1932

Abstract

As an overarching immune mechanism, RNA interference (RNAi) displays pathogen specificity and memory via different pathways. The small interfering RNA (siRNA) pathway is the primary antiviral defense mechanism against RNA viruses of insects and plays a lesser role in defense against DNA viruses. Reflecting the pivotal role of the siRNA pathway in virus selection, different virus families have independently evolved unique strategies to counter this host response, including protein-mediated, decoy RNA–based, and microRNA-based strategies. In this review, we outline the interplay between insect viruses and the different pathways of the RNAi antiviral response; describe practical application of these interactions for improved expression systems and for pest and disease management; and highlight research avenues for advancement of the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-033020-090410
2021-01-07
2024-06-14
Loading full text...

Full text loading...

/deliver/fulltext/en/66/1/annurev-ento-033020-090410.html?itemId=/content/journals/10.1146/annurev-ento-033020-090410&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adelman ZN, Blair CD, Carlson JO, Beaty BJ, Olson KE 2001. Sindbis virus-induced silencing of dengue viruses in mosquitoes. Insect. Mol. Biol. 10:265–73
    [Google Scholar]
  2. 2. 
    Aliyari R, Wu Q, Li HW, Wang XH, Li F et al. 2008. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 4:387–97
    [Google Scholar]
  3. 3. 
    Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215–33
    [Google Scholar]
  4. 4. 
    Behrens S, Peuß R, Milutinović B, Eggert H, Esser D et al. 2014. Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis. BMC Genom 15:445
    [Google Scholar]
  5. 5. 
    Bernstein E, Caudy AA, Hammond SM, Hannon GJ 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–66
    [Google Scholar]
  6. 6. 
    Berry B, Deddouche S, Kirschner D, Imler JL, Antoniewski C 2009. Viral suppressors of RNA silencing hinder exogenous and endogenous small RNA pathways in Drosophila. PLOS ONE 4:e5866
    [Google Scholar]
  7. 7. 
    Brennecke J, Aravin AA, Stark A, Dus M, Kellis M et al. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–103
    [Google Scholar]
  8. 8. 
    Bronkhorst AW, van Cleef KW, Venselaar H, van Rij RP 2014. A dsRNA-binding protein of a complex invertebrate DNA virus suppresses the Drosophila RNAi response. Nucleic Acids Res 42:12237–48
    [Google Scholar]
  9. 9. 
    Bronkhorst AW, van Cleef KWR, Vodovar N, İnce İA, Blanc H et al. 2012. The DNA virus Invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. PNAS 109:E3604–13
    [Google Scholar]
  10. 10. 
    Bronkhorst AW, Vogels R, Overheul GJ, Pennings B, Gausson-Dorey V et al. 2019. A DNA virus-encoded immune antagonist fully masks the potent antiviral activity of RNAi in Drosophila. PNAS 116:24296–302
    [Google Scholar]
  11. 11. 
    Brutscher LM, Daughenbaugh KF, Flenniken ML 2017. Virus and dsRNA-triggered transcriptional responses reveal key components of honey bee antiviral defense. Sci. Rep. 7:6448
    [Google Scholar]
  12. 12. 
    Campbell CL, Black WC, Hess AM, Foy BD 2008. Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genom 9:425
    [Google Scholar]
  13. 13. 
    Carrillo-Tripp J, Dolezal AG, Goblirsch MJ, Miller WA, Toth AL, Bonning BC 2016. In vivo and in vitro infection dynamics of honey bee viruses. Sci. Rep. 6:22265
    [Google Scholar]
  14. 14. 
    Carrillo-Tripp J, Krueger EN, Harrison RL, Toth AL, Miller WA, Bonning BC 2014. Lymantria dispar iflavirus 1 (LdIV1), a new model to study iflaviral persistence in lepidopterans. J. Gen. Virol. 95:2285–96
    [Google Scholar]
  15. 15. 
    Cenik ES, Zamore PD. 2011. Argonaute proteins. Curr. Biol. 21:R446–49
    [Google Scholar]
  16. 16. 
    Chao JA, Lee JH, Chapados BR, Debler EW, Schneemann A, Williamson JR 2005. Dual modes of RNA-silencing suppression by Flock House virus protein B2. Nat. Struct. Mol. Biol. 12:952–57
    [Google Scholar]
  17. 17. 
