Innate immunity is a key factor for the resolution of inflammation in asthma

European Respiratory Review

Volumn 24, Issue 135, 2015, Pages 141-153

  Barnig, Cindy ^a   Levy, Bruce D ^b  

^a UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTEROID DERIVATIVE; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; LIPOXIN A; NATURAL PRODUCTS AND THEIR SYNTHETIC DERIVATIVES; POLYUNSATURATED FATTY ACID; PROTECTIN D1; RESOLVIN D1; RESOLVIN E1; RESOLVIN E3; UNCLASSIFIED DRUG; LIPOXIN;

ARTICLE; ASTHMA; CORTICOSTEROID THERAPY; EOSINOPHIL; HUMAN; INNATE IMMUNITY; INNATE LYMPHOID CELL; LYMPHOCYTE; NATURAL KILLER CELL; NONHUMAN; RESPIRATORY TRACT INFLAMMATION; IMMUNOLOGY; INFLAMMATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

ASTHMA; EOSINOPHILS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; KILLER CELLS, NATURAL; LIPOXINS;

EID: 84923919566     PISSN: 09059180     EISSN: 16000617     Source Type: Journal    
DOI: 10.1183/09059180.00012514     Document Type: Article

References (131)

1. Djukanović R, Roche WR, Wilson JW, et al. Mucosal inflammation in asthma. Am Rev Respir Dis 1990; 142: 434–457.
2. Lloyd CM, Hessel EM. Functions of T cells in asthma: more than just TH2 cells. Nature Rev Immunol 2010; 10: 838–848.
3. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med 2012; 18: 673–683.
4. Deckers J, Branco Madeira F, Hammad H. Innate immune cells in asthma. Trends Immunol 2013; 34: 540–547.
5. Busse WW, Lemanske RF Jr. Asthma. N Engl J Med 2001; 344: 350–362.
6. Gilroy DW, Lawrence T, Perretti M, et al. Inflammatory resolution: new opportunities for drug discovery. Nature Rev Drug Discov 2004; 3: 401–416.
7. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Rev Immunol 2008; 8: 349–361.
8. Levy BD, Serhan CN. Resolution of acute inflammation in the lung. Annu Rev Physiol 2014; 76: 467–492.
9. Lawrence T, Willoughby DA, Gilroy DW. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nature Rev Immunol 2002; 2: 787–795.
10. Larsen GL, Henson PM. Mediators of inflammation. Annu Rev Immunol 1983; 1: 335–359.
11. Nathan C, Ding A. Nonresolving inflammation. Cell 2010; 140: 871–882.
12. Serhan CN, Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol 2005; 6: 1191–1197.
13. Henson PM. Dampening inflammation. Nat Immunol 2005; 6: 1179–1181.
14. Savill J. Apoptosis. Phagocytic docking without shocking. Nature 1998; 392: 442–443.
15. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature 2013; 496: 445–455.
16. Fadok VA, Bratton DL, Konowal A, et al. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J Clin Invest 1998; 101: 890–898.
17. Freire-de-Lima CG, Xiao YQ, Gardai SJ, et al. Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J Biol Chem 2006; 281: 38376–38384.
18. Serhan CN. Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol 2007; 25: 101–137.
19. Planaguma A, Levy BD. Uncontrolled airway inflammation in lung disease represents a defect in counter-regulatory signaling. Future Lipidol 2008; 3: 697–704.
20. Serhan CN, Clish CB, Brannon J, et al. Novel functional sets of lipid-derived mediators with anti-inflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med 2000; 192: 1197–1204.
21. Serhan CN, Hong S, Gronert K, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 2002; 196: 1025–1037.
22. Serhan CN, Brain SD, Buckley CD, et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J 2007; 21: 325–332.
23. Levy BD, Clish CB, Schmidt B, et al. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2001; 2: 612–619.
24. Soyombo O, Spur BW, Lee TH. Effects of lipoxin A4 on chemotaxis and degranulation of human eosinophils stimulated by platelet-activating factor and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Allergy 1994; 49: 230–234.
