1887

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Volume 101, Issue 8

miR-927 has pro-viral effects during acute and persistent infection with dengue virus type 2 in C6/36 mosquito cells Free

Abstract

Dengue virus (DENV) is an important flavivirus that is transmitted to humans by mosquitoes, where it can establish a persistent infection underlying vertical and horizontal transmission. However, the exact mechanism of persistent DENV infection is not well understood. Recently miR-927 was found to be upregulated in C6/36-HT cells at 57 weeks of persistent infection (C6-L57), suggesting its participation during this type of infection. The aim of this study was to determine the role of miR-927 during infection with DENV type 2. The results indicate an overexpression of miR-927 in C6-L57 cells and acutely infected cells according to the time of infection and the m.o.i. used. The downregulation of miR-927 in C6-L57 cells results in a reduction of both viral titre and viral genome copy number. The overexpression of miR-927 in C6-L40 and C6/36 cells infected at an m.o.i. of 0.1 causes an increase in both viral titre and viral genome copy number, suggesting a pro-viral activity of miR-927. prediction analysis reveals target mRNAs for miR-927 are implicated in post-translational modifications (SUMO), translation factors (eIF-2B), the innate immune system (NKIRAS), exocytosis (EXOC-2), endocytosis (APM1) and the cytoskeleton (FLN). The expression levels of FLN were the most affected by both miR-927 overexpression and inhibition, and FLN was determined to be a direct target of miR-927 by a dual-luciferase gene reporter assay. FLN has been associated with the regulation of the Toll pathway and either overexpression or downregulation of miR-927 resulted in expression changes of antimicrobial peptides (Cecropins A and G, and Defensin D) involved in the Toll pathway response.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): dengue , filamin , innate immune response , microRNAs , mosquito cells and persistent infection
Funding
This study was supported by the:
  • Secretaría de Investigación y Posgrado, Instituto Politécnico Nacional (Award 20160946, 20181010, 20195702)
    • Principle Award Recipient: Juan Santiago Salas-Benito
© 2020 The Authors
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2020-06-01
2024-04-24
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References

  1. Drury RE, O'Connor D, Pollard AJ. The clinical application of microRNAs in infectious disease. Front Immunol 2017; 8:1182 [View Article][PubMed]
     [Google Scholar]
  2. Bavia L, Mosimann ALP, Aoki MN, Duarte Dos Santos CN, Pamplona MAL. A glance at subgenomic flavivirus RNAs and microRNAs in flavivirus infections. Virol J 2016; 13:84 [View Article][PubMed]
     [Google Scholar]
  3. Skalsky RL, Vanlandingham DL, Scholle F, Higgs S, Cullen BR. Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus . BMC Genomics 2010; 11:119 [View Article][PubMed]
     [Google Scholar]
  4. Etebari K, Osei-Amo S, Blomberg SP, Asgari S. Dengue virus infection alters post-transcriptional modification of microRNAs in the mosquito vector Aedes aegypti . Sci Rep 2015; 5:15968 [View Article][PubMed]
     [Google Scholar]
  5. Miesen P, Ivens A, Buck AH, van Rij RP. Small RNA profiling in dengue virus 2-infected Aedes mosquito cells reveals viral piRNAs and novel host miRNAs. PLoS Negl Trop Dis 2016; 10:e0004452 [View Article][PubMed]
     [Google Scholar]
  6. Etebari K, Hegde S, Saldaña MA, Widen SG, Wood TG et al. Global transcriptome analysis of Aedes aegypti mosquitoes in response to Zika virus infection. mSphere 2017; 2:e00456-17 [View Article][PubMed]
     [Google Scholar]
  7. Liu Y, Zhou Y, Wu J, Zheng P, Li Y et al. The expression profile of Aedes albopictus miRNAs is altered by dengue virus serotype-2 infection. Cell Biosci 2015; 5:16 [View Article][PubMed]
     [Google Scholar]
