Pulmonary receptor for advanced glycation end-products promotes asthma pathogenesis through IL-33 and accumulation of group 2 innate lymphoid cells

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 3, 2015, Pages 747-756.e4

  Oczypok, Elizabeth A ^a   Milutinovic, Pavle S ^a   Alcorn, John F ^b   Khare, Anupriya ^a   Crum, Lauren T ^a   Manni, Michelle L ^b   Epperly, Michael W ^c   Pawluk, Adriane M ^a   Ray, Anuradha ^a   Oury, Tim D ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Asthma; group 2 innate lymphoid cells; IL 33; receptor for advanced glycation end products

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; INTERLEUKIN 33; AGER PROTEIN, MOUSE; ALLERGEN; HOUSE DUST ALLERGEN; IL33 PROTEIN, MOUSE; INTERLEUKIN 13; INTERLEUKIN 5;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BONE MARROW; CHIMERA; CONTROLLED STUDY; IMMUNOPATHOGENESIS; LUNG PARENCHYMA; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; ALTERNARIA; ANIMAL; ANTIBODY SPECIFICITY; CELL PROLIFERATION; CHEMICALLY INDUCED; CHEMISTRY; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; HISTOCOMPATIBILITY; IMMUNOLOGY; INNATE IMMUNITY; LUNG; LYMPHOCYTE; PATHOLOGY; PERITONEUM; PYROGLYPHIDAE; SIGNAL TRANSDUCTION; SPLEEN;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ALLERGENS; ALTERNARIA; ANIMALS; ANTIGENS, DERMATOPHAGOIDES; ASTHMA; BONE MARROW; CELL PROLIFERATION; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INTERLEUKIN-13; INTERLEUKIN-33; INTERLEUKIN-5; LUNG; LYMPHOCYTES; MICE; ORGAN SPECIFICITY; PERITONEUM; PYROGLYPHIDAE; SIGNAL TRANSDUCTION; SPLEEN; TRANSPLANTATION CHIMERA;

EID: 84941181442     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.03.011     Document Type: Article

References (73)

1. J.L. Barlow, S. Peel, J. Fox, V. Panova, C.S. Hardman, A. Camelo, and 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 132 2013 933 941
2. D.K. Chu, A. Llop-Guevara, T.D. Walker, K. Flader, S. Goncharova, J.E. Boudreau, and et al. IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization J Allergy Clin Immunol 131 2013 187 200 e1-8
3. V. Carriere, L. Roussel, N. Ortega, D.A. Lacorre, L. Americh, L. Aguilar, and et al. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo Proc Natl Acad Sci U S A 104 2007 282 287
4. M.J. Townsend, P.G. Fallon, D.J. Matthews, H.E. Jolin, and A.N. McKenzie T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses J Exp Med 191 2000 1069 1076
5. J. Schmitz, A. Owyang, E. Oldham, Y. Song, E. Murphy, T.K. McClanahan, and 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 23 2005 479 490
6. N.E. Humphreys, D. Xu, M.R. Hepworth, F.Y. Liew, and R.K. Grencis IL-33, a potent inducer of adaptive immunity to intestinal nematodes J Immunol 180 2008 2443 2449
7. J.L. Barlow, A. Bellosi, C.S. Hardman, L.F. Drynan, S.H. Wong, J.P. Cruickshank, and 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 e1-4
8. K. Oboki, T. Ohno, N. Kajiwara, K. Arae, H. Morita, A. Ishii, and et al. IL-33 is a crucial amplifier of innate rather than acquired immunity Proc Natl Acad Sci U S A 107 2010 18581 18586
9. D. Prefontaine, S. Lajoie-Kadoch, S. Foley, S. Audusseau, R. Olivenstein, A.J. Halayko, and et al. Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells J Immunol 183 2009 5094 5103
10. K. Moro, T. Yamada, M. Tanabe, T. Takeuchi, T. Ikawa, H. Kawamoto, and et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells Nature 463 2010 540 544
11. D.R. Neill, S.H. Wong, A. Bellosi, R.J. Flynn, M. Daly, T.K. Langford, and et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity Nature 464 2010 1367 1370
12. A.E. Price, H.E. Liang, B.M. Sullivan, R.L. Reinhardt, C.J. Eisley, D.J. Erle, and et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity Proc Natl Acad Sci U S A 107 2010 11489 11494
13. H. Spits, D. Artis, M. Colonna, A. Diefenbach, J.P. Di Santo, G. Eberl, and et al. Innate lymphoid cells - a proposal for uniform nomenclature Nat Rev Immunol 13 2013 145 149
