A question of self-preservation: Immunopathology in influenza virus infection

Immunology and Cell Biology

Volumn 85, Issue 2, 2007, Pages 85-92

  La Gruta, Nicole L ^a   Kedzierska, Katherine ^a   Stambas, John ^a   Doherty, Peter C ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Chemokines; Cytokines; Immunopathology; Influenza A virus; Macrophages; T cells

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; HYDROGEN PEROXIDE; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 18 BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; RANTES; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANTIMICROBIAL ACTIVITY; CD8+ T LYMPHOCYTE; CLINICAL FEATURE; CYTOKINE PRODUCTION; HUMAN; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOPATHOLOGY; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; LITERATURE; LUNG INJURY; MACROPHAGE; MONOCYTE; NONHUMAN; REVIEW; TISSUE INJURY; VIRUS INFECTION; VIRUS PNEUMONIA;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHEMOKINES; CYTOKINES; HUMANS; IMMUNE SYSTEM; IMMUNE SYSTEM DISEASES; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MONOCYTES;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 33947108477     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/sj.icb.7100026     Document Type: Review

References (97)

1. Lamb RA, Krug RM. Orthomyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM (eds). Fields Virology, 4th edn, vol 1. Lippincott Williams & Wilkins, Philadelphia, USA, 2001, pp 1487-1531.
2. Potter CW. A history of influenza. J Appl Microbiol 2001; 91: 572-579.
3. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. Avian flu: influenza virus receptors in the human airway. Nature 2006; 440: 435-436.
4. Hsieh YC, Wu TZ, Liu DP, Shao PL, Chang LY, Lu CY et al. Influenza pandemics: past, present and future. J Formos Med Assoc 2006; 105: 1-6.
5. Doherty PC, Turner SJ, Webby RG, Thomas PG. Influenza and the challenge for immunology. Nat Immunol 2006; 7: 449-455.
6. Bender BS, Small Jr PA. Influenza: pathogenesis and host defense. Semin Respir Infect 1992; 7: 38-45.
7. Fesq H, Bacher M, Nain M, Gemsa D. Programmed cell death (apoptosis) in human monocytes infected by influenza A virus. Immunobiology 1994; 190: 175-182.
8. Julkunen I, Melen K, Nyqvist M, Pirhonen J, Sareneva T, Matikainen S. Inflammatory responses in influenza A virus infection. Vaccine 2000; 19 (Suppl 1): S32-S37.
9. Julkunen I, Sareneva T, Pirhonen J, Ronni T, Melen K, Matikainen S. Molecular pathogenesis of influenza A virus infection and virus-induced regulation of cytokine gene expression. Cytokine Growth Factor Rev 2001; 12: 171-180.
10. Sprenger H, Meyer RG, Kaufmann A, Bussfeld D, Rischkowsky E, Gemsa D. Selective induction of monocyte and not neutrophil-attracting chemokines after influenza A virus infection. J Exp Med 1996; 184: 1191-1196.
11. Adachi M, Matsukura S, Tokunaga H, Kokubu F. Expression of cytokines on human bronchial epithelial cells induced by influenza virus A. Int Arch Allergy Immunol 1997; 113: 307-311.
12. Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, Chan YO et al. Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir Res 2005; 6: 135.
13. Ada GL, Jones PD. The immune response to influenza infection. Curr Top Microbiol Immunol 1986; 128: 1-54.
14. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006; 12: 1203-1207.
15. Peiris JS, Yu WC, Leung CW, Cheung CY, Ng WF, Nicholls JM et al. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 2004; 363: 617-619.
16. To KF, Chan PK, Chan KF, Lee WK, Lam WY, Wong KF et al. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 2001; 63: 242-246.
17. Mou SS, Nakagawa TA, Riemer EC, McLean TW, Hines MH, Shetty AK. Hemophagocytic lymphohistiocytosis complicating influenza A infection. Pediatrics 2006; 118: e216-e219.
18. Fisman DN. Hemophagocytic syndromes and infection. Emerg Infect Dis 2000; 6: 601-608.
19. Akashi K, Hayashi S, Gondo H, Mizuno S, Harada M, Tamura K et al. Involvement of interferon-gamma and macrophage colony-stimulating factor in pathogenesis of haemophagocytic lymphohistiocytosis in adults. Br J Haematol 1994; 87: 243-250.
20. Imashuku S, Hibi S, Fujiwara F, Todo S. Hyper-interleukin (IL)-6-naemia in haemophagocytic lymphohistiocytosis. Br J Haematol 1996; 93: 803-807.
21. Taubenberger JK, Reid AH, Krafft AE, Bijwaard KE, Fanning TG. Initial genetic characterization of the 1918 "Spanish" influenza virus. Science 1997; 275: 1793-1796.
22. Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S et al. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 2004; 431: 703-707.
23. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ et al. 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 2005; 79: 14933-14944.
24. Beigel JH, Farrar J, Han AM, Hayden FG, Hyer R, de Jong MD et al. Avian influenza A (H5N1) infection in humans. N Engl J Med 2005; 353: 1374-1385.
25. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF et al. 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.
26. Hayden FG, Fritz R, Lobo MC, Alvord W, Strober W, Straus SE. Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J Clin Invest 1998; 101: 643-649.
27. 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.
28. Nguyen HH, van Ginkel FW, Vu HL, Novak MJ, McGhee JR, Mestecky J. Gamma interferon is not required for mucosal cytotoxic T-lymphocyte responses or heterosubtypic immunity to influenza A virus infection in mice. J Virol 2000; 74: 5495-5501.
29. Bot A, Bot S, Bona CA. Protective role of gamma interferon during the recall response to influenza virus. J Virol 1998; 72: 6637-6645.
30. Baumgarth N, Kelso A. In vivo blockade of gamma interferon affects the influenza virus-induced humoral and the local cellular immune response in lung tissue. J Virol 1996; 70: 4411-4418.
31. Price GE, Gaszewska-Mastarlarz A, Moskophidis D. The role of alpha/beta and gamma interferons in development of immunity to influenza A virus in mice. J Virol 2000; 74: 3996-4003.
32. Wiley JA, Cerwenka A, Harkema JR, Dutton RW, Harmsen AG. Production of interferon-gamma by influenza hemagglutinin-specific CD8 effector T cells influences the development of pulmonary immunopathology. Am J Pathol 2001; 158: 119-130.
33. Ostler T, Davidson W, Ehl S. Virus clearance and immunopathology by CD8(+) T cells during infection with respiratory syncytial virus are mediated by IFN-gamma. Eur J Immunol 2002; 32: 2117-2123.
34. Bruder D, Srikiatkhachorn A, Enelow RI. Cellular immunity and lung injury in respiratory virus infection. Viral Immunol 2006; 19: 147-155.
35. Peper RL, Van Campen H. Tumor necrosis factor as a mediator of inflammation in influenza A viral pneumonia. Microb Pathog 1995; 19: 175-183.
36. Hussell T, Pennycook A, Openshaw PJ. Inhibition of tumor necrosis factor reduces the severity of virus-specific lung immunopathology. Eur J Immunol 2001; 31: 2566-2573.
37. Zhang WJ, Sarawar S, Nguyen P, Daly K, Rehg JE, Doherty PC et al. Lethal synergism between influenza infection and staphylococcal enterotoxin B in mice. J Immunol 1996; 157: 5049-5060.
38. Cook DN, Beck MA, Coffman TM, Kirby SL, Sheridan JF, Pragnell IB et al. Requirement of MIP-1 alpha for an inflammatory response to viral infection. Science 1995; 269: 1583-1585.
39. Kozak W, Poli V, Soszynski D, Conn CA, Leon LR, Kluger MJ. Sickness behavior in mice deficient in interleukin-6 during turpentine abscess and influenza pneumonitis. Am J Physiol 1997; 272: R621-R630.
40. Larsen DL, Dybdahl-Sissoko N, McGregor MW, Drape R, Neumann V, Swain WF et al. Coadministration of DNA encoding interleukin-6 and hemagglutinin confers protection from influenza virus challenge in mice. J Virol 1998; 72: 1704-1708.
41. Lee SW, Youn JW, Seong BL, Sung YC. IL-6 induces long-term protective immunity against a lethal challenge of influenza virus. Vaccine 1999; 17: 490-496.
42. Schmitz N, Kurrer M, Bachmann MF, Kopf M. Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 2005; 79: 6441-6448.
43. 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.
44. Neumann G, Kawaoka Y. Host range restriction and pathogenicity in the context of influenza pandemic. Emerg Infect Dis 2006; 12: 881-886.
45. Geiss GK, Salvatore M, Tumpey TM, Carter VS, Wang X, Basler CF et al. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc Natl Acad Sci USA 2002; 99: 10736-10741.
46. Seo SH, Hoffmann E, Webster RG. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 2002; 8: 950-954.
47. Lipatov AS, Andreansky S, Webby RJ, Hulse DJ, Rehg JE, Krauss S et al. Pathogenesis of Hong Kong H5N1 influenza virus NS gene reassortants in mice: the role of cytokines and B- and T-cell responses. J Gen Virol 2005; 86: 1121-1130.
48. Doherty PC, Topham DJ, Tripp RA, Cardin RD, Brooks JW, Stevenson PG. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev 1997; 159: 105-117.
49. Wyde PR, Peavy DL, Cate TR. Morphological and cytochemical characterization of cells infiltrating mouse lungs after influenza infection. Infect Immun 1978; 21: 140-146.
50. Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, Doherty PC. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 1998; 8: 683-691.
