1887

Abstract

Infectious bursal disease virus (IBDV) belongs to the family Birnaviridae and is economically important to the poultry industry worldwide. IBDV infects B cells in the bursa of Fabricius (BF), causing immunosuppression and morbidity in young chickens. In addition to strains that cause classical Gumboro disease, the so-called ‘very virulent’ (vv) strain, also in circulation, causes more severe disease and increased mortality. IBDV has traditionally been controlled through the use of live attenuated vaccines, with attenuation resulting from serial passage in non-lymphoid cells. However, the factors that contribute to the vv or attenuated phenotypes are poorly understood. In order to address this, we aimed to investigate host cell–IBDV interactions using a recently described chicken primary B-cell model, where chicken B cells are harvested from the BF and cultured ex vivo in the presence of chicken CD40L. We demonstrated that these cells could support the replication of IBDV when infected ex vivo in the laboratory. Furthermore, we evaluated the gene expression profiles of B cells infected with an attenuated strain (D78) and a very virulent strain (UK661) by microarray. We found that key genes involved in B-cell activation and signalling (TNFSF13B, CD72 and GRAP) were down-regulated following infection relative to mock, which we speculate could contribute to IBDV-mediated immunosuppression. Moreover, cells responded to infection by expressing antiviral type I IFNs and IFN-stimulated genes, but the induction was far less pronounced upon infection with UK661, which we speculate could contribute to its virulence.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000979
2017-11-20
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/12/2918.html?itemId=/content/journal/jgv/10.1099/jgv.0.000979&mimeType=html&fmt=ahah

References

  1. Thornton PK. Livestock production: recent trends, future prospects. Philos Trans R Soc Lond B Biol Sci 2010; 365: 2853– 2867 [CrossRef] [PubMed]
    [Google Scholar]
  2. Hoerr FJ. Clinical aspects of immunosuppression in poultry. Avian Dis 2010; 54: 2– 15 [CrossRef] [PubMed]
    [Google Scholar]
  3. Cazaban C, Gardin Y, Rv O. Gumboro disease- a persisting problem. CEVA 2017; 4
    [Google Scholar]
  4. Ingrao F, Rauw F, Lambrecht B, van den Berg T. Infectious bursal disease: a complex host-pathogen interaction. Dev Comp Immunol 2013; 41: 429– 438 [CrossRef] [PubMed]
    [Google Scholar]
  5. van den Berg TP, Eterradossi N, Toquin D, Meulemans G. Infectious bursal disease (Gumboro disease). Rev Sci Tech 2000; 19: 509– 543 [PubMed] [Crossref]
    [Google Scholar]
  6. Müller H, Mundt E, Eterradossi N, Islam MR. Current status of vaccines against infectious bursal disease. Avian Pathol 2012; 41: 133– 139 [CrossRef] [PubMed]
    [Google Scholar]
  7. Heine HG, Haritou M, Failla P, Fahey K, Azad A. Sequence analysis and expression of the host-protective immunogen VP2 of a variant strain of infectious bursal disease virus which can circumvent vaccination with standard type I strains. J Gen Virol 1991; 72: 1835– 1843 [CrossRef] [PubMed]
    [Google Scholar]
  8. Snyder DB, Lana DP, Savage PK, Yancey FS, Mengel SA et al. Differentiation of infectious bursal disease viruses directly from infected tissues with neutralizing monoclonal antibodies: evidence of a major antigenic shift in recent field isolates. Avian Dis 1988; 32: 535– 539 [CrossRef] [PubMed]
    [Google Scholar]