14. J.L. Barlow, and A.N. McKenzie Nuocytes: expanding the innate cell repertoire in type-2 immunity J Leukoc Biol 90 2011 867 874
15. J.M. Mjosberg, S. Trifari, N.K. Crellin, C.P. Peters, C.M. van Drunen, B. Piet, and et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161 Nat Immunol 12 2011 1055 1062
16. L.A. Monticelli, G.F. Sonnenberg, M.C. Abt, T. Alenghat, C.G. Ziegler, T.A. Doering, and et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus Nat Immunol 12 2011 1045 1054
17. Z. Allakhverdi, M.R. Comeau, D.E. Smith, D. Toy, L.M. Endam, M. Desrosiers, and et al. CD34+ hemopoietic progenitor cells are potent effectors of allergic inflammation J Allergy Clin Immunol 123 2009 472 478
18. C. Barnig, M. Cernadas, S. Dutile, X. Liu, M.A. Perrella, S. Kazani, and et al. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma Sci Transl Med 5 2013 174ra26
19. E.M. Akirav, O. Henegariu, P. Preston-Hurlburt, A.M. Schmidt, R. Clynes, and K.C. Herold The receptor for advanced glycation end products (RAGE) affects T cell differentiation in OVA induced asthma PLoS One 9 2014 e95678
20. P.S. Milutinovic, J.F. Alcorn, J.M. Englert, L.T. Crum, and T.D. Oury The receptor for advanced glycation end products is a central mediator of asthma pathogenesis Am J Pathol 181 2012 1215 1225
21. M.A. Ullah, Z. Loh, W.J. Gan, V. Zhang, H. Yang, J.H. Li, and et al. Receptor for advanced glycation end products and its ligand high-mobility group box-1 mediate allergic airway sensitization and airway inflammation J Allergy Clin Immunol 134 2014 440 450
22. D.B. Hancock, M. Eijgelsheim, J.B. Wilk, S.A. Gharib, L.R. Loehr, K.D. Marciante, and et al. Meta-analyses of genome-wide association studies identify multiple loci associated with pulmonary function Nat Genet 42 2010 45 52
23. E. Repapi, I. Sayers, L.V. Wain, P.R. Burton, T. Johnson, M. Obeidat, and et al. Genome-wide association study identifies five loci associated with lung function Nat Genet 42 2010 36 44
24. R.G. Klein Wolterink, A. Kleinjan, M. van Nimwegen, I. Bergen, M. de Bruijn, Y. Levani, and 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
25. R. Constien, A. Forde, B. Liliensiek, H.J. Grone, P. Nawroth, G. Hammerling, and et al. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line Genesis 30 2001 36 44
26. J.M. Englert, L.E. Hanford, N. Kaminski, J.M. Tobolewski, R.J. Tan, C.L. Fattman, and et al. A role for the receptor for advanced glycation end products in idiopathic pulmonary fibrosis Am J Pathol 172 2008 583 591
27. T.A. Doherty, N. Khorram, J.E. Chang, H.K. Kim, P. Rosenthal, M. Croft, and et al. STAT6 regulates natural helper cell proliferation during lung inflammation initiated by Alternaria Am J Physiol Lung Cell Mol Physiol 303 2012 L577 L588
28. J.F. Alcorn, L.M. Rinaldi, E.F. Jaffe, M. van Loon, J.H. Bates, Y.M. Janssen-Heininger, and et al. Transforming growth factor-beta1 suppresses airway hyperresponsiveness in allergic airway disease Am J Respir Crit Care Med 176 2007 974 982
29. C. Moolenbeek, and E.J. Ruitenberg The "Swiss roll": a simple technique for histological studies of the rodent intestine Lab Anim 15 1981 57 59
30. M.L. Manni, M.W. Epperly, W. Han, T.S. Blackwell, S.R. Duncan, J.D. Piganelli, and et al. Leukocyte-derived extracellular superoxide dismutase does not contribute to airspace EC-SOD after interstitial pulmonary injury Am J Physiol Lung Cell Mol Physiol 302 2012 L160 L166
31. M.B. Everhart, W. Han, K.S. Parman, V.V. Polosukhin, H. Zeng, R.T. Sadikot, and et al. Intratracheal administration of liposomal clodronate accelerates alveolar macrophage reconstitution following fetal liver transplantation J Leukoc Biol 77 2005 173 180
32. J. Brett, A.M. Schmidt, S.D. Yan, Y.S. Zou, E. Weidman, D. Pinsky, and et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues Am J Pathol 143 1993 1699 1712
