Host genetics determine susceptibility to avian influenza infection and transmission dynamics

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ruiz Hernandez, Raul ^a   Mwangi, William ^a   Peroval, Marylene ^a   Sadeyen, Jean Remy ^a   Ascough, Stephanie ^a   Balkissoon, Devanand ^a   Staines, Karen ^a,d   Boyd, Amy ^b   McCauley, John ^c   Smith, Adrian ^b   Butter, Colin ^a,d  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^d UNIVERSITY OF LINCOLN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIBODY;

ADAPTIVE IMMUNITY; ANIMAL; AVIAN INFLUENZA; BIOSYNTHESIS; BIRD DISEASE; CELL CULTURE; CHICK EMBRYO; CHICKEN; CLOACA; COMPARATIVE STUDY; FIBROBLAST; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; IMMUNOLOGY; INBREEDING; INFLUENZA A VIRUS (H7N7); INFLUENZA A VIRUS (H9N2); OROPHARYNX; PATHOGENICITY; PHYSIOLOGY; TRANSMISSION; VIROLOGY; VIRUS REPLICATION; VIRUS SHEDDING;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, VIRAL; CELLS, CULTURED; CHICK EMBRYO; CHICKENS; CLOACA; FIBROBLASTS; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; INBREEDING; INFLUENZA A VIRUS, H7N7 SUBTYPE; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; OROPHARYNX; POULTRY DISEASES; VIRUS REPLICATION; VIRUS SHEDDING;

EID: 84973860949     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26787     Document Type: Article

References (46)

