About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 250938, 10 pages
http://dx.doi.org/10.1155/2013/250938
Research Article

Interleukin-33 Drives Activation of Alveolar Macrophages and Airway Inflammation in a Mouse Model of Acute Exacerbation of Chronic Asthma

Department of Pathology, Inflammation and Infection Research Centre, School of Medical Sciences, University of New South Wales, Sydney, NSW 2052, Australia

Received 8 February 2013; Revised 23 April 2013; Accepted 29 April 2013

Academic Editor: Carlo Jose Freire de Oliveira

Copyright © 2013 Melissa M. Bunting et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. H. Dougherty and J. V. Fahy, “Acute exacerbations of asthma: epidemiology, biology and the exacerbation-prone phenotype,” Clinical and Experimental Allergy, vol. 39, no. 2, pp. 193–202, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Simpson, V. Y. F. Tan, J. Winn et al., “Beyond atopy: multiple patterns of sensitization in relation to asthma in a birth cohort study,” American Journal of Respiratory and Critical Care Medicine, vol. 181, no. 11, pp. 1200–1206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. R. J. Martin, “Therapeutic significance of distal airway inflammation in asthma,” Journal of Allergy and Clinical Immunology, vol. 109, no. 2, pp. S447–S460, 2002. View at Scopus
  4. S. E. Wenzel, L. B. Schwartz, E. L. Langmack et al., “Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics,” American Journal of Respiratory and Critical Care Medicine, vol. 160, no. 3, pp. 1001–1008, 1999. View at Scopus
  5. J. C. C. M. In 't Veen, H. H. Smits, P. S. Hiemstra, A. E. Zwinderman, P. J. Sterk, and E. H. Bel, “Lung function and sputum characteristics of patients with severe asthma during an induced exacerbation by double-blind steroid withdrawal,” American Journal of Respiratory and Critical Care Medicine, vol. 160, no. 1, pp. 93–99, 1999. View at Scopus
  6. E. R. McFadden Jr., “Acute severe asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 168, no. 7, pp. 740–759, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. S. T. Holgate, “Exacerbations: the asthma paradox,” American Journal of Respiratory and Critical Care Medicine, vol. 172, no. 8, pp. 941–943, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. R. M. Green, A. Custovic, G. Sanderson, J. Hunter, S. L. Johnston, and A. Woodcock, “Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study,” British Medical Journal, vol. 324, article 763, 2002. View at Publisher · View at Google Scholar
  9. C. S. Murray, G. Poletti, T. Kebadze et al., “Study of modifiable risk factors for asthma exacerbations: virus infection and allergen exposure increase the risk of asthma hospital admissions in children,” Thorax, vol. 61, no. 5, pp. 376–382, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. N. W. Bartlett, R. P. Walton, M. R. Edwards et al., “Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation,” Nature Medicine, vol. 14, no. 2, pp. 199–204, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. P. G. Holt and D. H. Strickland, “Interactions between innate and adaptive immunity in asthma pathogenesis: new perspectives from studies on acute exacerbations,” Journal of Allergy and Clinical Immunology, vol. 125, no. 5, pp. 963–972, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Borish, “IL-4 and IL-13 dual antagonism: a promising approach to the dilemma of generating effective asthma biotherapeutics,” American Journal of Respiratory and Critical Care Medicine, vol. 181, no. 8, pp. 769–770, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. J. S. Siegle, N. Hansbro, C. Herbert, M. Yang, P. S. Foster, and R. K. Kumar, “Airway hyperreactivity in exacerbation of chronic asthma is independent of eosinophilic inflammation,” American Journal of Respiratory Cell and Molecular Biology, vol. 35, no. 5, pp. 565–570, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Temelkovski, S. P. Hogan, D. P. Shepherd, P. S. Foster, and R. K. Kumar, “An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolised allergen,” Thorax, vol. 53, no. 10, pp. 849–856, 1998. View at Scopus
  15. R. K. Kumar and P. S. Foster, “Modeling allergic asthma in mice: pitfalls and opportunities,” American Journal of Respiratory Cell and Molecular Biology, vol. 27, no. 3, pp. 267–272, 2002. View at Scopus
