Innate lymphoid cells contribute to allergic airway disease exacerbation by obesity

Journal of Allergy and Clinical Immunology

Volumn 138, Issue 5, 2016, Pages 1309-1318.e11

  Everaere, Laetitia ^a,b,c,d,e   Ait Yahia, Saliha ^a,b,c   Molendi Coste, Olivier ^b,c,d,e   Vorng, Han ^a,b,c   Quemener, Sandrine ^b,c,d,e   LeVu, Pauline ^b,c,d,e   Fleury, Sebastien ^b,c,d,e   Bouchaert, Emmanuel ^b,c,d,e   Fan, Ying ^a,b,c   Duez, Catherine ^a,b,c   de Nadai, Patricia ^a,b,c   Staels, Bart ^b,c,d,e   Dombrowicz, David ^b,c,d,e   Tsicopoulos, Anne ^a,b,c,f  

^a INSERM U1019   (France)

^b INSTITUT PASTEUR DE LILLE   (France)

^c UNIV LILLE   (France)

^d INSERM   (France)

^e France   (France)

^f LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

allergy; asthma; high fat diet; house dust mite; Innate lymphoid cells; obesity; TH17; TH2

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; MESSENGER RNA; CYTOKINE; HOUSE DUST ALLERGEN; IMMUNOGLOBULIN E;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DISEASE EXACERBATION; EOSINOPHILIA; HUMORAL IMMUNITY; INTRAPERITONEAL FAT; LIPID DIET; LYMPHOID CELL; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; TH17 CELL; TH2 CELL; ANIMAL; ASTHMA; BLOOD; C57BL MOUSE; CYTOLOGY; IMMUNOLOGY; INNATE IMMUNITY; LUNG; LYMPHOCYTE; PATHOPHYSIOLOGY; SPLEEN; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, DERMATOPHAGOIDES; ASTHMA; CYTOKINES; DIET, HIGH-FAT; IMMUNITY, INNATE; IMMUNOGLOBULIN E; LUNG; LYMPHOCYTES; MICE, INBRED C57BL; MICE, TRANSGENIC; OBESITY; SPLEEN;

EID: 84975125294     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.03.019     Document Type: Article

References (60)

