The anopheles innate immune system in the defense against malaria infection

Journal of Innate Immunity

Volumn 6, Issue 2, 2014, Pages 169-181

  Clayton, April M ^a   Dong, Yuemei ^a   Dimopoulos, George ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Anopheles; Innate immunity; Malaria; Mosquito; Plasmodium

Indexed keywords

COMPLEMENT; JANUS KINASE; STAT PROTEIN;

ANOPHELES; ANOPHELES GAMBIAE; BACTERIAL IMMUNITY; BLOOD CELL; CELLULAR IMMUNITY; COMPLEMENT SYSTEM; GENE SILENCING; HUMAN; INNATE IMMUNITY; INTESTINE FLORA; MALARIA; MIDGUT; NONHUMAN; PARASITE IMMUNITY; PARASITE TRANSMISSION; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DISEASE CARRIER; HOST PARASITE INTERACTION; IMMUNOLOGY; PARASITOLOGY; PHYSIOLOGY;

ANIMALS; ANOPHELES; HEMOCYTES; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY, INNATE; INSECT VECTORS; MALARIA; PLASMODIUM; SIGNAL TRANSDUCTION;

EID: 84896365311     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000353602     Document Type: Review

References (128)

1. Cirimotich CM, Clayton AM, Dimopoulos G: Low- and high-tech approaches to control plasmodium parasite transmission by anopheles mosquitoes. J Trop Med 2011; 2011: 891342.
2. Baton LA, Ranford-Cartwright LC: How do malaria ookinetes cross the mosquito midgut wall? Trends Parasitol 2005; 21: 22-28. (Pubitemid 40082095)
3. Whitten MM, Shiao SH, Levashina EA: Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol 2006; 28: 121-130.
4. Sinden RE, Billingsley PF: Plasmodium invasion of mosquito cells: hawk or dove? Trends Parasitol 2001; 17: 209-212.
5. Baton LA, Ranford-Cartwright LC: Plasmodium falciparum ookinete invasion of the midgut epithelium of Anopheles stephensi is consistent with the time bomb model. Parasitology 2004; 129: 663-676. (Pubitemid 39657758)
6. Maier WA, Becker-Feldman H, Seitz HM: Pathology of malaria-infected mosquitoes. Parasitol Today 1987; 3: 216-218. (Pubitemid 17128434)
7. Gupta L, Kumar S, Han YS, Pimenta PF, Barillas- Mury C: Midgut epithelial responses of different mosquito-plasmodium combinations: the actin cone zipper repair mechanism in Aedes aegypti. Proc Natl Acad Sci USA 2005; 102: 4010-4015. (Pubitemid 40388547)
8. Han YS, Thompson J, Kafatos FC, Barillas- Mury C: Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei : the time bomb theory of ookinete ookinete invasion of mosquitoes. EMBO J 2000; 19: 6030-6040.
9. Torii M, Nakamura K, Sieber KP, Miller LH, Aikawa M: Penetration of the mosquito (Aedes aegypti) midgut wall by the ookinetes of Plasmodium gallinaceum. J Protozool 1992; 39: 449-454.
10. Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M, Miller LH: Plasmodium gallinaceum : a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Exp Parasitol 1995; 80: 583-595.
11. Vlachou D, Zimmermann T, Cantera R, Janse CJ, Waters AP, Kafatos FC: Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol 2004; 6: 671-685. (Pubitemid 38812061)
12. Zieler H, Dvorak JA: Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells. Proc Natl Acad Sci USA 2000; 97: 11516-11521.
