Innate and adaptive T cells in asthmatic patients: Relationship to severity and disease mechanisms

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 2, 2015, Pages 323-333

  Hinks, Timothy S C ^a,b   Zhou, Xiaoying ^a   Staples, Karl J ^a   Dimitrov, Borislav D ^a,b   Manta, Alexander ^c   Petrossian, Tanya ^d   Lum, Pek Y ^d   Smith, Caroline G ^a   Ward, Jon A ^a,b   Howarth, Peter H ^a,b   Walls, Andrew F ^a   Gadola, Stephan D ^a,e   Djukanović, Ratko ^a,b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

^c Ayasdi ^*  (Germany)

^d Ayasdi   (United States)

^e NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Asthma; cytokines; endotype; mast cells; mucosal associated invariant T cell; phenotype; regulatory T; T lymphocytes; TH17; TH2

Indexed keywords

CD4 ANTIGEN; CORTICOSTEROID; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; VITAMIN D; ANTIASTHMATIC AGENT; LYMPHOCYTE ANTIGEN RECEPTOR;

ADAPTIVE IMMUNITY; ADULT; AGED; ARTICLE; ASTHMA; BASOPHIL; BAYES THEOREM; BRONCHUS BIOPSY; CELL HETEROGENEITY; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DRUG MEGADOSE; ENDOBRONCHIAL BIOPSY; FEMALE; FLOW CYTOMETRY; GRANULOCYTE; HUMAN; INNATE IMMUNITY; LUNG LAVAGE; MAJOR CLINICAL STUDY; MALE; MAST CELL; MUCOSAL ASSOCIATED INVARIANT T LYMPHOCYTE; PATHOLOGY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPUTUM; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; ADOLESCENT; BRONCHOALVEOLAR LAVAGE FLUID; CASE CONTROL STUDY; CHEMISTRY; CYTOLOGY; GENE EXPRESSION; GENETICS; IMMUNOLOGY; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; TH2 CELL;

ADAPTIVE IMMUNITY; ADOLESCENT; ADRENAL CORTEX HORMONES; ADULT; AGED; ANTI-ASTHMATIC AGENTS; ASTHMA; BASOPHILS; BAYES THEOREM; BRONCHOALVEOLAR LAVAGE FLUID; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-13; MALE; MAST CELLS; MIDDLE AGED; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SEVERITY OF ILLNESS INDEX; SPUTUM; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TH2 CELLS;

EID: 84938513563     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.01.014     Document Type: Article

References (48)