  16. A. T. Nials and S. Uddin, “Mouse models of allergic asthma: acute and chronic allergen challenge,” Disease Models and Mechanisms, vol. 1, no. 4-5, pp. 213–220, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Herbert, M. M. Scott, K. H. Scruton et al., “Alveolar macrophages stimulate enhanced cytokine production by pulmonary CD4+ T-lymphocytes in an exacerbation of murine chronic asthma,” American Journal of Pathology, vol. 177, no. 4, pp. 1657–1664, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati, “The chemokine system in diverse forms of macrophage activation and polarization,” Trends in Immunology, vol. 25, no. 12, pp. 677–686, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. J. P. Edwards, X. Zhang, K. A. Frauwirth, and D. M. Mosser, “Biochemical and functional characterization of three activated macrophage populations,” Journal of Leukocyte Biology, vol. 80, no. 6, pp. 1298–1307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Schmitz, A. Owyang, E. Oldham et al., “IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines,” Immunity, vol. 23, no. 5, pp. 479–490, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. F. Y. Liew, N. I. Pitman, and I. B. McInnes, “Disease-associated functions of IL-33: the new kid in the IL-1 family,” Nature Reviews Immunology, vol. 10, no. 2, pp. 103–110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Kurowska-Stolarska, B. Stolarski, P. Kewin et al., “IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation,” Journal of Immunology, vol. 183, no. 10, pp. 6469–6477, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. X. Liu, M. Li, Y. Wu, Y. Zhou, L. Zeng, and T. Huang, “Anti-IL-33 antibody treatment inhibits airway inflammation in a murine model of allergic asthma,” Biochemical and Biophysical Research Communications, vol. 386, no. 1, pp. 181–185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Mizutani, T. Nabe, and S. Yoshino, “IL-33 and alveolar macrophages contribute to the mechanisms underlying the exacerbation of IgE-mediated airway inflammation and remodeling in mice,” Immunology, vol. 139, no. 2, pp. 205–218, 2013. View at Publisher · View at Google Scholar
  26. T. Ohno, K. Oboki, H. Morita et al., “Paracrine IL-33 stimulation enhances lipopolysaccharide-mediated macrophage activation,” PLoS ONE, vol. 6, no. 4, Article ID e18404, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. R. K. Kumar, C. Herbert, D. C. Webb, L. Li, and P. S. Foster, “Effects of anticytokine therapy in a mouse model of chronic asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 170, no. 10, pp. 1043–1048, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Schneider and A. C. Issekutz, “Quantitation of eosinophil and neutrophil infiltration into rat lung by specific assays for eosinophil peroxidase and myeloperoxidase. Application in a Brown Norway rat model of allergic pulmonary inflammation,” Journal of Immunological Methods, vol. 198, no. 1, pp. 1–14, 1996. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Ito, C. Herbert, J. S. Siegle et al., “Steroid-resistant neutrophilic inflammation in a mouse model of an acute exacerbation of asthma,” American Journal of Respiratory Cell and Molecular Biology, vol. 39, no. 5, pp. 543–550, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Herbert, A. Hettiaratchi, D. C. Webb, P. S. Thomas, P. S. Foster, and R. K. Kumar, “Suppression of cytokine expression by roflumilast and dexamethasone in a model of chronic asthma,” Clinical and Experimental Allergy, vol. 38, no. 5, pp. 847–856, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. R. K. Kumar, P. S. Thomas, D.-Q. Seetoo et al., “Eotaxin expression by epithelial cells and plasma cells in chronic asthma,” Laboratory Investigation, vol. 82, no. 4, pp. 495–504, 2002. View at Scopus
  32. I. N. Mbawuike and H. B. Herscowitz, “MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics,” Journal of Leukocyte Biology, vol. 46, no. 2, pp. 119–127, 1989. View at Scopus