51. Shimomura E, Suzuki F, Ishida N. Characterization of cells infiltrating the lungs of x-irradiated and nude mice after influenza virus infection. Microbiol Immunol 1982; 26: 129-138.
52. Wells MA, Albrecht P, Ennis FA. Recovery from a viral respiratory infection. I. Influenza pneumonia in normal and T-deficient mice. J Immunol 1981; 126: 1036-1041.
53. Moskophidis D, Kioussis D. Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J Exp Med 1998; 188: 223-232.
54. Bender BS, Taylor SF, Zander DS, Cottey R. Pulmonary immune response of young and aged mice after influenza challenge. J Lab Clin Med 1995; 126: 169-177.
55. Enelow RI, Mohammed AZ, Stoler MH, Liu AN, Young JS, Lou YH et al. Structural and functional consequences of alveolar cell recognition by CD8(+) T lymphocytes in experimental lung disease. J Clin Invest 1998; 102: 1653-1661.
56. Hsieh SM, Chang SC. Insufficient perforin expression in CD8+ T cells in response to hemagglutinin from avian influenza (H5N1) virus. J Immunol 2006; 176: 4530-4533.
57. Xu L, Yoon H, Zhao MQ, Liu J, Ramana CV, Enelow RI. wCutting edge: pulmonary immunopathology mediated by antigen-specific expression of TNF-alpha by antiviral CD8+ T cells. J Immunol 2004; 173: 721-725.
58. Zhao MQ, Foley MP, Stoler MH, Enelow RI. Alveolar epithelial cell chemokine expression induced by specific antiviral CD8+ T-cell recognition plays a critical role in the perpetuation of experimental interstitial pneumonia. Chest 2001; 120: 11S-13S.
59. Small BA, Dressel SA, Lawrence CW, Drake III DR, Stoler MH, Enelow RI et al. CD8(+) T cell-mediated injury in vivo progresses in the absence of effector T cells. J Exp Med 2001; 194: 1835-1846.
60. Liu AN, Mohammed AZ, Rice WR, Fiedeldey DT, Liebermann JS, Whitsett JA et al. Perforin-independent CD8(+) T-cell-mediated cytotoxicity of alveolar epithelial cells is preferentially mediated by tumor necrosis factor-alpha: relative insensitivity to Fas ligand. Am J Respir Cell Mol Biol 1999; 20: 849-858.
61. Gramaglia I, Weinberg AD, Lemon M, Croft M. Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J Immunol 1998; 161: 6510-6517.
62. Kopf M, Ruedl C, Schmitz N, Gallimore A, Lefrang K, Ecabert B et al. OX40-deficient mice are defective in Th cell proliferation but are competent in generating B cell and CTL Responses after virus infection. Immunity 1999; 11: 699-708.
63. Humphreys IR, Walzl G, Edwards L, Rae A, Hill S, Hussell T. A critical role for OX40 in T cell-mediated immunopathology during lung viral infection. J Exp Med 2003; 198: 1237-1242.
64. Hofmann P, Sprenger H, Kaufmann A, Bender A, Hasse C, Nain M et al. Susceptibility of mononuclear phagocytes to influenza A virus infection and possible role in the antiviral response. J Leukoc Biol 1997; 61: 408-414.
65. Doherty PC. Immune responses to viruses. In: Rich RR, Fleisher TA, Schwarz BD, Shearer WT, Strober W (eds). Clinical Immunology, vol 1. Mosby-Year Book, Inc., Missouri, USA, 1996, pp 535-549.
66. Fujisawa H, Tsuru S, Taniguchi M, Zinnaka Y, Nomoto K. 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 1987; 68 (Part 2): 425-432.
67. Shaw MW, Arden NH, Maassab HF. New aspects of influenza viruses. Clin Microbiol Rev 1992; 5: 74-92.
68. Gong JH, Sprenger H, Hinder F, Bender A, Schmidt A, Horch S et al. Influenza A virus infection of macrophages. Enhanced tumor necrosis factor-alpha (TNF-alpha) gene expression and lipopolysaccharide-triggered TNF-alpha release. J Immunol 1991; 147: 3507-3513.
69. Kaufmann A, Salentin R, Meyer RG, Bussfeld D, Pauligk C, Fesq H et al. Defense against influenza A virus infection: essential role of the chemokine system. Immunobiology 2001; 204: 603-613.
70. Nain M, Hinder F, Gong JH, Schmidt A, Bender A, Sprenger H et al. Tumor necrosis factor-alpha production of influenza A virus-infected macrophages and potentiating effect of lipopolysaccharides. J Immunol 1990; 145: 1921-1928.
71. Pauligk C, Nain M, Reiling N, Gemsa D, Kaufmann A. CD14 is required for influenza A virus-induced cytokine and chemokine production. Immunobiology 2004; 209: 3-10.
