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  • 1 Directorate of Veterinary Medicinal Products, Budapest, Hungary
  • Ceva-Phylaxia Co. Ltd., Szállás u. 5, H-1107 Budapest, Hungary
  • 2 Semmelweis University, Budapest, Hungary
  • 3 Prophyl Ltd., Mohács, Hungary
  • 4 Veterinary Diagnostic Directorate, Budapest, Hungary
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The aim of this immunocytochemical study was to compare mannose-binding lectin (MBL) production induced by avian coronavirus in the spleen and caecal tonsil (CT). One-day-old specific-pathogen-free (SPF) chickens were experimentally infected with six QX field isolates and the H120 vaccine strain. In the negative control birds, the spleen was MBL negative, while the CT showed scattered MBL-positive cells in close proximity and within the surface epithelium and germinal centre (GC)-like cell clusters. MBL was detectable in the ellipsoid-associated cells (EACs) and cell clusters in the periarterial lymphoid sheath (PALS) by 7 days post infection (dpi). In both organs, the MBL-positive cells occupy antigen-exposed areas, indicating that GC formation depends on resident precursors of dendritic cells. The majority of MBL-positive EACs express the CD83 antigen, providing evidence that coronavirus infection facilitated the maturation of dendritic cell precursors. Surprisingly, co-localisation of MBL and CD83 was not detectable in the CT. In the spleen (associated with circulation), the EACs producing MBL and expressing CD83 are a common precursor of both follicular (FDC) and interdigitating dendritic cells (IDC). In the CT (gut-associated lymphoid tissue, GALT) the precursors of FDC and IDC are MBL-producing cells and CD83-positive cells, respectively. In the CT the two separate precursors of lymphoid dendritic cells provide some ‘autonomy’ for the GALT.

  • Ambali, A. G. and Jones, R. C. (1990): Early pathogenesis in chicks of infection with an enterotropic strain of infectious bronchitis virus. Avian Dis. 34, 809817.

    • Search Google Scholar
    • Export Citation
  • Bódi, I., Minkó, K., Molnár, D., Nagy, N. and Oláh, I. (2015): A novel aspect of the structure of the avian thymic medulla. Cell and Tissue Res. 359, 489501.

    • Search Google Scholar
    • Export Citation
  • Cavanagh, D. (2007): Coronavirus avian infectious bronchitis virus. Vet. Res. 38, 281297.

  • Cook, J. K. A. (1971): Recovery of infectious bronchitis virus from eggs and chicks produced by experimentally inoculated hens. J. Comp. Pathol. 81, 203211.

    • Search Google Scholar
    • Export Citation
  • Cumming, R. B. (1962): The etiology of uraemia of chickens. Aust. Vet. J. 38, 554.

  • Dalgaard, T., Skovgaard, K., Norup, L. R., Pleidrup, J., Permin, A., Schou, T. W., Vadekar, D. F., Jungersen, G. and Juul-Madsen, H. R. (2015): Immune gene expression in the spleen of chickens experimentally infected with Ascaridia galli. Vet. Immunol. Immunopathol. 164, 7986.

    • Search Google Scholar
    • Export Citation
  • Dhinakar Raj, G. and Jones, R. C. (1997): Infectious bronchitis virus: Immunopathogenesis of infection in the chicken. Avian Pathol. 26, 677706.

    • Search Google Scholar
    • Export Citation
  • Farsang, A., Bódi, I., Fölker, O., Minkó, K., Benyeda, Zs., Bálint, Á., Kiss, L. A. and Oláh, I. (2018): Coronavirus infection retards the development of the cortico-medullary capillary network in the bursa of Fabricius of chicken. Acta Vet. Hung. 66, 2027.

    • Search Google Scholar
    • Export Citation
  • Flores-Romo, L. (2001): In vivo maturation and migration of dendritic cells. Immunology 102, 255262.

  • Gelb, J. Jr., Lunt, R. L., Metz, A. L. and Fries, P. A. (1991): Attenuation of avian infectious bronchitis virus by cold adaptation. Avian Dis. 35, 847853.

    • Search Google Scholar
    • Export Citation
  • Gunn, M. D. (2003): Chemokine mediated control of dendritic cell migration and function. Semin. Immunol. 15, 271276.

  • Hamzić, E., Kjarup, R. B., Mach, N., Minozzi, G., Strozzi, F., Gualdi, V., Williams, J. L., Chen, J., Wattrang, E., Buitenhuis, B., Juul-Madsen, H. R. and Dalgaard, T. S. (2016): RNA sequencing-based analysis of the spleen transcriptome following infectious bronchitis virus infection of chickens selected for different mannose-binding lectin serum concentrations. BMC Genomics 17, 82.

    • Search Google Scholar
    • Export Citation
  • Hansell, C., Zhu, X. W., Brooks, H., Sheppard, M., Withanage, S., Maskell, D. and McConnell, I. (2007): Unique features and distribution of the chicken CD83+ cell. J. Immunol. 179, 51175125.

