Table of Contents
Journal of Allergy
Volume 2012, Article ID 182090, 9 pages
http://dx.doi.org/10.1155/2012/182090
Review Article

Interleukin-4 in the Generation of the AERD Phenotype: Implications for Molecular Mechanisms Driving Therapeutic Benefit of Aspirin Desensitization

1Asthma and Allergic Disease Center, Beirne Carter B. Center for Immunology Research, University of Virginia Health System, Charlottesville, VA 22908, USA
2Department of Medicine, University of Virginia Health System, Charlottesville, VA 22908, USA
3Department of Otolaryngology—Head and Neck Surgery, University of Virginia Health System, Charlottesville, VA 22908, USA

Received 1 July 2011; Accepted 4 October 2011

Academic Editor: Hae-Sim Park

Copyright © 2012 John W. Steinke 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. K. Mascia, T. Haselkorn, Y. M. Deniz, D. P. Miller, E. R. Bleecker, and L. Borish, “Aspirin sensitivity and severity of asthma: evidence for irreversible airway obstruction in patients with severe or difficult-to-treat asthma,” Journal of Allergy and Clinical Immunology, vol. 116, no. 5, pp. 970–975, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Mascia, L. Borish, J. Patrie, J. Hunt, C. D. Phillips, and J. W. Steinke, “Chronic hyperplastic eosinophilic sinusitis as a predictor of aspirin-exacerbated respiratory disease,” Annals of Allergy, Asthma and Immunology, vol. 94, no. 6, pp. 652–657, 2005. View at Google Scholar · View at Scopus
  3. A. Szczeklik and D. D. Stevenson, “Aspirin-induced asthma: advances in pathogenesis and management,” Journal of Allergy and Clinical Immunology, vol. 104, no. 1, pp. 5–13, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Szczeklik and E. Nizankowska, “Clinical features and diagnosis of aspirin induced asthma,” Thorax, vol. 55, no. 2, pp. S42–S44, 2000. View at Google Scholar · View at Scopus
  5. M. P. Berges-Gimeno, R. A. Simon, and D. D. Stevenson, “The natural history and clinical characteristics of aspirin-exacerbated respiratory disease,” Annals of Allergy, Asthma and Immunology, vol. 89, no. 5, pp. 474–478, 2002. View at Google Scholar · View at Scopus
  6. A. Antczak, P. Montuschi, S. Kharitonov, P. Gorski, and P. J. Barnes, “Increased exhaled cysteinyl-leukotrienes and 8-isoprostane in aspirin-induced asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 166, no. 3, pp. 301–306, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. P. J. Daffern, D. Muilenburg, T. E. Hugli, and D. D. Stevenson, “Association of urinary leukotriene E4 excretion during aspirin challenges with severity of respiratory responses,” Journal of Allergy and Clinical Immunology, vol. 104, no. 3, pp. 559–564, 1999. View at Google Scholar · View at Scopus
  8. J. W. Steinke, D. Bradley, P. Arango et al., “Cysteinyl leukotriene expression in chronic hyperplastic sinusitis-nasal polyposis: importance to eosinophilia and asthma,” Journal of Allergy and Clinical Immunology, vol. 111, no. 2, pp. 342–349, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. T. C. Beller, D. S. Friend, A. Maekawa, B. K. Lam, K. F. Austen, and Y. Kanaoka, “Cysteinyl leukotriene 1 receptor controls the severity of chronic pulmonary inflammation and fibrosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 3047–3052, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. A. P. Sampson, A. S. Cowburn, K. Sladek et al., “Profound overexpression of leukotriene C4 synthase in bronchial biopsies from aspirin-intolerant asthmatic patients,” International Archives of Allergy and Immunology, vol. 113, no. 1–3, pp. 355–357, 1997. View at Google Scholar · View at Scopus
  11. A. S. Cowburn, K. Sladek, J. Soja et al., “Overexpression of leukotriene C4 synthase in bronchial biopsies from patients with aspirin-intolerant asthma,” Journal of Clinical Investigation, vol. 101, no. 4, pp. 834–846, 1998. View at Google Scholar · View at Scopus
  12. C. A. Pérez-Novo, J. B. Watelet, C. Claeys, P. van Cauwenberge, and C. Bachert, “Prostaglandin, leukotriene, and lipoxin balance in chronic rhinosinusitis with and without nasal polyposis,” Journal of Allergy and Clinical Immunology, vol. 115, no. 6, pp. 1189–1196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Israel, A. R. Fischer, M. A. Rosenberg et al., “The pivotal role of 5-lipoxygenase products in the reaction of aspirin- sensitive asthmatics to aspirin,” American Review of Respiratory Disease, vol. 148, no. 6, pp. 1447–1451, 1993. View at Google Scholar · View at Scopus
