A mouse model of lethal synergism between influenza virus and Haemophilus influenzae

American Journal of Pathology

Volumn 176, Issue 2, 2010, Pages 800-811

  Lee, Lian Ni ^a,c   Dias, Peter ^a   Han, Dongun ^a,d   Yoon, Sorah ^a,e   Shea, Ashley ^a   Zakharov, Vladislav ^b   Parham, David ^b   Sarawar, Sally R ^a  

^a TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d Cheonan Yonam College   (South Korea)

^e Animal Plant and Fisheries Quarantine and Inspection Agency   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CXCR3; FAS ANTIGEN; INTERLEUKIN 6; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BRAIN; BRONCHUS MUCOSA; CELL DEATH; CONTROLLED STUDY; DISEASE SEVERITY; EPITHELIUM CELL; FEMALE; HAEMOPHILUS INFECTION; HAEMOPHILUS INFLUENZAE; IMMUNOCOMPETENCE; IMMUNOCOMPETENT CELL; INFLUENZA; INFLUENZA VIRUS; INNATE IMMUNITY; INOCULATION; KNOCKOUT MOUSE; LETHAL SYNERGISM; LETHALITY; LUNG INJURY; MIXED INFECTION; MORTALITY; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; SECONDARY INFECTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS VIRULENCE; WILD TYPE;

EID: 76149100613     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090596     Document Type: Article

References (93)

