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Clinical and Translational Allergy
Published in: Clinical and Translational Allergy 1/2015

Open Access 01-12-2015 | Review

Innate lymphocyte cells in asthma phenotypes

Authors: Leyla Pur Ozyigit, Hideaki Morita, Mubeccel Akdis

Published in: Clinical and Translational Allergy | Issue 1/2015

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Abstract

T helper type 2 (TH2) cells were previously thought to be the main initiating effector cell type in asthma; however, exaggerated TH2 cell activities alone were insufficient to explain all aspects of asthma. Asthma is a heterogeneous syndrome comprising different phenotypes that are characterized by their different clinical features, treatment responses, and inflammation patterns. The most-studied subgroups of asthma include TH2-associated early-onset allergic asthma, late-onset persistent eosinophilic asthma, virus-induced asthma, obesity-related asthma, and neutrophilic asthma. The recent discovery of human innate lymphoid cells capable of rapidly producing large amounts of cytokines upon activation and the mouse data pointing to an essential role for these cells in asthma models have emphasized the important role of the innate immune system in asthma and have provided a new means of better understanding asthma mechanisms and differentiating its phenotypes.
Literature
1.
Annunziato F, Romagnani C, Romagnani S. The 3 major types of innate and adaptive cell-mediated effector immunity. J Allergy and Clinical Immunology. 2014. doi:10.1016/j.jaci.2014.11.001
2.
Mjosberg J, Eidsmo L. Update on innate lymphoid cells in atopic and non-atopic inflammation in the airways and skin. Clin Exp Allergy. 2014;44(8):1033–43. doi:10.1111/cea.12353.PubMedCrossRef
3.
Mebius RE, Rennert P, Weissman IL. Developing lymph nodes collect CD4 + CD3- LTbeta + cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity. 1997;7(4):493–504.PubMedCrossRef
4.
Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol. 2011;12(11):1045–54. doi:10.1031/ni.2131.PubMedCentralPubMedCrossRef
5.
Artis D, Spits H. The biology of innate lymphoid cells. Nature. 2015;517(7534):293–301. doi:10.1038/nature14189.PubMedCrossRef
6.
Klose CS, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell. 2014;157(2):340–56. doi:10.1016/j.cell.2014.03.030.PubMedCrossRef
7.
Daussy C, Faure F, Mayol K, Viel S, Gasteiger G, Charrier E, et al. T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J Exp Med. 2014;211(3):563–77. doi:10.1084/jem.20131560.PubMedCentralPubMedCrossRef
8.
9.
Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley AM, et al. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992;326(5):298–304. doi:10.1056/nejm199201303260504.PubMedCrossRef
10.
Lotvall J, Akdis CA, Bacharier LB, Bjermer L, Casale TB, Custovic A, et al. Asthma endotypes: a new approach to classification of disease entities within the asthma syndrome. J Allergy Clin Immunol. 2011;127(2):355–60. doi:10.1016/j.jaci.2010.11.037.PubMedCrossRef
11.
Wenzel SE. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med. 2012;18(5):716–25. doi:10.1038/nm.2678.PubMedCrossRef
12.
Agache I, Akdis C, Jutel M, Virchow JC. Untangling asthma phenotypes and endotypes. Allergy. 2012;67(7):835–46. doi:10.1111/j.1398-9995.2012.02832.x.PubMedCrossRef
13.
Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL, Weijer K, et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol. 2013;14(3):221–9. doi:10.1038/ni.2534.PubMedCrossRef
14.
15.
Korsgren M, Persson CG, Sundler F, Bjerke T, Hansson T, Chambers BJ, et al. Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J Exp Med. 1999;189(3):553–62.PubMedCentralPubMedCrossRef
16.
Barnig C, Cernadas M, Dutile S, Liu X, Perrella MA, Kazani S, et al. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci Transl Med. 2013;5(174):174ra26. doi:10.1126/scitranslmed.3004812.PubMedCrossRef
17.
Huang YJ. The respiratory microbiome and innate immunity in asthma. Curr Opin Pulm Med. 2015;21(1):27–32. doi:10.1097/MCP.0000000000000124.PubMedCrossRef
18.
Fuchs A, Vermi W, Lee JS, Lonardi S, Gilfillan S, Newberry RD, et al. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-gamma-producing cells. Immunity. 2013;38(4):769–81. doi:10.1016/j.immuni.2013.02.010.PubMedCentralPubMedCrossRef
19.
