Non-Genetic Determinants of Mosquito Competence for Malaria Parasites

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Lefèvre, Thierry ^a   Vantaux, Amélie ^a   Dabiré, Kounbobr R ^b,c   Mouline, Karine ^a,b   Cohuet, Anna ^a,b  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b Public Health Research Institute for Health Sciences   (Burkina Faso)

^c CENTRE MURAZ   (Burkina Faso)

Author keywords

[No Author keywords available]

Indexed keywords

INTRINSIC FACTOR;

BACTERIAL LOAD; BODY SIZE; BREEDING; DISEASE CONTROL; DISEASE SURVEILLANCE; ENVIRONMENTAL FACTOR; FOOD AVAILABILITY; FOOD QUALITY; HEREDITY; IMMUNE RESPONSE; INFECTION; INTESTINE FLORA; MALARIA; MALARIA CONTROL; MOSQUITO; NONHUMAN; PARASITE PREVALENCE; PARASITE TRANSMISSION; PLASMODIUM; REVIEW; SPOROZOITE; TEMPERATURE;

ANIMALS; CULICIDAE; HOST-PATHOGEN INTERACTIONS; INSECT VECTORS; MALARIA; PLASMODIUM;

EID: 84879511868     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003365     Document Type: Review

References (119)

1. Lehane MJ, Aksoy S, Levashina E, (2004) Immune responses and parasite transmission in blood-feeding insects. Trends Parasitol 20: 433-439 doi:10.1016/j.pt.2004.07.002.
2. Dinglasan RR, Kalume DE, Kanzok SM, Ghosh AK, Muratova O, et al. (2007) Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc Natl Acad Sci U S A 104: 13461-13466.
3. Smith TA, Chitnis N, Briët OT, Tanner M, (2011) Uses of mosquito-stage transmission-blocking vaccines against Plasmodium falciparum. Trends Parasitol 27: 190-196.
4. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G, (2010) Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 34: 387-395.
5. Marois E, (2011) The multifaceted mosquito anti-Plasmodium response. Curr Opin Microbiol 14: 429-435 doi:10.1016/j.mib.2011.07.016.
6. Mitri C, Vernick KD, (2012) Anopheles gambiae pathogen susceptibility: the intersection of genetics, immunity and ecology. Curr Opin Microbiol 15: 285-291.
7. Blandin S, Marois E, Levashina EA, (2008) Antimalarial responses in Anopheles gambiae: from a complement-like protein to a complement-like pathway. Cell Host Microbe 3: 364-374.
8. Povelones M, Waterhouse RM, Kafatos FC, Christophides GK, (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324: 258-261.
9. Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J, et al. (2012) Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog 8: e1002737 doi:10.1371/journal.ppat.1002737.
10. Gupta L, Molina-Cruz A, Kumar S, Rodrigues J, Dixit R, et al. (2009) The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 5: 498-507.
11. Dong Y, Das S, Cirimotich CM, Souza-Neto JA, McLean KJ, et al. (2011) Engineered Anopheles immunity to Plasmodium infection. PLoS Pathog 7: e1002458 doi:10.1371/journal.ppat.1002458.
12. Isaacs AT, Li F, Jasinskiene N, Chen X, Nirmala X, et al. (2011) Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi. PLoS Pathog 7: e1002017 doi:10.1371/journal.ppat.1002017.
13. 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.
14. Tripet F, Aboagye-Antwi F, Hurd H, (2008) Ecological immunology of mosquito-malaria interactions. Trends Parasitol 24: 219-227.
15. 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.
16. Harris C, Lambrechts L, Rousset F, Abate L, Nsango SE, et al. (2010) Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog 6: e1001112 doi:10.1371/journal.ppat.1001112.
17. Mitri C, Jacques J-C, Thiery I, Riehle MM, Xu J, et al. (2009) Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog 5: e1000576 doi:10.1371/journal.ppat.1000576.
18. 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 doi:10.1186/1475-2875-4-3.
19. Lambrechts L, (2010) Dissecting the genetic architecture of host-pathogen specificity. PLoS Pathog 6: e1001019 doi:10.1371/journal.ppat.1001019.
20. Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT, (2009) Ecological immunology. Philos Trans R Soc Lond B Biol Sci 364: 3-14.
21. Wolinska J, King KC, (2009) Environment can alter selection in host-parasite interactions. Trends Parasitol 25: 236-244.