1. Simonsen L: The global impact of influenza on morbidity and mortality. Vaccine 1999, 17(Suppl 1):S3-S10
2. Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB: Cox NJ, Fukuda K: Influenza-associated hospitalizations in the United States. JAMA 2004, 292:1333-1340
3. Wong CM, Chan KP, Hedley AJ, Peiris JS: Influenza-associated mortality in Hong Kong. Clin Infect Dis 2004, 39:1611-1617
4. Yap FH, Ho PL, Lam KF, Chan PK, Cheng YH, Peiris JS: Excess hospital admissions for pneumonia, chronic obstructive pulmonary disease, and heart failure during influenza seasons in Hong Kong. J Med Virol 2004, 73:617-623
5. Sethi S: Bacterial pneumonia. Managing a deadly complication of influenza in older adults with comorbid disease Geriatrics 2002, 57:56-61
6. Hament JM, Kimpen JL, Fleer A, Wolfs TF: Respiratory viral infection predisposing for bacterial disease: a concise review. FEMS Immunol Med Microbiol 1999, 26:189-195
7. Loosli CG: Influenza and the interaction of viruses and bacteria in respiratory infections. Medicine (Baltimore) 1973, 52:369-384
8. Seki M, Kosai K, Yanagihara K, Higashiyama Y, Kurihara S, Izumikawa K, Miyazaki Y, Hirakata Y, Tashiro T, Kohno S: Disease severity in patients with simultaneous influenza and bacterial pneumonia. Intern Med 2007, 46:953-958
9. McCullers JA, Webster R: A mouse model of dual infection with influenza virus and Streptococcus pneumoniae. Options for control of influenza IV. Edited by Osterhaus A, Cox N, Hampson A. Amsterdam. Elsevier Science, 2001, pp 601-607
10. Okamoto S, Kawabata S, Nakagawa I, Okuno Y, Goto T, Sano K, Hamada S: Influenza A virus-infected hosts boost an invasive type of Streptococcus pyogenes infection in mice. J Virol 2003, 77: 4104-4112
11. Alonso JM, Guiyoule A, Zarantonelli ML, Ramisse F, Pires R, Antignac A, Deghmane AE, Huerre M, van der Werf S, Taha MK: A model of meningococcal bacteremia after respiratory superinfection in influenza A virus-infected mice. FEMS Microbiol Lett 2003, 222:99-106
12. Jarstrand C, Tunevall G: The influence of bacterial superinfection on the clinical course of influenza. Studies from the influenza epidemics in Stockholm during the winters 1969-70 and 1971-72. Scand J Infect Dis 1975, 7:243-247
13. Schwarzmann SW, Adler JL, Sullivan RJ Jr, Marine WM: Bacterial pneumonia during the Hong Kong influenza epidemic of 1968-1969. Arch Intern Med 1971, 127:1037-1041
14. Kilbourne ED: Influenza. New York, Plenum, 1987, pp 220-240
15. McCullers JA: Insights into the interaction between influenza virus and pneumococcus. Clin Microbiol Rev 2006, 19:571-582
16. Morens DM, Taubenberger JK, Fauci AS: Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008, 198:962-970
17. Taubenberger JK, Morens DM: The pathology of influenza virus infections. Annu Rev Pathol 2008, 3:499-522
18. Brundage JF, Shanks GD: Deaths from bacterial pneumonia during 1918-19 influenza pandemic. Emerg Infect Dis 2008, 14:1193-1199
19. Brundage JF, Shanks GD: What really happened during the 1918 influenza pandemic? The importance of bacterial secondary infections. J Infect Dis 2007, 196:1717-1719
20. Levine J, Buchman CA, Fregien N: Influenza A virus infection of human Schwann cells in vitro. Acta Otolaryngol 2003, 123:41-45
21. Wyde PR, Six HR, Ambrose MW, Throop BJ: Influenza virus infection and bacterial clearance in young adult and aged mice. J Gerontol 1989, 44:B118-B124
22. Nickerson CL, Jakab GJ: Pulmonary antibacterial defenses during mild and severe influenza virus infection. Infect Immun 1990, 58:2809-2814
23. Gardner ID, Kung TM: Histopathological changes in the lungs of influenza-infected mice superinfected with Staphylococcus aureus. Br J Exp Pathol 1980, 61:415-420
24. Aubrey R, Tang C: The pathogenesis of disease due to Type b Haemophilus influenzae. Methods in Molecular Medicine, vol 71: Haemophilus influenzae Protocols. Edited by Herbert M, Hood DW, Moxon ER. Totowa, NJ, Humana Press, 2002, pp 29-50
25. Chin CL, Manzel LJ, Lehman EE, Humlicek AL, Shi L, Starner TD, Denning GM, Murphy TF, Sethi S, Look DC: Haemophilus influenzae from patients with chronic obstructive pulmonary disease exacerbation induce more inflammation than colonizers. Am J Respir Crit Care Med 2005, 172:85-91
26. Masuda K, Masuda R, Nishi J, Tokuda K, Yoshinaga M, Miyata K: Incidences of nasopharyngeal colonization of respiratory bacterial pathogens in Japanese children attending day-care centers. Pediatr Int 2002, 44:376-380
27. Wilkinson TM, Hurst JR, Perera WR, Wilks M, Donaldson GC, Wedzicha JA: Effect of interactions between lower airway bacterial and rhinoviral infection in exacerbations of COPD. Chest 2006, 129:317-324
28. Grant GB, Campbell H, Dowell SF, Graham SM, Klugman KP, Mulholland EK, Steinhoff M, Weber MW, Qazi S: Recommendations for treatment of childhood non-severe pneumonia. Lancet Infect Dis 2009, 9:185-196
29. Murphy TF: Respiratory infections caused by non-typeable Haemophilus influenzae. Curr Opin Infect Dis 2003, 16:129-134
30. Rosenstein NE, Perkins BA: Update on Haemophilus influenzae serotype b and meningococcal vaccines. Pediatr Clin North Am 2000, 47:337-352, vi
31. Burns IT, Zimmerman RK: Haemophilus influenzae type B disease, vaccines, and care of exposed individuals. J Fam Pract 2000, 49:S7-S14