Saenz SA, Siracusa MC, Monticelli LA, Ziegler CG, Kim BS, Brestoff JR, et al. IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MPPtype2) cells. J Exp Med. 2013;210(9):1823–37. doi:10.1084/jem.20122332.PubMedCentralPubMedCrossRef
20.
Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TK, et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010;464(7293):1367–70. doi:10.1038/nature08900.PubMedCentralPubMedCrossRef
21.
Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010;463(7280):540–4. doi:10.1038/nature08636.PubMedCrossRef
22.
Halim TY, Krauss RH, Sun AC, Takei F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity. 2012;36(3):451–63. doi:10.1016/j.immuni.2011.12.020.PubMedCrossRef
23.
Mjosberg JM, Trifari S, Crellin NK, Peters CP, van Drunen CM, Piet B, 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(11):1055–62. doi:10.1038/ni.2104.PubMedCrossRef
24.
Bartemes KR, Kephart GM, Fox SJ, Kita H. Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J Allergy Clin Immunol. 2014;134(3):671–8. doi:10.1016/j.jaci.2014.06.024.PubMedCentralPubMedCrossRef
25.
Allakhverdi Z, Comeau MR, Jessup HK, Yoon BR, Brewer A, Chartier S, 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. 2007;204(2):253–8. doi:10.1084/jem.20062211.PubMedCentralPubMedCrossRef
26.
Angkasekwinai P, Park H, Wang YH, Wang YH, Chang SH, Corry DB, et al. Interleukin 25 promotes the initiation of proallergic type 2 responses. J Exp Med. 2007;204(7):1509–17. doi:10.1084/jem.20061675.PubMedCentralPubMedCrossRef
27.
Oliphant CJ, Barlow JL, McKenzie AN. Insights into the initiation of type 2 immune responses. Immunology. 2011;134(4):378–85. doi:10.1111/j.1365-2567.2011.03499.x.PubMedCentralPubMedCrossRef
28.
Kondo Y, Yoshimoto T, Yasuda K, Futatsugi-Yumikura S, Morimoto M, Hayashi N, et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol. 2008;20(6):791–800. doi:10.1093/intimm/dxn037.PubMedCrossRef
29.
Bartemes KR, Iijima K, Kobayashi T, Kephart GM, McKenzie AN, Kita H. IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol. 2012;188(3):1503–13. doi:10.4049/jimmunol.1102832.PubMedCentralPubMedCrossRef
30.
Price AE, Liang HE, Sullivan BM, Reinhardt RL, Eisley CJ, Erle DJ, et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci U S A. 2010;107(25):11489–94. doi:10.1073/pnas.1003988107.PubMedCentralPubMedCrossRef
31.
Barlow JL, Bellosi A, Hardman CS, Drynan LF, Wong SH, Cruickshank JP, et al. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol. 2012;129(1):191–8 e1-4. 10.1016/j.jaci.2011.09.041.PubMedCrossRef
32.
Doherty TA, Khorram N, Lund S, Mehta AK, Croft M, Broide DH. Lung type 2 innate lymphoid cells express cysteinyl leukotriene receptor 1, which regulates TH2 cytokine production. J Allergy Clin Immunol. 2013;132(1):205–13. doi:10.1016/j.jaci.2013.03.048.PubMedCentralPubMedCrossRef
33.
Kim HY, Chang YJ, Subramanian S, Lee HH, Albacker LA, Matangkasombut P, et al. Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity. J Allergy Clin Immunol. 2012;129(1):216–27 e1-6. doi:10.1016/j.jaci.2011.10.036.PubMedCentralPubMedCrossRef
34.
Klein Wolterink RG, Kleinjan A, van Nimwegen M, Bergen I, de Bruijn M, Levani Y, 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(5):1106–16. doi:10.1002/eji.201142018.PubMedCrossRef
35.
Wilhelm C, Hirota K, Stieglitz B, Van Snick J, Tolaini M, Lahl K, et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol. 2011;12(11):1071–7. doi:10.1038/ni.2133.PubMedCentralPubMedCrossRef
36.