    Chavez-Pena C, Kamen AA. 2018. RNA interference technology to improve the baculovirus-insect cell expression system. Biotechnol. Adv. 36:443–51
    [Google Scholar]
  18. 18. 
    Cora E, Pandey RR, Xiol J, Taylor J, Sachidanandam R et al. 2014. The MID-PIWI module of Piwi proteins specifies nucleotide- and strand-biases of piRNAs. RNA 20:773–81
    [Google Scholar]
  19. 19. 
    Cullen BR. 2011. Viruses and microRNAs: RISCy interactions with serious consequences. Genes Dev 25:1881–94
    [Google Scholar]
  20. 20. 
    Czech B, Hannon GJ. 2016. One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem. Sci. 41:324–37
    [Google Scholar]
  21. 21. 
    de Oliveira VC, da Silva Morgado F, Ardisson-Araujo DM, Resende RO, Ribeiro BM 2015. The silencing suppressor (NSs) protein of the plant virus Tomato spotted wilt virus enhances heterologous protein expression and baculovirus pathogenicity in cells and lepidopteran insects. Arch. Virol. 160:2873–79
    [Google Scholar]
  22. 22. 
    Deddouche S, Matt N, Budd A, Mueller S, Kemp C et al. 2008. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat. Immunol 9:1425–32
    [Google Scholar]
  23. 23. 
    Elbashir SM, Lendeckel W, Tuschl T 2001. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188–200
    [Google Scholar]
  24. 24. 
    Elbashir SM, Martinez J, Patkaniowska A, Lendeckel W, Tuschl T 2001. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J 20:6877–88
    [Google Scholar]
  25. 25. 
    Fareh M, van Lopik J, Katechis I, Bronkhorst AW, Haagsma AC et al. 2018. Viral suppressors of RNAi employ a rapid screening mode to discriminate viral RNA from cellular small RNA. Nucleic Acids Res 46:3187–97
    [Google Scholar]
  26. 26. 
    Ferreira ÁG, Naylor H, Esteves SS, Pais IS, Martins NE, Teixeira L 2014. The Toll-dorsal pathway is required for resistance to viral oral infection in Drosophila. PLOS Pathog 10:e1004507
    [Google Scholar]
  27. 27. 
    Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9:397–405
    [Google Scholar]
  28. 28. 
    Förstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD 2007. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 130:287–97
    [Google Scholar]
  29. 29. 
    Fujino K, Horie M, Honda T, Merriman DK, Tomonaga K 2014. Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome. PNAS 111:13175–80
    [Google Scholar]
  30. 30. 
    Gainetdinov I, Colpan C, Arif A, Cecchini K, Zamore PD 2018. A single mechanism of biogenesis, initiated and directed by PIWI proteins, explains piRNA production in most animals. Mol. Cell 71:775–90
    [Google Scholar]
  31. 31. 
    Galbraith DA, Yang X, Nino EL, Yi S, Grozinger C 2015. Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLOS Pathog 11:e1004713
    [Google Scholar]
  32. 32. 
    Garbutt JS, Reynolds SE. 2012. Induction of RNA interference genes by double-stranded RNA: implications for susceptibility to RNA interference. Insect Biochem. Mol. Biol. 42:621–28
    [Google Scholar]
  33. 33. 
    Ghildiyal M, Seitz H, Horwich MD, Li C, Du T et al. 2008. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320:1077–81
    [Google Scholar]
  34. 34. 
    Goic B, Stapleford KA, Frangeul L, Doucet AJ, Gausson V et al. 2016. Virus-derived DNA drives mosquito vector tolerance to arboviral infection. Nat. Commun. 7:12410
    [Google Scholar]
  35. 35. 
    Goic B, Vodovar N, Mondotte JA, Monot C, Frangeul L et al. 2013. RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila. Nat. Immunol 14:396–403
    [Google Scholar]
  36. 36. 
    Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y et al. 2007. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315:1587–90
    [Google Scholar]
  37. 37. 
