Activation of Nrf2 by the dengue virus causes an increase in CLEC5A, which enhances TNF-α production by mononuclear phagocytes

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Cheng, Yi Lin ^a,b   Lin, Yee Shin ^a,b   Chen, Chia Ling ^c   Tsai, Tsung Ting ^d   Tsai, Cheng Chieh ^e   Wu, Yan Wei ^a,b   Ou, Yi Dan ^a   Chu, Yu Yi ^b   Wang, Ju Ming ^a,b   Yu, Chia Yi ^a   Lin, Chiou Feng ^b,d  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e CHUNG HWA UNIVERSITY OF MEDICAL TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CLEC5A PROTEIN, HUMAN; CLEC5A PROTEIN, MOUSE; LECTIN; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR; VIRAL PROTEIN;

ANIMAL; BIOSYNTHESIS; CELL LINE; CELL NUCLEUS; DENGUE VIRUS; GENETICS; HAMSTER; HUMAN; METABOLISM; MONOCYTE; MOUSE; NUCLEOCYTOPLASMIC TRANSPORT; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; VIROLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE; CELL NUCLEUS; CRICETINAE; DENGUE VIRUS; HUMANS; LECTINS, C-TYPE; MICE; MONOCYTES; NF-E2-RELATED FACTOR 2; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84984636083     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32000     Document Type: Article

References (64)

1. Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504-507, doi: 10.1038/nature12060 (2013).
2. Simmons, C. P., Farrar, J. J., Nguyen v, V. & Wills, B. Dengue. The New England journal of medicine 366, 1423-1432, doi: 10.1056/ NEJMra1110265 (2012).
3. Perera, R. & Kuhn, R. J. Structural proteomics of dengue virus. Current opinion in microbiology 11, 369-377, doi: 10.1016/j. mib.2008.06.004 (2008).
4. Diamond, M. S. & Pierson, T. C. Molecular Insight into Dengue Virus Pathogenesis and Its Implications for Disease Control. Cell 162, 488-492, doi: 10.1016/j.cell.2015.07.005 (2015).
5. Guzman, M. G. & Harris, E. Dengue. Lancet 385, 453-465, doi: 10.1016/S0140-6736(14)60572-9 (2015).
6. Back, A. T. & Lundkvist, A. Dengue viruses - an overview. Infection ecology & epidemiology 3, doi: 10.3402/iee.v3i0.19839 (2013).
7. Rothman, A. L. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 11, 532-543, doi: 10.1038/nri3014 (2011).
8. Chen, S. T. et al. CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453, 672-676, doi: 10.1038/nature07013 (2008).
9. Cheung, R. et al. Activation of MDL-1 (CLEC5A) on immature myeloid cells triggers lethal shock in mice. J Clin Invest 121, 4446-4461, doi: 10.1172/JCI57682 (2011).
10. Hoang, L. T. et al. The early whole-blood transcriptional signature of dengue virus and features associated with progression to dengue shock syndrome in Vietnamese children and young adults. Journal of virology 84, 12982-12994, doi: 10.1128/JVI.01224-10 (2010).
11. Morrison, J., Aguirre, S. & Fernandez-Sesma, A. Innate immunity evasion by Dengue virus. Viruses 4, 397-413, doi: 10.3390/ v4030397 (2012).
12. Tsai, Y. T., Chen, Y. H., Chang, D. M., Chen, P. C. & Lai, J. H. Janus kinase/signal transducer and activator of transcription 3 signaling pathway is crucial in chemokine production from hepatocytes infected by dengue virus. Exp Biol Med (Maywood) 236, 1156-1165, doi: 10.1258/ebm.2011.011060 (2011).
13. Li, L. L. et al. Positive transcription elongation factor b (P-TEFb) contributes to dengue virus-stimulated induction of interleukin-8 (IL-8). Cell Microbiol 12, 1589-1603, doi: 10.1111/j.1462-5822.2010.01493.x (2010).
