Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice

Journal of Virology

Volumn 84, Issue 15, 2010, Pages 7569-7580

  Tate, Michelle D ^a   Pickett, Danielle L ^a   Van Rooijen, Nico ^b   Brooks, Andrew G ^a   Reading, Patrick C ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c WHO COLLABORATING CENTRE FOR REFERENCE AND RESEARCH ON INFLUENZA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CLODRONIC ACID; CYTOKINE; LIPOSOME;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; INFLUENZA; INFLUENZA VIRUS; LUNG EDEMA; LUNG INJURY; LUNG PARENCHYMA; LYMPHOCYTOPENIA; MACROPHAGE; MALE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; THYMUS ATROPHY; VIRUS PNEUMONIA; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; BODY WEIGHT; CELLS, CULTURED; HISTOCYTOCHEMISTRY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; LEUKOCYTE REDUCTION PROCEDURES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA, VIRAL; SURVIVAL ANALYSIS; VIRULENCE;

MURINAE; MUS; ORTHOMYXOVIRIDAE;

EID: 77954492854     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00291-10     Document Type: Article

References (73)

1. Anders, E. M., C. A. Hartley, P. C. Reading, and R. A. Ezekowitz. 1994. Complement-dependent neutralization of influenza virus by a serum mannose-binding lectin. J. Gen. Virol. 75:615-622.
2. Ayala, A., C. S. Chung, J. L. Lomas, G. Y. Song, L. A. Doughty, S. H. Gregory, W. G. Cioffi, B. W. LeBlanc, J. Reichner, H. H. Simms, and P. S. Grutkoski. 2002. Shock-induced neutrophil mediated priming for acute lung injury in mice: divergent effects of TLR-4 and TLR-4/FasL deficiency. Am. J. Pathol. 161:2283-2294.
3. Baez, M., P. Palese, and E. D. Kilbourne. 1980. Gene composition of highyielding influenza vaccine strains obtained by recombination. J. Infect. Dis. 141:362-365.
4. Bem, R. A., A. W. Farnand, V. Wong, A. Koski, M. E. Rosenfeld, N. van Rooijen, C. W. Frevert, T. R. Martin, and G. Matute-Bello. 2008. Depletion of resident alveolar macrophages does not prevent Fas-mediated lung injury in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 295:L314-L325.
5. Bender, B. S., and P. A. Small, Jr. 1992. Influenza: pathogenesis and host defense. Semin. Respir. Infect. 7:38-45.
6. Benoit, A., Y. Huang, J. Proctor, G. Rowden, and R. Anderson. 2006. Effects of alveolar macrophage depletion on liposomal vaccine protection against respiratory syncytial virus (RSV). Clin. Exp. Immunol. 145:147-154.
7. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43.
8. Carbonetti, N. H., G. V. Artamonova, N. Van Rooijen, and V. I. Ayala. 2007. Pertussis toxin targets airway macrophages to promote Bordetella pertussis infection of the respiratory tract. Infect. Immun. 75:1713-1720.
9. Cheung, C. Y., L. L. Poon, A. S. Lau, W. Luk, Y. L. Lau, K. F. Shortridge, S. Gordon, Y. Guan, and J. S. Peiris. 2002. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360:1831-1837.
10. Crouch, E. C. 1998. Collectins and pulmonary host defense. Am. J. Respir. Cell Mol. Biol. 19:177-201.
11. Dawson, T. C., M. A. Beck, W. A. Kuziel, F. Henderson, and N. Maeda. 2000. Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am. J. Pathol. 156:1951-1959.
12. de Jong, M. D., C. P. Simmons, T. T. Thanh, V. M. Hien, G. J. Smith, T. N. Chau, D. M. Hoang, N. V. Chau, T. H. Khanh, V. C. Dong, P. T. Qui, B. V. Cam, Q. Ha do, Y. Guan, J. S. Peiris, N. T. Chinh, T. T. Hien, and J. Farrar. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12:1203-1207.
13. Engblom, E., T. O. Ekfors, O. H. Meurman, A. Toivanen, and J. Nikoskelainen. 1983. Fatal influenza A myocarditis with isolation of virus from the myocardium. Acta Med. Scand. 213:75-78.
14. Franke-Ullmann, G., C. Pfortner, P. Walter, C. Steinmuller, M. L. Lohmann-Matthes, L. Kobzik, and J. Freihorst. 1995. Alteration of pulmonary macrophage function by respiratory syncytial virus infection in vitro. J. Immunol. 154:268-280.