13. Levashina EA: Immune responses in Anopheles gambiae. Insect Biochem Mol Biol 2004; 34: 673-678. (Pubitemid 38893139)
14. Vlachou D, Schlegelmilch T, Runn E, Mendes A, Kafatos FC: The developmental migration of plasmodium in mosquitoes. Curr Opin Genet Dev 2006; 16: 384-391. (Pubitemid 43994449)
15. Sinden RE: Molecular interactions between Plasmodium and its insect vectors. Cell Microbiol 2002; 4: 713-724. (Pubitemid 35378711)
16. Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC, Gwadz RW: Genetic selection of a plasmodium-refractory strain of the malaria vector anopheles gambiae. Science 1986; 234: 607-610. (Pubitemid 17186176)
17. Niare O, Markianos K, Volz J, Oduol F, Toure A, Bagayoko M, Sangare D, Traore SF, Wang R, Blass C, Dolo G, Bouare M, Kafatos FC, Kruglyak L, Toure YT, Vernick KD: Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science 2002; 298: 213-216.
18. Hillyer JF, Barreau C, Vernick KD: Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito haemocoel. International Journal for Parasitology 2007; 37: 673-681. (Pubitemid 46440942)
19. Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, Sinden RE: The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol 2003; 33: 933-943. (Pubitemid 37297460)
20. Dimopoulos G, Seeley D, Wolf A, Kafatos FC: Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J 1998; 17: 6115-6123. (Pubitemid 28497785)
21. Osta MA, Christophides GK, Kafatos FC: Effects of mosquito genes on plasmodium development. Science 2004; 303: 2030-2032. (Pubitemid 38393280)
22. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G: Mosquito immune defenses against plasmodium infection. Dev Comp Immunol 2010; 34: 387-395.
23. Michel K, Kafatos FC: Mosquito immunity against plasmodium. Insect Biochem Mol Biol 2005; 35: 677-689. (Pubitemid 40707631)
24. Meister S, Koutsos AC, Christophides GK: The plasmodium parasite - a 'new' challenge for insect innate immunity. Int J Parasitol 2004; 34: 1473-1482.
25. Aggarwal K, Silverman N: Positive and negative regulation of the Drosophila immune response. BMB Rep 2008; 41: 267-277. (Pubitemid 351656920)
26. Ramirez JL, Dimopoulos G: The toll immune signaling pathway control conserved anti-dengue defenses across diverse Ae. aegypti strains and against multiple dengue virus serotypes. Dev Comp Immunol 2010; 34: 625-629.
27. Meister S, Kanzok SM, Zheng XL, Luna C, Li TR, Hoa NT, Clayton JR, White KP, Kafatos FC, Christophides GK, Zheng L: Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito anopheles gambiae. Proc Natl Acad Sci USA 2005; 102: 11420-11425. (Pubitemid 41153835)
28. Vizioli J, Bulet P, Hoffmann JA, Kafatos FC, Muller HM, Dimopoulos G: Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector anopheles gambiae. Proc Natl Acad Sci USA 2001; 98: 12630-12635. (Pubitemid 33019997)
29. Luna C, Hoa NT, Lin H, Zhang L, Nguyen HL, Kanzok SM, Zheng L: Expression of immune responsive genes in cell lines from two different Anopheline species. Insect Mol Biol 2006; 15: 721-729. (Pubitemid 44952707)
30. Frolet C, Thoma M, Blandin S, Hoffmann JA, Levashina EA: Boosting NF-?B-dependent basal immunity of Anopheles gambiae aborts development of plasmodium berghei. Immunity 2006; 25: 677-685. (Pubitemid 44529039)
31. Garver LS, Dong Y, Dimopoulos G: Caspar controls resistance to Plasmodium falciparum in diverse Anopheline species. PLoS Pathog 2009; 5:e1000335.
32. Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J, Dong Y, Dimopoulos G: Anopheles Imd pathway factors and effectors in infection intensity-dependent anti- Plasmodium action. PLoS Pathog 2012; 8:e1002737.
33. Mitri C, Jacques JC, Thiery I, Riehle MM, Xu J, Bischoff E, Morlais I, Nsango SE, Vernick KD, Bourgouin C: Fine pathogen discrimination within the apl1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog 2009; 5:e1000576.
34. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, Dimopoulos G: Anopheles gambiae immune responses to human and rodent plasmodium parasite species. PLoS Pathog 2006; 2:e52.
35. Riehle MM, Xu J, Lazzaro BP, Rottschaefer SM, Coulibaly B, Sacko M, Niare O, Morlais I, Traore SF, Vernick KD: Anopheles gambiae APL1 is a family of variable LRR proteins required for Rel1-mediated protection from the malaria parasite, Plasmodium berghei. PLoS One 2008; 3:e3672.
36. Povelones M, Waterhouse RM, Kafatos FC, Christophides GK: Leucine-rich repeat protein complex activates mosquito complement in defense against plasmodium parasites. Science 2009; 324: 258-261.
37. Rottschaefer SM, Riehle MM, Coulibaly B, Sacko M, Niare O, Morlais I, Traore SF, Vernick KD, Lazzaro BP: Exceptional diversity, maintenance of polymorphism, and recent directional selection on the apl1 malaria resistance genes of anopheles gambiae. PLoS Biol 2011; 9:e1000600.
38. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, Kafatos FC, Levashina EA: Complement- like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 2004; 116: 661-670. (Pubitemid 38326725)
39. Fraiture M, Baxter RH, Steinert S, Chelliah Y, Frolet C, Quispe-Tintaya W, Hoffmann JA, Blandin SA, Levashina EA: Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of plasmodium. Cell Host Microbe 2009; 5: 273-284.
40. Dong Y, Das S, Cirimotich C, Souza-Neto JA, McLean KJ, Dimopoulos G: Engineered anopheles immunity to plasmodium infection. PLoS Pathog 2011; 7:e1002458.
41. Clayton AM, Cirimotich CM, Dong Y, Dimopoulos G: Caudal is a negative regulator of the Anopheles IMD pathway that controls resistance to Plasmodium falciparum infection. Dev Comp Immunol 2013; 39: 323-332.
42. Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam Y-D, Bae J-W, Lee DG, Shin SC, Ha E-M, Lee W-J: Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 2008; 319: 777-782. (Pubitemid 351225861)
43. Chen Y, Dong Y, Sandiford S, Dimopoulos G: Transcriptional mediators Kto and Skd are involved in the regulation of the IMD pathway and anti- Plasmodium defense in Anopheles gambiae. PLoS One 2012; 7:e45580.
44. Dostert C, Jouanguy E, Irving P, Troxler L, Galiana- Arnoux D, Hetru C, Hoffmann JA, Imler JL: The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat Immunol 2005; 6: 946-953. (Pubitemid 43090450)
45. Souza-Neto JA, Sim S, Dimopoulos G: An evolutionary conserved function of the Jak- STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 2009; 106: 17841-17846.
46. Gupta L, Molina-Cruz A, Kumar S, Rodrigues J, Dixit R, Zamora RE, Barillas-Mury C: The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 2009; 5: 498-507.
47. Bahia AC, Kubota MS, Tempone AJ, Araujo HR, Guedes BA, Orfano AS, Tadei WP, Rios- Velasquez CM, Han YS, Secundino NF, Barillas- Mury C, Pimenta PF, Traub-Cseko YM: The JAK-STAT pathway controls Plasmodium vivax load in early stages of Anopheles aquasalis infection. PLoS Negl Trop Dis 2011; 5:e1317.
48. Barillas-Mury C, Han Y-S, Seeley D, Kafatos FC: Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. EMBO J 1999; 18: 959-967. (Pubitemid 29082275)
49. Agaisse H, Perrimon N: The roles of JAK/ STAT signaling in Drosophila immune responses. Immunol Rev 2004; 198: 72-82. (Pubitemid 38406936)
50. Wormald S, Hilton DJ: Inhibitors of cytokine signal transduction. J Biol Chem 2004; 279: 821-824. (Pubitemid 38082600)
51. Christophides GK, Vlachou D, Kafatos FC: Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol Rev 2004; 198: 127-148. (Pubitemid 38406941)
52. Luckhart S, Riehle MA: The insulin signaling cascade from nematodes to mammals: insights into innate immunity of Anopheles mosquitoes to malaria parasite infection. Dev Comp Immunol 2007; 31: 647-656. (Pubitemid 46509795)
53. Pakpour N, Corby-Harris V, Green GP, Smithers HM, Cheung KW, Riehle MA, Luckhart S: Ingested human insulin inhibits the mosquito NF-?B-dependent immune response to Plasmodium falciparum. Infect Immun 2012; 80: 2141-2149.
