Comprehensive attenuation of IL-25-induced airway hyperresponsiveness, inflammation and remodelling by the PI3K inhibitor LY294002

Respirology

Volumn 22, Issue 1, 2017, Pages 78-85

  Huang, Ping ^a   Li, Yan ^a,b   Lv, Ze ^a   Wang, Jingjing ^a   Zhang, Qian ^c   Yao, Xiujuan ^c   Corrigan, Chris J ^d   Huang, Kewu ^b   Wang, Wei ^a   Ying, Sun ^a,d  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

airway inflammation; asthma; interleukin 25; phosphoinositide 3 kinase inhibitors; remodelling

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CHEMOKINE; CYTOKINE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; D17WSU104E PROTEIN, MOUSE; ENZYME INHIBITOR; INTERLEUKIN DERIVATIVE; MORPHOLINE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE;

AIRWAY REMODELING; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CELL INFILTRATION; COLLAGEN DISEASE; CONTROLLED STUDY; EOSINOPHILIA; FEMALE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; LUNG FUNCTION TEST; LUNG LAVAGE; MOUSE; MUCUS SECRETION; MUSCLE HYPERTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; PATHOLOGY; PROCEDURES; TREATMENT OUTCOME;

AIRWAY REMODELING; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CHROMONES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; INTERLEUKINS; MICE; MICE, INBRED BALB C; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; RESPIRATORY FUNCTION TESTS; RESPIRATORY HYPERSENSITIVITY; TREATMENT OUTCOME;

EID: 84983418138     PISSN: 13237799     EISSN: 14401843     Source Type: Journal    
DOI: 10.1111/resp.12880     Document Type: Article

References (38)

