The possible impact of persistent virus infection on the function of the RNAi machinery in insects: A hypothesis

Frontiers in Physiology

Volumn 4 NOV, Issue , 2013, Pages

  Swevers, Luc ^a   Broeck, Jozef Vanden ^b   Smagghe, Guy ^c  

^a INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Innate immune response; Insects; Persistent virus infection; Pest control; RNA virus; RNAi

Indexed keywords

DOUBLE STRANDED RNA; SMALL INTERFERING RNA;

ARTICLE; DROSOPHILA; GENE EXPRESSION; GENE SILENCING; IMMUNITY; INNATE IMMUNITY; INSECT; MICROARRAY ANALYSIS; NONHUMAN; PEST CONTROL; RNA INTERFERENCE; RNA VIRUS; RNA VIRUS INFECTION; SUPPRESSION SUBTRACTIVE HYBRIDIZATION;

EID: 84889690076     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00319     Document Type: Article

References (188)

1. Aliyari, R., Wu, Q., Li, W.-H., Wang, X.-H., Li, F., Green, L. D., et al. (2008). Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 4, 387-397. doi: 10.1016/j.chom.2008.09.001
2. Arimatsu, Y., Kotani, E., Sugimura, Y., and Furusawa, T. (2007). Molecular characterization of a cDNA encoding extracellular dsRNase and its expression in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 37, 176-183. doi: 10.1016/j.ibmb.2006.11.004
3. Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Rufa, I. K., Pritchard, C. C., Gibson, D. F., et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U.S.A. 108, 5003-5008. doi: 10.1073/pnas.1019055108
4. Badisco, L., Marchal, E., Van Wielendaele, P., Verlinden, H., Vleugels, R., and Vanden Broeck, J. (2011). RNA interference of insulin-related peptide and neuroparsins affects vitellogenesis in the desert locust, Schistocerca gregaria. Peptides 32, 573-580. doi: 10.1016/j.peptides.2010.11.008
5. Bahia, A. C., Kubota, M. S., Tempone, A. J., Araújo, H. R., Guedes, B. A. M., Orfanó, A. S., et al. (2011). The JAK-STAT Pathway Controls Plasmodium vivax Load in Early Stages of Anopheles aquasalis Infection. PLoS Negl. Trop. Dis. 5:e1317. doi: 10.1371/journal.pntd.0001317
6. Baum, J. A., Bogaert, T., Clinton, W., Heck, G. R., Feldmann, P., Ilagan, O., et al. (2007). Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322-1326. doi: 10.1038/nbt1359
7. Baumann, P. (2005). Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155-189. doi: 10.1146/annurev.micro.59.030804.121041
8. Berry, B., Deddouche, S., Kirschner, D., Imler, J. L., and Antoniewski, C. (2009). Viral suppressors of RNA silencing hinder exogenous and endogenous small RNA pathways in Drosophila. PLoS ONE 4:e5866. doi: 10.1371/journal.pone.0005866
9. Biessmann, H., Andronopoulou, E., Biessmann, M. R., Douris, V., Dimitratos, S. D., Eliopoulos, E., et al. (2010). The Anopheles gambiae odorant binding protein 1 (AgamOBP1) mediates indole recognition in the antennae of female mosquitoes. PLoS ONE 5:e9471. doi: 10.1371/journal.pone.0009471
10. Boissona, B., Jacques, J.-C., Choumet, V., Martin, E., Xu, J., Vernick, K., et al. (2006). Gene silencing in mosquito salivary glands by RNAi. FEBS Lett. 580, 1988-1992. doi: 10.1016/j.febslet.2006.02.069
11. Bolognesi, R., Ramaseshadri, P., Anderson, J., Bachman, P., Clinton, W., Flannagan, R., et al. (2012). Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoS ONE 7:e47534. doi: 10.1371/journal.pone.0047534
12. Brackney, D. E., Scott, J. C., Sagawa, F., Woodward, J. E., Miller, N. A., Schilkey, F. D., et al. (2010). C6/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl. Trop. Dis. 4:e856. doi: 10.1371/journal.pntd.0000856
13. Braxton, S. M., Onstad, D. W., Dockter, D. E., Giordano, R., Larsson, R., and Humber, R. A. (2003). Description and analysis of two internet-based databases of insect pathogens: EDWIP and VIDIL. J. Invertebr. Pathol. 83, 185-195. doi: 10.1016/S0022-2011(03)00089-2
14. Bronkhorst, A. W., van Cleef, K. W. R., Vodovar, N., Ince, I. A., Blanc, H., Vlak, J. M., et al. (2012). The DNA virus Invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. Proc. Natl. Acad. Sci. U.S.A. 109, 3604-3613. doi: 10.1073/pnas.1207213109
15. Brown, J. K., and Czosnek, H. (2002). Whitefly transmission of plant viruses. Adv. Bot. Res. 36, 65-100. doi: 10.1016/S0065-2296(02)36059-2
16. Campbell, C. L., Keene, K. M., Brackney, D. E., Olson, K. E., Blair, C. D., Wilusz, J., et al. (2008). Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol. 8:47. doi: 10.1186/1471-2180-8-47
17. Carthew, R. W., and Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655. doi: 10.1016/j.cell.2009.01.035
18. Caudy, A. A., Ketting, R. F., Hammond, S. M., Denli, A. M., Bathoorn, A. M. P., Tops, B. B. J., et al. (2003). A micrococcal nuclease homologue in RNAi effector complexes. Nature 425, 411-414. doi: 10.1038/nature01956
19. Chougule, N. P., and Bonning, B. C. (2012). Toxins for transgenic resistance to Hemipteran pests. Toxins 4, 405-429. doi: 10.3390/toxins4060405
20. Christiaens, O. (2013). Key role and diversity of EcR/USP and other nuclear receptors in selected arthropoda species, Ph.D. thesis. Ghent University, Ghent.