14. Cheng, Y. L. et al. Dengue Virus Infection Causes the Activation of Distinct NF-kappaB Pathways for Inducible Nitric Oxide Synthase and TNF-alpha Expression in RAW264.7 Cells. Mediators Inflamm 2015, 274025, doi: 10.1155/2015/274025 (2015).
15. Hirotsu, Y. et al. Nrf2-MafG heterodimers contribute globally to antioxidant and metabolic networks. Nucleic acids research 40, 10228-10239, doi: 10.1093/nar/gks827 (2012).
16. Katze, M. G., He, Y. & Gale, M. Jr. Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2, 675-687, doi: 10.1038/nri888 (2002).
17. Wang, X. J., Hayes, J. D., Henderson, C. J. & Wolf, C. R. Identification of retinoic acid as an inhibitor of transcription factor Nrf2 through activation of retinoic acid receptor alpha. Proceedings of the National Academy of Sciences of the United States of America 104, 19589-19594, doi: 10.1073/pnas.0709483104 (2007).
18. Pena, J. & Harris, E. Dengue virus modulates the unfolded protein response in a time-dependent manner. The Journal of biological chemistry 286, 14226-14236, doi: 10.1074/jbc.M111.222703 (2011).
19. Urano, F. et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666 (2000).
20. Nishitoh, H. et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes & development 16, 1345-1355, doi: 10.1101/gad.992302 (2002).
21. Cullinan, S. B. et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Molecular and cellular biology 23, 7198-7209 (2003).
22. Digaleh, H., Kiaei, M. & Khodagholi, F. Nrf2 and Nrf1 signaling and ER stress crosstalk: implication for proteasomal degradation and autophagy. Cell Mol Life Sci 70, 4681-4694, doi: 10.1007/s00018-013-1409-y (2013).
23. Yu, C. Y., Hsu, Y. W., Liao, C. L. & Lin, Y. L. Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. Journal of virology 80, 11868-11880, doi: 10.1128/JVI.00879-06 (2006).
24. Tsai, T. T. et al. Microglia retard dengue virus-induced acute viral encephalitis. Sci Rep 6, 27670, doi: 10.1038/srep27670 (2016).
25. Edwards, M. J., Heniford, B. T. & Miller, F. N. Tumor necrosis factor mediates disseminated intravascular inflammation (DII) in the genesis of multiple organ edema. J Surg Res 54, 140-144, doi: 10.1006/jsre.1993.1022 (1993).
26. Hober, D., Delannoy, A. S., Benyoucef, S., De Groote, D. & Wattre, P. High levels of sTNFR p75 and TNF alpha in dengue-infected patients. Microbiol Immunol 40, 569-573 (1996).
27. Chakravarti, A. & Kumaria, R. Circulating levels of tumour necrosis factor-alpha & interferon-gamma in patients with dengue & dengue haemorrhagic fever during an outbreak. Indian J Med Res 123, 25-30 (2006).
28. Chunhakan, S., Butthep, P., Yoksan, S., Tangnararatchakit, K. & Chuansumrit, A. Vascular leakage in dengue hemorrhagic Fever is associated with dengue infected monocytes, monocyte activation/exhaustion, and cytokines production. Int J Vasc Med 2015, 917143, doi: 10.1155/2015/917143 (2015).
29. Cardier, J. E. et al. Proinflammatory factors present in sera from patients with acute dengue infection induce activation and apoptosis of human microvascular endothelial cells: possible role of TNF-alpha in endothelial cell damage in dengue. Cytokine 30, 359-365, doi: 10.1016/j.cyto.2005.01.021 (2005).
30. Fernandez-Mestre, M. T., Gendzekhadze, K., Rivas-Vetencourt, P. & Layrisse, Z. TNF-alpha-308A allele, a possible severity risk factor of hemorrhagic manifestation in dengue fever patients. Tissue Antigens 64, 469-472, doi: 10.1111/j.1399-0039.2004.00304.x (2004).