15. Frankova, V. 1975. Inhalatory infection of mice with influenza A0/PR8 virus. I. The site of primary virus replication and its spread in the respiratory tract. Acta Virol. 19:29-34.
16. Fujisawa, H., S. Tsuru, M. Taniguchi, Y. Zinnaka, and K. Nomoto. 1987. Protective mechanisms against pulmonary infection with influenza virus. I. Relative contribution of polymorphonuclear leukocytes and of alveolar macrophages to protection during the early phase of intranasal infection. J. Gen. Virol. 68:425-432.
17. Gao, P., S. Watanabe, T. Ito, H. Goto, K. Wells, M. McGregor, A. J. Cooley, and Y. Kawaoka. 1999. Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J. Virol. 73:3184-3189. (Pubitemid 29135710)
18. Grose, C., and K. Chokephaibulkit. 2004. Avian influenza virus infection of children in Vietnam and Thailand. Pediatr. Infect. Dis. J. 23:793-794.
19. Gu, J., Z. Xie, Z. Gao, J. Liu, C. Korteweg, J. Ye, L. T. Lau, J. Lu, Z. Gao, B. Zhang, M. A. McNutt, M. Lu, V. M. Anderson, E. Gong, A. C. Yu, and W. I. Lipkin. 2007. H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370:1137-1145.
20. Hall, J. N., M. C. Stone, and J. C. Simpson. 1918. The epidemic of pneumonia following influenza at Camp Logan, Texas. JAMA 71:1986-1987.
21. Hartshorn, K. L., E. C. Crouch, M. R. White, P. Eggleton, A. I. Tauber, D. Chang, and K. Sastry. 1994. Evidence for a protective role of pulmonary surfactant protein D (SP-D) against influenza A viruses. J. Clin. Invest. 94:311-319.
22. Hartshorn, K. L., K. B. Reid, M. R. White, J. C. Jensenius, S. M. Morris, A. I. Tauber, and E. Crouch. 1996. Neutrophil deactivation by influenza A viruses: mechanisms of protection after viral opsonization with collectins and hemagglutination-inhibiting antibodies. Blood 87:3450-3461.
23. Hartshorn, K. L., M. R. White, V. Shepherd, K. Reid, J. C. Jensenius, and E. C. Crouch. 1997. Mechanisms of anti-influenza activity of surfactant proteins A and D: comparison with serum collectins. Am. J. Physiol. 273:L1156-L1166.
24. Hashimoto, Y., T. Moki, T. Takizawa, A. Shiratsuchi, and Y. Nakanishi. 2007. Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J. Immunol. 178:2448-2457. (Pubitemid 46233445)
25. Herold, S., M. Steinmueller, W. von Wulffen, L. Cakarova, R. Pinto, S. Pleschka, M. Mack, W. A. Kuziel, N. Corazza, T. Brunner, W. Seeger, and J. Lohmeyer. 2008. Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J. Exp. Med. 205:3065-3077.
26. Herold, S., W. von Wulffen, M. Steinmueller, S. Pleschka, W. A. Kuziel, M. Mack, M. Srivastava, W. Seeger, U. A. Maus, and J. Lohmeyer. 2006. Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J. Immunol. 177:1817-1824. (Pubitemid 44092519)
27. Hofmann, P., H. Sprenger, A. Kaufmann, A. Bender, C. Hasse, M. Nain, and D. Gemsa. 1997. Susceptibility of mononuclear phagocytes to influenza A virus infection and possible role in the antiviral response. J. Leukoc. Biol. 61:408-414.
28. Jakab, G. J. 1982. Immune impairment of alveolar macrophage phagocytosis during influenza virus pneumonia. Am. Rev. Respir. Dis. 126:778-782.
29. Julkunen, I., T. Sareneva, J. Pirhonen, T. Ronni, K. Melen, and S. Matikainen. 2001. Molecular pathogenesis of influenza A virus infection and virus-induced regulation of cytokine gene expression. Cytokine Growth Factor Rev. 12:171-180.
30. Kim, H. M., Y. W. Lee, K. J. Lee, H. S. Kim, S. W. Cho, N. van Rooijen, Y. Guan, and S. H. Seo. 2008. Alveolar macrophages are indispensable for controlling influenza viruses in lungs of pigs. J. Virol. 82:4265-4274.
31. Kirby, A. C., J. G. Raynes, and P. M. Kaye. 2006. CD11b regulates recruitment of alveolar macrophages but not pulmonary dendritic cells after pneumococcal challenge. J. Infect. Dis. 193:205-213.
32. Kobasa, D., S. M. Jones, K. Shinya, J. C. Kash, J. Copps, H. Ebihara, Y. Hatta, J. H. Kim, P. Halfmann, M. Hatta, F. Feldmann, J. B. Alimonti, L. Fernando, Y. Li, M. G. Katze, H. Feldmann, and Y. Kawaoka. 2007. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319-323.