21. Cirimotich, C. M., Scott, J. C., Phillips, A. T., Geiss, B. J., and Olson, K. E. (2009). Suppression of RNA interference increases alphavirus replication and virus-associated mortality in Aedes aegypti mosquitoes. BMC Microbiol. 9:49. doi: 10.1186/1471-2180-9-49
22. Ciudad, L., Bellés, X., and Piulachs, M. D. (2007). Structural and RNAi characterization of the German cockroach lipophorin receptor, and the evolutionary relationships of lipoprotein receptors. BMC Mol. Biol. 8:53. doi: 10.1186/1471-2199-8-53
23. Costa, A., Jan, E., Sarnow, P., and Schneider, D. (2009). The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 10:e7436. doi: 10.1371/journal.pone.0007436
24. Dai, H., Jiang, R., Wang, J., Xu, G., Cao, M., Wang, Z., et al. (2007). Development of a heat shock inducible and inheritable RNAi system in silkworm. Biomol. Eng. 24, 625-630. doi: 10.1016/j.bioeng.2007.10.004
25. Dalzell, J. J., McVeigh, P., Warnock, N. D., Mitreva, M., McK Bird, D., Abad, P., et al. (2011). RNAi effector diversity in nematodes. PLoS Negl. Trop. Dis. 5:e1176. doi: 10.1371/journal.pntd.0001176
26. Dasgupta, R., Cheng, L.-L., Bartholomay, L. C., and Christensen, B. M. (2003). Flock house virus replicates and expresses green fluorescent protein in mosquitoes. J. Gene. Virol. 84, 1789-1797. doi: 10.1099/vir.0.18938-0
27. Dasgupta, R., Free, H. M., Zietlow, S. L., Paskewitz, S. M., Aksoy, S., Shi, L., et al. (2007). Replication of flock house virus in three genera of medically important insects. J. Med. Entomol. 44, 102-110. doi: 10.1603/0022-2585(2007)44[102:ROFHVI]2.0.CO;2
28. Deddouche, S., Matt, N., Budd, A., Mueller, S., Kemp, C., Galiana-Arnoux, D., et al. (2008). The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat. Immunol. 9, 1425-1432. doi: 10.1038/ni.1664
29. Deng, H., Zhang, J., Li, Y., Zheng, S., Liu, L., Huang, L., et al. (2012). Homeodomain POU and Abd-A proteins regulate the transcription of pupal genes during metamorphosis of the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. U.S.A. 109, 12598-12603. doi: 10.1073/pnas.1203149109
30. Dillen, S., Zels, S., Verlinden, H., Spit, J., Van Wielendaele, P., and Vanden Broeck, J. (2013). Functional characterization of the short Neuropeptide F receptor in the desert locust, Schistocerca gregaria. PLoS ONE 8:e53604. doi: 10.1371/journal.pone.0053604
31. Ding, S. W., and Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell 130, 413-426. doi: 10.1016/j.cell.2007.07.039
32. Dostert, C., Jouanguy, E., Irving, P., Troxler, L., Galiana-Arnoux, D., Hetru, C., et al. (2005). The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 9, 946-953. doi: 10.1038/ni1237
33. Douglas, A. E. (2003). "Buchnera bacteria and other symbionts of aphids," in Insect Symbiosis. Contemporary Topics in Entomology Series Volume, eds K. Bourtzis and T. A. Miller (Boca Raton, FL: CRC Press), 23-38.
34. Dow, J. A. T. (1992). pH gradients in lepidopteran midgut. J. Exp. Biol. 172, 355-375.
35. Dzitoyeva, S., Dimitrijevic, N., and Manev, H. (2001). Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol. Psychiatry 6, 665-670. doi: 10.1038/sj.mp.4000955
36. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498. doi: 10.1038/35078107
37. Elias-Neto, M., Soares, M. P. M., Simões, Z. L. P., Hartfelder, K., and Bitondi, M. G. M. (2010). Developmental characterization, function and regulation of a Laccase2 encoding gene in the honey bee, Apis mellifera (Hymenoptera, Apinae). Insect Biochem. Mol. Biol. 40, 241-251. doi: 10.1016/j.ibmb.2010.02.004
38. Félix, M. A., Ashe, A., Piffaretti, J., Wu, G., Nuez, I., Bélicard, T., et al. (2011). Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol. 9:e1000586. doi: 10.1371/journal.pbio.1000586
39. Félix, M. A. (2008). RNA interference in nematodes and the chance that favored Sydney Brenner. J. Biol. 7:34. doi: 10.1186/jbiol97
40. Flynt, A., Liu, N., Martin, R., and Alai, E. C. (2009). Dicing of viral replication intermediates during silencing of latent Drosophila viruses. Proc. Natl. Acad. Sci. U.S.A. 106, 5270-5275. doi: 10.1073/pnas.0813412106
41. Gao, K., Deng, X., Qian, H., Wu, P., Qin, G., and Guo, X. (2012a). Cloning, characterization, and expression analysis of a novel BmGDAP1 gene from silkworm, Bombyx mori, involved in cytoplasmic polyhedrosis virus infection. Gene 497 208-213. doi: 10.1016/j.gene.2012.01.037
42. Gao, K., Deng, X.-Y., Qian, H.-Y., Wu, P., Qin, G.-X., Liu, T., et al. (2012b). cDNA cloning and characterization of LASP1 from silkworm, Bombyx mori, involved in cytoplasmic polyhedrosis virus infection. Gene 511, 389-397. doi: 10.1016/j.gene.2012.09.062
43. Gao, K., Deng, X.-Y., Qian, H.-Y., Wu, P., Qin, G.-X., Liu, T., et al. (2012c). Novel protein of IBP from silkworm, Bombyx mori, involved in cytoplasmic polyhedrosis virus infection. J. Invertebr. Pathol. 110, 83-91. doi: 10.1016/j.jip.2012.02.011
44. Garbutt, J. S., and Reynolds, S. E. (2012). Induction of RNA interference genes by double-stranded RNA; implications for susceptibility to RNA interference. Insect Biochem. Mol. Biol. 42, 621-628. doi: 10.1016/j.ibmb.2012.05.001