1. Masoli M, Fabian D, Holt S, Beasley R Global Initiative for Asthma (GINA) Program. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 2004; 59: 469–78.
2. National Asthma Education and Prevention Program. Expert Panel Report 3 (EPR-3): guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. J. Allergy Clin. Immunol. 2007; 120(Suppl. 5): S94–138.
3. Proceedings of the ATS workshop on refractory asthma: current understanding, recommendations, and unanswered questions. American Thoracic Society. Am. J. Respir. Crit. Care Med. 2000; 162: 2341–51.
4. Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, Menon S, Seymour B, Jackson C, Kung TT et al. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J. Immunol. 2002; 169: 443–53.
5. Yao XJ, Huang KW, Li Y, Zhang Q, Wang JJ, Wang W, Liu J, Lv Z, An YQ, Ding YZ et al. Direct comparison of the dynamics of IL-25- and ‘allergen’-induced airways inflammation, remodelling and hypersensitivity in a murine asthma model. Clin. Exp. Allergy 2014; 44: 765–77.
6. Takeda M, Ito W, Tanabe M, Ueki S, Kihara J, Kato H, Tanigai T, Kayaba H, Sasaki T, Chihara J. The pathophysiological roles of PI3Ks and therapeutic potential of selective inhibitors in allergic inflammation. Int. Arch. Allergy Immunol. 2010; 152(Suppl. 1): 90–5.
7. Duan W, Aguinaldo Datiles AM, Leung BP, Vlahos CJ, Wong WS. An anti-inflammatory role for a phosphoinositide 3-kinase inhibitor LY294002 in a mouse asthma model. Int. Immunopharmacol. 2005; 5: 495–502.
8. Kwak YG, Song CH, Yi HK, Hwang PH, Kim JS, Lee KS, Lee YC. Involvement of PTEN in airway hyperresponsiveness and inflammation in bronchial asthma. J. Clin. Invest. 2003; 111: 1083–92.
9. Corrigan CJ, Wang W, Meng Q, Fang C, Wu H, Reay V, Lv Z, Fan Y, An Y, Wang YH et al. T-helper cell type 2 (Th2) memory T cell-potentiating cytokine IL-25 has the potential to promote angiogenesis in asthma. Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 1579–84.
10. Wang W, Fan YQ, Lv Z, Yao XJ, Wang W, Huang KW, Meng Q, Fang CL, Lee TH, Corrigan CJ et al. Interleukin-25 promotes basic fibroblast growth factor expression by human endothelial cells through interaction with IL-17RB, but not IL-17RA. Clin. Exp. Allergy 2012; 42: 1604–14.
11. Jonasson S, Hedenstierna G, Hedenstrom H, Hjoberg J. Comparisons of effects of intravenous and inhaled methacholine on airway physiology in a murine asthma model. Respir. Physiol. Neurobiol. 2009; 165: 229–36.
12. Riesenfeld E, Allen GB, Bates JH, Poynter ME, Wu M, Aimiand S, Lundblad LK. The temporal evolution of airways hyperresponsiveness and inflammation. J. Allergy Ther. 2012; 1: 1–7.
13. Rickel EA, Siegel LA, Yoon BR, Rottman JB, Kugler DG, Swart DA, Anders PM, Tocker JE, Comeau MR, Budelsky AL. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J. Immunol. 2008; 181: 4299–310.
14. Gregory LG, Jones CP, Walker SA, Sawant D, Gowers KH, Campbell GA, McKenzie AN, Lloyd CM. IL-25 drives remodelling in allergic airways disease induced by house dust mite. Thorax 2013; 68: 82–90.
15. Angkasekwinai P, Park H, Wang YH, Wang YH, Chang SH, Corry DB, Liu YJ, Zhu Z, Dong C. Interleukin 25 promotes the initiation of proallergic type 2 responses. J. Exp. Med. 2007; 204: 1509–17.
16. Ballantyne SJ, Barlow JL, Jolin HE, Nath P, Williams AS, Chung KF, Sturton G, Wong SH, McKenzie AN. Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. J. Allergy Clin. Immunol. 2007; 120: 1324–31.
17. Pinho V, Souza DG, Barsante MM, Hamer FP, DeFreitas MS, Rossi AG, Teixeira MM. Phosphoinositide-3 kinases critically regulate the recruitment and survival of eosinophils in vivo: importance for the resolution of allergic inflammation. J. Leukoc. Biol. 2005; 77: 800–10.
18. Salogni L, Musso T, Bosisio D, Mirolo M, Jala VR, Haribabu B, Locati M, Sozzani S. Activin A induces dendritic cell migration through the polarized release of CXC chemokine ligands 12 and 14. Blood 2009; 113: 5848–56.
19. Del PA, Vermi W, Dander E, Otero K, Barberis L, Luini W, Bernasconi S, Sironi M, Santoro A, Garlanda C et al. Defective dendritic cell migration and activation of adaptive immunity in PI3Kgamma-deficient mice. EMBO J. 2004; 23: 3505–15.
20. Ali K, Bilancio A, Thomas M, Pearce W, Gilfillan AM, Tkaczyk C, Kuehn N, Gray A, Giddings J, Peskett E et al. Essential role for the p110delta phosphoinositide 3-kinase in the allergic response. Nature 2004; 431: 1007–11.