25. Bandeira-Melo C, Serra MF, Diaz BL, et al. Cyclooxygenase-2-derived prostaglandin E2 and lipoxin A4 accelerate resolution of allergic edema in Angiostrongylus costaricensis-infected rats: relationship with concurrent eosinophilia. J Immunol 2000; 164: 1029–1036.
26. Serhan CN, Maddox JF, Petasis NA, et al. Design of lipoxin A4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry 1995; 34: 14609–14615.
27. Colgan SP, Serhan CN, Parkos CA, et al. Lipoxin A4 modulates transmigration of human neutrophils across intestinal epithelial monolayers. J Clin Invest 1993; 92: 75–82.
28. Papayianni A, Serhan CN, Brady HR. Lipoxin A4 and B4 inhibit leukotriene-stimulated interactions of human neutrophils and endothelial cells. J Immunol 1996; 156: 2264–2272.
29. Levy BD, Fokin VV, Clark JM, et al. Polyisoprenyl phosphate (PIPP) signaling regulates phospholipase D activity: a ‘stop’ signaling switch for aspirin-triggered lipoxin A4. FASEB J 1999; 13: 903–911.
30. Lee TH, Horton CE, Kyan-Aung U, et al. Lipoxin A4 and lipoxin B4 inhibit chemotactic responses of human neutrophils stimulated by leukotriene B4 and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Clin Sci 1989; 77: 195–203.
31. Barnig C, Cernadas M, Dutile S, et al. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci Transl Med 2013; 5: 174ra126.
32. Ramstedt U, Serhan CN, Nicolaou KC, et al. Lipoxin A-induced inhibition of human natural killer cell cytotoxicity: studies on stereospecificity of inhibition and mode of action. J Immunol 1987; 138: 266–270.
33. Bonnans C, Vachier I, Chavis C, et al. Lipoxins are potential endogenous antiinflammatory mediators in asthma. Am J Respir Crit Care Med 2002; 165: 1531–1535.
34. Maddox JF, Serhan CN. Lipoxin A4 and B4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. J Exp Med 1996; 183: 137–146.
35. József L, Zouki C, Petasis NA, et al. Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit peroxynitrite formation, NF-κB and AP-1 activation, and IL-8 gene expression in human leukocytes. Proc Natl Acad Sci USA 2002; 99: 13266–13271.
36. Godson C, Mitchell S, Harvey K, et al. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol 2000; 164: 1663–1667.
37. Mitchell S, Thomas G, Harvey K, et al. Lipoxins, aspirin-triggered epi-lipoxins, lipoxin stable analogues, and the resolution of inflammation: stimulation of macrophage phagocytosis of apoptotic neutrophils in vivo. J Am Soc Nephrol 2002; 13: 2497–2507.
38. Aliberti J, Hieny S, Reis e Sousa C, et al. Lipoxin-mediated inhibition of IL-12 production by DCs: a mechanism for regulation of microbial immunity. Nat Immunol 2002; 3: 76–82.
39. Bonnans C, Fukunaga K, Levy MA, et al. Lipoxin A4 regulates bronchial epithelial cell responses to acid injury. Am J Pathol 2006; 168: 1064–1072.
40. Bonnans C, Mainprice B, Chanez P, et al. Lipoxin A4 stimulates a cytosolic Ca2+ increase in human bronchial epithelium. J Biol Chem 2003; 278: 10879–10884.
41. Brezinski ME, Gimbrone MA Jr, Nicolaou KC, et al. Lipoxins stimulate prostacyclin generation by human endothelial cells. FEBS Lett 1989; 245: 167–172.
42. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, et al. Aspirin-triggered lipoxin A4 blocks reactive oxygen species generation in endothelial cells: a novel antioxidative mechanism. Thromb Haemost 2007; 97: 88–98.
