1887

Journal of General Virology header logo

Volume 103, Issue 5

The antiviral role of NF-κB-mediated immune responses and their antagonism by viruses in insects Open Access

Abstract

The antiviral role of innate immune responses mediated by the NF-κB family of transcription factors is well established in vertebrates but was for a long time less clear in insects. Insects encode two canonical NF-κB pathways, the Toll and Imd (‘immunodeficiency’) pathways, which are best characterised for their role in antibacterial and antifungal defence. An increasing body of evidence has also implicated NF-κB-mediated innate immunity in antiviral responses against some, but not all, viruses. Specific pattern recognition receptors (PRRs) and molecular events leading to NF-κB activation by viral pathogen-associated molecular patterns (PAMPs) have been elucidated for a number of viruses and insect species. Particularly interesting are recent findings indicating that the cyclic GMP-AMP synthase (cGAS)-stimulator of interferon genes (STING) pathway detects viral RNA to activate NF-κB-regulated gene expression. We summarise the literature on virus-NF-κB pathway interactions across the class , with a focus on the dipterans and . We discuss potential reasons for differences observed between different virus-host combinations, and highlight similarities and differences between cGAS-STING signalling in insects versus vertebrates. Finally, we summarise the increasing number of known molecular mechanisms by which viruses antagonise NF-κB responses, which suggest that NF-κB-mediated immunity exerts strong evolutionary pressures on viruses. These developments in our understanding of insect antiviral immunity have relevance to the large number of insect species that impact on humans through their transmission of human, livestock and plant diseases, exploitation as biotechnology platforms, and role as parasites, pollinators, livestock and pests.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): cGAS-STING signalling , Imd pathway , immune antagonism , NF-κB and Toll pathway
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/I/00007034)
    • Principle Award Recipient: KevinMaringer
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/I/00007033)
    • Principle Award Recipient: KevinMaringer
  • Department for International Development (Award MR/R010315/1)
    • Principle Award Recipient: KevinMaringer
  • Medical Research Council (Award MR/R010315/1)
    • Principle Award Recipient: KevinMaringer
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001741
2022-05-05
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/103/5/jgv001741.html?itemId=/content/journal/jgv/10.1099/jgv.0.001741&mimeType=html&fmt=ahah

References

  1. Vargas V, Cime-Castillo J, Lanz-Mendoza H. Immune priming with inactive dengue virus during the larval stage of Aedes aegypti protects against the infection in adult mosquitoes. Sci Rep 2020; 10:6723 [View Article] [PubMed]
     [Google Scholar]
  2. Rosendo Machado S, van der Most T, Miesen P. Genetic determinants of antiviral immunity in dipteran insects - Compiling the experimental evidence. Dev Comp Immunol 2021; 119:104010 [View Article] [PubMed]
     [Google Scholar]
  3. van Rij RP, Berezikov E. Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol 2009; 17:163–171 [View Article] [PubMed]
     [Google Scholar]
  4. Bronkhorst AW, van Rij RP. The long and short of antiviral defense: small RNA-based immunity in insects. Curr Opin Virol 2014; 7:19–28 [View Article] [PubMed]
     [Google Scholar]
  5. Merkling SH, van Rij RP. Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. J Insect Physiol 2013; 59:159–170 [View Article] [PubMed]
     [Google Scholar]