45. Garbutt, J. S., Bellés, X., Richards, E. H., and Reynolds, S. E. (2013). Persistence of double-stranded RNA in hemolymph as a potential determiner of RNA interference success: evidence from Manduca sexta and Blatella germanica. J. Insect Physiol. 59, 171-178. doi: 10.1016/j.jinsphys.2012.05.013
46. Gempe, T., Hasselmann, M., Schiøtt, M., Hause, G., Otte, M., and Beye, M. (2009). Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biol. 7:e1000222. doi: 10.1371/journal.pbio.1000222
47. Ghanim, M., Kontsedalov, S., and Czosneck, H. (2007). Tissue-specific gene silencing by RNA interference in the whitefly Bemisia tabaci (Gennadius). Insect Biochem. Mol. Biol. 37, 732-738. doi: 10.1016/j.ibmb.2007.04.006
48. Goic, B., and Saleh, M.-C. (2012). Living with the enemy: viral persistent infections from a friendly viewpoint. Curr. Opin. Microbiol. 15, 531-537. doi: 10.1016/j.mib.2012.06.002
49. Goic, B., Vodovar, N., Mondotte, J. A., Monot, C., Frangeul, L., Blanc, H., 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. doi: 10.1038/ni.2542
50. Gordon, K. H. J., and Waterhouse, P. M. (2007). RNAi for insect-proof plants. Nat. Biotechnol. 25, 1231-1232. doi: 10.1038/nbt1107-1231
51. Goto, A., Blandin, S., Royet, J., Reichhart, J. M., and Levashina, E. A. (2003). Silencing of Toll pathway components by direct injection of double-stranded RNA into Drosophila adult flies. Nucleic Acids Res. 31, 6619-6623. doi: 10.1093/nar/gkg852
52. Habayeb, M. S., Ekström, J.-A., and Hultmark, D. (2009). Nora virus persistent infections are not affected by the RNAi machinery. PLoS ONE 4:e5731. doi: 10.1371/journal.pone.0005731
53. Han, B. W., Hung, J.-H., Weng, Z., Zamore, P. D., and Ameres, S. L. (2011). The 3'-to-5' exoribonuclease Nibbler shapes the 3' ends of microRNAs bound to Drosophila Argonaute1. Curr. Biol. 21, 1878-1887. doi: 10.1016/j.cub.2011.09.034
54. Havelda, Z., Hornyik, C., Válóczi, A., and Burgyán, J. (2005). Defective interfering RNA hinders the activity of a tombusvirus-encoded posttranscriptional gene silencing suppressor. J. Virol. 79, 450-457. doi: 10.1128/JVI.79.1.450-457.2005
55. Hess, A. M., Prasad, A. N., Ptitsyn, A., Ebel, G. D., Olson, K. E., Barbacioru, C., Monighetti, C., and Campbell, C. L. (2011). Small RNA profiling of dengue virus mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol. 11:45. doi: 10.1186/1471-2180-11-45
56. Hirai, M., Terenius, O., Li, W., and Faye, I. (2004). Baculovirus and dsRNA induce Hemolin, but no antibacterial activity, in Antheraea pernyi. Insect Mol. Biol. 13, 399-405. doi: 10.1111/j.0962-1075.2004.00497.x
57. Hunter, C. P., Winston, W. M., Molodowitch, C., Feinberg, E. H., Shih, J., Sutherlin, M., et al. (2006). Systemic RNAi in Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 71, 95-100. doi: 10.1101/sqb.2006.71.060
58. Hunter, W., Ellis, J., van Engelsdorp, D., Hayes, J., Westervelt, D., Glick, E., et al. (2010). Large-scale field application of RNAi technology reducing israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae). PLoS Pathog. 6:e1001160. doi: 10.1371/journal.ppat.1001160
59. Hussain, M., Abraham, A. M., and Asgari, S. (2010). An ascovirus-encoded RNase III autoregulates its expression and suppresses RNA interference-mediated gene silencing. J. Virol. 84, 3624-3630. doi: 10.1128/JVI.02362-09
60. Huvenne, H., and Smagghe, G. (2010). Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 56, 227-235. doi: 10.1016/j.jinsphys.2009.10.004
61. Jaubert-Possamai, S., Le Trionnaire, G., Bonhomme, J., Christophides, G. K., Rispe, C., and Tagu, D. (2007). Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnol. 7:63. doi: 10.1186/1472-6750-7-63
62. Jayachandran, B., Hussain, M., and Asgari, S. (2012). RNA interference as a cellular defense mechanism against the DNA virus baculovirus. J. Virol. 86 13729-13734. doi: 10.1128/JVI.02041-12
63. Jinek, M., and Doudna, J. A. (2009). A three-dimensional view of the molecular machinery of RNA interference. Nature 457, 405-412. doi: 10.1038/nature07755
64. Kakumani, P. K., Ponia, S. S, Rajgokul, K.S, Sood, V., Chinnappan, M., Banerjea, A. C., et al. (2013). Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor. J Virol. 87, 8870-8883. doi: 10.1128/JVI.02774-12
65. Kanginakudru, S., Royer, C., Edupalli, S. V., Jalabert, A., Mauchamp, B., Chandrashekaraiah, et al. (2007). Targeting ie-1 gene by RNAi induces baculoviral resistance in lepidopteran cell lines and in transgenic silkworms. Insect Mol. Biol. 16, 635-644. doi: 10.1111/j.1365-2583.2007.00753.x
66. Keene, K. M., Foy, B. D., Sanchez-Vargas, I., Beaty, B. J., Blair, C. D., and Olson, K. E. (2004). RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 101, 17240-17245. doi: 10.1073/pnas.0406983101
67. Kennedy, S., Wang, D., and Ruvkun, G. (2004). A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427, 645-649. doi: 10.1038/nature02302
68. Khila, A., and Grbic, M. (2007). Gene silencing in the spider mite Tetranychus urticae: dsRNA and siRNA parental silencing of the Distal-less gene. Dev. Genes Evol. 217, 241-251. doi: 10.1007/s00427-007-0132-9