43. Cezar-de-Mello PF, Nascimento-Silva V, Villela CG, et al. Aspirin-triggered lipoxin A4 inhibition of VEGF-induced endothelial cell migration involves actin polymerization and focal adhesion assembly. Oncogene 2006; 25: 122–129.
44. Sodin-Semrl S, Taddeo B, Tseng D, et al. Lipoxin A4 inhibits IL-1 β-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. J Immunol 2000; 164: 2660–2666.
45. Wu SH, Wu XH, Lu C, et al. Lipoxin A4 inhibits proliferation of human lung fibroblasts induced by connective tissue growth factor. Am J Respir Cell Mol Biol 2006; 34: 65–72.
46. Parameswaran K, Radford K, Fanat A, et al. Modulation of human airway smooth muscle migration by lipid mediators and Th-2 cytokines. Am J Respir Cell Mol Biol 2007; 37: 240–247.
47. Campbell EL, Louis NA, Tomassetti SE, et al. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J 2007; 21: 3162–3170.
48. Hasturk H, Kantarci A, Ohira T, et al. RvE1 protects from local inflammation and osteoclast-mediated bone destruction in periodontitis. FASEB J 2006; 20: 401–403.
49. Schwab JM, Chiang N, Arita M, et al. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007; 447: 869–874.
50. Arita M, Bianchini F, Aliberti J, et al. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med 2005; 201: 713–722.
51. Arita M, Yoshida M, Hong S, et al. 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 USA 2005; 102: 7671–7676.
52. Isobe Y, Arita M, Matsueda S, et al. Identification and structure determination of novel anti-inflammatory mediator resolvin E3, 17,18-dihydroxyeicosapentaenoic acid. J Biol Chem 2012; 287: 10525–10534.
53. Sun YP, Oh SF, Uddin J, et al. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 2007; 282: 9323–9334.
54. Rogerio AP, Haworth O, Croze R, et al. Resolvin D1 and aspirin-triggered resolvin D1 promote resolution of allergic airways responses. J Immunol 2012; 189: 1983–1991.
55. Duffield JS, Hong S, Vaidya VS, et al. Resolvin D series and protectin D1 mitigate acute kidney injury. J Immunol 2006; 177: 5902–5911.
56. Ariel A, Li PL, Wang W, et al. The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering. J Biol Chem 2005; 280: 43079–43086.
57. Bannenberg GL, Chiang N, Ariel A, et al. Molecular circuits of resolution: formation and actions of resolvins and protectins. J Immunol 2005; 174: 4345–4355.
58. Ariel A, Fredman G, Sun YP, et al. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat Immunol 2006; 7: 1209–1216.
59. Serhan CN, Hamberg M, Samuelsson B. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc Natl Acad Sci USA 1984; 81: 5335–5339.
60. Haworth O, Cernadas M, Yang R, et al. Resolvin E1 regulates interleukin 23, interferon-γ and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat Immunol 2008; 9: 873–879.
61. Hunter JA, Finkbeiner WE, Nadel JA, et al. Predominant generation of 15-lipoxygenase metabolites of arachidonic acid by epithelial cells from human trachea. Proc Natl Acad Sci USA 1985; 82: 4633–4637.
62. Levy BD, Romano M, Chapman HA, et al. Human alveolar macrophages have 15-lipoxygenase and generate 15 (S)-hydroxy-5,8,11-cis-13-trans-eicosatetraenoic acid and lipoxins. J Clin Invest 1993; 92: 1572–1579.
63. Serhan CN, Hirsch U, Palmblad J, et al. Formation of lipoxin A by granulocytes from eosinophilic donors. FEBS Lett 1987; 217: 242–246.
64. Shannon VR, Chanez P, Bousquet J, et al. Histochemical evidence for induction of arachidonate 15-lipoxygenase in airway disease. Am Rev Respir Dis 1993; 147: 1024–1028.
