Intracellular immune responses of dipteran insects

Immunological Reviews

Volumn 240, Issue 1, 2011, Pages 129-140

  Steinert, Stefanie ^a   Levashina, Elena A ^a  

^a INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Arbovirus; Autophagy; Drosophila; Immune signaling; Mosquito; RNAi

Indexed keywords

ARTHROPOD; DENGUE; DISEASE CARRIER; ENDOSYMBIONT; FLY; HUMAN; IMMUNE RESPONSE; INTRACELLULAR KILLING; MALARIA; MICROBIAL IMMUNITY; NONHUMAN; PARASITE IMMUNITY; PRIORITY JOURNAL; REVIEW; YELLOW FEVER;

EID: 79951931738     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2010.00985.x     Document Type: Review

References (120)

1. Whitten MM, Shiao SH, Levashina EA. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol 2006;28:121-130.
2. Mota MM, et al. Migration of Plasmodium sporozoites through cells before infection. Science 2001;291:141-144.
3. Peterson TM, Gow AJ, Luckhart S. Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Radic Biol Med 2007;42:132-142.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. Volohonsky G, Steinert S, Levashina EA. Focusing on complement in the antiparasitic defense of mosquitoes. Trends Parasitol 2010;26:1-3.
11. 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 invasion of mosquitoes. EMBO J 2000;19:6030-6040.
12. Herrera-Ortiz A, et al. Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro. Insect Biochem Mol Biol 2004;34:893-901.
13. 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.
14. Okuda K, de Almeida F, Mortara RA, Krieger H, Marinotti O, Bijovsky AT. Cell death and regeneration in the midgut of the mosquito, Culex quinquefasciatus. J Insect Physiol 2007;53:1307-1315.
15. Levashina EA, et al. Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila. Science 1999;285:1917-1919.
16. Leclerc V, et al. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep 2006;7:231-235.
17. Danielli A, Kafatos FC, Loukeris TG. Cloning and characterization of four Anopheles gambiae serpin isoforms, differentially induced in the midgut by Plasmodium berghei invasion. J Biol Chem 2003;278:4184-4193.
18. Danielli A, Barillas-Mury C, Kumar S, Kafatos FC, Loukeris TG. Overexpression and altered nucleocytoplasmic distribution of Anopheles ovalbumin-like SRPN10 serpins in Plasmodium-infected midgut cells. Cell Microbiol 2005;7:181-190.
19. Abraham EG, et al. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci USA 2005;102:16327-16332.
20. 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.
21. Yassine H, Osta MA. Anopheles gambiae innate immunity. Cell Microbiol 2010;12:1-9.
22. Ghosh AK, Jacobs-Lorena M. Plasmodium sporozoite invasion of the mosquito salivary gland. Curr Opin Microbiol 2009;12:394-400.
23. Dixit R, Sharma A, Mourya DT, Kamaraju R, Patole MS, Shouche YS. Salivary gland transcriptome analysis during Plasmodium infection in malaria vector Anopheles stephensi. Int J Infect Dis 2009;13:636-646.
24. Rosinski-Chupin I, et al. SAGE analysis of mosquito salivary gland transcriptomes during Plasmodium invasion. Cell Microbiol 2007;9:708-724.
25. Chertemps T, et al. Anopheles gambiae PRS1 modulates Plasmodium development at both midgut and salivary gland steps. PLoS ONE 2010;5:e11538.
26. 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.
27. Oyston PC, Isherwood KE. The many and varied niches occupied by Yersinia pestis as an arthropod-vectored zoonotic pathogen. Antonie Van Leeuwenhoek 2005;87:171-177.
28. Kamhawi S. Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol 2006;22:439-445.
29. Kemp C, Imler JL. Antiviral immunity in Drosophila. Curr Opin Immunol 2009;21:3-9.
30. Galiana-Arnoux D, Dostert C, Schneemann A, Hoffmann JA, Imler JL. Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat Immunol 2006;7:590-597.
31. van Rij RP, et al. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 2006;20:2985-2995.
32. Wang XH, et al. RNA interference directs innate immunity against viruses in adult Drosophila. Science 2006;312:452-454.