Bando JK, Nussbaum JC, Liang HE, Locksley RM. Type 2 innate lymphoid cells constitutively express arginase-I in the naive and inflamed lung. J Leukoc Biol. 2013;94(5):877–84. doi:10.1189/jlb.0213084.PubMedCentralPubMedCrossRef
37.
Maarsingh H, Dekkers BG, Zuidhof AB, Bos IS, Menzen MH, Klein T, et al. Increased arginase activity contributes to airway remodelling in chronic allergic asthma. Eur Respir J. 2011;38(2):318–28. doi:10.1183/09031936.00057710.PubMedCrossRef
38.
Maarsingh H, Zaagsma J, Meurs H. Arginase: a key enzyme in the pathophysiology of allergic asthma opening novel therapeutic perspectives. Br J Pharmacol. 2009;158(3):652–64. doi:10.1111/j.1476-5381.2009.00374.x.PubMedCentralPubMedCrossRef
39.
Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH, Brewer JM, et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity. 2014;41(2):283–95. doi:10.1016/j.immuni.2014.06.016.PubMedCentralPubMedCrossRef
40.
Drake LY, Iijima K, Kita H. Group 2 innate lymphoid cells and CD4+ T cells cooperate to mediate type 2 immune response in mice. Allergy. 2014;69(10):1300–7. doi:10.1111/all.12446.PubMedCentralPubMedCrossRef
41.
Mirchandani AS, Besnard AG, Yip E, Scott C, Bain CC, Cerovic V, et al. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J Immunol. 2014;192(5):2442–8. doi:10.4049/jimmunol.1300974.PubMedCrossRef
42.
Miranda C, Busacker A, Balzar S, Trudeau J, Wenzel SE. Distinguishing severe asthma phenotypes: role of age at onset and eosinophilic inflammation. J Allergy Clin Immunol. 2004;113(1):101–8. doi:10.1016/j.jaci.2003.10.041.PubMedCrossRef
43.
Miljkovic D, Bassiouni A, Cooksley C, Ou J, Hauben E, Wormald PJ, et al. Association between group 2 innate lymphoid cells enrichment, nasal polyps and allergy in chronic rhinosinusitis. Allergy. 2014;69(9):1154–61. doi:10.1111/all.12440.PubMedCrossRef
44.
Shaw JL, Fakhri S, Citardi MJ, Porter PC, Corry DB, Kheradmand F, 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. 2013;188(4):432–9. doi:10.1164/rccm.201212-2227OC.PubMedCrossRef
45.
Ho J, Bailey M, Zaunders J, Mrad N, Sacks R, Sewell W, et al. Group 2 innate lymphoid cells (ILC2s) are increased in chronic rhinosinusitis with nasal polyps or eosinophilia. Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology. 2015;45(2):394–403. doi:10.1111/cea.12462.CrossRef
46.
Lam M, Hull L, McLachlan R, Snidvongs K, Chin D, Pratt E, et al. Clinical severity and epithelial endotypes in chronic rhinosinusitis. International forum of allergy & rhinology. 2013;3(2):121–8. doi:10.1002/alr.21082.CrossRef
47.
Mjosberg J, Bernink J, Golebski K, Karrich JJ, Peters CP, Blom B, et al. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity. 2012;37(4):649–59. doi:10.1016/j.immuni.2012.08.015.PubMedCrossRef
48.
Singh AM, Moore PE, Gern JE, Lemanske Jr RF, Hartert TV. Bronchiolitis to asthma: a review and call for studies of gene-virus interactions in asthma causation. Am J Respir Crit Care Med. 2007;175(2):108–19. doi:10.1164/rccm.200603-435PP.PubMedCrossRef
49.
Bacharier LB, Boner A, Carlsen KH, Eigenmann PA, Frischer T, Gotz M, et al. Diagnosis and treatment of asthma in childhood: a PRACTALL consensus report. Allergy. 2008;63(1):5–34. doi:10.1111/j.1398-9995.2007.01586.x.PubMedCrossRef
50.
51.
Jackson DJ, Evans MD, Gangnon RE, Tisler CJ, Pappas TE, Lee WM, et al. Evidence for a causal relationship between allergic sensitization and rhinovirus wheezing in early life. Am J Respir Crit Care Med. 2012;185(3):281–5. doi:10.1164/rccm.201104-0660OC.PubMedCentralPubMedCrossRef
52.
Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN, Smith DE, et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol. 2011;12(7):631–8. doi:10.1038/ni.2045.PubMedCentralPubMedCrossRef
53.
