Characterization of the localized immune response in the respiratory tract of ferrets following infection with influenza A and B viruses

Journal of Virology

Volumn 90, Issue 6, 2016, Pages 2838-2848

  Carolan, Louise A ^a   Rockman, Steve ^b,c   Borg, Kathryn ^a,d   Guarnaccia, Teagan ^a,d   Reading, Patrick ^a   Mosse, Jennifer ^d   Kelso, Anne ^a   Barr, Ian ^a   Laurie, Karen L ^a  

^a PETER DOHERTY INSTITUTE FOR INFECTION AND IMMUNITY   (Australia)

^b CSL LIMITED   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF BALLARAT   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GRANZYME A; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ADULT; ALPHA INTERFERON GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA INTERFERON GENE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FERRET; GENE EXPRESSION; IMMUNE RESPONSE; INFLUENZA A; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA B; INTERLEUKIN 12P40 GENE; INTERLEUKIN 1ALPHA GENE; INTERLEUKIN 1BETA GENE; INTERLEUKIN 6 GENE; LOWER RESPIRATORY TRACT; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROCONVERSION; SYMPTOM ASSESSMENT; TUMOR NECROSIS FACTOR ALPHA GENE; UPPER RESPIRATORY TRACT; VIRUS SHEDDING; VIRUS STRAIN; ANIMAL; BODY TEMPERATURE; BODY WEIGHT; DISEASE MODEL; GENE EXPRESSION PROFILING; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA B VIRUS; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; RESPIRATORY SYSTEM; SEVERITY OF ILLNESS INDEX; VIROLOGY; VIRUS LOAD;

ANIMALS; BODY TEMPERATURE; BODY WEIGHT; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; GENE EXPRESSION PROFILING; HUMANS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; MALE; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY SYSTEM; SEVERITY OF ILLNESS INDEX; VIRAL LOAD; VIRUS SHEDDING;

EID: 84961162048     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02797-15     Document Type: Article

References (54)