  6. Lamiable O, Imler JL. Induced antiviral innate immunity in Drosophila. Curr Opin Microbiol 2014; 20:62–68 [View Article] [PubMed]
     [Google Scholar]
  7. Marques JT, Imler JL. The diversity of insect antiviral immunity: insights from viruses. Curr Opin Microbiol 2016; 32:71–76 [View Article] [PubMed]
     [Google Scholar]
  8. Valanne S, Wang J-H, Rämet M. The Drosophila Toll signaling pathway. J Immunol 2011; 186:649–656 [View Article] [PubMed]
     [Google Scholar]
  9. Vlisidou I, Wood W. Drosophila blood cells and their role in immune responses. FEBS J 2015; 282:1368–1382 [View Article] [PubMed]
     [Google Scholar]
  10. Wang L, Kounatidis I, Ligoxygakis P. Drosophila as a model to study the role of blood cells in inflammation, innate immunity and cancer. Front Cell Infect Microbiol 2013; 3:113
     [Google Scholar]
  11. Eleftherianos I, Heryanto C, Bassal T, Zhang W, Tettamanti G et al. Haemocyte-mediated immunity in insects: Cells, processes and associated components in the fight against pathogens and parasites. Immunology 2021; 164:401–432 [View Article] [PubMed]
     [Google Scholar]
  12. Leite T, Ferreira ÁGA, Imler J-L, Marques JT. Distinct roles of hemocytes at different stages of infection by dengue and zika viruses in Aedes aegypti mosquitoes. Front Immunol 2021; 12:660873 [View Article]
     [Google Scholar]
  13. Lamiable O, Arnold J, de Faria IJ da S, Olmo RP, Bergami F et al. Analysis of the contribution of hemocytes and autophagy to drosophila antiviral immunity. J Virol 2016; 90:5415–5426 [View Article]
     [Google Scholar]
  14. Nainu F, Tanaka Y, Shiratsuchi A, Nakanishi Y. Protection of insects against viral infection by apoptosis-dependent phagocytosis. J Immunol 2015; 195:5696–5706 [View Article] [PubMed]
     [Google Scholar]
  15. Qiu P, Pan PC, Govind S. A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 1998; 125:1909–1920 [View Article] [PubMed]
     [Google Scholar]
  16. Sorrentino RP, Melk JP, Govind S. Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 2004; 166:1343–1356 [View Article] [PubMed]
     [Google Scholar]
  17. Baxter RHG, Contet A, Krueger K. Arthropod innate immune systems and vector-borne diseases. Biochemistry 2017; 56:907–918 [View Article] [PubMed]
     [Google Scholar]
  18. Small C, Paddibhatla I, Rajwani R, Govind S. An introduction to parasitic wasps of Drosophila and the antiparasite immune response. J Vis Exp 2012; 1:e3347 [View Article] [PubMed]
     [Google Scholar]
  19. Sheehan G, Farrell G, Kavanagh K. Immune priming: the secret weapon of the insect world. Virulence 2020; 11:238–246 [View Article] [PubMed]
     [Google Scholar]
  20. Melillo D, Marino R, Italiani P, Boraschi D. Innate immune memory in invertebrate metazoans: a critical appraisal. Front Immunol 2018; 9:1915 [View Article] [PubMed]
     [Google Scholar]
  21. Moreno-García M, Vargas V, Ramírez-Bello I, Hernández-Martínez G, Lanz-Mendoza H et al. Bacterial exposure at the larval stage induced sexual immune dimorphism and priming in adult Aedes aegypti mosquitoes. PLoS ONE 2015; 10:e0133240 [View Article] [PubMed]
     [Google Scholar]
  22. Mondotte JA, Gausson V, Frangeul L, Suzuki Y, Vazeille M et al. Evidence for long-lasting transgenerational antiviral immunity in insects. Cell Rep 2020; 33:108506 [View Article] [PubMed]
     [Google Scholar]
  23. Tetreau G, Dhinaut J, Gourbal B, Moret Y. Trans-generational immune priming in invertebrates: current knowledge and future prospects. Front Immunol 2019; 10:1938 [View Article]
     [Google Scholar]
  24. Strand MR. Polydnavirus gene products that interact with the host immune system. In Parasitoid Viruses: Symbionts and Pathogens Academic Press; 2012 pp 149–161
     [Google Scholar]