  33. A. Varin and S. Gordon, “Alternative activation of macrophages: immune function and cellular biology,” Immunobiology, vol. 214, no. 7, pp. 630–641, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. P. J. Murray and T. A. Wynn, “Obstacles and opportunities for understanding macrophage polarization,” Journal of Leukocyte Biology, vol. 89, no. 4, pp. 557–563, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. M. P. Nelson, B. S. Christmann, J. L. Werner et al., “IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina,” Journal of Immunology, vol. 186, no. 4, pp. 2372–2381, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Bhatia, M. Fei, M. Yarlagadda et al., “Rapid host defense against Aspergillus fumigatus involves alveolar macrophages with a predominance of alternatively activated phenotype,” PLoS ONE, vol. 6, no. 1, Article ID e15943, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. K. J. Mylonas, M. G. Nair, L. Prieto-Lafuente, D. Paape, and J. E. Allen, “Alternatively activated macrophages elicited by helminth infection can be reprogrammed to enable microbial killing,” Journal of Immunology, vol. 182, no. 5, pp. 3084–3094, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. D. R. Nagarkar, E. R. Bowman, D. Schneider et al., “Rhinovirus infection of allergen-sensitized and -challenged mice induces eotaxin release from functionally polarized macrophages,” Journal of Immunology, vol. 185, no. 4, pp. 2525–2535, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. L. J. H. van Tits, R. Stienstra, P. L. van Lent, M. G. Netea, L. A. B. Joosten, and A. F. H. Stalenhoef, “Oxidized LDL enhances pro-inflammatory responses of alternatively activated M2 macrophages: a crucial role for Krüppel-like factor 2,” Atherosclerosis, vol. 214, no. 2, pp. 345–349, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Y. Kim, J. T. Battaile, A. C. Patel et al., “Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease,” Nature Medicine, vol. 14, no. 6, pp. 633–640, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. B. N. Melgert, T. B. Oriss, Z. Qi et al., “Macrophages: regulators of sex differences in asthma?” American Journal of Respiratory Cell and Molecular Biology, vol. 42, no. 5, pp. 595–603, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. L. S. Subrata, J. Bizzintino, E. Mamessier et al., “Interactions between innate antiviral and atopic immunoinflammatory pathways precipitate and sustain asthma exacerbations in children,” Journal of Immunology, vol. 183, no. 4, pp. 2793–2800, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. D. A. Hume, “Macrophages as APC and the dendritic cell myth,” Journal of Immunology, vol. 181, no. 9, pp. 5829–5835, 2008. View at Scopus
  44. S. M. Pope, P. C. Fulkerson, C. Blanchard et al., “Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation,” Journal of Biological Chemistry, vol. 280, no. 14, pp. 13952–13961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Iwashita, S. Morita, Y. Sagiya, and A. Nakanishi, “Role of eosinophil chemotactic factor by T lymphocytes on airway hyperresponsiveness in a murine model of allergic asthma,” American Journal of Respiratory Cell and Molecular Biology, vol. 35, no. 1, pp. 103–109, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Chen, B. A. Jacobson, L. Mason, S. F. Wolf, and M. R. Bowman, “FIZZ1 potentiates the carbachol-induced tracheal smooth muscle contraction,” European Respiratory Journal, vol. 36, no. 5, pp. 1165–1173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Raes, L. Brys, B. K. Dahal et al., “Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation,” Journal of Leukocyte Biology, vol. 77, no. 3, pp. 321–327, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Kearley, K. F. Buckland, S. A. Mathie, and C. M. Lloyd, “Resolution of allergic inflammation and airway hyperreactivity is dependent upon disruption of the T1/ST2-IL-33 pathway,” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 9, pp. 772–781, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. A. D. Joshi, S. R. Oak, A. J. Hartigan et al., “Interleukin-33 contributes to both M1 and M2 chemokine marker expression in human macrophages,” BMC Immunology, vol. 11, article 52, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. W. A. Verri Jr., F. O. Souto, S. M. Vieira et al., “IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy,” Annals of the Rheumatic Diseases, vol. 69, no. 9, pp. 1697–1703, 2010. View at Publisher · View at Google Scholar · View at Scopus