Infectious bronchitis virus infection in chicken: viral load and immune responses in Harderian gland, choanal cleft and turbinate tissues compared to trachea

References

• Abaidullah, M., S. Peng, X. Song, Y. Zou, L. Li, R. Jia, and Z. Yin. 2021. “Chlorogenic Acid Is a Positive Regulator of MDA5, TLR7 and NF-κB Signaling Pathways Mediated Antiviral Responses against Gammacoronavirus Infection.” International Immunopharmacology 96: 107671. doi:10.1016/j.intimp.2021.107671.
   PubMed Web of Science ®Google Scholar
• Asif, M., J. W. Lowenthal, M. E. Ford, K. A. Schat, W. G. Kimpton, and A. G. Bean. 2007. “Interleukin-6 Expression after Infectious Bronchitis Virus Infection in Chickens.” Viral Immunology 20 (3): 479–486. doi:10.1089/vim.2006.0109.
   PubMed Web of Science ®Google Scholar
• Awad, F., A. Forrester, M. Baylis, S. Lemiere, K. Ganapathy, H. A. Hussien, and I. Capua. 2015. “Protection Conferred by Live Infectious Bronchitis Vaccine Viruses against Variant Middle East IS/885/00-like and IS/1494/06-like Isolates in Commercial Broiler Chicks.” Veterinary Record Open 2 (2). doi:10.1136/vetreco-2014-000111.
   PubMedGoogle Scholar
• Awad, F., S. Hutton, A. Forrester, M. Baylis, and K. Ganapathy. 2016. “Heterologous Live Infectious Bronchitis Virus Vaccination in Day-old Commercial Broiler Chicks: Clinical Signs, Ciliary Health, Immune Responses and Protection against Variant Infectious Bronchitis Viruses.” Avian Pathology 45 (2): 169–177. doi:10.1080/03079457.2015.1137866.
   PubMed Web of Science ®Google Scholar
• Ball, C., S. Bennett, A. Forrester, and K. Ganapathy. 2016. “Genetic Mutations in Live Infectious Bronchitis Vaccine Viruses following Single or Dual in Vitro Infection of Tracheal Organ Cultures.” Journal of General Virology 97 (12): 3232–3237. doi:10.1099/jgv.0.000628.
   PubMed Web of Science ®Google Scholar
• Ball, C., A. Forrester, A. Herrmann, S. Lemiere, and K. Ganapathy. 2019. “Comparative Protective Immunity Provided by Live Vaccines of Newcastle Disease Virus or Avian Metapneumovirus When Co-administered Alongside Classical and Variant Strains of Infectious Bronchitis Virus in Day-old Broiler Chicks.” Vaccine 37 (52): 7566–7575. doi:10.1016/j.vaccine.2019.09.081.
   PubMed Web of Science ®Google Scholar
• Cavanagh, D. 2007. “Coronavirus Avian Infectious Bronchitis Virus.” Veterinary Research 38 (2): 281–297. doi:10.1051/vetres:2006055.
   PubMed Web of Science ®Google Scholar
• Chhabra, R., J. Chantrey, and K. Ganapathy. 2015a. “Immune Responses to Virulent and Vaccine Strains of Infectious Bronchitis Viruses in Chickens.” Viral Immunology 28 (9): 478–488. doi:10.1089/vim.2015.0027.
   PubMed Web of Science ®Google Scholar
• Chhabra, R., A. Forrester, S. Lemiere, F. Awad, J. Chantrey, and K. Ganapathy. 2015b. “Mucosal, Cellular, and Humoral Immune Responses Induced by Different Live Infectious Bronchitis Virus Vaccination Regimes and Protection Conferred against Infectious Bronchitis Virus Q1 Strain.” Clinical Vaccine Immunology 22 (9): 1050–1059. doi:10.1128/cvi.00368-15.
   PubMedGoogle Scholar
• Chhabra, R., S. V. Kuchipudi, J. Chantrey, and K. Ganapathy. 2016. “Pathogenicity and Tissue Tropism of Infectious Bronchitis Virus Is Associated with Elevated Apoptosis and Innate Immune Responses.” Virology 488: 232–241. doi:10.1016/j.virol.2015.11.011.
