A mast cell-ILC2-Th9 pathway promotes lung inflammation in cystic fibrosis

Nature Communications

Volumn 8, Issue , 2017, Pages

  Moretti, Silvia ^a   Renga, Giorgia ^a   Oikonomou, Vasilis ^a   Galosi, Claudia ^a   Pariano, Marilena ^a   Iannitti, Rossana G ^a   Borghi, Monica ^a   Puccetti, Matteo ^a   De Zuani, Marco ^b   Pucillo, Carlo E ^b   Paolicelli, Giuseppe ^a   Zelante, Teresa ^a   Renauld, Jean Christophe ^c   Bereshchenko, Oxana ^a   Sportoletti, Paolo ^d   Lucidi, Vincenzina ^e   Russo, Maria Chiara ^f   Colombo, Carla ^f   Fiscarelli, Ersilia ^e   Lass Flörl, Cornelia ^g   Majo, Fabio ^e   Ricciotti, Gabriella ^e   Ellemunter, Helmut ^g   Ratclif, Luigi ^h   Talesa, Vincenzo Nicola ^a   Napolioni, Valerio ^a   Romani, Luigina ^a   more..

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITY OF UDINE   (Italy)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^d SANTA MARIA DELLA MISERICORDIA HOSPITAL   (Italy)

^e BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^f UNIVERSITY OF MILAN   (Italy)

^g INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^h Istituto Ospedale G Tatarella   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; IMATINIB; IMMUNOGLOBULIN E; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 22; INTERLEUKIN 33; INTERLEUKIN 7; INTERLEUKIN 9; STAT5 PROTEIN; STAT6 PROTEIN; TRANSCRIPTION FACTOR GATA 3; STEM CELL FACTOR RECEPTOR;

ALLERGY; ANTIBODY; CELLS AND CELL COMPONENTS; COLONIZATION; GENE EXPRESSION; IMMUNOASSAY; INHIBITION; MICROBIAL ACTIVITY; PATHOLOGY;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD25+ TYPE 2 INNATE LYMPHOID CELL; CD4+ T LYMPHOCYTE; CELL ISOLATION; COLONY FORMING UNIT; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; FUNGUS GROWTH; GENE EXPRESSION; GENE FREQUENCY; HAPLOTYPE; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG ASPERGILLOSIS; LUNG FUNCTION; LYMPHOCYTE ACTIVATION; LYMPHOID CELL; MALE; MAST CELL; MASTOCYTOSIS; MICROBIAL COLONIZATION; MOUSE; NONHUMAN; PNEUMONIA; POSITIVE FEEDBACK; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSEUDOAUTOSOMAL REGION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TH17 CELL; TH9 CELL; ADOLESCENT; ADULT; ANIMAL; C57BL MOUSE; CHILD; GENETICS; HELPER CELL; IMMUNOLOGY; INFANT; INNATE IMMUNITY; LUNG; LYMPHOCYTE; MIDDLE AGED; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; CHILD; CHILD, PRESCHOOL; CYSTIC FIBROSIS; FEMALE; HUMANS; IMMUNITY, INNATE; INFANT; INTERLEUKIN-9; LUNG; LYMPHOCYTES; MALE; MAST CELLS; MICE; MICE, INBRED C57BL; MIDDLE AGED; PROTO-ONCOGENE PROTEINS C-KIT; T-LYMPHOCYTES, HELPER-INDUCER; YOUNG ADULT;

EID: 85009460733     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14017     Document Type: Article

References (70)

