Virologica Sinica

, Volume 31, Issue 1, pp 57–68 | Cite as

Responses of the Toll-like receptor and melanoma differentiation-associated protein 5 signaling pathways to avian infectious bronchitis virus infection in chicks

  • Yining He
  • Zhiwen Xie
  • Jinglong Dai
  • Yanjie Cao
  • Jinlian Hou
  • Yansheng Zheng
  • Tianchao Wei
  • Meilan Mo
  • Ping Wei
Research Article

Abstract

Avian infectious bronchitis virus (IBV) is a Gammacoronavirus in the family Coronaviridae and causes highly contagious respiratory disease in chickens. Innate immunity plays significant roles in host defense against IBV. Here, we explored the interaction between IBV and the host innate immune system. Severe histopathological lesions were observed in the tracheal mucosa at 3-5 days post inoculation (dpi) and in the kidney at 8 dpi, with heavy viral loads at 1-11 and 1-28 dpi, respectively. The expression of mRNAs encoding Toll-like receptor (TLR) 3 and TLR7 were upregulated at 3-8 dpi, and that of TIR-domain-containing adapter-inducing interferon (IFN) β (TRIF) was upregulated at 21 dpi in the trachea and kidney. Myeloid differentiation primary response protein 88 (MyD88) was upregulated in the trachea during early infection. Tumor necrosis factor receptor-associated factor (TRAF) 3 and TRAF6 were upregulated expression in both tissues. Moreover, melanoma differentiation-associated protein 5 (MDA5), laboratory of genetics and physiology 2 (LGP2), stimulator of IFN genes (STING), and mitochondrial antiviral signaling protein (MAVS), as well as TANK binding kinase 1 (TBK1), inhibitor of kappaB kinase (IKK) ε, IKKα, IKKβ, IFN regulatory factor (IRF) 7, nuclear factor of kappaB (NF-ĸB), IFN-α, IFN-β, various interleukins(ILs), and macrophage inflammatory protein-1β (MIP-1β) were significantly upregulated in the trachea and downregulated in the kidney. These results suggested that the TLR and MDA5 signaling pathways and innate immune cytokine were induced after IBV infection. Additionally, consistent responses to IBV infection were observed during early infection, with differential and complicated responses in the kidney.