   PubMed Web of Science ®Google Scholar
• Chhabra, R., C. Ball, J. Chantrey, and K. Ganapathy. 2018. “Differential Innate Immune Responses Induced by Classical and Variant Infectious Bronchitis Viruses in Specific Pathogen Free Chicks.” Developmental and Comparative Immunology 87: 16–23. doi:10.1016/j.dci.2018.04.026.
   PubMed Web of Science ®Google Scholar
• Cook, J. K., J. H. Darbyshire, and R. W. Peters. 1976. “The Use of Chicken Tracheal Organ Cultures for the Isolation and Assay of Avian Infectious Bronchitis Virus.” Archives of Virology 50 (1–2): 109–118. doi:10.1007/BF01318005.
   PubMed Web of Science ®Google Scholar
• Cook, J. K., S. J. Orbell, M. A. Woods, and M. B. Huggins. 1999. “Breadth of Protection of the Respiratory Tract Provided by Different Live-attenuated Infectious Bronchitis Vaccines against Challenge with Infectious Bronchitis Viruses of Heterologous Serotypes.” Avian Pathology 28 (5): 477–485. doi:10.1080/03079459994506.
   PubMed Web of Science ®Google Scholar
• Darbyshire, J. H., J. K. A. Cook, and R. W. Peters. 1978. “Growth Comparisons of Avian Infectious Bronchitis Virus Strains in Organ Cultures of Chicken Tissues.” Archives of Virology 56 (4): 317–325. doi:10.1007/BF01315282.
   PubMed Web of Science ®Google Scholar
• Davelaar, F. G., A. Noordzij, and J. A. Vanderdonk. 1982. “A Study on the Synthesis and Secretion of Immunoglobulins by the Jarderian Gland of the Fowl after Eyedrop Vaccination against Infectious Bronchitis at 1‐day‐old.” Avian Pathology 11 (1): 63–79. doi:10.1080/03079458208436082.
   PubMed Web of Science ®Google Scholar
• DEFRA. 2002. “Meat Chickens and Breeding Chickens. Code of Recommendations for the Welfare of Livestock.” PB7275.
   Google Scholar
• Dolz, R., J. Vergara-Alert, M. Perez, J. Pujols, and N. Majo. 2012. “New Insights on Infectious Bronchitis Virus Pathogenesis: Characterization of Italy 02 Serotype in Chicks and Adult Hens.” Veterinary Microbiology 156 (3–4): 256–264. doi:10.1016/j.vetmic.2011.11.001.
   PubMed Web of Science ®Google Scholar
• Eldemery, F., K. S. Joiner, H. Toro, and V. L. van Santen. 2017. “Protection against Infectious Bronchitis Virus by Spike Ectodomain Subunit Vaccine.” Vaccine 35 (43): 5864–5871. doi:10.1016/j.vaccine.2017.09.013.
   PubMed Web of Science ®Google Scholar
• Fernando, F. S., C. H. Okino, K. R. Silva, C. C. Fernandes, M. C. M. Gonçalves, M. F. S. Montassier, R. O. Vasconcelos, and H. J. Montassier. 2015. “Increased Expression of Interleukin-6 Related to Nephritis in Chickens Challenged with an Avian Infectious Bronchitis Virus Variant.” Pesquisa Veterinária Brasileira 35 (3): 216–222. doi:10.1590/S0100-736X2015000300002.
   Web of Science ®Google Scholar
• Fournier-Caruana, J., B. Poirier, G. Haond, C. Jallet, F. Fuchs, N. Tordo, and P. Perrin. 2003. “Inactivated Rabies Vaccine Control and Release: Use of an ELISA Method.” Biologicals 31 (1): 9–16. doi:10.1016/S1045-1056(02)00070-2.
   PubMed Web of Science ®Google Scholar
• Ganapathy, K., P. W. Cargill, and R. C. Jones. 2005. “A Comparison of Methods of Inducing Lachrymation and Tear Collection in Chickens for Detection of Virus-specific Immuoglobulins after Infection with Infectious Bronchitis Virus.” Avian Pathology 34 (3): 248–251. doi:10.1080/03079450500112344.