22. Lazzaro BP, Little TJ, (2009) Immunity in a variable world. Philos Trans R Soc Lond B Biol Sci 364: 15-26.
23. Grassi B, (1901) Studi di uno zoologo sulla malaria. Atti dei Linncei Mem 3: 229-505.
24. Detinova TS, (1962) Age-grouping methods in Diptera of medical importance. Monogr Ser World Health Organ 47: 13-191.
25. Lyons CL, Coetzee M, Terblanche JS, Chown SL, (2012) Thermal limits of wild and laboratory strains of two African malaria vector species, Anopheles arabiensis and Anopheles funestus. Malar J 11: 226.
26. Murdock CC, Paaijmans KP, Bell AS, King JG, Hillyer JF, et al. (2012) Complex effects of temperature on mosquito immune function. Proc Biol Sci 279: 3357-3366.
27. Murdock CC, Paaijmans KP, Cox-Foster D, Read AF, Thomas MB, (2012) Rethinking vector immunology: the role of environmental temperature in shaping resistance. Nat Rev Microbiol 10: 869-876 doi:10.1038/nrmicro2900.
28. Suwanchaichinda C, Paskewitz SM, (1998) Effects of larval nutrition, adult body size, and adult temperature on the ability of Anopheles gambiae (Diptera: Culicidae) to melanize sephadex beads. J Med Entomol 35: 157-161.
29. Boyd M, (1932) Studies on Plasmodium vivax. II. The influence of temperature on the duration of the extrinsic incubation period. J Hyg (Land) 16: 851.
30. Kligler J, Mer G, (1937) Studies on the effect of various factors on the infection of Anopheles elutus with different species of Plasmodium. Ann Trop Med Parasitol 31: 71.
31. Boyd MF (1949) Epidemiology: factors related to the definitive host. In: Boyd MF, editor. Malariology: a comprehensive survey of all aspects of this group of diseases from a global standpoint. Philadelphia: W.B. Saunders. pp. 608-697.
32. Noden BH, Kent MD, Beier JC, (1995) The impact of variations in temperature on early Plasmodium falciparum development in Anopheles stephensi. Parasitology 111: 539-545.
33. Eling W, Hooghof J, Sauerwein R, Gemert G Van, (2001) Tropical temperatures can inhibit development of the human malaria parasite Plasmodium falciparum in the mosquito. Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society 12: 151-156.
34. Vanderberg JP, Yoeli M, (1966) On sporogonic development effects of temperature of Plasmodium berghei. J Parasitol 52: 559-564.
35. Okech BA, Gouagna LC, Walczak E, Kabiru EW, Beier JC, et al. (2004) Resistance of early midgut stages of natural Plasmodium falciparum parasites to high temperatures in experimentally infected Anopheles gambiae (Diptera: Culicidae). J Parasitol 90: 764-768 doi:10.1016/j.actatropica.2004.06.003.
36. Paaijmans KP, Blanford S, Chan BHK, Thomas MB, (2012) Warmer temperatures reduce the vectorial capacity of malaria mosquitoes. Biol Lett 8: 465-468 doi:10.1098/rsbl.2011.1075.
37. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, et al. (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci U S A 107: 15135-15139.
38. Paaijmans KP, Thomas MB, (2011) The influence of mosquito resting behaviour and associated microclimate for malaria risk. Malar J 10: 183.
39. Cory JS, Hoover K, (2006) Plant-mediated effects in insect-pathogen interactions. Trends Ecol Evol 21: 278-286.
40. Lefèvre T, Oliver L, Hunter MD, De Roode JC, Letters E, (2010) Evidence for trans-generational medication in nature. Ecol Lett 13: 1485-1493 doi:10.1111/j.1461-0248.2010.01537.x.
41. Alaux C, Ducloz F, Crauser D, Le Conte Y, (2010) Diet effects on honeybee immunocompetence. Biol Lett 6: 562-565 doi:10.1098/rsbl.2009.0986.
42. Lambrechts L, Chavatte J-M, Snounou G, Koella J, (2006) Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proc Biol Sci 273: 1501-1506.
43. Ferguson HM, Read AF, (2002) Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proc Biol Sci 269: 1217-1224.
44. Okech BA, Gouagna LC, Kabiru EW, Beier JC, Yan G, et al. (2004) Influence of age and previous diet of Anopheles gambiae on the infectivity of natural Plasmodium falciparum gametocytes from human volunteers. J Insect Sci 4: 33.
