Resolvin D1 and resolvin E1 promote the resolution of allergic airway inflammation via shared and distinct molecular counter-regulatory pathways

Frontiers in Immunology

Volumn 3, Issue DEC, 2012, Pages

  Levy, Bruce D ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Asthma; Inflammation; Lung; Resolution; Resolvins

Indexed keywords

EID: 84874309361     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00390     Document Type: Article

References (98)

1. Alcorn, J. F., Crowe, C. R., and Kolls, J. K. (2010). TH17 cells in asthma, and COPD. Annu. Rev. Physiol. 72, 495-516.
2. Al-Ramli, W., Prefontaine, D., Chouiali, F., Martin, J. G., Olivenstein, R., Lemière, C., et al. (2009). TH17-associated cytokines IL-17A and IL-17F in severe asthma. J. Allergy Clin. Immunol. 123, 1185-1187.
3. Aoki, H., Hisada, T., Ishizuka, T., Utsugi, M., Kawata, T., Shimizu, Y., et al. (2008). Resolvin E1 dampens airway inflammation,andhyperresponsive-ness in a murine model of asthma. Biochem. Biophys. Res. Commun. 367, 509-515.
4. Ariel, A., Chiang, N., Arita, M., Peta-sis, N. A., and Serhan, C. N. (2003). Aspirin-triggered lipoxin A4, and B4 analogs block extracellular signal-regulated kinase-dependent TNF-alpha secretion from human T cells. J. Immunol. 170, 6266-6272.
5. Arita, M., Bianchini, F., Aliberti, J., Sher, A., Chiang, N., Hong, S., et al. (2005a). Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med. 201, 713-722.
6. Arita, M., Yoshida, M., Hong, S., Tjonahen, E., Glickman, J. N., Petasis, N. A., et al. (2005b). Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc. Natl. Acad. Sci. U.S.A. 102, 7671-7676.
7. Arita, M., Ohira, T., Sun, Y. P., Elan-govan, S., Chiang, N., and Ser-han, C. N. (2007). Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1, and ChemR23 to regulate inflammation. J. Immunol. 178, 3912-3917.
8. Barczyk, A., Pierzchala, W., and Sozan-ska, E. (2003). Interleukin-17 in sputum correlates with airway hyper-responsiveness to methacholine. Respir. Med. 97, 726-733.
9. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., et al. (2006). Reciprocal developmental pathways for the generation of pathogenic effector TH17, and regulatory T cells. Nature 441, 235-238.
10. Bhavsar, P. K., Levy, B. D., Hew, M. J., Pfeffer, M. A., Kazani, S., Israel, E., et al. (2010). Corticosteroid suppression of lipoxin A4, and leukotriene B4 from alveolar macrophages in severe asthma. Respir. Res. 11, 71.
11. Bilal, S., Haworth, O., Wu, L., Weylandt, K. H., Levy, B. D., and Kang, J. X. (2011). Fat-1 transgenic mice with elevated omega-3 fatty acids are protected from allergic airway responses. Biochim. Biophys. Acta 1812, 1164-1169.
12. Bondue, B., Vosters, O., de Nadai, P., Glineur, S., De Henau, O., Luangsay, S., et al. (2011). ChemR23 dampens lung inflammation, and enhances anti-viral immunity in a mouse model of acute viral pneumonia. PLoS Pathog 7:e1002358. doi:10.1371/journal.ppat. 1002358
13. Bonnans, C., Fukunaga, K., Levy, M. A., and Levy, B. D. (2006). Lipoxin A4 regulates bronchial epithelial cell responses to acid injury. Am. J. Pathol. 168, 1064-1072.
14. Bonnans, C., Mainprice, B., Chanez, P., Bousquet, J., and Urbach, V. (2003). Lipoxin A4 stimulates a cytosolic Ca2 increase in human bronchial epithelium. J. Biol. Chem. 278, 10879-10884.
15. Bozinovski, S., Hutchinson, A., Thompson, M., Macgregor, L., Black, J., Giannakis, E., et al. (2008). Serum amyloid a is a biomarker of acute exacerbations of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 177, 269-278.