54. Drexler A, Nuss A, Hauck E, Glennon E, Cheung K, Brown M, Luckhart S: Human IGF1 extends lifespan and enhances resistance to Plasmodium falciparum infection in the malaria vector anopheles stephensi. J Exp Biol 2013; 216: 208-217.
55. Tahar R, Boudin C, Thiery I, Bourgouin C: Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J 2002; 21: 6673-6680. (Pubitemid 36014539)
56. Blandin SA, Marois E, Levashina EA: Antimalarial responses in Anopheles gambiae : from a complement-like protein to a complement-like pathway. Cell Host Microbe 2008; 3: 364-374. (Pubitemid 351784366)
57. Waterhouse RM, Povelones M, Christophides GK: Sequence-structure-function relations of the mosquito leucine-rich repeat immune proteins. BMC Genomics 2010; 11: 531.
58. 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: Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 2006; 312: 577-579.
59. Menge DM, Zhong D, Guda T, Gouagna L, Githure J, Beier J, Yan G: Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya. Genetics 2006; 173: 235-241. (Pubitemid 43800198)
60. Riehle MM, Markianos K, Lambrechts L, Xia A, Sharakhov I, Koella JC, Vernick KD: A major genetic locus controlling natural Plasmodium falciparum infection is shared by East and West African Anopheles gambiae. Malar J 2007; 6: 87.
61. Schnitger AK, Yassine H, Kafatos FC, Osta MA: Two C-type lectins cooperate to defend Anopheles gambiae against Gram-negative bacteria. J Biol Chem 2009; 284: 17616-17624.
62. Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC: Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 2005; 15: 1185-1195. (Pubitemid 40950515)
63. Gupta L, Noh JY, Jo YH, Oh SH, Kumar S, Noh MY, Lee YS, Cha SJ, Seo SJ, Kim I, Han YS, Barillas-Mury C: Apolipophorin-III mediates antiplasmodial epithelial responses in Anopheles gambiae (G3) mosquitoes. PLoS One 2010; 5:e15410.
64. Rono MK, Whitten MM, Oulad-Abdelghani M, Levashina EA, Marois E: The major yolk protein vitellogenin interferes with the antiplasmodium response in the malaria mosquito Anopheles gambiae. PLoS Biol 2010; 8:e1000434.
65. Dong Y, Dimopoulos G: Anopheles fibrinogenrelated proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 2009; 284: 9835-9844.
66. Wang X, Zhao Q, Christensen BM: Identification and characterization of the fibrinogenlike domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes. BMC Genomics 2005; 6: 114.
67. Middha S, Wang X: Evolution and potential function of fibrinogen-like domains across twelve Drosophila species. BMC Genomics 2008; 9: 260.
68. Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, Bartholomay LC, Barillas- Mury C, Bian G, Blandin S, Christensen BM, Dong Y, Jiang H, Kanost MR, Koutsos AC, Levashina EA, Li J, Ligoxygakis P, Maccallum RM, Mayhew GF, Mendes A, Michel K, Osta MA, Paskewitz S, Shin SW, Vlachou D, Wang L, Wei W, Zheng L, Zou Z, Severson DW, Raikhel AS, Kafatos FC, Dimopoulos G, Zdobnov EM, Christophides GK: Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007; 316: 1738-1743. (Pubitemid 46988547)
69. Dimopoulos G, Casavant TL, Chang S, Scheetz T, Roberts C, Donohue M, Schultz J, Benes V, Bork P, Ansorge W, Soares MB, Kafatos FC: Anopheles gambiae pilot gene discovery project: identification of mosquito innate immunity genes from expressed sequence tags generated from immune-competent cell lines. Proc Natl Acad Sci USA 2000; 97: 6619-6624. (Pubitemid 30412763)
70. Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, Kafatos FC: Genome expression analysis of Anopheles gambiae : responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA 2002; 99: 8814-8819. (Pubitemid 34693641)
71. Dimopoulos G, Richman A, Muller HM, Kafatos FC: Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci USA 1997; 94: 11508-11513. (Pubitemid 27451029)
72. Dong Y, Taylor HE, Dimopoulos G: AgDscam, a hypervariable immunoglobulin domaincontaining receptor of the Anopheles gambiae innate immune system. PLoS Biol 2006; 4:e229.
73. Dong Y, Cirimotich CM, Pike A, Chandra R, Dimopoulos G: Anopheles NF-?B-regulated splicing factors direct pathogen-specific repertoires of the hypervariable pattern recognition receptor AgDscam. Cell Host Microbe 2012; 12: 521-530.
74. Han YS, Barillas-Mury C: Implications of time bomb model of ookinete invasion of midgut cells. Insect Biochem Mol Biol 2002; 32: 1311-1316.
75. Luckhart S, Vodovotz Y, Cui L, Rosenberg R: The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci USA 1998; 95: 5700-5705. (Pubitemid 28224159)
76. Kumar S, Gupta L, Han YS, Barillas-Mury C: Inducible peroxidases mediate nitration of anopheles midgut cells undergoing apoptosis in response to plasmodium invasion. J Biol Chem 2004; 279: 53475-53482. (Pubitemid 40051853)
77. Kumar S, Barillas-Mury C: Ookinete-induced midgut peroxidases detonate the time bomb in anopheline mosquitoes. Insect Biochem Mol Biol 2005; 35: 721-727. (Pubitemid 40707635)
78. Oliveira Gde A, Lieberman J, Barillas-Mury C: Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 2012; 335: 856-859.
79. Shiao SH, Whitten MM, Zachary D, Hoffmann JA, Levashina EA: Fz2 and Cdc42 mediate melanization and actin polymerization but are dispensable for plasmodium killing in the mosquito midgut. PLoS Pathog 2006; 2:e133.
80. Baxter RH, Steinert S, Chelliah Y, Volohonsky G, Levashina EA, Deisenhofer J: A heterodimeric complex of the LRR proteins LRIM1 and APL1C regulates complementlike immunity in Anopheles gambiae. Proc Natl Acad Sci USA 2010; 107: 16817-16822.
81. Lavine MD, Strand MR: Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 2002; 32: 1295-1309.
82. Castillo J, Robertson A, Strand M: Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem Mol Biol 2006; 36: 891-903. (Pubitemid 46053792)
83. King JG, Hillyer JF: Infection-induced interaction between the mosquito circulatory and immune systems. PLoS Pathog 2012; 8:e1003058.
84. Baton LA, Robertson A, Warr E, Strand MR, Dimopoulos G: Genome-wide transcriptomic profiling of anopheles gambiae hemocytes reveals pathogen-specific signatures upon bacterial challenge and Plasmodium berghei infection. BMC Genomics 2009; 10: 257.
85. Coggins S, Estevez-Lao T, Hillyer J: Increased survivorship following bacterial infection by the mosquito Aedes aegypti as compared to Anopheles gambiae correlates with increased transcriptional induction of antimicrobial peptides. Dev Comp Immunol 2012; 37: 390-401.
86. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010; 329: 1353-1355.
87. Castillo J, Brown M, Strand M: Blood feeding and insulin-like peptide 3 stimulate proliferation of hemocytes in the mosquito Aedes aegypti. PLoS Pathog 2011; 7:e1002274.