32. Peltola H: Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clin Microbiol Rev 2000, 13:302-317
33. Peltola VT, McCullers JA: Respiratory viruses predisposing to bacterial infections: role of neuraminidase. Pediatr Infect Dis J 2004, 23:S87-S97
34. Broker M: Burden of invasive disease caused by Haemophilus influenzae type b in Asia. Jpn J Infect Dis 2009, 62:87-92
35. Ulanova M, Tsang RS: Invasive Haemophilus influenzae disease: changing epidemiology and host-parasite interactions in the 21st century. Infect Genet Evol 2009, 9:594-605
36. Takano M, Ozaki K, Nitahara Y, Higuchi W, Takano T, Nishiyama A, Yamamoto T: Streptococcus pneumoniae and Haemophilus influenzae at the initial stage of influenza. Pediatr Int 2009, 51:687-695
37. Shope R: Swine Influenza III. Filtration experiments and etiology. J Exp Med 1931, 54:373-385
38. Orticoni M, Barbie M, Auge M: Pathogenie de la Grippe. La Presse Medical 1919, 26:247-249
39. Michaels RH, Myerowitz RL, Klaw R: Potentiation of experimental meningitis due to Haemophilus influenzae by influenza A virus. J Infect Dis 1977, 135:641-645
40. Bakaletz LO, Hoepf TM, DeMaria TF, Lim DJ: The effect of antecedent influenza A virus infection on the adherence of Hemophilus influenzae to chinchilla tracheal epithelium. Am J Otolaryngol 1988, 9:127-134
41. Francis T, de Torregrosa MV: Combined infection of mice with H. influenzae and influenza virus by the intranasal route. J Infect Dis 1944, 76:70-77
42. Tannock GA, Paul JA, Barry RD: Relative immunogenicity of the cold-adapted influenza virus A/Ann Arbor/6/60 (A/AA/6/60-ca), recombinants of A/AA/6/60-ca, and parental strains with similar surface antigens. Infect Immun 1984, 43:457-462
43. Lysenko E, Richards JC, Cox AD, Stewart A, Martin A, Kapoor M, Weiser JN: The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing. Mol Microbiol 2000, 35:234-245
44. Sarawar SR, Doherty PC: Concurrent production of interleukin-2, interleukin-10, and gamma interferon in the regional lymph nodes of mice with influenza pneumonia. J Virol 1994, 68:3112-3119
45. Matute-Bello G, Liles WC, Steinberg KP, Kiener PA, Mongovin S, Chi EY, Jonas M, Martin TR: Soluble Fas ligand induces epithelial cell apoptosis in humans with acute lung injury (ARDS). J Immunol 1999, 163:2217-2225
46. Wareing MD, Lyon AB, Lu B, Gerard C, Sarawar SR: Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J Leukoc Biol 2004, 76:886-895
47. Wareing MD, Lyon A, Inglis C, Giannoni F, Charo I, Sarawar SR: Chemokine regulation of the inflammatory response to a low-dose influenza infection in CCR2-/- mice. J Leukoc Biol 2007, 81:793-801
48. Kaufmann A, Salentin R, Meyer RG, Bussfeld D, Pauligk C, Fesq H, Hofmann P, Nain M, Gemsa D, Sprenger H: Defense against influenza A virus infection: essential role of the chemokine system. Immunobiology 2001, 204:603-613
49. Wang X, Moser C, Louboutin JP, Lysenko ES, Weiner DJ, Weiser JN, Wilson JM: Toll-like receptor 4 mediates innate immune responses to Haemophilus influenzae infection in mouse lung. J Immunol 2002, 168:810-815
50. Wieland CW, Florquin S, Maris NA, Hoebe K, Beutler B, Takeda K, Akira S, van der Poll T: The MyD88-dependent, but not the MyD88-independent, pathway of TLR4 signaling is important in clearing nontypeable haemophilus influenzae from the mouse lung. J Immunol 2005, 175:6042-6049
51. Zhang WJ, Sarawar S, Nguyen P, Daly K, Rehg JE, Doherty PC, Woodland DL, Blackman MA: Lethal synergism between influenza infection and staphylococcal enterotoxin B in mice. J Immunol 1996, 157:5049-5060
52. Conn CA, McClellan JL, Maassab HF, Smitka CW, Majde JA, Kluger MJ: Cytokines and the acute phase response to influenza virus in mice. Am J Physiol 1995, 268:R78-R84
53. Kaiser L, Fritz RS, Straus SE, Gubareva L, Hayden FG: Symptom pathogenesis during acute influenza: interleukin-6 and other cytokine responses. J Med Virol 2001, 64:262-268
54. Doughty L, Nguyen K, Durbin J, Biron C: A role for IFN-alpha beta in virus infection-induced sensitization to endotoxin. J Immunol 2001, 166:2658-2664
55. Nguyen KB, Biron CA: Synergism for cytokine-mediated disease during concurrent endotoxin and viral challenges: roles for NK and T cell IFN-gamma production. J Immunol 1999, 162:5238-5246
56. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B: Defective LPS signaling in C3H/HeJ and C57BL/ 10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088
57. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S: Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999, 162:3749-3752
58. Brundage JF: Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness. Lancet Infect Dis 2006, 6:303-312
59. Brundage JF: Cases and deaths during influenza pandemics in the United States. Am J Prev Med 2006, 31:252-256
60. Kawana A, Naka G, Fujikura Y, Kato Y, Mizuno Y, Kondo T, Kudo K: Spanish influenza in Japanese armed forces, 1918-1920. Emerg Infect Dis 2007, 13:590-593
61. Taubenberger JK, Morens DM: 1918 Influenza: the mother of all pandemics. Emerg Infect Dis 2006, 12:15-22
62. Luk J, Gross P, Thompson WW: Observations on mortality during the 1918 influenza pandemic. Clin Infect Dis 2001, 33:1375-1378