  25. Bitra K, Suderman RJ, Strand MR, Schneider DS. Polydnavirus Ank proteins bind NF-κB homodimers and inhibit processing of Relish. PLoS Pathog 2012; 8:e1002722 [View Article] [PubMed]
     [Google Scholar]
  26. Herniou EA, Huguet E, Thézé J, Bézier A, Periquet G et al. When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos Trans R Soc Lond B Biol Sci 2013; 368:20130051 [View Article] [PubMed]
     [Google Scholar]
  27. Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS et al. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007; 316:1738–1743 [View Article] [PubMed]
     [Google Scholar]
  28. Tzou P, Ohresser S, Ferrandon D, Capovilla M, Reichhart JM et al. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 2000; 13:737–748 [View Article] [PubMed]
     [Google Scholar]
  29. Silverman N, Zhou R, Erlich RL, Hunter M, Bernstein E et al. Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J Biol Chem 2003; 278:48928–48934 [View Article] [PubMed]
     [Google Scholar]
  30. Delaney JR, Stöven S, Uvell H, Anderson KV, Engström Y et al. Cooperative control of Drosophila immune responses by the JNK and NF-kappaB signaling pathways. EMBO J 2006; 25:3068–3077 [View Article] [PubMed]
     [Google Scholar]
  31. Chowdhury M, Zhang J, Xu X-X, He Z, Lu Y et al. An in vitro study of NF-κB factors cooperatively in regulation of Drosophila melanogaster antimicrobial peptide genes. Dev Comp Immunol 2019; 95:50–58 [View Article] [PubMed]
     [Google Scholar]
  32. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 2002; 21:2568–2579 [View Article] [PubMed]
     [Google Scholar]
  33. Nakamoto M, Moy RH, Xu J, Bambina S, Yasunaga A et al. Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity 2012; 36:658–667 [View Article] [PubMed]
     [Google Scholar]
  34. Weber ANR, Tauszig-Delamasure S, Hoffmann JA, Lelièvre E, Gascan H et al. Binding of the Drosophila cytokine Spätzle to Toll is direct and establishes signaling. Nat Immunol 2003; 4:794–800 [View Article] [PubMed]
     [Google Scholar]
  35. Sun H, Bristow BN, Qu G, Wasserman SA. A heterotrimeric death domain complex in Toll signaling. Proc Natl Acad Sci U S A 2002; 99:12871–12876 [View Article] [PubMed]
     [Google Scholar]
  36. Towb P, Bergmann A, Wasserman SA. The protein kinase Pelle mediates feedback regulation in the Drosophila Toll signaling pathway. Development 2001; 128:4729–4736 [View Article] [PubMed]
     [Google Scholar]
  37. Parthier C, Stelter M, Ursel C, Fandrich U, Lilie H et al. Structure of the Toll-Spatzle complex, a molecular hub in Drosophila development and innate immunity. Proc Natl Acad Sci U S A 2014; 111:6281–6286 [View Article] [PubMed]
     [Google Scholar]
  38. McIlroy G, Foldi I, Aurikko J, Wentzell JS, Lim MA et al. Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nat Neurosci 2013; 16:1248–1256 [View Article] [PubMed]
     [Google Scholar]
  39. Krantz DE, Zipursky SL. Drosophila chaoptin, a member of the leucine-rich repeat family, is a photoreceptor cell-specific adhesion molecule. EMBO J 1990; 9:1969–1977 [View Article] [PubMed]
     [Google Scholar]
  40. Rose D, Zhu X, Kose H, Hoang B, Cho J et al. Toll, a muscle cell surface molecule, locally inhibits synaptic initiation of the RP3 motoneuron growth cone in Drosophila. Development 1997; 124:1561–1571 [View Article] [PubMed]
     [Google Scholar]
  41. Kambris Z, Hoffmann JA, Imler JL, Capovilla M. Tissue and stage-specific expression of the Tolls in Drosophila embryos. Gene Expr Patterns 2002; 2:311–317 [View Article] [PubMed]
     [Google Scholar]
  42. Antonova Y, Alvarez KS, Kim YJ, Kokoza V, Raikhel AS. The role of NF-kappaB factor REL2 in the Aedes aegypti immune response. Insect Biochem Mol Biol 2009; 39:303–314 [View Article] [PubMed]
     [Google Scholar]
