Inhibiting avian influenza virus shedding using a novel RNAi antiviral vector technology: proof of concept in an avian cell model

AMB Express

Volumn 6, Issue 1, 2016, Pages 1-10

  Linke, Lyndsey M ^a   Wilusz, Jeffrey ^a   Pabilonia, Kristy L ^a   Fruehauf, Johannes ^b   Magnuson, Roberta ^a   Olea Popelka, Francisco ^a   Triantis, Joni ^a   Landolt, Gabriele ^a   Salman, Mo ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b Cambridge Biolabs   (United States)

Author keywords

Avian influenza; Bacterial vector; Influenza antiviral; siRNA delivery; Transkingdom RNAi

Indexed keywords

BETA1 INTEGRIN; NUCLEOPROTEIN; PEPTIDES AND PROTEINS; POLYMERASE ACIDIC PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AVIAN INFLUENZA VIRUS; BIRD; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; FLOW CYTOMETRY; GENE EXPRESSION; HEPATOCELLULAR CARCINOMA CELL LINE; ID50 (INFECTIOUS); MDCK CELL LINE; NONHUMAN; POLYMERASE CHAIN REACTION; RNA VECTOR; RNAI THERAPEUTICS; VIRUS SHEDDING;

EID: 84975755295     PISSN: None     EISSN: 21910855     Source Type: Journal    
DOI: 10.1186/s13568-016-0187-y     Document Type: Article

References (54)