45. Okech BA, Gouagna LC, Yan GY, Githure JI, Beier JC, (2007) Larval habitats of Anopheles gambiae s.s. (Diptera: Culicidae) influences vector competence to Plasmodium falciparum parasites. Malar J 6: 50.
46. Koella JC, Sorensen FL, (2002) Effect of adult nutrition on the melanization immune response of the malaria vector Anopheles stephensi. Med Vet Entomol 16: 316-320.
47. Ponton F, Wilson K, Cotter SC, Raubenheimer D, Simpson SJ, (2011) Nutritional immunology: a multi-dimensional approach. PLoS Pathog 7: e1002223 doi:10.1371/journal.ppat.1002223.
48. Foster WA, (1995) Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol 40: 443-474.
49. Cirimotich CM, Ramirez JL, Dimopoulos G, (2011) Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10: 307-310.
50. Dong Y, Manfredini F, Dimopoulos G, (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423 doi:10.1371/journal.ppat.1000423.
51. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, et al. (2011) Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332: 855-858.
52. Meister S, Agianian B, Turlure F, Relógio A, Morlais I, et al. (2009) Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 5: e1000542 doi:10.1371/journal.ppat.1000542.
53. Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, et al. (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog 8: e1002742 doi:10.1371/journal.ppat.1002742.
54. Blanford S, Chan BHK, Jenkins N, Sim D, Turner RJ, et al. (2005) Fungal pathogen reduces potential for malaria transmission. Science 308: 1638-1641.
55. Aliota MT, Chen C-C, Dagoro H, Fuchs JF, Christensen BM, (2011) Filarial worms reduce Plasmodium infectivity in mosquitoes. PLoS Negl Trop Dis 5: e963 doi:10.1371/journal.pntd.0000963.
56. Bargielowski I, Koella JC, (2009) A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis. PLoS ONE 4: e4676 doi:10.1371/journal.pone.0004676.
57. Imwong M, Nakeesathit S, Day NPJ, White NJ, (2011) A review of mixed malaria species infections in anopheline mosquitoes. Malar J 10: 12.
58. Paul REL, Nu VT, Krettli AU, Brey PT, (2002) Interspecific competition during transmission of two sympatric malaria parasite species to the mosquito vector. Proc Biol Sci 269: 2551-2557.
59. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C, (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329: 1353-1355.
60. Voordouw MJ, Lambrechts L, Koella J, (2008) No maternal effects after stimulation of the melanization response in the yellow fever mosquito Aedes aegypti. Oikos 117: 1269-1279.
61. Lorenz L, Koella J, (2011) Maternal environment shapes the life history and susceptibility to malaria of Anopheles gambiae mosquitoes. Malar J 10: 382.
62. Hillyer JF, Schmidt SL, Fuchs JF, Boyle JP, Christensen BM, (2005) Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell Microbiol 7: 39-51.
63. Stanley D, (2012) Aging and immunosenescence in invertebrates. Invertebrate Surviv J 9: 102-109.
64. Chun J, Riehle M, Paskewitz SM, (1995) Effect of mosquito age and reproductive status on melanization of sephadex beads in Plasmodium-refractory and-susceptible strains of Anopheles gambiae. J Invertebr Pathol 66: 11-17.
65. Mnyone LL, Kirby MJ, Mpingwa MW, Lwetoijera DW, Knols BG, et al. (2011) Infection of Anopheles gambiae mosquitoes with entomopathogenic fungi: effect of host age and blood-feeding status. Parasitol Res 108: 317-322.
66. Smith DL, Ellis McKenzie F, (2004) Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar J 3: 13.
67. Nidelet T, Koella JC, Kaltz O, (2009) Effects of shortened host life span on the evolution of parasite life history and virulence in a microbial host-parasite system. BMC Evol Biol 9: 65.
68. Donnell DM, Hunter MS, (2002) Developmental rates of two congeneric parasitoids, Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), utilizing different egg provisioning strategies. J Insect Physiol 48: 487-493.
69. Hu JS, Gelman DB, Blackburn MB, (2003) Age-specific interaction between the parasitoid, Encarsia formosa and its host, the silverleaf whitefly, Bemisia tabaci (Strain B). J Insect Sci 3: 28.