    • Search Google Scholar
    • Export Citation
  • Hock, B. D., Kato, M., McKenzie, J. L. and Hart, D. N. (2001): A soluble form of CD83 is released from activated dendritic cells and B lymphocytes, and is detectable in normal human sera. Int. Immunol. 13, 959967.

    • Search Google Scholar
    • Export Citation
  • Igyártó, B. Z., Magyar, A. and Oláh, I. (2007): Origin of follicular dendritic cell in the chicken spleen. Cell and Tissue Res. 327, 8392.

    • Search Google Scholar
    • Export Citation
  • Igyártó, B. Z., Nagy, N., Magyar, A. and Oláh, I. (2008): Identification of the avian B-cell-specific Bu1 alloantigen by a novel monoclonal antibody. Poult. Sci. 87, 351355.

    • Search Google Scholar
    • Export Citation
  • Jeurissen, S. and Janse, E. M. (1996): The microenvironment of the chicken immune system. In: Davison, T. F., Morris, T. R. and Payne, L. N. (eds) Poultry Immunology. Poultry Science Symposium Series, Vol. 24. Carfax Publishing Company, Abingdon. pp. 4766.

    • Search Google Scholar
    • Export Citation
  • Jeurissen, S., Claassen, E. and Janse, E. M. (1992): Histological and functional differentiation of non-lymphoid cells in the chicken spleen. Immunology 77, 7580.

    • Search Google Scholar
    • Export Citation
  • Kinde, H., Daft, B. M., Castro, A. E., Bickford, A. A., Gelb, J. and Reynolds, B. (1991): Viral pathogenesis of a nephrotropic infectious bronchitis virus isolated from commercial pullets. Avian Dis. 35, 415421.

    • Search Google Scholar
    • Export Citation
  • Kiss, I., Mató, T., Homonnay, Z. G., Kojer, J., Farsang, A., Bálint, Á. and Palya, V. (2015): Survey indicates circulation of 4/91 and QX-type infectious bronchitis viruses in Hungary in 2014 – Short communication. Acta Vet. Hung. 63, 382388.

    • Search Google Scholar
    • Export Citation
  • Kjaerup, R. M., Dalgaard, T. S., Norup, L. R., Bergman, I. M., Sorensen, P. and Juul-Madsen, H. R. (2013): Adjuvant effects of mannose-binding lectin ligands on the immune response to infectious bronchitis vaccine in chickens with high or low serum mannose-binding lectin concentrations. Immunobiology 219, 263274.

    • Search Google Scholar
    • Export Citation
  • Kjaerup, R. M., Dalgaard, T. S., Norup, L. R., Hamzic, E., Sorensen, P. and Juul-Madsen, H. R. (2014): Characterization of cellular and humoral immune responses after IBV infection in chicken lines differing in MBL serum concentration. Viral Immunol. 27, 529542.

    • Search Google Scholar
    • Export Citation
  • Lambrechts, C., Pensaert, M. and Ducatelle, R. (1993): Challenge experiments to evaluate cross-protection induced at the trachea and kidney level by vaccine strains and Belgian nephropathogenic isolates of avian infectious bronchitis virus. Avian Pathol. 22, 577590.

    • Search Google Scholar
    • Export Citation
  • Laursen, S. B., Dalgaard, T. S., Thiel, S., Lim, B. L., Jensen, T. V., Juul-Madsen, H. R., Takahashi, A., Hamana, T., Kawakami, M. and Jensenius, J. C. (1998): Cloning and sequencing of a cDNA encoding chicken mannan-binding lectin (MBL) and comparison with mammalian analogues. Immunology 93, 421430.

    • Search Google Scholar
    • Export Citation
  • Lechmann, M., Berchtold, S., Hauber, J. and Steinkasserer, A. (2002): CD83 on dendritic cells: more than just a marker for maturation. Trends Immunol. 23, 273575.

    • Search Google Scholar
    • Export Citation
  • Mast, J., Goddeeris, B. M., Peeters, K., Vandesande, F. and Berghman, L. R. (1998): Characterisation of chicken monocytes, macrophages and interdigitating cells by the monoclonal antibody KUL01.Vet. Immunol. Immunopathol. 61, 343357.

    • Search Google Scholar
    • Export Citation
  • Nielsen, O. L., Jorgensen, P. H., Hedemand, J., Jensenius, J. C., Koch, C. and Laurse, S. B. (1998): Immunohistochemical investigation of the tissue distribution of mannan-binding lectin in noninfected and virus-infected chickens. Immunology 94, 122128.

    • Search Google Scholar
    • Export Citation
  • Nielsen, O. L., Jensenius, J. C., Jorgensen, P. H. and Laursen, S. B. (1999): Serum levels of chicken mannan-binding lectin (MBL) during virus infections; indication that chicken MBL is an acute phase reactant. Vet. Immunol. Immunopathol. 70, 309316.

