Modulation of the transcriptional response of innate immune and RNAi genes upon exposure to dsRNA and LPS in silkmoth-derived Bm5 cells overexpressing BmToll9-1 receptor

Journal of Insect Physiology

Volumn 66, Issue , 2014, Pages 10-19

  Liu, Jisheng ^a   Kolliopoulou, Anna ^b   Smagghe, Guy ^a   Swevers, Luc ^b  

^a GHENT UNIVERSITY   (Belgium)

^b INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

Author keywords

AMP; Bm5; Bombyx mori; DsRNA; RNAi; Toll9 1

Indexed keywords

CELL ORGANELLE; GENE EXPRESSION; IMMUNE RESPONSE; MOLECULAR ANALYSIS; MOTH; PATHOGEN; RNA;

DOUBLE STRANDED RNA; INSECT PROTEIN; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 9;

ANIMAL; ANTIBODY SPECIFICITY; BOMBYX; CELL LINE; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LARVA; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; BOMBYX; CELL LINE; CLONING, MOLECULAR; INSECT PROTEINS; LARVA; LIPOPOLYSACCHARIDES; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; TOLL-LIKE RECEPTOR 9;

EID: 84901478093     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2014.05.008     Document Type: Article

References (67)

1. Aggarwal K., Silverman N. Positive and negative regulation of the Drosophila immune response. BMB Rep. 2008, 41:267-277.
2. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
3. Bellés X. Beyond Drosophila RNAi: in vivo and functional genomics in insects. Annu. Rev. Entomol. 2010, 55:111-128.
4. Bettencourt R., Tanji T., Yagi Y., Ip Y.T. Toll and Toll-9 in Drosophila innate immune response. J. Endotoxin Res. 2004, 10:261-268.
5. Bilak H., Tauszig-Delamasure S., Imler J.L. Toll and Toll-like receptors in Drosophila. Biochem. Soc. Trans. 2003, 31:648-651.
6. Burand J.P., Hunter W.B. RNAi: future in insect management. J. Invertebr. Pathol. 2013, 112:S68-S74.
7. Carthew R.W., Sontheimer E.J. Origins and mechanisms of miRNAs and siRNAs. Cell 2009, 136:642-655.
8. Cherry S. Genomic RNAi screening in Drosophila S2 cells: what have we learned about host-pathogen interactions?. Curr. Opin. Microbiol. 2008, 11:262-270.
9. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., et al. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298:159-165.
10. Douris V., Swevers L., Labropoulou V., Andronopoulou E., Georgoussi Z., Iatrou K. Stably transformed insect cell lines: tools for expression of secreted and membrane-anchored proteins and high-throughput screening platforms for drug and insecticide discovery. Adv. Virus Res. 2006, 68:113-156.
11. Doyle S.E., O'Connell R., Vaidya S.A., Chow E.K., Yee K., Cheng G. Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J. Immunol. 2003, 170:3565-3571.
12. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., et al. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.
13. Ferrandon D., Imler J.L., Hoffmann J.A. Sensing infection in Drosophila: toll and beyond. Semin. Immunol. 2004, 16:43-53.
14. Ferrandon D., Imler J.L., Hetru C., Hoffmann J.A. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 2007, 7:862-874.
15. Garbutt J.S., Reynolds S.E. Induction of RNA interference genes by double-stranded RNA; implications for susceptibility to RNA interference. Insect Biochem. Mol. Biol. 2012, 42:621-628.
16. Gu L., Knipple D.C. Recent advances in RNAi research in insects: implications for future insect pest management strategies. Crop Prot. 2013, 45:36-40.
17. Hetru C., Hoffmann J.A. NF-kappaB in the immune response of Drosophila. Cold Spring Harb. Perspect. Biol. 2009, 1:a000232.
18. Huvenne H., Smagghe G. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 2010, 56:227-235.
19. Johnson R., Meidinger R.G., Iatrou K. A cellular promoter-based expression cassette for generating recombinant baculoviruses directing rapid expression of passenger genes in infected insects. Virology 1992, 190:815-823.
20. Kambris Z., Hoffmann J.A., Imler J.L., Capovilla M. Tissue and stage-specific expression of the Tolls in Drosophila embryos. Gene Expr. Patterns 2002, 2:311-317.