1. Spits, H. , et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13, 145-149 (2013).
2. Roediger, B., Weninger, W. Group 2 innate lymphoid cells in the regulation of immune responses. Adv. Immunol. 125, 111-154 (2015).
3. Lund, S., Walford, H. H., Doherty, T. A. Type 2 innate lymphoid cells in allergic disease. Curr. Immunol. Rev. 9, 214-221 (2013).
4. Drake, L. Y., Kita, H. Group 2 innate lymphoid cells in the lung. Adv. Immunol. 124, 1-16 (2014).
5. 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).
6. Monticelli, L. A. , et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12, 1045-1054 (2011).
7. Morita, H. , et al. An interleukin-33-mast cell-interleukin-2 axis suppresses papain-induced allergic inflammation by promoting regulatory T cell numbers. Immunity 43, 175-186 (2015).
8. Turner, J. E. , et al. IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J. Exp. Med. 210, 2951-2965 (2013).
9. Wilhelm, C. , et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat. Immunol. 12, 1071-1077 (2011).
10. Stephens, G. L. , et al. IL-9 is a Th17-derived cytokine that limits pathogenic activity in organ-specific autoimmune disease. Eur. J. Immunol. 41, 952-962 (2011).
11. Lu, L. F. , et al. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442, 997-1002 (2006).
12. Godfraind, C. , et al. Intraepithelial infiltration by mast cells with both connective tissue-type and mucosal-type characteristics in gut, trachea, and kidneys of IL-9 transgenic mice. J. Immunol. 160, 3989-3996 (1998).
13. Galli, S. J., Grimbaldeston, M., Tsai, M. Immunomodulatory mast cells: negative, as well as positive, regulators of immunity. Nat. Rev. Immunol. 8, 478-486 (2008).
14. Hershko, A. Y. , et al. Mast cell interleukin-2 production contributes to suppression of chronic allergic dermatitis. Immunity 35, 562-571 (2011).
15. Chen, C. Y. , et al. Induction of interleukin-9-producing mucosal mast cells promotes susceptibility to IgE-mediated experimental food allergy. Immunity 43, 788-802 (2015).
16. Frossi, B. , et al. Single-cell dynamics of mast cell-CD4\+ CD25\+ regulatory T cell interactions. Eur. J. Immunol. 41, 1872-1882 (2011).
17. Cohen, T. S., Prince, A. Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat. Med. 18, 509-519 (2012).
18. Iannitti, R. G. , et al. Th17/Treg imbalance in murine cystic fibrosis is linked to indoleamine 2, 3-dioxygenase deficiency but corrected by kynurenines. Am. J. Respir. Crit. Care. Med. 187, 609-620 (2013).
19. Armstead, J., Morris, J., Denning, D. W. Multi-country estimate of different manifestations of aspergillosis in cystic fibrosis. PLoS ONE 9, e98502 (2014).
20. Jones, A. M., Horsley, A., Denning, D. W. What is the importance of classifying Aspergillus disease in cystic fibrosis patients? Expert Rev. Respir. Med. 8, 389-392 (2014).
21. Tan, C. , et al. Antigen-specific Th9 cells exhibit uniqueness in their kinetics of cytokine production and short retention at the inflammatory site. J. Immunol. 185, 6795-6801 (2010).
22. Moro, K. , et al. Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat. Immunol. 17, 76-86 (2016).
23. Taube, C. , et al. IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS ONE 6, e21799 (2011).
24. Harris, W. T. , et al. Myofibroblast differentiation and enhanced TGF-B signaling in cystic fibrosis lung disease. PLoS ONE 8, e70196 (2013).
25. Schmitz, J. , 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, 479-490 (2005).
26. Cohen, E. S. , et al. Oxidation of the alarmin IL-33 regulates ST2-dependent inflammation. Nat. Commun. 6, 8327 (2015).