  9. Brown MD, Green P, Skinner MA. VP2 sequences of recent European 'very virulent' isolates of infectious bursal disease virus are closely related to each other but are distinct from those of 'classical' strains. J Gen Virol 1994; 75: 675– 680 [CrossRef] [PubMed]
    [Google Scholar]
  10. Brown MD, Skinner MA. Coding sequences of both genome segments of a European 'very virulent' infectious bursal disease virus. Virus Res 1996; 40: 1– 15 [CrossRef] [PubMed]
    [Google Scholar]
  11. Schermuly J, Greco A, Härtle S, Osterrieder N, Kaufer BB et al. In vitro model for lytic replication, latency, and transformation of an oncogenic alphaherpesvirus. Proc Natl Acad Sci USA 2015; 112: 7279– 7284 [CrossRef] [PubMed]
    [Google Scholar]
  12. Guo X, Wang L, Cui D, Ruan W, Liu F et al. Differential expression of the Toll-like receptor pathway and related genes of chicken bursa after experimental infection with infectious bursa disease virus. Arch Virol 2012; 157: 2189– 2199 [CrossRef] [PubMed]
    [Google Scholar]
  13. He X, Chen Y, Kang S, Chen G, Wei P. Differential regulation of chTLR3 by infectious bursal disease viruses with different virulence in vitro and in vivo. Viral Immunol 2017; 30: 490– 499 [CrossRef] [PubMed]
    [Google Scholar]
  14. Ou C, Wang Q, Zhang Y, Kong W, Zhang S et al. Transcription profiles of the responses of chicken bursae of Fabricius to IBDV in different timing phases. Virol J 2017; 14: 93 [CrossRef] [PubMed]
    [Google Scholar]
  15. Rasoli M, Yeap SK, Tan SW, Roohani K, Kristeen-Teo YW et al. 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 2015; 11: 75 [CrossRef] [PubMed]
    [Google Scholar]
  16. Ruby T, Whittaker C, Withers DR, Chelbi-Alix MK, Morin V et al. Transcriptional profiling reveals a possible role for the timing of the inflammatory response in determining susceptibility to a viral infection. J Virol 2006; 80: 9207– 9216 [CrossRef] [PubMed]
    [Google Scholar]
  17. Smith J, Sadeyen JR, Butter C, Kaiser P, Burt DW. Analysis of the early immune response to infection by infectious bursal disease virus in chickens differing in their resistance to the disease. J Virol 2015; 89: 2469– 2482 [CrossRef] [PubMed]
    [Google Scholar]
  18. Tregaskes CA, Glansbeek HL, Gill AC, Hunt LG, Burnside J et al. Conservation of biological properties of the CD40 ligand, CD154 in a non-mammalian vertebrate. Dev Comp Immunol 2005; 29: 361– 374 [CrossRef] [PubMed]
    [Google Scholar]
  19. Kothlow S, Morgenroth I, Tregaskes CA, Kaspers B, Young JR. CD40 ligand supports the long-term maintenance and differentiation of chicken B cells in culture. Dev Comp Immunol 2008; 32: 1015– 1026 [CrossRef] [PubMed]
    [Google Scholar]
  20. Terasaki K, Hirayama H, Kasanga CJ, Maw MT, Ohya K et al. Chicken B lymphoma DT40 cells as a useful tool for in vitro analysis of pathogenic infectious bursal disease virus. J Vet Med Sci 2008; 70: 407– 410 [CrossRef] [PubMed]
    [Google Scholar]
  21. Masuda T, Wada Y, Kawamura S. ES1 is a mitochondrial enlarging factor contributing to form mega-mitochondria in zebrafish cones. Sci Rep 2016; 6: 22360 [CrossRef] [PubMed]
    [Google Scholar]
  22. Sun L, Hua Y, Vergarajauregui S, Diab HI, Puertollano R. Novel role of TRPML2 in the regulation of the innate immune response. J Immunol 2015; 195: 4922– 4932 [CrossRef] [PubMed]
    [Google Scholar]
  23. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011; 1: 519– 525 [CrossRef] [PubMed]
    [Google Scholar]
  24. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011; 472: 481– 485 [CrossRef] [PubMed]
    [Google Scholar]