1. Nicholson KG, Webster RG, Hay AJ. 1998. Textbook of influenza. Blackwell Science Ltd, London, United Kingdom.
2. Vijaykrishna D, Holmes EC, Joseph U, Fourment M, Su YCF, Halpin R, Lee RTC, Deng YM, Gunalan V, Lin X, Stockwell TB, Fedorova NB, Zhou B, Spirason N, Kühnert D, Bošková V, Stadler T, Costa AM, Dwyer DE, Huang QS, Jennings LC, Rawlinson W, Sullivan SG, Hurt AC, Maurer-Stroh S, Wentworth DE, Smith GJ, Barr IG. 2015. The contrasting phylodynamics of human influenza B viruses. eLife 4:e05055. http://dx.doi.org/10.7554/eLife.05055.
3. CDC. 19 August 2015, posting date. Flu symptoms and severity. http://www.cdc.gov/flu/about/disease/symptoms.htm.
4. McCullers JA, Hayden FG. 2012. Fatal influenza B infections: time to reexamine influenza research priorities. J Infect Dis 205:870-872. http://dx.doi.org/10.1093/infdis/jir865.
5. Paddock CD, Liu L, Denison AM, Bartlett JH, Holman RC, Deleon-Carnes M, Emery SL, Drew CP, Shieh WJ, Uyeki TM, Zaki SR. 2012. Myocardial injury and bacterial pneumonia contribute to the pathogenesis of fatal influenza B virus infection. J Infect Dis 205:895-905. http://dx.doi.org/10.1093/infdis/jir861.
6. Tate MD, Schilter HC, Brooks AG, Reading PC. 2011. Responses of mouse airway epithelial cells and alveolar macrophages to virulent and avirulent strains of influenza A virus. Virus Immunol 24:77-88. http://dx.doi.org/10.1089/vim.2010.0118.
7. La Gruta NL, Kedzierska K, Stambas J, Doherty PC. 2007. A question of self-preservation: immunopathology in influenza virus infection. Immunol Cell Biol 85:85-92. http://dx.doi.org/10.1038/sj.icb.7100026.
8. Oshansky CM, Gartland AJ, Wong SS, Jeevan T, Wang D, Roddam PL, Caniza MA, Hertz T, Devincenzo JP, Webby RJ, Thomas PG. 2014. Mucosal immune responses predict clinical outcomes during influenza infection independently of age and viral load. Am J Respir Crit Care Med 189:449-462. http://dx.doi.org/10.1164/rccm.201309-1616OC.
9. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203-1207. http://dx.doi.org/10.1038/nm1477.
10. Chiaretti A, Pulitanò S, Conti G, Barone G, Buonsenso D, Manni L, Capozzi D, Ria F, Riccardi R. 2013. Interleukin and neurotrophin upregulation correlates with severity of H1N1 infection in children: a casecontrol study. Int J Infect Dis 17:e1186-93. http://dx.doi.org/10.1016/j.ijid.2013.07.006.
11. Paquette SG, Banner D, Zhao Z, Fang Y, Huang SS, Leün AJ, Ng DC, Almansa R, Martin-Loeches I, Ramirez P, Socias L, Loza A, Blanco J, Sansonetti P, Rello J, Andaluz D, Shum B, Rubino S, de Lejarazu RO, Tran D, Delogu G, Fadda G, Krajden S, Rubin BB, Bermejo-Martin JF, Kelvin AA, Kelvin DJ. 2012. Interleukin-6 is a potential biomarker for severe pandemic H1N1 influenza A infection. PLoS One 7:e38214. http://dx.doi.org/10.1371/journal.pone.0038214.
12. Yu X, Zhang X, Zhao B, Wang J, Zhu Z, Teng Z, Shao J, Shen J, Gao Y, Yuan Z, Wu F. 2011. Intensive cytokine induction in pandemic H1N1 influenza virus infection accompanied by robust production of IL-10 and IL-6. PLoS One 6:e28680. http://dx.doi.org/10.1371/journal.pone.0028680.
13. Hayden FG, Treanor JJ, Fritz RS, Lobo M, Betts RF, Miller M, Kinnersley N, Mills RG, Ward P, Straus SE. 1999. Use of the oral neuraminidase inhibitor oseltamivir in experimental human influenza: randomized controlled trials for prevention and treatment. JAMA 282:1240-1246. http://dx.doi.org/10.1001/jama.282.13.1240.
14. Maines T, Belser J, Gustin K, van Hoeven N, Zeng H, Svitek N, von Messling V, Katz J, Tumpey T. 2012. Local innate immune responses and influenza virus transmission and virulence in ferrets. J Infect Dis 205:474-485. http://dx.doi.org/10.1093/infdis/jir768.
