Cellular Oxidative Stress Response Controls the Antiviral and Apoptotic Programs in Dengue Virus-Infected Dendritic Cells

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Olagnier, David ^a   Peri, Suraj ^b   Steel, Courtney ^a   van Montfoort, Nadine ^a   Chiang, Cindy ^a   Beljanski, Vladimir ^a   Slifker, Michael ^b   He, Zhong ^a   Nichols, Carmen N ^a   Lin, Rongtuan ^c   Balachandran, Siddharth ^b   Hiscott, John ^a  

^a Vaccine and Gene Therapy Institute   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD14 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROTEIN BCL X; PROTEIN NOXA; RANTES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STAT1 PROTEIN; T6 ANTIGEN; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA; IRF3 PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN;

ANTIOXIDANT ACTIVITY; ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DENDRITIC CELL; DENGUE VIRUS 2; DOWN REGULATION; FLOW CYTOMETRY; GENE REGULATORY NETWORK; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOBLOTTING; INNATE IMMUNITY; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS REPLICATION; CELL CULTURE; DENGUE VIRUS; GENE EXPRESSION PROFILING; IN VITRO STUDY; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ARTHROPODA; DENGUE VIRUS; FLAVIVIRUS;

APOPTOSIS; CELLS, CULTURED; DENDRITIC CELLS; DENGUE VIRUS; GENE EXPRESSION PROFILING; HUMANS; IMMUNITY, INNATE; IN VITRO TECHNIQUES; INTERFERON REGULATORY FACTOR-3; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; STAT1 TRANSCRIPTION FACTOR; VIRUS REPLICATION;

EID: 84919639950     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004566     Document Type: Article

References (79)