65. Serhan CN. Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 2005; 73: 141–162.
66. Clària J, Serhan CN. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc Natl Acad Sci USA 1995; 92: 9475–9479.
67. Chiang N, Serhan CN, Dahlen SE, et al. The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo. Pharmacol Rev 2006; 58: 463–487.
68. Levy BD, De Sanctis GT, Devchand PR, et al. Multi-pronged inhibition of airway hyper-responsiveness and inflammation by lipoxin A4. Nat Med 2002; 8: 1018–1023.
69. Schaldach CM, Riby J, Bjeldanes LF. Lipoxin A4: a new class of ligand for the Ah receptor. Biochemistry 1999; 38: 7594–7600.
70. Schwartz J, Weiss ST. The relationship of dietary fish intake to level of pulmonary function in the first National Health and Nutrition Survey (NHANES I). Eur Respir J 1994; 7: 1821–1824.
71. Bannenberg G, Serhan CN. Specialized pro-resolving lipid mediators in the inflammatory response: an update. Biochim Biophys Acta 2010; 1801: 1260–1273.
72. Serhan CN. Pro-resolving lipid mediators are leads for resolution physiology. Nature 2014; 510: 92–101.
73. Cash JL, Hart R, Russ A, et al. Synthetic chemerin-derived peptides suppress inflammation through ChemR23. J Exp Med 2008; 205: 767–775.
74. Samson M, Edinger AL, Stordeur P, et al. ChemR23, a putative chemoattractant receptor, is expressed in monocyte-derived dendritic cells and macrophages and is a coreceptor for SIV and some primary HIV-1 strains. Eur J Immunol 1998; 28: 1689–1700.
75. Wittamer V, Franssen JD, Vulcano M, et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J Exp Med 2003; 198: 977–985.
76. Levy BD, Lukacs NW, Berlin AA, et al. Lipoxin A4 stable analogs reduce allergic airway responses via mechanisms distinct from CysLT1 receptor antagonism. FASEB J 2007; 21: 3877–3884.
77. Levy BD, Kohli P, Gotlinger K, et al. Protectin D1 is generated in asthma and dampens airway inflammation and hyperresponsiveness. J Immunol 2007; 178: 496–502.
78. Lee TH, Crea AE, Gant V, et al. Identification of lipoxin A4 and its relationship to the sulfidopeptide leukotrienes C4, D4, and E4 in the bronchoalveolar lavage fluids obtained from patients with selected pulmonary diseases. Am Rev Respir Dis 1990; 141: 1453–1458.
79. Planagumà A, Kazani S, Marigowda G, et al. Airway lipoxin A4 generation and lipoxin A4 receptor expression are decreased in severe asthma. Am J Respir Crit Care Med 2008; 178: 574–582.
80. Vachier I, Bonnans C, Chavis C, et al. Severe asthma is associated with a loss of LX4, an endogenous anti-inflammatory compound. J Allergy Clin Immunol 2005; 115: 55–60.
81. Christie PE, Spur BW, Lee TH. The effects of lipoxin A4 on airway responses in asthmatic subjects. Am Rev Respir Dis 1992; 145: 1281–1284.
82. Levy BD, Bonnans C, Silverman ES, et al. Diminished lipoxin biosynthesis in severe asthma. Am J Respir Crit Care Med 2005; 172: 824–830.
83. Sanak M, Levy BD, Clish CB, et al. Aspirin-tolerant asthmatics generate more lipoxins than aspirin-intolerant asthmatics. Eur Respir J 2000; 16: 44–49.
84. Yamaguchi H, Higashi N, Mita H, et al. Urinary concentrations of 15-epimer of lipoxin A4 are lower in patients with aspirin-intolerant compared with aspirin-tolerant asthma. Clin Exp Allergy 2011; 41: 1711–1718.
85. Kupczyk M, Antczak A, Kuprys-Lipinska I, et al. Lipoxin A4 generation is decreased in aspirin-sensitive patients in lysine-aspirin nasal challenge in vivo model. Allergy 2009; 64: 1746–1752.