33. Kobasa, D., A. Takada, K. Shinya, M. Hatta, P. Halfmann, S. Theriault, H. Suzuki, H. Nishimura, K. Mitamura, N. Sugaya, T. Usui, T. Murata, Y. Maeda, S. Watanabe, M. Suresh, T. Suzuki, Y. Suzuki, H. Feldmann, and Y. Kawaoka. 2004. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703-707.
34. Kodihalli, S., V. Sivanandan, K. V. Nagaraja, D. Shaw, and D. A. Halvorson. 1994. Effect of avian influenza virus infection on the phagocytic function of systemic phagocytes and pulmonary macrophages of turkeys. Avian Dis. 38:93-102. (Pubitemid 2072630)
35. Kotaka, M., Y. Kitaura, H. Deguchi, and K. Kawamura. 1990. Experimental influenza A virus myocarditis in mice. Light and electron microscopic, virologic, and hemodynamic study. Am. J. Pathol. 136:409-419.
36. Leemans, J. C., N. P. Juffermans, S. Florquin, N. van Rooijen, M. J. Vervoordeldonk, A. Verbon, S. J. van Deventer, and T. van der Poll. 2001. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice. J. Immunol. 166:4604-4611.
37. Louria, D. B., H. L. Blumenfeld, J. T. Ellis, E. D. Kilbourne, and D. E. Rogers. 1959. Studies on influenza in the pandemic of 1957-1958. II. Pulmonary complications of influenza. J. Clin. Invest. 38:213-265.
38. Lu, X., T. M. Tumpey, T. Morken, S. R. Zaki, N. J. Cox, and J. M. Katz. 1999. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J. Virol. 73:5903-5911. (Pubitemid 29274877)
39. Malhotra, R., J. S. Haurum, S. Thiel, and R. B. Sim. 1994. Binding of human collectins (SP-A and MBP) to influenza virus. Biochem. J. 304:455-461. (Pubitemid 24368224)
40. McCormack, F. X., and J. A. Whitsett. 2002. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J. Clin. Invest. 109:707-712.
41. McGill, J., N. Van Rooijen, and K. L. Legge. 2008. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J. Exp. Med. 205:1635-1646.
42. Morty, R. E., O. Eickelberg, and W. Seeger. 2007. Alveolar fluid clearance in acute lung injury: what have we learned from animal models and clinical studies? Intensive Care Med. 33:1229-1240.
43. Neumann, G., T. Watanabe, H. Ito, S. Watanabe, H. Goto, P. Gao, M. Hughes, D. R. Perez, R. Donis, E. Hoffmann, G. Hobom, and Y. Kawaoka. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 96:9345-9350.
44. Perrone, L. A., J. K. Plowden, A. Garcia-Sastre, J. M. Katz, and T. M. Tumpey. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4:e1000115.
45. Peschke, T., A. Bender, M. Nain, and D. Gemsa. 1993. Role of macrophage cytokines in influenza A virus infections. Immunobiology 189:340-355. (Pubitemid 24001405)
46. Pontow, S. E., V. Kery, and P. D. Stahl. 1992. Mannose receptor. Int. Rev. Cytol. 137B:221-244.
47. Pribul, P. K., J. Harker, B. Wang, H. Wang, J. S. Tregoning, J. Schwarze, and P. J. Openshaw. 2008. Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J. Virol. 82:4441-4448.
48. Reading, P. C., J. L. Miller, and E. M. Anders. 2000. Involvement of the mannose receptor in infection of macrophages by influenza virus. J. Virol. 74:5190-5197.
49. Reading, P. C., L. S. Morey, E. C. Crouch, and E. M. Anders. 1997. Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J. Virol. 71:8204-8212.
50. Reading, P. C., P. G. Whitney, D. L. Pickett, M. D. Tate, and A. G. Brooks. February 2010. Influenza viruses differ in ability to infect macrophages and to induce a local inflammatory response following intraperitoneal injection of mice. Immunol. Cell Biol. doi:10.1038/icb.2010.11.
51. Reed, J. L., Y. A. Brewah, T. Delaney, T. Welliver, T. Burwell, E. Benjamin, E. Kuta, A. Kozhich, L. McKinney, J. Suzich, P. A. Kiener, L. Avendano, L. Velozo, A. Humbles, R. C. Welliver, Sr., and A. J. Coyle. 2008. Macrophage impairment underlies airway occlusion in primary respiratory syncytial virus bronchiolitis. J. Infect. Dis. 198:1783-1793.