33. Zambon RA, Vakharia VN, Wu LP. RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell Microbiol 2006;8:880-889.
34. Chotkowski HL, et al. West Nile virus infection of Drosophila melanogaster induces a protective RNAi response. Virology 2008;377:197-206.
35. Li H, Li WX, Ding SW. Induction and suppression of RNA silencing by an animal virus. Science 2002;296:1319-1321.
36. Sabin LR, Hanna SL, Cherry S. Innate antiviral immunity in Drosophila. Curr Opin Immunol 2010;22:4-9.
37. Sanchez-Vargas I, et al. RNA interference, arthropod-borne viruses, and mosquitoes. Virus Res 2004;102:65-74.
38. Li WX, et al. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc Natl Acad Sci USA 2004;101:1350-1355.
39. Campbell CL, Black WCt, Hess AM, Foy BD. Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genomics 2008;9:425.
40. Fragkoudis R, Attarzadeh-Yazdi G, Nash AA, Fazakerley JK, Kohl A. Advances in dissecting mosquito innate immune responses to arbovirus infection. J Gen Virol 2009;90:2061-2072.
41. Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, Blair CD, Olson KE. RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc Natl Acad Sci USA 2004;101:17240-17245.
42. Sanchez-Vargas I, et al. Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito's RNA interference pathway. PLoS Pathog 2009;5:e1000299.
43. Campbell CL, et al. Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol 2008;8:47.
44. Caudy AA, et al. A micrococcal nuclease homologue in RNAi effector complexes. Nature 2003;425:411-414.
45. Caudy AA, Myers M, Hannon GJ, Hammond SM. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev 2002;16:2491-2496.
46. Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol 2007;5:e220.
47. Aliyari R, et al. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 2008;4:387-397.
48. Flynt A, Liu N, Martin R, Lai EC. Dicing of viral replication intermediates during silencing of latent Drosophila viruses. Proc Natl Acad Sci USA 2009;106:5270-5275.
49. van Rij RP, Berezikov E. Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol 2009;17:163-171.
50. Brackney DE, Beane JE, Ebel GD. RNAi targeting of West Nile virus in mosquito midguts promotes virus diversification. PLoS Pathog 2009;5:e1000502.
51. Myles KM, Wiley MR, Morazzani EM, Adelman ZN. Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc Natl Acad Sci USA 2008;105:19938-19943.
52. Myles KM, Morazzani EM, Adelman ZN. Origins of alphavirus-derived small RNAs in mosquitoes. RNA Biol 2009;6:387-391.
53. Roignant JY, Carre C, Mugat B, Szymczak D, Lepesant JA, Antoniewski C. Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 2003;9:299-308.
54. Saleh MC, et al. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol 2006;8:793-802.
55. Ulvila J, et al. Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem 2006;281:14370-14375.
56. Saleh MC, et al. Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 2009;458:346-350.
57. Attarzadeh-Yazdi G, et al. Cell-to-cell spread of the RNA interference response suppresses Semliki Forest virus (SFV) infection of mosquito cell cultures and cannot be antagonized by SFV. J Virol 2009;83:5735-5748.
58. Chao DY, King CC, Wang WK, Chen WJ, Wu HL, Chang GJ. Strategically examining the full-genome of dengue virus type 3 in clinical isolates reveals its mutation spectra. Virol J 2005;2:72.
59. Nayak A, et al. Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nat Struct Mol Biol 2010;17:547-554.
60. Cirimotich CM, Scott JC, Phillips AT, Geiss BJ, Olson KE. Suppression of RNA interference increases alphavirus replication and virus-associated mortality in Aedes aegypti mosquitoes. BMC Microbiol 2009;9:49.
61. Berry B, Deddouche S, Kirschner D, Imler JL, Antoniewski C. Viral suppressors of RNA silencing hinder exogenous and endogenous small RNA pathways in Drosophila. PLoS ONE 2009;4:e5866.
62. Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009;10:141-148.
63. Lecellier CH, et al. A cellular microRNA mediates antiviral defense in human cells. Science 2005;308:557-560.