  8. Liu Y-X, Li F-X, Liu Z-Z, Jia Z-R, Zhou Y-H et al. Integrated analysis of miRNAs and transcriptomes in Aedes albopictus midgut reveals the differential expression profiles of immune-related genes during dengue virus serotype-2 infection. Insect Sci 2016; 23:377–385 [View Article][PubMed]
     [Google Scholar]
  9. Su J, Li C, Zhang Y, Yan T, Zhu X et al. Identification of microRNAs expressed in the midgut of Aedes albopictus during dengue infection. Parasit Vectors 2017; 10:63 [View Article][PubMed]
     [Google Scholar]
  10. Bernhardt SA, Simmons MP, Olson KE, Beaty BJ, Blair CD et al. Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti . PLoS One 2012; 7:e44198 [View Article][PubMed]
     [Google Scholar]
  11. Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol 2013; 425:4921–4936 [View Article][PubMed]
     [Google Scholar]
  12. Lee M, Etebari K, Hall-Mendelin S, van den Hurk AF, Hobson-Peters J et al. Understanding the role of microRNAs in the interaction of Aedes aegypti mosquitoes with an insect-specific flavivirus. J Gen Virol 2017; 98:1892–1903 [View Article][PubMed]
     [Google Scholar]
  13. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J et al. Dengue: a continuing global threat. Nat Rev Microbiol 2010; 8:S7–S16 [View Article][PubMed]
     [Google Scholar]
  14. Olson KE, Blair CD. Arbovirus–mosquito interactions: RNAi pathway. Curr Opin Virol 2015; 15:119–126 [View Article][PubMed]
     [Google Scholar]
  15. Goic B, Vodovar N, Mondotte JA, Monot C, Frangeul L et al. RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila . Nat Immunol 2013; 14:396–403 [View Article][PubMed]
     [Google Scholar]
  16. Poirier EZ, Goic B, Tomé-Poderti L, Frangeul L, Boussier J et al. Dicer-2-dependent generation of viral DNA from defective genomes of RNA viruses modulates antiviral immunity in insects. Cell Host Microbe 2018; 23:353–365 [View Article][PubMed]
     [Google Scholar]
  17. Juárez-Martínez AB, Vega-Almeida TO, Salas-Benito M, García-Espitia M, De Nova-Ocampo M et al. Detection and sequencing of defective viral genomes in C6/36 cells persistently infected with dengue virus 2. Arch Virol 2013; 158:583–599 [View Article][PubMed]
     [Google Scholar]
  18. Scott JC, Brackney DE, Campbell CL, 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 [View Article]
     [Google Scholar]
  19. Shinde SP, Banerjee AK, Arora N, Murty USN, Sripathi VR et al. Computational approach for elucidating interactions of cross-species miRNAs and their targets in flaviviruses. J Vector Borne Dis 2015; 52:11–22[PubMed]
     [Google Scholar]
  20. Zhang Y, Jing J, Li X, Wang J, Feng X et al. Integration analysis of miRNA and mRNA expression profiles in swine testis cells infected with Japanese encephalitis virus. Infect Genet Evol 2015; 32:342–347 [View Article][PubMed]
     [Google Scholar]
  21. Avila-Bonilla RG, Yocupicio-Monroy M, Marchat LA, De Nova-Ocampo MA, Del Ángel RM et al. Analysis of the miRNA profile in C6/36 cells persistently infected with dengue virus type 2. Virus Res 2017; 232:139–151 [View Article][PubMed]
     [Google Scholar]
  22. Igarashi A. Isolation of a Singh’s Aedes albopictus cell clone sensitive to dengue and chikungunya viruses. J Gen Virol 1978; 40:531–544 [View Article][PubMed]
     [Google Scholar]
  23. Kuno G, Oliver A. Maintaining mosquito cell lines at high temperatures: effects on the replication of flaviviruses. In Vitro Cell Dev Biol 1989; 25:193–196 [View Article][PubMed]
     [Google Scholar]
  24. Gould EA, Clegg JCS. Growth titration and purification of alphaviruses and flaviviruses. In Mahy BWJ. editor Virology: a Practical Approach Oxford: IRL Press; 1991 pp 43–78
     [Google Scholar]
  25. Luplertlop N, Surasombatpattana P, Patramool S, Dumas E, Wasinpiyamongkol L et al. Induction of a peptide with activity against a broad spectrum of pathogens in the Aedes aegypti salivary gland, following infection with dengue virus. PLoS Pathog 2011; 7:e1001252 [View Article][PubMed]