1. Abrahamyan A, Nagy E, Golovan SP. Human H1 promoter expressed short hairpin RNAs (shRNAs) suppress avian influenza virus replication in chicken CH-SAH and canine MDCK cells. Antiviral Res. 2009;84(2):159–67. doi:10.1016/j.antiviral.2009.08.009.
2. Aigner A. Transkingdom RNA interference (tkRNAi) as a new delivery tool for therapeutic RNA. Expert Opin Biol Ther. 2009;9(12):1533–42. doi:10.1517/14712590903307354.
3. Arzt J, White WR, Thomsen BV, Brown CC. Agricultural diseases on the move early in the third millennium. Vet Pathol. 2010;47(1):15–27. doi:10.1177/0300985809354350.
4. Barik S, Lu P. Therapy of respiratory viral infections with intranasal siRNAs. Methods Mol Biol. 2015;1218:251–62. doi:10.1007/978-1-4939-1538-5_14.
5. Beer S, Bellovin DI, Lee JS, Komatsubara K, Wang LS, Koh H, Börner K, Storm TA, Davis CR, Kay MA, Felsher DW, Grimm D. Low-level shRNA cytotoxicity can contribute to MYC-induced hepatocellular carcinoma in adult mice. Mol Ther. 2010;18(1):161–70. doi:10.1038/mt.2009.222.
6. Bennink JR, Palmore TN. The promise of siRNAs for the treatment of influenza. Trends Mol Med. 2004;10(12):571–4.
7. Bessler WG, Kleine B, Martinez Alonso C, Biesert L, Strecker M, Wiesmüller KH, Metzger J, Jung G. Biological activity of bacterial surface components: bacterial extracts and defined bacterial cell wall components as immunomodulators. Lung. 1990;168(Suppl):707–15.
8. Bevis BJ, Glick BS. Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat Biotechnol. 2002;20(1):83–7.
9. Buttaro C, Fruehauf JH. Engineered E. coli as vehicles for targeted therapeutics. Curr Gene Ther. 2010;10:27–33.
10. Caprile T, Osorio G, Henríquez JP, Montecinos H. Polarized expression of integrin beta1 in diencephalic roof plate during chick development, a possible receptor for SCO-spondin. Dev Dyn. 2009;238(10):2494–504. doi:10.1002/dvdy.22070.
11. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs 673. Cell. 2009;136(4):642–55. doi:10.1016/j.cell.2009.01.035.
12. Chen M, Payne W, Dunn J, Chang S, Zhang H, Hunt H, Dodgson J. Retroviral delivery of RNA interference against marek’s disease virus in vivo. Poult Sci. 2009;88(7):1373–80. doi:10.3382/ps.2009-00070.
13. Conte MP, Longhi C, Buonfiglio V, Polidoro M, Seganti L, Valenti P. The effect of iron on the invasiveness of Escherichia coli carrying the inv gene of Yersinia pseudotuberculosis. J Med Microbiol. 1994;40(4):236–40.
14. Davidson BL, McCray PB Jr. Current prospects for RNA interference-based therapies. Nat Rev Genet. 2011;12(5):329–40. doi:10.1038/nrg2968.
15. De Vincenzo JP. The promise, pitfalls and progress of RNA-interference-based antiviral therapy for respiratory viruses. Antivir Ther. 2012;17(1 Pt B):213–25. doi:10.3851/IMP2064.
16. Escorcia M, Vazquez L, Mendez ST, Rodriguez-Ropon A, Lucio E, Nava GM. Avian influenza: genetic evolution under vaccination pressure. Virol J. 2008;5:15. doi:10.1186/1743-422X-5-15.
17. Ge Q, Eisen HE, Chen J. Use of siRNAs to prevent and treat influenza virus infection. Virus Res. 2004;102(1):37–42.
18. Ge Q, McManus MT, Nguyen T, Shen CH, Sharp PA, Eisen HN, Chen J. RNA interference of influenza virus production by directly targeting mRNA for degradation and indirectly inhibiting all viral RNA transcription. Proc Natl Acad Sci USA. 2003;100(5):2718–23.
19. Grillot-Courvalin C, Goussard S, Huetz F, Ojicius DM, Courvalin P. Functional gene transfer from intracellular bacteria to mammalian cells. Nat Biotechnol. 1998;16(9):862–6.
20. Grimm D, Streetz KL, Jopling CL, Storm TA, Pandey K, Davis CR, Marion P, Salazar F, Kay MA. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature. 2006;441(7092):537–41.
21. Hacein-Bey-Abina S, Garrigue A, Wang GP, Soulier J, Lim A, Morillon E, Clappier E, Caccavelli L, Delabesse E, Beldjord K, Asnafi V, MacIntyre E, Dal Cortivo L, Radford I, Brousse N, Sigaux F, Moshous D, Hauer J, Borkhardt A, Belohradsky BH, Wintergerst U, Velez MC, Leiva L, Sorensen R, Wulffraat N, Blanche S, Bushman FD, Fischer A, Cavazzana-Calvo M. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest. 2008;118(9):3132–42. doi:10.1172/JCI35700.
22. Halvorson DA. Control of low pathogenicity avian influenza. In: Swayne DE, editor. avian influenza. Ames: Blackwell Publishing; 2008. p. 513–30.
23. Isberg RR, Barnes P. Subversion of integrins by enteropathogenic Yersinia. J Cell Sci. 2001;114(Pt 1):21–8.
24. Isberg RR, Leong JM. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990;60:861–71.
25. Jiao H, Du L, Hao Y, Cheng Y, Luo J, Kuang W, Zhang D, Lei M, Jia X, Zhang X, Qi C, He H, Wang F. Effective inhibition of mRNA accumulation and protein expression of H5N1 avian influenza virus NS1 gene in vitro by small interfering RNAs. Folia Microbiol (Praha). 2013;58(4):335–42. doi:10.1007/s12223-012-0212-8.
26. Khantasup K, Kopermsub P, Chaichoun K, Dharakul T. Targeted small interfering RNA-immunoliposomes as a promising therapeutic agent against highly pathogenic Avian Influenza A (H5N1) virus infection. Antimicrob Agents Chemother. 2014;58(5):2816–24. doi:10.1128/AAC.02768-13.
27. Kim JH, Skountzou I, Compans R, Jacob J. Original antigenic sin responses to influenza viruses. J Immunol. 2009;183(5):3294–301. doi:10.4049/jimmunol.0900398.
