Microbial ligand costimulation drives neutrophilic steroid-refractory asthma

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Hadebe, Sabelo ^a   Kirstein, Frank ^a   Fierens, Kaat ^b   Chen, Kong ^c   Drummond, Rebecca A ^a   Vautier, Simon ^a   Sajaniemi, Sara ^a   Murray, Graeme ^d   Williams, David L ^e   Redelinghuys, Pierre ^a   Reinhart, Todd A ^f   Junecko, Beth A Fallert ^f   Kolls, Jay K ^c   Lambrecht, Bart N ^b,g   Brombacher, Frank ^a   Brown, Gordon D ^a   Ryffel, Bernhard ^h  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b GHENT UNIVERSITY   (Belgium)

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

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e East Tennessee State University   (United States)

^f UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^g ERASMUS MEDICAL CENTER   (Netherlands)

^h French National Centre for Scientific Research   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; DECTIN 1; DEXAMETHASONE; HOUSE DUST ALLERGEN; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 4; STEROID;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CELL POLARITY; CONTROLLED STUDY; MOUSE; NONHUMAN; PATHOGENESIS; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; TH17 CELL; TH2 CELL; ANIMAL; DISEASE MODEL; DRUG RESISTANCE; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PYROGLYPHIDAE;

ANIMALS; ASTHMA; BETA-GLUCANS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; PYROGLYPHIDAE; STEROIDS; TH17 CELLS; TH2 CELLS;

EID: 84943167312     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134219     Document Type: Article

References (55)

1. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol. 2008; 8(3):183-92. Epub 2008/02/16. doi: nri2254 [pii] doi: 10.1038/nri2254 PMID: 18274560.
2. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N EnglJ Med. 2006; 355(21):2226-35. Epub 2006/11/25. doi: 355/21/2226 [pii] doi: 10.1056/NEJMra054308 PMID: 17124020.
3. Schaub B, Lauener R, von Mutius E. The many faces of the hygiene hypothesis. J Allergy Clin Immunol. 2006; 117(5):969-77; quiz 78. Epub 2006/05/06. doi:S0091-6749(06)00645-2 [pii] doi: 10.1016/j.jaci.2006.03.003 PMID: 16675321.
4. Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015; 16(1):45-56. doi: 10.1038/ni.3049 PMID: 25521684
5. Pearce N, Pekkanen J, Beasley R. How much asthma is really attributable to atopy? Thorax. 1999; 54 (3):268-72. Epub 1999/05/18. PMID: 10325905; PubMed Central PMCID: PMC1745435.
6. Anderson GP. Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet. 2008; 372(9643):1107-19. Epub 2008/09/23. doi:S0140-6736(08)61452-X [pii] doi: 10.1016/S0140-6736(08)61452-X PMID: 18805339.
7. Hammad H, Chieppa M, Perros F., Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med. 2009; 15(4):410-6. doi: http://www.nature.com/nm/journal/v15/n4/suppinfo/nm.1946S1.html. doi: 10.1038/nm.1946 PMID: 19330007
8. Simpson JL, Brooks C, Douwes J. Innate immunity in asthma. Paediatr Respir Rev. 2008; 9(4):263-70. Epub 2008/11/26. doi:S1526-0542(08)00042-0 [pii] doi: 10.1016/j.prrv.2008.05.007 PMID: 19026367.
9. Douwes J. (1 - >3)-Beta-D-glucans and respiratory health: a review of the scientific evidence. Indoor Air. 2005; 15(3):160-9. PMID: 15865616.
10. Nathan AT, Peterson EA, Chakir J, Wills-Karp M. Innate Immune Responses of Airway Epithelium to House Dust Mite Are Mediated through β-Glucan-Dependent Pathways. J Allergy Clin Immunol. 2009; 123(3):612-8. doi: 10.1016/j.jaci.2008.12.006 PMID: 19178937
11. Rylander R, Lin RH. (1 - >3)-beta-D-glucan - relationship to indoor air-related symptoms, allergy and asthma. Toxicology. 2000; 152(1-3):47-52. PMID: 11090939
12. Reed CE, Milton DK Endotoxin-stimulated innate immunity: A contributing factor for asthma. J Allergy Clin Immunol. 2001; 108(2):157-66. doi:10.1067/mai.2001.116862 PMID: 11496229.
13. Wilson RH, Whitehead GS, Nakano H, Free M.E., Kolls JK, Cook DN. Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am J Respir Crit Care Med. 2009; 180(8):720-30. Epub 2009/08/08. doi:200904-0573OC [pii] doi: 10.1164/rccm.200904-0573OC PMID: 19661246; PubMed Central PMCID: PMC2778149.
14. Bonlokke JH, Stridh G, Sigsgaard T, Kjaergaard SK, Lofsted H, Andersson K, et al. Upper-airway inflammation in relation to dust spiked with aldehydes or glucan. Scand J Work Environ Health. 2006; 32(5):374-82. Epub 2006/11/09. doi:1033 [pii]. PMID: 17091205.
15. Gerosa F, Baldani-Guerra B, Lyakh L.A., Batoni G., Esin S, Winkler-Pickett RT, et al. Differential regulation of interleukin 12 and interleukin 23 production in human dendritic cells. J Exp Med. 2008; 205:1447-61. PMID: 18490488. doi:10.1084/jem.20071450
16. Dennehy KM, Ferwerda G, Faro-Trindade I, Pyz E, Willment JA, Taylor PR, et al. Syk kinase is required for collaborative cytokine production induced through Dectin-1 and Toll-like receptors. Eur J Immunol. 2008; 38(2):500-6. PMID: 18200499. doi:10.1002/eji.200737741
17. Dennehy KM, Willment JA, Williams D.L., Brown GD. Reciprocal regulation of IL-23and IL-12 following co-activation of Dectin-1 and TLR signaling pathways. Eur J Immunol. 2009; 39(5):1379-86. Epub 2009/03/18. doi:10.1002/eji.200838543 PMID: 19291703.
18. Plantinga M, Guilliams M, Vanheerswynghels M., Deswarte K, Branco-Madeira F, Toussaint W, et al Conventional and Monocyte-Derived CD11b+ Dendritic Cells Initiate and Maintain T Helper 2 Cell-Mediated Immunity to House Dust Mite Allergen. Immunity. 2013; 38(2):322-35. doi: 10.1016/j.immuni.2012.10.016 PMID: 23352232
19. Ensley HE, Tobias B, Pretus H.A., McNamee RB, Jones EL, Browder IW, et al NMR spectral analysis of a water-insoluble (1 - >3)-beta-D-glucan isolated from Saccharomyces cerevisiae. Carbohydr Res. 1994; 258:307-11. Epub 1994/05/20. PMID: 8039185.