21. Ali K, Camps M, Pearce WP, Ji H, Ruckle T, Kuehn N, Pasquali C, Chabert C, Rommel C, Vanhaesebroeck B. Isoform-specific functions of phosphoinositide 3-kinases: p110 delta but not p110 gamma promotes optimal allergic responses in vivo. J. Immunol. 2008; 180: 2538–44.
22. Endo D, Gon Y, Nunomura S, Yamashita K, Hashimoto S, Ra C. PI3Kγ differentially regulates Fc ε RI-mediated degranulation and migration of mast cells by and toward antigen. Int. Arch. Allergy Immunol. 2009; 149: 66–72.
23. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, Wakeham A, Itie A, Bouchard D, Kozieradzki I et al. Function of PI3K γ in thymocyte development, T cell activation, and neutrophil migration. Science 2000; 287: 1040–6.
24. Nashed BF, Zhang T, Al-Alwan M, Srinivasan G, Halayko AJ, Okkenhaug K, Vanhaesebroeck B, Hayglass KT, Marshall AJ. Role of the phosphoinositide 3-kinase p110delta in generation of type 2 cytokine responses and allergic airway inflammation. Eur. J. Immunol. 2007; 37: 416–24.
25. Takeda M, Ito W, Tanabe M, Ueki S, Kato H, Kihara J, Tanigai T, Chiba T, Yamaguchi K, Kayaba H et al. Allergic airway hyperresponsiveness, inflammation, and remodeling do not develop in phosphoinositide 3-kinase gamma-deficient mice. J. Allergy Clin. Immunol. 2009; 123: 805–12.
26. Lim DH, Cho JY, Song DJ, Lee SY, Miller M, Broide DH. PI3K gamma-deficient mice have reduced levels of allergen-induced eosinophilic inflammation and airway remodeling. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009; 296: L210–9.
27. Thomas M, Edwards MJ, Sawicka E, Duggan N, Hirsch E, Wymann MP, Owen C, Trifilieff A, Walker C, Westwick J et al. Essential role of phosphoinositide 3-kinase gamma in eosinophil chemotaxis within acute pulmonary inflammation. Immunology 2009; 126: 413–22.
28. Lee KS, Lee HK, Hayflick JS, Lee YC, Puri KD. Inhibition of phosphoinositide 3-kinase delta attenuates allergic airway inflammation and hyperresponsiveness in murine asthma model. FASEB J. 2006; 20: 455–65.
29. Doukas J, Eide L, Stebbins K, Racanelli-Layton A, Dellamary L, Martin M, Dneprovskaia E, Noronha G, Soll R, Wrasidlo W et al. Aerosolized phosphoinositide 3-kinase gamma/delta inhibitor TG100-115 [3-[2,4-diamino-6-(3-hydroxyphenyl) pteridin-7-yl]phenol] as a therapeutic candidate for asthma and chronic obstructive pulmonary disease. J. Pharmacol. Exp. Ther. 2009; 328: 758–65.
30. Chung KF. Targeting the interleukin pathway in the treatment of asthma. Lancet 2015; 386: 1086–96.
31. Xie S, Sukkar MB, Issa R, Khorasani NM, Chung KF. Mechanisms of induction of airway smooth muscle hyperplasia transforming growth factor-β. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007; 293: 245–53.
32. Gang C, Nasreen K. TGF-β1 increases proliferation of airway smooth muscle cells by phosphorylation of map kinases. Respir. Res. 2006; 7: 2.
33. Elovic A, Wong DT, Weller PF, Matossian K, Galli SJ. Expression of transforming growth factors-alpha and beta1 messenger RNA and product by eosinophils in nasal polyps. J. Allergy Clin. Immunol. 1994; 93: 864–9.
34. Fernandes DJ, Mitchell RW, Lakser O, Dowell M, Stewart AG, Solway J. Do inflammatory mediators influence the contribution of airway smooth muscle contraction to airway hyperresponsiveness in asthma? J. Appl. Physiol. 2003; 95: 844–53.
35. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF, Waterfield MD. Exploring the specificity of the PI3K family inhibitor LY294002. Biochem. J. 2007; 404: 15–21.
36. Arrowsmith CH, Audia JE, Austin C, Baell J, Bennett J, Blagg J, Bountra C, Brennan PE, Brown PJ, Bunnage ME et al. Corrigendum: the promise and peril of chemical probes. Nat. Chem. Biol. 2015; 11: 887.
37. Nakagome K, Dohi M, Okunishi K, Tanaka R, Kouro T, Kano MR, Miyazono K, Miyazaki J, Takatsu K, Yamamoto K. IL-5-induced hypereosinophilia suppresses the antigen-induced immune response via a TGF-β-dependent mechanism. J. Immunol. 2007; 179: 284–94.
38. Vargaftig BB, Singer M. Leukotrienes mediate murine bronchopulmonary, hyperreactivity, inflammation, and part of mucosal metaplasia and tissue injury induced by recombinant murine interleukin-13. Am. J. Respir. Cell Mol. Biol. 2003; 28: 410–9.