88. Hillyer J, Schmidt S, Fuchs J, Boyle J, Christensen B: Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell Microbiol 2005; 7: 39-51.
89. Markus R, Laurinyecz B, Kurucz E, Honti V, Bajusz I, Sipos B, Somogyi K, Kronhamn J, Hultmark D, Ando I: Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci USA 2009; 106: 4805-4809.
90. Ratcliffe N, Rowley A: A comparative synopsis of the structure and function of the blood cells of insects and other invertebrates. Dev Comp Immunol 1979; 3: 189-221. (Pubitemid 9234632)
91. King J, Hillyer J: Spatial and temporal in vivo analysis of circulating and sessile immune cells in mosquitoes: hemocyte mitosis following infection. BMC Biology 2013; 11: 55.
92. Roth O, Sadd BM, Schmid-Hempel P, Kurtz J: Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc Biol Sci 2009; 276: 145-151.
93. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS: A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 2007; 3:e26.
94. Sadd BM, Schmid-Hempel P: Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 2006; 16: 1206-1210. (Pubitemid 43867309)
95. Schmid-Hempel P: Evolutionary ecology of insect immune defenses. Annu Rev Entomol 2005; 50: 529-551.
96. Moret Y, Siva-Jothy MT: Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 2003; 270: 2475-2480. (Pubitemid 37500241)
97. Lanot R, Zachary D, Holder F, Meister M: Postembryonic hematopoiesis in Drosophila. Dev Biol 2001; 230: 243-257. (Pubitemid 32171421)
98. Zheng L, Wang S, Romans P, Zhao H, Luna C, Benedict MQ: Quantitative trait loci in Anopheles gambiae controlling the encapsulation response against Plasmodium cynomolgi Ceylon. BMC Genet 2003; 4: 16.
99. Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, Ansorge W, Kafatos FC, Collins FH: Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science 1997; 276: 425-428. (Pubitemid 27180706)
100. Nappi AJ, Christensen BM: Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol 2005; 35: 443-459. (Pubitemid 40440937)
101. Barillas-Mury C: Clip proteases and plasmodium melanization in Anopheles gambiae. Trends Parasitol 2007; 23: 297-299. (Pubitemid 46935570)
102. Volz J, Muller HM, Zdanowicz A, Kafatos FC, Osta MA: A genetic module regulates the melanization response of anopheles to plasmodium. Cell Microbiol 2006; 8: 1392-1405. (Pubitemid 44194573)
103. Yassine H, Kamareddine L, Osta MA: The mosquito melanization response is implicated in defense against the entomopathogenic fungus Beauveria bassiana. PLoS Pathog 2012; 8:e1003029.
104. Volz J, Osta MA, Kafatos FC, Muller HM: The roles of two clip domain serine proteases in innate immune responses of the malaria vector Anopheles gambiae. J Biol Chem 2005; 280: 40161-40168. (Pubitemid 41779152)
105. Michel K, Budd A, Pinto S, Gibson TJ, Kafatos FC: Anopheles gambiae SRPN2 facilitates midgut invasion by the malaria parasite Plasmodium berghei. EMBO Rep 2005; 6: 891-897. (Pubitemid 43108682)
106. Michel K, Suwanchaichinda C, Morlais I, Lambrechts L, Cohuet A, Awono-Ambene PH, Simard F, Fontenille D, Kanost MR, Kafatos FC: Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc Natl Acad Sci USA 2006; 103: 16858-16863. (Pubitemid 44737343)
107. An C, Budd A, Kanost MR, Michel K: Characterization of a regulatory unit that controls melanization and affects longevity of mosquitoes. Cell Mol Life Sci 2011; 68: 1929-1939.
