1887

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Volume 101, Issue 1

Dengue virus infects the mouse eye following systemic or intracranial infection and induces inflammatory responses Free

Abstract

Dengue virus (DENV) infection is associated with clinical ocular presentations and here DENV infection of the eye was assessed in mice. In an AG129 mouse model of antibody-dependent enhancement of DENV infection, DENV RNA was detected in the eye and vascular changes were present in the retinae. Intraocular CD8 and IFN-γ mRNA were increased in mice born to DENV-naïve, but not DENV-immune mothers, while TNF-α mRNA was induced and significantly higher in mice born to DENV-immune than DENV-naïve mothers. DENV RNA was detected in the eye following intracranial DENV infection and CD8 mRNA but not IFN-γ nor TNF-α were induced. In all models, viperin was increased following DENV infection. Thus, DENV in the circulation or the brain can infect the eye and stimulate innate immune responses, with induction of viperin as one response that consistently occurs in multiple DENV eye-infection models in both an IFN-dependent and independent manner.

  • Received:
  • Accepted:
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Keyword(s): AG129 mouse , Dengue virus , eye infection and viperin
© 2020 The Authors
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2020-01-01
2024-04-25
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References

  1. Kawali A, Mahendradas P, Mohan A, Mallavarapu M, Shetty B. Epidemic retinitis. Ocul Immunol Inflamm 20181–7
     [Google Scholar]
  2. Khairallah M, Chee SP, Rathinam SR, Attia S, Nadella V. Novel infectious agents causing uveitis. Int Ophthalmol 2010; 30:465–483 [View Article]
     [Google Scholar]
  3. de Andrade GC, Ventura CV, Mello Filho PA de A, Maia M, Vianello S et al. Arboviruses and the eye. Int J Retina Vitreous 2017; 3:4 [View Article]
     [Google Scholar]
  4. Karesh JW, Mazzoli RA, Heintz SK. Ocular manifestations of Mosquito-Transmitted diseases. Mil Med 2018; 183:450–458 [View Article]
     [Google Scholar]
  5. Khairallah M, Kahloun R. Ocular manifestations of emerging infectious diseases. Curr Opin Ophthalmol 2013; 24:574–580 [View Article]
     [Google Scholar]
  6. Singh S, Farr D, Kumar A. Ocular manifestations of emerging flaviviruses and the blood-retinal barrier. Viruses 2018; 10:530 [View Article]
     [Google Scholar]
  7. Shukla J, Saxena D, Rathinam S, Lalitha P, Joseph CR et al. Molecular detection and characterization of West Nile virus associated with multifocal retinitis in patients from southern India. Int J Infect Dis 2012; 16:e53–e59 [View Article]
     [Google Scholar]
  8. Babu K, Kini R, Philips M, Subbakrishna DK. Clinical profile of isolated viral anterior uveitis in a South Indian patient population. Ocul Immunol Inflamm 2014; 22:356–359 [View Article]
     [Google Scholar]
  9. Mahendradas P, Shetty R, Malathi J, Madhavan HN. Chikungunya virus iridocyclitis in Fuchs′ heterochromic iridocyclitis. Indian J Ophthalmol 2010; 58:545–547 [View Article]
     [Google Scholar]
  10. Furtado JM, Espósito DL, Klein TM, Teixeira-Pinto T, da Fonseca BA. Uveitis associated with Zika virus infection. N Engl J Med 2016; 375:394–396 [View Article]
     [Google Scholar]
  11. Chlebicki MP, Ang B, Barkham T, Laude A. Retinal hemorrhages in 4 patients with dengue fever. Emerg Infect Dis 2005; 11:770–772 [View Article]
     [Google Scholar]
  12. Ng AW, Teoh SC. Dengue eye disease. Surv Ophthalmol 2015; 60:106–114 [View Article]
     [Google Scholar]
  13. Yip VC-H, Sanjay S, Koh YT. Ophthalmic complications of dengue fever: a systematic review. Ophthalmol Ther 2012; 1:2 [View Article]
     [Google Scholar]
  14. Lim W, Mathur R, Koh A, Yeoh R, Chee S. Ocular manifestations of dengue fever☆. Ophthalmology 2004; 111:2057–2064 [View Article]
     [Google Scholar]