31. Yen, Y. T., Chen, H. C., Lin, Y. D., Shieh, C. C. & Wu-Hsieh, B. A. Enhancement by tumor necrosis factor alpha of dengue virusinduced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. Journal of virology 82, 12312-12324, doi: 10.1128/JVI.00968-08 (2008).
32. Chen, H. C., Hofman, F. M., Kung, J. T., Lin, Y. D. & Wu-Hsieh, B. A. Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. Journal of virology 81, 5518-5526, doi: 10.1128/ JVI.02575-06 (2007).
33. Atrasheuskaya, A., Petzelbauer, P., Fredeking, T. M. & Ignatyev, G. Anti-TNF antibody treatment reduces mortality in experimental dengue virus infection. FEMS Immunol Med Microbiol 35, 33-42 (2003).
34. Shresta, S., Sharar, K. L., Prigozhin, D. M., Beatty, P. R. & Harris, E. Murine model for dengue virus-induced lethal disease with increased vascular permeability. Journal of virology 80, 10208-10217, doi: 10.1128/JVI.00062-06 (2006).
35. Modhiran, N. et al. Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci Transl Med 7, 304ra142, doi: 10.1126/scitranslmed.aaa3863 (2015).
36. Chen, J., Ng, M. M. & Chu, J. J. Activation of TLR2 and TLR6 by Dengue NS1 Protein and Its Implications in the Immunopathogenesis of Dengue Virus Infection. PLoS Pathog 11, e1005053, doi: 10.1371/journal.ppat.1005053 (2015).
37. Nasirudeen, A. M. et al. RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection. PLoS Negl Trop Dis 5, e926, doi: 10.1371/journal.pntd.0000926 (2011).
38. Nagila, A. et al. Inhibition of p38MAPK and CD137 signaling reduce dengue virus-induced TNF-alpha secretion and apoptosis. Virol J 10, 105, doi: 10.1186/1743-422X-10-105 (2013).
39. Wu, M. F. et al. CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood 121, 95-106, doi: 10.1182/blood-2012-05-430090 (2013).
40. Chen, S. T. et al. CLEC5A regulates Japanese encephalitis virus-induced neuroinflammation and lethality. PLoS Pathog 8, e1002655, doi: 10.1371/journal.ppat.1002655 (2012).
41. Batliner, J. et al. CLEC5A (MDL-1) is a novel PU.1 transcriptional target during myeloid differentiation. Mol Immunol 48, 714-719, doi: 10.1016/j.molimm.2010.10.016 (2011).
42. Ma, Q. Role of nrf2 in oxidative stress and toxicity. Annual review of pharmacology and toxicology 53, 401-426, doi: 10.1146/ annurev-pharmtox-011112-140320 (2013).
43. Kensler, T. W., Wakabayashi, N. & Biswal, S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annual review of pharmacology and toxicology 47, 89-116, doi: 10.1146/annurev.pharmtox.46.120604.141046 (2007).
44. Deramaudt, T. B., Dill, C. & Bonay, M. Regulation of oxidative stress by Nrf2 in the pathophysiology of infectious diseases. Med Mal Infect 43, 100-107, doi: 10.1016/j.medmal.2013.02.004 (2013).
45. Yu, C. Y. et al. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathog 8, e1002780, doi: 10.1371/journal.ppat.1002780 (2012).
46. Aguirre, S. et al. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog 8, e1002934, doi: 10.1371/journal.ppat.1002934 (2012).
47. Rodriguez-Madoz, J. R. et al. Inhibition of the type I interferon response in human dendritic cells by dengue virus infection requires a catalytically active NS2B3 complex. Journal of virology 84, 9760-9774, doi: 10.1128/JVI.01051-10 (2010).