Gorski SA, Hahn YS, Braciale TJ. Group 2 innate lymphoid cell production of IL-5 is regulated by NKT cells during influenza virus infection. PLoS Pathog. 2013;9(9), e1003615. doi:10.1371/journal.ppat.1003615.PubMedCentralPubMedCrossRef
54.
Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, 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(1):443–53.PubMedCrossRef
55.
Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity. 2005;23(5):479–90. doi:10.1016/j.immuni.2005.09.015.PubMedCrossRef
56.
Gregory LG, Jones CP, Walker SA, Sawant D, Gowers KH, Campbell GA, et al. IL-25 drives remodelling in allergic airways disease induced by house dust mite. Thorax. 2013;68(1):82–90. doi:10.1136/thoraxjnl-2012-202003.PubMedCentralPubMedCrossRef
57.
Ballantyne SJ, Barlow JL, Jolin HE, Nath P, Williams AS, Chung KF, et al. Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. J Allergy Clin Immunol. 2007;120(6):1324–31. doi:10.1016/j.jaci.2007.07.051.PubMedCrossRef
58.
Cherry WB, Yoon J, Bartemes KR, Iijima K, Kita H. A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol. 2008;121(6):1484–90. doi:10.1016/j.jaci.2008.04.005.PubMedCentralPubMedCrossRef
59.
Silver MR, Margulis A, Wood N, Goldman SJ, Kasaian M, Chaudhary D. IL-33 synergizes with IgE-dependent and IgE-independent agents to promote mast cell and basophil activation. Inflamm Res. 2010;59(3):207–18. doi:10.1007/s00011-009-0088-5.PubMedCrossRef
60.
Barlow JL, Peel S, Fox J, Panova V, Hardman CS, Camelo A, et al. IL-33 is more potent than IL-25 in provoking IL-13-producing nuocytes (type 2 innate lymphoid cells) and airway contraction. J Allergy Clin Immunol. 2013;132(4):933–41. doi:10.1016/j.jaci.2013.05.012.PubMedCrossRef
61.
Liu X, Li M, Wu Y, Zhou Y, Zeng L, Huang T. Anti-IL-33 antibody treatment inhibits airway inflammation in a murine model of allergic asthma. Biochem Biophys Res Commun. 2009;386(1):181–5. doi:10.1016/j.bbrc.2009.06.008.PubMedCrossRef
62.
63.
Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol. 2008;8(5):349–61. doi:10.1038/nri2294.PubMedCentralPubMedCrossRef
64.
Serhan CN, Yang R, Martinod K, Kasuga K, Pillai PS, Porter TF, et al. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J Exp Med. 2009;206(1):15–23. doi:10.1084/jem.20081880.PubMedCentralPubMedCrossRef
65.
Krishnamoorthy N, Burkett PR, Dalli J, Abdulnour RE, Colas R, Ramon S, et al. Cutting edge: maresin-1 engages regulatory T cells to limit type 2 innate lymphoid cell activation and promote resolution of lung inflammation. J Immunol. 2015;194(3):863–7. doi:10.4049/jimmunol.1402534.PubMedCrossRef
66.
Xue L, Salimi M, Panse I, Mjosberg JM, McKenzie AN, Spits H, et al. Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells. J Allergy Clin Immunol. 2014;133(4):1184–94. doi:10.1016/j.jaci.2013.10.056.PubMedCentralPubMedCrossRef
67.
Pettipher R, Hansel TT, Armer R. Antagonism of the prostaglandin D2 receptors DP1 and CRTH2 as an approach to treat allergic diseases. Nat Rev Drug Discov. 2007;6(4):313–25. doi:10.1038/nrd2266.PubMedCrossRef
68.
Lao-Araya M, Steveling E, Scadding GW, Durham SR, Shamji MH. Seasonal increases in peripheral innate lymphoid type 2 cells are inhibited by subcutaneous grass pollen immunotherapy. J Allergy Clin Immunol. 2014;134(5):1193–5. doi:10.1016/j.jaci.2014.07.029. 5.PubMedCrossRef
69.
Kudo M, Melton AC, Chen C, Engler MB, Huang KE, Ren X, et al. IL-17A produced by alphabeta T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat Med. 2012;18(4):547–54. doi:10.1038/nm.2684.PubMedCentralPubMedCrossRef
70.