33. M. Hayakawa, H. Hayakawa, Y. Matsuyama, H. Tamemoto, H. Okazaki, and S. Tominaga Mature interleukin-33 is produced by calpain-mediated cleavage in vivo Biochem Biophys Res Commun 387 2009 218 222
34. E. Lefrancais, S. Roga, V. Gautier, A. Gonzalez-de-Peredo, B. Monsarrat, J.P. Girard, and et al. IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G Proc Natl Acad Sci U S A 109 2012 1673 1678
35. A.U. Luthi, S.P. Cullen, E.A. McNeela, P.J. Duriez, I.S. Afonina, C. Sheridan, and et al. Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases Immunity 31 2009 84 98
36. K.R. Bartemes, K. Iijima, T. Kobayashi, G.M. Kephart, A.N. McKenzie, and H. Kita 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
37. H. Kouzaki, K. Iijima, T. Kobayashi, S.M. O'Grady, and H. Kita The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses J Immunol 186 2011 4375 4387
38. R.J. Snelgrove, L.G. Gregory, T. Peiro, S. Akthar, G.A. Campbell, S.A. Walker, and et al. Alternaria-derived serine protease activity drives IL-33-mediated asthma exacerbations J Allergy Clin Immunol 134 2014 583 592.e6
39. H.K. Kim, S. Lund, R. Baum, P. Rosenthal, N. Khorram, and T.A. Doherty Innate type 2 response to Alternaria extract enhances ryegrass-induced lung inflammation Int Arch Allergy Immunol 163 2014 92 105
40. T.Y. Halim, C.A. Steer, L. Matha, M.J. Gold, I. Martinez-Gonzalez, K.M. McNagny, and 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
41. H. Fehrenbach, M. Kasper, T. Tschernig, M.S. Shearman, D. Schuh, and M. Muller Receptor for advanced glycation endproducts (RAGE) exhibits highly differential cellular and subcellular localisation in rat and human lung Cell Mol Biol (Noisy-le-grand) 44 1998 1147 1157
42. N. Demling, C. Ehrhardt, M. Kasper, M. Laue, L. Knels, and E.P. Rieber Promotion of cell adherence and spreading: a novel function of RAGE, the highly selective differentiation marker of human alveolar epithelial type I cells Cell Tissue Res 323 2006 475 488
43. K. Dahlin, E.M. Mager, L. Allen, Z. Tigue, L. Goodglick, M. Wadehra, and et al. Identification of genes differentially expressed in rat alveolar type I cells Am J Respir Cell Mol Biol 31 2004 309 316
44. C.S. Curran, and P.J. Bertics Human eosinophils express RAGE, produce RAGE ligands, exhibit PKC-delta phosphorylation and enhanced viability in response to the RAGE ligand, S100B Int Immunol 23 2011 713 728
45. E.M. Akirav, P. Preston-Hurlburt, J. Garyu, O. Henegariu, R. Clynes, A.M. Schmidt, and et al. RAGE expression in human T cells: a link between environmental factors and adaptive immune responses PLoS One 7 2012 e34698
46. A.B. Robinson, K.D. Johnson, B.G. Bennion, and P.R. Reynolds RAGE signaling by alveolar macrophages influences tobacco smoke-induced inflammation Am J Physiol Lung Cell Mol Physiol 302 2012 L1192 L1199
47. D.R. Neill, and A.N. McKenzie Nuocytes and beyond: new insights into helminth expulsion Trends Parasitol 27 2011 214 221
48. L.E. Hanford, C.L. Fattman, L.M. Shaefer, J.J. Enghild, Z. Valnickova, and T.D. Oury Regulation of receptor for advanced glycation end products during bleomycin-induced lung injury Am J Respir Cell Mol Biol 29 suppl 2003 S77 S81
49. K. Yasuda, T. Muto, T. Kawagoe, M. Matsumoto, Y. Sasaki, K. Matsushita, and et al. Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice Proc Natl Acad Sci U S A 109 2012 3451 3456
50. C.S. Hardman, V. Panova, and A.N. McKenzie IL-33 citrine reporter mice reveal the temporal and spatial expression of IL-33 during allergic lung inflammation Eur J Immunol 43 2013 488 498
51. A. Llop-Guevara, D.K. Chu, T.D. Walker, S. Goncharova, R. Fattouh, J.S. Silver, and et al. A GM-CSF/IL-33 pathway facilitates allergic airway responses to sub-threshold house dust mite exposure PLoS One 9 2014 e88714
52. M. Koval Sharing signals: connecting lung epithelial cells with gap junction channels Am J Physiol Lung Cell Mol Physiol 283 2002 L875 L893