    Gupta V, Vasanthakrishnan RB, Siva-Jothy J, Monteith KM, Brown SP, Vale PF 2017. The route of infection determines Wolbachia antibacterial protection in Drosophila. Proc. R. Soc. B 284:20170809
    [Google Scholar]
  38. 38. 
    Hajeri S, Killiny N, El-Mohtar C, Dawson WO, Gowda S 2014. Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). J. Biotechnol. 176:42–49
    [Google Scholar]
  39. 39. 
    Han BW, Wang W, Li C, Weng Z, Zamore PD 2015. piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production. Science 348:817–21
    [Google Scholar]
  40. 40. 
    Harsh S, Ozakman Y, Kitchen SM, Paquin-Proulx D, Nixon DF, Eleftherianos I 2018. Dicer-2 regulates resistance and maintains homeostasis against Zika virus infection in Drosophila. J. Immunol 201:3058–72
    [Google Scholar]
  41. 41. 
    Hayashi R, Schnabl J, Handler D, Mohn F, Ameres SL, Brennecke J 2016. Genetic and mechanistic diversity of piRNA 3′-end formation. Nature 539:588–92
    [Google Scholar]
  42. 42. 
    Hodgson JJ, Wenger LW, Clem RJ, Passarelli AL 2019. Inhibition of dicer activity in lepidopteran and dipteran cells by baculovirus-mediated expression of Flock House virus B2. Sci. Rep. 9:14494
    [Google Scholar]
  43. 43. 
    Holmes EC. 2011. The evolution of endogenous viral elements. Cell Host Microbe 10:368–77
    [Google Scholar]
  44. 44. 
    Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H 2013. A major epigenetic programming mechanism guided by piRNAs. Dev. Cell 24:502–16
    [Google Scholar]
  45. 45. 
    Hussain M, Abraham AM, Asgari S 2010. An Ascovirus-encoded RNase III autoregulates its expression and suppresses RNA interference-mediated gene silencing. J. Virol. 84:3624–30
    [Google Scholar]
  46. 46. 
    Hussain M, Taft RJ, Asgari S 2008. An insect virus-encoded microRNA regulates viral replication. J. Virol. 82:9164–70
    [Google Scholar]
  47. 47. 
    Hussain M, Torres S, Schnettler E, Funk A, Grundhoff A et al. 2012. West Nile virus encodes a microRNA-like small RNA in the 3′ untranslated region which up-regulates GATA4 mRNA and facilitates virus replication in mosquito cells. Nucleic Acids Res 40:2210–23
    [Google Scholar]
  48. 48. 
    Iwakawa HO, Tomari Y. 2015. The functions of microRNAs: mRNA decay and translational repression. Trends Cell Biol 25:651–65
    [Google Scholar]
  49. 49. 
    Junglen S, Korries M, Grasse W, Wieseler J, Kopp A et al. 2017. Host range restriction of insect-specific flaviviruses occurs at several levels of the viral life cycle. mSphere 2:e00375–16
    [Google Scholar]
  50. 50. 
    Kakumani PK, Ponia SS, S RK, Sood V, Chinnappan M et al. 2013. Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor. J. Virol. 87:8870–83
    [Google Scholar]
  51. 51. 
    Katzourakis A, Gifford RJ. 2010. Endogenous viral elements in animal genomes. PLOS Genet 6:e1001191
    [Google Scholar]
  52. 52. 
    Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, Blair CD, Olson KE 2004. RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. PNAS 101:17240–45
    [Google Scholar]
  53. 53. 
    Kerr CH, Wang QS, Keatings K, Khong A, Allan D et al. 2015. The 5′ untranslated region of a novel infectious molecular clone of the dicistrovirus Cricket paralysis virus modulates infection. J. Virol. 89:5919–34
    [Google Scholar]
  54. 54. 
    Khan AM, Ashfaq M, Khan AA, Naseem MT, Mansoor S 2018. Evaluation of potential RNA-interference-target genes to control cotton mealybug, Phenacoccus solenopsis (Hemiptera: Pseudococcuidae). Insect Sci 25:778–86
    [Google Scholar]
  55. 55. 
    Khan AM, Ashfaq M, Kiss Z, Khan AA, Mansoor S, Falk BW 2013. Use of recombinant Tobacco mosaic virus to achieve RNA interference in plants against the citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae). PLOS ONE 8:e73657
    [Google Scholar]
  56. 56. 