     [Google Scholar]
  26. Bajan S, Hutvagner G. RNA-based therapeutics: from antisense oligonucleotides to miRNAs. Cells 2020; 9:137 [View Article][PubMed]
     [Google Scholar]
  27. Bao W, Greenwold MJ, Sawyer RH. Expressed miRNAs target feather related mRNAs involved in cell signaling, cell adhesion and structure during chicken epidermal development. Gene 2016; 591:393–402 [View Article][PubMed]
     [Google Scholar]
  28. Ling L, Kokoza VA, Zhang C, Aksoy E, Raikhel AS. MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. Proc Natl Acad Sci USA 2017; 114:E8017–E8024 [View Article][PubMed]
     [Google Scholar]
  29. Igarashi A. Characteristics of Aedes albopictus cells persistently infected with dengue viruses. Nature 1979; 280:690–691 [View Article][PubMed]
     [Google Scholar]
  30. Reyes-Ruiz JM, Osuna-Ramos JF, Bautista-Carbajal P, Jaworski E, Soto-Acosta R et al. Mosquito cells persistently infected with dengue virus produce viral particles with host-dependent replication. Virology 2019; 531:1–18 [View Article][PubMed]
     [Google Scholar]
  31. Ezzell RM, Kenney DM, Egan S, Stossel TP, Hartwig JH. Localization of the domain of actin-binding protein that binds to membrane glycoprotein Ib and actin in human platelets. J Biol Chem 1988; 263:13303–13309[PubMed]
     [Google Scholar]
  32. Sharma CP, Ezzell RM, Arnaout MA. Direct interaction of filamin (ABP-280) with the beta 2-integrin subunit CD18. J Immunol 1995; 154:3461–3470[PubMed]
     [Google Scholar]
  33. Edwards DN, Towb P, Wasserman SA. An activity-dependent network of interactions links the Rel protein Dorsal with its cytoplasmic regulators. Development 1997; 124:3855–3864[PubMed]
     [Google Scholar]
  34. Loo DT, Kanner SB, Aruffo A. Filamin binds to the cytoplasmic domain of the beta1-integrin: identification of amino acids responsible for this interaction. J Biol Chem 1998; 273:23304–23312 [View Article][PubMed]
     [Google Scholar]
  35. Xi Z, Ramirez JL, Dimopoulos G. The Aedes aegypti Toll pathway controls dengue virus infection. PLoS Pathog 2008; 4:e1000098 [View Article][PubMed]
     [Google Scholar]
  36. Ramirez JL, 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 [View Article][PubMed]
     [Google Scholar]
  37. Behura SK, Gomez-Machorro C, Harker BW, deBruyn B, Lovin DD et al. Global cross-talk of genes of the mosquito Aedes aegypti in response to dengue virus infection. PLoS Negl Trop Dis 2011; 5:e1385 [View Article][PubMed]
     [Google Scholar]
  38. Colpitts TM, Cox J, Vanlandingham DL, Feitosa FM, Cheng G et al. Alterations in the Aedes aegypti transcriptome during infection with West Nile, dengue and yellow fever viruses. PLoS Pathog 2011; 7:e1002189 [View Article][PubMed]
     [Google Scholar]
  39. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Marinotti O et al. Complex modulation of the Aedes aegypti transcriptome in response to dengue virus infection. PLoS One 2012; 7:e50512 [View Article][PubMed]
     [Google Scholar]
  40. Sim S, Jupatanakul N, Ramirez JL, Kang S, Romero-Vivas CM et al. Transcriptomic profiling of diverse Aedes aegypti strains reveals increased basal-level immune activation in dengue virus-refractory populations and identifies novel virus-vector molecular interactions. PLoS Negl Trop Dis 2013; 7:e2295 [View Article][PubMed]
     [Google Scholar]
  41. Pompon J, Manuel M, Ng GK, Wong B, Shan C et al. Dengue subgenomic flaviviral RNA disrupts immunity in mosquito salivary glands to increase virus transmission. PLoS Pathog 2017; 13:e1006535 [View Article][PubMed]
     [Google Scholar]
  42. Zhang G, Hussain M, O'Neill SL, Asgari S. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti . Proc Natl Acad Sci USA 2013; 110:10276–10281 [View Article][PubMed]
     [Google Scholar]
  43. Hussain M, Walker T, O'Neill SL, Asgari S. Blood meal induced microRNA regulates development and immune associated genes in the dengue mosquito vector, Aedes aegypti . Insect Biochem Mol Biol 2013; 43:146–152 [View Article][PubMed]