86. Celik GE, Erkekol FO, Misirligil Z, et al. Lipoxin A4 levels in asthma: relation with disease severity and aspirin sensitivity. Clin Exp Allergy 2007; 37: 1494–1501.
87. Tahan F, Saraymen R, Gumus H. The role of lipoxin A4 in exercise-induced bronchoconstriction in asthma. J Asthma 2008; 45: 161–164.
88. Bhavsar PK, Levy BD, Hew MJ, et al. Corticosteroid suppression of lipoxin A4 and leukotriene B4 from alveolar macrophages in severe asthma. Respir Res 2010; 11: 71.
89. Wu SH, Yin PL, Zhang YM, et al. Reversed changes of lipoxin A4 and leukotrienes in children with asthma in different severity degree. Pediatr Pulmonol 2010; 45: 333–340.
90. Hasan RA, O’Brien E, Mancuso P. Lipoxin A4 and 8-isoprostane in the exhaled breath condensate of children hospitalized for status asthmaticus. Pediatr Crit Care Med 2012; 13: 141–145.
91. Kazani S, Planaguma A, Ono E, et al. Exhaled breath condensate eicosanoid levels associate with asthma and its severity. J Allergy Clin Immunol 2013; 132: 547–553.
92. Fritscher LG, Post M, Rodrigues MT, et al. Profile of eicosanoids in breath condensate in asthma and COPD. J Breath Res 2012; 6: 026001.
93. Eke Gungor H, Tahan F, Gokahmetoglu S, et al. Decreased levels of lipoxin A4 and annexin A1 in wheezy infants. Int Arch Allergy Immunol 2014; 163: 193–197.
94. Miyata J, Fukunaga K, Iwamoto R, et al. Dysregulated synthesis of protectin D1 in eosinophils from patients with severe asthma. J Allergy Clin Immunol 2013; 131: 353–360.
95. Bilal S, Haworth O, Wu L, et al. Fat-1 transgenic mice with elevated omega-3 fatty acids are protected from allergic airway responses. Biochim Biophys Acta 2011; 1812: 1164–1169.
96. Aoki H, Hisada T, Ishizuka T, et al. Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem Biophys Res Commun 2008; 367: 509–515.
97. Haworth O, Cernadas M, Levy BD. NK cells are effectors for resolvin E1 in the timely resolution of allergic airway inflammation. J Immunol 2011; 186: 6129–6135.
98. Diefenbach A, Colonna M, Koyasu S. Development, differentiation, and diversity of innate lymphoid cells. Immunity 2014; 41: 354–365.
99. Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011; 331: 44–49.
100. Karimi K, Forsythe P. Natural killer cells in asthma. Front Immunol 2013; 4: 159.
101. Korsgren M, Persson CG, Sundler F, et al. Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J Exp Med 1999; 189: 553–562.
102. Ple C, Barrier M, Amniai L, et al. Natural killer cells accumulate in lung-draining lymph nodes and regulate airway eosinophilia in a murine model of asthma. Scand J immunol 2010; 72: 118–127.
103. Thorén FB, Riise RE, Ousbäck J, et al. Human NK cells induce neutrophil apoptosis via an NKp46- and Fas-dependent mechanism. J Immunol 2012; 188: 1668–1674.
104. Awad A, Yassine H, Barrier M, et al. Natural killer cells induce eosinophil activation and apoptosis. PLoS One 2014; 9: e94492.
105. Woolley KL, Gibson PG, Carty K, et al. Eosinophil apoptosis and the resolution of airway inflammation in asthma. Am J Respir Crit Care Med 1996; 154: 237–243.
106. Ramstedt U, Ng J, Wigzell H, et al. Action of novel eicosanoids lipoxin A and B on human natural killer cell cytotoxicity: effects on intracellular cAMP and target cell binding. J Immunol 1985; 135: 3434–3438.