    Khong A, Kerr CH, Yeung CH, Keatings K, Nayak A et al. 2017. Disruption of stress granule formation by the multifunctional Cricket paralysis virus 1A protein. J. Virol. 91:e01779–16
    [Google Scholar]
  57. 57. 
    Khoo CC, Doty JB, Heersink MS, Olson KE, Franz AW 2013. Transgene-mediated suppression of the RNA interference pathway in Aedes aegypti interferes with gene silencing and enhances Sindbis virus and dengue virus type 2 replication. Insect Mol. Biol. 22:104–14
    [Google Scholar]
  58. 58. 
    Klenerman P, Hengartner H, Zinkernagel RM 1997. A non-retroviral RNA virus persists in DNA form. Nature 390:298–301
    [Google Scholar]
  59. 59. 
    Kumar P, Pandit SS, Baldwin IT 2012. Tobacco rattle virus vector: a rapid and transient means of silencing Manduca sexta genes by plant mediated RNA interference. PLOS ONE 7:e31347
    [Google Scholar]
  60. 60. 
    Lamp B, Url A, Seitz K, Eichhorn J, Riedel C et al. 2016. Construction and rescue of a molecular clone of Deformed wing virus (DWV). PLOS ONE 11:e0164639
    [Google Scholar]
  61. 61. 
    Lee HS, Lee HY, Kim YJ, Jung HD, Choi KJ et al. 2015. Small interfering (Si) RNA mediated baculovirus replication reduction without affecting target gene expression. Virus Res 199:68–76
    [Google Scholar]
  62. 62. 
    Lee Y, Ahn C, Han J, Choi H, Kim J et al. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–19
    [Google Scholar]
  63. 63. 
    Lee Y, Kim M, Han J, Yeom KH, Lee S et al. 2004. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–60
    [Google Scholar]
  64. 64. 
    Lee YS, Nakahara K, Pham JW, Kim K, He Z et al. 2004. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117:69–81
    [Google Scholar]
  65. 65. 
    Lewis SH, Salmela H, Obbard DJ 2016. Duplication and diversification of dipteran Argonaute genes, and the evolutionary divergence of Piwi and Aubergine. Genome Biol. Evol. 8:507–18
    [Google Scholar]
  66. 66. 
    Lingel A, Simon B, Izaurralde E, Sattler M 2005. The structure of the flock house virus B2 protein, a viral suppressor of RNA interference, shows a novel mode of double-stranded RNA recognition. EMBO Rep 6:1149–55
    [Google Scholar]
  67. 67. 
    Liu Y, Zhang L, Zhang Y, Liu D, Du E, Yang Z 2015. Functional analysis of RNAi suppressor P19 on improving baculovirus yield and transgene expression in Sf9 cells. Biotechnol. Lett. 37:2159–66
    [Google Scholar]
  68. 68. 
    Lozano J, Gomez-Orte E, Lee H-J, Belles X 2012. Super-induction of Dicer-2 expression by alien double-stranded RNAs: an evolutionary ancient response to viral infection. Dev. Genes Evol. 222:229–35
    [Google Scholar]
  69. 69. 
    Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U 2004. Nuclear export of microRNA precursors. Science 303:95–98
    [Google Scholar]
  70. 70. 
    Ma J-B, Yuan Y-R, Meister G, Pei Y, Tuschl T, Patel DJ 2005. Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434:666–70
    [Google Scholar]
  71. 71. 
    Maori E, Tanne E, Sela I 2007. Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 362:342–49
    [Google Scholar]
  72. 72. 
    Martinez J, Patkaniowska A, Urlaub H, Lührmann R, Tuschl T 2002. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 110:563–74
    [Google Scholar]
  73. 73. 
    Martins NE, Faria VG, Teixeira L, Magalhães S, Sucena É 2013. Host adaptation is contingent upon the infection route taken by pathogens. PLOS Pathog 9:e1003601
    [Google Scholar]
  74. 74. 
    Mehrabadi M, Hussain M, Matindoost L, Asgari S 2015. The baculovirus antiapoptotic p35 protein functions as an inhibitor of the host RNA interference antiviral response. J. Virol. 89:8182–92
    [Google Scholar]
  75. 75. 