     [Google Scholar]
  44. Campbell CL, Harrison T, Hess AM, Ebel GD. MicroRNA levels are modulated in Aedes aegypti after exposure to dengue-2. Insect Mol Biol 2014; 23:132–139 [View Article][PubMed]
     [Google Scholar]
  45. Saldaña MA, Etebari K, Hart CE, Widen SG, Wood TG et al. Zika virus alters the microRNA expression profile and elicits an RNAi response in Aedes aegypti mosquitoes. PLoS Negl Trop Dis 2017; 11:e0005760 [View Article][PubMed]
     [Google Scholar]
  46. Zhou Y, Liu Y, Yan H, Li Y, Zhang H et al. miR-281, an abundant midgut-specific miRNA of the vector mosquito Aedes albopictus enhances dengue virus replication. Parasit Vectors 2014; 7:488 [View Article][PubMed]
     [Google Scholar]
  47. Yan H, Zhou Y, Liu Y, Deng Y, Chen X. miR-252 of the Asian tiger mosquito Aedes albopictus regulates dengue virus replication by suppressing the expression of the dengue virus envelope protein. J Med Virol 2014; 86:1428–1436 [View Article][PubMed]
     [Google Scholar]
  48. Slonchak A, Hussain M, Torres S, Asgari S, Khromykh AA. Expression of mosquito microRNA Aae-miR-2940-5p is downregulated in response to West Nile virus infection to restrict viral replication. J Virol 2014; 88:8457–8467 [View Article][PubMed]
     [Google Scholar]
  49. Shrinet J, Jain S, Jain J, Bhatnagar RK, Sunil S. Next generation sequencing reveals regulation of distinct Aedes microRNAs during Chikungunya virus development. PLoS Negl Trop Dis 2014; 8:e2616 [View Article][PubMed]
     [Google Scholar]
  50. Kanokudom S, Vilaivan T, Wikan N, Thepparit C, Smith DR et al. miR-21 promotes dengue virus serotype 2 replication in HepG2 cells. Antiviral Res 2017; 142:169–177 [View Article][PubMed]
     [Google Scholar]
  51. Wu S, He L, Li Y, Wang T, Feng L et al. miR-146a facilitates replication of dengue virus by dampening interferon induction by targeting TRAF6. J Infect 2013; 67:329–341 [View Article][PubMed]
     [Google Scholar]
  52. Hussain M, Torres S, Schnettler E, Funk A, Grundhoff A et al. 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 2012; 40:2210–2223 [View Article][PubMed]
     [Google Scholar]
  53. Huang Y, Zou Q, Song H, Song F, Wang L et al. A study of miRNAs targets prediction and experimental validation. Protein Cell 2010; 1:979–986 [View Article][PubMed]
     [Google Scholar]
  54. Gebert LFR, MacRae IJ. Regulation of microRNA function in animals. Nat Rev Mol Cell Biol 2019; 20:21–37 [View Article][PubMed]
     [Google Scholar]
  55. Sokol NS, Cooley L. Drosophila filamin encoded by the cheerio locus is a component of ovarian ring canals. Curr Biol 1999; 9:1221–1230 [View Article][PubMed]
     [Google Scholar]
  56. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 1996; 84:345–357 [View Article][PubMed]
     [Google Scholar]
  57. Guo Y, Zhang SX, Sokol N, Cooley L, Boulianne GL. Physical and genetic interaction of filamin with presenilin in Drosophila . J Cell Sci 2000; 113:3499–3508[PubMed]
     [Google Scholar]
  58. Li MG, Serr M, Edwards K, Ludmann S, Yamamoto D et al. Filamin is required for ring canal assembly and actin organization during Drosophila oogenesis. J Cell Biol 1999; 146:1061–1074 [View Article][PubMed]
     [Google Scholar]
  59. Sim S, Dimopoulos G. Dengue virus inhibits immune responses in Aedes aegypti cells. PLoS One 2010; 5:e10678 [View Article][PubMed]
     [Google Scholar]
  60. Souza-Neto JA, Sim S, Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 2009; 106:17841–17846 [View Article][PubMed]
     [Google Scholar]
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miR-927 has pro-viral effects during acute and persistent infection with dengue virus type 2 in C6/36 mosquito cells
J. Gen. Virol. 101, 825 (2020); https://doi.org/10.1099/jgv.0.001441
/content/journal/jgv/10.1099/jgv.0.001441
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