1. T.R. Mosmann, H. Cherwinski, M.W. Bond, M.A. Giedlin, and R.L. Coffman Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins J Immunol 136 1986 2348 2357
2. P. Parronchi, D. Macchia, M.P. Piccinni, P. Biswas, C. Simonelli, E. Maggi, and et al. Allergen- and bacterial antigen-specific T-cell clones established from atopic donors show a different profile of cytokine production Proc Natl Acad Sci U S A 88 1991 4538 4542
3. D.S. Robinson, Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A.M. Bentley, and et al. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma N Engl J Med 326 1992 298 304
4. M. Azzawi, B. Bradley, P.K. Jeffery, A.J. Freq, A.J. Wardlaw, G. Knowles, and et al. Identification of activated T lymphocytes and eosinophils in bronchial biopsies in stable atopic asthma Am Rev Respir Dis 142 1990 1407 1413
5. S.E. Wenzel, L.B. Schwartz, E.L. Langmack, J.L. Halliday, J.B. Trudeau, R.L. Gibbs, and et al. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics Am J Respir Crit Care Med 160 1999 1001 1008
6. C.E. Brightling, P. Bradding, F.A. Symon, S.T. Holgate, A.J. Wardlaw, and I.D. Pavord Mast-cell infiltration of airway smooth muscle in asthma N Engl J Med 346 2002 1699 1705
7. J. Bousquet, P. Chanez, J.Y. Lacoste, G. Barneon, N. Ghavanian, I. Enander, and et al. Eosinophilic inflammation in asthma N Engl J Med 323 1990 1033 1039
8. G.P. Anderson Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease Lancet 372 2008 1107 1119
9. W.C. Moore, D.A. Meyers, S.E. Wenzel, W.G. Teague, H. Li, X. Li, and et al. Identification of asthma phenotypes using cluster analysis in the Severe Asthma Research Program Am J Respir Crit Care Med 181 2010 315 323
10. P. Haldar, I.D. Pavord, D.E. Shaw, M.A. Berry, M. Thomas, C.E. Brightling, and et al. Cluster analysis and clinical asthma phenotypes Am J Respir Crit Care Med 178 2008 218 224
11. J. Lotvall, C.A. Akdis, L.B. Bacharier, L. Bjermer, T.B. Casale, A. Custovic, and et al. Asthma endotypes: a new approach to classification of disease entities within the asthma syndrome J Allergy Clin Immunol 127 2011 355 360
12. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases J Immunol 155 1995 1151 1164
13. D.S. Robinson, M. Larche, and S.R. Durham Tregs and allergic disease J Clin Invest 114 2004 1389 1397
14. F. Fossiez, O. Djossou, P. Chomarat, L. Flores-Romo, S. Ait-Yahia, C. Maat, and et al. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines J Exp Med 183 1996 2593 2603
15. P. Vijayanand, G. Seumois, C. Pickard, R.M. Powell, G. Angco, D. Sammut, and et al. Invariant natural killer T cells in asthma and chronic obstructive pulmonary disease N Engl J Med 356 2007 1410 1422
16. S. Balzar, M.L. Fajt, S.A. Comhair, S.C. Erzurum, E. Bleecker, W.W. Busse, and 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 2011 299 309
17. R. Djukanovic, J.W. Wilson, K.M. Britten, S.J. Wilson, A.F. Walls, W.R. Roche, and et al. Quantitation of mast cells and eosinophils in the bronchial mucosa of symptomatic atopic asthmatics and healthy control subjects using immunohistochemistry Am Rev Respir Dis 142 1990 863 871
18. P.G. Gibson, N. Saltos, and T. Borgas Airway mast cells and eosinophils correlate with clinical severity and airway hyperresponsiveness in corticosteroid-treated asthma J Allergy Clin Immunol 105 2000 752 759
19. M. Dusseaux, E. Martin, N. Serriari, I. Peguillet, V. Premel, D. Louis, and et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells Blood 117 2011 1250 1259
20. Global Initiative for Asthma (GIFA). Global strategy for asthma management and prevention 2012. Available at: http://www.ginasthma.org/. Accessed September 5, 2013.
21. P.Y. Lum, G. Singh, A. Lehman, T. Ishkanov, M. Vejdemo-Johansson, M. Alagappan, and et al. Extracting insights from the shape of complex data using topology Sci Rep 3 2013 1236
22. G. Carlsson Topology and data Bull Am Math Soc 46 2009 255 308
23. R. Djukanovic, P.J. Sterk, J.V. Fahy, and F.E. Hargreave Standardised methodology of sputum induction and processing Eur Respir J Suppl 37 2002 1s 2s
24. E. Mamessier, A. Nieves, A.M. Lorec, P. Dupuy, D. Pinot, C. Pinet, and et al. T-cell activation during exacerbations: a longitudinal study in refractory asthma Allergy 63 2008 1202 1210
25. D.N. Reshef, Y.A. Reshef, H.K. Finucane, S.R. Grossman, G. McVean, P.J. Turnbaugh, and et al. Detecting novel associations in large data sets Science 334 2011 1518 1524
