Abstract
Inflammatory responses are an important part of the innate immune response during viral infection. Various inflammasome complexes have been identified. The pyrin domain-containing 3 (NLRP3) inflammasome plays a critical role in detecting some RNA viruses, such as influenza virus. However, the effect of the NLRP3 inflammasome on infectious bursal disease virus (IBDV) replication is still unclear. Here, we report that IBDV-infection induces the transcription of NLRP3 inflammasome and IL-1β genes in the immortalized chicken embryo fibroblast cell line DF-1. Inhibition of caspase-1 by Belnacasan (VX-765) suppressed the transcription of IL-1β, reduced cell lysis, and significantly promoted IBDV replication in DF-1 cells. Furthermore, knockdown of NLRP3 by small interfering RNA promoted IBDV replication in the host cells. Thus, IBDV can induce NLRP3 inflammasome activation in DF-1 cells through a mechanism requiring viral replication, revealing a new antiviral mechanism employed by the host.
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Abbreviations
- IBDV:
-
Infectious bursal disease virus
- VX-765:
-
Belnacasan
- LDH:
-
Lactate dehydrogenase
- RNAi:
-
RNA interference
References
Abdul-Careem MF, Hunter BD, Lee LF, Fairbrother JH, Haghighi HR, Read L, Parvizi P, Heidari M, Sharif S (2008) Host responses in the bursa of Fabricius of chickens infected with virulent Marek’s disease virus. Virology 379:256–265
Azad AA, Barrett SA, Fahey KJ (1985) The characterization and molecular cloning of the double-stranded RNA genome of an Australian strain of infectious bursal disease virus. Virology 143:35–44
Barber MR, Aldridge JJ, Webster RG, Magor KE (2010) Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci USA 107:5913–5918
Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, Fernandes-Alnemri T, Wu J, Monks BG, Fitzgerald KA, Hornung V, Latz E (2009) Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 183:787–791
Becker CE, O’Neill LA (2007) Inflammasomes in inflammatory disorders: the role of TLRs and their interactions with NLRs. Semin Immunopathol 29:239–248
Bergsbaken T, Fink SL, Cookson BT (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7:99–109
Bowie AG, Fitzgerald KA (2007) RIG-I: tri-ing to discriminate between self and non-self RNA. Trends Immunol 28:147–150
Brodsky IE, Medzhitov R (2011) Pyroptosis: macrophage suicide exposes hidden invaders. Curr Biol 21:R72–R75
Burdette D, Haskett A, Presser L, McRae S, Iqbal J, Waris G (2012) Hepatitis C virus activates interleukin-1beta via caspase-1-inflammasome complex. J Gen Virol 93:235–246
Da CL, Outlioua A, Anginot A, Akarid K, Arnoult D (2019) RNA viruses promote activation of the NLRP3 inflammasome through cytopathogenic effect-induced potassium efflux. Cell Death Dis 10:346
Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O, Hunt PW, Hatano H, Sowinski S, Munoz-Arias I, Greene WC (2014) Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505:509–514
Ermler ME, Traylor Z, Patel K, Schattgen SA, Vanaja SK, Fitzgerald KA, Hise AG (2014) Rift Valley fever virus infection induces activation of the NLRP3 inflammasome. Virology 449:174–180
Fahey KJ, Erny K, Crooks J (1989) A conformational immunogen on VP-2 of infectious bursal disease virus that induces virus-neutralizing antibodies that passively protect chickens. J Gen Virol 70(Pt 6):1473–1481
Fink SL, Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73:1907–1916
Fink SL, Cookson BT (2006) Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8:1812–1825
Fink SL, Bergsbaken T, Cookson BT (2008) Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA 105:4312–4317
Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, Latz E, Fitzgerald KA (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514–518
Hu B, Zhang Y, Jia L, Wu H, Fan C, Sun Y, Ye C, Liao M, Zhou J (2015) Binding of the pathogen receptor HSP90AA1 to avibirnavirus VP2 induces autophagy by inactivating the AKT-MTOR pathway. Autophagy 11:503–515
Ito M, Yanagi Y, Ichinohe T (2012) Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. Plos Pathog 8:e1002857
Kayagaki N, Stowe IB, Lee BL, O’Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526:666–671
Lawrence TM, Hudacek AW, de Zoete MR, Flavell RA, Schnell MJ (2013) Rabies virus is recognized by the NLRP3 inflammasome and activates interleukin-1beta release in murine dendritic cells. J Virol 87:5848–5857
Le Bourhis L, Benko S, Girardin SE (2007) Nod1 and Nod2 in innate immunity and human inflammatory disorders. Biochem Soc Trans 35:1479–1484