15. Meunier I, Embury-Hyatt C, Stebner S, Gray M, Bastien N, Li Y, Plummer F, Kobinger G, von Messling V. 2012. Virulence differences of closely related pandemic 2009 H1N1 isolates correlate with increased inflammatory responses in ferrets. Virology 422:125-131. http://dx.doi.org/10.1016/j.virol.2011.10.018.
16. Svitek N, Rudd P, Obojes K, Pillet S, von Messling V. 2008. Severe seasonal influenza in ferrets correlates with reduced interferon and increased IL-6 induction. Virology 376:53-59. http://dx.doi.org/10.1016/j.virol.2008.02.035.
17. Korteweg C, Gu J. 2010. Pandemic influenza A (H1N1) virus infection and avian influenza A (H5N1) virus infection: a comparative analysis. Biochem Cell Biol 88:575-587. http://dx.doi.org/10.1139/O10-017.
18. Wang C, Yu H, Horby PW, Cao B, Wu P, Yang S, Gao H, Li H, Tsang TK, Liao Q, Gao Z, Ip DKM, Jia H, Jiang H, Liu B, Ni MY, Dai X, Liu F, Van Kinh N, Liem NT, Hien TT, Li Y, Yang J, Wu JT, Zheng Y, Leung GM, Farrar JJ, Cowling BJ, Uyeki TM, Li L. 2014. Comparison of patients hospitalized with influenza A subtypes H7N9, H5N1, and 2009 pandemic H1N1. Clin Infect Dis 58:1095-1103. http://dx.doi.org/10.1093/cid/ciu053.
19. Reed C, Chaves SS, Perez A, D'Mello T, Kirley PD, Aragon D, Meek JI, Farley MM, Ryan P, Lynfield R, Morin CA, Hancock EB, Bennett NM, Zansky SM, Thomas A, Lindegren ML, Schaffner W, Finelli L. 2014. Complications among adults hospitalized with influenza: a comparison of seasonal influenza and the 2009 H1N1 pandemic. Clin Infect Dis 59:166-174. http://dx.doi.org/10.1093/cid/ciu285.
20. Carcione D, Giele C, Dowse MDGK, Goggin L, Kwan K, Williams S, Smith D, Effler P. 2010. Comparison of pandemic (H1N1)2009 and seasonal influenza, Western Australia, 2009. Emerg Infect Dis 16:1388-1395. http://dx.doi.org/10.3201/eid1609.100076.
21. Chang Y-S, van Hal SJ, Spencer PM, Gosbell IB, Collett PW. 2010. Comparison of adult patients hospitalised with pandemic (H1N1) 2009 influenza and seasonal influenza during the "PROTECT" phase of the pandemic response. Med J Aust 192:90-93.
22. Kang Y, Song B, Lee J, Kim H, Seo S. 2011. Pandemic H1N1 influenza virus causes a stronger inflammatory response than seasonal H1N1 influenza virus in ferrets. Arch Virol 156:759-767. http://dx.doi.org/10.1007/s00705-010-0914-7.
23. Rowe T, León A, Crevar C, Carter D, Xu L, Ran L, Fang Y, Cameron C, Cameron M, Banner D, Ng D, Ran R, Weirback H, Wiley C, Kelvin D, Ross T. 2010. Modeling host responses in ferrets during A/California/07/2009 influenza infection. Virology 401:257-265. http://dx.doi.org/10.1016/j.virol.2010.02.020.
24. Carolan LA, Butler J, Rockman S, Guarnaccia T, Hurt AC, Reading PA, Kelso A, Barr A, Laurie KL. 2014. TaqMan real time RT-PCR assays for detecting ferret innate and adaptive immune responses. J Virol Methods 205:38-52. http://dx.doi.org/10.1016/j.jviromet.2014.04.014.
25. McVernon J, Laurie KL, Nolan T, Owen R, Irving D, Capper H, Hyland C, Faddy H, Carolan L, Barr I, Kelso A. 2010. Seroprevalence of 2009 pandemic influenza A(H1N1) virus in Australian blood donors, October-December 2009. Eurosurveillance 15:19678.
26. Oh DY, Barr IG, Mosse JA, Laurie KL. 2008. MDCK-SIAT1 cells show improved isolation rates for recent human influenza viruses compared to conventional MDCK cells. J Clin Microbiol 46:2189-2194. http://dx.doi.org/10.1128/JCM.00398-08.
27. Guarnaccia T, Carolan LA, Maurer-Stroh S, Lee RTC, Job E, Reading PC, Petrie S, McCaw JM, McVernon J, Hurt AC, Kelso A, Mosse J, Barr IG, Laurie KL. 2013. Antigenic drift of the pandemic 2009 A(H1N1) influenza virus in a ferret model. PLoS Pathog 9:e1003354. http://dx.doi.org/10.1371/journal.ppat.1003354.
28. Laurie KL, Guarnaccia TA, Carolan LA, Yan AWC, Aban M, Petrie S, Cao P, Heffernan JM, McVernon J, Mosse J, Kelso A, McCaw JM, Barr IG. 5 May 2015. Interval between infections and viral hierarchies are determinants of viral interference following influenza virus infection in a ferret model. J Infect Dis http://dx.doi.org/10.1093/infdis/jiv260.