   PubMed Web of Science ®Google Scholar
• Gelb, J., Jr, W. A. Nix, and S. D. Gellman. 1998. “Infectious Bronchitis Virus Antibodies in Tears and Their Relationship to Immunity.” Avian Diseases 42 (2): 364–374. doi:10.2307/1592487.
   PubMed Web of Science ®Google Scholar
• Gillette, K. G. 1980. “Avian Infectious Bronchitis in Specific-pathogen-free Chickens: Quantitation of Serum Immunoglobulins by Electroimmunoassay.” Avian Diseases 24 (2): 345–357. doi:10.2307/1589702.
   PubMed Web of Science ®Google Scholar
• Guo, X., A. J. Rosa, D. G. Chen, and X. Wang. 2008. “Molecular Mechanisms of Primary and Secondary Mucosal Immunity Using Avian Infectious Bronchitis Virus as a Model System.” Veterinary Immunology and Immunopathology 121 (3–4): 332–343. doi:10.1016/j.vetimm.2007.09.016.
   PubMed Web of Science ®Google Scholar
• Gurjar, R. S., S. L. Gulley, and F. W. van Ginkel. 2013. “Cell-mediated Immune Responses in the Head-associated Lymphoid Tissues Induced to a Live Attenuated Avian Coronavirus Vaccine.” Developmental & Comparative Immunology 41 (4): 715–722. doi:10.1016/j.dci.2013.08.002.
   PubMed Web of Science ®Google Scholar
• Hawkes, R. A., J. H. Darbyshire, R. W. Peters, A. P. A. Mockett, and D. Cavanagh. 1983. “Presence of Viral Antigens and Antibody in the Trachea of Chickens Infected with Avian Infectious Bronchitis Virus.” Avian Pathology 12 (3): 331–340. doi:10.1080/03079458308436175.
   PubMed Web of Science ®Google Scholar
• He, Y., Z. Xie, J. Dai, Y. Cao, J. Hou, Y. Zheng, T. Wei, M. Mo, and P. Wei. 2016. “Responses of the Toll-like Receptor and Melanoma Differentiation-associated Protein 5 Signaling Pathways to Avian Infectious Bronchitis Virus Infection in Chicks.” Virologica Sinica 31 (1): 57–68. doi:10.1007/s12250-015-3696-y.
   PubMed Web of Science ®Google Scholar
• Ignjatovic, J., and P. G. McWaters. 1991. “Monoclonal Antibodies to Three Structural Proteins of Avian Infectious Bronchitis Virus: Characterization of Epitopes and Antigenic Differentiation of Australian Strains.” Journal of General Virology 72 (12): 2915–2922. doi:10.1099/0022-1317-72-12-2915.
   PubMed Web of Science ®Google Scholar
• Jackwood, M. W. 2012. “Review of Infectious Bronchitis Virus around the World.” Avian Diseases 56 (4): 634–641. doi:10.1637/10227-043012-Review.1.
   PubMed Web of Science ®Google Scholar
• Joiner, K. S., F. J. Hoerr, S. J. Ewald, V. L. Van Santen, J. C. Wright, F. W. Van Ginkel, and H. Toro. 2007. “Pathogenesis of Infectious Bronchitis Virus in Vaccinated Chickens of Two Different Major Histocompatibility B Complex Genotypes.” Avian Diseases 51 (3): 758–763. doi:10.1637/0005-2086(2007)51[758:POIBVI]2.0.CO;2.
   PubMed Web of Science ®Google Scholar
• Kameka, A. M., S. Haddadi, D. S. Kim, S. C. Cork, and M. F. Abdul-Careem. 2014. “Induction of Innate Immune Response following Infectious Bronchitis Corona Virus Infection in the Respiratory Tract of Chickens.” Virology 450-451: 114–121. doi:10.1016/j.virol.2013.12.001.
   PubMed Web of Science ®Google Scholar
• Kint, J., M. A. Langereis, H. J. Maier, P. Britton, F. J. van Kuppeveld, J. Koumans, G. F. Wiegertjes, and M. Forlenza. 2016. “Infectious Bronchitis Coronavirus Limits Interferon Production by Inducing a Host Shutoff that Requires Accessory Protein 5b.” Journal of Virology 90 (16): 7519–7528. doi:10.1128/JVI.00627-16.