    Mi S, Lee X, Li X, Veldman GM, Finnerty H et al. 2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–89
    [Google Scholar]
  76. 76. 
    Miesen P, Girardi E, van Rij RP 2015. Distinct sets of PIWI proteins produce arbovirus and transposon-derived piRNAs in Aedes aegypti mosquito cells. Nucl. Acids Res. 43:6545–56
    [Google Scholar]
  77. 77. 
    Miesen P, Joosten J, van Rij RP 2016. PIWIs go viral: arbovirus-derived piRNAs in vector mosquitoes. PLOS Pathog 12:e1006017
    [Google Scholar]
  78. 78. 
    Mohn F, Handler D, Brennecke J 2015. piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 348:812–17
    [Google Scholar]
  79. 79. 
    Mondotte JA, Gausson V, Frangeul L, Blanc H, Lambrechts L, Saleh MC 2018. Immune priming and clearance of orally acquired RNA viruses in Drosophila. Nat. Microbiol 3:1394–403
    [Google Scholar]
  80. 80. 
    Mondotte JA, Saleh M-C. 2018. Antiviral immune response and the route of infection in Drosophila melanogaster. Adv. Virus Res 100:247–78
    [Google Scholar]
  81. 81. 
    Monsanto-Hearne V, Johnson KN. 2018. miRNAs in insects infected by animal and plant viruses. Viruses 10:354
    [Google Scholar]
  82. 82. 
    Monsanto-Hearne V, Johnson KN. 2019. miRNA modulation of insect virus replication. Curr. Issues Mol. Biol. 34:61–82
    [Google Scholar]
  83. 83. 
    Monsanto-Hearne V, Tham ALY, Wong ZS, Asgari S, Johnson KN 2017. Drosophila miR-956 suppression modulates Ectoderm-expressed 4 and inhibits viral replication. Virology 502:20–27
    [Google Scholar]
  84. 84. 
    Monsion B, Incarbone M, Hleibieh K, Poignavent V, Ghannam A et al. 2018. Efficient detection of long dsRNA in vitro and in vivo using the dsRNA binding domain from FHV B2 protein. Front. Plant Sci. 9:70
    [Google Scholar]
  85. 85. 
    Mueller S, Gausson V, Vodovar N, Deddouche S, Troxler L et al. 2010. RNAi-mediated immunity provides strong protection against the negative-strand RNA vesicular stomatitis virus in Drosophila. PNAS 107:19390–95
    [Google Scholar]
  86. 86. 
    Mussabekova A, Daeffler L, Imler J-L 2017. Innate and intrinsic antiviral immunity in Drosophila. Cell. Mol. Life Sci 74:2039–54
    [Google Scholar]
  87. 87. 
    Nagata Y, Lee JM, Mon H, Imanishi S, Hong SM et al. 2013. RNAi suppression of beta-N-acetylglucosaminidase (BmFDL) for complex-type N-linked glycan synthesis in cultured silkworm cells. Biotechnol. Lett. 35:1009–16
    [Google Scholar]
  88. 88. 
    Nasar F, Palacios G, Gorchakov RV, Guzman H, Da Rosa AP et al. 2012. Eilat virus, a unique alphavirus with host range restricted to insects by RNA replication. PNAS 109:14622–27
    [Google Scholar]
  89. 89. 
    Nayak A, Berry B, Tassetto M, Kunitomi M, Acevedo A et al. 2010. Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nat. Struct. Mol. Biol 17:547–54
    [Google Scholar]
  90. 90. 
    Nayak A, Kim DY, Trnka MJ, Kerr CH, Lidsky PV et al. 2018. A viral protein restricts Drosophila RNAi immunity by regulating Argonaute activity and stability. Cell Host Microbe 24:542–57.e9
    [Google Scholar]
  91. 91. 
    Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK et al. 2012. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491:284–87
    [Google Scholar]
  92. 92. 
    Niu J, Smagghe G, De Coninck DIM, Van Nieuwerburgh F, Deforce D, Meeus I 2016. In vivo study of Dicer-2-mediated immune response of the small interfering RNA pathway upon systemic infections of virulent and avirulent viruses in Bombus terrestris. Insect Biochem. Mol. Biol 70:127–37
    [Google Scholar]
  93. 93. 