29. Chaves SS, Aragon D, Bennett N, Cooper T, D'Mello T, Farley M, Fowler B, Hancock E, Daily Kirley P, Lynfield R, Ryan P, Schaffner W, Sharangpani R, Tengelsen L, Thomas A, Thurston D, Williams J, Yousey-Hindes K, Zansky S, Finelli L. 2013. Patients hospitalized with laboratory-confirmed influenza during the 2010-2011 influenza season: exploring disease severity by virus type and subtype. J Infect Dis 208:1305-1314. http://dx.doi.org/10.1093/infdis/jit316.
30. Dawood FS, Chaves SS, Pérez A, Reingold A, Meek J, Farley MM, Ryan P, Lynfield R, Morin C, Baumbach J, Bennett NM, Zansky S, Thomas A, Lindegren ML, Schaffner W, Finelli L. 2014. Complications and associated bacterial coinfections among children hospitalized with seasonal or pandemic influenza, United States, 2003-2010. J Infect Dis 209: 686-694. http://dx.doi.org/10.1093/infdis/jit473.
31. Irving SA, Patel DC, Kieke BA, Donahue JG, Vandermause MF, Shay DK, Belongia EA. 2012. Comparison of clinical features and outcomes of medically attended influenza A and influenza B in a defined population over four seasons: 2004-2005 through 2007-2008. Influenza Other Respir Viruses 6:37-43. http://dx.doi.org/10.1111/j.1750-2659.2011.00263.x.
32. Silvennoinen H, Peltola V, Vainionpää R, Ruuskanen O, Heikkinen T. 2012. Admission diagnoses of children 0-16 years of age hospitalized with influenza. Eur J Clin Microbiol Infect Dis 31:225-231. http://dx.doi.org/10.1007/s10096-011-1297-8.
33. Silvennoinen HS, Peltola V, Vainionpää R, Ruuskanen O, Heikkinen T. 2011. Incidence of influenza-related hospitalizations in different age groups of children in Finland. A 16-year study. Pediatr Infect Dis J 30:e24. http://dx.doi.org/10.1097/INF.0b013e3181fe37c8.
34. Punpanich W, Chotpitayasunondh T. 2012. A review on the clinical spectrum and natural history of human influenza. Int J Infect Dis 16: e714-e723. http://dx.doi.org/10.1016/j.ijid.2012.05.1025.
35. Belser JA, Katz JM, Tumpey TM. 2011. The ferret as a model organism to study influenza A virus infection. Dis Model Mech 4:575-579. http://dx.doi.org/10.1242/dmm.007823.
36. Jayaraman A, Chandrasekaran A, Viswanathan K, Raman R, Fox JG, Sasisekharan R. 2012. Decoding the distribution of glycan receptors for human-adapted influenza A viruses in ferret respiratory tract. PLoS One 7:e27517. http://dx.doi.org/10.1371/journal.pone.0027517.
37. O'Donnell CD, Subbarao K. 2011. The contribution of animal models to the understanding of the host range and virulence of influenza A viruses. Microbes Infect 13:502-515. http://dx.doi.org/10.1016/j.micinf.2011.01.014.
38. Kobinger G, Meunier I, Patel A, Pillet S, Gren J, Stebner S, Leung A, Neufeld J, Kobasa D, von Messling V. 2010. Assessment of the efficacy of commercially available and candidate vaccines against a pandemic H1N1 2009 virus. J Infect Dis 201:1000-1006. http://dx.doi.org/10.1086/651171.
39. Deshmane SL, Kremlev S, Amini S, Sawaya BE. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313-326. http://dx.doi.org/10.1089/jir.2008.0027.
40. Leon AJ, Banner D, Xu L, Ran L, Peng Z, Ti K, Chen C, Xu F, Huang J, Zhao Z, Lin Z, Huang SHS, Fang Y, Kelvin AA, Ross TM, Farooqui A, Kelvin DJ. 2013. Sequencing, annotation, and characterization of the influenza ferret infectome. J Virol 87:1957-1966. http://dx.doi.org/10.1128/JVI.02476-12.
41. Takano T, Tajiri H, Kashiwagi Y, Kiura S, Kawashima H. 2011. Cytokine and chemokine response in children with the 2009 pandemic influenza A (H1N1) virus infection. Eur J Clin Microbiol Infect Dis 30:117-120. http://dx.doi.org/10.1007/s10096-010-1041-9.