  43. Deddouche S, Matt N, Budd A, Mueller S, Kemp C et al. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat Immunol 2008; 9:1425–1432 [View Article] [PubMed]
     [Google Scholar]
  44. Zambon RA, Nandakumar M, Vakharia VN, Wu LP. The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci 2005; 102:7262 [View Article]
     [Google Scholar]
  45. Morales-Hojas R, Hinsley M, Armean IM, Silk R, Harrup LE et al. The genome of the biting midge Culicoides sonorensis and gene expression analyses of vector competence for bluetongue virus. BMC Genomics 2018; 19:624 [View Article] [PubMed]
     [Google Scholar]
  46. Dostert C, Jouanguy E, Irving P, Troxler L, Galiana-Arnoux D et al. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat Immunol 2005; 6:946–953 [View Article] [PubMed]
     [Google Scholar]
  47. Souza-Neto JA, Sim S, Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci U S A 2009; 106:17841–17846 [View Article] [PubMed]
     [Google Scholar]
  48. Merkling SH, Overheul GJ, van Mierlo JT, Arends D, Gilissen C et al. The heat shock response restricts virus infection in Drosophila. Sci Rep 2015; 5:12758 [View Article] [PubMed]
     [Google Scholar]
  49. Ferreira ÁG, Naylor H, Esteves SS, Pais IS, Martins NE et al. The Toll-dorsal pathway is required for resistance to viral oral infection in Drosophila. PLoS Pathog 2014; 10:e1004507 [View Article] [PubMed]
     [Google Scholar]
  50. Xiao X, Liu Y, Zhang X, Wang J, Li Z et al. Complement-related proteins control the flavivirus infection of Aedes aegypti by inducing antimicrobial peptides. PLoS Pathog 2014; 10:e1004027 [View Article] [PubMed]
     [Google Scholar]
  51. He Y-J, Lu G, Qi Y-H, Zhang Y, Zhang X-D et al. Activation of toll immune pathway in an insect vector induced by a plant virus. Front Immunol 2020; 11:613957 [View Article] [PubMed]
     [Google Scholar]
  52. Yagi Y, Nishida Y, Ip YT. Functional analysis of Toll-related genes in Drosophila. Dev Growth Differ 2010; 52:771–783 [View Article] [PubMed]
     [Google Scholar]
  53. Russell TA, Ayaz A, Davidson AD, Fernandez-Sesma A, Maringer K. Imd pathway-specific immune assays reveal NF-κB stimulation by viral RNA PAMPs in Aedes aegypti Aag2 cells. PLoS Negl Trop Dis 2021; 15:1–23 [View Article] [PubMed]
     [Google Scholar]
  54. Hua X, Li B, Song L, Hu C, Li X et al. Stimulator of interferon genes (STING) provides insect antiviral immunity by promoting Dredd caspase-mediated NF-κB activation. J Biol Chem 2018; 293:11878–11890 [View Article] [PubMed]
     [Google Scholar]
  55. Angleró-Rodríguez YI, Tikhe CV, Kang S, Dimopoulos G. Aedes aegypti Toll pathway is induced through dsRNA sensing in endosomes. Dev Comp Immunol 2021; 122:104138 [View Article] [PubMed]
     [Google Scholar]
  56. Zhang R, Zhu Y, Pang X, Xiao X, Zhang R et al. Regulation of antimicrobial peptides in Aedes aegypti Aag2 cells. Front Cell Infect Microbiol 2017; 7:22 [View Article] [PubMed]
     [Google Scholar]
  57. Slavik KM, Morehouse BR, Ragucci AE, Zhou W, Ai X et al. cGAS-like receptors sense RNA and control 3’2’-cGAMP signalling in Drosophila. Nature 2021; 597:109–113 [View Article] [PubMed]
     [Google Scholar]
  58. Holleufer A, Winther KG, Gad HH, Ai X, Chen Y et al. Two cGAS-like receptors induce antiviral immunity in Drosophila. Nature 2021; 597:114–118 [View Article] [PubMed]
     [Google Scholar]
  59. Maringer K, Fernandez-Sesma A. Message in a bottle: lessons learned from antagonism of STING signalling during RNA virus infection. Cytokine Growth Factor Rev 2014; 25:669–679 [View Article] [PubMed]
     [Google Scholar]
  60. Goto A, Okado K, Martins N, Cai H, Barbier V et al. The Kinase IKKβ Regulates a STING- and NF-κB-Dependent Antiviral Response Pathway in Drosophila. Immunity 2018; 49:225–234 [View Article] [PubMed]
     [Google Scholar]