26. J. Kearley, J.E. Barker, D.S. Robinson, and C.M. Lloyd Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+CD25+ regulatory T cells is interleukin 10 dependent J Exp Med 202 2005 1539 1547
27. E.F. Juniper, P.M. O'Byrne, P.J. Ferrie, D.R. King, and J.N. Roberts Measuring asthma control. Clinic questionnaire or daily diary? Am J Respir Crit Care Med 162 2000 1330 1334
28. J.L. Simpson, R. Scott, M.J. Boyle, and P.G. Gibson Inflammatory subtypes in asthma: assessment and identification using induced sputum Respirology 11 2006 54 61
29. W. Busse, J. Corren, B.Q. Lanier, M. McAlary, A. Fowler-Taylor, G.D. Cioppa, and et al. Omalizumab, anti-IgE recombinant humanized monoclonal antibody, for the treatment of severe allergic asthma J Allergy Clin Immunol 108 2001 184 190
30. P. Haldar, C.E. Brightling, B. Hargadon, S. Gupta, W. Monteiro, A. Sousa, and et al. Mepolizumab and exacerbations of refractory eosinophilic asthma N Engl J Med 360 2009 973 984
31. J. Corren, R.F. Lemanske, N.A. Hanania, P.E. Korenblat, M.V. Parsey, J.R. Arron, and et al. Lebrikizumab treatment in adults with asthma N Engl J Med 365 2011 1088 1098
32. G.G. Brusselle, T. Maes, and K.R. Bracke Eosinophils in the spotlight: eosinophilic airway inflammation in nonallergic asthma Nat Med 19 2013 977 979
33. K.J. Staples, T.S. Hinks, J.A. Ward, V. Gunn, C. Smith, and R. Djukanovic Phenotypic characterization of lung macrophages in asthmatic patients: overexpression of CCL17 J Allergy Clin Immunol 130 2012 1404 1412.e7
34. S.K. Saha, M.A. Berry, D. Parker, S. Siddiqui, A. Morgan, R. May, and et al. Increased sputum and bronchial biopsy IL-13 expression in severe asthma J Allergy Clin Immunol 121 2008 685 691
35. S. Balzar, H.W. Chu, M. Strand, and S. Wenzel Relationship of small airway chymase-positive mast cells and lung function in severe asthma Am J Respir Crit Care Med 171 2005 431 439
36. G. Garcia, A. Magnan, R. Chiron, C. Contin-Bordes, P. Berger, C. Taille, and et al. A proof-of-concept, randomized, controlled trial of omalizumab in patients with severe, difficult-to-control, nonatopic asthma Chest 144 2013 411 419
37. S. Molet, Q. Hamid, F. Davoine, E. Nutku, R. Taha, N. Page, and et al. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines J Allergy Clin Immunol 108 2001 430 438
38. D.M. Bullens, E. Truyen, L. Coteur, L. Couteur, E. Dilissen, P.W. Hellings, and et al. IL-17 mRNA in sputum of asthmatic patients: linking T cell driven inflammation and granulocytic influx? Respir Res 7 2006 135
39. W.W. Busse, S. Holgate, E. Kerwin, Y. Chon, J. Feng, J. Lin, and et al. Randomized, double-blind, placebo-controlled study of brodalumab, a human anti-IL-17 receptor monoclonal antibody, in moderate to severe asthma Am J Respir Crit Care Med 188 2013 1294 1302
40. L. McKinley, J.F. Alcorn, A. Peterson, R.B. Dupont, S. Kapadia, A. Logar, and et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice J Immunol 181 2008 4089 4097
41. J.D. Fontenot, M.A. Gavin, and A.Y. Rudensky Foxp3 programs the development and function of CD4+CD25+ regulatory T cells Nat Immunol 4 2003 330 336
42. L. Kjer-Nielsen, O. Patel, A.J. Corbett, J. Le Nours, B. Meehan, L. Liu, and et al. MR1 presents microbial vitamin B metabolites to MAIT cells Nature 49 2012 717 723
43. L. Brossay, M. Chioda, N. Burdin, Y. Koezuka, G. Casorati, P. Dellabona, and et al. CD1d-mediated recognition of an alpha-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution J Exp Med 188 1998 1521 1528
44. A. Meierovics, W.J. Yankelevich, and S.C. Cowley MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection Proc Natl Acad Sci U S A 110 2013 E3119 E3128
45. T.R. Talbot, T.V. Hartert, E. Mitchel, N.B. Halasa, P.G. Arbogast, K.A. Poehling, and et al. Asthma as a risk factor for invasive pneumococcal disease N Engl J Med 352 2005 2082 2090
46. P. Klemets, O. Lyytikainen, P. Ruutu, J. Ollgren, T. Kaijalainen, M. Leinonen, and et al. Risk of invasive pneumococcal infections among working age adults with asthma Thorax 65 2010 698 702
47. B.J. Green, S. Wiriyachaiporn, C. Grainge, G.B. Rogers, V. Kehagia, L. Lau, and et al. Potentially pathogenic airway bacteria and neutrophilic inflammation in treatment resistant severe asthma PLoS One 9 2014 e100645
48. C. Auffray, I.M. Adcock, K.F. Chung, R. Djukanovic, C. Pison, and P.J. Sterk An integrative systems biology approach to understanding pulmonary diseases Chest 137 2010 1410 1416