28. Kruhn A, Wang A, Fruehauf JH, Lage H. Delivery of short hairpin RNAs by transkingdom RNA interference modulates the classical ABCB1-mediated multidrug-resistant phenotype of cancer cells. Cell Cycle. 2009;8(20):3349–54.
29. Li CX, Parker A, Menocal E, Xiang S, Borodyansky L, Fruehauf JH. Delivery of RNA interference. Cell Cycle. 2006;5(18):2103–9.
30. Li YC, Kong LH, Cheng BZ, Li KS. Construction of influenza virus siRNA Expression vectors and their inhibitory effects on multiplication of influenza virus. Avian Dis. 2005;49(4):562–73.
31. Li L, Shen Y. Overcoming obstacles to develop effective and safe siRNA therapeutics. Expert Opin Biol Ther. 2009;9(5):609–19. doi:10.1517/14712590902911420.
32. Long CR, Tessanne KJ, Golding MC. Applications of RNA interference-based gene silencing in animal agriculture. Reprod Fertil Dev. 2010;22(1):47–58. doi:10.1071/RD09211.
33. Lyall J, Irvine RM, Sherman A, McKinley TJ, Núñez A, Purdie A, Outtrim L, Brown IH, Rolleston-Smith G, Sang H, Tiley L. Suppression of avian influenza transmission in genetically modified chickens. Science. 2011;331(6014):223–6. doi:10.1126/science.1198020.
34. Ma JB, Yuan YR, Meister G, Pei Y, Tuschl T, Patel DJ. Structural basis for 680 5′-end-specific recognition of guide RNA by the A. fulgidus piwi protein. Nature. 2005;434(7033):666–70.
35. Martinez J, Patkaniowska A, Urlaub H, Luhrmann R, Tuschl T. Single-684 stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell. 2002;110(5):563–74.
36. Mathew E, Hardee GE, Bennett CF, Lee KD. Cytosolic delivery of antisense oligonucleotides by listeriolysin O-containing liposomes. Gene Ther. 2003;10(13):1105–15.
37. Nguyen TA, Fruehauf JH. Transkingdom RNA interference (tkRNAi): a novel method to induce therapeutic gene silencing. Methods Mol Biol. 2009;514:27–34. doi:10.1007/978-1-60327-527-9_3.
38. Radford KJ, Higgins DE, Pasquini S, Cheadle EJ, Carta L, Jackson AM, Lemoine NR, Vassaux G. A recombinant E. coli vaccine to promote MHC class I-dependent antigen presentation: application to cancer immunotherapy. Gene Ther. 2002;9(21):1455–63.
39. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg. 1938;27:493–7.
40. Rudolf M, Pöppel M, Fröhlich A, Breithaupt A, Teifke J, Blohm U, Mettenleiter T, Beer M, Harder T. Longitudinal 2 years field study of conventional vaccination against highly pathogenic avian influenza H5N1 in layer hens. Vaccine. 2010;28(42):6832–40. doi:10.1016/j.vaccine.2010.08.038.
41. Schoen C, Stritzker J, Goebel W, Pilgrim S. Bacteria as DNA vaccine carriers for genetic immunization. Int J Med Microbiol. 2004;294(5):319–35.
42. Shi J, Wang M, Wang J, Wang S, Luo E. Comparison of inhibitory efficacy of short interfering RNAs targeting different genes on Measles virus replication. J Basic Microbiol. 2012;52(3):332–9. doi:10.1002/jobm.201100207.
43. Shinya K, Awakura T, Shimada A, Silvano FD, Umemura T, Otsuki K. Pathogenesis of pancreatic atrophy by avian influenza A virus infection. Avian Pathol. 1995;24(4):623–32.
44. Stoppani E, Bassi I, Dotti S, Lizier M, Ferrari M, Lucchini F. Expression of a single siRNA against a conserved region of NP gene strongly inhibits in vitro replication of different influenza A virus strains of avian and swine origin. Antiviral Res. 2015;120:16–22. doi:10.1016/j.antiviral.2015.04.017.
45. Sui HY, Zhao GY, Huang JD, Jin DY, Yuen KY, Zheng BJ. Small interfering RNA targeting m2 gene induces effective and long term inhibition of influenza A virus replication. PLoS One. 2009;4(5):e5671. doi:10.1371/journal.pone.0005671.
46. Swayne DE. Impact of vaccines and vaccination on global control of avian influenza. Avian Dis. 2012;56:818–28.
47. Swayne DE, Kapczynski DR. Vaccines, vaccination, and immunology for avian influenza viruses in poultry. In: Swayne DE, editor. Avian Influenza. Ames: Blackwell Publishing; 2008. p. 407–51.
48. Swayne DE, Pantin-Jackwood MJ. Pathogenicity of avian influenza viruses in poultry. Dev Biol (Basel). 2006;124:61–7.
49. Tompkins SM, Lo CY, Tumpey TM, Epstein SL. Protection against lethal influenza virus challenge by RNA interference in vivo. Proc Natl Acad Sci USA. 2004;101(23):8682–6.
50. Xiang S, Fruehauf J, Li CJ. Short hairpin RNA-expressing bacteria elicit RNA interference in mammals. Nat Biotechnol. 2006;24(6):697–702.
51. Xiang S, Keates AC, Fruehauf J, Yang Y, Guo H, Nguyen T, Li CJ. In vitro and in vivo gene silencing by transkingdom RNAi (tkRNAi). Methods Mol Biol. 2009;487:147–60. doi:10.1007/978-1-60327-547-7_7.
52. Zhao H, L’Abbé D, Jolicoeur N, Wu M, Li Z, Yu Z, Shen SH. High-throughput screening of effective siRNAs from RNAi libraries delivered via bacterial invasion. Nat Methods. 2005;2(12):967–73.
53. Zhou H, Jin M, Yu YuZ, Xu X, Peng Y, Wu H, Liu J, Liu H, Cao S, Chen H. Effective small interfering RNAs targeting matrix and nucleocapsid protein gene inhibit influenza A virus replication in cells and mice. Antiviral Res. 2007;76(2):186–93.
54. Zhou K, He H, Wu Y, Duan M. RNA interference of avian influenza virus H5N1 by inhibiting viral mRNA with siRNA expression plasmids. J Biotechnol. 2008;135(2):140–4. doi:10.1016/j.jbiotec.2008.03.007.