  25. Li L, Sevinsky JR, Rowland MD, Bundy JL, Stephenson JL et al. Proteomic analysis reveals virus-specific Hsp25 modulation in cardiac myocytes. J Proteome Res 2010; 9: 2460– 2471 [CrossRef] [PubMed]
    [Google Scholar]
  26. Giotis ES, Robey RC, Skinner NG, Tomlinson CD, Goodbourn S et al. Chicken interferome: avian interferon-stimulated genes identified by microarray and RNA-seq of primary chick embryo fibroblasts treated with a chicken type I interferon (IFN-α). Vet Res 2016; 47: 75 [CrossRef] [PubMed]
    [Google Scholar]
  27. Cui P, Ma SJ, Zhang YG, Li XS, Gao XY et al. Genomic sequence analysis of a new reassortant infectious bursal disease virus from commercial broiler flocks in Central China. Arch Virol 2013; 158: 1973– 1978 [CrossRef] [PubMed]
    [Google Scholar]
  28. Kasanga CJ, Yamaguchi T, Munang'andu HM, Ohya K, Fukushi H. Genomic sequence of an infectious bursal disease virus isolate from Zambia: classical attenuated segment B reassortment in nature with existing very virulent segment A. Arch Virol 2013; 158: 685– 689 [CrossRef] [PubMed]
    [Google Scholar]
  29. Kurukulsuriya S, Ahmed KA, Ojkic D, Gunawardana T, Gupta A et al. Circulating strains of variant infectious bursal disease virus may pose a challenge for antibiotic-free chicken farming in Canada. Res Vet Sci 2016; 108: 54– 59 [CrossRef] [PubMed]
    [Google Scholar]
  30. Phillips RA, Opitz HM. Pathogenicity and persistence of Salmonella enteritidis and egg contamination in normal and infectious bursal disease virus-infected leghorn chicks. Avian Dis 1995; 39: 778– 787 [CrossRef] [PubMed]
    [Google Scholar]
  31. Subler KA, Mickael CS, Jackwood DJ. Infectious bursal disease virus-induced immunosuppression exacerbates Campylobacter jejuni colonization and shedding in chickens. Avian Dis 2006; 50: 179– 184 [CrossRef] [PubMed]
    [Google Scholar]
  32. Chaudhry M, Rashid HB, Thrusfield M, Welburn S, Bronsvoort BM. A case-control study to identify risk factors associated with avian influenza subtype H9N2 on commercial poultry farms in Pakistan. PLoS One 2015; 10: e0119019 [CrossRef] [PubMed]
    [Google Scholar]
  33. Motamed N, Mayahi M, Seifi MR, Jafari RA. Effect of infectious bursal disease virus on pathogenicity of avian influenza virus subtype H9N2 in broiler chicks. J Vet Med Anim Health 2013; 5: 276– 280
    [Google Scholar]
  34. Ramirez-Nieto G, Shivaprasad HL, Kim CH, Lillehoj HS, Song H et al. Adaptation of a mallard H5N2 low pathogenicity influenza virus in chickens with prior history of infection with infectious bursal disease virus. Avian Dis 2010; 54: 513– 521 [CrossRef] [PubMed]
    [Google Scholar]
  35. Hui RK, Leung FC. Differential Expression Profile of Chicken Embryo Fibroblast DF-1 Cells Infected with Cell-Adapted Infectious Bursal Disease Virus. PLoS One 2015; 10: e0111771 [CrossRef] [PubMed]
    [Google Scholar]
  36. Li YP, Handberg KJ, Juul-Madsen HR, Zhang MF, Jørgensen PH. Transcriptional profiles of chicken embryo cell cultures following infection with infectious bursal disease virus. Arch Virol 2007; 152: 463– 478 [CrossRef] [PubMed]
    [Google Scholar]
  37. Lin J, Xia J, Zhang K, Yang Q. Genome-wide profiling of chicken dendritic cell response to infectious bursal disease. BMC Genomics 2016; 17: 878 [CrossRef] [PubMed]
    [Google Scholar]
  38. Quan R, Zhu S, Wei L, Wang J, Yan X et al. Transcriptional profiles in bursal B-lymphoid DT40 cells infected with very virulent infectious bursal disease virus. Virol J 2017; 14: 7 [CrossRef] [PubMed]
    [Google Scholar]