  14. K. Sladek and A. Szczeklik, “Cysteinyl leukotrienes overproduction and mast cell activation in aspirin-provoked bronchospasm in asthma,” European Respiratory Journal, vol. 6, no. 3, pp. 391–399, 1993. View at Google Scholar · View at Scopus
  15. A. R. Fischer, M. A. Rosenberg, C. M. Lilly et al., “Direct evidence for a role of the mast cell in the nasal response to aspirin in aspirin-sensitive asthma,” Journal of Allergy and Clinical Immunology, vol. 94, no. 6, pp. 1046–1056, 1994. View at Publisher · View at Google Scholar · View at Scopus
  16. S. M. S. Nasser, M. Patel, G. S. Bell, and T. H. Lee, “The effect of aspirin desensitization on urinary leukotriene E4 concentrations in aspirin-sensitive asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 5, pp. 1326–1330, 1995. View at Google Scholar · View at Scopus
  17. F. H. Hsieh, B. K. Lam, J. F. Penrose, K. F. Austen, and J. A. Boyce, “T helper cell type 2 cytokines coordinately regulate immunoglobulin E-dependent cysteinyl leukotriene production by human cord blood-derived mast cells: profound induction of leukotriene C4 synthase expression by interleukin 4,” Journal of Experimental Medicine, vol. 193, no. 1, pp. 123–133, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Denburg, “Haemopoietic mechanisms in nasal polyposis and asthma,” Thorax, vol. 55, no. 2, pp. S24–S25, 2000. View at Google Scholar · View at Scopus
  19. D. L. Hamilos, D. Y. M. Leung, R. Wood et al., “Evidence for distinct cytokine expression in allergic versus nonallergic chronic sinusitis,” Journal of Allergy and Clinical Immunology, vol. 96, no. 4, pp. 537–544, 1995. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Riechelmann, T. Deutschle, A. Rozsasi, T. Keck, D. Polzehl, and H. Bürner, “Nasal biomarker profiles in acute and chronic rhinosinusitis,” Clinical and Experimental Allergy, vol. 35, no. 9, pp. 1186–1191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Kamil, O. Ghaffar, F. Lavigne, R. Taha, P. M. Renzi, and Q. Hamid, “Comparison of inflammatory cell profile and Th2 cytokine expression in the ethmoid sinuses, maxillary sinuses, and turbinates of atopic subjects with chronic sinusitis,” Otolaryngology—Head and Neck Surgery, vol. 118, no. 6, pp. 804–809, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. J. P. Arm, S. P. O'Hickey, B. W. Spur, and T. H. Lee, “Airway responsiveness to histamine and leukotriene E4 in subjects with aspirin-induced asthma,” American Review of Respiratory Disease, vol. 140, no. 1, pp. 148–153, 1989. View at Google Scholar · View at Scopus
  23. A. R. Sousa, A. Parikh, G. Scadding, C. J. Corrigan, and T. H. Lee, “Leukotriene-receptor expression on nasal mucosal inflammatory cells in aspirin-sensitive rhinosinusitis,” The New England Journal of Medicine, vol. 347, no. 19, pp. 1493–1499, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. K. F. Austen, A. Maekawa, Y. Kanaoka, and J. A. Boyce, “The leukotriene E4 puzzle: finding the missing pieces and revealing the pathobiologic implications,” Journal of Allergy and Clinical Immunology, vol. 124, no. 3, pp. 406–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. K. R. Lynch, G. P. O'Neill, Q. Liu et al., “Characterization of the human cysteinyl leukotriene CysLT1 receptor,” Nature, vol. 399, no. 6738, pp. 789–793, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. S. E. Dahlén, K. Malmström, E. W. A. Nizankowska et al., “Improvement of aspirin-intolerant asthma by montelukast, a leukotriene antagonist: a randomized, double-blind, placebo-controlled trial,” American Journal of Respiratory and Critical Care Medicine, vol. 165, no. 1, pp. 9–14, 2002. View at Google Scholar
  27. A. White, E. Ludington, P. Mehra, D. D. Stevenson, and R. A. Simon, “Effect of leukotriene modifier drugs on the safety of oral aspirin challenges,” Annals of Allergy, Asthma and Immunology, vol. 97, no. 5, pp. 688–693, 2006. View at Google Scholar · View at Scopus
  28. C. E. Heise, B. F. O'Dowd, D. J. Figueroa et al., “Characterization of the human cysteinyl leukotriene 2 receptor,” Journal of Biological Chemistry, vol. 275, no. 39, pp. 30531–30536, 2000. View at Google Scholar · View at Scopus