1. Rothman AL, (2011) Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nature reviews Immunology 11: 532–543.
2. Halstead SB, (2008) Dengue virus-mosquito interactions. Annu Rev Entomol 53: 273–291.
3. Wilder-Smith A, Ooi EE, Vasudevan SG, Gubler DJ, (2010) Update on dengue: epidemiology, virus evolution, antiviral drugs, and vaccine development. Curr Infect Dis Rep 12: 157–164.
4. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, et al. (2013) The global distribution and burden of dengue. Nature 496: 504–507.
5. Roche C, Cassar O, Laille M, Murgue B, (2007) Dengue-3 virus genomic differences that correlate with in vitro phenotype on a human cell line but not with disease severity. Microbes Infect 9: 63–69.
6. Silva RL, de Silva AM, Harris E, MacDonald GH, (2008) Genetic analysis of Dengue 3 virus subtype III 5′ and 3′ non-coding regions. Virus Res 135: 320–325.
7. Vasilakis N, Fokam EB, Hanson CT, Weinberg E, Sall AA, et al. (2008) Genetic and phenotypic characterization of sylvatic dengue virus type 2 strains. Virology 377: 296–307.
8. Zhou Y, Mammen MP, JrKlungthong C, Chinnawirotpisan P, Vaughn DW, et al. (2006) Comparative analysis reveals no consistent association between the secondary structure of the 3′-untranslated region of dengue viruses and disease syndrome. J Gen Virol 87: 2595–2603.
9. Shurtleff AC, Beasley DW, Chen JJ, Ni H, Suderman MT, et al. (2001) Genetic variation in the 3′ non-coding region of dengue viruses. Virology 281: 75–87.
10. Nasirudeen AM, Wong HH, Thien P, Xu S, Lam KP, et al. (2011) RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection. PLoS Negl Trop Dis 5: e926.
11. Sun P, Fernandez S, Marovich MA, Palmer DR, Celluzzi CM, et al. (2009) Functional characterization of ex vivo blood myeloid and plasmacytoid dendritic cells after infection with dengue virus. Virology 383: 207–215.
12. Tsai YT, Chang SY, Lee CN, Kao CL, (2009) Human TLR3 recognizes dengue virus and modulates viral replication in vitro. Cell Microbiol 11: 604–615.
13. Goubau D, Deddouche S, Reis e Sousa C, (2013) Cytosolic sensing of viruses. Immunity 38: 855–869.
14. Takeuchi O, Akira S, (2009) Innate immunity to virus infection. Immunol Rev 227: 75–86.
15. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805–820.
16. Wilkins C, Gale M, Jr (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22: 41–47.
17. Jaiyen Y, Masrinoul P, Kalayanarooj S, Pulmanausahakul R, Ubol S, (2009) Characteristics of dengue virus-infected peripheral blood mononuclear cell death that correlates with the severity of illness. Microbiol Immunol 53: 442–450.
18. Rada B, Leto TL, (2008) Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15: 164–187.
19. Gonzalez-Dosal R, Horan KA, Rahbek SH, Ichijo H, Chen ZJ, et al. (2011) HSV infection induces production of ROS, which potentiate signaling from pattern recognition receptors: role for S-glutathionylation of TRAF3 and 6. PLoS Pathog 7: e1002250.
20. Kim HJ, Kim CH, Ryu JH, Kim MJ, Park CY, et al. (2013) Reactive oxygen species induce antiviral innate immune response through IFN-lambda regulation in human nasal epithelial cells. Am J Respir Cell Mol Biol 49: 855–865.
21. Narayanan A, Amaya M, Voss K, Chung M, Benedict A, et al. (2014) Reactive oxygen species activate NFkappaB (p65) and p53 and induce apoptosis in RVFV infected liver cells. Virology 449: 270–286.
22. Soucy-Faulkner A, Mukawera E, Fink K, Martel A, Jouan L, et al. (2010) Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression. PLoS Pathog 6: e1000930.
23. Strengert M, Jennings R, Davanture S, Hayes P, Gabriel G, et al. (2013) Mucosal Reactive Oxygen Species Are Required for Antiviral Response: Role of Duox in Influenza A Virus Infection. Antioxid Redox Signal
24. Bryan HK, Olayanju A, Goldring CE, Park BK, (2013) The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem Pharmacol 85: 705–717.
25. Ma Q, (2013) Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 53: 401–426.
26. Ma Q, He X, (2012) Molecular basis of electrophilic and oxidative defense: promises and perils of Nrf2. Pharmacol Rev 64: 1055–1081.
27. Ibeh BO, Emeka-Nwabunnia IK, (2012) Increased oxidative stress condition found in different stages of HIV disease in patients undergoing antiretroviral therapy in Umuahia (Nigeria). Immunopharmacol Immunotoxicol 34: 1060–1066.
28. Isaguliants M, Smirnova O, Ivanov AV, Kilpelainen A, Kuzmenko Y, et al. (2013) Oxidative stress induced by HIV-1 reverse transcriptase modulates the enzyme's performance in gene immunization. Hum Vaccin Immunother 9: 2111–2119.