   PubMed Web of Science ®Google Scholar
• Kuchipudi, S. V., M. Tellabati, R. K. Nelli, B. B. Perez, S. Sebastian, S. P. Dunham, K. C. Chang, et al. 2012. “18S rRNA Is a Reliable Normalisation Gene for Real Time PCR Based on Influenza Virus Infected Cells.” Virology Journal 9 (1). doi:10.1186/1743-422X-9-230.
   PubMed Web of Science ®Google Scholar
• Kuchipudi, S. V., M. Tellabati, S. Sebastian, B. Z. Londt, C. Jansen, L. Vervelde, S. M. Brookes, I. H. Brown, S. P. Dunham, and K. Chang. 2014. “Highly Pathogenic Avian Influenza Virus Infection in Chickens but Not Ducks is Associated with Elevated Host Immune and Pro-Inflammatory Responses.” Veterinary Research 45 (1): 1–18. doi:10.1186/s13567-014-0118-3.
   PubMed Web of Science ®Google Scholar
• Lay, D. C., Jr., R. M. Fulton, P. Y. Hester, D. M. Karcher, J. B. Kjaer, J. A. Mench, B. A. Mullens, et al. 2011. “Hen Welfare in Different Housing Systems 1.” Poultry Science 90 (1): 278–294. doi:10.3382/ps.2010-00962.
   PubMed Web of Science ®Google Scholar
• McMartin, D. A. 1993. “Infectious Bronchitis.” In Virus Infections of Birds, edited by J. B. McFerran and M. S. McNulty, 249–275. Amsterdam: Elsevier Science.
   Google Scholar
• Mockett, A. P., and J. K. Cook. 1986. “The Detection of Specific IgM to Infectious Bronchitis Virus in Chicken Serum Using an ELISA.” Avian Pathology 15 (3): 437–446. doi:10.1080/03079458608436305.
   PubMed Web of Science ®Google Scholar
• Okino, C. H., A. C. Alessi, F. Montassier Mde, A. J. Rosa, X. Wang, and H. J. Montassier. 2013. “Humoral and Cell-mediated Immune Responses to Different Doses of Attenuated Vaccine against Avian Infectious Bronchitis Virus.” Viral Immunology 26 (4): 259–267. doi:10.1089/vim.2013.0015.
   PubMed Web of Science ®Google Scholar
• Okino, C. H., I. L. Dos Santos, F. S. Fernando, A. C. Alessi, X. Q. Wang, and H. J. Montassier. 2014. “Inflammatory and Cell-mediated Immune Responses in the Respiratory Tract of Chickens to Infection with Avian Infectious Bronchitis Virus.” Viral Immunology 27 (8): 383–391. doi:10.1089/vim.2014.0054.
   PubMed Web of Science ®Google Scholar
• Okino, C. H., M. A. Mores, I. M. Trevisol, A. Coldebella, H. J. Montassier, and L. Brentano. 2017. “Early Immune Responses and Development of Pathogenesis of Avian Infectious Bronchitis Viruses with Different Virulence Profiles.” PLoS One 12 (2): e0172275. doi:10.1371/journal.pone.0172275.
   PubMed Web of Science ®Google Scholar
• Oladele, O. A., D. F. Adene, T. U. Obi, and H. O. Nottidge. 2009. “Comparative Susceptibility of Chickens, Turkeys and Ducks to Infectious Bursal Disease Virus Using Immunohistochemistry.” Veterinary Research Communincations 33 (2): 111–121. doi:10.1007/s11259-008-9078-2.
   PubMed Web of Science ®Google Scholar
• Orr-Burks, N., S. Gulley, R. A. Gallardo, H. Toro, and F. Van Ginkel. 2014. “Immunoglobulin A as an Early Humoral Responder after Mucosal Avian Coronavirus Vaccination.” Avian Diseases 58 (2): 279–286. doi:10.1637/10740-120313-Reg.1.