69. Kolliopoulou, A., and Swevers, L. (2013). Functional analysis of the RNAi response in ovary-derived silkmoth Bm5 cells. Insect Biochem. Mol. Biol. 43, 654-663. doi: 10.1016/j.ibmb.2013.05.001
70. Konopova, B., and Jindra, M. (2007). Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. U.S.A. 104, 10488-10493. doi: 10.1073/pnas.0703719104
71. Kupsco, J. M., Wu, M. J., Marzluff, W. F., Thapar, R., and Duronio, R. J. (2006). Genetic and biochemical characterization of Drosophila Snipper: a promiscuous member of the metazoan 3'hExo/ERI-1 family of 3' to 5' exonucleases. RNA 12, 2103-2117. doi: 10.1261/rna.186706
72. Lee, Y. S., Pressman, S., Andress, A. P., Kim, K., White, J. L., Cassidy, J. J., et al. (2009). Silencing by small RNAs is linked to endosomal trafficking. Nat. Cell Biol. 11, 1150-1156. doi: 10.1038/ncb1930
73. Li, H., Li, W. X., and Ding, S. W. (2002). Induction and suppression of RNA silencing by an animal virus. Science 296, 1319-1321. doi: 10.1126/science.1070948
74. Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., et al. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773. doi: 10.1038/nature03315
75. Lingel, A., Simon, B., Izaurralde, E., and Sattler, M. (2005). The structure of the Flock house virus B2 protein, a viral suppressor of RNAinterference, shows a novel mode of double-stranded RNA recognition. EMBO Rep. 6, 1149-1155. doi: 10.1038/sj.embor.7400583
76. Liu, J., Smagghe, G., and Swevers, L. (2013). Transcriptional response of BmToll9-1 and RNAi machinery genes to exogenous dsRNA in the midgut of Bombyx mori. J. Insect Physiol. 59, 646-654. doi: 10.1016/j.jinsphys.2013.03.013
77. Liu, J., Swevers, L., Iatrou, K., Huvenne, H., and Smagghe, G. (2012). Bombyx mori DNA/RNA non-specific nuclease isoforms: expression in insect culture cells, subcellular localization and functional assays. J. Insect Physiol. 58, 1166-1176. doi: 10.1016/j.jinsphys.2012.05.016
78. Liu, Q., Rand, T. A., Kalidas, S., Du, F., Kim, H. E., Smith, D. P., et al. (2003). R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301, 1921-1925. doi: 10.1126/science.1088710
79. Liu, S., Vijayendran, D., and Bonning, B. C. (2011). Next generation sequencing technologies for insect virus discovery. Viruses 3, 1849-1869. doi: 10.3390/v3101849
80. Liu, Y., Ye, X., Jiang, F., Liang, C., Chen, D., Peng, J., et al. (2009). C3PO, an endoribonuclease that promotes RNAi by facilitating RISC activation. Science 325, 750-753. doi: 10.1126/science.1176325
81. Lozano, J., Gomez-Orte, E., Lee, H.-J., and 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, 229-235. doi: 10.1007/s00427-012-0404-x
82. Lu, S., and Cullen, B. R. (2004). Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J. Virol. 78, 12868-12876. doi: 10.1128/JVI.78.23.12868-12876.2004
83. Lu, R., Maduro, M., Li, F., Li, H. W., Broitman-Maduro, G., Li, W. X., et al. (2005). Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436, 1040-1043. doi: 10.1038/nature03870
84. Mané-Padrós, D., Cruz, J., Vilaplana, L., Nieva, C., Ureña, E., Bellés, X., et al. (2010). The hormonal pathway controlling cell death during metamorphosis in a hemimetabolous insect. Dev. Biol. 346, 150-160. doi: 10.1016/j.ydbio.2010.07.012
85. Mao, Y. B., Cai, W. J., Wang, J. W., Hong, G. J., Tao, X. Y., Wang, L. J., et al. (2007). Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25, 1307-1313. doi: 10.1038/nbt1352
86. Marchal, E., Zhang, J., Badisco, L., Verlinden, H., Hult, E. F., Van Wielendaele, P., et al. (2011a). Final steps in juvenile hormone biosynthesis in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 41, 219-227. doi: 10.1016/j.ibmb.2010.12.007
87. Marchal, E., Badisco, L., Verlinden, H., Vandersmissen, H. P., Van Soest, S., Van Wielendaele, P., et al. (2011b). Role of the Halloween genes, Spook and Phantom in ecdysteroidogenesis in the desert locust, Schistocerca gregaria. J. Insect Physiol. 57, 1240-1248. doi: 10.1016/j.jinsphys.2011.05.009
88. Marchal, E., Verlinden, H., Badisco, L., Van Wielendaele, P., and Vanden Broeck, J. (2012). RNAi-mediated knockdown of Shade negatively affects ecdysone-20-hydroxylation in the desert locust, Schistocerca gregaria. J. Insect Physiol. 58, 890-896. doi: 10.1016/j.jinsphys.2012.03.013
89. Marcus, J. M. (2005). Jumping genes and AFLP maps: transforming lepidopteran color pattern genetics. Evol. Dev. 7 2, 108-114. doi: 10.1111/j.1525-142X.2005.05012.x
90. Merkling, S. H., and van Rij, R. P. (2013). Beyond RNAi: Antiviral defense strategies in Drosophila and mosquito. J. Insect Physiol. 59, 159-170. doi: 10.1016/j.jinsphys.2012.07.004
91. Miller, S. C., Brown, S. J., and Tomoyasu, Y. (2008). Larval RNAi in Drosophila. Dev. Genes Evol. 218, 505-510. doi: 10.1007/s00427-008-0238-8
92. Miska, E. A., and Ahringer, J. (2007). RNA interference has second helpings. Nat. Biotechnol. 25, 302-303. doi: 10.1038/nbt0307-302
93. Moar, W. J., Clark, T., Segers, G., Ramaseshadri, P., Hibbard, B., and Head, G. (2010). "dsRNA: the next generation of pyramided insect protection traits," in Abstract Book 58th Annual Meeting of the Entomological Society of America (San Diego, CA), 108.