Lee CC, Wu CC, Lin TL (2012) Characterization of chicken melanoma differentiation-associated gene 5 (MDA5) from alternative translation initiation. Comp Immunol Microbiol Infect Dis 35:335–343
Li YP, Handberg KJ, Juul-Madsen HR, Zhang MF, Jorgensen PH (2007) Transcriptional profiles of chicken embryo cell cultures following infection with infectious bursal disease virus. Arch Virol 152:463–478
Li Z, Wang Y, Xue Y, Li X, Cao H, Zheng SJ (2012) Critical role for voltage-dependent anion channel 2 in infectious bursal disease virus-induced apoptosis in host cells via interaction with VP5. J Virol 86:1328–1338
Liu A, Li H, Qi X, Wang Q, Yang B, Wu T, Yan N, Li Y, Pan Q, Gao Y, Gao L, Liu C, Zhang Y, Cui H, Li K, Wang Y, Wang X (2019) Macrophage migration inhibitory factor triggers inflammatory responses during very virulent infectious bursal disease virus infection. Front Microbiol 10:2225
Liu H, Zhang M, Han H, Yuan J, Li Z (2010) Comparison of the expression of cytokine genes in the bursal tissues of the chickens following challenge with infectious bursal disease viruses of varying virulence. Virol J 7:364
Lupfer C, Malik A, Kanneganti TD (2015) Inflammasome control of viral infection. Curr Opin Virol 12:38–46
Müller H, Islam MR, Raue R (2003) Research on infectious bursal disease—the past, the present and the future. Vet Microbiol 97:153–165
Nielsen OL, Sorensen P, Hedemand JE, Laursen SB, Jorgensen PH (1998) Inflammatory response of different chicken lines and B haplotypes to infection with infectious bursal disease virus. Avian Pathol 27:181–189
O’Neill AM, Livant EJ, Ewald SJ (2010) Interferon alpha-induced inhibition of infectious bursal disease virus in chicken embryo fibroblast cultures differing in Mx genotype. Avian Dis 54:802–806
Palsson-McDermott EM, O’Neill LA (2007) Building an immune system from nine domains. Biochem Soc Trans 35:1437–1444
Petrilli V, Dostert C, Muruve DA, Tschopp J (2007) The inflammasome: a danger sensing complex triggering innate immunity. Curr Opin Immunol 19:615–622
Ragland WL, Novak R, El-Attrache J, Savic V, Ester K (2002) Chicken anemia virus and infectious bursal disease virus interfere with transcription of chicken IFN-alpha and IFN-gamma mRNA. J Interferon Cytokine Res 22:437–441
Rajan JV, Rodriguez D, Miao EA, Aderem A (2011) The NLRP3 inflammasome detects encephalomyocarditis virus and vesicular stomatitis virus infection. J Virol 85:4167–4172
Rasoli M, Yeap SK, Tan SW, Roohani K, Kristeen-Teo YW, Alitheen NB, Rahaman YA, Aini I, Bejo MH, Kaiser P, Omar AR (2015) Differential modulation of immune response and cytokine profiles in the bursae and spleen of chickens infected with very virulent infectious bursal disease virus. Bmc Vet Res 11:75
Sharma JM, Kim I, Rautenschlein S, Yeh H (2000) Infectious bursal disease virus of chickens: pathogenesis and immunosuppression. Dev Comp Immunol 24:223–235
Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526:660–665
Takeuchi O, Akira S (2009) Innate immunity to virus infection. Immunol Rev 227:75–86
Tan TY, Chu JJ (2013) Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1beta secretion and pyroptosis. J Gen Virol 94:2215–2220
Xu ZY, Yu Y, Liu Y, Ou CB, Zhang YH, Liu TY, Wang QX, Ma JY (2019) Differential expression of pro-inflammatory and anti-inflammatory genes of layer chicken bursa after experimental infection with infectious bursal disease virus. Poult Sci 98:5307–5314
Zhang L, Hu TJ, Liu HL, Shuai XH (2011) Inhibitory effect of Sargassum polysaccharide on oxidative stress induced by infectious bursa disease virus in chicken bursal lymphocytes. Int J Biol Macromol 49:607–615
Zhang Y, Zheng Y (2016) Effects and mechanisms of potent caspase-1 inhibitor VX765 treatment on collagen-induced arthritis in mice. Clin Exp Rheumatol 34:111–118
Acknowledgements
The authors thank Drs. Jue Liu and Wenhai Feng for their generous assistance. This work was supported in part by grants from the National Natural Science Foundation of China (31402172) and the Beijing Municipal Commission of Education for Science and Technology Development (D161100001516001). The funders had no role in the study design, data collection and analysis, or in deciding to prepare or publish this manuscript.
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He, Z., Ma, Y., Wu, D. et al. Protective effects of the NLRP3 inflammasome against infectious bursal disease virus replication in DF-1 cells. Arch Virol 166, 1943–1950 (2021). https://doi.org/10.1007/s00705-021-05099-7
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DOI: https://doi.org/10.1007/s00705-021-05099-7