1887

Abstract

Sampling the complete organ instead of defined parts might affect analysis at both the cellular and transcriptional levels. We defined host responses to H9N2 avian influenza virus (AIV) in trachea and different parts of the lung. Chickens were spray-inoculated with either saline or H9N2 AIV. Trachea and lung were sampled at 1 and 3 days post-inoculation (p.i.) for immunocytochemistry, real-time quantitative RT-PCR and gene-expression profiling. The trachea was divided into upper and lower parts and the lung into four segments, according to anatomy and airflow. Two segments contained the primary and secondary bronchi, cranial versus caudal (parts L1 and L3), and two segments contained the tertiary bronchi, cranial versus caudal (parts L2 and L4). Between the upper and lower trachea in both control and infected birds, minor differences in gene expression and host responses were found. In the lung of control birds, differences in anatomy were reflected in gene expression, and in the lung of infected birds, virus deposition enhanced the differences in gene expression. Differential gene expression in trachea and lung suggested common responses to a wide range of agents and site-specific responses. In trachea, site-specific responses were related to heat shock and lysozyme activity. In lung L1, which contained most virus, site-specific responses were related to genes involved in innate responses, interleukin activity and endocytosis. Our study indicates that the anatomy of the chicken lung must be taken into account when investigating responses to respiratory virus infections.

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2009-09-01
2019-11-13
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References