48. de-Oliveira-Pinto, L. M. et al. Profile of circulating levels of IL-1Ra, CXCL10/IP-10, CCL4/MIP-1beta and CCL2/MCP-1 in dengue fever and parvovirosis. Mem Inst Oswaldo Cruz 107, 48-56 (2012).
49. Lin, J. C. et al. Dengue viral protease interaction with NF-kappaB inhibitor alpha/beta results in endothelial cell apoptosis and hemorrhage development. Journal of immunology 193, 1258-1267, doi: 10.4049/jimmunol.1302675 (2014).
50. Olagnier, D. et al. Cellular oxidative stress response controls the antiviral and apoptotic programs in dengue virus-infected dendritic cells. PLoS Pathog 10, e1004566, doi: 10.1371/journal.ppat.1004566 (2014).
51. Cho, H. Y. et al. Antiviral activity of Nrf2 in a murine model of respiratory syncytial virus disease. American journal of respiratory and critical care medicine 179, 138-150, doi: 10.1164/rccm.200804-535OC (2009).
52. Kosmider, B. et al. Nrf2 protects human alveolar epithelial cells against injury induced by influenza A virus. Respiratory research 13, 43, doi: 10.1186/1465-9921-13-43 (2012).
53. Schachtele, S. J., Hu, S. & Lokensgard, J. R. Modulation of experimental herpes encephalitis-associated neurotoxicity through sulforaphane treatment. PloS one 7, e36216, doi: 10.1371/journal.pone.0036216 (2012).
54. Schaedler, S. et al. Hepatitis B virus induces expression of antioxidant response element-regulated genes by activation of Nrf2. The Journal of biological chemistry 285, 41074-41086, doi: 10.1074/jbc.M110.145862 (2010).
55. Burdette, D., Olivarez, M. & Waris, G. Activation of transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway. The Journal of general virology 91, 681-690, doi: 10.1099/vir.0.014340-0 (2010).
56. Page, A. et al. Marburgvirus hijacks nrf2-dependent pathway by targeting nrf2-negative regulator keap1. Cell reports 6, 1026-1036, doi: 10.1016/j.celrep.2014.02.027 (2014).
57. McLean, J. E., Wudzinska, A., Datan, E., Quaglino, D. & Zakeri, Z. Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. The Journal of biological chemistry 286, 22147-22159, doi: 10.1074/jbc.M110.192500 (2011).
58. Sessions, O. M. et al. Host cell transcriptome profile during wild-type and attenuated dengue virus infection. PLoS Negl Trop Dis 7, e2107, doi: 10.1371/journal.pntd.0002107 (2013).
59. Fink, J. et al. Host gene expression profiling of dengue virus infection in cell lines and patients. PLoS Negl Trop Dis 1, e86, doi: 10.1371/journal.pntd.0000086 (2007).
60. Simmons, C. P. et al. Patterns of host genome-wide gene transcript abundance in the peripheral blood of patients with acute dengue hemorrhagic fever. The Journal of infectious diseases 195, 1097-1107, doi: 10.1086/512162 (2007).
61. Fernandez-Garcia, M. D., Mazzon, M., Jacobs, M. & Amara, A. Pathogenesis of flavivirus infections: using and abusing the host cell. Cell Host Microbe 5, 318-328, doi: 10.1016/j.chom.2009.04.001 (2009).
62. Sessions, O. M. et al. Discovery of insect and human dengue virus host factors. Nature 458, 1047-1050, doi: 10.1038/nature07967 (2009).
63. Krishnan, M. N. & Garcia-Blanco, M. A. Targeting host factors to treat West Nile and dengue viral infections. Viruses 6, 683-708, doi: 10.3390/v6020683 (2014).
64. Hsieh, C. Y. et al. Inhibiting glycogen synthase kinase-3 decreases 12-O-tetradecanoylphorbol-13-acetate-induced interferongamma- mediated skin inflammation. The Journal of pharmacology and experimental therapeutics 343, 125-133, doi: 10.1124/ jpet.112.194100 (2012).