94. Moazed, D. (2009). Small RNAs in transcriptional gene silencing and genome defense. Nature 457, 413-420. doi: 10.1038/nature07756
95. Morazzani, E. M., Wiley, M. R., Mureddu, M. G., Adelman, Z. N., and Myles, K. M. (2012). Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog. 8:e1002470. doi: 10.1371/journal.ppat.1002470
96. Moreira, L. A., Iturbe-Ormaetxe, I., Jeffery, J. A., Lu, G., Pyke, A. T., Hedges, L. M., et al. (2009). A Wolbachia symbiont in aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 139, 1268-1278. doi: 10.1016/j.cell.2009.11.042
97. Mori, H., and Metcalf, P. (2010). "Cypoviruses," in Insect Virology, eds A. Sassan and J. Karyn (Norfolk: Caister Academic Press), 307-323.
98. Mousson, L., Zouache, K., Arias-Goeta, C., Raquin, V., Mavingui, P., and Failloux, A.-B. (2012). The native Wolbachia symbionts limit transmission of Dengue virus in Aedes albopictus. PLoS Negl. Trop. Dis. 6:e1989. doi: 10.1371/journal.pntd.0001989
99. Mukha, D. V., Chumachenko, A. G., Dykstra, M. J., Kurtti, T. J., and Schal, C. (2006). Characterization of a new densovirus infecting the German cockroach, Blattella germanica. J. Gen. Virol. 87, 1567-1575. doi: 10.1099/vir.0.81638-0
100. Mutti, N. S., Louis, J., Pappan, L. K., Pappan, K., Begum, K., Chen, M.-S., et al. (2008). A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc. Natl. Acad. Sci. U.S.A. 105, 9965-9969. doi: 10.1073/pnas.0708958105
101. Myles, K. M., Wiley, M. R., Morazzani, E. M., and Adelman, Z. N. (2008). Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc. Natl. Acad. Sci. U.S.A. 105, 19938-19943. doi: 10.1073/pnas.0803408105
102. Narayanan, K. (2004). Insect defence: its impact on microbial control of insect pests. Curr. Sci. 86, 800-814.
103. Nayak, A., Berry, B., Tassetto, M., Kunitomi, M., Acevedo, A., Deng, C., et al. (2010). Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nat. Struct. Mol. Biol. 17, 547-554. doi: 10.1038/nsmb.1810
104. Ng, T. F. N., Willner, D. L., Lim, Y. W., Schmieder, R., Chau, B., Nilsson, C., et al. (2011). Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE 6:e20579. doi: 10.1371/journal.pone.0020579
105. Nuez, I., and Félix, M.-A. (2012). Evolution of susceptibility to ingested double-stranded RNAs in Caenorhabditis nematodes. PLoS ONE 7:e29811. doi: 10.1371/journal.pone.0029811
106. Obbard, D. J., Jiggins, F. M., Halligan, D. L., and Little, T. J. (2006). Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr. Biol. 16, 580-585. doi: 10.1016/j.cub.2006.01.065
107. Ohnishi, A., Hull, J. J., and Matsumoto, S. (2006). Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. Proc. Natl. Acad. Sci. U.S.A. 103, 4398-4403. doi: 10.1073/pnas.0511270103
108. Ortego, F. (2012). "Physiological adaptations of the insect gut to herbivory," in Arthropod-Plant Interactions, Novel Insights and Approaches for IPM, Progress in Biological Control, Vol. 14, eds G. Smagghe and I. Diaz (Dordrecht: Springer-Verlag), 75-88.
109. Ott, S. R., Verlinden, H., Rogers, S. M., Brighton, C. H., Quah, P. S., Vleugels, R., et al. (2012). Critical role for PKA in the acquisition of gregarious behaviour in the desert locust. Proc. Natl. Acad. Sci. U.S.A. 109, E381-E387. doi: 10.1073/pnas.1114990109
110. Pane, A., Wehr, K., and Schüpbach, T. (2007). Zucchini and Squash encode two putative nucleases required for rasiRNA production in the Drosophila Germline. Dev. Cell 12, 851-862. doi: 10.1016/j.devcel.2007.03.022
111. Pathak, K. B., and Nagy, P. D. (2009). Defective interfering RNAs: foes of viruses and friends of virologists. Viruses 1, 895-919. doi: 10.3390/v1030895
112. Payne, C. C., and Mertens, P. P. C. (1983). "Cytoplasmic polyhedrosis viruses," in The Reoviridae, eds W. K. Joklik, H. Fraenkel-Conrat, and R. R. Wagner (New York, YN: Plenum press), 425-504. doi: 10.1007/978-1-4899-0580-2_9
113. Pelletier, J., Aline Guidolin, A., Syed, Z., Cornel, A. J., and Leal, W. S. (2010). Knockdown of a mosquito odorant-binding protein involved in the sensitive detection of oviposition attractants. J. Chem. Ecol. 36, 245-248. doi: 10.1007/s10886-010-9762-x
114. Petruk, S., Sedkov, Y., Riley, K. M., Hodgson, J., Schweisguth, F., Hirose, S., et al. (2006). Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell 127, 1209-1221. doi: 10.1016/j.cell.2006.10.039
115. Pires da Silva, A., and Sommer, R. (2004). Conservation of the global sex determination gene tra-1 in distantly related nematodes. Genes Dev. 18, 1198-1208. doi: 10.1101/gad.293504
116. Pirofski, L.-A., and Casadevall, A. (2012). QandA: what is a pathogen. A question that begs the point. BMC Biol. 10:6. doi: 10.1186/1741-7007-10-6
117. Pitaluga, A. N., Mason, P. W., and Traub-Cseko, Y. M. (2008). Non-specific antiviral response detected in RNA-treated cultured cells of the sandfly, Lutzomyia longipalpis. Dev. Comp. Immunol. 32, 191-197. doi: 10.1016/j.dci.2007.06.008
118. Ponnuvel, K. M., Nakazawa, H., Furukawa, S., Asaoka, A., Ishibashi, J., Tanaka, H., et al. (2003). A lipase isolated from the silkworm Bombyx mori shows antiviral activity against nucleopolyhedrovirus. J. Virol. 77, 10725-10729. doi: 10.1128/JVI.77.19.10725-10729.2003
119. Price, D. R. G., and Gatehouse, J. A. (2008). RNAi-mediated crop protection against insects. Trends Biotechnol. 26, 393-400. doi: 10.1016/j.tibtech.2008.04.004
120. Quan, G. X., Kanda, T., and Tamura, T. (2002). Induction of the white egg 3 mutant phenotype by injection of the double-stranded RNA of the silkworm white gene. Insect Mol. Biol. 11, 217-222. doi: 10.1046/j.1365-2583.2002.00328.x