53. B.E. Isakson, G.J. Seedorf, R.L. Lubman, W.H. Evans, and S. Boitano Cell-cell communication in heterocellular cultures of alveolar epithelial cells Am J Respir Cell Mol Biol 29 2003 552 561
54. S. Boitano, Z. Safdar, D.G. Welsh, J. Bhattacharya, and M. Koval Cell-cell interactions in regulating lung function Am J Physiol Lung Cell Mol Physiol 287 2004 L455 L459
55. K. Hara, K. Iijima, M.K. Elias, S. Seno, I. Tojima, T. Kobayashi, and et al. Airway uric acid is a sensor of inhaled protease allergens and initiates type 2 immune responses in respiratory mucosa J Immunol 192 2014 4032 4042
56. A.J. Halayko, and S. Ghavami S100A8/A9: a mediator of severe asthma pathogenesis and morbidity? Can J Physiol Pharmacol 87 2009 743 755
57. E.J. Shim, E. Chun, H.S. Lee, B.R. Bang, T.W. Kim, S.H. Cho, and et al. The role of high-mobility group box-1 (HMGB1) in the pathogenesis of asthma Clin Exp Allergy 42 2012 958 965
58. E. Abraham, J. Arcaroli, A. Carmody, H. Wang, and K.J. Tracey HMG-1 as a mediator of acute lung inflammation J Immunol 165 2000 2950 2954
59. M. Yu, H. Wang, A. Ding, D.T. Golenbock, E. Latz, C.J. Czura, and et al. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2 Shock 26 2006 174 179
60. P.S. Milutinovic, J.M. Englert, L.T. Crum, N.S. Mason, L. Ramsgaard, J.J. Enghild, and et al. Clearance kinetics and matrix binding partners of the receptor for advanced glycation end products PLoS One 9 2014 e88259
61. T. Chavakis, A. Bierhaus, N. Al-Fakhri, D. Schneider, S. Witte, T. Linn, and et al. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: a novel pathway for inflammatory cell recruitment J Exp Med 198 2003 1507 1515
62. K.L. Cepek, S.K. Shaw, C.M. Parker, G.J. Russell, J.S. Morrow, D.L. Rimm, and et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin Nature 372 1994 190 193
63. G. Gorfu, J. Rivera-Nieves, and K. Ley Role of beta7 integrins in intestinal lymphocyte homing and retention Curr Mol Med 9 2009 836 850
64. M.P. Schon, A. Arya, E.A. Murphy, C.M. Adams, U.G. Strauch, W.W. Agace, and et al. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice J Immunol 162 1999 6641 6649
65. B. Liliensiek, M.A. Weigand, A. Bierhaus, W. Nicklas, M. Kasper, S. Hofer, and et al. Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response J Clin Invest 113 2004 1641 1650
66. Y. Yamamoto, A. Harashima, H. Saito, K. Tsuneyama, S. Munesue, S. Motoyoshi, and et al. Septic shock is associated with receptor for advanced glycation end products ligation of LPS J Immunol 186 2011 3248 3257
67. A.M. Schmidt, O. Hori, J.X. Chen, J.F. Li, J. Crandall, J. Zhang, and et al. Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes J Clin Invest 96 1995 1395 1403
68. N. Braach, D. Frommhold, K. Buschmann, J. Pflaum, L. Koch, H. Hudalla, and et al. RAGE controls activation and anti-inflammatory signalling of protein C PLoS One 9 2014 e89422
69. D. Frommhold, A. Kamphues, S. Dannenberg, K. Buschmann, V. Zablotskaya, R. Tschada, and et al. RAGE and ICAM-1 differentially control leukocyte recruitment during acute inflammation in a stimulus-dependent manner BMC Immunol 12 2011 56
70. D. Frommhold, A. Kamphues, I. Hepper, M. Pruenster, I.K. Lukic, I. Socher, and et al. RAGE and ICAM-1 cooperate in mediating leukocyte recruitment during acute inflammation in vivo Blood 116 2010 841 849
71. A.S. Mirchandani, A.G. Besnard, E. Yip, C. Scott, C.C. Bain, V. Cerovic, and et al. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses J Immunol 192 2014 2442 2448
72. S.T. Scanlon, and A.N. McKenzie The messenger between worlds: the regulation of innate and adaptive type-2 immunity by innate lymphoid cells Clin Exp Allergy 45 2015 9 20
73. C.A. Christianson, N.P. Goplen, I. Zafar, C. Irvin, J.T. Good Jr., D.R. Rollins, and et al. Persistence of asthma requires multiple feedback circuits involving type 2 innate lymphoid cells and IL-33 J Allergy Clin Immunol 136 2015 59 68.e14