Thymic stromal lymphopoietin controls prostaglandin D2 generation in patients with aspirin-exacerbated respiratory disease

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 5, 2016, Pages 1566-1576.e5

  Buchheit, Kathleen M ^a,b   Cahill, Katherine N ^a,b   Katz, Howard R ^a,b   Murphy, Katherine C ^b   Feng, Chunli ^b   Lee Sarwar, Kathleen ^a   Lai, Juying ^b   Bhattacharyya, Neil ^a,b   Israel, Elliot ^a,b   Boyce, Joshua A ^a,b   Laidlaw, Tanya M ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Aspirin exacerbated respiratory disease; cysteinyl leukotrienes; eosinophils; innate immunity; mast cells; nasal polyps; prostaglandin D2; Samter triad; thymic stromal lymphopoietin

Indexed keywords

ACETYLSALICYLIC ACID; ICOSANOID; INTERLEUKIN 33; MESSENGER RNA; PROSTAGLANDIN D2; THYMIC STROMAL LYMPHOPOIETIN; TRYPTASE; 9-HYDROXY-11,15-DIOXO-2,3,18,19-TETRANORPROST-5-ENE-1,20-DIOIC ACID; CYTOKINE; PROSTAGLANDIN D;

ADULT; AGED; ARTICLE; ASPIRIN EXACERBATED RESPIRATORY DISEASE; CELL SELECTION; CELL STIMULATION; CHEST TIGHTNESS; CHRONIC RHINOSINUSITIS; CONTROLLED STUDY; DISEASE SEVERITY; EOSINOPHIL COUNT; EOSINOPHILIA; FEMALE; FLOW CYTOMETRY; FORCED EXPIRATORY VOLUME; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG FUNCTION; MAJOR CLINICAL STUDY; MALE; MAST CELL; NOSE OBSTRUCTION; NOSE POLYP; OCULAR PRURITUS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSTAGLANDIN URINE LEVEL; QUANTITATIVE ANALYSIS; SNEEZING; URINE LEVEL; WESTERN BLOTTING; WHEEZING; BLOOD; CELL CULTURE; IMMUNOLOGY; LEUKOCYTE COUNT; MIDDLE AGED; RHINITIS; SINUSITIS; URINE; YOUNG ADULT;

ADULT; AGED; ASTHMA, ASPIRIN-INDUCED; CELLS, CULTURED; CYTOKINES; EOSINOPHILIA; FEMALE; HUMANS; LEUKOCYTE COUNT; MALE; MAST CELLS; MIDDLE AGED; NASAL POLYPS; PROSTAGLANDIN D2; PROSTAGLANDINS D; RHINITIS; SINUSITIS; YOUNG ADULT;

EID: 84949650780     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.10.020     Document Type: Article

References (54)