121. Ratcliff, F., Harrison, B. D., and Baulcombe, D. C. (1997). A similarity between viral defense and gene silencing in plants. Science 276, 1558-1560. doi: 10.1126/science.276.5318.1558
122. Robalino, J., Bartlett, T., Shepard, E., Prior, S., Jaramillo, G., Scura, E., et al. (2005). Double-stranded RNA induces sequence-specific antiviral silencing in addition to nonspecific immunity in a marine shrimp: convergence of RNA interference and innate immunity in the invertebrate antiviral response. J. Virol. 79, 1356-13561-13571. doi: 10.1128/JVI.79.21.13561-13571.2005
123. Robalino, J., Browdy, C. L., Prior, S., Metz, A., Parnell, P., Gross, P., et al. (2004). Induction of antiviral immunity by double-stranded RNA in a marine invertebrate. J. Virol. 78, 10442-10448. doi: 10.1128/JVI.78.19.10442-10448.2004
124. Rocha, J. J. E., Korolchuk, V. I., Robinson, I. M., and O'Kane, C. J. (2011). A phagocytic route for uptake of double-stranded RNA in RNAi. PLoS ONE 6:e19087. doi: 10.1371/journal.pone.0019087
125. Rocheleau, C. E. (2012). RNA interference: systemic RNAi SIDes with endosomes. Curr. Biol. 22, R873-R875. doi: 10.1016/j.cub.2012.08.039
126. Sadler, A. J., and Williams, B. R. (2008). Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8, 559-568. doi: 10.1038/nri2314
127. Saleh, M. C., Tassetto, M., van Rij, R. P., Goic, B., Gausson, V., Berry, B., et al. (2009). Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 458, 346-350. doi: 10.1038/nature07712
128. Saleh, M. C., van Rij, R. P., Hekele, A., Gillis, A., Foley, E., O'Farrell, P. H., et al. (2006). The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol. 8, 793-802. doi: 10.1038/ncb1439
129. Sanchez-Vargas, I., Scott, J. C., Poole-Smith, B. K., Franz, A. W., Barbosa-Solomieu, V., Wilusz, J., et al. (2009). Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito's RNA interference pathway. PLoS Pathog. 5:e1000299. doi: 10.1371/journal.ppat.1000299
130. Schneider, M. D., Najand, N., Chaker, S., Pare, J. M., Haskins, J., Hughes, S. C., et al. (2006). Gawky is a component of cytoplasmic mRNA processing bodies for early Drosophila development. J. Cell Biol. 174, 349-358. doi: 10.1083/jcb.200512103
131. Schnettler, E., Sterken, M. G., Leung, J. Y., Metz, S. W., Geertsema, C., Goldbach, R. W., et al. (2012). Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 86, 13486-13500. doi: 10.1128/JVI.01104-12
132. Schott, D. H., Cureton, D. K., Whelan, S. P., and Hunter, C. P. (2005). An antiviral role for the RNA interference machinery in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 102, 18420-18424. doi: 10.1073/pnas.0507123102
133. Scott, J. C., Brackney, D. E., Campbell, C. L., Bondu-Hawkins, V., Hjelle, B., Ebel, G. D., et al. (2010). Comparison of dengue virus type 2-specific small RNAs from RNA interference competent and -incompetent mosquito cells. PLoS Negl. Trop. Dis. 4:e848. doi: 10.1371/journal.pntd.0000848
134. Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63. doi: 10.1038/nature07228
135. Shabalina, S. A., and Koonin, E. V. (2008). Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23, 578-587. doi: 10.1016/j.tree.2008.06.005
136. Shakesby, A. J., Wallace, I. S., Isaacs, H. V., Pritchard, J., Roberts, D. M., and Douglas, A. E. (2009). A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem. Mol. Biol. 39, 1-10. doi: 10.1016/j.ibmb.2008.08.008
137. Shannon, A., Tyson, T., Dix, I., Boyd, J., and Burnell, A. (2008). Systemic RNAi mediated gene silencing in the anhydrobiotic nematode Panagrolaimus superbus. BMC Mol. Biol. 9:58. doi: 10.1186/1471-2199-9-58
138. Singh, C. P., Singh, J., and Nagaraju, J. (2012). A baculovirus-encoded microRNA (miRNA) suppresses its host miRNA biogenesis by regulating the exportin-5 cofactor Ran. J. Virol. 86, 7867-7879. doi: 10.1128/JVI.00064-12
139. Singh, G., Popli, S., Hari, Y., Malhotra, P., Mukherjee, S., and Bhatnagar, R. K. (2009). Suppression of RNA silencing by Flock house virus B2 protein is mediated through its interaction with the PAZ domain of Dicer. FASEB J. 23, 1845-1857. doi: 10.1096/fj.08-125120
140. Singh, J., Singh, C. P., Bhavani, A., and Nagaraju, J. (2010). Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virology 407, 120-128. doi: 10.1016/j.virol.2010.07.033
141. Siomi, H., and Siomi, M. C. (2009a). On the road to reading the RNA-interference code. Nature 457, 396-404. doi: 10.1038/nature07754
142. Siomi, H., and Siomi, M. C. (2009b). RISC hitches onto endosome trafficking. Nat. Cell Biol. 11, 1049-1051. doi: 10.1038/ncb0909-1049
143. Siu, R. W. C., Fragkoudis, R., Simmonds, P., Donald, C. L., Chase-Topping, M. E., Barry, G., 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, 2907-2917. doi: 10.1128/JVI.02052-10
144. Sorrell, I., White, A., Pedersen, A. B., Hails, R. S., and Boots, M. (2009). The evolution of covert, silent infection as a parasite strategy. Proc. R. Soc. Biol. 276, 2217-2226. doi: 10.1098/rspb.2008.1915
145. Souza-Neto, J. A., Sim, S., and Dimopoulos, G. (2009). An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc. Natl. Acad. Sci. U.S.A. 42, 17841-17846. doi: 10.1073/pnas.0905006106
146. Sylvester, E. S. (1989). "Viruses transmitted by Aphids," in Aphids. Their Biology, Natural Enemies and Control; Vol. C, eds A. K. Minks and P. Harrewij (Amsterdam: Elsevier), 65-88.