1. 1 Ford, E.S., The epidemiology of obesity and asthma. J Allergy Clin Immunol 115 (2005), 897–909.
2. 2 Beuther, D.A., Sutherland, E.R., Overweight, obesity, and incident asthma: a meta-analysis of prospective epidemiologic studies. Am J Respir Crit Care Med 175 (2007), 661–666.
3. 3 Dixon, A.E., Pratley, R.E., Forgione, P.M., Kaminsky, D.A., Whittaker-Leclair, L.A., Griffes, L.A., et al. Effects of obesity and bariatric surgery on airway hyperresponsiveness, asthma control, and inflammation. J Allergy Clin Immunol 128 (2011), 508–515.
4. 4 Scott, H.A., Gibson, P.G., Garg, M.L., Pretto, J.J., Morgan, P.J., Callister, R., et al. Dietary restriction and exercise improve airway inflammation and clinical outcomes in overweight and obese asthma: a randomized trial. Clin Exp Allergy 43 (2013), 36–49.
5. 5 Scott, H.A., Gibson, P.G., Garg, M.L., Wood, L.G., Airway inflammation is augmented by obesity and fatty acids in asthma. Eur Respir J 38 (2011), 594–602.
6. 6 Telenga, E.D., Tideman, S.W., Kerstjens, H.A., Hacken, N.H., Timens, W., Postma, D.S., et al. Obesity in asthma: more neutrophilic inflammation as a possible explanation for a reduced treatment response. Allergy 67 (2012), 1060–1068.
7. 7 Desai, D., Newby, C., Symon, F.A., Haldar, P., Shah, S., Gupta, S., et al. Elevated sputum interleukin-5 and submucosal eosinophilia in obese individuals with severe asthma. Am J Respir Crit Care Med 188 (2013), 657–663.
8. 8 Peters, M.C., Fahy, J.V., Type 2 immune responses in obese individuals with asthma. Am J Respir Crit Care Med 188 (2013), 633–634.
9. 9 Forno, E., Acosta-Perez, E., Brehm, J.M., Han, Y.Y., Alvarez, M., Colon-Semidey, A., et al. Obesity and adiposity indicators, asthma, and atopy in Puerto Rican children. J Allergy Clin Immunol 133 (2014), 1308–1314.
10. 10 Hancox, R.J., Milne, B.J., Poulton, R., Taylor, D.R., Greene, J.M., McLachlan, C.R., et al. Sex differences in the relation between body mass index and asthma and atopy in a birth cohort. Am J Respir Crit Care Med 171 (2005), 440–445.
11. 11 Ma, J., Xiao, L., Knowles, S.B., Obesity, insulin resistance and the prevalence of atopy and asthma in US adults. Allergy 65 (2010), 1455–1463.
12. 12 Sutherland, T.J., Cowan, J.O., Young, S., Goulding, A., Grant, A.M., Williamson, A., et al. The association between obesity and asthma: interactions between systemic and airway inflammation. Am J Respir Crit Care Med 178 (2008), 469–475.
13. 13 Quinto, K.B., Zuraw, B.L., Poon, K.Y., Chen, W., Schatz, M., Christiansen, S.C., The association of obesity and asthma severity and control in children. J Allergy Clin Immunol 128 (2011), 964–969.
14. 14 Rasmussen, F., Hancox, R.J., Mechanisms of obesity in asthma. Curr Opin Allergy Clin Immunol 14 (2014), 35–43.
15. 15 Shore, S.A., Obesity, airway hyperresponsiveness, and inflammation. J Appl Physiol (1985) 108 (2010), 735–743.
16. 16 Shore, S.A., Schwartzman, I.N., Mellema, M.S., Flynt, L., Imrich, A., Johnston, R.A., Effect of leptin on allergic airway responses in mice. J Allergy Clin Immunol 115 (2005), 103–109.
17. 17 Shore, S.A., Terry, R.D., Flynt, L., Xu, A., Hug, C., Adiponectin attenuates allergen-induced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 118 (2006), 389–395.
18. 18 Jartti, T., Saarikoski, L., Jartti, L., Lisinen, I., Jula, A., Huupponen, R., et al. Obesity, adipokines and asthma. Allergy 64 (2009), 770–777.
19. 19 Sutherland, T.J., Sears, M.R., McLachlan, C.R., Poulton, R., Hancox, R.J., Leptin, adiponectin, and asthma: findings from a population-based cohort study. Ann Allergy Asthma Immunol 103 (2009), 101–107.
20. 20 Schnyder-Candrian, S., Togbe, D., Couillin, I., Mercier, I., Brombacher, F., Quesniaux, V., et al. Interleukin-17 is a negative regulator of established allergic asthma. J Exp Med 203 (2006), 2715–2725.