64. Otsuka M, et al. Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 2007;27:123-134.
65. Gottwein E, Cullen BR. Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 2008;3:375-387.
66. Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997;124:2463-2476.
67. O'Donnell KA, Boeke JD. Mighty Piwis defend the germline against genome intruders. Cell 2007;129:37-44.
68. Gunawardane LS, et al. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 2007;315:1587-1590.
69. Brennecke J, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007;128:1089-1103.
70. Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007;318:761-764.
71. Pane A, Wehr K, Schupbach T. zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell 2007;12:851-862.
72. Dostert C, et al. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat Immunol 2005;6:946-953.
73. Deddouche S, et al. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat Immunol 2008;9:1425-1432.
74. Xi Z, Ramirez JL, Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 2008;4:e1000098.
75. 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.
76. Lin CC, et al. Characterization of two mosquito STATs, AaSTAT and CtSTAT. Differential regulation of tyrosine phosphorylation and DNA binding activity by lipopolysaccharide treatment and by Japanese encephalitis virus infection. J Biol Chem 2004;279:3308-3317.
77. Hetru C, Hoffmann JA. NF-kappaB in the immune response of Drosophila. Cold Spring Harb Perspect Biol 2009;1:a000232.
78. Christophides GK, et al. Immunity-related genes and gene families in Anopheles gambiae. Science 2002;298:159-165.
79. Zambon RA, Nandakumar M, Vakharia VN, Wu LP. The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci USA 2005;102:7257-7262.
80. Sabatier L, et al. Pherokine-2 and -3. Eur J Biochem 2003;270:3398-3407.
81. Costa A, Jan E, Sarnow P, Schneider D. The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 2009;4:e7436.
82. Avadhanula V, Weasner BP, Hardy GG, Kumar JP, Hardy RW. A novel system for the launch of alphavirus RNA synthesis reveals a role for the Imd pathway in arthropod antiviral response. PLoS Pathog 2009;5:e1000582.
83. Sanders HR, et al. Sindbis virus induces transport processes and alters expression of innate immunity pathway genes in the midgut of the disease vector, Aedes aegypti. Insect Biochem Mol Biol 2005;35:1293-1307.
84. Fragkoudis R, et al. Semliki Forest virus strongly reduces mosquito host defence signaling. Insect Mol Biol 2008;17:647-656.
85. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN. Wolbachia and virus protection in insects. Science 2008;322:702.
86. Teixeira L, Ferreira A, Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 2008;6:e2.
87. Shelly S, Lukinova N, Bambina S, Berman A, Cherry S. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 2009;30:588-598.
88. Yano T, et al. Autophagic control of listeria through intracellular innate immune recognition in Drosophila. Nat Immunol 2008;9:908-916.
89. Bhat SA, Bashir I, Kamili AS. Microsporidiosis of silkworm, Bombyx mori L. (Lepidoptera-bombycidae): a review. Afr J Agric Res 2009;4:1519-1523.
90. Higes M, et al. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 2008;10:2659-2669.
91. Coyle CM, et al. Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. N Engl J Med 2004;351:42-47.
92. Visvesvara GS, Moura H, Leitch GJ, Schwartz DA, Xiao LX. Public health importance of Brachiola algerae (Microsporidia) - an emerging pathogen of humans. Folia Parasitol (Praha) 2005;52:83-94.
93. Kucerova Z, Moura H, Visvesvara GS, Leitch GJ. Differences between Brachiola (Nosema) algerae isolates of human and insect origin when tested using an in vitro spore germination assay and a cultured cell infection assay. J Eukaryot Microbiol 2004;51:339-343.
94. Weidner E, Canning EU, Rutledge CR, Meek CL. Mosquito (Diptera: Culicidae) host compatibility and vector competency for the human myositic parasite Trachipleistophora hominis (Phylum Microspora). J Med Entomol 1999;36:522-525.