    Obbard DJ, Gordon KH, Buck AH, Jiggins FM 2009. The evolution of RNAi as a defence against viruses and transposable elements. Philos. Trans. R. Soc. Lond. B 364:99–115
    [Google Scholar]
  94. 94. 
    Orban TI, Izaurralde E. 2005. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11:459–69
    [Google Scholar]
  95. 95. 
    Palatini U, Miesen P, Carballar-Lejarazu R, Ometto L, Rizzo E et al. 2017. Comparative genomics shows that viral integrations are abundant and express piRNAs in the arboviral vectors Aedes aegypti and Aedes albopictus. BMC Genom 18:512
    [Google Scholar]
  96. 96. 
    Palmer WH, Varghese FS, Van Rij RP 2018. Natural variation in resistance to virus infection in dipteran insects. Viruses 10:118
    [Google Scholar]
  97. 97. 
    Parry R, Bishop C, De Hayr L, Asgari S 2019. Density-dependent enhanced replication of a densovirus in Wolbachia-infected Aedes cells is associated with production of piRNAs and higher virus-derived siRNAs. Virology 528:89–100
    [Google Scholar]
  98. 98. 
    Petit M, Mongelli V, Frangeul L, Blanc H, Jiggins F, Saleh M-C 2016. piRNA pathway is not required for antiviral defense in Drosophila melanogaster. PNAS 113:E4218–27
    [Google Scholar]
  99. 99. 
    Petrillo JE, Venter PA, Short JR, Gopal R, Deddouche S et al. 2013. Cytoplasmic granule formation and translational inhibition of nodaviral RNAs in the absence of the double-stranded RNA binding protein B2. J. Virol. 87:13409–21
    [Google Scholar]
  100. 100. 
    Poirier EZ, Goic B, Tomé-Poderti L, Frangeul L, Boussier J et al. 2018. Dicer-2-dependent generation of viral DNA from defective genomes of RNA viruses modulates antiviral immunity in insects. Cell Host Microbe 23:353–65
    [Google Scholar]
  101. 101. 
    Possee RD, Chambers AC, Graves LP, Aksular M, King LA 2019. Recent developments in the use of baculovirus expression vectors. Curr. Issues Mol. Biol. 34:215–30
    [Google Scholar]
  102. 102. 
    Qi N, Cai D, Qiu Y, Xie J, Wang Z et al. 2011. RNA binding by a novel helical fold of b2 protein from Wuhan nodavirus mediates the suppression of RNA interference and promotes b2 dimerization. J. Virol. 85:9543–54
    [Google Scholar]
  103. 103. 
    Qi N, Zhang L, Qiu Y, Wang Z, Si J et al. 2012. Targeting of dicer-2 and RNA by a viral RNA silencing suppressor in Drosophila cells. J. Virol. 86:5763–73
    [Google Scholar]
  104. 104. 
    Rand TA, Ginalski K, Grishin NV, Wang X 2004. Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. PNAS 101:14385–89
    [Google Scholar]
  105. 105. 
    Rand TA, Petersen S, Du F, Wang X 2005. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123:621–29
    [Google Scholar]
  106. 106. 
    Rosa C, Kuo YW, Wuriyanghan H, Falk BW 2018. RNA interference mechanisms and applications in plant pathology. Annu. Rev. Phytopathol. 56:581–610
    [Google Scholar]
  107. 107. 
    Ryabov EV, Childers AK, Lopez D, Grubbs K, Posada-Florez F et al. 2019. Dynamic evolution in the key honey bee pathogen deformed wing virus: novel insights into virulence and competition using reverse genetics. PLOS Biol 17:e3000502
    [Google Scholar]
  108. 108. 
    Sabin LR, Zheng Q, Thekkat P, Yang J, Hannon GJ et al. 2013. Dicer-2 processes diverse viral RNA species. PLOS ONE 8:e55458
    [Google Scholar]
  109. 109. 