147. Swevers, L., Liu, J., Huvenne, H., and Smagghe, G. (2011). Search for limiting factors in the RNAi pathway in silkmoth tissues and the Bm5 cell line: the RNA-binding proteins R2D2 and Translin. PLoS ONE 6:e20250. doi: 10.1371/journal.pone.0020250
148. Swevers, L., and Smagghe, G. (2012). "Use of RNAi for control of insect crop pests," in Arthropod-Plant Interactions, Novel Insights and Approaches for IPM, Progress in Biological Control, Vol. 14, eds G. Smagghe and I. Diaz (Dordrecht: Springer-Verlag), 177-197.
149. Tamura, T., Thibert, C., Royer, C., Kanda, T., Abraham, E., Kamba, M., et al. (2000). Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat. Biotechnol. 18, 81-84. doi: 10.1038/71978
150. Tan, A., and Palli, S. R. (2008). Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 38, 430-439. doi: 10.1016/j.ibmb.2007.09.012
151. Tang, S., Patel, A., and Krause, P. R. (2009). Novel less-abundant viral microRNAs encoded by herpes simplex virus 2 latency associated transcript and their roles in regulating ICP34.5 and ICP0 mRNAs. J. Virol. 83, 1433-1442. doi: 10.1128/JVI.01723-08
152. Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., et al. (2011). RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 57, 231-245. doi: 10.1016/j.jinsphys.2010.11.006
153. Tian, L., Guo, E., Dia, Y., Zhou, S., Peng, Q., Cao, Y., et al. (2010). Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body. BMC Genomics 11:549. doi: 10.1186/1471-2164-11-549
154. Tijsterman, M., Okihara, K. L., Thijssen, K., and Plasterk, R. H. (2002). PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans. Curr. Biol. 12, 1535-1540. doi: 10.1016/S0960-9822(02)01110-7
155. Tomari, Y., Du, T., and Zamore, P. D. (2007). Sorting of Drosophila small silencing RNAs. Cell 130, 299-308. doi: 10.1016/j.cell.2007.05.057
156. Tomita, M., Munetsuna, H., Sato, T., Adachi, T., Hino, R., Hayashi, M., et al. (2003). Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nat. Biotechnol. 21, 52-56. doi: 10.1038/nbt771
157. Tomoyasu, Y., Miller, S. C., Tomita, S., Schoppmeier, M., Grossmann, D., and Bucher, G. (2008). Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 9:R10. doi: 10.1186/gb-2008-9-1-r10
158. Uhlirova, M., Foy, B. D., Beaty, B. J., Olson, K. E., Riddiford, L. M., and Jindra, M. (2003). Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proc. Natl. Acad. Sci. U.S.A. 100, 15607-15612. doi: 10.1073/pnas.2136837100
159. Ulvila, J., Parikka, M., Kleino, A., Sormunen, R., Ezekowitz, R. A., Kocks, C., et al. (2006). Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J. Biol. Chem. 281, 14370-14375. doi: 10.1074/jbc.M513868200
160. Umbach, J. L., and Cullen, B. R. (2009). The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 23, 1151-1164. doi: 10.1101/gad.1793309
161. Umbach, J. L., Kramer, M. F., Jurak, I., Karnowski, H. W., Coen, D. M., and Cullen, B. R. (2008). MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454, 780-783. doi: 10.1038/nature07103
162. Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P. D. (2006). A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320-324. doi: 10.1126/science.1129333
163. van Hoef, V., Breugelmans, B., Spit, J., Simonet, G., Zels, S., Billen, J., et al. (2011). Functional analysis of a pancreatic secretory trypsin inhibitor-like protein in insects: silencing effects resemble the human pancreatic autodigestion phenotype. Insect Biochem. Mol. Biol. 41, 688-695. doi: 10.1016/j.ibmb.2011.04.012
164. van Mierlo, J. T., Bronkhorst, A. W., Overheul, G. J., Sadanandan, S. A., Ekström, J.-A., Heestermans, M., et al. (2012). Convergent evolution of Argonaute-2 Slicer antagonism in two distinct insect RNA viruses. PLoS Pathog. 8:e1002872. doi: 10.1371/journal.ppat.1002872
165. van Rij, R. P., Saleh, M. C., Berry, B., Foo, C., Houk, A., Antoniewski, C., et al. (2006). The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev. 20, 2985-2995. doi: 10.1101/gad.1482006
166. Van Wielendaele, P., Dillen, S., Marchal, E., Badisco, L., and Vanden Broeck, J. (2012). CRF-like diuretic hormone negatively affects both feeding and reproduction in the desert locust, Schistocerca gregaria. PLoS ONE 7:e31425. doi: 10.1371/journal.pone.0031425
167. Van Wielendaele, P., Dillen, S., Zels, S., Badisco, L., and Vanden Broeck, J. (2013a). Regulation of feeding by Neuropeptide F in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 43, 102-114. doi: 10.1016/j.ibmb.2012.10.002