  61. Ganesan S, Aggarwal K, Paquette N, Silverman N. NF-κB/Rel proteins and the humoral immune responses of Drosophila melanogaster. In Current Topics in Microbiology and Immunology vol 349 2012 pp 25–60 [View Article]
     [Google Scholar]
  62. Cai H, Holleufer A, Simonsen B, Schneider J, Lemoine A et al. 2’3’-cGAMP triggers a STING- and NF-κB-dependent broad antiviral response in Drosophila. Sci Signal 2020; 13:1 [View Article] [PubMed]
     [Google Scholar]
  63. Saleh M-C, van Rij RP, Hekele A, Gillis A, Foley E et al. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol 2006; 8:793–802 [View Article] [PubMed]
     [Google Scholar]
  64. Abbasi R, Heschuk D, Kim B, Whyard S. A novel paperclip double-stranded RNA structure demonstrates clathrin-independent uptake in the mosquito Aedes aegypti. Insect Biochem Mol Biol 2020; 127:103492 [View Article] [PubMed]
     [Google Scholar]
  65. Margolis SR, Wilson SC, Vance RE. Evolutionary Origins of cGAS-STING Signaling. Trends Immunol 2017; 38:733–743 [View Article] [PubMed]
     [Google Scholar]
  66. Wu X, Wu F-H, Wang X, Wang L, Siedow JN et al. Molecular evolutionary and structural analysis of the cytosolic DNA sensor cGAS and STING. Nucleic Acids Res 2014; 42:8243–8257 [View Article] [PubMed]
     [Google Scholar]
  67. Kranzusch PJ, Wilson SC, Lee ASY, Berger JM, Doudna JA et al. Ancient Origin of cGAS-STING Reveals Mechanism of Universal 2’,3’ cGAMP Signaling. Mol Cell 2015; 59:891–903 [View Article] [PubMed]
     [Google Scholar]
  68. Palmer WH, Medd NC, Beard PM, Obbard DJ. Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses. PLoS Pathog 2018; 14:e1007050 [View Article] [PubMed]
     [Google Scholar]
  69. Paradkar PN, Duchemin JB, Voysey R, Walker PJ. Dicer-2-dependent activation of Culex Vago occurs via the TRAF-Rel2 signaling pathway. PLoS Negl Trop Dis 2014; 8:e2823 [View Article] [PubMed]
     [Google Scholar]
  70. Wang Z, Wu D, Liu Y, Xia X, Gong W et al. Drosophila Dicer-2 has an RNA interference-independent function that modulates Toll immune signaling. Sci Adv 2015; 1:e1500228 [View Article] [PubMed]
     [Google Scholar]
  71. Costa A, Jan E, Sarnow P, Schneider D, Sommer P. The IMD pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 2009; 4:e7436 [View Article]
     [Google Scholar]
  72. 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 [View Article] [PubMed]
     [Google Scholar]
  73. Sansone CL, Cohen J, Yasunaga A, Xu J, Osborn G et al. Microbiota-dependent priming of antiviral intestinal immunity in Drosophila. Cell Host Microbe 2015; 18:571–581 [View Article] [PubMed]
     [Google Scholar]
  74. Huang Z, Kingsolver MB, Avadhanula V, Hardy RW. An antiviral role for antimicrobial peptides during the arthropod response to alphavirus replication. J Virol 2013; 87:4272–4280 [View Article] [PubMed]
     [Google Scholar]
  75. Palmer WH, Joosten J, Overheul GJ, Jansen PW, Vermeulen M et al. Induction and Suppression of NF-κB Signalling by a DNA Virus of Drosophila. J Virol 2019; 93:1443–1461 [View Article]
     [Google Scholar]
  76. Zambon RA, Nandakumar M, Vakharia VN, Wu LP. The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci U S A 2005; 102:7257–7262 [View Article] [PubMed]
     [Google Scholar]
  77. Fragkoudis R, Chi Y, Siu RWC, Barry G, Attarzadeh-Yazdi G et al. Semliki Forest virus strongly reduces mosquito host defence signaling. Insect Mol Biol 2008; 17:647–656 [View Article] [PubMed]
     [Google Scholar]
  78. McFarlane M, Arias-Goeta C, Martin E, O’Hara Z, Lulla A et al. Characterization of Aedes aegypti innate-immune pathways that limit Chikungunya virus replication. PLoS Negl Trop Dis 2014; 8:e2994 [View Article] [PubMed]
     [Google Scholar]