108. Abraham EG, Pinto SB, Ghosh A, Vanlandingham DL, Budd A, Higgs S, Kafatos FC, Jacobs-Lorena M, Michel K: An immuneresponsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci USA 2005; 102: 16327-16332. (Pubitemid 41688913)
109. Pinto SB, Kafatos FC, Michel K: The parasite invasion marker SRPN6 reduces sporozoite numbers in salivary glands of Anopheles gambiae. Cell Microbiol 2008; 10: 891-898. (Pubitemid 351386944)
110. Smith RC, Eappen AG, Radtke AJ, Jacobs- Lorena M: Regulation of anti-plasmodium immunity by a LITAF-like transcription factor in the malaria vector Anopheles gambiae. PLoS Pathog 2012; 8:e1002965.
111. Warr E, Lambrechts L, Koella JC, Bourgouin C, Dimopoulos G: Anopheles gambiae immune responses to sephadex beads: involvement of anti-plasmodium factors in regulating melanization. Insect Biochem Mol Biol 2006; 36: 769-778. (Pubitemid 44486782)
112. Molina-Cruz A, DeJong RJ, Ortega C, Haile A, Abban E, Rodrigues J, Jaramillo-Gutierrez G, Barillas-Mury C: Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. Proc Natl Acad Sci USA 2012; 109:E1957-E1962.
113. Meister S, Agianian B, Turlure F, Relogio A, Morlais I, Kafatos FC, Christophides GK: Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 2009; 5:e1000542.
114. Dong Y, Manfredini F, Dimopoulos G: Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 2009; 5:e1000423.
115. Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, Rizzi A, Urso R, Brusetti L, Borin S, Mora D, Scuppa P, Pasqualini L, Clementi E, Genchi M, Corona S, Negri I, Grandi G, Alma A, Kramer L, Esposito F, Bandi C, Sacchi L, Daffonchio D: Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci USA 2007; 104: 9047-9051. (Pubitemid 47175434)
116. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, Dimopoulos G: Natural microbe-mediated refractoriness to plasmodium infection in Anopheles gambiae. Science 2011; 332: 855-858.
117. Cirimotich CM, Ramirez JL, Dimopoulos G: Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 2011; 10: 307-310.
118. Pumpuni CB, Beier MS, Nataro JP, Guers LD, Davis JR: Plasmodium falciparum : inhibition of sporogonic development in Anopheles stephensi by Gram-negative bacteria. Exp Parasitol 1993; 77: 195-199. (Pubitemid 23279547)
119. Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE: Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J Med Entomol 2003; 40: 371-374. (Pubitemid 37399433)
120. Azambuja P, Garcia ES, Ratcliffe NA: Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 2005; 21: 568-572. (Pubitemid 41572269)
121. Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C: A peroxidase/ dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 2010; 327: 1644-1648.
122. Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M: Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc Natl Acad Sci USA 2012; 109: 12734-12739.
123. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC: Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 2001; 104: 709-718. (Pubitemid 32241021)
124. Warr E, Das S, Dong Y, Dimopoulos G: The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of Anopheles gambiae and in antiplasmodium defence. Insect Mol Biol 2008; 17: 39-51. (Pubitemid 351171298)
125. Garver LS, Xi Z, Dimopoulos G: Immunoglobulin superfamily members play an important role in the mosquito immune system. Dev Comp Immunol 2008; 32: 519-531. (Pubitemid 351172447)
126. Kajla MK, Andreeva O, Gilbreath TM 3rd, Paskewitz SM: Characterization of expression, activity and role in antibacterial immunity of Anopheles gambiae lysozyme c-1. Comp Biochem Physiol B Biochem Mol Biol 2010; 155: 201-209.
127. Kajla MK, Shi L, Li B, Luckhart S, Li J, Paskewitz SM: A new role for an old antimicrobial: Lysozyme c-1 can function to protect malaria parasites in Anopheles mosquitoes. PLoS One 2011; 6:e19649.
128. Lapcharoen P, Komalamisra N, Rongsriyam Y, Wangsuphachart V, Dekumyoy P, Prachumsri J, Kajla MK, Paskewitz SM: Investigations on the role of a lysozyme from the malaria vector Anopheles dirus during malaria parasite development. Dev Comp Immunol 2012; 36: 104-111.