Interleukin-6 limits influenza-induced inflammation and protects against fatal lung pathology

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2613-2625

  Lauder, Sarah N ^a   Jones, Emma ^a   Smart, Kathryn ^a   Bloom, Anja ^a   Williams, Anwen S ^a   Hindley, James P ^a   Ondondo, Beatrice ^a   Taylor, Philip R ^a   Clement, Mathew ^a   Fielding, Ceri ^a   Godkin, Andrew J ^a   Jones, Simon A ^a   Gallimore, Awen M ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Adaptive immunity Heterosubtypic immunity IL 6 Innate immunity Pulmonary damage

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FEMALE; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INFLAMMATION; INFLUENZA; INNATE IMMUNITY; LUNG INJURY; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL; T LYMPHOCYTE; VIRUS IMMUNITY; VIRUS REPLICATION;

ADAPTIVE IMMUNITY · HETEROSUBTYPIC IMMUNITY · IL-6 · INNATE IMMUNITY · PULMONARY DAMAGE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; FEMALE; INFLAMMATION MEDIATORS; INFLUENZA A VIRUS; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA, VIRAL; VIRAL LOAD; VIRUS REPLICATION;

EID: 84885772985     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201243018     Document Type: Article

References (48)

1. Murray, C. J., Lopez, A. D., Chin, B., Feehan, D. and Hill, K. H., Estimation of potential global pandemic influenza mortality on the basis of vital registry data from the 1918-20 pandemic: a quantitative analysis. Lancet 2006. 368: 2211-2218.
2. de Jong, M. D., Simmons, C. P., Thanh, T. T., Hien, V. M., Smith, G. J., Chau, T. N., Hoang, D. M. et al., Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 2006. 12: 1203-1207.
3. Peiris, J. S., Yu, W. C., Leung, C. W., Cheung, C. Y., Ng, W. F., Nicholls, J. M., Ng, T. K. et al., Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 2004. 363: 617-619.
4. Yuen, K. Y., Chan, P. K., Peiris, M., Tsang, D. N., Que, T. L., Shortridge, K. F., Cheung, P. T. et al., Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 1998. 351: 467-471.
5. Kaiser, L., Fritz, R. S., Straus, S. E., Gubareva, L. and Hayden, F. G., Symptom pathogenesis during acute influenza: interleukin-6 and other cytokine responses. J. Med. Virol. 2001. 64: 262-268.
6. Svitek, N., Rudd, P. A., Obojes, K., Pillet, S. and von Messling, V., Severe seasonal influenza in ferrets correlates with reduced interferon and increased IL-6 induction. Virology 2008. 376: 53-59.
7. Dienz, O., Eaton, S. M., Bond, J. P., Neveu, W., Moquin, D., Noubade, R., Briso, E. M., et al., The induction of antibody production by IL-6 is indirectly mediated by IL-21 produced by CD4+ T cells. J. Exp. Med. 2009. 206: 69-78.
8. Hurst, S. M., Wilkinson, T. S., McLoughlin, R. M., Jones, S., Horiuchi, S., Yamamoto, N., Rose-John, S. et al., IL-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 2001. 14: 705-714.
9. McLoughlin, R. M., Witowski, J., Robson, R. L., Wilkinson, T. S., Hurst, S. M., Williams, A. S., Williams, J. D. et al., Interplay between IFN-gamma and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J. Clin. Invest. 2003. 112: 598-607.
10. McLoughlin, R. M., Jenkins, B. J., Grail, D., Williams, A. S., Fielding, C. A., Parker, C. R., Ernst, M. et al., IL-6 trans-signaling via STAT3 directs T cell infiltration in acute inflammation. Proc. Natl. Acad. Sci. USA 2005. 102(27): 9589-9594
11. Jones, S. A., Directing transition from innate to acquired immunity: defining a role for IL-6. J. Immunol. 2005. 175: 3463-3468.
12. Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R. et al., Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994. 368: 339-342.
13. Ladel, C. H., Blum, C., Dreher, A., Reifenberg, K., Kopf, M. and Kaufmann, S. H., Lethal tuberculosis in interleukin-6-deficient mutant mice. Infect. Immun. 1997. 65: 4843-4849.
14. van der Poll, T., Keogh, C. V., Guirao, X., Buurman, W. A., Kopf, M. and Lowry, S. F., Interleukin-6 gene-deficient mice show impaired defense against pneumococcal pneumonia. J. Infect. Dis. 1997. 176: 439-444.
15. Eugster, H. P., Frei, K., Kopf, M., Lassmann, H. and Fontana, A., IL-6-deficient mice resist myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. Eur. J. Immunol. 1998. 28: 2178-2187.
16. Ohshima, S., Saeki, Y., Mima, T., Sasai, M., Nishioka, K., Nomura, S., Kopf, M. et al., Interleukin 6 plays a key role in the development of antigen-induced arthritis. Proc. Natl. Acad. Sci. USA 1998. 95: 8222-8226.
17. Jones, G. W., McLoughlin, R. M., Hammond, V. J., Parker, C. R., Williams, J. D., Malhotra, R., Scheller, J. et al., Loss of CD4+ T cell IL-6R expression during inflammation underlines a role for IL-6 trans signaling in the local maintenance of Th17 cells. J. Immunol. 2010. 184: 2130-2139.
18. Renauld, J. C., Vink, A. and Van Snick, J., Accessory signals in murine cytolytic T cell responses. Dual requirement for IL-1 and IL-6. J. Immunol. 1989. 143: 1894-1898.
19. Dienz, O. and Rincon, M., The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 2009. 130: 27-33.
20. Longhi, M. P., Wright, K., Lauder, S. N., Nowell, M. A., Jones, G. W., Godkin, A. J., Jones, S. A. et al., Interleukin-6 is crucial for recall of influenza-specific memory CD4 T cells. PLoS Pathog. 2008. doi: 10.1371/journal.ppat.1000006.
21. Fukushi, M., Ito, T., Oka, T., Kitazawa, T., Miyoshi-Akiyama, T., Kirikae, T., Yamashita, M. et al., Serial histopathological examination of the lungs of mice infected with influenza A virus PR8 strain. PLoS One 2011. doi10.1371/journal.pone.0021207.
22. Wong, J. P., Saravolac, E. G., Clement, J. G. and Nagata, L. P., Development of a murine hypothermia model for study of respiratory tract influenza virus infection. Lab. Anim. Sci. 1997. 47: 143-147.
23. Tsuchiya, K., Jo, T., Takeda, N., Al Heialy, S., Siddiqui, S., Shalaby, K. H., Risse, P. A. et al., EGF receptor activation during allergic sensitization affects IL-6-induced T-cell influx to airways in a rat model of asthma. Eur. J. Immunol. 2010. 40: 1590-1602.
24. Rochman, I., Paul, W. E and Ben-Sasson, S. Z., IL-6 increases primed cells expansion and survival. J. Immunol. 2005. 174: 4761-4767.
25. Hou, S., Hyland, L., Ryan, K. W., Portner, A. and Doherty, P. C., Virus-specific CD8+ T-cell memory determined by clonal burst size. Nature 1994. 369: 652-654.
26. Kozak, W., Poli, V., Soszynski, D., Conn, C. A., Leon, L. R. and Kluger, M. J., Sickness behaviour in mice deficient in interleukin-6 during turpentine abscess and influenza pneumonitis. Am. J. Physiol. 1997. 272: 621-630.
27. Dienz, O., Rud, J. G., Eaton, S. M., Lanthier, P. A., Burg, E., Drew, A., Bunn, J. et al., Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol. 2012. 5: 258-266.
28. Herold, S., Steinmueller, M., von Wulffen, W., Cakarova, L., Pinto, R., Pleschka, S., Mack, M. et al., Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J. Exp. Med. 2008. 205: 3065-3077.