29. Kalinowska M, Bazdar DA, Lederman MM, Funderburg N, Sieg SF, (2013) Decreased IL-7 responsiveness is related to oxidative stress in HIV disease. PLoS One 8: e58764.
30. Lee YH, Lai CL, Hsieh SH, Shieh CC, Huang LM, et al. (2013) Influenza A virus induction of oxidative stress and MMP-9 is associated with severe lung pathology in a mouse model. Virus Res 178: 411–422.
31. Paracha UZ, Fatima K, Alqahtani M, Chaudhary A, Abuzenadah A, et al. (2013) Oxidative stress and hepatitis C virus. Virol J 10: 251.
32. Reddy PV, Agudelo M, Atluri VS, Nair MP, (2012) Inhibition of nuclear factor erythroid 2-related factor 2 exacerbates HIV-1 gp120-induced oxidative and inflammatory response: role in HIV associated neurocognitive disorder. Neurochem Res 37: 1697–1706.
33. Reddy PV, Gandhi N, Samikkannu T, Saiyed Z, Agudelo M, et al. (2012) HIV-1 gp120 induces antioxidant response element-mediated expression in primary astrocytes: role in HIV associated neurocognitive disorder. Neurochem Int 61: 807–814.
34. Cho HY, Imani F, Miller-DeGraff L, Walters D, Melendi GA, et al. (2009) Antiviral activity of Nrf2 in a murine model of respiratory syncytial virus disease. Am J Respir Crit Care Med 179: 138–150.
35. Garofalo RP, Kolli D, Casola A, (2013) Respiratory syncytial virus infection: mechanisms of redox control and novel therapeutic opportunities. Antioxid Redox Signal 18: 186–217.
36. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, et al. (2008) Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235–249.
37. Ivanov AV, Bartosch B, Smirnova OA, Isaguliants MG, Kochetkov SN, (2013) HCV and oxidative stress in the liver. Viruses 5: 439–469.
38. Ke PY, Chen SS, (2012) Hepatitis C virus and cellular stress response: implications to molecular pathogenesis of liver diseases. Viruses 4: 2251–2290.
39. Lin YL, Liu CC, Chuang JI, Lei HY, Yeh TM, et al. (2000) Involvement of oxidative stress, NF-IL-6, and RANTES expression in dengue-2-virus-infected human liver cells. Virology 276: 114–126.
40. Wang J, Chen Y, Gao N, Wang Y, Tian Y, et al. (2013) Inhibitory effect of glutathione on oxidative liver injury induced by dengue virus serotype 2 infections in mice. PLoS One 8: e55407.
41. Gil L, Martinez G, Tapanes R, Castro O, Gonzalez D, et al. (2004) Oxidative stress in adult dengue patients. Am J Trop Med Hyg 71: 652–657.
42. Seet RC, Lee CY, Lim EC, Quek AM, Yeo LL, et al. (2009) Oxidative damage in dengue fever. Free Radic Biol Med 47: 375–380.
43. Soundravally R, Hoti SL, Patil SA, Cleetus CC, Zachariah B, et al. (2014) Association between proinflammatory cytokines and lipid peroxidation in patients with severe dengue disease around defervescence. Int J Infect Dis 18: 68–72.
44. Soundravally R, Sankar P, Hoti SL, Selvaraj N, Bobby Z, et al. (2008) Oxidative stress induced changes in plasma protein can be a predictor of imminent severe dengue infection. Acta Trop 106: 156–161.
45. Al-Alimi AA, Ali SA, Al-Hassan FM, Idris FM, Teow SY, et al. (2014) Dengue virus type 2 (DENV2)-induced oxidative responses in monocytes from glucose-6-phosphate dehydrogenase (G6PD)-deficient and G6PD normal subjects. PLoS Negl Trop Dis 8: e2711.
46. Kwissa M, Nakaya HI, Onlamoon N, Wrammert J, Villinger F, et al. (2014) Dengue Virus Infection Induces Expansion of a CD14CD16 Monocyte Population that Stimulates Plasmablast Differentiation. Cell Host Microbe
47. Green S, Rothman A, (2006) Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis 19: 429–436.
48. Palucka AK, (2000) Dengue virus and dendritic cells. Nat Med 6: 748–749.
49. Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, et al. (2000) Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6: 816–820.
50. Nightingale ZD, Patkar C, Rothman AL, (2008) Viral replication and paracrine effects result in distinct, functional responses of dendritic cells following infection with dengue 2 virus. J Leukoc Biol 84: 1028–1038.
51. Aguirre S, Maestre AM, Pagni S, Patel JR, Savage T, et al. (2012) DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog 8: e1002934.
52. Yang Y, Bazhin AV, Werner J, Karakhanova S, (2013) Reactive oxygen species in the immune system. Int Rev Immunol 32: 249–270.
53. Ho LJ, Wang JJ, Shaio MF, Kao CL, Chang DM, et al. (2001) Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production. J Immunol 166: 1499–1506.
54. Libraty DH, Pichyangkul S, Ajariyakhajorn C, Endy TP, Ennis FA, (2001) Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis. J Virol 75: 3501–3508.
55. Rodriguez-Madoz JR, Bernal-Rubio D, Kaminski D, Boyd K, Fernandez-Sesma A, (2010) Dengue virus inhibits the production of type I interferon in primary human dendritic cells. Journal of virology 84: 4845–4850.