21. 21 Winer, S., Paltser, G., Chan, Y., Tsui, H., Engleman, E., Winer, D., et al. Obesity predisposes to Th17 bias. Eur J Immunol 39 (2009), 2629–2635.
22. 22 Calixto, M.C., Lintomen, L., Schenka, A., Saad, M.J., Zanesco, A., Antunes, E., Obesity enhances eosinophilic inflammation in a murine model of allergic asthma. Br J Pharmacol 159 (2010), 617–625.
23. 23 Dietze, J., Bocking, C., Heverhagen, J.T., Voelker, M.N., Renz, H., Obesity lowers the threshold of allergic sensitization and augments airway eosinophilia in a mouse model of asthma. Allergy 67 (2012), 1519–1529.
24. 24 de Vries, A., Hazlewood, L., Fitch, P.M., Seckl, J.R., Foster, P., Howie, S.E., High-fat feeding redirects cytokine responses and decreases allergic airway eosinophilia. Clin Exp Allergy 39 (2009), 731–739.
25. 25 Ge, X.N., Greenberg, Y., Hosseinkhani, M.R., Long, E.K., Bahaie, N.S., Rao, A., et al. High-fat diet promotes lung fibrosis and attenuates airway eosinophilia after exposure to cockroach allergen in mice. Exp Lung Res 39 (2013), 365–378.
26. 26 Wood, I.S., Wang, B., Trayhurn, P., IL-33, a recently identified interleukin-1 gene family member, is expressed in human adipocytes. Biochem Biophys Res Commun 384 (2009), 105–109.
27. 27 Prefontaine, D., Nadigel, J., Chouiali, F., Audusseau, S., Semlali, A., Chakir, J., et al. Increased IL-33 expression by epithelial cells in bronchial asthma. J Allergy Clin Immunol 125 (2010), 752–754.
28. 28 Zeyda, M., Wernly, B., Demyanets, S., Kaun, C., Hammerle, M., Hantusch, B., et al. Severe obesity increases adipose tissue expression of interleukin-33 and its receptor ST2, both predominantly detectable in endothelial cells of human adipose tissue. Int J Obes (Lond) 37 (2013), 658–665.
29. 29 Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J.P., Eberl, G., et al. Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol 13 (2013), 145–149.
30. 30 Bartemes, K.R., Kephart, G.M., Fox, S.J., Kita, H., Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J Allergy Clin Immunol 134 (2014), 671–678.
31. 31 Barlow, J.L., Bellosi, A., Hardman, C.S., Drynan, L.F., Wong, S.H., Cruickshank, J.P., et al. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol 129 (2012), 191–198.
32. 32 Bartemes, K.R., Iijima, K., Kobayashi, T., Kephart, G.M., McKenzie, A.N., Kita, H., IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol 188 (2012), 1503–1513.
33. 33 Halim, T.Y., Krauss, R.H., Sun, A.C., Takei, F., Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36 (2012), 451–463.
34. 34 Klein Wolterink, R.G., 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 42 (2012), 1106–1116.
35. 35 Gold, M.J., Antignano, F., Halim, T.Y., Hirota, J.A., Blanchet, M.R., Zaph, C., et al. Group 2 innate lymphoid cells facilitate sensitization to local, but not systemic, TH2-inducing allergen exposures. J Allergy Clin Immunol 133 (2014), 1142–1148.
36. 36 Halim, T.Y., Steer, C.A., Matha, L., Gold, M.J., Martinez-Gonzalez, I., McNagny, K.M., et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40 (2014), 425–435.
37. 37 Mirchandani, A.S., Besnard, A.G., Yip, E., Scott, C., Bain, C.C., Cerovic, V., et al. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J Immunol 192 (2014), 2442–2448.
38. 38 Oliphant, C.J., Hwang, Y.Y., Walker, J.A., Salimi, M., Wong, S.H., Brewer, J.M., 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 41 (2014), 283–295.
39. 39 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 463 (2010), 540–544.
40. 40 Hams, E., Locksley, R.M., McKenzie, A.N., Fallon, P.G., Cutting edge: IL-25 elicits innate lymphoid type 2 and type II NKT cells that regulate obesity in mice. J Immunol 191 (2013), 5349–5353.
41. 41 Molofsky, A.B., Nussbaum, J.C., Liang, H.E., Van Dyken, S.J., Cheng, L.E., Mohapatra, A., et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med 210 (2013), 535–549.