16. Bozinovski, S., Uddin, M., Vlahos, R., Thompson, M., McQualter, J. L., Merritt, A. S., et al. (2012). Serum amyloid A opposes lipoxin A4 to mediate glucocorticoid refractory lung inflammation in chronic obstructive pulmonary disease. Proc. Natl. Acad. Sci. U.S.A. 109, 935-940.
17. Busse, W. W., and Lemanske, R. F. Jr. (2001). Asthma.N. Engl. J. Med.344, 350-362.
18. Cash, J. L., Hart, R., Russ, A., Dixon, J. P., Colledge, W. H., Doran, J., et al. (2008). Synthetic chemerin-derived peptides suppress inflammation through ChemR23. J. Exp. Med. 205, 767-775.
19. Celik, G. E., Erkekol, F. O., Misirligil, Z., and Melli, M. (2007).LipoxinA4lev-els in asthma: relation with disease severity, and aspirin sensitivity. Clin. Exp. Allergy 37, 1494-1501.
20. Chan, J. R., Blumenschein, W., Murphy, E., Diveu, C., Wiekowski, M., Abbondanzo, S., et al. (2006). IL-23 stimulates epidermal hyperplasia via TNF, and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J. Exp. Med. 203, 2577-2587.
21. Chen, Y., Thai, P., Zhao, Y. H., Ho, Y. S., DeSouza, M. M., and Wu, R. (2003). Stimulation of airway mucin gene expression by interleukin IL-17 through IL-6paracrine/autocrine loop. J. Biol. Chem. 278, 17036-17043.
22. Cheung, P. F., Wong, C. K., and Lam, C. W. (2008). Molecular Mechanisms of cytokine, and chemokine release from eosinophils activated by IL-17A, IL-17F, and IL-23: implication for Th17 lymphocytes-mediated allergic inflammation. J. Immunol. 180, 5625-5635.
23. Chiang, N., Serhan, C. N., Dahlen, S. E., Drazen, J. M., Hay, D. W., Rovati, G. E., et al. (2006). The lipoxin receptor ALX: potent ligand-specific, and stereoselective actions in vivo. Pharmacol. Rev. 58, 463-487.
24. Chiron, R., Grumbach, Y. Y., Quynh, N. V., Verriere, V., and Urbach, V. (2008). Lipoxin A4, and interleukin-8 levels in cystic fibrosis sputum after antibiotherapy. J. Cyst. Fibros. 7, 463-468.
25. Christie, P. E., Spur, B. W., and Lee, T. H. (1992). The effects of lipoxin A4 on airway responses in asthmatic subjects. Am. Rev. Respir. Dis. 145, 1281-1284.
26. Corry, D. B., and Irvin, C. G. (2006). Promise, and pitfalls in animal-based asthma research: building a better mousetrap. Immunol. Res. 35, 279-294.
27. Demoor, T., Bracke, K. R., Dupont, L. L., Plantinga, M., Bondue, B., Roy, M. O., et al. (2011). The role of ChemR23 in the induction, and resolution of cigarette smoke-induced inflammation. J. Immunol. 186, 5457-5467.
28. Devchand, P. R., Arita, M., Hong, S., Bannenberg, G., Moussignac, R. L., Gronert, K., et al. (2003). Human ALX receptor regulates neutrophil recruitment in transgenic mice: roles in inflammation, and host defense. FASEB J. 17, 652-659.
29. Dufton, N., Hannon, R., Brancaleone, V., Dalli, J., Patel, H. B., Gray, M., et al. (2010). Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses, and experimental inflammation. J. Immunol. 184, 2611-2619.
30. Eickmeier, O., Seki, H., Haworth, O., Hilberath, J. N., Gao, F., Uddin, M.,et al. (2012). Aspirin-triggered resolvin D1 reduces mucosal inflammation, and promotes resolutioninamurine model of acute lung injury. Mucosal Immunol. doi:10.1038/mi.2012.66
31. El Kebir, D., Gjorstrup, P., and Filep, J. G. (2012). Resolvin E1 promotes phagocytosis-induced neu-trophil apoptosis, and accelerates resolution of pulmonary inflammation.Proc. Natl. Acad. Sci. U.S.A. 109, 14983-14988.
32. Fanta, C. H. (2009). Asthma. N. Engl. J. Med. 360, 1002-1014.
33. Fiore, S., Maddox, J. F., Perez, H. D., and Serhan, C. N. (1994). Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor. J. Exp. Med. 180, 253-260.
