Eosinophils are dispensable for allergic remodeling and immunity in a model of house dust mite-induced airway disease

American Journal of Respiratory and Critical Care Medicine

Volumn 183, Issue 2, 2011, Pages 179-188

  Fattouh, Ramzi ^a   Al Garawi, Amal ^a   Fattouh, Marcia ^a   Arias, Katherine ^a   Walker, Tina D ^a   Goncharova, Susanna ^a   Coyle, Anthony J ^b   Humbles, Alison A ^b   Jordana, Manel ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b Medlmmune LLC   (United States)

Author keywords

Airway remodeling; Allergic asthma; Eosinophils; House dust mite; Mouse

Indexed keywords

CHEMOKINE RECEPTOR CCR3; COLLAGEN; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 5; METHACHOLINE; RECEPTOR ANTIBODY;

AIRWAY REMODELING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DERMATOPHAGOIDES; EOSINOPHIL; EOSINOPHILIA; FEMALE; HOUSE DUST ALLERGY; IMMUNOGLOBULIN BLOOD LEVEL; LONG TERM EXPOSURE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; SMOOTH MUSCLE; SPLEEN CELL; TH2 CELL; WILD TYPE;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; COLLAGEN; DISEASE MODELS, ANIMAL; EOSINOPHILS; FEMALE; IMMUNOGLOBULIN E; INFLAMMATION; MICE; MICE, INBRED BALB C; PYROGLYPHIDAE; RESPIRATORY HYPERSENSITIVITY; RESPIRATORY MUCOSA;

EID: 78751691489     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200905-0736OC     Document Type: Article

References (45)

1. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745. (Pubitemid 30329053)
2. James AL, Wenzel S. Clinical relevance of airway remodelling in airway diseases. Eur Respir J 2007;30:134-155. (Pubitemid 47074016)
3. McParland BE, Macklem PT, Pare PD. Airway wall remodeling: friend or foe? J Appl Physiol 2003;95:426-434.
4. Ochkur SI, Jacobsen EA, Protheroe CA, Biechele TL, Pero RS, McGarry MP, Wang H, O'Neill KR, Colbert DC, Colby TV, et al. Coexpression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J Immunol 2007;178:7879-7889.
5. Blyth DI, Wharton TF, Pedrick MS, Savage TJ, Sanjar S. Airway subepithelial fibrosis in a murine model of atopic asthma: suppression by dexamethasone or anti-interleukin-5 antibody. Am J Respir Cell Mol Biol 2000;23:241-246. (Pubitemid 30656435)
6. Cho JY, Miller M, Baek KJ, Han JW, Nayar J, Lee SY, McElwain K, McElwain S, Friedman S, Broide DH. Inhibition of airway remodeling in IL-5-deficient mice. J Clin Invest 2004;113:551-560. (Pubitemid 38542504)
7. Foster PS, Ming Y, Matthei KI, Young IG, Temelkovski J, Kumar RK. Dissociation of inflammatory and epithelial responses in a murine model of chronic asthma. Lab Invest 2000;80:655-662. (Pubitemid 30340649)
8. Kumar RK, Herbert C, Webb DC, Li L, Foster PS. Effects of anticytokine therapy in a mouse model of chronic asthma. Am J Respir Crit Care Med 2004;170:1043-1048. (Pubitemid 39488615)
9. Leigh R, Ellis R, Wattie JN, Hirota JA, Matthaei KI, Foster PS, O'Byrne PM, Inman MD. Type 2 cytokines in the pathogenesis of sustained airway dysfunction and airway remodeling in mice. Am J Respir Crit Care Med 2004;169:860-867.
10. Tanaka H, Komai M, Nagao K, Ishizaki M, Kajiwara D, Takatsu K, Delespesse G, Nagai H. Role of interleukin-5 and eosinophils in allergen-induced airway remodeling in mice. Am J Respir Cell Mol Biol 2004;31:62-68.
11. Humbles AA, Lloyd CM, McMillan SJ, Friend DS, Xanthou G, McKenna EE, Ghiran S, Gerard NP, Yu C, Orkin SH, et al. A critical role for eosinophils in allergic airways remodeling. Science 2004;305:1776-1779.
12. Alcorn JF, Rinaldi LM, Jaffe EF, van Loon M, Bates JH, Janssen- Heininger YM, Irvin CG. Transforming growth factor-beta1 suppresses airway hyperresponsiveness in allergic airway disease. Am J Respir Crit Care Med 2007;176:974-982.
13. Le AV, Cho JY, Miller M, McElwain S, Golgotiu K, Broide DH. Inhibition of allergen-induced airway remodeling in Smad 3-deficient mice. J Immunol 2007;178:7310-7316.
14. McMillan SJ, Xanthou G, Lloyd CM. Manipulation of allergeninduced airway remodeling by treatment with anti-TGF-beta antibody: effect on the Smad signaling pathway. J Immunol 2005;174:5774-5780.
15. Fattouh R, Midence NG, Arias K, Johnson JR,Walker TD, Goncharova S, Souza KP, Gregory RC Jr, Lonning S, Gauldie J, et al. Transforming growth factor-beta regulates house dust mite-induced allergic airway inflammation but not airway remodeling. Am J Respir Crit Care Med 2008;177:593-603.
16. Fattouh, R., A. Al-Garawi, M. Fattouh, K. Arias, T. D. Walker, S. Goncharova, and M. Jordana. House dust mite-induced allergic airway remodeling develops independently of eosinophils [abstract]. Am J Respir Crit Care Med 2009;179:A1396.
17. Lee JJ, Dimina D, Macias MP, Ochkur SI, McGarry MP, O'Neill KR, Protheroe C, Pero R, Nguyen T, Cormier SA, et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science 2004;305:1773-1776.
18. Grimaldi JC, Yu NX, Grunig G, Seymour BW, Cottrez F, Robinson DS, Hosken N, Ferlin WG, Wu X, Soto H, et al. Depletion of eosinophils in mice through the use of antibodies specific for C-C chemokine receptor 3 (CCR3). J Leukoc Biol 1999;65:846-853.
19. Justice JP, Borchers MT, Crosby JR, Hines EM, Shen HH, Ochkur SI, McGarry MP, Lee NA, Lee JJ. Ablation of eosinophils leads to a reduction of allergen-induced pulmonary pathology. Am J Physiol Lung Cell Mol Physiol 2003;284:L169-L178.
20. ShenHH,Xu F,ZhangGS,Wang SB, XuWH.CCR3monoclonal antibody inhibits airway eosinophilic inflammation and mucus overproduction in a mouse model of asthma. Acta Pharmacol Sin 2006;27:1594-1599.
21. Jacobsen EA, Ochkur SI, Pero RS, Taranova AG, Protheroe CA, Colbert DC, Lee NA, Lee JJ. Allergic pulmonary inflammation in mice is dependent on eosinophil-induced recruitment of effector T cells. J Exp Med 2008;205:699-710.
22. Asokananthan N, Graham PT, Stewart DJ, Bakker AJ, Eidne KA, Thompson PJ, Stewart GA. House dust mite allergens induce proin- flammatory cytokines from respiratory epithelial cells: the cysteine protease allergen, Der p 1, activates protease-activated receptor (PAR)-2 and inactivates PAR-1. J Immunol 2002;169:4572-4578.