1. M.F. Gurish, A. Humbles, H. Tao, S. Finkelstein, J.A. Boyce, C. Gerard, and et al. CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis J Immunol 168 2002 5730 5736
2. J. Bousquet, P. Chanez, J.Y. Lacoste, G. Barneon, N. Ghavanian, I. Enander, and et al. Eosinophilic inflammation in asthma N Engl J Med 323 1990 1033 1039
3. C.A. Perez-Novo, C. Claeys, P. Van Cauwenberge, and C. Bachert Expression of eicosanoid receptors subtypes and eosinophilic inflammation: implication on chronic rhinosinusitis Respir Res 7 2006 75
4. A. Straumann Eosinophilic esophagitis: emerging therapies and future perspectives Gastroenterol Clin North Am 43 2014 385 394
5. G.M. Gauvreau, P.M. O'Byrne, L.P. Boulet, Y. Wang, D. Cockcroft, J. Bigler, and et al. Effects of an anti-TSLP antibody on allergen-induced asthmatic responses N Engl J Med 370 2014 2102 2110
6. Z. Guo, J. Wu, J. Zhao, F. Liu, Y. Chen, L. Bi, and et al. IL-33 promotes airway remodeling and is a marker of asthma disease severity J Asthma 51 2014 863 869
7. C.J. Corrigan, W. Wang, Q. Meng, C. Fang, G. Eid, M.R. Caballero, and et al. Allergen-induced expression of IL-25 and IL-25 receptor in atopic asthmatic airways and late-phase cutaneous responses J Allergy Clin Immunol 128 2011 116 124
8. S. Ying, B. O'Connor, J. Ratoff, Q. Meng, K. Mallett, D. Cousins, and et al. Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity J Immunol 174 2005 8183 8190
9. V. Soumelis, P.A. Reche, H. Kanzler, W. Yuan, G. Edward, B. Homey, and et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP Nat Immunol 3 2002 673 680
10. T. Liu, T.L. Li, F. Zhao, C. Xie, A.M. Liu, X. Chen, and et al. Role of thymic stromal lymphopoietin in the pathogenesis of nasal polyposis Am J Med Sci 341 2011 40 47
11. S. Kimura, R. Pawankar, S. Mori, M. Nonaka, S. Masuno, T. Yagi, and et al. Increased expression and role of thymic stromal lymphopoietin in nasal polyposis Allergy Asthma Immunol Res 3 2011 186 193
12. D.R. Nagarkar, J.A. Poposki, B.K. Tan, M.R. Comeau, A.T. Peters, K.E. Hulse, and et al. Thymic stromal lymphopoietin activity is increased in nasal polyps of patients with chronic rhinosinusitis J Allergy Clin Immunol 132 2013 593 600.e12
13. C. Ober, and T.C. Yao The genetics of asthma and allergic disease: A 21st century perspective Immunol Rev 242 2011 10 30
14. Z. Allakhverdi, M.R. Comeau, H.K. Jessup, B.R. Yoon, A. Brewer, S. Chartier, and et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells J Exp Med 204 2007 253 258
15. B.S. Kim, M.C. Siracusa, S.A. Saenz, M. Noti, L.A. Monticelli, G.F. Sonnenberg, and et al. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation Sci Transl Med 5 2013 170ra16
16. C. Vissinga, T. Martin, and M.R. Comeau TSLP driven expansion and activation of type 2 innate lymphoid cells is augmented by IL-25 and IL-33 Cytokine 63 2013
17. Z. Allakhverdi, M.R. Comeau, D.E. Smith, D. Toy, L.M. Endam, M. Desrosiers, and et al. CD34+ hemopoietic progenitor cells are potent effectors of allergic inflammation J Allergy Clin Immunol 123 2009 472 478
18. E.B. Cook, J.L. Stahl, E.A. Schwantes, K.E. Fox, and S.K. Mathur IL-3 and TNFalpha increase Thymic Stromal Lymphopoietin Receptor (TSLPR) expression on eosinophils and enhance TSLP-stimulated degranulation Clin Mol Allergy 10 2012 8
19. M. Noti, E.D. Wojno, B.S. Kim, M.C. Siracusa, P.R. Giacomin, M.G. Nair, and et al. Thymic stromal lymphopoietin-elicited basophil responses promote eosinophilic esophagitis Nat Med 19 2013 1005 1013
20. C.C. Hardy, C. Robinson, A.E. Tattersfield, and S.T. Holgate The bronchoconstrictor effect of inhaled prostaglandin D2 in normal and asthmatic men N Engl J Med 311 1984 209 213