42. Gao R, Bhatnagar J, Blau DM, Greer P, Rollin DC, Denison AM, Deleon-Carnes M, Shieh W-J, Sambhara S, Tumpey TM, Patel M, Liu L, Paddock C, Drew C, Shu Y, Katz JM, Zaki SR. 2013. Cytokine and chemokine profiles in lung tissues from fatal cases of 2009 pandemic influenza A(H1N1): role of the host immune response in pathogenesis. Am J Pathol 183:1258-1268. http://dx.doi.org/10.1016/j.ajpath.2013.06.023.
43. Khatri M, Dwivedi V, Krakowka S, Manickam C, Ali A, Wang L, Qin Z, Renukaradhya GJ, Lee CW. 2010. Swine influenza H1N1 virus induces acute inflammatory immune responses in pig lungs: a potential animal model for human H1N1 influenza virus. J Virol 84:11210-11218. http://dx.doi.org/10.1128/JVI.01211-10.
44. Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y, Hatta M, Muramoto Y, Tamura D, Sakai-Tagawa Y, Noda T, Sakabe S, Imai M, Hatta Y, Watanabe S, Li C, Yamada S, Fujii K, Murakami S, Imai H, Kakugawa S, Ito M, Takano R, Iwatsuki-Horimoto K, Shimojima M, Horimoto T, Goto H, Takahashi K, Makino A, Ishigaki H, Nakayama M, Okamatsu M, Warshauer D, Shult PA, Saito R, Suzuki H, Furuta Y, Yamashita M, Mitamura K, Nakano K, Nakamura M, Brockman-Schneider R, Mitamura H, Yamazaki M, Sugaya N, Suresh M, Ozawa M, Neumann G, Gern J, Kida H, Ogasawara K, Kawaoka Y. 2009. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460: 1021-1025. http://dx.doi.org/10.1038/nature08260.
45. Kim Y, Kim H, Cho S, Seo S. 2009. Influenza B virus causes milder pathogenesis and weaker inflammatory responses in ferrets than influenza A virus. Viral Immunol 22:423-430. http://dx.doi.org/10.1089/vim.2009.0045.
46. Bodewes R, Kreijtz JH, van Amerongen G, Fouchier RA, Osterhaus AD, Rimmelzwaan GF, Kuiken T. 2011. Pathogenesis of influenza A/H5N1 virus infection in ferrets differs between intranasal and intratracheal routes of inoculation. Am J Pathol 179:30-36. http://dx.doi.org/10.1016/j.ajpath.2011.03.026.
47. Belser JA, Gustin KM, Maines TR, Pantin-Jackwood MJ, Katz JM, Tumpey TM. 2012. Influenza virus respiratory infection and transmission following ocular inoculation in ferrets. PLoS Pathog 8:e1002569. http://dx.doi.org/10.1371/journal.ppat.1002569.
48. Moore IN, Lamirande EW, Paskel M, Donahue D, Qin J, Subbarao K. 2014. Severity of clinical disease and pathology in ferrets experimentally infected with influenza viruses is influenced by inoculum volume. J Virol 88:13879-13891. http://dx.doi.org/10.1128/JVI.02341-14.
49. van den Brand JM, Stittelaar KJ, Leijten LM, van Amerongen G, Simon JH, Osterhaus AD, Kuiken T. 2012. Modification of the ferret model for pneumonia from seasonal human influenza A virus infection. Vet Pathol 49:562-568. http://dx.doi.org/10.1177/0300985811429812.
50. Martel C, Aasted B. 2009. Characterization of antibodies against ferret immunoglobulins, cytokines and CD markers. Vet Immunol Immunopathol 132:109-115. http://dx.doi.org/10.1016/j.vetimm.2009.05.011.
51. Pillet S, Kobasa D, Meunier I, Gray M, Laddy D, Weiner D, von Messling V, Kobinger G. 2011. Cellular immune response in the presence of protective antibody levels correlates with protection against 1918 influenza in ferrets. Vaccine 29:6793-6801. http://dx.doi.org/10.1016/j.vaccine.2010.12.059.
52. Rutigliano J, Doherty P, Franks J, Morris M, Reynolds C, Thomas P. 2008. Screening monoclonal antibodies for cross-reactivity in the ferret model of influenza infection. J Immunol Methods 336:71-77. http://dx.doi.org/10.1016/j.jim.2008.04.003.
53. Music N, Reber AJ, Lipatov AS, Kamal RP, Blanchfield K, Wilson JR, Donis RO, Matz JM, York IA. 2014. Influenza vaccination accelerates recovery of ferrets from lymphopenia. PLoS One 9:e100926. http://dx.doi.org/10.1371/journal.pone.0100926.
54. Vandesompele J, de Preter K, Pattyn F, Poppe B, van Roy N, de Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034.