Keywords

infectious bronchitis virus Toll-like receptor signal pathway melanoma differentiation-associated protein 5 signal pathway cytokines 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Awad F, Chhabra R, Baylis M, Ganapathy K. 2014. An overview of infectious bronchitis virus in chickens. World Poultry Sci J, 70: 375–383.CrossRefGoogle Scholar
  2. Benyeda Z, Mato T, Suveges T, Szabo E, Kardi V, Abonyi-Toth Z, Rusvai M, Palya V. 2009. Comparison of the pathogenicity of QX-like, M41 and 793/B infectious bronchitis strains from different pathological conditions. Avian Pathol, 38: 449–456.CrossRefPubMedGoogle Scholar
  3. Cao L, Ge X, Gao Y, Ren Y, Ren X, Li G. 2015. Porcine epidemic diarrhea virus infection induces NF-kappaB activation through the TLR2, TLR3 and TLR9 pathways in porcine intestinal epithelial cells. J Gen Virol, 96: 1757–1767.CrossRefPubMedGoogle Scholar
  4. Cavanagh D. 2005. Coronaviruses in poultry and other birds. Avian Pathol, 34: 439–448.CrossRefPubMedGoogle Scholar
  5. Cavanagh D. 2007. Coronavirus avian infectious bronchitis virus. Vet Res, 38: 281–297.CrossRefPubMedGoogle Scholar
  6. Chen L, Zhang T, Han Z, Liang S, Xu Y, Xu Q, Chen Y, Zhao Y, Shao Y, Li H, Wang K, Kong X, Liu S. 2015. Molecular and antigenic characteristics of Massachusetts genotype infectious bronchitis coronavirus in China. Vet Microbiol. 181: 241–251.CrossRefPubMedGoogle Scholar
  7. Cheng Y, Sun Y, Wang H, Yan Y, Ding C, Sun J. 2015. Chicken STING Mediates Activation of the IFN Gene Independently of the RIG-I Gene. J Immunol, 195: 3922–3936.CrossRefPubMedGoogle Scholar
  8. Chousalkar KK, Roberts JR, Reece R. 2007. Comparative histopathology of two serotypes of infectious bronchitis virus (T and n1/88) in laying hens and cockerels. Poult Sci, 86: 50–58.CrossRefPubMedGoogle Scholar
  9. Cong F, Liu X, Han Z, Shao Y, Kong X, Liu S. 2013. Transcriptome analysis of chicken kidney tissues following coronavirus avian infectious bronchitis virus infection. BMC Genomics, 14: 743.PubMedCentralCrossRefPubMedGoogle Scholar
  10. Cook JK, Jackwood M, Jones RC. 2012. The long view: 40 years of infectious bronchitis research. Avian Pathol, 41: 239–250.CrossRefPubMedGoogle Scholar
  11. Dar A, Tikoo S, Potter A, Babiuk LA, Townsend H, Gerdts V, Mutwiri G. 2014. CpG-ODNs induced changes in cytokine/chemokines genes expression associated with suppression of infectious bronchitis virus replication in chicken lungs. Vet Immunol Immunopathol, 160: 209–217.CrossRefPubMedGoogle Scholar
  12. Dosch SF, Mahajan SD, Collins AR. 2009. SARS coronavirus spike protein-induced innate immune response occurs via activation of the NF-kappaB pathway in human monocyte macrophages in vitro. Virus Res, 142: 19–27.PubMedCentralCrossRefPubMedGoogle Scholar
  13. Fan WQ, Wang HN, Zhang Y, Guan ZB, Wang T, Xu CW, Zhang AY, Yang X. 2012. Comparative dynamic distribution of avian infectious bronchitis virus M41, H120, and SAIBK strains by quantitative real-time RT-PCR in SPF chickens. Biosci Biotechnol Biochem, 76: 2255–2260.CrossRefPubMedGoogle Scholar
  14. Frieman M, Ratia K, Johnston RE, Mesecar AD, Baric RS. 2009. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J Virol, 83: 6689–6705.PubMedCentralCrossRefPubMedGoogle Scholar
  15. Guo X, Rosa AJ, Chen DG, Wang X. 2008. Molecular mechanisms of primary and secondary mucosal immunity using avian infectious bronchitis virus as a model system. Vet Immunol Immunopathol, 121: 332–343.CrossRefPubMedGoogle Scholar
  16. Ignjatovic J, Ashton DF, Reece R, Scott P, Hooper P. 2002. Pathogenicity of Australian strains of avian infectious bronchitis virus. J Comp Pathol, 126: 115–123.CrossRefPubMedGoogle Scholar
  17. Jang H, Koo BS, Jeon EO, Lee HR, Lee SM, Mo IP. 2013. Altered pro-inflammatory cytokine mRNA levels in chickens infected with infectious bronchitis virus. Poult Sci, 92: 2290–2298.CrossRefPubMedGoogle Scholar