  29. D. J. Figueroa, R. M. Breyer, S. K. Defoe et al., “Expression of the cysteinyl leukotriene 1 receptor in normal human lung and peripheral blood leukocytes,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 1, pp. 226–233, 2001. View at Google Scholar · View at Scopus
  30. D. J. Figueroa, L. Borish, D. Baramki, G. Philip, C. P. Austin, and J. F. Evans, “Expression of cysteinyl leukotriene synthetic and signalling proteins in inflammatory cells in active seasonal allergic rhinitis,” Clinical and Experimental Allergy, vol. 33, no. 10, pp. 1380–1388, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. S. B. Early, E. Barekzi, J. Negri, K. Hise, L. Borish, and J. W. Steinke, “Concordant modulation of cysteinyl leukotriene receptor expression by IL-4 and IFN-γ on peripheral immune cells,” American Journal of Respiratory Cell and Molecular Biology, vol. 36, no. 6, pp. 715–720, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. J. W. Steinke, C. D. Crouse, D. Bradley et al., “Characterization of interleukin-4-stimulated nasal polyp fibroblasts,” American Journal of Respiratory Cell and Molecular Biology, vol. 30, no. 2, pp. 212–219, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. E. A. Mellor, K. F. Austen, and J. A. Boyce, “Cysteinyl leukotrienes and uridine diphosphate induce cytokine generation by human mast cells through an interleukin 4-regulated pathway that is inhibited by leukotriene receptor antagonists,” Journal of Experimental Medicine, vol. 195, no. 5, pp. 583–592, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. E. A. Mellor, N. Frank, D. Soler et al., “Expression of the type 2 receptor for cysteinyl leukotrienes (CysLT2r) by human mast cells: functional distinction from CysLT1r,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 20, pp. 11589–11593, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Thivierge, J. Staňková, and M. Rola-Pleszczynski, “IL-13 and IL-4 up-regulate cysteinyl leukotriene 1 receptor expression in human monocytes and macrophages,” Journal of Immunology, vol. 167, no. 5, pp. 2855–2860, 2001. View at Google Scholar · View at Scopus
  36. G. Woszczek, R. Pawliczak, H. Y. Qi et al., “Functional characterization of human cysteinyl leukotriene 1 receptor gene structure,” Journal of Immunology, vol. 175, no. 8, pp. 5152–5159, 2005. View at Google Scholar · View at Scopus
  37. M. Schmid, U. Göde, D. Schäfer, and M. E. Wigand, “Arachidonic acid metabolism in nasal tissue and peripheral blood cells in aspirin intolerant asthmatics,” Acta Oto-Laryngologica, vol. 119, no. 2, pp. 277–280, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Sestini, L. Armetti, C. Gambaro et al., “Inhaled PGE2 prevents aspirin-induced bronchoconstriction and urinary LTE4 excretion in aspirin-sensitive asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 153, no. 2, pp. 572–575, 1996. View at Google Scholar · View at Scopus
  39. C. Feng, E. M. Beller, S. Bagga, and J. A. Boyce, “Human mast cells express multiple EP receptors for prostaglandin E 2 that differentially modulate activation responses,” Blood, vol. 107, no. 8, pp. 3243–3250, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Ying, Q. Meng, G. Scadding, A. Parikh, C. J. Corrigan, and T. H. Lee, “Aspirin-sensitive rhinosinusitis is associated with reduced E-prostanoid 2 receptor expression on nasal mucosal inflammatory cells,” Journal of Allergy and Clinical Immunology, vol. 117, no. 2, pp. 312–318, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Picado, J. C. Fernandez-Morata, M. Juan et al., “Cyclooxygenase-2 mRNA is downexpressed in nasal polyps from aspirin- sensitive asthmatics,” American Journal of Respiratory and Critical Care Medicine, vol. 160, no. 1, pp. 291–296, 1999. View at Google Scholar · View at Scopus