1. OIE. http://www.oie.int/fileadmin/Home/eng/Health-standards/tahm/2.03.04-AI.pdf. World Organisation for Animal Health. OIE Terrestrial Manual. Avian Influenza, Chapter 2.3.4. Pages 1-6 (2014) 13/04/2016.
2. Alexander, D. J. An overview of the epidemiology of avian influenza. Vaccine 25, 5637-5644, doi: 10.1016/j.vaccine.2006.10.051 (2007).
3. Alexander, D. J. A review of avian influenza in different bird species. Vet. Microbiol. 74, 3-13 (2000).
4. Maines, T. R. et al. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol. Rev. 225, 68-84, doi: 10.1111/j.1600-065X.2008.00690.x (2008).
5. Watanabe, T. et al. Circulating avian influenza viruses closely related to the 1918 virus have pandemic potential. Cell host & microbe 15, 692-705, doi: 10.1016/j.chom.2014.05.006 (2014).
6. Klenk, H. D. Influenza viruses en route from birds to man. Cell host & microbe 15, 653-654, doi: 10.1016/j.chom.2014.05.019 (2014).
7. Perdue, M. L. & Nguyen, T. The WHO research agenda for influenza: two years later. Bull. World Health Organ. 90, 246, doi: 10.2471/ BLT.11.090175 (2012).
8. O'Donnell, C. D. & Subbarao, K. The contribution of animal models to the understanding of the host range and virulence of influenza A viruses. Microb. Infect. 13, 502-515, doi: DOI 10.1016/j.micinf.2011.01.014 (2011).
9. Korth, M. J., Tchitchek, N., Benecke, A. G. & Katze, M. G. Systems approaches to influenza-virus host interactions and the pathogenesis of highly virulent and pandemic viruses. Semin. Immunol. 25, 228-239, doi: 10.1016/j.smim.2012.11.001 (2013).
10. Horby, P., Nguyen, N. Y., Dunstan, S. J. & Baillie, J. K. The role of host genetics in susceptibility to influenza: a systematic review. PLoS One 7, e33180, doi: 10.1371/journal.pone.0033180 (2012).
11. Herfst, S. et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534-1541, doi: 10.1126/ science.1213362 (2012).
12. Ferris, M. T. et al. Modeling Host Genetic Regulation of Influenza Pathogenesis in the Collaborative Cross. PLoS Path. 9, doi: DOI 10.1371/journal.ppat.1003196 (2013).
13. Belser, J. A., Katz, J. M. & Tumpey, T. M. The ferret as a model organism to study influenza A virus infection. Dis. Model. Mech. 4, 575-579, doi: Doi 10.1242/Dmm.007823 (2011).
14. Howell, W. M. HLA and disease: guilt by association. Int. J. Immunogenet. 41, 1-12, doi: Doi 10.1111/Iji.12088 (2014).
15. Davison, T. F., Kaspers, B. & Schat, K. A. Avian immunology. 164-168 (Academic, 2008).
16. Banat, G. R. et al. Association of the chicken MHC B haplotypes with resistance to avian coronavirus. Dev. Comp. Immunol. 39, 430-437, doi: 10.1016/j.dci.2012.10.006 (2013).
17. Zhang, L., Katz, J. M., Gwinn, M., Dowling, N. F. & Khoury, M. J. Systems-based candidate genes for human response to influenza infection. Infect. Genet. Evol. 9, 1148-1157, doi: 10.1016/j.meegid.2009.07.006 (2009).
18. Boonyanuwat, K., Thummabutra, S., Sookmanee, N., Vatchavalkhu, V. & Siripholvat, V. Influences of major histocompatibility complex class I haplotypes on avian influenza virus disease traits in Thai indigenous chickens. Anim Sci J 77, 285-289, doi: 10.1111/j.1740-0929.2006.00350.x (2006).
19. Hunt, H. D., Jadhao, S. & Swayne, D. E. Major Histocompatibility Complex and Background Genes in Chickens Influence Susceptibility to High Pathogenicity Avian Influenza Virus. Avian Dis. 54, 572-575, doi: 10.1637/8888-042409-ResNote.1 (2010).
20. Miller, M. M. et al. 2004 Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56, 261-279, doi: 10.1007/s00251-004-0682-1 (2004).
21. Heldt, F. S., Frensing, T. & Reichl, U. Modeling the Intracellular Dynamics of Influenza Virus Replication To Understand the Control of Viral RNA Synthesis. J. Virol. 86, 7806-7817, doi: 10.1128/Jvi.00080-12 (2012).
22. Iqbal, M., Yaqub, T., Reddy, K. & McCauley, J. W. Novel genotypes of H9N2 influenza A viruses isolated from poultry in Pakistan containing NS genes similar to highly pathogenic H7N3 and H5N1 viruses. PLos One 4, e5788, doi: 10.1371/journal.pone.0005788 (2009).
23. Iqbal, M., Yaqub, T., Mukhtar, N., Shabbir, M. Z. & McCauley, J. W. Infectivity and transmissibility of H9N2 avian influenza virus in chickens and wild terrestrial birds. Vet. Res. 44, 100, doi: 10.1186/1297-9716-44-100 (2013).
24. Chervyakova, O. V. et al. Molecular and genetic analysis of NS gene from high pathogenic strains of the avian influenza (H5N1) virus isolated in Kazakhstan. Gene 476, 15-19, doi: 10.1016/j.gene.2011.02.003 (2011).