  18. Kameka AM, Haddadi S, Kim DS, Cork SC, Abdul-Careem MF. 2014. Induction of innate immune response following infectious bronchitis corona virus infection in the respiratory tract of chickens. Virology, 450–451: 114–121.CrossRefPubMedGoogle Scholar
  19. Karpala AJ, Lowenthal JW, Bean AG. 2008. Activation of the TLR3 pathway regulates IFNbeta production in chickens. Dev Comp Immunol, 32: 435–444.CrossRefPubMedGoogle Scholar
  20. Kawasaki T, Kawai T. 2014. Toll-Like Receptor Signaling Pathways. Front Immunol, 5: 46.CrossRefGoogle Scholar
  21. Kint J, Fernandez-Gutierrez M, Maier HJ, Britton P, Langereis MA, Koumans J, Wiegertjes GF, Forlenza M. 2015. Activation of the Chicken Type I Interferon Response by Infectious Bronchitis Coronavirus. J Virol, 89: 1156–1167.PubMedCentralCrossRefPubMedGoogle Scholar
  22. Law HK, Cheung CY, Sia SF, Chan YO, Peiris JS, Lau YL. 2009. Toll-like receptors, chemokine receptors and death receptor ligands responses in SARS coronavirus infected human monocyte derived dendritic cells. BMC Immunol, 10: 35.PubMedCentralCrossRefPubMedGoogle Scholar
  23. Li M, Jiang JJ, He K, Sun XK, Liang XB, Zhang YQ, Liang YD, Mo ML, Wei TC, W P. 2012. The detection and comparative analysis of antibodies IB in clinical serum samples using the self-developed Indirect N-ELISA kits. Guangxi J Animal Husb Vet Med, 28: 195–197. (In Chinese)Google Scholar
  24. Li M, Wang XY, Wei P, Chen QY, Wei ZJ, Mo ML. 2012. Serotype and genotype diversity of infectious bronchitis viruses isolated during 1985-2008 in Guangxi, China. Arch Virol, 157: 467–474.CrossRefPubMedGoogle Scholar
  25. Liniger M, Summerfield A, Zimmer G, McCullough KC, Ruggli N. 2011. Chicken Cells Sense Influenza A Virus Infection through MDA5 and CARDIF Signaling Involving LGP2. J Virol, 86: 705–717.CrossRefPubMedGoogle Scholar
  26. Li J, Liu Y, Zhang X. 2010. Murine Coronavirus Induces Type I Interferon in Oligodendrocytes through Recognition by RIG-I and MDA5. J Virol, 84: 6472–6482.PubMedCentralCrossRefPubMedGoogle Scholar
  27. Li Y, Bang D, Handberg K, Jorgensen P, Zhang M. 2005. Evaluation of the suitability of six host genes as internal control in real-time RT-PCR assays in chicken embryo cell cultures infected with infectious bursal disease virus. Vet Microbiol, 110: 155–165.CrossRefPubMedGoogle Scholar
  28. Mazaleuskaya L, Veltrop R, Ikpeze N, Martin-Garcia J, Navas-Martin S. 2012. Protective role of Toll-like Receptor 3-induced type I interferon in murine coronavirus infection of macrophages. Viruses, 4: 901–923.PubMedCentralCrossRefPubMedGoogle Scholar
  29. Mo ML, Cheng QY, Hou JL, Fan WS, Li M, Wei P, Wei TC, Wei ZJ. 2011. Development of a real-time PCR assay for detection of infectious bronchitis virus. China Poultry, 41: 193–198. (In Chinese)Google Scholar
  30. Mo ML, Li M, Huang BC, Fan WS, Wei P, Wei TC, Cheng QY, Wei ZJ, Lang YH. 2013. Molecular characterization of major structural protein genes of avian coronavirus infectious bronchitis virus isolates in southern china. Viruses, 5: 3007–3020.PubMedCentralCrossRefPubMedGoogle Scholar
  31. Mogensen TH. 2009. Pathogen Recognition and Inflammatory Signaling in Innate Immune Defenses. Clin Microbiol Rev, 22: 240.PubMedCentralCrossRefPubMedGoogle Scholar
  32. Nakhaei P, Genin P, Civas A, Hiscott J. 2009. RIG-I-like receptors: sensing and responding to RNA virus infection. Semin Immunol, 21:215–222.CrossRefPubMedGoogle Scholar
  33. Nii T, Isobe N, Yoshimura Y. 2014. Effects of avian infectious bronchitis virus antigen on eggshell formation and immunoreaction in hen oviduct. Theriogenology, 81: 1129–1138.CrossRefPubMedGoogle Scholar
