characterization and role in lipid transport to developing oocyte. Insect Biochem Mol Biol 36: 375-386.
28. Rodenburg KW, Van der Horst DJ (2005) Lipoprotein-mediated lipid transport in insects: analogy to the mammalian lipid carrier system and novel concepts for the functioning of LDL receptor family members. Biochim Biophys Acta 1736: 10-29.
29. Panakova D, Sprong H, Marois E, Thiele C, Eaton S (2005) Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435: 58-65.
30. Cheon HM, Shin SW, Bian G, Park JH, Raikhel AS (2006) Regulation of lipid metabolism genes, lipid carrier protein lipophorin, and its receptor during immune challenge in the mosquito Aedes aegypti. J Biol Chem 281: 8426-8435.
31. Billingsley PF, Lehane MJ (1996) Structure and ultrastructure of the insect midgut. London: Chapman & Hall.
32. Vierstraete E, Verleyen P, Sas F, Van den Bergh G, De Loof A, et al. (2004) The instantly released Drosophila immune proteome is infection-specific. Biochem Biophys Res Commun 317: 1052-1060.
33. Scherfer C, Karlsson C, Loseva O, Bidla G, Goto A, et al. (2004) Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr Biol 14: 625-629.
34. Bartholomay LC, Cho WL, Rocheleau TA, Boyle JP, Beck ET, et al. (2004) Description of the transcriptomes of immune response-activated hemocytes from the mosquito vectors Aedes aegypti and Armigeres subalbatus. Infect Immun 72: 4114-4126.
35. Halwani AE, Niven DF, Dunphy GB (2000) Apolipophorin-III and the interactions of lipoteichoic acids with the immediate immune responses of Galleria mellonella. J Invertebr Pathol 76: 233-241.
36. Park SY, Kim CH, Jeong WH, Lee JH, Seo SJ, et al. (2005) Effects of two hemolymph proteins on humoral defense reactions in the wax moth, Galleria mellonella. Dev Comp Immunol 29: 43-51.
37. Vlachou D, Zimmermann T, Cantera R, Janse CJ, Waters AP, et al. (2004) Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol 6: 671-685.
38. Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M, et al. (1995) Plasmodium gallinaceum: a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Exp Parasitol 80: 583-595.
39. Shiao SH, Whitten MM, Zachary D, Hoffmann JA, Levashina EA (2006) Fz2 and cdc42 mediate melanization and actin polymerization but are dispensable for Plasmodium killing in the mosquito midgut. PLoS Pathog 2: e133. doi:10.1371/journal.ppat.0020133.
40. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, et al. (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17: 1467-1482.
41. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc Biol Sci 270: 357-366.
42. Michel K, Suwanchaichinda C, Morlais I, Lambrechts L, Cohuet A, et al. (2006) Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc Natl Acad Sci U S A 103: 16858-16863.
43. Morlais I, Poncon N, Simard F, Cohuet A, Fontenille D (2004) Intraspecific nucleotide variation in Anopheles gambiae: new insights into the biology of malaria vectors. Am J Trop Med Hyg 71: 795-802.
44. Favia G, Lanfrancotti A, Spanos L, Siden-Kiamos I, Louis C (2001) Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 10: 19-23.
45. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, et al. (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298: 159-165.
46. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163.
47. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
48. Wright S (1978) Evolution and the Genetics of Populations: Variability Within and Among natural Populations. Chicago: University Press.
49. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
50. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19: 153-170.
51. Mulder B, Tchuinkam T, Dechering K, Verhave JP, Carnevale P, et al. (1994) Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg 88: 121-125.
52. Franke-Fayard B, Trueman H, Ramesar J, Mendoza J, van der Keur M, et al. (2004) A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137: 23-33.
53. Sinden RE, Butcher GA, Billker O, Fleck SL (1996) Regulation of infectivity of Plasmodium to the mosquito vector. Adv Parasitol 38: 53-117.