20. Kirstein F, Horsnell WG, Kuperman D.A., Huang X., Erle DJ, Lopata AL, et al. Expression of IL-4 receptor alpha on smooth muscle cells is not necessary for development of experimental allergic asthma. J Allergy Clin Immunol. 2010; 126(2):347-54. doi:10.1016/j.jaci.2010.04.028 PMID: 20579713; PubMed Central PMCID: PMC2917502.
21. Lambrecht BN, Salomon B, Klatzmann D, Pauwels RA. Dendritic cells are required for the development of chronic eosinophilic airway inflammation in response to inhaled antigen in sensitized mice. J Immunol. 1998; 160(8):4090-7. PMID: 9558120.
22. Fallert BA, Reinhart TA Improved detection of simian immunodeficiency virus RNA by in situ hybridization in fixed tissue sections: combined effects of temperatures fortissue fixation and probe hybridization. J Virol Methods. 2002; 99(1-2):23-32. PMID: 11684300.
23. Brown GD, Gordon S. Immune recognition: A new receptor for beta-glucans. Nature. 2001; 413 (6851):36-7.
24. Eisenbarth SC, Piggott DA, Huleatt J.W., Visintin I., Herrick CA, Bottomly K. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J Exp Med. 2002; 196(12):1645-51. PMID: 12486107; PubMed Central PMCID: PMC2196061.
25. LambrechtBN, Hammad H. The airway epithelium in asthma. Nat Med. 2012; 18(5):684-92. doi:10.1038/nm.2737 PMID: 22561832.
26. Gregory LG, Lloyd CM Orchestrating house dust mite-associated allergy in the lung. Trends Immunol. 2011; 32(9):402-11. doi:10.1016/j.it.2011.06.006 PMID: 21783420; PubMed Central PMCID: PMC3381841.
27. Zhao J, Lloyd CM, Noble A. Th17 responses in chronic allergic airway inflammation abrogate regulatory T-cell-mediated tolerance and contribute to airway remodeling. Mucosal Immunol. 2013; 6(2):335-46. doi:10.1038/mi.2012.76 PMID: 22892938.
28. Cates EC, Fattouh R, Wattie J., Inman MD, Goncharova S, Coyle AJ, et al. Intranasal exposure of mice to house dust mite elicits allergic airway inflammation via a GM-CSF-mediated mechanism. J Immunol. 2004; 173(10):6384-92. PMID: 15528378.
29. Jarjour NN, Erzurum SC, Bleecker ER, Calhoun WJ, Castro M, Comhair SA, et al. Severe asthma: lessons learned from the National Heart, Lung, and Blood Institute Severe Asthma Research Program. Am J RespirCritCare Med. 2012; 185(4):356-62. doi:10.1164/rccm.201107-1317PP PMID: 22095547; PubMed Central PMCID: PMC3297096.
30. Trinchieri G, Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat Rev Immunol. 2007; 7(3):179-90. PMID: 17318230.
31. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med. 2002; 347(12):869-77. doi:10.1056/NEJMoa020057 PMID: 12239255.
32. Moore WC, Hastie AT, Li X, Li H, Busse WW, Jarjour NN, et al. Sputum neutrophil counts are associated with more severe asthma phenotypes using cluster analysis. J Allergy Clin Immunol. 2014; 133 (6):1557-63e5. doi:10.1016/j.jaci.2013.10.011 PMID: 24332216; PubMed Central PMCID: PMC4040309.
33. Dong L, Li H, Wang S., Li Y. Different doses of lipopolysaccharides regulate the lung inflammation of asthmatic mice via TLR4 pathway in alveolar macrophages. J Asthma. 2009; 46(3):229-33. Epub 2009/04/18. doi:910511639 [pii] doi: 10.1080/02770900802610050 PMID: 19373628.
34. Porter PC, Lim DJ, Maskatia Z.K., Mak G, Tsai CL, Citardi MJ, et al. Airway surface mycosis in chronic TH2-associated airway disease. J Allergy Clin Immunol. 2014; 134(2):325-31. doi:10.1016/j.jaci.2014. 04.028 PMID: 24928648; PubMed Central PMCID: PMC4119856.
35. Thorn J, Beijer L, Rylander R. Effects after inhalation of (1 - >3)-beta-D-glucan in healthy humans. Mediators Inflamm. 2001; 10(4):173-8. PMID: 11577993.
36. Rosas M, Liddiard K, Kimberg M., Faro-Trindade I, McDonald JU, Williams D.L., et al. The induction of inflammation by dectin-1 in vivo is dependent on myeloid cell programming and the progression of phagocytosis. J Immunol. 2008; 181(5):3549-57. PMID: 18714028.
37. Goodridge HS, Reyes CN, Becker C.A., Katsumoto TR, Ma J, Wolf AJ, et al. Activation of the innate immune receptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature. 2011; 472(7344):471-5. Epub 2011/04/29. doi:nature10071 [pii] doi: 10.1038/nature10071 PMID: 21525931; PubMed Central PMCID: PMC3084546.
38. Drummond RA, Brown GD Signalling C-type lectins in antimicrobial immunity. PLoS Pathog. 2013; 9 (7):e1003417. Epub 2013/08/13. doi:10.1371/journal.ppat.1003417 PPATHOGENS-D-13-00632 [pii]. PMID: 23935480; PubMed Central PMCID: PMC3723563.