  42. J. Gosepath, R. G. Amedee, and W. J. Mann, “Nasal provocation testing as an international standard for evaluation of allergic and nonallergic rhinitis,” Laryngoscope, vol. 115, no. 3, pp. 512–516, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. J. W. Steinke, J. A. Culp, E. Kropf, and L. Borish, “Modulation by aspirin of nuclear phospho-signal transducer and activator of transcription 6 expression: possible role in therapeutic benefit associated with aspirin desensitization,” Journal of Allergy and Clinical Immunology, vol. 124, no. 4, pp. 724.e4–730.e4, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Murakami, K. Nakashima, D. Kamei et al., “Cellular prostaglandin E2 production by membrane-bound prostaglandin E synthase-2 via both cyclooxygenases-1 and -2,” Journal of Biological Chemistry, vol. 278, no. 39, pp. 37937–37947, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Yano, H. A. Hopkins, S. L. Hempel, M. Monick, and G. W. Hunninghake, “Interleukin-4 inhibits lipopolysaccharide-induced expression of prostaglandin H synthase-2 in human alveolar macrophages,” Journal of Cellular Physiology, vol. 165, no. 1, pp. 77–82, 1995. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Dworski and J. R. Sheller, “Differential sensitivities of human blood monocytes and alveolar macrophages to the inhibition of prostaglandin endoperoxide synthase-2 by interleukin-4,” Prostaglandins, vol. 53, no. 4, pp. 237–251, 1997. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. Sweet, D. D. Stevenson, R. A. Simon, and D. A. Mathison, “Long-term effects of aspirin desensitization—treatment for aspirin-sensitive rhinosinusitis-asthma,” Journal of Allergy and Clinical Immunology, vol. 85, no. 1, pp. 59–65, 1990. View at Google Scholar · View at Scopus
  48. D. D. Stevenson and R. A. Simon, “Selection of patients for aspirin desensitization treatment,” Journal of Allergy and Clinical Immunology, vol. 118, no. 4, pp. 801–804, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. U. R. Juergens, S. C. Christiansen, D. D. Stevenson, and B. L. Zuraw, “Inhibition of monocyte leukotriene B4 production after aspirin desensitization,” Journal of Allergy and Clinical Immunology, vol. 96, no. 2, pp. 148–156, 1995. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Kopp and S. Ghosh, “Inhibition of NF-κB by sodium salicylate and aspirin,” Science, vol. 265, no. 5174, pp. 956–959, 1994. View at Google Scholar · View at Scopus
  51. I. Tegeder, J. Pfeilschifter, and G. Geisslinger, “Cyclooxygenase-independent actions of cyclooxygenase inhibitors,” FASEB Journal, vol. 15, no. 12, pp. 2057–2072, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Aceves, A. Dueñas, C. Gómez, E. san Vicente, M. S. Crespo, and C. García-Rodríguez, “A new pharmacological effect of salicylates: inhibition of NFAT-dependent transcription,” Journal of Immunology, vol. 173, no. 9, pp. 5721–5729, 2004. View at Google Scholar
  53. A. Cianferoni, J. T. Schroeder, J. Kim et al., “Selective inhibition of interleukin-4 gene expression in human T cells by aspirin,” Blood, vol. 97, no. 6, pp. 1742–1749, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. R. K. Katial, M. Strand, T. Prasertsuntarasai, R. Leung, W. Zheng, and R. Alam, “The effect of aspirin desensitization on novel biomarkers in aspirin-exacerbated respiratory diseases,” Journal of Allergy and Clinical Immunology, vol. 126, no. 4, pp. 738–744, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. G. M. Perez, M. Melo, A. D. Keegan, and J. Zamorano, “Aspirin and salicylates inhibit the IL-4- and IL-13-induced activation of STAT6,” Journal of Immunology, vol. 168, no. 3, pp. 1428–1434, 2002. View at Google Scholar · View at Scopus
  56. A. White, T. Bigby, and D. Stevenson, “Intranasal ketorolac challenge for the diagnosis of aspirin-exacerbated respiratory disease,” Annals of Allergy, Asthma and Immunology, vol. 97, no. 2, pp. 190–195, 2006. View at Google Scholar · View at Scopus
  57. R. U. Lee, A. A. White, D. Ding et al., “Use of intranasal ketorolac and modified oral aspirin challenge for desensitization of aspirin-exacerbated respiratory disease,” Annals of Allergy, Asthma and Immunology, vol. 105, no. 2, pp. 130–135, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Sczeklik and E. Nizankowska, “Asthma improved by aspirin-like drugs,” British Journal of Diseases of the Chest, vol. 77, no. 2, pp. 153–158, 1983. View at Google Scholar · View at Scopus
  59. B. Dahlén, E. Nizankowska, A. Szczeklik et al., “Benefits from adding the 5-lipoxygenase inhibitor zileuton to conventional therapy in aspirin-intolerant asthmatics,” American Journal of Respiratory and Critical Care Medicine, vol. 157, no. 4, pp. 1187–1194, 1998. View at Google Scholar · View at Scopus