56. Boudreau HE, Emerson SU, Korzeniowska A, Jendrysik MA, Leto TL, (2009) Hepatitis C virus (HCV) proteins induce NADPH oxidase 4 expression in a transforming growth factor beta-dependent manner: a new contributor to HCV-induced oxidative stress. J Virol 83: 12934–12946.
57. Comstock AT, Ganesan S, Chattoraj A, Faris AN, Margolis BL, et al. (2011) Rhinovirus-induced barrier dysfunction in polarized airway epithelial cells is mediated by NADPH oxidase 1. J Virol 85: 6795–6808.
58. Song HY, Ju SM, Seo WY, Goh AR, Lee JK, et al. (2011) Nox2-based NADPH oxidase mediates HIV-1 Tat-induced up-regulation of VCAM-1/ICAM-1 and subsequent monocyte adhesion in human astrocytes. Free Radic Biol Med 50: 576–584.
59. Vilhardt F, Plastre O, Sawada M, Suzuki K, Wiznerowicz M, et al. (2002) The HIV-1 Nef protein and phagocyte NADPH oxidase activation. J Biol Chem 277: 42136–42143.
60. Wu RF, Ma Z, Myers DP, Terada LS, (2007) HIV-1 Tat activates dual Nox pathways leading to independent activation of ERK and JNK MAP kinases. J Biol Chem 282: 37412–37419.
61. Bureau C, Bernad J, Chaouche N, Orfila C, Beraud M, et al. (2001) Nonstructural 3 protein of hepatitis C virus triggers an oxidative burst in human monocytes via activation of NADPH oxidase. J Biol Chem 276: 23077–23083.
62. Lefevre L, Lugo-Villarino G, Meunier E, Valentin A, Olagnier D, et al. (2013) The C-type lectin receptors dectin-1, MR, and SIGNR3 contribute both positively and negatively to the macrophage response to Leishmania infantum. Immunity 38: 1038–1049.
63. Chen ST, Lin YL, Huang MT, Wu MF, Cheng SC, et al. (2008) CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453: 672–676.
64. Wu MF, Chen ST, Yang AH, Lin WW, Lin YL, et al. (2013) CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood 121: 95–106.
65. Yang CS, Kim JJ, Lee SJ, Hwang JH, Lee CH, et al. (2013) TLR3-triggered reactive oxygen species contribute to inflammatory responses by activating signal transducer and activator of transcription-1. J Immunol 190: 6368–6377.
66. Koarai A, Sugiura H, Yanagisawa S, Ichikawa T, Minakata Y, et al. (2010) Oxidative stress enhances toll-like receptor 3 response to double-stranded RNA in airway epithelial cells. Am J Respir Cell Mol Biol 42: 651–660.
67. To EE, Broughton BR, Hendricks KS, Vlahos R, Selemidis S, (2014) Influenza A virus and TLR7 activation potentiate NOX2 oxidase-dependent ROS production in macrophages. Free Radic Res 48: 940–947.
68. Indukuri H, Castro SM, Liao SM, Feeney LA, Dorsch M, et al. (2006) Ikkepsilon regulates viral-induced interferon regulatory factor-3 activation via a redox-sensitive pathway. Virology 353: 155–165.
69. Tal MC, Sasai M, Lee HK, Yordy B, Shadel GS, et al. (2009) Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci U S A 106: 2770–2775.
70. Edwards MR, Johnson B, Mire CE, Xu W, Shabman RS, et al. (2014) The Marburg virus VP24 protein interacts with Keap1 to activate the cytoprotective antioxidant response pathway. Cell Rep 6: 1017–1025.
71. Page A, Volchkova VA, Reid SP, Mateo M, Bagnaud-Baule A, et al. (2014) Marburgvirus hijacks nrf2-dependent pathway by targeting nrf2-negative regulator keap1. Cell Rep 6: 1026–1036.
72. Kosmider B, Messier EM, Janssen WJ, Nahreini P, Wang J, et al. (2012) Nrf2 protects human alveolar epithelial cells against injury induced by influenza A virus. Respir Res 13: 43.
73. Yageta Y, Ishii Y, Morishima Y, Masuko H, Ano S, et al. (2011) Role of Nrf2 in host defense against influenza virus in cigarette smoke-exposed mice. J Virol 85: 4679–4690.
74. Banchereau J, Steinman RM, (1998) Dendritic cells and the control of immunity. Nature 392: 245–252.
75. Luplertlop N, Misse D, Bray D, Deleuze V, Gonzalez JP, et al. (2006) Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep 7: 1176–1181.
76. Yang CM, Lee IT, Hsu RC, Chi PL, Hsiao LD, (2013) NADPH oxidase/ROS-dependent PYK2 activation is involved in TNF-alpha-induced matrix metalloproteinase-9 expression in rat heart-derived H9c2 cells. Toxicol Appl Pharmacol 272: 431–442.
77. Yu F, Kamada H, Niizuma K, Endo H, Chan PH, (2008) Induction of mmp-9 expression and endothelial injury by oxidative stress after spinal cord injury. J Neurotrauma 25: 184–195.
78. Yen YT, Chen HC, Lin YD, Shieh CC, Wu-Hsieh BA, (2008) Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virol 82: 12312–12324.
79. Olagnier D, Scholte FE, Chiang C, Albulescu IC, Nichols C, et al. (2014) Inhibition of dengue and chikungunya virus infections by RIG-I-mediated type I interferon-independent stimulation of the innate antiviral response. J Virol 88: 4180–4194.