    Santos D, Mingels L, Vogel E, Wang L, Christiaens O et al. 2019. Generation of virus- and dsRNA-derived siRNAs with species-dependent length in insects. Viruses 11:738
    [Google Scholar]
  110. 110. 
    Santos D, Wynant N, Van den Brande S, Verdonckt TW, Mingels L et al. 2018. Insights into RNAi-based antiviral immunity in Lepidoptera: acute and persistent infections in Bombyx mori and Trichoplusia ni cell lines. Sci. Rep. 8:2423
    [Google Scholar]
  111. 111. 
    Schnettler E, Donald CL, Human S, Watson M, Siu RWC et al. 2013. Knockdown of piRNA pathway proteins results in enhanced Semliki Forest virus production in mosquito cells. J. Gen. Virol. 94:1680–89
    [Google Scholar]
  112. 112. 
    Schnettler E, Sterken MG, Leung JY, Metz SW, Geertsema C et al. 2012. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 86:13486–500
    [Google Scholar]
  113. 113. 
    Schuster S, Miesen P, van Rij RP 2019. Antiviral RNAi in insects and mammals: parallels and differences. Viruses 11:448
    [Google Scholar]
  114. 114. 
    Schuster S, Zirkel F, Kurth A, van Cleef KW, Drosten C et al. 2014. A unique nodavirus with novel features: Mosinovirus expresses two subgenomic RNAs, a capsid gene of unknown origin, and a suppressor of the antiviral RNA interference pathway. J. Virol. 88:13447–59
    [Google Scholar]
  115. 115. 
    Singh CP, Singh J, Nagaraju J 2014. bmnpv-miR-3 facilitates BmNPV infection by modulating the expression of viral P6.9 and other late genes in Bombyx mori. Insect Biochem. Mol. Biol 49:59–69
    [Google Scholar]
  116. 116. 
    Singh J, Singh CP, Bhavani A, Nagaraju J 2010. Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virology 407:120–28
    [Google Scholar]
  117. 117. 
    Siomi H, Siomi MC. 2009. On the road to reading the RNA-interference code. Nature 457:396–404
    [Google Scholar]
  118. 118. 
    Siu RW, Fragkoudis R, Simmonds P, Donald CL, Chase-Topping ME et al. 2011. Antiviral RNA interference responses induced by Semliki Forest virus infection of mosquito cells: characterization, origin, and frequency-dependent functions of virus-derived small interfering RNAs. J. Virol. 85:2907–17
    [Google Scholar]
  119. 119. 
    Spellberg MJ, Marr MT. 2015. FOXO regulates RNA interference in Drosophila and protects from RNA virus infection. PNAS 112:14587–92
    [Google Scholar]
  120. 120. 
    Sullivan CS, Ganem D. 2005. A virus-encoded inhibitor that blocks RNA interference in mammalian cells. J. Virol. 79:7371–79
    [Google Scholar]
  121. 121. 
    Suzuki Y, Kobayashi Y, Horie M, Tomonaga K 2014. Origin of an endogenous bornavirus-like nucleoprotein element in thirteen-lined ground squirrels. Genes Genet. Syst. 89:143–48
    [Google Scholar]
  122. 122. 
    Taning CNT, Christiaens O, Li X, Swevers L, Casteels H et al. 2018. Engineered Flock house virus for targeted gene suppression through RNAi in fruit flies (Drosophila melanogaster) in vitro and in vivo. Front. Physiol 9:805
    [Google Scholar]
  123. 123. 
    Tassetto M, Kunitomi M, Andino R 2017. Circulating immune cells mediate a systemic RNAi-based adaptive antiviral response in Drosophila. Cell 169:314–25
    [Google Scholar]
  124. 124. 