29. Aldridge, J. R., Jr., Moseley, C. E., Boltz, D. A., Negovetich, N. J., Reynolds, C., Franks, J., Brown, S. A. et al., TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc. Natl. Acad. Sci. USA 2009. 106: 5306-5311.
30. Herold, S., von Wulffen, W., Steinmueller, M., Pleschka, S., Kuziel, W. A., Mack, M., Srivastava, M. et al., Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J. Immunol. 2006. 177: 1817-1824.
31. Lin, K. L., Suzuki, Y., Nakano, H., Ramsburg, E. and Gunn, M. D., CCR2 +monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J. Immunol. 2008. 180: 2562-2572.
32. Dalrymple, S. A., Lucian, L. A., Slattery, R., McNeil, T., Aud, D. M., Fuchino, S., Lee, F. et al., Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia. Infect. Immun. 1995. 63: 2262-2268.
33. Diehl, S., Anguita, J., Hoffmeyer, A., Zapton, T., Ihle, J. N., Fikrig, E. and Rincon, M., Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 2000. 13: 805-815.
34. Dodge, I. L., Carr, M. W., Cernadas, M. and Brenner, M. B., IL-6 production by pulmonary dendritic cells impedes Th1 immune responses. J. Immunol. 2003. 170: 4457-4464.
35. Xing, Z., Gauldie, J., Cox, G., Baumann, H., Jordana, M., Lei, X. F. and Achong, M. K., IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 1998. 101: 311-320.
36. Blier, J. I., Pillarisetty, V. G., Shah, A. B. and DeMatteo, R. P., Increased and long-term generation of dendritic cells with reduced function from IL-6-deficient bone marrow. J. Immunol. 2004. 172: 7408-7416.
37. Park, S., Nakagawa, T., Kitamura, H., Atsumi, T., Kamon, H., Sawa, S., Kamimura, D. et al., IL-6 regulates in vivo dendritic cell differentation through STAT3 activation. J. Immunol. 2004. 173: 3844-3854.
38. + T-cell memory determined by clonal burst size. Nature 1994. 369(6482): 652-654
39. Grivennikov, S., Karin, E., Terzic, J., Mucida, D., Yu, G. Y., Vallabhapurapu, S., Scheller, J. et al., IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009. 15: 103-113.
40. Jones, S.A., Scheller, J. and Rose-John, S., Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J. Clin. Invest. 2011. 121: 3375-3383.
41. Barton, B. E. and Jackson, J. V., Protective role of interleukin 6 in the lipopolysaccharide-galactosamine septic shock model. Infect. Immun. 1993. 61(4): 1496-1499
42. Hussell, T., Pennycook, A. and Openshaw, P. J., Inhibition of tumor necrosis factor reduces the severity of virus-specific lung immunopathology. Eur. J. Immunol. 2001. 31(9): 2566-2573.
43. Baez, M., Palese, P. and Kilbourne, E. D., Gene composition of high-yielding influenza vaccine strains obtained by recombination. J. Infect. Dis. 1980. 141: 362-365.
44. Bachmann, M. F., Ecabert, B. and Kopf, M., Influenza virus: a novel method to assess viral and neutralizing antibody titers in vitro. J. Immunol. Methods 1999. 225: 105-111.
45. Longhi, M. P., Williams, A., Wise, M., Morgan, B. P. and Gallimore, A., CD59a deficiency exacerbates influenza-induced lung inflammation through complement-dependent and -independent mechanisms. Eur. J. Immunol. 2007. 37: 1266-1274.
46. Ashcroft, T., Simpson, J. M. and Timbrell, V., Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J. Clin. Pathol. 1998. 41: 467-470.
47. Jones, E., Price, D. A., Dahm-Vicker, M., Cerundolo, V., Klenerman, P. and Gallimore, A., The influence of macrophage inflammatory protein-1alpha on protective immunity mediated by antiviral cytotoxic T cells. Immunology 2003. 109: 68-75.
48. Schmitz, N., Kurrer, M., Bachmann, M. F. and Kopf, M., Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol. 2005. 79: 6441-6448.