A novel outbred mouse model of 2009 pandemic influenza and bacterial co-infection severity

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  McHugh, Kevin J ^a   Mandalapu, Sivanarayana ^a   Kolls, Jay K ^a   Ross, Ted M ^b,c   Alcorn, John F ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c Vaccine and Gene Therapy Institute of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

2009 H1N1 INFLUENZA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE SEVERITY; HISTOPATHOLOGY; INFECTION RISK; MALE; MIXED INFECTION; MOUSE; NONHUMAN; OUTBRED MOUSE STRAIN; PHENOTYPE; STAPHYLOCOCCUS INFECTION; VIRUS LOAD; WEIGHT REDUCTION;

ANIMALS; ANIMALS, OUTBRED STRAINS; BACTERIAL LOAD; CHICK EMBRYO; COINFECTION; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; MALE; MICE; ORTHOMYXOVIRIDAE INFECTIONS; PHENOTYPE; PNEUMONIA; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRAL LOAD; WEIGHT LOSS;

EID: 84891908659     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082865     Document Type: Article

References (47)

1. Taubenberger JK, Morens DM (2006) 1918 Influenza: the mother of all pandemics. Emerg Infect Dis 12:15-22. doi:10.3201/eid1209.050979. PubMed: 16494711. (Pubitemid 43143529)
2. Nguyen-Van-Tam JS, Hampson AW (2003) The epidemiology and clinical impact of pandemic influenza. Vaccine 21:1762-1768. doi: 10.1016/S0264-410X (03) 00069-0. PubMed: 12686091. (Pubitemid 36398370)
3. Morens DM, Taubenberger JK, Fauci AS (2008) Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 198:962-970. doi:10.1086/591708. PubMed: 18710327.
4. Reed C, Angulo FJ, Swerdlow DL, Lipsitch M, Meltzer MI et al. (2009) Estimates of the prevalence of pandemic (H1N1) 2009, United States, April-July 2009. Emerg Infect Dis 15:2004-2007. doi:10.3201/eid1512.091413. PubMed: 19961687.
5. enters for Disease Control and Prevention (CDC) (2009) Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1) - United States, May-August 2009. MMWR Morb Mortal Wkly Rep 58:1071-1074. PubMed: 19798021.
6. Jakab GJ, Warr GA, Knight ME (1979) Pulmonary and systemic defenses against challenge with Staphylococcus aureus in mice with pneumonia due to influenza A virus. J Infect Dis 140:105-108. doi: 10.1093/infdis/140.1.105. PubMed: 458195. (Pubitemid 9238502)
7. Small CL, Shaler CR, McCormick S, Jeyanathan M, Damjanovic D et al. (2010) Influenza infection leads to increased susceptibility to subsequent bacterial superinfection by impairing NK cell responses in the lung. J Immunol 184:2048-2056. doi:10.4049/jimmunol.0902772. PubMed: 20083661.
8. Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L et al. (2008) Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 205:323-329. doi:10.1084/jem.20070891. PubMed: 18227219. (Pubitemid 351281598)
9. Goulding J, Snelgrove R, Saldana J, Didierlaurent A, Cavanagh M et al. (2007) Respiratory infections: do we ever recover? Proc Am Thorac Soc 4:618-625. doi:10.1513/pats.200706-066TH. PubMed: 18073393. (Pubitemid 350291624)
10. McCullers JA, Bartmess KC (2003) Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J Infect Dis 187:1000-1009. doi:10.1086/368163. PubMed: 12660947. (Pubitemid 36337913)
11. Miettinen M, Sareneva T, Julkunen I, Matikainen S (2001) IFNs activate toll-like receptor gene expression in viral infections. Genes Immun 2:349-355. doi:10.1038/sj.gene.6363791. PubMed: 11607792. (Pubitemid 33674248)
12. Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM et al. (2011) Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 186:1666-1674. doi:10.4049/jimmunol.1002194. PubMed: 21178015.
13. Shahangian A, Chow EK, Tian X, Kang JR, Ghaffari A et al. (2009) Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 119:1910-1920. doi:10.1172/JCI35412. PubMed: 19487810.
