1918 H1N1 Influenza Virus Replicates and Induces Proinflammatory Cytokine Responses in Extrarespiratory Tissues of Ferrets

Journal of Infectious Diseases

Volumn 217, Issue 8, 2018, Pages 1237-1246

  De Wit, Emmie ^a   Siegers, Jurre Y ^b   Cronin, Jacqueline M ^a   Weatherman, Sarah ^a   Van Den Brand, Judith M ^b   Leijten, Lonneke M ^b   Van Run, Peter ^b   Begeman, Lineke ^b   Van Den Ham, Henk Jan ^b   Andeweg, Arno C ^b   Bushmaker, Trenton ^a   Scott, Dana P ^a   Saturday, Greg ^a   Munster, Vincent J ^a   Feldmann, Heinz ^a   Van Riel, Debby ^b  

^a National Institute   (New Zealand)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

1918 H1N1 virus; CNS disease; extrarespiratory; influenza A virus; pathogenesis

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 8; NUCLEOPROTEIN; TUMOR NECROSIS FACTOR; CYTOKINE;

1918 H1N1 INFLUENZA VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CYTOKINE RESPONSE; FEMALE; HEART; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INFANT; INFLUENZA A VIRUS (H1N1); INOCULATION; LIVER; LUNG PARENCHYMA; MUSTELA PUTORIUS FURO; NONHUMAN; OLFACTORY BULB; PANCREAS; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RESPIRATORY SYSTEM; SPANISH INFLUENZA; SPINAL CORD; UPREGULATION; VIROLOGY; VIRUS PATHOGENESIS; VIRUS REPLICATION; ANIMAL; BODY WEIGHT LOSS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INFLAMMATION; LUNG; METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; RESPIRATORY TRACT DISEASE; TISSUE DISTRIBUTION;

ANIMALS; CYTOKINES; FERRETS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY TRACT DISEASES; TISSUE DISTRIBUTION; VIRUS REPLICATION; WEIGHT LOSS;

EID: 85048083098     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiy003     Document Type: Article

References (32)