McKinley L, Alcorn JF, Peterson A, Dupont RB, Kapadia S, Logar A, et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol. 2008;181(6):4089–97.PubMedCentralPubMedCrossRef
71.
Geremia A, Arancibia-Carcamo CV, Fleming MP, Rust N, Singh B, Mortensen NJ, et al. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J Exp Med. 2011;208(6):1127–33. doi:10.1084/jem.20101712.PubMedCentralPubMedCrossRef
72.
Kim HY, Lee HJ, Chang YJ, Pichavant M, Shore SA, Fitzgerald KA, et al. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat Med. 2014;20(1):54–61. doi:10.1038/nm.3423.PubMedCentralPubMedCrossRef
73.
Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S, Sinha R, et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature. 2013;498(7452):113–7. doi:10.1038/nature12240.PubMedCentralPubMedCrossRef
74.
Taube C, Tertilt C, Gyulveszi G, Dehzad N, Kreymborg K, Schneeweiss K, et al. IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS One. 2011;6(7):e21799. doi:10.1371/journal.pone.0021799.PubMedCentralPubMedCrossRef
75.
Buonocore S, Ahern PP, Uhlig HH, Ivanov II, Littman DR, Maloy KJ, et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature. 2010;464(7293):1371–5. doi:10.1038/nature08949.PubMedCentralPubMedCrossRef
76.
Sun YC, Zhou QT, Yao WZ. Sputum interleukin-17 is increased and associated with airway neutrophilia in patients with severe asthma. Chin Med J (Engl). 2005;118(11):953–6.
77.
Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med. 2010;104(8):1131–7. doi:10.1016/j.rmed.2010.02.018.PubMedCrossRef
78.
Zhao Y, Yang J, Gao YD, Guo W. Th17 immunity in patients with allergic asthma. Int Arch Allergy Immunol. 2010;151(4):297–307. doi:10.1159/000250438.PubMedCrossRef
79.
Sherkat R, Yazdani R, Ganjalikhani Hakemi M, Homayouni V, Farahani R, Hosseini M, et al. Innate lymphoid cells and cytokines of the novel subtypes of helper T cells in asthma. Asia Pacific allergy. 2014;4(4):212–21. doi:10.5415/apallergy.2014.4.4.212.PubMedCentralPubMedCrossRef
80.
Gibeon D, Batuwita K, Osmond M, Heaney LG, Brightling CE, Niven R, et al. Obesity-associated severe asthma represents a distinct clinical phenotype: analysis of the British Thoracic Society Difficult Asthma Registry Patient cohort according to BMI. Chest. 2013;143(2):406–14. doi:10.1378/chest.12-0872.PubMedCrossRef
81.
Brestoff JR, Kim BS, Saenz SA, Stine RR, Monticelli LA, Sonnenberg GF, et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature. 2014. doi:10.1038/nature14115.PubMed
82.
Lee MW, Odegaard JI, Mukundan L, Qiu Y, Molofsky AB, Nussbaum JC, et al. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell. 2015;160(1–2):74–87. doi:10.1016/j.cell.2014.12.011.PubMedCrossRef
83.
Spencer SP, Wilhelm C, Yang Q, Hall JA, Bouladoux N, Boyd A, et al. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science. 2014;343(6169):432–7. doi:10.1126/science.1247606.PubMedCentralPubMedCrossRef
84.
Chen J, Waddell A, Lin YD, Cantorna MT. Dysbiosis caused by vitamin D receptor deficiency confers colonization resistance to Citrobacter rodentium through modulation of innate lymphoid cells. Mucosal immunology. 2014. doi:10.1038/mi.2014.94.
85.
Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science. 2014;343(6178):1249288. doi:10.1126/science.1249288.PubMedCentralPubMedCrossRef
86.
Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, et al. Disordered microbial communities in asthmatic airways. PLoS One. 2010;5(1):e8578. doi:10.1371/journal.pone.0008578.PubMedCentralPubMedCrossRef
Metadata
Title
Innate lymphocyte cells in asthma phenotypes
Authors
Leyla Pur Ozyigit
Hideaki Morita
Mubeccel Akdis
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Clinical and Translational Allergy / Issue 1/2015
Electronic ISSN: 2045-7022
DOI
https://doi.org/10.1186/s13601-015-0068-5

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