27. Allard, J. B. , et al. Aspergillus fumigatus generates an enhanced Th2-biased immune response in mice with defective cystic fibrosis transmembrane conductance regulator. J. Immunol. 177, 5186-5194 (2006).
28. Zelante, T. , et al. CD103\+ dendritic cells control Th17 cell function in the lung. Cell Rep. 12, 1789-1801 (2015).
29. Bischoff, S. C. Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat. Rev. Immunol. 7, 93-104 (2007).
30. Kosanovic, D. , et al. Histological characterization of mast cell chymase in patients with pulmonary hypertension and chronic obstructive pulmonary disease. Pulm. Circ. 4, 128-136 (2014).
31. Andersson, C. K. , et al. Activated MCTC mast cells infiltrate diseased lung areas in cystic fibrosis and idiopathic pulmonary fibrosis. Respir. Res. 12, 139 (2011).
32. Sabatino, G. , et al. Impact of IL-9 and IL-33 in mast cells. J. Biol. Regul. Homeost. Agents 26, 577-586 (2012).
33. Hubeau, C. , et al. Dysregulation of IL-2 and IL-8 production in circulating T lymphocytes from young cystic fibrosis patients. Clin. Exp. Immunol. 135, 528-534 (2004).
34. Tiringer, K. , et al. Differential expression of IL-33 and HMGB1 in the lungs of stable cystic fibrosis patients. Eur. Respir. J. 44, 802-805 (2014).
35. Bonfield, T. L., Hodges, C. A., Cotton, C. U., Drumm, M. L. Absence of the cystic fibrosis transmembrane regulator (Cftr) from myeloid-derived cells slows resolution of inflammation and infection. J. Leukoc. Biol. 92, 1111-1122 (2012).
36. Aschard, H. , et al. Sex-specific effect of IL9 polymorphisms on lung function and polysensitization. Genes Immun. 10, 559-565 (2009).
37. Schuurhof, A. , et al. Interleukin-9 polymorphism in infants with respiratory syncytial virus infection: an opposite effect in boys and girls. Pediatr. Pulmonol. 45, 608-613 (2010).
38. 1000 Genomes Project Consortium. , et al. An integrated map of genetic variation from 1, 092 human genomes. Nature 491, 56-65 (2012).
39. Barnig, C. , et al. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Science Transl. Med. 5, 174ra126 (2013).
40. Bradding, P., Walls, A. F., Holgate, S. T. The role of the mast cell in the pathophysiology of asthma. J. Allergy Clin. Immunol. 117, 1277-1284 (2006).
41. Bankova, L. G., Dwyer, D. F., Liu, A. Y., Austen, K. F., Gurish, M. F. Maturation of mast cell progenitors to mucosal mast cells during allergic pulmonary inflammation in mice. Mucosal Immunol. 8, 596-606 (2015).
42. Brightling, C. E. , et al. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346, 1699-1705 (2002).
43. Erjefalt, J. S. Mast cells in human airways: the culprit? Eur. Respir. Rev. 23, 299-307 (2014).
44. Kaplan, M. H. Th9 cells: differentiation and disease. Immunol. Rev. 252, 104-115 (2013).
45. Noelle, R. J., Nowak, E. C. Cellular sources and immune functions of interleukin-9. Nat. Rev. Immunol. 10, 683-687 (2010).
46. Kearley, J. , et al. IL-9 governs allergen-induced mast cell numbers in the lung and chronic remodeling of the airways. Am. J. Respir. Crit. Care. Med. 183, 865-875 (2011).
47. Lora, J. M. , et al. FcepsilonRI-dependent gene expression in human mast cells is differentially controlled by T helper type 2 cytokines. J. Allergy Clin. Immunol. 112, 1119-1126 (2003).
48. McMillan, S. J., Xanthou, G., Lloyd, C. M. Manipulation of allergen-induced airway remodeling by treatment with anti-TGF-beta antibody: effect on the Smad signaling pathway. J. Immunol. 174, 5774-5780 (2005).