23. Chen CL, Lee CT, Liu YC, Wang JY, Lei HY, Yu CK. House dust mite Dermatophagoides farinae augments proinflammatory mediator productions and accessory function of alveolar macrophages: implications for allergic sensitization and inflammation. J Immunol 2003;170:528-536.
24. Hammad H, ChieppaM, Perros F, Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 2009;15:410-416.
25. King C, Brennan S, Thompson PJ, Stewart GA. Dust mite proteolytic allergens induce cytokine release from cultured airway epithelium. J Immunol 1998;161:3645-3651.
26. Schulz O, Sewell HF, Shakib F. Proteolytic cleavage of CD25, the alpha subunit of the human T cell interleukin 2 receptor, by Der p 1, a major mite allergen with cysteine protease activity. J Exp Med 1998;187:271-275.
27. Sun G, Stacey MA, Schmidt M, Mori L, Mattoli S. Interaction of mite allergens Der p3 and Der p9 with protease-activated receptor-2 expressed by lung epithelial cells. J Immunol 2001;167:1014-1021.
28. Trompette A, Divanovic S, Visintin A, Blanchard C, Hegde RS, Madan R, Thorne PS,Wills-Karp M, Gioannini TL,Weiss JP, et al. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 2009;457:585-588.
29. Wan H, Winton HL, Soeller C, Tovey ER, Gruenert DC, Thompson PJ, Stewart GA, Taylor GW, Garrod DR, Cannell MB, et al. Der p 1 facilitates transepithelial allergen delivery by disruption of tight junctions. J Clin Invest 1999;104:123-133.
30. Kool M, Petrilli V, De Smedt T, Rolaz A, Hammad H, van Nimwegen M, Bergen IM, Castillo R, Lambrecht BN, Tschopp J. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J Immunol 2008;181:3755-3759.
31. Kool M, Soullie T, van Nimwegen M, Willart MA, Muskens F, Jung S, Hoogsteden HC, Hammad H, Lambrecht BN. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 2008;205:869-882.
32. Cates EC, Fattouh R, Wattie J, Inman MD, Goncharova S, Coyle AJ, Gutierrez-Ramos JC, Jordana M. Intranasal exposure of mice to house dust mite elicits allergic airway inflammation via a GM-CSF-mediated mechanism. J Immunol 2004;173:6384-6392. (Pubitemid 39487798)
33. Flood-Page P, Menzies-Gow A, Phipps S, Ying S, Wangoo A, Ludwig MS, Barnes N, Robinson D, Kay AB. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest 2003;112:1029-1036.
34. Chakir J, Loubaki L, Laviolette M, Milot J, Biardel S, Jayaram L, Pizzichini M, Pizzichini E, Hargreave FE, Nair P, et al. Monitoring sputum eosinophils on mucosal inflammation and remodelling: a pilot study. Eur Respir J 2010;35:48-53.
35. Walsh ER, Sahu N, Kearley J, Benjamin E, Kang BH, Humbles A, August A. Strain-specific requirement for eosinophils in the recruitment of T cells to the lung during the development of allergic asthma. J Exp Med 2008;205:1285-1292.
36. Fulkerson PC, Fischetti CA, McBride ML, Hassman LM, Hogan SP, Rothenberg ME. A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc Natl Acad Sci USA 2006;103:16418-16423.
37. Foster PS, Hogan SP, Ramsay AJ, Matthaei KI, Young IG. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J Exp Med 1996;183:195-201.
38. Fattouh R, Jordana M. TGF-beta, eosinophils and IL-13 in allergic airway remodeling: a critical appraisal with therapeutic considerations. Inflamm Allergy Drug Targets 2008;7:224-236.
39. Flood-Page PT, Menzies-Gow AN, Kay AB, Robinson DS. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am J Respir Crit Care Med 2003;167:199-204.
40. Haldar P, Brightling CE, Hargadon B, Gupta S, Monteiro W, Sousa A, Marshall RP, Bradding P, Green RH, Wardlaw AJ, et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med 2009;360:973-984.
41. Kips JC, O'Connor BJ, Langley SJ, Woodcock A, Kerstjens HA, Postma DS, Danzig M, Cuss F, Pauwels RA. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am J Respir Crit Care Med 2003;167:1655-1659.
42. Leckie MJ, ten Brinke A, Khan J, Diamant Z, O'Connor BJ, Walls CM, Mathur AK, Cowley HC, Chung KF, Djukanovic R, et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet 2000;356:2144-2148.
43. Nair P, PizzichiniMM, Kjarsgaard M, InmanMD, EfthimiadisA, Pizzichini E, Hargreave FE, O'Byrne PM. Mepolizumab for prednisonedependent asthma with sputum eosinophilia. N Engl J Med 2009;360:985-993.
44. Anderson GP. Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 2008;372:1107-1119.
45. Borish, L., and J. A. Culp. Asthma: a syndrome composed of heterogeneous diseases. Ann Allergy Asthma Immunol 2008;101:1-8; quiz 8-11, 50.