107. Parolini S, Santoro A, Marcenaro E, et al. The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood 2007; 109: 3625–3632.
108. Mjösberg JM, Trifari S, Crellin NK, et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol 2011; 12: 1055–1062.
109. Barlow JL, Bellosi A, Hardman CS, et al. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol 2012; 129: 191–198.
110. Halim TY, Krauss RH, Sun AC, et al. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 2012; 36: 451–463.
111. Liang HE, Reinhardt RL, Bando JK, et al. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol 2012; 13: 58–66.
112. Chang YJ, Kim HY, Albacker LA, et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 2011; 12: 631–638.
113. Klein Wolterink RG, Kleinjan A, van Nimwegen M, et al. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol 2012; 42: 1106–1116.
114. Kim HY, Chang YJ, Subramanian S, et al. Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity. J Allergy Clin Immunol 2012; 129: 216–227.
115. Monticelli LA, Sonnenberg GF, Abt MC, et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 2011; 12: 1045–1054.
116. Li J, Razumilava N, Gores GJ, et al. Biliary repair and carcinogenesis are mediated by IL-33-dependent cholangiocyte proliferation. J Clin Invest 2014; 124: 3241–3251.
117. Fulkerson PC, Rothenberg ME. Targeting eosinophils in allergy, inflammation and beyond. Nature Rev Drug Discov 2013; 12: 117–129.
118. Rothenberg ME, Hogan SP. The eosinophil. Annu Rev Immunol 2006; 24: 147–174.
119. Fattouh R, Al-Garawi A, Fattouh M, et al. Eosinophils are dispensable for allergic remodeling and immunity in a model of house dust mite-induced airway disease. Am J Respir Crit Care Med 2011; 183: 179–188.
120. Leckie MJ. Anti-interleukin-5 monoclonal antibodies: preclinical and clinical evidence in asthma models. Am J Respir Med 2003; 2: 245–259.
121. Flood-Page P, Swenson C, Faiferman I, et al. A study to evaluate safety and efficacy of mepolizumab in patients with moderate persistent asthma. Am J Respir Crit Care Med 2007; 176: 1062–1071.
122. Yamada T, Tani Y, Nakanishi H, et al. Eosinophils promote resolution of acute peritonitis by producing proresolving mediators in mice. FASEB J 2011; 25: 561–568.
123. Tani Y, Isobe Y, Imoto Y, et al. Eosinophils control the resolution of inflammation and draining lymph node hypertrophy through the proresolving mediators and CXCL13 pathway in mice. FASEB J 2014 [In press DOI: 10.1096/fj.14-251132].
124. Takeda K, Shiraishi Y, Ashino S, et al. Eosinophils contribute to the resolution of lung-allergic responses following repeated allergen challenge. J Allergy Clin Immunol 2014 [In press DOI: 10.1016/j.jaci.2014.08.014].
125. Stolarski B, Kurowska-Stolarska M, Kewin P, et al. IL-33 exacerbates eosinophil-mediated airway inflammation. J Immunol 2010; 185: 3472–3480.
126. Kurowska-Stolarska M, Stolarski B, Kewin P, et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol 2009; 183: 6469–6477.
127. Wu D, Molofsky AB, Liang HE, et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011; 332: 243–247.
128. Qiu Y, Nguyen KD, Odegaard JI, et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 2014; 157: 1292–1308.
129. Pelaia G, Vatrella A, Maselli R. The potential of biologics for the treatment of asthma. Nature Rev Drug Discov 2012; 11: 958–972.
130. Chung KF, Wenzel SE, Brozek JL, et al. International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma. Eur Respir J 2014; 43: 343–373.
131. Wu SH, Chen XQ, Liu B, et al. Efficacy and safety of 15(R/S)-methyl-lipoxin A4 in topical treatment of infantile eczema. Br J Dermatol 2013; 168: 172–178.