  15. Su DHW, Bacsal K, Chee SP, Flores JVP, Lim W-K et al. Prevalence of dengue maculopathy in patients hospitalized for dengue fever. Ophthalmology 2007; 114:1743–1747 [View Article]
     [Google Scholar]
  16. Carr JM, Ashander LM, Calvert JK, Ma Y, Aloia A et al. Molecular responses of human retinal cells to infection with dengue virus. Mediators Inflamm 2017; 2017:316437516 [View Article]
     [Google Scholar]
  17. JK N, Zhang SL, Tan HC, Yan B, Martinez JM et al. First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS pathogens 2014; 10:e1004031
     [Google Scholar]
  18. Halstead SB. Pathogenesis of dengue: dawn of a new era. F1000Res 2015; 4:1353 [View Article]
     [Google Scholar]
  19. Kliks SC, Nimmanitya S, Burke DS, Nisalak A. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg 1988; 38:411–419 [View Article]
     [Google Scholar]
  20. Srichaikul T, Nimmanitaya S, Artchararit N, Siriasawakul T, Sungpeuk P. Fibrinogen metabolism and disseminated intravascular coagulation in dengue hemorrhagic fever. Am J Trop Med Hyg 1977; 26:525–532 [View Article]
     [Google Scholar]
  21. Aggarwal K, Agarwal A, Katoch D, Sharma M, Gupta V. Optical coherence tomography angiography features of acute macular neuroretinopathy in dengue fever. Indian J Ophthalmol 2017; 65:1235–1238 [View Article]
     [Google Scholar]
  22. Tan P, Lye DC, Yeo TK, Cheung CY, Thein T-L et al. A prospective case-control study to investigate retinal microvascular changes in acute dengue infection. Sci Rep 2015; 5:17183 [View Article]
     [Google Scholar]
  23. Sierra B, Aguirre E, Volk H-D, Vogt K, Schmolke K et al. Variation in inflammatory/regulatory cytokines in secondary, tertiary, and quaternary challenges with dengue virus. Am J Trop Med Hyg 2012; 87:538–547 [View Article]
     [Google Scholar]
  24. Green S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Suntayakorn S et al. Early immune activation in acute dengue illness is related to development of plasma leakage and disease severity. J Infect Dis 1999; 179:755–762 [View Article]
     [Google Scholar]
  25. Hober D, Roblin B, Vergez-Pascal R, Granic G, Maniez-Montreuil M et al. Serum levels of tumor necrosis factor-α (TNF-α), interleukin-6 (IL-6), and interleukin-1β (IL-1β) in Dengue-Infected patients. Am J Trop Med Hyg 1993; 48:324–331 [View Article]
     [Google Scholar]
  26. Kittigul L, Temprom W, Sujirarat D, Kittigul C. Determination of tumor necrosis factor-alpha levels in dengue virus infected patients by sensitive biotin-streptavidin enzyme-linked immunosorbent assay. J Virol Methods 2000; 90:51–57 [View Article]
     [Google Scholar]
  27. Chen HC, Hofman FM, Kung JT, Lin YD, Wu-Hsieh BA. Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 2007; 81:5518–5526 [View Article]
     [Google Scholar]
  28. Gualano RC, Pryor MJ, Cauchi MR, Wright PJ, Davidson AD. Identification of a major determinant of mouse neurovirulence of dengue virus type 2 using stably cloned genomic-length cDNA. J Gen Virol 1998; 79:437–446 [View Article]
     [Google Scholar]
  29. Al-Shujairi WH, Clarke JN, Davies LT, Alsharifi M, Pitson SM et al. Intracranial injection of dengue virus induces interferon stimulated genes and CD8+ T cell infiltration by sphingosine kinase 1 independent pathways. PLoS One 2017; 12:e0169814 [View Article]
     [Google Scholar]
  30. Miner JJ, Sene A, Richner JM, Smith AM, Santeford A et al. Zika virus infection in mice causes panuveitis with shedding of virus in tears. Cell Rep 2016; 16:3208–3218 [View Article]
     [Google Scholar]
  31. Manangeeswaran M, Kielczewski JL, Sen HN, Xu BC, Ireland DDC et al. Zika virus infection causes persistent chorioretinal lesions. Emerg Microbes Infect 2018; 7:1–15 [View Article]
     [Google Scholar]
  32. van den Pol AN, Mao G, Yang Y, Ornaghi S, Davis JN. Zika virus targeting in the developing brain. J Neurosci 2017; 37:2161–2175 [View Article]
     [Google Scholar]