  1. Ariaans, M. P., Matthijs, M. G., van Haarlem, D., van de Haar, P., van Eck, J. H., Hensen, E. J. & Vervelde, L. ( 2008; ). The role of phagocytic cells in enhanced susceptibility of broilers to colibacillosis after infectious bronchitis virus infection. Vet Immunol Immunopathol 123, 240–250.[CrossRef]
    [Google Scholar]
  2. Baas, T., Baskin, C. R., Diamond, D. L., Garcia-Sastre, A., Bielefeldt-Ohmann, H., Tumpey, T. M., Thomas, M. J., Carter, V. S., Teal, T. H. & other authors ( 2006; ). Integrated molecular signature of disease: analysis of influenza virus-infected macaques through functional genomics and proteomics. J Virol 80, 10813–10828.[CrossRef]
    [Google Scholar]
  3. Baskin, C. R., García-Sastre, A., Tumpey, T. M., Bielefeldt-Ohmann, H., Carter, V. S., Nistal-Villán, E. & Katze, M. G. ( 2004; ). Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J Virol 78, 10420–10432.[CrossRef]
    [Google Scholar]
  4. Breed, D. G., Carr, P. & Vermeulen, A. N. ( 1996; ). Differential binding of two monoclonal antibodies directed against the chicken CD8α molecule. Vet Immunol Immunopathol 52, 117–125.[CrossRef]
    [Google Scholar]
  5. Chong, K. T., Thangavel, R. R. & Tang, X. ( 2008; ). Enhanced expression of murine β-defensins (MBD-1, -2,- 3, and -4) in upper and lower airway mucosa of influenza virus infected mice. Virology 380, 136–143.[CrossRef]
    [Google Scholar]
  6. Corbanie, E. A., Matthijs, M. G., van Eck, J. H., Remon, J. P., Landman, W. J. & Vervaet, C. ( 2006; ). Deposition of differently sized airborne microspheres in the respiratory tract of chickens. Avian Pathol 35, 475–485.[CrossRef]
    [Google Scholar]
  7. Degen, W. G., Smith, J., Simmelink, B., Glass, E. J., Burt, D. W. & Schijns, V. E. ( 2006; ). Molecular immunophenotyping of lungs and spleens in control and vaccinated chickens early after pulmonary avian influenza A (H9N2) virus infection. Vaccine 24, 6096–6109.[CrossRef]
    [Google Scholar]
  8. Eldaghayes, I., Rothwell, L., Williams, A., Withers, D., Balu, S., Davison, F. & Kaiser, P. ( 2006; ). Infectious bursal disease virus: strains that differ in virulence differentially modulate the innate immune response to infection in the chicken bursa. Viral Immunol 19, 83–91.[CrossRef]
    [Google Scholar]
  9. Etchart, N., Baaten, B., Andersen, S. R., Hyland, L., Wong, S. Y. & Hou, S. ( 2006; ). Intranasal immunisation with inactivated RSV and bacterial adjuvants induces mucosal protection and abrogates eosinophilia upon challenge. Eur J Immunol 36, 1136–1144.[CrossRef]
    [Google Scholar]
  10. Fagerland, J. A. & Arp, L. H. ( 1993; ). Structure and development of bronchus-associated lymphoid tissue in conventionally reared broiler chickens. Avian Dis 37, 10–18.[CrossRef]
    [Google Scholar]
  11. Fedde, M. R. ( 1998; ). Relationship of structure and function of the avian respiratory system to disease susceptibility. Poult Sci 77, 1130–1138.[CrossRef]
    [Google Scholar]
  12. Hayter, R. B. & Besch, E. L. ( 1974; ). Airborne-particle deposition in the respiratory tract of chickens. Poult Sci 53, 1507–1511.[CrossRef]
    [Google Scholar]
  13. Hogenkamp, A., Isohadouten, N., Reemers, S. S., Romijn, R. A., Hemrika, W., White, M. R., Tefsen, B., Vervelde, L., van Eijk, M. & other authors ( 2008; ). Chicken lung lectin is a functional C-type lectin and inhibits haemagglutination by influenza A virus. Vet Microbiol 130, 37–46.[CrossRef]
    [Google Scholar]
  14. Jenkins, K. A., Lowenthal, J. W., Kimpton, W. & Bean, A. G. ( 2009; ). The in vitro and in ovo responses of chickens to TLR9 subfamily ligands. Dev Comp Immunol 33, 660–667.[CrossRef]
    [Google Scholar]
  15. Jenner, R. G. & Young, R. A. ( 2005; ). Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 3, 281–294.[CrossRef]
    [Google Scholar]
  16. Karpala, A. J., Lowenthal, J. W. & Bean, A. G. ( 2008; ). Activation of the TLR3 pathway regulates IFNβ production in chickens. Dev Comp Immunol 32, 435–444.[CrossRef]
    [Google Scholar]
  17. Kash, J. C., Basler, C. F., García-Sastre, A., Carter, V., Billharz, R., Swayne, D. E., Przygodzki, R. M., Taubenberger, J. K., Katze, M. G. & Tumpey, T. M. ( 2004; ). Global host immune response: pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J Virol 78, 9499–9511.[CrossRef]
    [Google Scholar]
  18. Kothlow, S. & Kaspers, B. ( 2008; ). The avian respiratory immune system. In Avian Immunology, 1st edn, pp. 273–288. Edited by F. Davison, B. Kaspers & K. Schat. London: Academic Press.
  19. Lakadamyali, M., Rust, M. J. & Zhuang, X. ( 2004; ). Endocytosis of influenza viruses. Microbes Infect 6, 929–936.[CrossRef]
    [Google Scholar]
  20. Liang, B., Hyland, L. & Hou, S. ( 2001; ). Nasal-associated lymphoid tissue is a site of long-term virus-specific antibody production following respiratory virus infection of mice. J Virol 75, 5416–5420.[CrossRef]
    [Google Scholar]
  21. Luhtala, M., Tregaskes, C. A., Young, J. R. & Vainio, O. ( 1997; ). Polymorphism of chicken CD8-α, but not CD8-β. Immunogenetics 46, 396–401.[CrossRef]
    [Google Scholar]
  22. Mast, J., Goddeeris, B. M., Peeters, K., Vandesande, F. & Berghman, L. R. ( 1998; ). Characterisation of chicken monocytes, macrophages and interdigitating cells by the monoclonal antibody KUL01. Vet Immunol Immunopathol 61, 343–357.[CrossRef]
    [Google Scholar]