52. Rodgers, B., and C. A. Mims. 1981. Interaction of influenza virus with mouse macrophages. Infect. Immun. 31:751-757.
53. Rogers, G. N., J. C. Paulson, R. S. Daniels, J. J. Skehel, I. A. Wilson, and D. C. Wiley. 1983. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304:76-78.
54. Sakamoto, M., F. Suzuki, S. Arai, T. Takishima, and N. Ishida. 1981. Experimental myocarditis induced in mice by infection with influenza A2 virus. Microbiol. Immunol. 25:173-181.
55. Seo, S. H., R. Webby, and R. G. Webster. 2004. No apoptotic deaths and different levels of inductions of inflammatory cytokines in alveolar macrophages infected with influenza viruses. Virology 329:270-279.
56. Slepushkin, V. A., P. D. Staber, G. Wang, P. B. McCray, Jr., and B. L. Davidson. 2001. Infection of human airway epithelia with H1N1, H2N2, and H3N2 influenza A virus strains. Mol. Ther. 3:395-402.
57. Spooner, L. H., L. H. Scoot, and, E. H. Heathe. 1919. A bacteriologic study of the influenza epidemic at Camp Devens, Mass. JAMA 72:155-159.
58. Sun, K., and D. W. Metzger. 2008. Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat. Med. 14:558-564.
59. Sur, S., J. S. Wild, B. K. Choudhury, N. Sur, R. Alam, and D. M. Klinman. 1999. Long term prevention of allergic lung inflammation in a mouse model of asthma by CpG oligodeoxynucleotides. J. Immunol. 162:6284-6293. (Pubitemid 29314994)
60. Szretter, K. J., S. Gangappa, X. Lu, C. Smith, W. J. Shieh, S. R. Zaki, S. Sambhara, T. M. Tumpey, and J. M. Katz. 2007. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81:2736-2744.
61. Tate, M. D., A. G. Brooks, and P. C. Reading. 2008. The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice. Respir. Res. 9:57.
62. Tate, M. D., Y. M. Deng, J. E. Jones, G. P. Anderson, A. G. Brooks, and P. C. Reading. 2009. Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J. Immunol. 183:7441-7450.
63. Tumpey, T. M., A. Garcia-Sastre, J. K. Taubenberger, P. Palese, D. E. Swayne, and C. F. Basler. 2004. Pathogenicity and immunogenicity of influenza viruses with genes from the 1918 pandemic virus. Proc. Natl. Acad. Sci. U. S. A. 101:3166-3171.
64. Tumpey, T. M., A. Garcia-Sastre, J. K. Taubenberger, P. Palese, D. E. Swayne, M. J. Pantin-Jackwood, S. Schultz-Cherry, A. Solorzano, N. Van Rooijen, J. M. Katz, and C. F. Basler. 2005. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J. Virol. 79:14933-14944.
65. Van Rooijen, N., and A. Sanders. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174:83-93. (Pubitemid 24297139)
66. van Rooijen, N., A. Sanders, and T. K. van den Berg. 1996. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J. Immunol. Methods 193:93-99.
67. Wagner, R., M. Matrosovich, and H. D. Klenk. 2002. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev. Med. Virol. 12:159-166.
68. Ward, A. C. 1997. Virulence of influenza A virus for mouse lung. Virus Genes 14:187-194.
69. Wells, M. A., P. Albrecht, S. Daniel, and F. A. Ennis. 1978. Host defense mechanisms against influenza virus: interaction of influenza virus with murine macrophages in vitro. Infect. Immun. 22:758-762.
70. Whitehead, G. S., L. H. Burch, K. G. Berman, C. A. Piantadosi, and D. A. Schwartz. 2006. Genetic basis of murine responses to hyperoxia-induced lung injury. Immunogenetics 58:793-804.
71. Wijburg, O. L., S. DiNatale, J. Vadolas, N. van Rooijen, and R. A. Strugnell. 1997. Alveolar macrophages regulate the induction of primary cytotoxic T-lymphocyte responses during influenza virus infection. J. Virol. 71:9450-9457.
72. Xu, T., J. Qiao, L. Zhao, G. Wang, G. He, K. Li, Y. Tian, M. Gao, J. Wang, H. Wang, and C. Dong. 2006. Acute respiratory distress syndrome induced by avian influenza A (H5N1) virus in mice. Am. J. Respir. Crit. Care Med. 174:1011-1017.
73. Yuen, K. Y., P. K. Chan, M. Peiris, D. N. Tsang, T. L. Que, K. F. Shortridge, P. T. Cheung, W. K. To, E. T. Ho, R. Sung, and A. F. Cheng. 1998. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467-471.