  34. Okino CH, Santos IL, Fernando FS, Alessi AC, Wang X, Montassier HJ. 2014. Inflammatory and cell-mediated immune responses in the respiratory tract of chickens to infection with avian infectious bronchitis virus. Viral Immunol, 27: 383–391.CrossRefPubMedGoogle Scholar
  35. Panda S, Nilsson JA, Gekara NO. 2015. Deubiquitinase MYSM1 Regulates Innate Immunity through Inactivation of TRAF3 and TRAF6 Complexes. Immunity, 43: 647–659.CrossRefPubMedGoogle Scholar
  36. Pfaffl MW, Horgan GW, Dempfle L. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res, 30: e36.PubMedCentralCrossRefPubMedGoogle Scholar
  37. Schalk AF, Hawn MC. 1931. An apparently new respiratory disease of baby chicks. J Am Vet Med Assoc, 78: 413–422.Google Scholar
  38. Sheahan T, Morrison TE, Funkhouser W, Uematsu S, Akira S, Baric RS, Heise MT. 2008. MyD88 is required for protection from lethal infection with a mouse-adapted SARS-CoV. PLoS Pathog, 4: e1000240.PubMedCentralCrossRefPubMedGoogle Scholar
  39. Shi CS, Qi HY, Boularan C, Huang NN, Abu-Asab M, Shelhamer JH, Kehrl JH. 2014. SARS-coronavirus open reading frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J Immunol, 193: 3080–3089.PubMedCentralCrossRefPubMedGoogle Scholar
  40. Smith J, Sadeyen J, Cavanagh D, Kaiser P, Burt DW. 2015. The early immune response to infection of chickens with Infectious Bronchitis Virus (IBV) in susceptible and resistant birds. BMC Vet Res, 11: 256.PubMedCentralCrossRefPubMedGoogle Scholar
  41. Sun L, Xing Y, Chen X, Zheng Y, Yang Y, Nichols DB, Clementz MA, Banach BS, Li K, Baker SC, Chen Z. 2012. Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS One, 7: e30802.PubMedCentralCrossRefPubMedGoogle Scholar
  42. Sun Y, Han M, Kim C, Calvert JG, Yoo D. 2012. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses, 4: 424–446.PubMedCentralCrossRefPubMedGoogle Scholar
  43. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol Rev, 227: 75–86.CrossRefPubMedGoogle Scholar
  44. Totura AL, Whitmore A, Agnihothram S, Schafer A, Katze MG, Heise MT, Baric RS. 2015. Toll-Like Receptor 3 Signaling via TRIF Contributes to a Protective Innate Immune Response to Severe Acute Respiratory Syndrome Coronavirus Infection. MBio, 6: e615–e638.Google Scholar
  45. Wickramasinghe INA, de Vries RP, Grone A, de Haan CAM, Verheije MH. 2011. Binding of Avian Coronavirus Spike Proteins to Host Factors Reflects Virus Tropism and Pathogenicity. J Virol, 85: 8903–8912.PubMedCentralCrossRefPubMedGoogle Scholar
  46. Wu B, Peisley A, Richards C, Yao H, Zeng X, Lin C, Chu F, Walz T, Hur S. 2013. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell, 152: 276–289.CrossRefPubMedGoogle Scholar
  47. Xu Y, Zhang T, Xu Q, Han Z, Liang S, Shao Y, Ma D, Liu S. 2015. Differential modulation of avian β-defensin and Toll-like receptor expression in chickens infected with infectious bronchitis virus. Appl Microbiol Biot, 99: 9011–9024.CrossRefGoogle Scholar
  48. Yu L, Jiang Y, Low S, Wang Z, Nam SJ, Liu W, Kwangac J. 2001. Characterization of three infectious bronchitis virus isolates from China associated with proventriculus in vaccinated chickens. Avian Dis, 45: 416–424.CrossRefPubMedGoogle Scholar
  49. Zhong Y, Tan YW, Liu DX. 2012. Recent progress in studies of arterivirus- and coronavirus-host interactions. Viruses, 4: 980–1010.PubMedCentralCrossRefPubMedGoogle Scholar
  50. Zou J, Chang M, Nie P, Secombes CJ. 2009. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol Biol, 9: 85.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer Science+Business Media Singapore 2016

Authors and Affiliations

  • Yining He
    • 1
  • Zhiwen Xie
    • 1
  • Jinglong Dai
    • 1
  • Yanjie Cao
    • 1
  • Jinlian Hou
    • 1
  • Yansheng Zheng
    • 1
  • Tianchao Wei
    • 1
  • Meilan Mo
    • 1
  • Ping Wei
    • 1
  1. 1.College of Animal Science and TechnologyGuangxi UniversityNanningChina

Personalised recommendations