70. Mideo N, Reece SE, (2012) Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiol 7: 17-24.
71. Fellous S, Lazzaro BP, (2010) Larval food quality affects adult (but not larval) immune gene expression independent of effects on general condition. Mol Ecol 19: 1462-1468.
72. Bize P, Jeanneret C, Klopfenstein A, Roulin A, (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. Am Nat 171: 107-118.
73. Lyimo EO, Koella JC, (1992) Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology 104: 233-237.
74. Kitthawee S, Edman JD, Sattabongkot J, (1990) Evaluation of survival potential and malaria susceptibility among different size classes of laboratory-reared Anopheles dirus. Am J Trop Med Hyg 43: 328-332.
75. Werner EE, Peacor SD, (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1083-1100.
76. Yin M, Laforsch C, Lohr JN, Wolinska J, (2011) Predator-induced defense makes Daphnia more vulnerable to parasites. Evolution 65: 1482-1488.
77. Decaestecker E, De Meester L, Ebert D, (2002) In deep trouble: habitat selection constrained by multiple enemies in zooplankton. Proc Natl Acad Sci U S A 99: 5481-5485.
78. Alto BW, Lounibos LP, Higgs S, Juliano SA, (2005) Larval competition differentially affects arbovirus infection in Aedes Mosquitoes. Ecology 86: 3279-3288.
79. Alto BW, Lounibos LP, Mores CN, Reiskind MH, (2008) Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection. Proc Biol Sci 275: 463-471.
80. Bevins SN, (2007) Invasive mosquitoes, larval competition, and indirect effects on the vector competence of native mosquito species (Diptera: Culicidae). Biol Invasions 10: 1109-1117.
81. Muturi EJ, Costanzo K, Kesavaraju B, Alto BW, (2011) Can pesticides and larval competition alter susceptibility of Aedes mosquitoes (Diptera: Culicidae) to arbovirus infection? J Med Entomol 48: 429-436.
82. Muturi EJ, Blackshear M, Montgomery A, (2012) Temperature and density-dependent effects of larval environment on Aedes aegypti competence for an alphavirus. J Vector Ecol 37: 154-161.
83. Muturi EJ, Lampman R, Costanzo K, Alto BW, (2011) Effect of temperature and insecticide stress on life-history traits of Culex restuans and Aedes albopictus (Diptera: Culicidae). J Med Entomol 48: 243-250.
84. Muturi EJ, Alto BW, (2011) Larval environmental temperature and insecticide exposure alter Aedes aegypti competence for arboviruses. Vector Borne Zoonotic Dis 11: 1157-1163.
85. Muturi EJ, Kim C-H, Alto BW, Berenbaum MR, Schuler MA, (2011) Larval environmental stress alters Aedes aegypti competence for Sindbis virus. Trop Med Int Health 16: 955-964.
86. Rottschaefer SM, Riehle MM, Coulibaly B, Sacko M, Niaré O, et al. (2011) Exceptional diversity, maintenance of polymorphism, and recent directional selection on the APL1 malaria resistance genes of Anopheles gambiae. PLoS Biol 9: e1000600 doi:10.1371/journal.pbio.1000600.
87. Dong Y, Taylor HE, Dimopoulos G, (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4: e229 doi:10.1371/journal.pbio.0040229.
88. Molina-Cruz A, DeJong RJ, Ortega C, Haile A, Abban E, et al. (2012) Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. Proc Natl Acad Sci U S A 109: E1957-62 doi:10.1073/pnas.1121183109.
89. Hogg JC, Hurd H, (1997) The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae sl in north east Tanzania. Parasitology 114: 325-331.
90. Ahmed AM, Hurd H, (2006) Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect 8: 308-315.
91. Aboagye-Antwi F, Guindo A, Traore AS, Hurd H, Coulibaly M, et al. (2010) Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes. Malar J 9: 12.
92. Vézilier J, Nicot A, Gandon S, Rivero A, (2012) Plasmodium infection decreases fecundity and increases survival of mosquitoes. Proc Biol Sci 279: 4033-4041 doi:10.1098/rspb.2012.1394.
93. Lefèvre T, Chiang A, Kelavkar M, Li H, Li J, et al. (2011) Behavioural resistance against a protozoan parasite in the monarch butterfly. J Anim Ecol 81: 70-79.