1. Korteweg C, Gu J. Pathology, molecular biology, and patho-genesis of avian infuenza A (H5N1) infection in humans. Am J Pathol 2008; 172:1155-70.
2. Kuiken T, Taubenberger JK. Pathology of human infuenza revisited. Vaccine 2008; 26(Suppl 4):D59-66.
3. Chi Y, Zhu Y, Wen T, et al. Cytokine and chemokine levels in patients infected with the novel avian infuenza A (H7N9) virus in China. J Infect Dis 2013; 208:1962-7.
4. de Jong MD, Simmons CP, Tanh TT, et al. Fatal outcome of human infuenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006; 12:1203-7.
5. Hayden FG, Fritz R, Lobo MC, Alvord W, Strober W, Straus SE. Local and systemic cytokine responses during experimental human infuenza A virus infection. Relation to symptom formation and host defense. J Clin Invest 1998; 101:643-9.
6. Skoner DP, Gentile DA, Patel A, Doyle WJ. Evidence for cyto-kine mediation of disease expression in adults experimentally infected with infuenza A virus. J Infect Dis 1999; 180:10-4.
7. Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG. Into the eye of the cytokine storm. Microbiol Mol Biol Rev 2012; 76:16-32.
8. Short KR, Veeris R, Leijten LM, et al. Proinfammatory cytokine responses in extra-respiratory tissues during severe infuenza. J Infect Dis 2017; 216:829-33.
9. Alexander JB. Cases resembling encephalitis lethargica occurring during the infuenza epidemic. Br Med J 1919; 1:794-5.
10. Holtenius J, Gillman A. The Spanish fu in Uppsala, clinical and epidemiological impact of the infuenza pandemic 1918-1919 on a Swedish county. Infect Ecol Epidemiol 2014; 4. doi:10.3402/iee.v4.21528.
11. Sheng ZM, Chertow DS, Ambroggio X, et al. Autopsy series of 68 cases dying before and during the 1918 infuenza pandemic peak. Proc Natl Acad Sci USA 2011; 108:16416-21.
12. Kash JC, Basler CF, Garcia-Sastre A, et al. Global host immune response: pathogenesis and transcriptional profl-ing of type A infuenza viruses expressing the hemagglu-tinin and neuraminidase genes from the 1918 pandemic virus. J Virol 2004; 78:9499-511.
13. Kobasa D, Takada A, Shinya K, et al. Enhanced virulence of infuenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 2004; 431:703-7.
14. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG. Characterization of the 1918 infuenza virus polymerase genes. Nature 2005; 437:889-93.
15. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Basler CF. Pathogenicity and immunogenicity of infuenza viruses with genes from the 1918 pandemic virus. Proc Natl Acad Sci USA 2004; 101:3166-71.
16. Watanabe T, Watanabe S, Shinya K, Kim JH, Hatta M, Kawaoka Y. Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets. Proc Natl Acad Sci USA 2009; 106:588-92.
17. Kobasa D, Jones SM, Shinya K, et al. Aberrant innate immune response in lethal infection of macaques with the 1918 infuenza virus. Nature 2007; 445:319-23.
18. National Institutes of Health. Guide for the care and use of laboratory animals. Available at: https://grants.nih.gov/grants/olaw/Guide-for-the-Care-and-use-of-laboratory-animals.pdf. Accessed 7 November 2017.
19. Rimmelzwaan GF, Baars M, Claas EC, Osterhaus AD. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofuorescence as methods for monitoring infuenza virus replication in vitro. J Virol Methods 1998; 74:57-66.
20. van Riel D, Rimmelzwaan GF, van Amerongen G, Osterhaus AD, Kuiken T. Highly pathogenic avian infuenza virus H7N7 isolated from a fatal human case causes respiratory disease in cats but does not spread systemically. Am J Pathol 2010; 177:2185-90.
21. Munster VJ, Baas C, Lexmond P, et al. Practical considerations for high-throughput infuenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J Clin Microbiol 2009; 47:666-73.
22. Carolan LA, Butler J, Rockman S, et al. TaqMan real time RT-PCR assays for detecting ferret innate and adaptive immune responses. J Virol Methods 2014; 205:38-52.
23. van den Brand JM, Stittelaar KJ, van Amerongen G, et al. Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian infuenza H5N1 virus infections in ferrets. PLoS One 2012; 7:e42343.
24. Edenborough KM, Lowther S, Laurie K, et al. Predicting disease severity and viral spread of H5N1 infuenza virus in ferrets in the context of natural exposure routes. J Virol 2015; 90:1888-97.
25. Schrauwen EJ, Herfst S, Leijten LM, et al. The multibasic cleavage site in H5N1 virus is critical for systemic spread along the olfactory and hematogenous routes in ferrets. J Virol 2012; 86:3975-84.
26. Yamada M, Bingham J, Payne J, et al. Multiple routes of invasion of wild-type clade 1 highly pathogenic avian infuenza H5N1 virus into the central nervous system (CNS) after intra-nasal exposure in ferrets. Acta Neuropathol 2012; 124:505-16.
27. Patton WD. Encephalitis lethargica: infuenza encephalitis. Can Med Assoc J 1927; 17:436-8.
28. Toms GL, Rosztoczy I, Smith H. The localization of infu-enza virus: minimal infectious dose determinations and single cycle kinetic studies on organ cultures of respiratory and other ferret tissues. Br J Exp Pathol 1974; 55:116-29.
29. Meunier I, Embury-Hyatt C, Stebner S, et al. Virulence differences of closely related pandemic 2009 H1N1 isolates correlate with increased infammatory responses in ferrets. Virology 2012; 422:125-31.
30. Calabrese F, Carturan E, Chimenti C, et al. Overexpression of tumor necrosis factor (TNF)alpha and TNFalpha receptor I in human viral myocarditis: clinicopathologic correlations. Mod Pathol 2004; 17:1108-18.
31. Siegers JY, van den Brand JM, Leijten LM, et al. Vaccination is more efective than prophylactic oseltamivir in preventing CNS invasion by H5N1 virus via the olfactory nerve. J Infect Dis 2016; 214:516-24.
32. Watanabe T, Zhong G, Russell CA, et al. Circulating avian infuenza viruses closely related to the 1918 virus have pandemic potential. Cell Host Microbe 2014; 15:692-705.