21. N.A. Soter, R.A. Lewis, E.J. Corey, and K.F. Austen Local effects of synthetic leukotrienes (LTC4, LTD4, LTE4, and LTB4) in human skin J Invest Dermatol 80 1983 115 119
22. K. Nagata, H. Hirai, K. Tanaka, K. Ogawa, T. Aso, K. Sugamura, and et al. CRTH2, an orphan receptor of T-helper-2-cells, is expressed on basophils and eosinophils and responds to mast cell-derived factor(s) FEBS Lett 459 1999 195 199
23. H. Hirai, K. Tanaka, O. Yoshie, K. Ogawa, K. Kenmotsu, Y. Takamori, and et al. Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2 J Exp Med 193 2001 255 261
24. I. Spik, C. Brenuchon, V. Angeli, D. Staumont, S. Fleury, M. Capron, and et al. Activation of the prostaglandin D2 receptor DP2/CRTH2 increases allergic inflammation in mouse J Immunol 174 2005 3703 3708
25. R. He, M.K. Oyoshi, J.Y. Wang, M.R. Hodge, H. Jin, and R.S. Geha The prostaglandin D(2) receptor CRTH2 is important for allergic skin inflammation after epicutaneous antigen challenge J Allergy Clin Immunol 126 2010 784 790
26. J.M. Mjosberg, S. Trifari, N.K. Crellin, C.P. Peters, C.M. van Drunen, B. Piet, and et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161 Nat Immunol 12 2011 1055 1062
27. L. Xue, M. Salimi, I. Panse, J.M. Mjosberg, A.N. McKenzie, H. Spits, and et al. Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells J Allergy Clin Immunol 133 2014 1184 1194
28. J.L. Shaw, S. Fakhri, M.J. Citardi, P.C. Porter, D.B. Corry, F. Kheradmand, and et al. IL-33-responsive innate lymphoid cells are an important source of IL-13 in chronic rhinosinusitis with nasal polyps Am J Respir Crit Care Med 188 2013 432 439
29. J.L. Shaw, F. Ashoori, S. Fakhri, M.J. Citardi, and A. Luong Increased percentage of mast cells within sinonasal mucosa of chronic rhinosinusitis with nasal polyp patients independent of atopy Int Forum Allergy Rhinol 2 2012 233 240
30. C.B. Johns, and T.M. Laidlaw Elevated total serum IgE in nonatopic patients with aspirin-exacerbated respiratory disease Am J Rhinol Allergy 28 2014 287 289
31. J.H. Lee, T. Haselkorn, L. Borish, L. Rasouliyan, B.E. Chipps, and S.E. Wenzel Risk factors associated with persistent airflow limitation in severe or difficult-to-treat asthma: insights from the TENOR study Chest 132 2007 1882 1889
32. G. Bochenek, K. Nagraba, E. Nizankowska, and A. Szczeklik A controlled study of 9alpha,11beta-PGF2 (a prostaglandin D2 metabolite) in plasma and urine of patients with bronchial asthma and healthy controls after aspirin challenge J Allergy Clin Immunol 111 2003 743 749
33. K.N. Cahill, J.C. Bensko, J.A. Boyce, and T.M. Laidlaw Prostaglandin D(2): A dominant mediator of aspirin-exacerbated respiratory disease J Allergy Clin Immunol 135 2015 245 252
34. J.D. Morrow, C. Guzzo, G. Lazarus, J.A. Oates, and L.J. Roberts 2nd Improved diagnosis of mastocytosis by measurement of the major urinary metabolite of prostaglandin D2 J Invest Dermatol 104 1995 937 940
35. H. Ochi, W.M. Hirani, Q. Yuan, D.S. Friend, K.F. Austen, and J.A. Boyce T helper cell type 2 cytokine-mediated comitogenic responses and CCR3 expression during differentiation of human mast cells in vitro J Exp Med 190 1999 267 280
36. Y. Jiang, Y. Kanaoka, C. Feng, K. Nocka, S. Rao, and J.A. Boyce Cutting edge: interleukin 4-dependent mast cell proliferation requires autocrine/intracrine cysteinyl leukotriene-induced signaling J Immunol 177 2006 2755 2759
37. M. Murakami, R. Matsumoto, K.F. Austen, and J.P. Arm Prostaglandin endoperoxide synthase-1 and -2 couple to different transmembrane stimuli to generate prostaglandin D2 in mouse bone marrow-derived mast cells J Biol Chem 269 1994 22269 22275