  23. Matthijs, M. G., Ariaans, M. P., Dwars, R. M., van Eck, J. H., Bouma, A., Stegeman, A. & Vervelde, L. ( 2009; ). Course of infection and immune responses in the respiratory tract of IBV infected broilers after superinfection with E. coli. Vet Immunol Immunopathol 127, 77–84.[CrossRef]
    [Google Scholar]
  24. Mensah, G. A. & Brain, J. D. ( 1982; ). Deposition and clearance of inhaled aerosol in the respiratory tract of chickens. J Appl Physiol 53, 1423–1428.
    [Google Scholar]
  25. Miettinen, M., Sareneva, T., Julkunen, I. & Matikainen, S. ( 2001; ). IFNs activate Toll-like receptor gene expression in viral infections. Genes Immun 2, 349–355.[CrossRef]
    [Google Scholar]
  26. Nili, H. & Asasi, K. ( 2002; ). Natural cases and an experimental study of H9N2 avian influenza in commercial broiler chickens of Iran. Avian Pathol 31, 247–252.[CrossRef]
    [Google Scholar]
  27. Pennings, J. L., Kimman, T. G. & Janssen, R. ( 2008; ). Identification of a common gene expression response in different lung inflammatory diseases in rodents and macaques. PLoS One 3, e2596 [CrossRef]
    [Google Scholar]
  28. Perkins, L. E. & Swayne, D. E. ( 2002; ). Susceptibility of laughing gulls (Larus atricilla) to H5N1 and H5N3 highly pathogenic avian influenza viruses. Avian Dis 46, 877–885.[CrossRef]
    [Google Scholar]
  29. Philbin, V. J., Iqbal, M., Boyd, Y., Goodchild, M. J., Beal, R. K., Bumstead, N., Young, J. & Smith, A. L. ( 2005; ). Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 114, 507–521.[CrossRef]
    [Google Scholar]
  30. Reading, P. C., Bozza, S., Gilbertson, B., Tate, M., Moretti, S., Job, E. R., Crouch, E. C., Brooks, A. G., Brown, L. E. & other authors ( 2008; ). Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J Immunol 180, 3391–3398.[CrossRef]
    [Google Scholar]
  31. Roepman, P., Wessels, L. F., Kettelarij, N., Kemmeren, P., Miles, A. J., Lijnzaad, P., Tilanus, M. G., Koole, R., Hordijk, G. J. & other authors ( 2005; ). An expression profile for diagnosis of lymph node metastases from primary head and neck squamous cell carcinomas. Nat Genet 37, 182–186.[CrossRef]
    [Google Scholar]
  32. Russell, P. H. & Koch, G. ( 1993; ). Local antibody forming cell responses to the Hitchner B1 and Ulster strains of Newcastle disease virus. Vet Immunol Immunopathol 37, 165–180.[CrossRef]
    [Google Scholar]
  33. Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N. & Kawaoka, Y. ( 2006; ). Avian flu: influenza virus receptors in the human airway. Nature 440, 435–436.[CrossRef]
    [Google Scholar]
  34. Van Alstine, W. G. & Arp, L. H. ( 1988; ). Histologic evaluation of lung and bronchus-associated lymphoid tissue in young turkeys infected with Bordetella avium. Am J Vet Res 49, 835–839.
    [Google Scholar]
  35. Van de Peppel, J., Kemmeren, P., van Bakel, H., Radonjic, M., van Leenen, D. & Holstege, F. C. ( 2003; ). Monitoring global messenger RNA changes in externally controlled microarray experiments. EMBO Rep 4, 387–393.[CrossRef]
    [Google Scholar]
  36. Van Ginkel, F. W., van Santen, V. L., Gulley, S. L. & Toro, H. ( 2008; ). Infectious bronchitis virus in the chicken Harderian gland and lachrymal fluid: viral load, infectivity, immune cell responses, and effects of viral immunodeficiency. Avian Dis 52, 608–617.[CrossRef]
    [Google Scholar]
  37. Van Riel, D., Munster, V. J., de Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D. & Kuiken, T. ( 2007; ). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171, 1215–1223.[CrossRef]
    [Google Scholar]
  38. Vervelde, L., Vermeulen, A. N. & Jeurissen, S. H. ( 1996; ). In situ characterization of leucocyte subpopulations after infection with Eimeria tenella in chickens. Parasite Immunol 18, 247–256.[CrossRef]
    [Google Scholar]
  39. Wan, H. & Perez, D. R. ( 2005; ). Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 346, 278–286.
    [Google Scholar]
  40. Withers, D. R., Young, J. R. & Davison, T. F. ( 2005; ). Infectious bursal disease virus-induced immunosuppression in the chick is associated with the presence of undifferentiated follicles in the recovering bursa. Viral Immunol 18, 127–137.[CrossRef]
    [Google Scholar]
  41. Wu, H., Kerr, M., Cui, X. & Churchill, G. ( 2003; ). maanova: a software package for the analysis of spotted cDNA microarray experiments. In The Analysis of Gene Expression Data: Methods and Software, pp. 313–341. Edited by G. Parmigiani, E. S. Garrett, R. A. Irizarry & S. L. Zeger. New York: Springer.
  42. Xing, Z., Cardona, C. J., Li, J., Dao, N., Tran, T. & Andrada, J. ( 2008; ). Modulation of the immune responses in chickens by low-pathogenicity avian influenza virus H9N2. J Gen Virol 89, 1288–1299.[CrossRef]
    [Google Scholar]
  43. Yang, Y. H., Dudoit, S., Luu, P., Lin, D. M., Peng, V., Ngai, J. & Speed, T. P. ( 2002; ). Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30, e15 [CrossRef]
    [Google Scholar]
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vol. , part 9, pp. 2134 –2146

Expression of immune-related genes induced by H9N2 infection in upper trachea at 3 days p.i.

Expression of immune-related genes induced by H9N2 infection in lung L1 at 3 days p.i.

Expression of immune-related genes induced by H9N2 infection in lung L4 at 3 days p.i.

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