  79. Luplertlop N, Surasombatpattana P, Patramool S, Dumas E, Wasinpiyamongkol L et al. Induction of a peptide with activity against a broad spectrum of pathogens in the Aedes aegypti salivary gland, following Infection with Dengue Virus. PLoS Pathog 2011; 7:e1001252 [View Article] [PubMed]
     [Google Scholar]
  80. 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 [View Article] [PubMed]
     [Google Scholar]
  81. Xi Z, Ramirez JL, Dimopoulos G, Schneider DS. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 2008; 4:e1000098 [View Article] [PubMed]
     [Google Scholar]
  82. Liu J, Liu Y, Nie K, Du S, Qiu J et al. Flavivirus NS1 protein in infected host sera enhances viral acquisition by mosquitoes. Nat Microbiol 2016; 1:16087 [View Article] [PubMed]
     [Google Scholar]
  83. Chowdhury A, Modahl CM, Tan ST, Wong Wei Xiang B, Missé D et al. JNK pathway restricts DENV2, ZIKV and CHIKV infection by activating complement and apoptosis in mosquito salivary glands. PLoS Pathog 2020; 16:e1008754 [View Article] [PubMed]
     [Google Scholar]
  84. Shi Z-K, Wen D, Chang M-M, Sun X-M, Wang Y-H et al. Juvenile hormone-sensitive ribosomal activity enhances viral replication in Aedes aegypti. mSystems 2021; 6:e0119020 [View Article]
     [Google Scholar]
  85. Liu K, Xiao C, Xi S, Hameed M, Wahaab A et al. Mosquito defensins enhance japanese encephalitis virus infection by facilitating virus adsorption and entry within the mosquito. J Virol 2020; 94:e01164-20 [View Article] [PubMed]
     [Google Scholar]
  86. Waldock J, Olson KE, Christophides GK. Anopheles gambiae antiviral immune response to systemic O’nyong-nyong infection. PLoS Negl Trop Dis 2012; 6:e1565 [View Article] [PubMed]
     [Google Scholar]
  87. Carissimo G, Pondeville E, McFarlane M, Dietrich I, Mitri C et al. Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota. Proc Natl Acad Sci U S A 2015; 112:E176–85 [View Article] [PubMed]
     [Google Scholar]
  88. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G et al. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 2012; 8:e1002735 [View Article] [PubMed]
     [Google Scholar]
  89. Liu Y, Gordesky-Gold B, Leney-Greene M, Weinbren NL, Tudor M et al. Inflammation-Induced, STING-dependent autophagy restricts zika virus infection in the Drosophila Brain. Cell Host Microbe 2018; 24:57–68 [View Article] [PubMed]
     [Google Scholar]
  90. Martin M, Hiroyasu A, Guzman RM, Roberts SA, Goodman AG. Analysis of Drosophila STING Reveals an Evolutionarily Conserved Antimicrobial Function. Cell Rep 2018; 23:3537–3550 [View Article] [PubMed]
     [Google Scholar]
  91. Elrefaey AME, Hollinghurst P, Reitmayer CM, Alphey L, Maringer K. Innate Immune Antagonism of Mosquito-Borne Flaviviruses in Humans and Mosquitoes. Viruses 2021; 13:2116 [View Article] [PubMed]
     [Google Scholar]
  92. West C, Rus F, Chen Y, Kleino A, Gangloff M et al. IIV-6 Inhibits NF-κB Responses in Drosophila. Viruses 2019; 11:409 [View Article]
     [Google Scholar]
  93. Lamiable O, Kellenberger C, Kemp C, Troxler L, Pelte N et al. Cytokine Diedel and a viral homologue suppress the IMD pathway in Drosophila. Proc Natl Acad Sci U S A 2016; 113:698–703 [View Article] [PubMed]
     [Google Scholar]
  94. Sim S, Dimopoulos G. Dengue virus inhibits immune responses in Aedes aegypti cells. PLoS One 2010; 5:e10678 [View Article] [PubMed]
     [Google Scholar]
  95. Pompon J, Manuel M, Ng GK, Wong B, Shan C et al. Dengue subgenomic flaviviral RNA disrupts immunity in mosquito salivary glands to increase virus transmission. PLoS Pathog 2017; 13:e1006535 [View Article] [PubMed]
     [Google Scholar]
  96. Méndez Y, Pacheco C, Herrera F. Inhibition of defensin A and cecropin A responses to dengue virus 1 infection in Aedes aegypti. Biomedica 2021; 41:161–167 [View Article] [PubMed]
     [Google Scholar]