63. Morens DM, Fauci AS: The 1918 influenza pandemic: insights for the 21st century. J Infect Dis 2007, 195:1018-1028
64. Harford CG aH, A: Effect of influenza virus on cilia and epithelial cells in the bronchi of mice. J Exp Med 1952, 95:173-190
65. Qureshi ST, Lariviere L, Leveque G, Clermont S, Moore KJ, Gros P, Malo D: Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J Exp Med 1999, 189:615-625
66. Beutler B, Du X, Poltorak A: Identification of Toll-like receptor 4 (Tlr4) as the sole conduit for LPS signal transduction: genetic and evolutionary studies. J Endotoxin Res 2001, 7:277-280
67. Nain M, Hinder F, Gong JH, Schmidt A, Bender A, Sprenger H, Gemsa D: Tumor necrosis factor-alpha production of influenza A virus-infected macrophages and potentiating effect of lipopolysaccharides. J Immunol 1990, 145:1921-1928
68. Nansen A, Christensen JP, Marker O, Thomsen AR: Sensitization to lipopolysaccharide in mice with asymptomatic viral infection: role of T cell-dependent production of interferon-gamma. J Infect Dis 1997, 176:151-157
69. Nansen A, Randrup Thomsen A: Viral infection causes rapid sensitization to lipopolysaccharide: central role of IFN-alpha beta. J Immunol 2001, 166:982-988
70. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF, Gordon S, Guan Y, Peiris JS: Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 2002, 360:1831-1837
71. Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, Chan YO, Chan RW, Long HT, Poon LL, Guan Y, Peiris JS: Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir Res 2005, 6:135
72. Kash JC, Tumpey TM, Proll SC, Carter V, Perwitasari O, Thomas MJ, Basler CF, Palese P, Taubenberger JK, Garcia-Sastre A, Swayne DE, Katze MG: Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 2006, 443:578-581
73. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonti JB, Fernando L, Li Y, Katze MG, Feldmann H, Kawaoka Y: Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007, 445:319-323
74. McCullers JA, Rehg JE: Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J Infect Dis 2002, 186:341-350
75. LeVine AM, Koeningsknecht V, Stark JM: Decreased pulmonary clearance of S. pneumoniae following influenza A infection in mice. J Virol Methods 2001, 94:173-186
76. Speshock JL, Doyon-Reale N, Rabah R, Neely MN, Roberts PC: Filamentous influenza A virus infection predisposes mice to fatal septicemia following superinfection with Streptococcus pneumoniae serotype 3. Infect Immun 2007, 75:3102-3111
77. Kleinerman ES, Snyderman R, Daniels CA: Depressed monocyte chemotaxis during acute influenza infection. Lancet 1975, 2:1063-1066
78. Kleinerman ES, Daniels CA, Polisson RP, Snyderman R: Effect of virus infection on the inflammatory response. Depression of macrophage accumulation in influenza-infected mice Am J Pathol 1976, 85: 373-382
79. Dawson TC, Beck MA, Kuziel WA, Henderson F, Maeda N: Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol 2000, 156: 1951-1959
80. Lin KL, Suzuki Y, Nakano H, Ramsburg E, Gunn MD: CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J Immunol 2008, 180:2562-2572
81. Sun K, Metzger DW: Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med 2008, 14:558-564
82. Sarawar SR, Blackman MA, Doherty PC: Superantigen shock in mice with an inapparent viral infection. J Infect Dis 1994, 170:1189-1194
83. Navarini AA, Recher M, Lang KS, Georgiev P, Meury S, Bergthaler A, Flatz L, Bille J, Landmann R, Odermatt B, Hengartner H, Zinkernagel RM: Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses. Proc Natl Acad Sci USA 2006, 103:15535-15539
84. Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L, Bebien M, Lawrence T, van Rijt LS, Lambrecht BN, Sirard JC, Hussell T: Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 2008, 205: 323-329
85. Renegar KB: Influenza virus infections and immunity: a review of human and animal models. Lab Anim Sci 1992, 42:222-232
86. Wareing MD, Shea AL, Inglis CA, Dias PB, Sarawar SR: CXCR2 is required for neutrophil recruitment to the lung during influenza virus infection, but is not essential for viral clearance. Viral Immunol 2007, 20:369-378
87. McCullers JA, Bartmess KC: Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J Infect Dis 2003, 187:1000-1009
88. Peltola VT, Murti KG, McCullers JA: Influenza virus neuraminidase contributes to secondary bacterial pneumonia. J Infect Dis 2005, 192:249-257
89. Nugent KM, Pesanti EL: Tracheal function during influenza infections. Infect Immun 1983, 42:1102-1108
90. Plotkowski MC, Puchelle E, Beck G, Jacquot J, Hannoun C: Adherence of type I Streptococcus pneumoniae to tracheal epithelium of mice infected with influenza A/PR8 virus. Am Rev Respir Dis 1986, 134:1040-1044
91. Kawakami K, Ahmed K, Utsunomiya Y, Rikitomi N, Hori A, Oishi K, Nagatake T: Attachment of nontypable Haemophilus influenzae to human pharyngeal epithelial cells mediated by a ganglioside receptor. Microbiol Immunol 1998, 42:697-702
92. Memoli MJ, Morens DM, Taubenberger JK: Pandemic and seasonal influenza: therapeutic challenges. Drug Discov Today 2008, 13: 590-595
93. Active Bacterial Core Surveillance Report EIPN: Haemophilus influenzae 2006. Centers for Disease Control and Prevention, 2007, p 1