Repertoire of virus-derived small RNAs produced by mosquito and mammalian cells in response to dengue virus infection

Virology

Volumn 476, Issue , 2015, Pages 54-60

  Schirtzinger, Erin E ^a,c   Andrade, Christy C ^a,d   Devitt, Nicholas ^b   Ramaraj, Thiruvarangan ^b   Jacobi, Jennifer L ^b   Schilkey, Faye ^b   Hanley, Kathryn A ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b NATIONAL CENTER FOR GENOME RESOURCES   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

^d WILLAMETTE UNIVERSITY   (United States)

Author keywords

Dengue; Flavivirus; HuH 7; Next generation sequencing; RNA interference; SiRNA; U4.4; Vero; ViRNA; Virus

Indexed keywords

INTERFERON; NUCLEOTIDE; RNA; UNCLASSIFIED DRUG; VIRUS DERIVED SMALL RNA; SMALL INTERFERING RNA; VIRUS RNA;

ANIMAL CELL; ARTICLE; CELL LINE; CYTOKINE RESPONSE; DENGUE; GENE TARGETING; HUH 7 CELL LINE; IMMUNOCOMPETENCE; MAMMAL CELL; MOSQUITO; NONHUMAN; PRIMATE; RNA INTERFERENCE; RNA SEQUENCE; RNA STRUCTURE; RNA SYNTHESIS; VERO CELL LINE; VIRUS GENOME; VIRUS IMMUNITY; VIRUS ISOLATION; AEDES; ANIMAL; DENGUE VIRUS; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; VIROLOGY;

ARBOVIRUS; ARTHROPODA; DENGUE VIRUS; FLAVIVIRUS; MAMMALIA; RNA VIRUSES; VERTEBRATA;

AEDES; ANIMALS; BASE SEQUENCE; CELL LINE; DENGUE; DENGUE VIRUS; HUMANS; MOLECULAR SEQUENCE DATA; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA, VIRAL;

EID: 84918768558     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.11.019     Document Type: Article

References (39)