34. Fiore, S., Ryeom, S. W., Weller, P. F., and Serhan, C. N. (1992). Lipoxin recognition sites. Specific binding of labeled lipoxin A4 with human neutrophils. J. Biol. Chem. 267, 16168-16176.
35. Freedman, S. D., Blanco, P. G., Zaman, M. M., Shea, J. C., Ollero, M., Hopper, I. K., et al. (2004). Association of cystic fibrosis with abnormalities in fatty acid metabolism. N. Engl. J. Med. 350, 560-569.
36. Fritscher, L. G., Post, M., Rodrigues, M. T., Silverman, F., Balter, M., Chapman, K. R., et al. (2012). Profile of eicosanoids in breath condensate in asthma, and COPD. J. Breath Res. 6, 1-5.
37. Godson, C., Mitchell, S., Harvey, K., Petasis, N. A., Hogg, N., and Brady, H. R. (2000). Cutting edge: lipoxins rapidly stimulate non-phlogistic phagocytosis of apop-totic neutrophils by monocyte-derived macrophages. J. Immunol. 164, 1663-1667.
38. Gronert, K., Gewirtz, A., Madara, J. L., and Serhan, C. N. (1998). Identification of a human enterocyte lipoxin A4 receptor that is regulated byinter-leukin IL-13, and interferon gamma, and inhibits tumor necrosis factor alpha-induced IL-8 release. J. Exp. Med. 187, 1285-1294.
39. Hasan, R. A., O'Brien, E., and Man-cuso, P. (2012). Lipoxin A4, and 8-isoprostane in the exhaled breath condensate of children hospitalized for status asthmaticus. Pediatr. Crit. Care Med. 13, 141-145.
40. Haworth, O., Cernadas, M., and Levy, B. D. (2011). NK cells are effectors for resolvin E1 in the timely resolution of allergic airway inflammation. J. Immunol. 186, 6129-6135.
41. Haworth, O., Cernadas, M., Yang, R., Serhan, C. N., and Levy, B. D. (2008). Resolvin E1 regulates interleukin 23, interferon-gamma, and lipoxin A4 to promote the resolution of allergic airway inflammation.Nat. Immunol. 9, 873-879.
42. Hudert, C. A., Weylandt, K. H., Lu, Y., Wang, J., Hong, S., Dignass, A., et al. (2006). Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proc. Natl. Acad. Sci. U.S.A. 103, 11276-11281.
43. Isobe, Y., Arita, M., Matsueda, S., Iwamoto, R., Fujihara, T., Nakanishi, H., et al. (2012). Identification, and structure determination of novel anti-inflammatory mediator resolvin E3, 17,18-dihydroxyeicosapentaenoic acid. J. Biol. Chem. 287, 10525-10534.
44. Karp, C. L., Flick, L. M., Park, K. W., Softic, S., Greer, T. M., Keledjian, R., et al. (2004). Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway. Nat. Immunol. 5, 388-392.
45. Kips, J. C., Anderson, G. P., Fredberg, J. J., Herz, U., Inman, M. D., Jordana, M., et al. (2003). Murine models of asthma. Eur. Respir. J. 22, 374-382.
46. Kowal-Bielecka, O., Kowal, K., Distler, O., Rojewska, J., Bodzenta-Lukaszyk, A., Michel, B. A., et al. (2005). Cyclooxygenase-, and lipoxygenase-derived eicosanoids in bronchoalve-olar lavage fluid from patients with scleroderma lung disease: an imbalance between proinflammatory, and antiinflammatory lipid mediators. Arthritis Rheum. 52, 3783-3791.
47. Krishnamoorthy, S., Recchiuti, A., Chiang, N., Fredman, G., and Ser-han, C. N. (2012). Resolvin D1 receptor stereoselectivity, and regulation of inflammation, and prore-solving microRNAs. Am. J. Pathol. 180, 2018-2027.
48. Krishnamoorthy, S., Recchiuti, A., Chiang, N., Yacoubian, S., Lee, C. H., Yang, R., et al. (2010). Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc. Natl. Acad. Sci. U.S.A. 107, 1660-1665.