38. E. Ono, M. Taniguchi, H. Mita, Y. Fukutomi, N. Higashi, E. Miyazaki, and et al. Increased production of cysteinyl leukotrienes and prostaglandin D2 during human anaphylaxis Clin Exp Allergy 39 2009 72 80
39. D.R. Nagarkar, J.A. Poposki, M.R. Comeau, A. Biyasheva, P.C. Avila, R.P. Schleimer, and et al. Airway epithelial cells activate TH2 cytokine production in mast cells through IL-1 and thymic stromal lymphopoietin J Allergy Clin Immunol 130 2012 225 232.e4
40. A.R. Fischer, M.A. Rosenberg, C.M. Lilly, J.C. Callery, P. Rubin, J. Cohn, and et al. Direct evidence for a role of the mast cell in the nasal response to aspirin in aspirin-sensitive asthma J Allergy Clin Immunol 94 1994 1046 1056
41. T. Yoshimura, M. Yoshikawa, N. Otori, S. Haruna, and H. Moriyama Correlation between the prostaglandin D(2)/E(2) ratio in nasal polyps and the recalcitrant pathophysiology of chronic rhinosinusitis associated with bronchial asthma Allergol Int 57 2008 429 436
42. T. Liu, T.M. Laidlaw, H.R. Katz, and J.A. Boyce Prostaglandin E2 deficiency causes a phenotype of aspirin sensitivity that depends on platelets and cysteinyl leukotrienes Proc Natl Acad Sci U S A 110 2013 16987 16992
43. K. Sladek, and A. Szczeklik Cysteinyl leukotrienes overproduction and mast cell activation in aspirin-provoked bronchospasm in asthma Eur Respir J 6 1993 391 399
44. M. Kupczyk, Z. Kurmanowska, I. Kuprys-Lipinska, M. Bochenska-Marciniak, and P. Kuna Mediators of inflammation in nasal lavage from aspirin intolerant patients after aspirin challenge Respir Med 104 2010 1404 1409
45. K. Hamada, Y. Yamada, Y. Kamada, S. Ueki, K. Yamaguchi, H. Oyamada, and et al. Prostaglandin D2 and interleukin-5 reduce CRTH2 surface expression on human eosinophils Allergol Int 53 2004 179 184
46. L. Machado-Carvalho, J. Roca-Ferrer, and C. Picado Prostaglandin E2 receptors in asthma and in chronic rhinosinusitis/nasal polyps with and without aspirin hypersensitivity Respir Res 15 2014 100
47. S.L. Johnston, N.J. Freezer, W. Ritter, S. O'Toole, and P.H. Howarth Prostaglandin D2-induced bronchoconstriction is mediated only in part by the thromboxane prostanoid receptor Eur Respir J 8 1995 411 415
48. E. Lai, I. De Lepeleire, T.M. Crumley, F. Liu, L.A. Wenning, N. Michiels, and et al. Suppression of niacin-induced vasodilation with an antagonist to prostaglandin D2 receptor subtype 1 Clin Pharmacol Ther 81 2007 849 857
49. Y. Kanaoka, H. Ago, E. Inagaki, T. Nanayama, M. Miyano, R. Kikuno, and et al. Cloning and crystal structure of hematopoietic prostaglandin D synthase Cell 90 1997 1085 1095
50. T. Luna-Gomes, K.G. Magalhaes, F.P. Mesquita-Santos, I. Bakker-Abreu, R.F. Samico, R. Molinaro, and et al. Eosinophils as a novel cell source of prostaglandin D2: Autocrine role in allergic inflammation J Immunol 187 2011 6518 6526
51. M. Okano, T. Fujiwara, M. Yamamoto, Y. Sugata, R. Matsumoto, K. Fukushima, and et al. Role of prostaglandin D2 and E2 terminal synthases in chronic rhinosinusitis Clin Exp Allergy 36 2006 1028 1038
52. N.R. Han, H.A. Oh, S.Y. Nam, P.D. Moon, D.W. Kim, H.M. Kim, and et al. TSLP induces mast cell development and aggravates allergic reactions through the activation of MDM2 and STAT6 J Invest Dermatol 134 2014 2521 2530
53. M. Miyata, K. Hatsushika, T. Ando, N. Shimokawa, Y. Ohnuma, R. Katoh, and et al. Mast cell regulation of epithelial TSLP expression plays an important role in the development of allergic rhinitis Eur J Immunol 38 2008 1487 1492
54. L. Xue, S.L. Gyles, F.R. Wettey, L. Gazi, E. Townsend, M.G. Hunter, and et al. Prostaglandin D2 causes preferential induction of proinflammatory Th2 cytokine production through an action on chemoattractant receptor-like molecule expressed on Th2 cells J Immunol 175 2005 6531 6536