14. Sun K, Metzger DW (2008) Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med 14:558-564. doi:10.1038/nm1765. PubMed: 18438414. (Pubitemid 351655219)
15. Li W, Moltedo B, Moran TM (2012) Type I interferon induction during influenza virus infection increases susceptibility to secondary Streptococcus pneumoniae infection by negative regulation of gammadelta T cells. J Virol 86:12304-12312. doi:10.1128/JVI. 01269-12. PubMed: 22951826.
16. Tashiro M, Ciborowski P, Klenk HD, Pulverer G, Rott R (1987) Role of Staphylococcus protease in the development of influenza pneumonia. Nature 325:536-537. doi:10.1038/325536a0. PubMed: 3543690. (Pubitemid 17056736)
17. Tashiro M, Ciborowski P, Reinacher M, Pulverer G, Klenk HD et al. (1987) Synergistic role of staphylococcal proteases in the induction of influenza virus pathogenicity. Virology 157:421-430. doi: 10.1016/0042-6822 (87) 90284-4. PubMed: 3029981. (Pubitemid 17047697)
18. Zhang WJ, Sarawar S, Nguyen P, Daly K, Rehg JE et al. (1996) Lethal synergism between influenza infection and staphylococcal enterotoxin B in mice. J Immunol 157:5049-5060. PubMed: 8943414. (Pubitemid 126449586)
19. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J et al. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29:1303-1310. doi:10.1097/00003246-200107000-00002. PubMed: 11445675. (Pubitemid 32641789)
20. Martin GS, Mannino DM, Eaton S, Moss M (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348:1546-1554. doi:10.1056/NEJMoa022139. PubMed: 12700374. (Pubitemid 36437931)
21. Beadling C, Slifka MK (2004) How do viral infections predispose patients to bacterial infections? Curr Opin Infect Dis 17:185-191. doi: 10.1097/00001432-200406000-00003. PubMed: 15166819. (Pubitemid 38703845)
22. Vardakas KZ, Matthaiou DK, Falagas ME (2009) Comparison of community-acquired pneumonia due to methicillin-resistant and methicillin-susceptible Staphylococcus aureus producing the Panton-Valentine leukocidin. Int J Tuberc Lung Dis 13:1476-1485. PubMed: 19919764.
23. Williams DJ, Hall M, Brogan TV, Farris RW, Myers AL et al. (2011) Influenza coinfection and outcomes in children with complicated pneumonia. Arch Pediatr Adolesc Med 165:506-512. doi:10.1001/archpediatrics.2010.295. PubMed: 21300649.
24. Chia R, Achilli F, Festing MF, Fisher EM (2005) The origins and uses of mouse outbred stocks. Nat Genet 37:1181-1186. doi:10.1038/ng1665. PubMed: 16254564. (Pubitemid 41568697)
25. Chesler EJ, Miller DR, Branstetter LR, Galloway LD, Jackson BL et al. (2008) The Collaborative Cross at Oak Ridge National Laboratory: developing a powerful resource for systems genetics. Mamm Genome 19:382-389. doi:10.1007/s00335-008-9135-8. PubMed: 18716833.
26. Bottomly D, Ferris MT, Aicher LD, Rosenzweig E, Whitmore A, et al. (2012) Expression quantitative trait Loci for extreme host response to influenza a in pre-collaborative cross mice. G3 (Bethesda) 2:213-221.
27. Ferris MT, Aylor DL, Bottomly D, Whitmore AC, Aicher LD et al. (2013) Modeling host genetic regulation of influenza pathogenesis in the collaborative cross. PLoS Pathog 9:e1003196. PubMed: 23468633.
28. Crowe CR, Chen K, Pociask DA, Alcorn JF, Krivich C et al. (2009) Critical role of IL-17RA in immunopathology of influenza infection. J Immunol 183:5301-5310. doi:10.4049/jimmunol.0900995. PubMed: 19783685.
29. Davey RT Jr, Lynfield R, Dwyer DE, Losso MH, Cozzi-Lepri A et al. (2013) The association between serum biomarkers and disease outcome in influenza A (H1N1) pdm09 virus infection: results of two international observational cohort studies. PLOS ONE 8:e57121. doi: 10.1371/journal.pone.0057121. PubMed: 23468921.
30. Hagau N, Slavcovici A, Gonganau DN, Oltean S, Dirzu DS et al. (2010) Clinical aspects and cytokine response in severe H1N1 influenza A virus infection. Crit Care 14:R203. doi:10.1186/cc8155. PubMed: 21062445.
