Short-term subcutaneous grass pollen immunotherapy under the umbrella of anti-IL-4: A randomized controlled trial

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 2, 2016, Pages 452-461.e9

  Chaker, Adam M ^a,d,e   Shamji, Mohamed H ^a,b   Dumitru, Florentina A ^a   Calderon, Moises A ^a   Scadding, Guy W ^a   Makatsori, Melina ^a   Jones, Ieuan ^c,f   He, Qiuling A ^c   Subramanian, Kulandayan K ^c   Arm, Jonathan P ^c   Durham, Stephen R ^a,b   Schmidt Weber, Carsten B ^a,d  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Allergic rhinitis; anti IL 4; FluoroSpot; intradermal late phase response; subcutaneous allergen immunotherapy

Indexed keywords

ANTIALLERGIC AGENT; CHEMOKINE RECEPTOR CCR4; GRASS POLLEN EXTRACT; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G4; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 4 ANTIBODY; PLACEBO; UNCLASSIFIED DRUG; VAK 694; ALLERGEN; BIOLOGICAL MARKER; IL10 PROTEIN, HUMAN; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY;

ADULT; ARTICLE; CELL COUNT; CLINICAL ARTICLE; COMPARATIVE EFFECTIVENESS; CONNECTIVE TISSUE DISEASE; CONTROLLED STUDY; CYTOKINE RELEASE; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; EYE DISEASE; FEMALE; FLOW CYTOMETRY; GASTROINTESTINAL DISEASE; HEADACHE; HEMATOLOGIC DISEASE; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; INFECTION; INFESTATION; INJECTION SITE ERYTHEMA; INJECTION SITE PRURITUS; INJECTION SITE SWELLING; INJURY; INNER EAR DISEASE; INTOXICATION; LYMPHATIC SYSTEM DISEASE; MALE; MAXIMUM PLASMA CONCENTRATION; MENTAL DISEASE; MUSCULOSKELETAL DISEASE; POLLEN ALLERGY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RHINOPHARYNGITIS; SKIN DISEASE; SUBCUTANEOUS IMMUNOTHERAPY; T LYMPHOCYTE; THORAX DISEASE; ADVERSE EFFECTS; ANTAGONISTS AND INHIBITORS; BLOOD; CLINICAL TRIAL; DESENSITIZATION; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MULTIMODALITY CANCER THERAPY; PHASE 2 CLINICAL TRIAL; POACEAE; POLLEN; PROCEDURES; RHINITIS, ALLERGIC, SEASONAL; RISK FACTOR; SUBCUTANEOUS DRUG ADMINISTRATION; T LYMPHOCYTE SUBPOPULATION; TREATMENT OUTCOME; YOUNG ADULT;

ADULT; ALLERGENS; ANTIBODIES, MONOCLONAL; BIOMARKERS; COMBINED MODALITY THERAPY; DESENSITIZATION, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INJECTIONS, SUBCUTANEOUS; INTERLEUKIN-10; INTERLEUKIN-4; MALE; MIDDLE AGED; POACEAE; POLLEN; RHINITIS, ALLERGIC, SEASONAL; RISK FACTORS; T-LYMPHOCYTE SUBSETS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84957956465     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.08.046     Document Type: Article

References (39)