49. Lajoie, S., Lewkowich, I. P., Suzuki, Y., Clark, J. R., Sproles, A. A., Dienger, K., et al. (2010). Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat. Immunol. 11, 928-935.
50. Langowski, J.L., Zhang, X., Wu, L., Matt-son, J. D., Chen, T., Smith, K., et al. (2006). IL-23 promotes tumour incidence, and growth. Nature 442, 461-465.
51. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedg-wick, J. D., et al. (2005). IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201, 233-240.
52. Levy, B. D. (2010). "Asthma," in Fundamentals of Inflammation, eds C. N. Serhan, P.A.Ward, and D.W. Gilroy, 1st Edn (New York: Cambridge University Press), 376-84.
53. Levy, B. D., Bonnans, C., Silverman, E. S., Palmer, L. J., Marigowda, G., and Israel, E. (2005). Diminished lipoxin biosynthesis in severe asthma. Am. J. Respir. Crit. Care Med. 172, 824-830.
54. Levy, B. D., De Sanctis, G. T., Devc-hand, P. R., Kim, E., Ackerman, K., Schmidt, B. A., et al. (2002). Multi-pronged inhibition of airway hyper-responsiveness, and inflammation by lipoxin A4. Nat. Med. 8, 1018-1023.
55. Levy, B. D., Kohli, P., Gotlinger, K., Haworth, O., Hong, S., Kazani, S., et al. (2007). Protectin D1 is generated in asthma, and dampens airway inflammation,andhyperresponsive-ness. J. Immunol. 178, 496-502.
56. Luangsay, S., Wittamer, V., Bondue, B., De Henau, O., Rouger, L., Brait, M., et al. (2009). Mouse ChemR23 is expressed in dendritic cell subsets, and macrophages, and mediates an anti-inflammatory activity of chemerin in a lung disease model. J. Immunol. 183, 6489-6499.
57. Maddox, J. F., and Serhan, C. N. (1996). Lipoxin A4, and B4 are potent stimuli for human monocyte migration, and adhesion: selective inactivation by dehydrogenation, and reduction. J. Exp. Med. 183, 137-146.
58. Majno, G. (1996). Cells, Tissues, and Disease: Principles of General Pathology. Cambridge, MA: Blackwell.
59. Mattoscio, D., Evangelista, V., De Cristo-faro, R., Recchiuti, A., Pandolfi, A., Di Silvestre, S., et al. (2010). Cystic fibrosis transmembrane conductance regulator CFTR expression in human platelets: impact on mediators, and mechanisms of the inflammatoryresponse. FASEB J.24, 3970-3980.
60. Molet, S., Hamid, Q., Davoine, F., Nutku, E., Taha, R., Pagé, N., et al. (2001). IL-17 is increased in asthmatic airways, and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108, 430-438.
61. Monnier, J., Lewén, S., O'Hara, E., Huang, K., Tu, H., Butcher, E. C., et al. (2012). Expression, regulation, and function of atypical chemerin receptor CCRL2 on endothelial cells. J. Immunol. 189, 956-967.
62. Morris, T., Stables, M., Colville-Nash, P., Newson, J., Bellingan, G.,de Souza, P. M.,et al. (2010).Dichotomyindura-tion, and severity of acute inflammatory responses in humans arising from differentially expressed prores-olution pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 8842-8847.
63. Norling, L. V., Dalli, J., Flower, R. J., Ser-han, C. N., and Perretti, M. (2012). Resolvin D1 limits PMN recruitment to inflammatory loci: receptor dependent actions. Arterioscler. Thromb. Vasc. Biol. 32, 1970-1978.
64. Oh, S. F., Dona, M., Fredman, G., Krish-namoorthy, S., Irimia, D., and Ser-han, C. N. (2012). Resolvin E2 formation, and impact in inflammation resolution. J. Immunol. 188, 4527-4534.
65. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., et al. (2005). A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141.
66. Parolini, S., Santoro, A., Marcenaro, E., Luini, W., Massardi, L., Facchetti, F., et al. (2007). The role of chemerin in the colocalization of, N. K., and dendritic cell subsets into inflamed tissues. Blood 109, 3625-3632.