    • Search Google Scholar
    • Export Citation
  • Oláh, I. and Glick, B. (1982): Splenic white pulp and associated vascular channels in chicken spleen. Am. J. Anat. 165, 445480.

  • Otsuki, K., Huggins, M. B. and Cook, J. K. A. (1990): Comparison of the susceptibility to avian infectious bronchitis virus infection of two inbred lines of White Leghorn chickens. Avian Pathol. 19, 467475.

    • Search Google Scholar
    • Export Citation
  • Otsuki, K., Nakamura, T., Kubota, N., Kawaoka, Y. and Tsubokura, M. (1987): Comparison of two strains of avian infectious bronchitis virus for their interferon induction, viral growth and development of virus-neutralizing antibody in experimentally-infected chickens. Vet. Microbiol. 12, 3140.

    • Search Google Scholar
    • Export Citation
  • Picault, J. P., Drouin, P., Toux, J. Y., Guittet, M. and Bennejean, G. (1991): Infectious bronchitis in France: epidemiological situation and prophylactic practices. Proceedings of the IInd International Symposium on Infectious Bronchitis, Rauischholzhausen, Germany. pp. 322.

    • Search Google Scholar
    • Export Citation
  • Prazma, C. M. and Tedder, T. F. (2007): Dendritic cell CD83: a therapeutic target or innocent bystander? Immunol. Lett. 115, 18.

  • Prechtel, A. T. and Steinkasserer, A. (2007): CD83: an update on functions and prospects of the maturation marker of dendritic cells. Arch. Dermatol. Res. 299, 5969.

    • Search Google Scholar
    • Export Citation
  • Randolph, G. J., Angeli, V. and Swartz, M. A. (2005): Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5, 617628.

    • Search Google Scholar
    • Export Citation
  • Sallusto, F., Cella, M., Danieli, C. and Lanzavecchia, A. (1995): Dendritic cells use micropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182, 389400.

    • Search Google Scholar
    • Export Citation
  • Schou, T. W., Permin, A., Christensen, J. P., Cu, H. P. and Juul-Madsen, H. R. (2010): Mannanbinding lectin (MBL) in two chicken breeds and the correlation with experimental Pasteurella multocida infection. Comp. Immunol. Microbiol. Infect. Dis. 33, 183195.

    • Search Google Scholar
    • Export Citation
  • Staines, K., Hunt, L. G., Young, J. R. and Butter, C. (2014): Evolution of an expanded mannose receptor gene family. PLoS One 12, e110330.

    • Search Google Scholar
    • Export Citation
  • Staines, K., Young, J. R. and Butter, C. (2013): Expression of chicken DEC205 reflects the unique structure and function of the avian immune system. PLoS One 8, e51799.

    • Search Google Scholar
    • Export Citation
  • Toro, H., Godoy, V., Larenas, J., Reyes, E. and Kaleta, E. F. (1996): Avian infectious bronchitis – viral persistence in the Harderian gland and histological changes after eye-drop vaccination. Avian Dis. 40, 114120.

    • Search Google Scholar
    • Export Citation
  • Ulrich-Lynge, S. L., Dalgaard, T. S., Norup, L. R., Kjaerup, R. M., Olsen, J. E., Sorensen, P. and Juul-Madsen, H. R. (2015a): The consequence of low mannose-binding lectin plasma concentration in relation to susceptibility to Salmonella Infantis in chickens. Vet. Immunol. Immunopathol. 163, 2332.

    • Search Google Scholar
    • Export Citation
  • Ulrich-Lynge, S. L., Dalgaard, T. S., Norup, L. R., Song, X., Sorensen, P. and Juul-Madsen, H. R. (2015b): Chicken mannose-binding lectin function in relation to antibacterial activity towards Salmonella enterica. Immunobiology 220, 555563.

    • Search Google Scholar
    • Export Citation
  • White, R. G., French, V. I. and Stark, J. M. (1970): A study of the localisation of a protein antigen in the chicken spleen and its relation to the formation of germinal centres. J. Med. Microbiol. 3, 6583.

    • Search Google Scholar
    • Export Citation
  • Zhang, W., Bouwman, K. M., van Beurden, S. J., Ordonez, S. R., van Eijk, M., Haagsman, H. P., Verheije, M. H. and Veldhuizen, E. J. A. (2017): Chicken mannose binding lectin has antiviral activity towards infectious bronchitis virus. Virology 509, 252259.

    • Search Google Scholar
    • Export Citation
  • Zhou, L. J. and Tedder, T. F. (1995): Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. J. Immunol. 154, 38213835.

    • Search Google Scholar
    • Export Citation
  • Zhou, L. J., Schwarting, R., Smith, H. M. and Tedder, T. F. (1992): A novel cell-surface molecule expressed by human interdigitating reticulum cells, Langerhans cells, and activated lymphocytes is a new member of the Ig superfamily. J. Immunol. 149, 735742.

    • Search Google Scholar
    • Export Citation

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