  97. Bidet K, Garcia-Blanco MA. Flaviviral RNAs: weapons and targets in the war between virus and host. Biochem J 2014; 462:215–230 [View Article] [PubMed]
     [Google Scholar]
  98. Roby JA, Pijlman GP, Wilusz J, Khromykh AA. Noncoding subgenomic flavivirus RNA: multiple functions in West Nile virus pathogenesis and modulation of host responses. Viruses 2014; 6:404–427 [View Article] [PubMed]
     [Google Scholar]
  99. Sepúlveda-Salinas KJ, Ramos-Castañeda J. Participation of dengue virus NS4B protein in the modulation of immune effectors dependent on ER stress in insect cells. Cell Stress Chaperones 2017; 22:799–810 [View Article] [PubMed]
     [Google Scholar]
  100. Jupatanakul N, Sim S, Dimopoulos G. The insect microbiome modulates vector competence for arboviruses. Viruses 2014; 6:4294–4313 [View Article] [PubMed]
     [Google Scholar]
  101. Ramirez JL, Souza-Neto J, Torres Cosme R, Rovira J, Ortiz A et al. Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis 2012; 6:e1561 [View Article] [PubMed]
     [Google Scholar]
  102. Lima LF, Torres AQ, Jardim R, Mesquita RD, Schama R. Evolution of Toll, Spatzle and MyD88 in insects: the problem of the Diptera bias. BMC Genomics 2021; 22:1–21 [View Article] [PubMed]
     [Google Scholar]
  103. Feng M, Fei S, Xia J, Labropoulou V, Swevers L et al. Antimicrobial Peptides as Potential Antiviral Factors in Insect Antiviral Immune Response. Front Immunol 2020; 11:2030 [View Article] [PubMed]
     [Google Scholar]
  104. Habayeb MS, Ekengren SK, Hultmark D. Nora virus, a persistent virus in Drosophila, defines a new picorna-like virus family. J Gen Virol 2006; 87:3045–3051 [View Article]
     [Google Scholar]
  105. Smartt CT, Shin D, Alto BW. Dengue serotype-specific immune response in Aedes aegypti and Aedes albopictus. Mem Inst Oswaldo Cruz 2017; 112:829–837 [View Article]
     [Google Scholar]
  106. Pan X, Zhou G, Wu J, Bian G, Lu P et al. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A 2012; 109:E23–31 [View Article]
     [Google Scholar]
  107. Barletta ABF, Nascimento-Silva MCL, Talyuli OAC, Oliveira JHM, Pereira LOR et al. Microbiota activates IMD pathway and limits Sindbis infection in Aedes aegypti. Parasit Vectors 2017; 10:103 [View Article]
     [Google Scholar]
  108. Angleró-Rodríguez YI, MacLeod HJ, Kang S, Carlson JS, Jupatanakul N et al. Aedes aegypti Molecular Responses to Zika Virus: Modulation of Infection by the Toll and Jak/Stat Immune Pathways and Virus Host Factors. Front Microbiol 2017; 8:2050 [View Article] [PubMed]
     [Google Scholar]
  109. Liu Y-X, Li F-X, Liu Z-Z, Jia Z-R, Zhou Y-H et al. Integrated analysis of miRNAs and transcriptomes in Aedes albopictus midgut reveals the differential expression profiles of immune-related genes during dengue virus serotype-2 infection. Insect Sci 2016; 23:377–385 [View Article] [PubMed]
     [Google Scholar]
  110. Paradkar PN, Duchemin J-B, Voysey R, Walker PJ, Olson KE. Dicer-2-dependent activation of Culex Vago occurs via the TRAF-Rel2 signaling pathway. PLoS Negl Trop Dis 2014; 8:e2823 [View Article] [PubMed]
     [Google Scholar]
  111. Barroso-Arévalo S, Vicente-Rubiano M, Puerta F, Molero F, Sánchez-Vizcaíno JM. Immune related genes as markers for monitoring health status of honey bee colonies. BMC Vet Res 2019; 15:72 [View Article] [PubMed]
     [Google Scholar]
  112. Kuster RD, Boncristiani HF, Rueppell O. Immunogene and viral transcript dynamics during parasitic Varroa destructor mite infection of developing honey bee (Apis mellifera) pupae. J Exp Biol 2014; 217:1710–1718 [View Article] [PubMed]
     [Google Scholar]
  113. Flenniken ML, Andino R, Smagghe G. Non-specific dsRNA-mediated antiviral response in the honey bee. PLoS ONE 2013; 8:e77263 [View Article] [PubMed]
     [Google Scholar]