25. Brown, J. D., Swayne, D. E., Cooper, R. J., Burns, R. E. & Stallknecht, D. E. Persistence of H5 and H7 avian influenza viruses in water. Avian Dis. 51, 285-289 (2007).
26. Schaffne, T. et al. Bursa of Fabricius-Central Organ Providing for Contact between Lymphoid System and Intestinal Content. Cell. Immunol. 13, 304-312, doi: 10.1016/0008-8749(74)90247-0 (1974).
27. Rohani, P., Breban, R., Stallknecht, D. E. & Drake, J. M. Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion. Proc. Natl. Acad. Sci. USA 106, 10365-10369, doi: 10.1073/pnas.0809026106 (2009).
28. Reemers, S. S. et al. Early host responses to avian influenza A virus are prolonged and enhanced at transcriptional level depending on maturation of the immune system. Mol. Immunol. 47, 1675-1685, doi: 10.1016/j.molimm.2010.03.008 (2010).
29. Karpala, A. J., Lowenthal, J. W. & Bean, A. G. Identifying innate immune pathways of the chicken may lead to new antiviral therapies. Vet. Immunol. Immunopathol. 148, 100-109, doi: 10.1016/j.vetimm.2011.05.031 (2012).
30. Uchida, Y. et al. Identification of Host Genes Linked with the Survivability of Chickens Infected with Recombinant Viruses Possessing H5N1 Surface Antigens from a Highly Pathogenic Avian Influenza Virus. J. Virol. 86, 2686-2695, doi: 10.1128/jvi.06374-11 (2012).
31. Butter, C., Staines, K., van Hateren, A., Davison, T. F. & Kaufman, J. The peptide motif of the single dominantly expressed class I molecule of the chicken MHC can explain the response to a molecular defined vaccine of infectious bursal disease virus (IBDV). Immunogenetics, doi: 10.1007/s00251-013-0705-x (2013).
32. Omar, A. R. & Schat, K. A. Syngeneic Marek's disease virus (MDV)-specific cell-mediated immune responses against immediate early, late, and unique MDV proteins. Virology 222, 87-99, doi: 10.1006/viro.1996.0400 (1996).
33. Baaten, B. J. G. et al. Early Replication in Pulmonary B Cells After Infection with Marek's Disease Herpesvirus by the Respiratory Route. Viral Immunol. 22, 431-444, doi: 10.1089/vim.2009.0047 (2009).
34. Kaufman, J. et al. The chicken B locus is a minimal essential major histocompatibility complex. Nature 401, 923-925, doi: 10.1038/44856 (1999).
35. Rogers, S. L. et al. Characterization of the chicken C-type lectin-like receptors B-NK and B-lec suggests that the NK complex and the MHC share a common ancestral region. J. Immunol. 174, 3475-3483 (2005).
36. Straub, C. et al. Chicken NK cell receptors. Dev. Comp. Immunol., doi: 10.1016/j.dci.2013.03.013 (2013).
37. Jansen, C. A. et al. Differential lung NK cell responses in avian influenza virus infected chickens correlate with pathogenicity. Sci. Rep. 3, 2478, doi: 10.1038/srep02478 (2013).
38. Gazit, R. et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 7, 517-523, doi: 10.1038/ni1322 (2006).
39. Kaufman, J., Volk, H. & Wallny, H. J. A Minimal-Essential-Mhc and an Unrecognized-Mhc-2 Extremes in Selection for Polymorphism. Immunol. Rev. 143, 63-88, doi: 10.1111/j.1600-065X.1995.tb00670.x (1995).
40. Boon, A. C. et al. Host genetic variation affects resistance to infection with a highly pathogenic H5N1 influenza A virus in mice. J. Virol. 83, 10417-10426, doi: 10.1128/JVI.00514-09 (2009).
41. Lyall, J. et al. Suppression of avian influenza transmission in genetically modified chickens. Science 331, 223-226, doi: 10.1126/ science.1198020 (2011).
42. Lin, T. Y. & Brass, A. L. Host genetic determinants of influenza pathogenicity. Curr. Opin. Virol., doi: 10.1016/j.coviro.2013.07.005 (2013).
43. Home Office, U. Guidance on the operation of the Animals (Scientific Procedures) Act 1986. (H.M.S.O. 1990).
44. Boyd, A. C. et al. Towards a universal vaccine for avian influenza: protective efficacy of modified Vaccinia virus Ankara and Adenovirus vaccines expressing conserved influenza antigens in chickens challenged with low pathogenic avian influenza virus. Vaccine 31, 670-675, doi: 10.1016/j.vaccine.2012.11.047 (2013).
45. Ruiz-Hernandez, R. et al. An infected chicken kidney cell co-culture ELISpot for enhanced detection of T cell responses to avian influenza and vaccination. J. Immunol. Methods 416, 40-48, doi: 10.1016/j.jim.2014.10.012 (2015).
46. Gaush, C. R. & Smith, T. F. Replication and plaque assay of influenza virus in an established line of canine kidney cells. Appl. Microbiol. 16, 588-594 (1968).