39. Cheng SC, Quintin J, Cramer R.A., Shepardson KM, Saeed S, Kumar V, et al. mTOR-and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014; 345 (6204):1250684. doi:10.1126/science.1250684 PMID: 25258083.
40. Laan M, Cui ZH, Hoshino H, Lotvall J., Sjostrand M, Gruenert DC, et al Neutrophil recruitment by human IL-17viaC-X-Cchemokine release in the airways. J Immunol. 1999; 162(4):2347-52. PMID: 9973514.
41. Fogli LK, Sundrud MS, Goel S, Bajwa S, Jensen K, Derudder E, et al. T cell-derived IL-17 mediates epithelial changes in the airway and drives pulmonary neutrophilia. J Immunol. 2013; 191(6):3100-11. doi:10.4049/jimmunol.1301360 PMID: 23966625; PubMed Central PMCID: PMC3822005.
42. McKinley L, Alcorn JF, Peterson A, Dupont R.B., Kapadia S, Logar A, et al. TH17cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol. 2008; 181 (6):4089-97. Epub 2008/09/05. doi:181/6/4089 [pii]. PMID: 18768865.
43. Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. RespirMed. 2010; 104(8):1131-7. doi:10.1016/j.rmed.2010.02.018 PMID: 20338742.
44. Newcomb DC, Peebles RS Jr. Th17-mediated inflammation in asthma. CurrOpin Immunol. 2013; 25 (6):755-60. doi: 10.1016/j.coi.2013.08.002 PMID: 24035139; PubMed Central PMCID: PMC3855890. doi: 10.1016/j.coi.2013.08.002 PMID: 24035139
45. Ano S, Morishima Y, Ishii Y., Yoh K, Yageta Y, Ohtsuka S., et al. Transcription factors GATA-3 and ROR-gammat are important for determining the phenotype of allergic airway inflammation in a murine model of asthma. J Immunol. 2013; 190(3):1056-65. doi:10.4049/jimmunol.1202386 PMID: 23293351.
46. Kudo M, Melton AC, Chen C, Engler MB, Huang KE, Ren X, et al. IL-17A produced by alphabetaT 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 PMID: 22388091; PubMed Central PMCID: PMC3321096.
47. Chakir J, Shannon J, Molet S, Fukakusa M, Elias J, Laviolette M, et al. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-beta, IL-11, IL-17, and type I and type III collagen expression. J Allergy Clin Immunol. 2003; 111(6):1293-8. PMID: 12789232.
48. Saad-El-Din Bessa S, Abo El-Magd GH, Mabrouk MM. Serum chemokines RANTES and monocyte chemoattractant protein-1 in Egyptian patients with atopic asthma: relationship to disease severity. Arch Med Res. 2012; 43(1):36-41. doi:10.1016/j.arcmed.2012.01.009 PMID: 22300682.
49. Pan ZZ, Parkyn L, Ray A., Ray P. Inducible lung-specific expression of RANTES: preferential recruitment of neutrophils. Am J Physiol Lung Cell Mol Physiol. 2000; 279(4):L658-66. PMID: 11000125.
50. Martin RA, Hodgkins SR, Dixon A.E., Poynter ME. Aligning mouse models of asthma to human endo-types of disease. Respirology. 2014; 19(6):823-33. doi:10.1111/resp.12315 PMID: 24811131; PubMed Central PMCID: PMC4107015.
51. O'Driscoll B.R., Hopkinson LC, Denning DW Mold sensitization is common amongst patients with severe asthma requiring multiple hospital admissions. BMC Pulm Med. 2005; 5:4. doi:10.1186/1471-2466-5-4 PMID: 15720706; PubMed Central PMCID: PMC550663.
52. Mintz-Cole R.A., Gibson AM, Bass S.A., Budelsky AL, Reponen T, Hershey GK. Dectin-1 and IL-17A suppress murine asthma induced by Aspergillus versicolor but not Cladosporium cladosporioides due to differences in beta-glucan surface exposure. J Immunol. 2012; 189(7):3609-17. doi:10.4049/jimmunol.1200589 PMID: 22962686; PubMed Central PMCID: PMC3470885.
53. Lilly LM, Gessner MA, Dunaway CW, Metz AE, Schwiebert L, Weaver CT, et al. The beta-glucan receptor dectin-1 promotes lung immunopathology during fungal allergy viaIL-22. J Immunol. 2012; 189 (7):3653-60. doi:10.4049/jimmunol.1201797 PMID: 22933634; PubMed Central PMCID: PMC3448838.
54. Mintz-Cole R.A., Brandt EB, Bass S.A., Gibson AM, Reponen T, Khurana Hershey GK. Surface availability of beta-glucans is critical determinant of host immune response to Cladosporium cladosporioides. J Allergy Clin Immunol. 2013; 132(1):159-69. doi:10.1016/j.jaci.2013.01.003 PMID: 23403046.
55. Allard JB, Rinaldi L, Wargo MJ, Allen G, Akira S, Uematsu S, et al. Th2 allergic immune response to inhaled fungal antigens is modulated by TLR-4-independent bacterial products. European journal of immunology. 2009; 39(3):776-88. Epub 2009/02/19. doi:10.1002/eji.200838932 PMID: 19224641; PubMed Central PMCID: PMC2750775.