Interleukin-17–producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity (original) (raw)

• Flegal, K.M., Carroll, M.D., Kit, B.K. & Ogden, C.L. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. J. Am. Med. Assoc. 307, 491–497 (2012).
  Article Google Scholar
• Osborn, O. & Olefsky, J.M. The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 18, 363–374 (2012).
  Article PubMed CAS Google Scholar
• Wenzel, S.E. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat. Med. 18, 716–725 (2012).
  Article PubMed CAS Google Scholar
• Holguin, F. et al. Obesity and asthma: an association modified by age of asthma onset. J. Allergy Clin. Immunol. 127, 1486–1493.e2 (2011).
  Article PubMed PubMed Central Google Scholar
• Camargo, C.A. Jr., Weiss, S.T., Zhang, S., Willett, W.C. & Speizer, F.E. Prospective study of body mass index, weight change, and risk of adult-onset asthma in women. Arch. Intern. Med. 159, 2582–2588 (1999).
  Article PubMed Google Scholar
• Dixon, A.E. et al. Effects of obesity and bariatric surgery on airway hyperresponsiveness, asthma control, and inflammation. J. Allergy Clin. Immunol. 128, 508–515.e1–2 (2011).
  Article PubMed PubMed Central Google Scholar
• Sutherland, E.R., Lehman, E.B., Teodorescu, M. & Wechsler, M.E. Body mass index and phenotype in subjects with mild-to-moderate persistent asthma. J. Allergy Clin. Immunol. 123, 1328–1334.e1 (2009).
  Article PubMed PubMed Central Google Scholar
• Shore, S.A. Obesity, airway hyperresponsiveness, and inflammation. J. Appl. Physiol. 108, 735–743 (2010).
  Article PubMed Google Scholar
• Farah, C.S. & Salome, C.M. Asthma and obesity: a known association but unknown mechanism. Respirology 17, 412–421 (2012).
  Article PubMed Google Scholar
• Kanneganti, T.D. & Dixit, V.D. Immunological complications of obesity. Nat. Immunol. 13, 707–712 (2012).
  Article PubMed CAS Google Scholar
• Feuerer, M. et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15, 930–939 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Nishimura, S. et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15, 914–920 (2009).
  Article PubMed CAS Google Scholar
• Olefsky, J.M. & Glass, C.K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219–246 (2010).
  Article PubMed CAS Google Scholar
• 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, 594–602 (2011).
  Article PubMed CAS Google Scholar
• Chen, Y., Dales, R. & Jiang, Y. The association between obesity and asthma is stronger in nonallergic than allergic adults. Chest 130, 890–895 (2006).
  Article PubMed Google Scholar
• Moore, W.C. et al. Identification of asthma phenotypes using cluster analysis in the Severe Asthma Research Program. Am. J. Respir. Crit. Care Med. 181, 315–323 (2010).
  Article PubMed Google Scholar
• Lu, F.L. et al. Increased pulmonary responses to acute ozone exposure in obese db/db mice. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L856–L865 (2006).
  Article PubMed CAS Google Scholar
• Arteaga-Solis, E. et al. Inhibition of leptin regulation of parasympathetic signaling as a cause of extreme body weight-associated asthma. Cell Metab. 17, 35–48 (2013).
  Article PubMed CAS Google Scholar
• Buonocore, S. et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464, 1371–1375 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Geremia, A. et al. IL-23–responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 208, 1127–1133 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Coccia, M. et al. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4+ TH17 cells. J. Exp. Med. 209, 1595–1609 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Klose, C.S. et al. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 494, 261–265 (2013).
  Article PubMed CAS Google Scholar
• Sun, Z. et al. Requirement for RORγ in thymocyte survival and lymphoid organ development. Science 288, 2369–2373 (2000).
  Article PubMed CAS Google Scholar
• Sawa, S. et al. RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 12, 320–326 (2011).
  Article PubMed CAS Google Scholar
• Cupedo, T. et al. Human fetal lymphoid tissue-inducer cells are interleukin 17–producing precursors to RORC+ CD127+ natural killer–like cells. Nat. Immunol. 10, 66–74 (2009).
  Article PubMed CAS Google Scholar
• Sanos, S.L. et al. RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22–producing NKp46+ cells. Nat. Immunol. 10, 83–91 (2009).
  Article PubMed CAS Google Scholar
• Luci, C. et al. Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 10, 75–82 (2009).
  Article PubMed CAS Google Scholar
• Chang, Y.-J. et al. Innate lymphoid cells mediate influenza-induced airway hyperreactivity independent of adaptive immunity. Nat. Immunol. 12, 631–638 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• 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, 451–463 (2012).