    Tassetto M, Kunitomi M, Whitfield ZJ, Dolan PT, Sánchez-Vargas I et al. 2019. Control of RNA viruses in mosquito cells through the acquisition of vDNA and endogenous viral elements. eLife 8:e41244
    [Google Scholar]
  125. 125. 
    ter Horst AM, Nigg JC, Dekker FM, Falk BW 2019. Endogenous viral elements are widespread in arthropod genomes and commonly give rise to PIWI-interacting RNAs. J. Virol. 93:e02124–18
    [Google Scholar]
  126. 126. 
    van Cleef KW, van Mierlo JT, Miesen P, Overheul GJ, Fros JJ et al. 2014. Mosquito and Drosophila entomobirnaviruses suppress dsRNA- and siRNA-induced RNAi. Nucleic Acids Res 42:8732–44
    [Google Scholar]
  127. 127. 
    van Mierlo JT, Overheul GJ, Obadia B, van Cleef KW, Webster CL et al. 2014. Novel Drosophila viruses encode host-specific suppressors of RNAi. PLOS Pathog 10:e1004256
    [Google Scholar]
  128. 128. 
    van Rij RP, Saleh MC, Berry B, Foo C, Houk A et al. 2006. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 20:2985–95
    [Google Scholar]
  129. 129. 
    Varjak M, Dietrich I, Sreenu VB, Till BE, Merits A et al. 2018. Spindle-e acts antivirally against alphaviruses in mosquito cells. Viruses 10:88
    [Google Scholar]
  130. 130. 
    Varjak M, Maringer K, Watson M, Sreenu VB, Fredericks AC et al. 2017. Aedes aegypti Piwi4 is a noncanonical PIWI protein involved in antiviral responses. mSphere 2:e00144–17
    [Google Scholar]
  131. 131. 
    Wang Q, Zhou Y, Chen K, Ju X 2016. Suppression of Bm-caspase-1 expression in BmN cells enhances recombinant protein production in a baculovirus expression vector system. Mol. Biotechnol. 58:319–27
    [Google Scholar]
  132. 132. 
    Wang W, Han BW, Tipping C, Ge DT, Zhang Z et al. 2015. Slicing and binding by Ago3 or Aub trigger Piwi-bound piRNA production by distinct mechanisms. Mol. Cell 59:819–30
    [Google Scholar]
  133. 133. 
    Wang XH, Aliyari R, Li WX, Li HW, Kim K et al. 2006. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452–54
    [Google Scholar]
  134. 134. 
    Watanabe M, Iwakawa HO, Tadakuma H, Tomari Y 2017. Biochemical and single-molecule analyses of the RNA silencing suppressing activity of CrPV-1A. Nucleic Acids Res 45:10837–44
    [Google Scholar]
  135. 135. 
    Whitfield ZJ, Dolan PT, Kunitomi M, Tassetto M, Seetin MG et al. 2017. The diversity, structure, and function of heritable adaptive immunity sequences in the Aedes aegypti genome. Curr. Biol. 27:3511–19
    [Google Scholar]
  136. 136. 
    Wuriyanghan H, Falk BW. 2013. RNA interference towards the potato psyllid, Bactericera cockerelli, is induced in plants infected with recombinant Tobacco mosaic virus (TMV). PLOS ONE 8:e66050
    [Google Scholar]
  137. 137. 
    Ye C, An X, Jiang Y-D, Ding B-Y, Shang F et al. 2019. Induction of RNAi core machinery's gene expression by exogenous dsRNA and the effects of pre-exposure to dsRNA on the gene silencing efficiency in the pea aphid (Acyrthosiphon pisum). Front. Physiol. 9:1906
    [Google Scholar]
  138. 138. 
    Zambon RA, Vakharia VN, Wu LP 2006. RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell. Microbiol 8:880–89
    [Google Scholar]
  139. 139. 
    Zhu KY, Palli SR. 2020. Mechanisms, applications, and challenges of insect RNA interference. Annu. Rev. Entomol. 65:293–311
    [Google Scholar]
  140. 140. 
    Zhu M, Wang J, Deng R, Wang X 2016. Functional regulation of an Autographa californica nucleopolyhedrovirus-encoded microRNA, AcMNPV-miR-1, in baculovirus replication. J. Virol. 90:6526–37
    [Google Scholar]
  141. 141. 
    Zhu M, Wang J, Deng R, Xiong P, Liang H, Wang X 2013. A microRNA encoded by Autographa californica nucleopolyhedrovirus regulates expression of viral gene ODV-E25. J. Virol. 87:13029–34
    [Google Scholar]
/content/journals/10.1146/annurev-ento-033020-090410
Loading
/content/journals/10.1146/annurev-ento-033020-090410
Loading

Data & Media loading...

  • Article Type: Review Article
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