168. Van Wielendaele, P., Wynant, N., Dillen, S., Zels, S., Badisco, L., and Vanden Broeck, J. (2013b). Neuropeptide F regulates male reproductive processes in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 43, 252-259. doi: 10.1016/j.ibmb.2012.12.004
169. Van Wielendaele, P., Wynant, N., Dillen, S., Badisco, L., Marchal, E., and Vanden Broeck, J. (2013c). In vivo effect of Neuropeptide F on ecdysteroidogenesis in adult female desert locusts (Schistocerca gregaria). J. Insect Physiol. 59, 624-630. doi: 10.1016/j.jinsphys.2013.03.005
170. Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., and Remaley, A. T. (2011). MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 13, 423-433. doi: 10.1038/ncb2210
171. Vodovar, N., Bronkhorst, A. W., van Cleef, K. W. R., Miesen, P., Blanc, H., van Rij, R. P., et al. (2012). Arbovirus-derived piRNAs Exhibit a ping-pong signature in mosquito cells. PLoS ONE 7:e30861. doi: 10.1371/journal.pone.0030861
172. Vodovar, N., and Saleh, M.-C. (2012). Of insects and viruses: the role of small RNAs in insect defence. Adv. Insect Physiol. 42, 1-36. doi: 10.1016/B978-0-12-387680-5.00001-X
173. Wang, K., Zhang, S., Weber, J., Baxter, D., and Galas, D. J. (2010). Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 38, 7248-7259. doi: 10.1093/nar/gkq601
174. Wang, X. H., Aliyari, R., Li, W. X., Li, H. W., Kim, K., Carthew, R., et al. (2006). RNA interference directs innate immunity against viruses in adult Drosophila. Science 312, 452-454. doi: 10.1126/science.1125694
175. Whangbo, J. S., and Hunter, C. P. (2008). Environmental RNA interference. Trends Genet. 24, 297-305. doi: 10.1016/j.tig.2008.03.007
176. Wilkins, C., Dishongh, R., Moore, S. C., Whitt, M. A., Chow, M., and Machaca, K. (2005). RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature 436, 1044-1047. doi: 10.1038/nature03957
177. Wu, P., Han, S., Chen, T., Qin, G., Li, L., and Guo, X.-J. (2013). Involvement of MicroRNAs in Infection of Silkworm with Bombyx mori Cytoplasmic Polyhedrosis Virus (BmCPV). PLoS ONE 8:e68209. doi: 10.1371/journal.pone.0068209
178. Wu, P., Li, M. W., Wang, X., Zhao, P., Wang, X. Y., Liu, T., et al. (2009). Differentially expressed genes in the midgut of Silkworm infected with cytoplasmic polyhedrosis virus. Afr. J. Biotechnol. 8, 3711-3720. doi: 10.1371/journal.pone.0019087
179. Wu, Q., Luo, Y., Lu, R., Lau, N., Lai, E. C., Li, W.-X., et al. (2010). Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc. Natl. Acad. Sci. U.S.A. 107, 1606-1611. doi: 10.1073/pnas.0911353107
180. Wu, P., Wang, X., Qin, G.-x., Liu, T., Jiang, Y.-F., Li, M.-W., et al. (2011). Microarray analysis of the gene expression profile in the midgut of silkworm infected with cytoplasmic polyhedrosis virus. Mol. Biol. Rep. 38, 333-341. doi: 10.1007/s11033-010-0112-4
181. Wynant, N., Verlinden, H., Breugelmans, B., Simonet, G., and Vanden Broeck, J. (2012). Tissue-dependence and sensitivity of the systemic RNA interference response in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 42, 911-917. doi: 10.1016/j.ibmb.2012.09.004
182. Xi, Z., Ramirez, J. L., and Dimopoulos, G. (2008). The Aedes aegypti Toll pathway controls Dengue virus infection. PLoS Pathog. 4:e1000098. doi: 10.1371/journal.ppat.1000098
183. Yamaguchi, J., Mizoguchi, T., and Fujiwara, H. (2011). siRNAs induce efficient RNAi response in Bombyx mori embryos. PLoS ONE 6:e25469. doi: 10.1371/journal.pone.0025469
184. Yan, Z., Hu, H. Y., Jiang, X., Maierhofer, V., Neb, E., He, L., et al. (2011). Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res. 39, 6596-6607. doi: 10.1093/nar/gkr298
185. You, H., Wan, H., Li, J., and Jin, B. R. (2010). Molecular cloning and characterization of a short peptidoglycan recognition protein (PGRP-S) with antibacterial activity from the bumblebee Bombus ignitus. Dev. Comp. Immunol. 34, 977-985. doi: 10.1016/j.dci.2010.04.007
186. Zambon, R. A., Vakharia, V. N., and Wu, L. P. (2006). RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell. Microbiol. 8, 880-889. doi: 10.1111/j.1462-5822.2006.00688.x
187. Zhu, F., Xu, J., Palli, R., Ferguson, J., and Palli, S. R. (2011). Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag. Sci. 67, 175-182. doi: 10.1002/ps.2048
188. Zhuang, J. J., and Hunter, C. P. (2012). RNA interference in Caenorhabditis elegans: uptake, mechanism and regulation. Parasitology 139, 560-573. doi: 10.1017/S0031182011001788