67. Perretti, M., Chiang, N., La, M., Fierro, I. M., Marullo, S., Getting, S. J., et al. (2002). Endogenous lipid-, and peptide-derived anti-inflammatory pathways generated with glucocorti-coid, and aspirin treatment activate the lipoxin A4 receptor. Nat. Med. 8, 1296-1302.
68. Pichavant, M., Goya, S., Hamelmann, E., Gelfand, E. W., and Umetsu, D. T. (2007). Animal models of airway sensitization. Curr. Protoc. Immunol. Chapter 15, Unit 15 8.
69. Planaguma, A., Kazani, S., Marigowda, G., Haworth, O., Mariani, T. J., Israel, E., et al. (2008). Airway lipoxin A4 generation, and lipoxin A4 receptor expression are decreased in severe asthma.Am. J. Respir. Crit. Care Med. 178, 574-582.
70. Ramstedt, U., Serhan, C. N., Nicolaou, K. C., Webber, S. E., Wigzell, H., and Samuelsson, B. (1987). Lipoxin A-induced inhibition of human natural killer cell cytotoxicity: studies on stereospecificity of inhibition, and modeofaction.J. Immunol.138, 266-270.
71. Rogerio, A. P., Haworth, O., Croze, R., Oh, S. F., Uddin, M., Carlo, T., et al. (2012). Resolvin d1, and aspirin-triggered resolvin d1 promote resolution of allergic airways responses. J. Immunol. 189, 1983-1991.
72. Sanak, M., Levy, B. D., Clish, C. B., Chiang, N., Gronert, K., Mastalerz, L., et al. (2000). Aspirin-tolerant asthmatics generate more lipoxins than aspirin-intolerant asthmatics. Eur. Respir. J. 16, 44-49.
73. Schnyder-Candrian, S., Togbe, D., Couillin, I., Mercier, I., Brombacher, F., Quesniaux, V., et al. (2006). Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203, 2715-2725.
74. Schwab, J. M., Chiang, N., Arita, M., and Serhan, C. N. (2007). Resolvin E1, and protectin D1 activate inflammation-resolution programmes. Nature 447, 869-874.
75. Seki, H., Fukunaga, K., Arita, M., Arai, H., Nakanishi, H., Taguchi, R., et al. (2010). The anti-inflammatory, and proresolving mediator resolvin E1 protects mice from bacterial pneumonia, and acute lung injury. J. Immunol. 184, 836-843.
76. Serhan, C. N. (2007). Resolution phase of inflammation: novel endogenous anti-inflammatory, and proresolv-ing lipid mediators, and pathways. Annu. Rev. Immunol. 25, 101-137.
77. Serhan, C.N., Chiang, N.,and VanDyke, T. E. (2008). Resolving inflammation: dual anti-inflammatory, and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361.
78. Serhan, C. N., Clish, C. B., Brannon, J., Colgan, S. P., Chiang, N., and Gronert, K. (2000). Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal anti-inflammatory drugs, and transcel-lular processing. J. Exp. Med. 192, 1197-1204.
79. Serhan, C. N., Hong, S., Gronert, K., Colgan, S. P., Devchand, P. R., Mir-ick, G., et al. (2002). Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J. Exp. Med. 196, 1025-1037.
80. Simiele, F., Recchiuti, A., Mattoscio, D., De Luca, A., Cianci, E., Franchi, S., et al. (2011). Transcriptional regulation of the human FPR2/ALX gene: evidence of a heritable genetic variant that impairs promoter activity. FASEB J. 26, 1323-1333.
81. Sodin-Semrl, S., Taddeo, B., Tseng, D., Varga, J., and Fiore, S. (2000). Lipoxin A4 inhibits IL-1 beta-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts, and enhances synthesis of tissue inhibitors of metalloproteinases. J. Immunol. 164, 2660-2666.
82. Stenke, L., Edenius, C., Samuelsson, J., and Lindgren, J. A. (1991). Deficient lipoxin synthesis: a novel platelet dysfunction in myeloproliferative disorders with special reference to blastic crisis of chronic myelogenous leukemia. Blood 78, 2989-2995.
83. Sun, Y. P., Oh, S. F., Uddin, J., Yang, R., Gotlinger, K., Campbell, E., et al. (2007). Resolvin D1, and its aspirin-triggered 17R epimer. Stereochemi-cal assignments, anti-inflammatory properties, and enzymatic inactiva-tion. J. Biol. Chem. 282, 9323-9334.