1. J. Bousquet, N. Khaltaev, A.A. Cruz, J. Denburg, W.J. Fokkens, A. Togias, and et al. Allergic Rhinitis and its Impact on Asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA(2)LEN and AllerGen) Allergy 63 suppl 86 2008 8 160
2. M.A. Calderon, B. Alves, M. Jacobson, B. Hurwitz, A. Sheikh, and S. Durham Allergen injection immunotherapy for seasonal allergic rhinitis Cochrane Database Syst Rev 1 2007 CD001936
3. S.R. Durham, S.M. Walker, E.M. Varga, M.R. Jacobson, F. O'Brien, W. Noble, and et al. Long-term clinical efficacy of grass-pollen immunotherapy N Engl J Med 341 1999 468 475
4. R. Shaaban, M. Zureik, D. Soussan, C. Neukirch, J. Heinrich, J. Sunyer, and et al. Rhinitis and onset of asthma: a longitudinal population-based study Lancet 372 2008 1049 1057
5. L. Jacobsen, B. Niggemann, S. Dreborg, H.A. Ferdousi, S. Halken, A. Høst, and et al. Specific immunotherapy has long-term preventive effect of seasonal and perennial asthma: 10-year follow-up on the PAT study Allergy 62 2007 943 948
6. L. Cosmi, F. Annunziato, M.I.G. Galli, R.M.E. Maggi, K. Nagata, S. Romagnani, and et al. CRTH2 is the most reliable marker for the detection of circulating human type 2 Th and type 2 T cytotoxic cells in health and disease Eur J Immunol 30 2000 2972 2979
7. C. Ebner, U. Siemann, B. Bohle, M. Willheim, U. Wiedermann, S. Schenk, and et al. Immunological changes during specific immunotherapy of grass pollen allergy: reduced lymphoproliferative responses to allergen and shift from TH2 to TH1 in T-cell clones specific for Phl p 1, a major grass pollen allergen Clin Exp Allergy 27 1997 1007 1015
8. Q.A. Hamid, E. Schotman, M.R. Jacobson, S.M. Walker, and S.R. Durham Increases in IL-12 messenger RNA+ cells accompany inhibition of allergen-induced late skin responses after successful grass pollen immunotherapy J Allergy Clin Immunol 99 1997 254 260
9. P.A. Wachholz, and S.R. Durham Induction of 'blocking' IgG antibodies during immunotherapy Clin Exp Allergy 33 2003 1171 1174
10. M. Jutel, M. Akdis, F. Budak, C. Aebischer-Casaulta, M. Wrzyszcz, K. Blaser, and et al. IL-10 and TGF-beta cooperate in the regulatory T cell response to mucosal allergens in normal immunity and specific immunotherapy Eur J Immunol 33 2003 1205 1214
11. D.S. Robinson, M. Larche, and S.R. Durham Tregs and allergic disease J Clin Invest 114 2004 1389 1397
12. C.A. Akdis, T. Blesken, M. Akdis, B. Wüthrich, and K. Blaser Role of interleukin 10 in specific immunotherapy J Clin Invest 102 1998 98 106
13. J.N. Francis, S.J. Till, and S.R. Durham Induction of IL-10+CD4+CD25+ T cells by grass pollen immunotherapy J Allergy Clin Immunol 111 2003 1255 1261
14. E.M. Ling, T. Smith, X.D. Nguyen, C. Pridgeon, M. Dallman, J. Arbery, and et al. Relation of CD4+CD25+ regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease Lancet 363 2004 608 615
15. S. Radulovic, M.R. Jacobson, S.R. Durham, and K.T. Nouri-Aria Grass pollen immunotherapy induces Foxp3-expressing CD4+ CD25+ cells in the nasal mucosa J Allergy Clin Immunol 121 2008 1467 1472.e1
16. E. Wambre, J.H. DeLong, E.A. James, N. Torres-Chinn, W. Pfützner, C. Möbs, and et al. Specific immunotherapy modifies allergen-specific CD4(+) T-cell responses in an epitope-dependent manner J Allergy Clin Immunol 133 2014 872 879.e7
17. L.K. James, M.H. Shamji, S.M. Walker, D.R. Wilson, P.A. Wachholz, J.N. Francis, and et al. Long-term tolerance after allergen immunotherapy is accompanied by selective persistence of blocking antibodies J Allergy Clin Immunol 127 2011 509 516 e1-5
18. M.H. Shamji, L.K. Wilcock, P.A. Wachholz, R.J. Dearman, I. Kimber, P.A. Wurtzen, and et al. The IgE-facilitated allergen binding (FAB) assay: validation of a novel flow-cytometric based method for the detection of inhibitory antibody responses J Immunol Methods 317 2006 71 79
19. K.T. Nouri-Aria, P.A. Wachholz, J.N. Francis, M.R. Jacobson, S.M. Walker, L.K. Wilcock, and et al. Grass pollen immunotherapy induces mucosal and peripheral IL-10 responses and blocking IgG activity J Immunol 172 2004 3252 3259