  33. Darwich L, Coma G, Peña R, Bellido R, Blanco EJJ et al. Secretion of interferon-γ by human macrophages demonstrated at the single-cell level after costimulation with interleukin (IL)-12 plus IL-18. Immunology 2009; 126:386–393 [View Article]
     [Google Scholar]
  34. Helbig KJ, Carr JM, Calvert JK, Wati S, Clarke JN et al. Viperin is induced following dengue virus type-2 (DENV-2) infection and has anti-viral actions requiring the C-terminal end of viperin. PLoS Negl Trop Dis 2013; 7:e2178 [View Article]
     [Google Scholar]
  35. Calvert JK, Helbig KJ, Dimasi D, Cockshell M, Beard MR et al. Dengue virus infection of primary endothelial cells induces innate immune responses, changes in endothelial cells function and is restricted by interferon-stimulated responses. J Interferon Cytokine Res 2015; 35:654–665 [View Article]
     [Google Scholar]
  36. Van der Hoek KH, Eyre NS, Shue B, Khantisitthiporn O, Glab-Ampi K et al. Viperin is an important host restriction factor in control of Zika virus infection. Sci Rep 2017; 7:4475 [View Article]
     [Google Scholar]
  37. Jiang D, Weidner JM, Qing M, Pan X-B, Guo H et al. Identification of five interferon-induced cellular proteins that inhibit West Nile virus and dengue virus infections. J Virol 2010; 84:8332–8341 [View Article]
     [Google Scholar]
  38. Szretter KJ, Brien JD, Thackray LB, Virgin HW, Cresswell P et al. The interferon-inducible gene viperin restricts West Nile virus pathogenesis. J Virol 2011; 85:11557–11566 [View Article]
     [Google Scholar]
  39. Chan YL, Chang TH, Liao CL, Lin YL. The cellular antiviral protein viperin is attenuated by proteasome-mediated protein degradation in Japanese encephalitis virus-infected cells. J Virol 2008; 82:10455–10464 [View Article]
     [Google Scholar]
  40. Chin KC, Cresswell P, Viperin CP. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci USA 2001; 98:15125–15130 [View Article]
     [Google Scholar]
  41. Nasr N, Maddocks S, Turville SG, Harman AN, Woolger N et al. Hiv-1 infection of human macrophages directly induces viperin which inhibits viral production. Blood 2012; 120:778–788 [View Article]
     [Google Scholar]
  42. Teng TS, Foo SS, Simamarta D, Lum FM, Teo TH et al. Viperin restricts Chikungunya virus replication and pathology. J Clin Invest 2012; 122:4447–4460 [View Article]
     [Google Scholar]
  43. Singh PK, Khatri I, Jha A, Pretto CD, Spindler KR et al. Determination of system level alterations in host transcriptome due to Zika virus (ZIKV) infection in retinal pigment epithelium. Sci Rep 2018; 8:11209 [View Article]
     [Google Scholar]
  44. Smith JR, Todd S, Ashander LM, Charitou T, Ma Y et al. Retinal pigment epithelial cells are a potential reservoir for Ebola virus in the human eye. Transl Vis Sci Technol 2017; 6:12 [View Article]
     [Google Scholar]
  45. Stirnweiss A, Ksienzyk A, Klages K, Rand U, Grashoff M et al. Ifn regulatory factor-1 bypasses IFN-mediated antiviral effects through viperin gene induction. J.i. 2010; 184:5179–5185 [View Article]
     [Google Scholar]
  46. Zhao Z, Yang M, Azar SR, Soong L, Weaver SC et al. Viral retinopathy in experimental models of Zika infection. Invest Ophthalmol Vis Sci 2017; 58:4355–4365 [View Article]
     [Google Scholar]
  47. Voigt V, Andoniou CE, Schuster IS, Oszmiana A, Ong ML et al. Cytomegalovirus establishes a latent reservoir and triggers long-lasting inflammation in the eye. PLoS Pathog 2018; 14:e1007040 [View Article]
     [Google Scholar]
  48. Heo WI, Lee KE, Hong JY, Kim MN, Oh MS et al. The role of interleukin-17 in mouse models of atopic dermatitis and contact dermatitis. Clin Exp Dermatol 2015; 40:665–671 [View Article]
     [Google Scholar]
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Dengue virus infects the mouse eye following systemic or intracranial infection and induces inflammatory responses
J. Gen. Virol. 101, 79 (2020); https://doi.org/10.1099/jgv.0.001354
/content/journal/jgv/10.1099/jgv.0.001354
/content/journal/jgv/10.1099/jgv.0.001354
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