  Article PubMed CAS Google Scholar
• Klein Wolterink, R.G. 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, 1106–1116 (2012).
  Article PubMed CAS Google Scholar
• Spits, H. et al. Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13, 145–149 (2013).
  Article PubMed CAS Google Scholar
• Winer, S. et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 15, 921–929 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Ivanov, I.I. et al. Induction of intestinal TH17 cells by segmented filamentous bacteria. Cell 139, 485–498 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Gaboriau-Routhiau, V. et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677–689 (2009).
  Article PubMed CAS Google Scholar
• Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M. & Stockinger, B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17–producing T cells. Immunity 24, 179–189 (2006).
  Article PubMed CAS Google Scholar
• Lynch, L. et al. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 37, 574–587 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Wen, H. et al. Fatty acid–induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12, 408–415 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Duewell, P. et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357–1361 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Larsen, C.M. et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N. Engl. J. Med. 356, 1517–1526 (2007).
  Article PubMed CAS Google Scholar
• Vandanmagsar, B. et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179–188 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Johnston, R.A. et al. Diet-induced obesity causes innate airway hyperresponsiveness to methacholine and enhances ozone-induced pulmonary inflammation. J. Appl. Physiol. 104, 1727–1735 (2008).
  Article PubMed CAS Google Scholar
• Williams, A.S. et al. Obesity and airway responsiveness: role of TNFR2. Pulm. Pharmacol. Ther. 26, 444–454 (2013).
  Article PubMed CAS Google Scholar
• Johnston, R.A. et al. Allergic airway responses in obese mice. Am. J. Respir. Crit. Care Med. 176, 650–658 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Calixto, M.C. et al. Obesity enhances eosinophilic inflammation in a murine model of allergic asthma. Br. J. Pharmacol. 159, 617–625 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Kudo, M. et al. IL-17A produced by αβ T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat. Med. 18, 547–554 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• McKinley, L. et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181, 4089–4097 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Wakashin, H. et al. IL-23 and TH17 cells enhance TH2-cell–mediated eosinophilic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 178, 1023–1032 (2008).
  Article PubMed CAS Google Scholar
• Lajoie, S. et al. 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 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Murdoch, J.R. & Lloyd, C.M. Resolution of allergic airway inflammation and airway hyperreactivity is mediated by IL-17–producing γδ T cells. Am. J. Respir. Crit. Care Med. 182, 464–476 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Naik, S. et al. Compartmentalized control of skin immunity by resident commensals. Science 337, 1115–1119 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Gross, O., Thomas, C.J., Guarda, G. & Tschopp, J. The inflammasome: an integrated view. Immunol. Rev. 243, 136–151 (2011).
  Article PubMed CAS Google Scholar
• Eisenbarth, S.C., Colegio, O.R., O'Connor, W., Sutterwala, F.S. & Flavell, R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453, 1122–1126 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Besnard, A.G. et al. NLRP3 inflammasome is required in murine asthma in the absence of aluminum adjuvant. Allergy 66, 1047–1057 (2011).
  Article PubMed CAS Google Scholar
• Allen, I.C. et al. Analysis of NLRP3 in the development of allergic airway disease in mice. J. Immunol. 188, 2884–2893 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Kool, M. et al. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 34, 527–540 (2011).
  Article PubMed CAS Google Scholar
• Marichal, T. et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat. Med. 17, 996–1002 (2011).
  Article PubMed CAS Google Scholar
• Crellin, N.K. et al. Regulation of cytokine secretion in human CD127+ LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 33, 752–764 (2010).
  Article PubMed CAS Google Scholar
• Winer, S. et al. Obesity predisposes to TH17 bias. Eur. J. Immunol. 39, 2629–2635 (2009).
  Article PubMed CAS Google Scholar
• Fantuzzi, G. Adipose tissue, adipokines and inflammation. J. Allergy Clin. Immunol. 115, 911–919, quiz 920 (2005).
  Article PubMed CAS Google Scholar
• Kim, H.Y., DeKruyff, R.H. & Umetsu, D.T. The many paths to asthma: phenotype shaped by innate and adaptive immunity. Nat. Immunol. 11, 577–584 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Nakae, S. et al. Antigen-specific T cell sensitization is impaired in IL-17–deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17, 375–387 (2002).
  Article PubMed CAS Google Scholar
• Sutterwala, F.S. et al. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317–327 (2006).
  Article PubMed CAS Google Scholar
• McKenzie, G.J., Fallon, P.G., Emson, C.L., Grencis, R.K. & McKenzie, A.N. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 189, 1565–1572 (1999).
  Article PubMed PubMed Central CAS Google Scholar
• Akbari, O. et al. Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 9, 582–588 (2003).
  Article PubMed CAS Google Scholar