95. Coyle CM, et al. Prevalence of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon (Septata) intestinalis among patients with AIDS-related diarrhea: determination by polymerase chain reaction to the microsporidian small-subunit rRNA gene. Clin Infect Dis 1996;23:1002-1006.
96. Andreadis TG. Microsporidian parasites of mosquitoes. J Am Mosq Control Assoc 2007;23:3-29.
97. Becnel JJ, White SE, Shapiro AM. Review of microsporidia-mosquito relationships: from the simple to the complex. Folia Parasitol (Praha) 2005;52:41-50.
98. Visvesvara GS, et al. Isolation of Nosema algerae from the cornea of an immunocompetent patient. J Eukaryot Microbiol 1999;46:10S.
99. Undeen AH, Alger NE. The effect of the microsporidan, Nosema algerae, on Anopheles stephensi. J Invertebr Pathol 1975;25:19-24.
100. Haq N, Reisen WK, Aslamkhan M. The effects of Nosema algerae on the horizontal life table attributes of Anopheles stephensi under laboratory conditions. J Invertebr Pathol 1981;37:236-242.
101. Margos G, Maier WA, Seitz HM. The effect of nosematosis on the development of Plasmodium falciparum in Anopheles stephensi. Parasitol Res 1992;78:168-171.
102. Schenker W, Maier WA, Seitz HM. The effects of Nosema algerae on the development of Plasmodium yoelii nigeriensis in Anopheles stephensi. Parasitol Res 1992;78:56-59.
103. Koella JC, Agnew P. Blood-feeding success of the mosquito Aedes aegypti depends on the transmission route of its parasite Edhazardia aedis. Oikos 1997;78:311-316.
104. Hulls RH. The adverse effects of a microsporidan on sporogony and infectivity of Plasmodium berghei. Trans R Soc Trop Med Hyg 1971;65:421-422.
105. Fox RM, Weiser J. A microsporidian parasite of Anopheles gambiae in Liberia. J Parasitol 1959;45:21-30.
106. Ward R, Savage K. Effects of microsporidian parasites upon anopheline mosquitoes and malarial infection. Proc Helminthol Soc Wash 1972;39:4.
107. Gajanana A, Tewari SC, Reuben R, Rajagopalan PK. Partial suppression of malaria parasites in Aedes aegypti and Anopheles stephensi doubly infected with Nosema algerae and Plasmodium. Indian J Med Res 1979;70:417-423.
108. Bargielowski I, Koella JC. A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis. PLoS ONE 2009;4:e4676.
109. Vijendravarma RK, Godfray HC, Kraaijeveld AR. Infection of Drosophila melanogaster by Tubulinosema kingi: stage-specific susceptibility and within-host proliferation. J Invertebr Pathol 2008;99:239-241.
110. Vijendravarma RK, Kraaijeveld AR, Godfray HC. Experimental evolution shows Drosophila melanogaster resistance to a microsporidian pathogen has fitness costs. Evolution 2009;63:104-114.
111. Biron DG, Agnew P, Marche L, Renault L, Sidobre C, Michalakis Y. Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis. Int J Parasitol 2005;35:1385-1397.
112. Levy F, Bulet P, Ehret-Sabatier L. Proteomic analysis of the systemic immune response of Drosophila. Mol Cell Proteomics 2004;3:156-166.
113. Roxstrom-Lindquist K, Terenius O, Faye I. Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO Rep 2004;5:207-212.
114. Cheng LW, Portnoy DA. Drosophila S2 cells: an alternative infection model for Listeria monocytogenes. Cell Microbiol 2003;5:875-885.
115. Mansfield BE, Dionne MS, Schneider DS, Freitag NE. Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell Microbiol 2003;5:901-911.
116. Dionne MS, Ghori N, Schneider DS. Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect Immun 2003;71:3540-3550.
117. Elwell C, Engel JN. Drosophila melanogaster S2 cells: a model system to study Chlamydia interaction with host cells. Cell Microbiol 2005;7:725-739.
118. Vonkavaara M, Telepnev MV, Ryden P, Sjostedt A, Stoven S. Drosophila melanogaster as a model for elucidating the pathogenicity of Francisella tularensis. Cell Microbiol 2008;10:1327-1338.
119. Kurata S. Extracellular and intracellular pathogen recognition by Drosophila PGRP-LE and PGRP-LC. Int Immunol 2010;22:143-148.
120. Franz AW, et al. Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc Natl Acad Sci USA 2006;103:4198-4203.