   PubMed Web of Science ®Google Scholar
• Otsuki, K., M. B. Huggins, and J. K. A. Cook. 1990. “Comparison of the Susceptibility to Avian Infectious Bronchitis Virus Infection of Two Inbred Lines of White Leghorn Chickens.” Avian Pathology 19 (3): 467–475. doi:10.1080/03079459008418700.
   PubMed Web of Science ®Google Scholar
• Qu, H., L. Yang, S. Meng, L. Xu, Y. Bi, X. Jia, J. Li, L. Sun, and W. Liu. 2013. “The Differential Antiviral Activities of Chicken Interferon α (ChIFN-α) and ChIFN-β are Related to Distinct Interferon-stimulated Gene Expression.” PLoS One 8 (3): e59307. doi:10.1371/journal.pone.0059307.
   PubMed Web of Science ®Google Scholar
• Raggi, L., and G. Lee. 1965. “Lack of Correlation between Infectivity, Serologic Response and Challenge Results in Immunization with an Avian Infectious Bronchitis Vaccine.” The Journal of Immunology 94 (4): 538–543.
   PubMed Web of Science ®Google Scholar
• Raj, G. D., and R. C. Jones. 1996. “Local Antibody Production in the Oviduct and Gut of Hens Infected with a Variant Strain of Infectious Bronchitis Virus.” Veterinary Immunology and Immunopathology 53 (1–2): 147–161. doi:10.1016/0165-2427(95)05545-2.
   PubMed Web of Science ®Google Scholar
• Raj, G. D., and R. C. Jones. 1997. “Infectious Bronchitis Virus: Immunopathogenesis of Infection in the Chicken.” Avian Pathology 26 (4): 677–706. doi:10.1080/03079459708419246.
   PubMed Web of Science ®Google Scholar
• Reed, L. J., and H. Muench. 1938. “A Simple Method of Estimating Fifty per Cent Endpoints.” American Journal of Epidemiology 27 (3): 493–497. doi:10.1093/oxfordjournals.aje.a118408.
   Google Scholar
• Sharma, B., N. Kakker, S. Bhadouriya, and R. Chhabra. 2020. “Effect of TLR Agonist on Infections Bronchitis Virus Replication and Cytokine Expression in Embryonated Chicken Eggs.” Molecular Immunology 120: 52–60. doi:10.1016/j.molimm.2020.02.001.
   PubMed Web of Science ®Google Scholar
• Smith, J., J. R. Sadeyen, D. Cavanagh, P. Kaiser, and D. W. Burt. 2015. “The Early Immune Response to Infection of Chickens with Infectious Bronchitis Virus (IBV) in Susceptible and Resistant Birds.” BMC Veterinary Research 11 (1): 256. doi:10.1186/s12917-015-0575-6.
   PubMed Web of Science ®Google Scholar
• Steyn, A., S. Keep, E. Bickerton, and M. Fife. 2020. “The Characterization of chIFITMs in Avian Coronavirus Infection in Vivo, Ex Vivo and in Vitro.” Genes (Basel) 11 (8): 918. doi:10.3390/genes11080918.
   PubMed Web of Science ®Google Scholar
• Toro, H., and I. Fernandez. 1994. “Avian Infectious Bronchitis: Specific Lachrymal IgA Level and Resistance against Challenge.” Journal of Veterinary Medicine, Series B 41 (1‐10): 467–472. doi:10.1111/j.1439-0450.1994.tb00252.x.
   Web of Science ®Google Scholar
• Toro, H., H. Hidalgo, and A. N. Collingwood-Selby. 1994. “Lachrymal Antibody Response of Specific Pathogen Free Chickens and Chickens with Maternal Immunity after Infectious Bronchitis Virus Vaccination.” Preventive Veterinary Medicine 18 (4): 267–274. doi:10.1016/0167-5877(94)90051-5.
   Web of Science ®Google Scholar
• van Ginkel, F. W., S. L. Gulley, A. Lammers, F. J. Hoerr, R. Gurjar, and H. Toro. 2012. “Conjunctiva-associated Lymphoid Tissue in Avian Mucosal Immunity.” Developmental and Comparitive Immunology 36 (2): 289–297. doi:10.1016/j.dci.2011.04.012.