21. Kaneko T., Goldman W.E., Mellroth P., Steiner H., Fukase K., Kusumoto S., Harley W., Fox A., Golenbock D., Silverman N. Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 2004, 20:637-649.
22. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
23. Kobayashi I., Tsukioka H., Kmoto N., Uchino K., Sezutsu H., Tamura T., Kusakabe T., Tomita S. SID-1 protein of Caenorhabditis elegans mediates uptake of dsRNA into Bombyx cells. Insect Biochem. Mol. Biol. 2012, 42:148-154.
24. Kolliopoulou A., Swevers L. Functional analysis of the RNAi response in ovary-derived silkmoth Bm5 cells. Insect Biochem. Mol. Biol. 2013, 43:654-663.
25. Labropoulou V., Douris V., Stefanou D., Magrioti C., Swevers L., Iatrou K. Endoparasitoid wasp bracovirus-mediated inhibition of hemolin function and lepidopteran host immunosuppression. Cell. Microbiol. 2008, 10:2118-2128.
26. Lee Y.S., Pressman S., Andress A.P., Kim K., White J.L., Cassidy J.J., et al. Silencing by small RNAs is linked to endosomal trafficking. Nat. Cell Biol. 2009, 11:1150-1156.
27. Lemaitre B. The road to Toll. Nat. Rev. Immunol. 2004, 4:521-527.
28. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
29. Leulier F., Parquet C., Pili-Floury S., Ryu J.H., Caroff M., Lee W.J., Mengin-Lecreulx D., Lemaitre B. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat. Immunol. 2003, 4:478-484.
30. Liu S., Vijayendran D., Bonning B.C. Next generation sequencing technologies for insect virus discovery. Viruses 2011, 3:1849-1869.
31. Liu J., Swevers L., Iatrou K., Huvenne H., Smagghe G. Bombyx mori DNA/RNA non-specific nuclease: expression of isoforms in insect culture cells, subcellular localization and functional assays. J. Insect Physiol. 2012, 58:1166-1176.
32. Liu J., Smagghe G., Swevers L. Transcriptional response of BmToll9-1 and RNAi machinery genes to exogenous dsRNA in the midgut of Bombyx mori. J. Insect Physiol. 2013, 59:646-654.
33. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
34. Lozano J., Gomez-Orte E., Lee H.-J., Belles X. Super-induction of Dicer-2 expression by alien double-stranded RNAs: an evolutionary ancient response to viral infection?. Dev. Genes Evol. 2012, 222:229-235.
35. Lu M., Farrell P.J., Johnson R., Iatrou K. A baculovirus (Bombyx mori nuclear polyhedrosis virus) repeat element functions as a powerful constitutive enhancer in transfected insect cells. J. Biol. Chem. 1997, 272:30724-30728.
36. Luna C., Wang X., Huang Y., Zhang J., Zheng L. Characterization of four Toll related genes during development and immune responses in Anopheles gambiae. Insect Biochem. Mol. Biol. 2002, 32:1171-1179.
37. Magkrioti C., Iatrou K., Labropoulou V. Differential inhibition of BmRelish1-dependent transcription in lepidopteran cells by bracovirus ankyrin-repeat proteins. Insect Biochem. Mol. Biol. 2011, 41:993-1002.
38. Merkling S.H., van Rij R.P. Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. J. Insect Physiol. 2012, 59:159-170.
39. Michel T., Reichhart J.M., Hoffmann J.A., Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 2001, 414:756-759.
40. Nakamoto M., Moy R.H., Xu J., Bambina S., Yasunaga A., Shelly S.S., Gold B., Cherry S. Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity 2012, 36:658-667.
41. Narbonne-Reveau K., Charroux B., Royet J. Lack of an antibacterial response defect in Drosophila Toll-9 mutant. PLoS One 2011, 6:e17470.
42. Ooi J.Y., Yagi Y., Hu X., Ip Y.T. The Drosophila Toll-9 activates a constitutive antimicrobial defense. EMBO Rep. 2002, 3:82-87.
43. Ramirez J.L., 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.
44. Reichhart J.M., Georgel P., Meister M., Lemaitre B., Kappler C., Hoffmann J.A. Expression and nuclear translocation of the rel/NF-kappa B-related morphogen dorsal during the immune response of Drosophila. C R Acad. Sci. III 1993, 316:1218-1224.
45. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8:559-568.