  114. Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog 2014; 10:e1004230 [View Article]
     [Google Scholar]
  115. Galbraith DA, Yang X, Niño EL, Yi S, Grozinger C. Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLoS Pathog 2015; 11:1–24 [View Article] [PubMed]
     [Google Scholar]
  116. Lourenço AP, Florecki MM, Simões ZLP, Evans JD. Silencing of Apis mellifera dorsal genes reveals their role in expression of the antimicrobial peptide defensin-1. Insect Mol Biol 2018; 27:577–589 [View Article] [PubMed]
     [Google Scholar]
  117. Núñez AI, Esteve-Codina A, Gómez-Garrido J, Brustolin M, Talavera S et al. Alteration in the Culex pipiens transcriptome reveals diverse mechanisms of the mosquito immune system implicated upon Rift Valley fever phlebovirus exposure. PLoS Negl Trop Dis 2020; 14:e0008870 [View Article] [PubMed]
     [Google Scholar]
  118. Kemp C, Mueller S, Goto A, Barbier V, Paro S et al. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J Immunol 2013; 190:650–658 [View Article] [PubMed]
     [Google Scholar]
  119. Lopez W, Page AM, Carlson DJ, Ericson BL, Cserhati MF et al. Analysis of immune-related genes during Nora virus infection of Drosophila melanogaster using next generation sequencing. AIMS Microbiol 2018; 4:123–139 [View Article] [PubMed]
     [Google Scholar]
  120. Tsai CW, McGraw EA, Ammar E-D, Dietzgen RG, Hogenhout SA. Drosophila melanogaster mounts a unique immune response to the Rhabdovirus sigma virus. Appl Environ Microbiol 2008; 74:3251–3256 [View Article] [PubMed]
     [Google Scholar]
  121. 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 [View Article] [PubMed]
     [Google Scholar]
  122. Zhao P, Xia F, Jiang L, Guo H, Xu G et al. Enhanced antiviral immunity against Bombyx mori cytoplasmic polyhedrosis virus via overexpression of peptidoglycan recognition protein S2 in transgenic silkworms. Dev Comp Immunol 2018; 87:84–89 [View Article] [PubMed]
     [Google Scholar]
  123. Bao Y-Y, Lv Z-Y, Liu Z-B, Xue J, Xu Y-P et al. Comparative analysis of Bombyx mori nucleopolyhedrovirus responsive genes in fat body and haemocyte of B. mori resistant and susceptible strains. Insect Mol Biol 2010; 19:347–358 [View Article] [PubMed]
     [Google Scholar]
  124. Wang Q, Liu Y, He HJ, Zhao XF, Wang JX. Immune responses of Helicoverpa armigera to different kinds of pathogens. BMC Immunol 2010; 11:9 [View Article] [PubMed]
     [Google Scholar]
  125. Nguyen Q, Chan LCL, Nielsen LK, Reid S. Genome scale analysis of differential mRNA expression of Helicoverpa Zea insect cells infected with a H. armigera baculovirus. Virology 2013; 444:158–170 [View Article] [PubMed]
     [Google Scholar]
  126. Zaghloul HAH, Hice R, Bideshi DK, Arensburger P, Federici BA. Mitochondrial and Innate Immunity Transcriptomes from Spodoptera frugiperda Larvae Infected with the Spodoptera frugiperda Ascovirus. J Virol 2020; 94:e01985-19 [View Article] [PubMed]
     [Google Scholar]
  127. Shrestha A, Bao K, Chen W, Wang P, Fei Z et al. Transcriptional responses of the Trichoplusia ni Midgut to Oral Infection by the Baculovirus Autographa californica multiple nucleopolyhedrovirus. J Virol 2019; 93:14 [View Article] [PubMed]
     [Google Scholar]
  128. Moreno-Habel DA, Biglang-awa IM, Dulce A, Luu DD, Garcia P et al. Inactivation of the budded virus of Autographa californica M nucleopolyhedrovirus by gloverin. J Invertebr Pathol 2012; 110:92–101 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001741
Loading
The antiviral role of NF-κB-mediated immune responses and their antagonism by viruses in insects
J. Gen. Virol. 103, 001741 (2022); https://doi.org/10.1099/jgv.0.001741
/content/journal/jgv/10.1099/jgv.0.001741
/content/journal/jgv/10.1099/jgv.0.001741
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error