   PubMed Web of Science ®Google Scholar
• van Ginkel, F. W., V. L. van Santen, S. L. Gulley, and H. Toro. 2008. “Infectious Bronchitis Virus in the Chicken Harderian Gland and Lachrymal Fluid: Viral Load, Infectivity, Immune Cell Responses, and Effects of Viral Immunodeficiency.” Avian Diseases 52 (4): 608–617. doi:10.1637/8349-050908-Reg.1.
   PubMed Web of Science ®Google Scholar
• van Santen, V. L., H. Toro, F. W. van Ginkel, K. S. Joiner, and F. J. Hoerr. 2006. “Effects of CAV And/or IBDV on IBV Infection and Immune Responses.” Paper presented at the Proceedings of the V International Symposium on Avian Corona-and Pneumoviruses and Complicating Pathogens, Rauischholzhausen, Germany.
   Google Scholar
• Wang, X., A. J. M. Rosa, H. N. Oliverira, G. J. M. Rosa, X. Guo, M. Travnicek, and T. Girshick. 2006. “Transcriptome of Local Innate and Adaptive Immunity during Early Phase of Infectious Bronchitis Viral Infection.” Viral Immunology 19 (4): 768–774. doi:10.1089/vim.2006.0051.
   PubMed Web of Science ®Google Scholar
• Wu, B., A. Peisley, C. Richards, H. Yao, X. Zeng, C. Lin, F. Chu, T. Walz, and S. Hur. 2013. “Structural Basis for dsRNA Recognition, Filament Formation, and Antiviral Signal Activation by MDA5.” Cell 152 (1–2): 276–289. doi:10.1016/j.cell.2012.11.048.
   PubMed Web of Science ®Google Scholar
• Yang, X., J. Li, H. Liu, P. Zhang, D. Chen, S. Men, X. Li, and H. Wang. 2018. “Induction of Innate Immune Response following Introduction of Infectious Bronchitis Virus (IBV) in the Trachea and Renal Tissues of Chickens.” Microbial Pathogenesis 116: 54–61. doi:10.1016/j.micpath.2018.01.008.
   PubMed Web of Science ®Google Scholar
• Yu, L. P., X. R. Zhang, T. Q. Wu, J. Su, Y. Y. Wang, Y. X. Wang, B. Y. Ruan, X. S. Niu, and Y. T. Wu. 2017. “Avian Infectious Bronchitis Virus Disrupts the Melanoma Differentiation Associated Gene 5 (MDA5) Signaling Pathway by Cleavage of the Adaptor Protein MAVS.” BMC Veterinary Research 13 (1). doi:10.1186/s12917-017-1253-7.
   Web of Science ®Google Scholar
• Zegpi, R. A., K. S. Joiner, V. L. van Santen, and H. Toro. 2020a. “Infectious Bronchitis Virus Population Structure Defines Immune Response and Protection.” Avian Diseases 64 (1): 60–68. doi:10.1637/0005-2086-64.1.60.
   PubMed Web of Science ®Google Scholar
• Zegpi, R. A., C. Breedlove, S. Gulley, and H. Toro. 2020b. “Infectious Bronchitis Virus Immune Responses in the Harderian Gland upon Initial Vaccination.” Avian Diseases 64 (1): 92–95. doi:10.1637/0005-2086-64.1.92.
   PubMed Web of Science ®Google Scholar
• Zhang, T., L. Deyin, Z. Jia, J. Chang, and X. Hou. 2017. “Cellular Immune Response in Chickens Infected with Avian Infectious Bronchitis Virus (IBV).” European Journal of Inflammation 15 (1): 35–41. doi:10.1177/1721727x17703886.
   Web of Science ®Google Scholar
• Zhao, X., J. Li, C. A. Winkler, P. An, and J. T. Guo. 2018. “IFITM Genes, Variants, and Their Roles in the Control and Pathogenesis of Viral Infections.” Frontiers in Microbiology 9: 3228. doi:10.3389/fmicb.2018.03228.
   PubMed Web of Science ®Google Scholar