84. Tahan, F., Saraymen, R., and Gumus, H. (2008). The role of lipoxin A4 in exercise-induced bronchocon-striction in asthma. J. Asthma 45, 161-164.
85. Terawaki, K., Yokomizo, T., Nagase, T., Toda, A., Taniguchi, M., Hashizume, K., et al. (2005). Absence of leukotriene B4 receptor 1 confers resistance to airway hyperre-sponsiveness, and Th2-type immune responses. J. Immunol. 175, 4217-4225.
86. Thornton, E. E., Looney, M. R., Bose, O., Sen, D., Sheppard, D., Locksley, R., et al. (2012). Spatiotemporally separated antigen uptake by alveolar dendritic cells, and airway presentation to T cells in the lung. J. Exp. Med. 209, 1183-1199.
87. Tjonahen, E., Oh, S. F., Siegel-man, J., Elangovan, S., Percarpio, K. B., Hong, S., et al. (2006). Resolvin E2: identification, and anti-inflammatory actions: pivotal role of human 5-lipoxygenase in resolvin E series biosynthesis. Chem. Biol. 13, 1193-1202.
88. Vachier, I., Bonnans, C., Chavis, C., Farce, M., Godard, P., Bousquet, J., et al. (2005). Severe asthma is associated with a loss of LX4, an endogenous anti-inflammatory compound. J. Allergy Clin. Immunol. 115, 55-60.
89. Wang, B., Gong, X., Wan, J. Y., Zhang, L., Zhang, Z., Li, H. Z., et al. (2011). ResolvinD1protectsmice fromLPS-induced acute lung injury. Pulm. Pharmacol. Ther. 24, 434-441.
90. Wong, D. T., Elovic, A., Matossian, K., Nagura, N., McBride, J., Chou, M. Y., et al. (1991). Eosinophils from patients with blood eosinophilia express transforming growth factor beta 1. Blood 78, 2702-2707.
91. Woodruff, P. G., Boushey, H. A., Dolganov, G. M., Barker, C. S., Yang, Y. H., Donnelly, S., et al. (2007). Genome-wide profiling identifies epithelial cell genes associated with asthma, and with treatment response to corticosteroids. Proc. Natl. Acad. Sci. U.S.A. 104, 15858-15863.
92. Wu, S. H., Yin, P. L., Zhang, Y. M., and Tao, H. X. (2010). Reversed changes of lipoxin A4, and leukotrienes in children with asthma in different severity degree. Pediatr. Pulmonol. 45, 333-340.
93. Yago, T., Nanke, Y., Kawamoto, M., Furuya, T., Kobashigawa, T., Kamatani, N., et al. (2007). IL-23 induces human osteoclastogenesis via IL-17 in vitro, and anti-IL-23 antibody attenuates collagen-induced arthritis in rats. Arthritis Res. Ther. 9, R96.
94. Yamaguchi, H., Higashi, N., Mita, H., Ono, E., Komase, Y., Nakagawa, T., et al. (2011). Urinary concentrations of 15-epimer of lipoxin A4 are lower in patients with aspirin-intolerant compared with aspirin-tolerant asthma. Clin. Exp. Allergy 41, 1711-1718.
95. Yang, J., Eiserich, J. P., Cross, C. E., Morrissey, B. M., and Hammock, B. D. (2012). Metabolomic profiling of regulatory lipid mediators in sputum from adult cystic fibrosis patients. Free Radic. Biol. Med. 53, 160-171.
96. Yang, L., Cohn, L., Zhang, D. H., Homer, R., Ray, A., and Ray, P. (1998). Essential role of nuclear factor kappaB in the induction of eosinophilia in allergic airway inflammation. J. Exp. Med. 188, 1739-1750.
97. Yen, D., Cheung, J., Scheerens, H., Poulet, F., McClanahan, T., McKen-zie, B., et al. (2006). IL-23 is essential for T cell-mediated colitis, and promotes inflammation via IL-17, and IL-6. J. Clin. Invest. 116, 1310-1316.
98. Zosky, G. R., and Sly, P. D. (2007). Animal models of asthma. Clin. Exp. Allergy 37, 973-988.