20. J.N. Francis, L.K. James, G. Paraskevopoulos, C. Wong, M.A. Calderon, S.R. Durham, and et al. Grass pollen immunotherapy: IL-10 induction and suppression of late responses precedes IgG4 inhibitory antibody activity J Allergy Clin Immunol 121 2008 1120 1125.e2
21. A. Strombeck, H. Rabe, A.C. Lundell, K. Andersson, S. Johansen, I. Adlerberth, and et al. High proportions of FOXP3(+) CD25(high) T cells in neonates are positively associated with allergic sensitization later in childhood Clin Exp Allergy 44 2014 940 952
22. L. Faustino, D. Mucida, A.C. Keller, J. Demengeot, K. Bortoluci, L.R. Sardinha, and et al. Regulatory T cells accumulate in the lung allergic inflammation and efficiently suppress T-cell proliferation but not Th2 cytokine production Clin Dev Immunol 2012 2012 721817
23. S. Burgler, P.Y. Mantel, C. Bassin, N. Ouaked, C.A. Akdis, C.B. Schmidt-Weber, and et al. RORC2 is involved in T cell polarization through interaction with the FOXP3 promoter J Immunol 184 2010 6161 6169
24. S. Burgler, N. Ouaked, C. Bassin, T.M. Basinski, P.Y. Mantel, K. Siegmund, and et al. Differentiation and functional analysis of human T(H)17 cells J Allergy Clin Immunol 123 2009 588 595 e1-7
25. P.Y. Mantel, H. Kuipers, O. Boyman, C. Rhyner, N. Ouaked, B. Rückert, and et al. GATA3-driven Th2 responses inhibit TGF-beta1-induced FOXP3 expression and the formation of regulatory T cells PLoS Biol 5 2007 e329
26. P.Y. Mantel, N. Ouaked, B. Rückert, C. Karagiannidis, R. Welz, K. Blaser, and et al. Molecular mechanisms underlying FOXP3 induction in human T cells J Immunol 176 2006 3593 3602
27. N. Ouaked, P.Y. Mantel, C. Bassin, S. Burgler, K. Siegmund, C.A. Akdis, and et al. Regulation of the foxp3 gene by the Th1 cytokines: the role of IL-27-induced STAT1 J Immunol 182 2009 1041 1049
28. Y. Kanno, G. Vahedi, K. Hirahara, K. Singleton, and J.J. O'Shea Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity Annu Rev Immunol 30 2012 707 731
29. B. Stott, P. Lavender, S. Lehmann, D. Pennino, S. Durham, C.B. Schmidt-Weber, and et al. Human IL-31 is induced by IL-4 and promotes TH2-driven inflammation J Allergy Clin Immunol 132 2013 446 454.e5
30. R.L. Coffman, J. Ohara, M.W. Bond, J. Carty, A. Zlotnik, and W.E. Paul B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells J Immunol 136 1986 4538 4541
31. R. Noelle, P.H. Krammer, J. Ohara, J.W. Uhr, E.S. Vitetta, and et al. Increased expression of Ia antigens on resting B cells: an additional role for B-cell growth factor Proc Natl Acad Sci U S A 81 1984 6149 6153
32. H. Gascan, J.F. Gauchat, M.G. Roncarolo, H. Yssel, H. Spits, and J.E. de Vries Human B cell clones can be induced to proliferate and to switch to IgE and IgG4 synthesis by interleukin 4 and a signal provided by activated CD4+ T cell clones J Exp Med 173 1991 747 750
33. T. Defrance, J.P. Aubry, F. Rousset, B. Vanbervliet, J.Y. Bonnefoy, N. Arai, and et al. Human recombinant interleukin 4 induces Fc epsilon receptors (CD23) on normal human B lymphocytes J Exp Med 165 1987 1459 1467
34. E. Alvarez-Cuesta, J. Bousquet, G.W. Canonica, S.R. Durham, H.J. Malling, E. Valovirta, and et al. Standards for practical allergen-specific immunotherapy Allergy 61 suppl 82 2006 1 20
35. M.T. Lima, D. Wilson, L. Pitkin, A. Roberts, K. Nouri-Aria, M. Jacobson, and et al. Grass pollen sublingual immunotherapy for seasonal rhinoconjunctivitis: a randomized controlled trial Clin Exp Allergy 32 2002 507 514
36. V.A. Varney, M. Gaga, A.J. Frew, V.R. Aber, A.B. Kay, and S.R. Durham Usefulness of immunotherapy in patients with severe summer hay fever uncontrolled by antiallergic drugs BMJ 302 1991 265 269
37. A.J. Frew, R.J. Powell, C.J. Corrigan, and S.R. Durham UK Immunotherapy Study Group. Efficacy and safety of specific immunotherapy with SQ allergen extract in treatment-resistant seasonal allergic rhinoconjunctivitis J Allergy Clin Immunol 117 2006 319 325
38. R. Quapp, N. Madsen, and L. Cameron Characterization of the promoter of human CRTh2, a prostaglandin D2 receptor Biochem Biophys Res Commun 363 2007 948 953
39. A.M. Crawley, A. Vranjkovic, C. Young, and J.B. Angel Interleukin-4 downregulates CD127 expression and activity on human thymocytes and mature CD8+ T cells Eur J Immunol 40 2010 1396 1407