72. Seo SH, Webby R, Webster RG. No apoptotic deaths and different levels of inductions of inflammatory cytokines in alveolar macrophages infected with influenza viruses. Virology 2004; 329: 270-279.
73. Bussfeld D, Kaufmann A, Meyer RG, Gemsa D, Sprenger H. Differential mononuclear leukocyte attracting chemokine production after stimulation with active and inactivated influenza A virus. Cell Immunol 1998; 186: 1-7.
74. Akaike T. Role of free radicals in viral pathogenesis and mutation. Rev Med Virol 2001; 11: 87-101.
75. Akaike T, Noguchi Y, Ijiri S, Setoguchi K, Suga M, Zheng YM et al. Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals. Proc Natl Acad Sci USA 1996; 93: 2448-2453.
76. Karupiah G, Chen JH, Mahalingam S, Nathan CF, MacMicking JD. Rapid interferon gamma-dependent clearance of influenza A virus and protection from consolidating pneumonitis in nitric oxide synthase 2-deficient mice. J Exp Med 1998; 188: 1541-1546.
77. Schwarz KB. Oxidative stress during viral infection: a review. Free Radical Biol Med 1996; 21: 641-649.
78. 2-generation by xanthine oxidase of pathogenesis of influenza virus infection in mice. J Clin Invest 1990; 85: 739-745.
79. Oda T, Akaike T, Hamamoto T, Suzuki F, Hirano T, Maeda H. Oxygen radicals in influenza-induced pathogenesis and treatment with pyran polymer-conjugated SOD. Science 1989; 244: 974-976.
80. Snelgrove RJ, Edwards L, Rae AJ, Hussell T. An absence of reactive oxygen species improves the resolution of lung influenza infection. Eur J Immunol 2006; 36: 1364-1373.
81. Rosenblum MD, Olasz E, Woodliff JE, Johnson BD, Konkol MC, Gerber KA et al. CD200 is a novel p53-target gene involved in apoptosis-associated immune tolerance. Blood 2004; 103: 2691-2698.
82. Brown DM, Roman E, Swain SL. CD4 T cell responses to influenza infection. Semin Immunol 2004; 16: 171-177.
83. Eichelberger M, Allan W, Zijlstra M, Jaenisch R, Doherty PC. Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J Exp Med 1991; 174: 875-880.
84. Hou S, Doherty PC, Zijlstra M, Jaenisch R, Katz JM. Delayed clearance of Sendai virus in mice lacking class I MHC-restricted CD8+ T cells. J Immunol 1992; 149: 1319-1325.
85. Mozdzanowska K, Furchner M, Maiese K, Gerhard W. CD4+ T cells are ineffective in clearing a pulmonary infection with influenza type A virus in the absence of B cells. Virology 1997; 239: 217-225.
86. Topham DJ, Doherty PC. Clearance of an influenza A virus by CD4+ T cells is inefficient in the absence of B cells. J Virol 1998; 72: 882-885.
87. Baumgarth N, Kelso A. Functionally distinct T cells in three compartments of the respiratory tract after influenza virus infection. Eur J Immunol 1996; 26: 2189-2197.
88. Mosmann TR, Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989; 7: 145-173.
89. Carding SR, Allan W, McMickle A, Doherty PC. Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J Exp Med 1993; 177: 475-482.
90. 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.
91. Graham MB, Braciale VL, Braciale TJ. Influenza virus-specific CD4+ T helper type 2T lymphocytes do not promote recovery from experimental virus infection. J Exp Med 1994; 180: 1273-1282.
92. Lukacher AE, Morrison LA, Braciale VL, Malissen B, Braciale TJ. Expression of specific cytolytic activity by H-2I region-restricted, influenza virus-specific T lymphocyte clones. J Exp Med 1985; 162: 171-187.
93. Taylor SF, Bender BS. Beta 2-microglobulin-deficient mice demonstrate class II MHC restricted anti-viral CD4+ but not CD8+ CTL against influenza-sensitized autologous splenocytes. Immunol Lett 1995; 46: 67-73.
94. Topham DJ, Tripp RA, Sarawar SR, Sangster MY, Doherty PC. Immune CD4+ T cells promote the clearance of influenza virus from major histocompatibility complex class II -/- respiratory epithelium. J Virol 1996; 70: 1288-1291.
95. Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, Lipatov AS et al. H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci USA 2004; 101: 8156-8161.
96. Kozak W, Zheng H, Conn CA, Soszynski D, van der Ploeg LH, Kluger MJ. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1 beta-deficient mice. Am J Physiol 1995; 269: R969-R977.
97. Zhou J, Law HK, Cheung CY, Ng IH, Peiris JS, Lau YL. Differential expression of chemokines and their receptors in adult and neonatal macrophages infected with human or avian influenza viruses. J Infect Dis 2006; 194: 61-70.