46. Scott J.C., Brackney D.E., Campbell C.L., Bondu-Hawkins V., Hjelle B., et al. Comparison of dengue virus type 2-specific small RNAs from RNA interference competent and -incompetent mosquito cells. PLoS Negl. Trop. Dis. 2010, 4:e848.
47. Scott J.G., Michel K., Bartholomay L.C., Siegfried B.D., Hunter W.B., Smagghe G., Zhu K.Y., Douglas A.E. Towards the elements of successful insect RNAi. J. Insect Physiol. 2013, 59:121-1221.
48. Siomi H., Siomi M.C. On the road to reading the RNA-interference code. Nature 2009, 457:396-404.
49. Soin T., Swevers L., Kotzia G., Iatrou K., Janssen C.R., Rouge P., Harada T., Nakagawa Y., Smagghe G. Comparison of the activity of non-steroidal ecdysone agonists between dipteran and lepidopteran insects, using cell-based EcR reporter assays. Pest Manag. Sci. 2010, 66:1215-1229.
50. Swevers L., Smagghe G. Use of RNAi for control of insect crop pests. Progress in Biological Control 2012, 177-197. Springer-Verlag, Dordrecht. G. Smagghe, I. Diaz (Eds.).
51. Swevers L., Liu J., Huvenne H., Smagghe G. 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 2011, 6:e20250.
52. Swevers L., Vanden Broeck J., Smagghe G. The possible impact of persistent virus infection on the function of the RNAi machinery in insects: a hypothesis. Front. Physiol. 2013, 4:319.
53. Tanaka H., Ishibashi J., Fujita K., Nakajima Y., Sagisaka A., Tomimoto K., Suzuki N., Yoshiyama M., Kaneko Y., Iwasaki T., Sunagawa T., Yamaji K., Asaoka A., Mita K., Yamakawa M. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem. Mol. Biol. 2008, 38:1087-1110.
54. Tanaka H., Sagisaka A., Fujita K., Kaneko Y., Imanishi S., Yamakawa M. Lipopolysaccharide elicits expression of immune-related genes in the silkworm, Bombyx mori. Insect Mol. Biol. 2009, 18:71-75.
55. Tatematsu M., Seya T., Matsumoto M. Beyond dsRNA: Toll-like receptor 3 signalling in RNA-induced immune responses. Biochem. J. 2014, 458:195-201.
56. Tauszig S., Jouanguy E., Hoffmann J.A., Imler J.L. Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc. Natl. Acad. Sci. USA 2000, 97:10520-10525.
57. Tomoyasu Y., Miller S.C., Tomita S., Schoppmeier M., Grossmann D., Bucher G. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 2008, 9:R10.
58. van Rij R.P., Saleh M.C., Berry B., Foo C., Houk A., Antoniewski C., Andino R. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev. 2006, 20:2985-2995.
59. Wang G.H., Xia Q.Y., Cheng D.J., Duan J., Zhao P., Chen J., Zhu L. Reference genes identified in the silkworm Bombyx mori during metamorphism based on oligonucleotide microarray and confirmed by qRT-PCR. Insect Sci. 2008, 15:405-413.
60. Weber A.N., Tauszig-Delamasure S., Hoffmann J.A., Lelievre E., Gascan H., Ray K.P., Morse M.A., Imler J.L., Gay N.J. Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat. Immunol. 2003, 4:794-800.
61. Wu S., Zhang X., Chen X., Cao P., Beerntsen B.T., Ling E. BmToll9, an Arthropod conservative Toll, is likely involved in the local gut immune response in the silkworm, Bombyx mori. Dev. Comp. Immunol. 2010, 34:93-96.
62. Wu S., Zhang X., He Y., Shuai J., Chen X., Ling E. Expression of antimicrobial peptide genes in Bombyx mori gut modulated by oral bacterial infection and development. Dev. Comp. Immunol. 2010, 34:1191-1198.
63. Xi Z., Ramirez J.L., Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog. 2008, 4:e1000098.
64. Xu X.-X., Zhong X., Yi H.-Y., Yu X.-Q. Manduca sexta gloverin binds microbial components and is active against bacteria and fungi. Dev. Comp. Immunol. 2012, 38:275-284.
65. Yokoi K., Koyama H., Minakuchi C., Tanaka T., Miura K. Antimicrobial peptide gene induction, involvement of Toll and IMD pathways and defense against bacteria in the red flour beetle Tribolium castaneum. Results Immunol. 2012, 2:72-82.
66. Zambon R.A., Nandakumar M., Vakharia V.N., Wu L.P. The Toll pathway is important for an antiviral response in Drosophila. Proc. Natl. Acad. Sci. USA 2005, 102:7257-7262.
67. Zhu F., Xu J., Palli R., Ferguson J., Palli S.R. Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag. Sci. 2011, 67:175-182.