42. 42 Nussbaum, J.C., Van Dyken, S.J., von Moltke, J., Cheng, L.E., Mohapatra, A., Molofsky, A.B., et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502 (2013), 245–248.
43. 43 Buonocore, S., Ahern, P.P., Uhlig, H.H., Ivanov, I.I., Littman, D.R., Maloy, K.J., et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464 (2010), 1371–1375.
44. 44 Kim, H.Y., Lee, H.J., Chang, Y.J., Pichavant, M., Shore, S.A., Fitzgerald, K.A., et al. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat Med 20 (2014), 54–61.
45. 45 Ait Yahia, S., Azzaoui, I., Everaere, L., Vorng, H., Chenivesse, C., Marquillies, P., et al. CCL17 production by dendritic cells is required for NOD1-mediated exacerbation of allergic asthma. Am J Respir Crit Care Med 189 (2014), 899–908.
46. 46 Staumont-Salle, D., Fleury, S., Lazzari, A., Molendi-Coste, O., Hornez, N., Lavogiez, C., et al. CX(3)CL1 (fractalkine) and its receptor CX(3)CR1 regulate atopic dermatitis by controlling effector T cell retention in inflamed skin. J Exp Med 211 (2014), 1185–1196.
47. 47 Mionnet, C., Buatois, V., Kanda, A., Milcent, V., Fleury, S., Lair, D., et al. CX3CR1 is required for airway inflammation by promoting T helper cell survival and maintenance in inflamed lung. Nat Med 16 (2010), 1305–1312.
48. 48 Lu, F.L., Johnston, R.A., Flynt, L., Theman, T.A., Terry, R.D., Schwartzman, I.N., et al. Increased pulmonary responses to acute ozone exposure in obese db/db mice. Am J Physiol Lung Cell Mol Physiol 290 (2006), L856–L865.
49. 49 Kim, S.H., Sutherland, E.R., Gelfand, E.W., Is there a link between obesity and asthma?. Allergy Asthma Immunol Res 6 (2014), 189–195.
50. 50 Lloyd, C.M., Saglani, S., Eosinophils in the spotlight: finding the link between obesity and asthma. Nat Med 19 (2013), 976–977.
51. 51 Mjosberg, J., Bernink, J., Golebski, K., Karrich, J.J., Peters, C.P., Blom, B., et al. The transcription factor GATA-3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37 (2012), 649–659.
52. 52 Makki, K., Froguel, P., Wolowczuk, I., Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm, 2013, 2013, 139239.
53. 53 Coccia, M., Harrison, O.J., Schiering, C., Asquith, M.J., Becher, B., Powrie, F., et al. IL-1beta mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J Exp Med 209 (2012), 1595–1609.
54. 54 Willart, M.A., Deswarte, K., Pouliot, P., Braun, H., Beyaert, R., Lambrecht, B.N., et al. Interleukin-1alpha controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. J Exp Med 209 (2012), 1505–1517.
55. 55 Drake, L.Y., Iijima, K., Kita, H., Group 2 innate lymphoid cells and CD4+ T cells cooperate to mediate type 2 immune response in mice. Allergy 69 (2014), 1300–1307.
56. 56 Hepworth, M.R., Monticelli, L.A., Fung, T.C., Ziegler, C.G., Grunberg, S., Sinha, R., et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498 (2013), 113–117.
57. 57 von Burg, N., Chappaz, S., Baerenwaldt, A., Horvath, E., Bose Dasgupta, S., Ashok, D., et al. Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc Natl Acad Sci U S A 111 (2014), 12835–12840.
58. Makki, K., Taront, S., Molendi-Coste, O., Bouchaert, E., Neve, B., Eury, E., et al. Beneficial metabolic effects of rapamycin are associated with enhanced regulatory cells in diet-induced obese mice. PLoS One, 9, 2014, e92684.
59. Takeda, K., Haczku, A., Lee, J.J., Irvin, C.G., Gelfand, E.W., Strain dependence of airway hyperresponsiveness reflects differences in eosinophil localization in the lung. Am J Physiol Lung Cell Mol Physiol 281 (2001), L394–L402.
60. Bossard, C., Busson, M., Vindrieux, D., Gaudin, F., Machelon, V., Brigitte, M., et al. Potential role of estrogen receptor beta as a tumor suppressor of epithelial ovarian cancer. PLoS One, 7, 2012, e44787.