31. Yu X, Zhang X, Zhao B, Wang J, Zhu Z et al. (2011) Intensive cytokine induction in pandemic H1N1 influenza virus infection accompanied by robust production of IL-10 and IL-6. PLOS ONE 6:e28680. doi: 10.1371/journal.pone. 0028680. PubMed: 22174866.
32. Dienz O, Rud JG, Eaton SM, Lanthier PA, Burg E et al. (2012) Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol 5:258-266. doi:10.1038/mi.2012.2. PubMed: 22294047.
33. Longhi MP, Wright K, Lauder SN, Nowell MA, Jones GW et al. (2008) Interleukin-6 is crucial for recall of influenza-specific memory CD4 T cells. PLoS Pathog 4:e1000006. PubMed: 18389078.
34. Li C, Yang P, Sun Y, Li T, Wang C et al. (2012) IL-17 response mediates acute lung injury induced by the 2009 pandemic influenza A (H1N1) virus. Cell Res 22:528-538. doi:10.1038/cr.2011.165.
35. Kumar P, Thakar MS, Ouyang W, Malarkannan S (2013) IL-22 from conventional NK cells is epithelial regenerative and inflammation protective during influenza infection. Mucosal Immunol 6:69-82. doi: 10.1038/mi.2012.49. PubMed: 22739232.
36. Paget C, Ivanov S, Fontaine J, Renneson J, Blanc F et al. (2012) Interleukin-22 is produced by invariant natural killer T lymphocytes during influenza A virus infection: potential role in protection against lung epithelial damages. J Biol Chem 287:8816-8829. doi:10.1074/jbc. M111.304758. PubMed: 22294696.
37. Pociask DA, Scheller EV, Mandalapu S, McHugh KJ, Enelow RI et al. (2013) IL-22 Is Essential for Lung Epithelial Repair following Influenza Infection. Am J Pathol 182:1286-1296. doi:10.1016/j.ajpath. 2012.12.007.
38. Cameron CM, Cameron MJ, Bermejo-Martin JF, Ran L, Xu L et al. (2008) Gene expression analysis of host innate immune responses during Lethal H5N1 infection in ferrets. J Virol 82:11308-11317. doi: 10.1128/JVI.00691-08. PubMed: 18684821.
39. Fadel SA, Bromley SK, Medoff BD, Luster AD (2008) CXCR3-deficiency protects influenza-infected CCR5-deficient mice from mortality. Eur J Immunol 38:3376-3387. doi:10.1002/eji.200838628. PubMed: 19039768.
40. Ichikawa A, Kuba K, Morita M, Chida S, Tezuka H et al. (2013) CXCL10-CXCR3 enhances the development of neutrophil-mediated fulminant lung injury of viral and nonviral origin. Am J Respir Crit Care Med 187:65-77. doi:10.1164/rccm.201203-0508OC. PubMed: 23144331.
41. García-Sastre A (2011) Induction and evasion of type I interferon responses by influenza viruses. Virus Res 162:12-18. doi:10.1016/j.virusres. 2011.10.017. PubMed: 22027189.
42. Coro ES, Chang WL, Baumgarth N (2006) Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection. J Immunol 176:4343-4351. PubMed: 16547272. (Pubitemid 44264414)
43. Kohlmeier JE, Cookenham T, Roberts AD, Miller SC, Woodland DL (2010) Type I interferons regulate cytolytic activity of memory CD8 (+) T cells in the lung airways during respiratory virus challenge. Immunity 33:96-105. doi:10.1016/j.immuni.2010.06.016. PubMed: 20637658.
44. Jia D, Rahbar R, Chan RW, Lee SM, Chan MC et al. (2010) Influenza virus non-structural protein 1 (NS1) disrupts interferon signaling. PLOS ONE 5:e13927. doi:10.1371/journal.pone.0013927. PubMed: 21085662.
45. Wu CL, Lee YL, Chang KM, Chang GC, King SL et al. (2003) Bronchoalveolar interleukin-1 beta: a marker of bacterial burden in mechanically ventilated patients with community-acquired pneumonia. Crit Care Med 31:812-817. doi:10.1097/01. CCM. 0000054865.47068.58. PubMed: 12626989.
46. Miller LS, Pietras EM, Uricchio LH, Hirano K, Rao S et al. (2007) Inflammasome-mediated production of IL-1beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J Immunol 179:6933-6942. PubMed: 17982084.
47. Robinson KM, Choi SM, McHugh KJ, Mandalapu S, Enelow RI et al. (2013) Influenza A Exacerbates Staphylococcus aureus Pneumonia by Attenuating IL-1beta Production in Mice. J Im ol.