  39. Wong RT, Hon CC, Zeng F, Leung FC. Screening of differentially expressed transcripts in infectious bursal disease virus-induced apoptotic chicken embryonic fibroblasts by using cDNA microarrays. J Gen Virol 2007; 88: 1785– 1796 [CrossRef] [PubMed]
    [Google Scholar]
  40. Soubies SM, Courtillon C, Abed M, Amelot M, Keita A et al. Propagation and titration of infectious bursal disease virus, including non-cell-culture-adapted strains, using ex vivo stimulated chicken bursal cells. Avian Pathol 2017; 1– 28 [CrossRef] [PubMed]
    [Google Scholar]
  41. García-Bartolomé A, Peñas A, Marín-Buera L, Lobo-Jarne T, Pérez-Pérez R et al. Respiratory chain enzyme deficiency induces mitochondrial location of actin-binding gelsolin to modulate the oligomerization of VDAC complexes and cell survival. Hum Mol Genet 2017; 26: 2493– 2506 [CrossRef] [PubMed]
    [Google Scholar]
  42. Mackay F, Browning JL. BAFF: a fundamental survival factor for B cells. Nat Rev Immunol 2002; 2: 465– 475 [CrossRef] [PubMed]
    [Google Scholar]
  43. Lyu M, Hao Y, Li Y, Lyu C, Liu W et al. Upregulation of CD72 expression on CD19(+) CD27(+) memory B cells by CD40L in primary immune thrombocytopenia. Br J Haematol 2017; 178: 308– 318 [CrossRef] [PubMed]
    [Google Scholar]
  44. Wu HJ, Bondada S. CD72, a coreceptor with both positive and negative effects on B lymphocyte development and function. J Clin Immunol 2009; 29: 12– 21 [CrossRef] [PubMed]
    [Google Scholar]
  45. Feng GS, Ouyang YB, Hu DP, Shi ZQ, Gentz R et al. Grap is a novel SH3-SH2-SH3 adaptor protein that couples tyrosine kinases to the Ras pathway. J Biol Chem 1996; 271: 12129– 12132 [CrossRef] [PubMed]
    [Google Scholar]
  46. Fujiwara N, Hidano S, Mamada H, Ogasawara K, Kitamura D et al. A novel avian homologue of CD72, chB1r, down modulates BCR-mediated activation signals. Int Immunol 2006; 18: 775– 783 [CrossRef] [PubMed]
    [Google Scholar]
  47. Eldaghayes I, Rothwell L, Williams A, Withers D, Balu S et al. Infectious bursal disease virus: strains that differ in virulence differentially modulate the innate immune response to infection in the chicken bursa. Viral Immunol 2006; 19: 83– 91 [CrossRef] [PubMed]
    [Google Scholar]
  48. Ye C, Jia L, Sun Y, Hu B, Wang L et al. Inhibition of antiviral innate immunity by birnavirus VP3 protein via blockage of viral double-stranded RNA binding to the host cytoplasmic RNA detector MDA5. J Virol 2014; 88: 11154– 11165 [CrossRef] [PubMed]
    [Google Scholar]
  49. Li Z, Wang Y, Li X, Li X, Cao H et al. Critical roles of glucocorticoid-induced leucine zipper in infectious bursal disease virus (IBDV)-induced suppression of type I Interferon expression and enhancement of IBDV growth in host cells via interaction with VP4. J Virol 2013; 87: 1221– 1231 [CrossRef] [PubMed]
    [Google Scholar]
  50. Baba TW, Giroir BP, Humphries EH. Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology 1985; 144: 139– 151 [CrossRef] [PubMed]
    [Google Scholar]
  51. Wark K. ‘Expression and processing of infectious bursal diseases virus proteins’ PhD Thesis University of Hertfordshire: 2000
    [Google Scholar]
  52. Reed R, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg 1938; 27: 494– 497
    [Google Scholar]
  53. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C T method. Nat Protoc 2008; 3: 1101– 1108 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000979
Loading
/content/journal/jgv/10.1099/jgv.0.000979
Loading

Data & Media loading...

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error