1. Alcaraz-Estrada S.L., Yocupicio-Monroy M., Del Angel R. Insights into dengue virus genome replication. Futur. Virol. 2010, 5:575-592.
2. Blair C.D. Mosquito RNAi is the major innate immune pathway controlling arbovirus infection and transmission. Futur. Microbiol. 2011, 6:265-277.
3. Blaney J.E., Sathe N.S., Goddard L., Hanson C.T., Romero T.A., Hanley K.A., Murphy B.R., Whitehead S.S. Dengue virus type 3 vaccine candidates generated by introduction of deletions in the 3' untranslated region (3'-UTR) or by exchange of the DENV-3 3'-UTR with that of DENV-4. Vaccine 2008, 26:817-828.
4. Bogerd H.P., Skalsky R.L., Kennedy E.M., Furuse Y., Whisnant A.W., Flores O., Schultz K.L., Putnam N., Barrows N.J., Sherry B., Scholle F., Garcia-Blanco M.A., Griffin D.E., Cullen B.R. Replication of many human viruses is refractory to inhibition by endogenous cellular microRNAs. J. Virol. 2014, 88:8065-8076.
5. Brackney D.E., Beane J.E., Ebel G.D. RNAi targeting of West Nile virus in mosquito midguts promotes virus diversification. PLoS Pathog. 2009, 5:e1000502.
6. Brackney D.E., Scott J.C., Sagawa F., Woodward J.E., Miller N.A., Schilkey F.D., Mudge J., Wilusz J., Olson K.E., Blair C.D., Ebel G.D. C6/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl. Trop. Dis. 2010, 4:e856.
7. Bronkhorst A.W., van Rij R.P. The long and short of antiviral defense: small RNA-based immunity in insects. Curr. Opin. Virol. 2014, 7C:19-28.
8. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 2004, 14:1188-1190.
9. Cullen B.R., Cherry S., tenOever B.R. Is RNA interference a physiologically relevant innate antiviral immune response in mammals?. Cell Host Microbe 2013, 14:374-378.
10. Desmyter J., Melnick J.L., Rawls W.E. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J. Virol. 1968, 2:955-961.
11. Diamond M.S., Zachariah M., Harris E. Mycophenolic acid inhibits dengue virus infection by preventing replication of viral RNA. Virology 2002, 304:211-221.
12. Ding S.W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
13. Donaszi-Ivanov A., Mohorianu I., Dalmay T., Powell P.P. Small RNA analysis in Sindbis virus infected human HEK293 cells. PLoS ONE 2013, 8:e84070.
14. Emeny J.M., Morgan M.J. Regulation of the interferon system: evidence that Vero cells have a genetic defect in interferon production. J. Gen. Virol. 1979, 43:247-252.
15. Hanley K.A., Nelson J.T., Schirtzinger E.E., Whitehead S.S., Hanson C.T. Superior infectivity for mosquito vectors contributes to competitive displacement among strains of dengue virus. BMC Ecol. 2008, 8:1.
16. Hess A.M., Prasad A.N., Ptitsyn A., Ebel G.D., Olson K.E., Barbacioru C., Monighetti C., Campbell C.L. Small RNA profiling of Dengue virus-mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol. 2011, 11:45.
17. Kakumani P.K., Ponia S.S., Sood S.R.K., Chinnappan V., Banerjea M., Medigeshi A.C., Malhotra G.R., Mukherjee P., Bhatnagar RK S.K. Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor. J. Virol. 2013, 87:8870-8883.
18. Lambrechts L., Quillery E., Noel V., Richardson J.H., Jarman R.G., Scott T.W., Chevillon C. Specificity of resistance to dengue virus isolates is associated with genotypes of the mosquito antiviral gene Dicer-2. Proc. Biol. Sci. 2013, 280:20122437.
19. Leger P., Lara E., Jagla B., Sismeiro O., Mansuroglu Z., Coppee J.Y., Bonnefoy E., Bouloy M. Dicer-2- and Piwi-mediated RNA interference in Rift Valley fever virus-infected mosquito cells. J. Virol. 2013, 87:1631-1648.
20. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
21. Li Y., Lu J., Han Y., Fan X., Ding S.W. RNA interference functions as an antiviral immunity mechanism in mammals. Science 2013, 342:231-234.
22. Maillard P.V., Ciaudo C., Marchais A., Li Y., Jay F., Ding S.W., Voinnet O. Antiviral RNA interference in mammalian cells. Science 2013, 342:235-238.
23. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 2011, 17.1:10-12.
24. Matskevich A.A., Jung J.S., Schumann M., Cascallo M., Moelling K. Vero cells as a model to study the effects of adenoviral gene delivery vectors on the RNAi system in context of viral infection. J. Innate Immun. 2009, 1:389-394.
25. Morazzani E.M., Wiley M.R., Murreddu M.G., Adelman Z.N., Myles K.M. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog. 2012, 8:e1002470.
26. Parameswaran P., Sklan E., Wilkins C., Burgon T., Samuel M.A., Lu R., Ansel K.M., Heissmeyer V., Einav S., Jackson W., Doukas T., Paranjape S., Polacek C., dos Santos F.B., Jalili R., Babrzadeh F., Gharizadeh B., Grimm D., Kay M., Koike S., Sarnow P., Ronaghi M., Ding S.W., Harris E., Chow M., Diamond M.S., Kirkegaard K., Glenn J.S., Fire A.Z. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog. 2010, 6:e1000764.
27. Pauli E.K., Schmolke M., Wolff T., Viemann D., Roth J., Bode J.G., Ludwig S. Influenza A virus inhibits type I IFN signaling via NF-kappaB-dependent induction of SOCS-3 expression. PLoS Pathog. 2008, 4:e1000196.
28. Sabin L.R., Zheng Q., Thekkat P., Yang J., Hannon G.J., Gregory B.D., Tudor M., Cherry S. Dicer-2 processes diverse viral RNA species. PLoS ONE 2013, 8:e55458.
29. Schneider T.D., Stephens R.M. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990, 18:6097-6100.
30. Schnettler E., Sterken M.G., Leung J.Y., Metz S.W., Geertsema C., Goldbach R.W., Vlak J.M., Kohl A., Khromykh A.A., Pijlman G.P. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 2012, 86:13486-13500.
31. Seo G.J., Kincaid R.P., Phanaksri T., Burke J.M., Pare J.M., Cox J.E., Hsiang T.Y., Krug R.M., Sullivan C.S. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 2013, 14:435-445.
32. Siu R.W., Fragkoudis R., Simmonds P., Donald C.L., Chase-Topping M.E., Barry G., Attarzadeh-Yazdi G., Rodriguez-Andres J., Nash A.A., Merits A., Fazakerley J.K., Kohl A. 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. 2011, 85:2907-2917.
33. Svoboda P. Renaissance of mammalian endogenous RNAi. FEBS Lett. 2014, 588:2550-2556.
34. Vodovar N., Bronkhorst A.W., van Cleef K.W., Miesen P., Blanc H., van Rij R.P., Saleh M.C. Arbovirus-derived piRNAs exhibit a ping-pong signature in mosquito cells. PLoS ONE 2012, 7:e30861.
35. Wathelet M.G., Berr P.M., Huez G.A. Regulation of gene expression by cytokines and virus in human cells lacking the type-I interferon locus. Eur. J. Biochem. 1992, 206:901-910.
36. Watson M., Schnettler E., Kohl A. viRome: an R package for the visualization and analysis of viral small RNA sequence datasets. Bioinformatics 2013, 29:1902-1903.
37. Wu T.D., Nacu S. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 2011, 26:873-881.
38. Zhang T., Lin R.T., Li Y., Douglas S.D., Maxcey C., Ho C., Lai J.P., Wang Y.J., Wan Q., Ho W.Z. Hepatitis C virus inhibits intracellular interferon alpha expression in human hepatic cell lines. Hepatology 2005, 42:819-827.
39. Zhou R., Rana T.M. RNA-based mechanisms regulating host-virus interactions. Immunol. Rev. 2013, 253:97-111.