94. Lefèvre T, De Roode JC, Kacsoh BZ, Schlenke TA, (2011) Defence strategies against a parasitoid wasp in Drosophila: fight or flight? Biol Lett 8: 230-233.
95. De Roode JC, Lefèvre T, (2012) Behavioral immunity in insects. Insects 3: 789-820.
96. Blanford S, Read AF, Thomas MB, (2009) Thermal behaviour of Anopheles stephensi in response to infection with malaria and fungal entomopathogens. Malar J 8: 72 doi:10.1186/1475-2875-8-72.
97. Hurd H, (2003) Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol 48: 141-161 doi:10.1146/annurev.ento.48.091801.112722.
98. Lefèvre T, Thomas F, (2008) Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol 8: 504-519 doi:10.1016/j.meegid.2007.05.008.
99. Lefèvre T, Koella JC, Renaud F, Hurd H, Biron DG, et al. (2006) New prospects for research on manipulation of insect vectors by pathogens. PLoS Pathog 2: e72 doi:10.1371/journal.ppat.0020072.
100. Cator LJ, Lynch PA, Read AF, Thomas MB, (2012) Do malaria parasites manipulate mosquitoes? Trends Parisitol 28: 466-470.
101. Fialho RF, Schall JJ, (1995) Thermal ecology of a malarial parasite and its insect vector: consequences for the parasite' s transmission success. J Anim Ecol 64: 553-562.
102. Castella G, Chapuisat M, Moret Y, Christe P, (2008) The presence of conifer resin decreases the use of the immune system in wood ants. Ecol Entomol 33: 408-412.
103. De Roode JC, Lopez Fernandez de Castillejo C, Faits T, Alizon S, (2011) Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies. J Evol Biol 24: 712-722.
104. De Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, et al. (2005) Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci U S A 102: 7624-7628.
105. Choisy M, De Roode JC, (2010) Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. Am Nat 175: E105-18.
106. Restif O, Koella JC, (2004) Concurrent evolution of resistance and tolerance to pathogens. Am Nat 164: E90-E102.
107. Roy BA, Kirchner JW, (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54: 51-63.
108. Miller MR, White A, Boots M, (2005) The evolution of host resistance: tolerance and control as distinct strategies. J Theor Biol 236: 198-207.
109. Sternberg ED, Lefèvre T, Li J, Lopez Fernandez de Castillejo C, Li H, et al. (2012) Food plant-derived disease tolerance and resistance in a natural butterfly-plant-parasite interaction. Evolution 66: 3367-3376.
110. Ayres JS, Schneider DS, (2012) Tolerance of infections. Annu Rev Immunol 30: 271-294.
111. Paaijmans KP, Read AF, Thomas MB, (2009) Understanding the link between malaria risk and climate. Proc Natl Acad Sci U S A 106: 13844-13849.
112. Mordecai EA, Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T, et al. (2012) Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett 16: 22-30.
113. Kambris Z, Blagborough AM, Pinto SB, Blagrove MSC, Godfray HCJ, et al. (2010) Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae. PLoS Pathog 6: e1001143 doi:10.1371/journal.ppat.1001143.
114. Hughes GL, Koga R, Xue P, Fukatsu T, Rasgon JL, (2011) Wolbachia infections are virulent and inhibit the human malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog 7: e1002043 doi:10.1371/journal.ppat.1002043.
115. Wang S, Jacobs-lorena M, (2013) Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends Biotechnol 31: 185-193.
116. Koella JC, (2003) On the evolutionary ecology of mosquito immunity and the use of transgenic mosquitoes for malaria control. Ecological Aspects for Application of Genetically Modified Mosquitoes 2: 173-185.
117. Boete C (2006) Malaria-refractoriness in mosquito: just a matter of harbouring genes? In: Boete C, editor. Genetically modified mosquitoes for malaria control. Georgetown: Eurekah/Landes Bioscience.
118. 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.
119. Rivero A, Vézilier J, Weill M, Read AF, Gandon S, (2010) Insecticide control of vector-borne diseases: when is insecticide resistance a problem? PLoS Pathog 6: e1001000 doi:10.1371/journal.ppat.1001000.