49. Brown, J. M., Swindle, E. J., Kushnir-Sukhov, N. M., Holian, A., Metcalfe, D. D. Silica-directed mast cell activation is enhanced by scavenger receptors. Am. J. Respir. Cell Mol. Biol. 36, 43-52 (2007).
50. Kleeberger, S. R., Seiden, J. E., Levitt, R. C., Zhang, L. Y. Mast cells modulate acute ozone-induced inflammation of the murine lung. Am. Rev. Respir. Dis. 148, 1284-1291 (1993).
51. O'Brien-Ladner, A. R., Wesselius, L. J., Stechschulte, D. J. Bleomycin injury of the lung in a mast-cell-deficient model. Agents. Actions. 39, 20-24 (1993).
52. Sehra, S. , et al. TH9 cells are required for tissue mast cell accumulation during allergic inflammation. J. Allergy Clin. Immunol. 136, 433-440 e431 (2015).
53. Sun, H. , et al. Tgf-beta downregulation of distinct chloride channels in cystic fibrosis-affected epithelia. PLoS ONE 9, e106842 (2014).
54. Drumm, M. L. , et al. Genetic modifiers of lung disease in cystic fibrosis. N. Engl. J. Med. 353, 1443-1453 (2005).
55. Goswami, R. , et al. STAT6-dependent regulation of Th9 development. J. Immunol. 188, 968-975 (2012).
56. Eller, K. , et al. IL-9 production by regulatory T cells recruits mast cells that are essential for regulatory T cell-induced immune suppression. J. Immunol. 186, 83-91 (2011).
57. Saluja, R., Khan, M., Church, M. K., Maurer, M. The role of IL-33 and mast cells in allergy and inflammation. Clin. Transl. Allergy 5, 33 (2015).
58. Roussel, L., Farias, R., Rousseau, S. IL-33 is expressed in epithelia from patients with cystic fibrosis and potentiates neutrophil recruitment. J. Allergy Clin. Immunol. 131, 913-916 (2013).
59. Hardman, C. S., Panova, V., McKenzie, A. N. IL-33 citrine reporter mice reveal the temporal and spatial expression of IL-33 during allergic lung inflammation. Eur. J. Immunol. 43, 488-498 (2013).
60. Chmiel, J. F., Konstan, M. W. Inflammation and anti-inflammatory therapies for cystic fibrosis. Clin. Chest Med. 28, 331-346 (2007).
61. del Fresno, C. , et al. Monocytes from cystic fibrosis patients are locked in an LPS tolerance state: down-regulation of TREM-1 as putative underlying mechanism. PLoS ONE 3, e2667 (2008).
62. Xiao, X. , et al. OX40 signaling favors the induction of TH9 cells and airway inflammation. Nat. Immunol. 13, 981-990 (2012).
63. Kreindler, J. L. , et al. Vitamin D3 attenuates Th2 responses to Aspergillus fumigatus mounted by CD4\+ T cells from cystic fibrosis patients with allergic bronchopulmonary aspergillosis. J. Clin. Invest. 120, 3242-3254 (2010).
64. Piliponsky, A. M. , et al. Mast cell-derived TNF can exacerbate mortality during severe bacterial infections in C57BL/6-KitW-sh/W-sh mice. Am. J. Pathol. 176, 926-938 (2010).
65. Lopes, J. P., Stylianou, M., Nilsson, G., Urban, C. F. Opportunistic pathogen Candida albicans elicits a temporal response in primary human mast cells. Sci. Rep. 5, 12287 (2015).
66. Balzar, S. , et al. Mast cell phenotype, location, and activation in severe asthma. Data from the Severe Asthma Research Program. Am. J. Respir. Crit. Care. Med. 183, 299-309 (2011).
67. Daniels, C. E. , et al. Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J. Clin. Invest. 114, 1308-1316 (2004).
68. Harness-Brumley, C. L., Elliott, A. C., Rosenbluth, D. B., Raghavan, D., Jain, R. Gender differences in outcomes of patients with cystic fibrosis. J. Women's Health 23, 1012-1020 (2014).
69. Zhou, L. , et al. Correction of lethal intestinal defect in a mouse model of cystic fibrosis by human CFTR. Science 266, 1705-1708 (1994).
70. Purcell, S. , et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).