T-cell responses during allergen-specific immunotherapy

Current Opinion in Allergy and Clinical Immunology

Volumn 12, Issue 1, 2012, Pages 1-6

  Maggi, Enrico ^a   Vultaggio, Alessandra ^a   Matucci, Andrea ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Allergy; Cytokines; Subcutaneous and sublingual immunotherapy; T effector and T regulatory cells

Indexed keywords

ALLERGEN; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA;

ANTIGEN SPECIFICITY; BRONCHITIS; DENDRITIC CELL; EFFECTOR CELL; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOTHERAPY; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT ALLERGY; REVIEW; SUBCUTANEOUS IMMUNOTHERAPY; SUBLINGUAL IMMUNOTHERAPY; TH2 CELL; UPREGULATION;

ADMINISTRATION, SUBLINGUAL; ALLERGENS; DESENSITIZATION, IMMUNOLOGIC; HUMANS; HYPERSENSITIVITY; INJECTIONS, SUBCUTANEOUS; T-LYMPHOCYTES, REGULATORY;

EID: 84857048300     PISSN: 15284050     EISSN: 14736322     Source Type: Journal    
DOI: 10.1097/ACI.0b013e32834ecc9a     Document Type: Review

References (69)

1. Maggi E. T-cell responses induced by allergen-specific immunotherapy. Clin Exp Immunol 2010; 161:10-18.
2. Vercelli D. Discovering susceptibility genes for asthma and allergy. Nat Rev Immunol 2008; 8:169-182. (Pubitemid 351323288)
3. Hammad H, Lambrecht BN. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol 2008; 8:193-204. (Pubitemid 351323293)
4. Trompette A, Divanovic S, Visintin A, et al. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 2009; 457:585-588.
5. Murugaiyan G, Mittal A, Weiner HL. Increased osteopontin expression in dendritic cells amplifies IL-17 production by CD4+ T cells in experimental autoimmune encephalomyelitis and in multiple sclerosis. J Immunol 2008; 181:7480-7488.
6. Annunziato F, Cosmi L, Santarlasci V, et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007; 204:1849-1861. (Pubitemid 47240944)
7. Cosmi L, De Palma R, Santarlasci V, et al. Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor. J Exp Med 2008; 205:1903-1916.
8. Oboki K, Ohno T, Saito H, Nakae S. Th17 and allergy. Allergol Int 2008; 57:121-134. (Pubitemid 351897666)
9. Cosmi L, Maggi L, Santarlasci V, et al. Demonstration of a small subset of human circulating memory CD161+CD4+ T cells that produce both IL-17A and IL-4. J Allergy Clin Immunol 2010; 125:222-230. An interesting insight into the plasticity of Th17 cells toward type 2 phenotype and on the role of such a novel subset in asthmatic patients.
10. Louten J, Boniface K, de Waal Malefyt R. Development and function of Th17 cells in health and disease. J Allergy Clin Immunol 2009; 123:1004-1011.
11. Shamji MH, Durham SR. Mechanisms of immunotherapy to aeroallergens. Allergy 2011; 41:1235-1246. A complete review on the main mechanisms induced by immunotherapy of allergy
12. Scadding G, Durham SR. Mechanisms of sublingual immunotherapy. Immunol Allergy Clin North Am 2011; 31:191-209. An interesting review on the main mechanisms induced by SLIT.
13. Calamita Z, Saconato H, Pela AB, Atallah AN. Efficacy of sublingual immunotherapy in asthma: systematic review of randomized clinical trials using the cochrane collaboration method. Allergy 2006; 61:1162-1172. (Pubitemid 44326350)
14. Penagos M, Passalacqua G, Compalati E, et al. Meta-analysis of the efficacy of sublingual immunotherapy in the treatment of allergic asthma in pediatric patients, 3 to 18 years of age. Chest 2008; 133:599-609. (Pubitemid 351367366)
15. Broide DH. Immunomodulation of allergic disease. Annu Rev Med 2009; 60:279-291.
16. Nieto A, Mazon A, Pamies R, et al. Sublingual immunotherapy for allergic respiratory diseases: an evaluation of meta-analyses. J Allergy Clin Immunol 2009; 124:157-161.
17. Röder E, Berger MY, de Groot H, van Wijk RG. Immunotherapy in children and adolescents with allergic rhinoconjunctivitis: a systematic review. Pediatr Allergy Immunol 2008; 19:197-207. (Pubitemid 351499173)
18. Compalati E, Passalacqua G, Bonini M, Canonica GW. The efficacy of sublingual immunotherapy for house dust mites respiratory allergy: results of a GA(2)LEN meta-analysis. Allergy 2009; 64:1570-1579
19. Calderon MA, Penagos M, Sheikh A, et al. Sublingual immunotherapy for allergic conjunctivitis: cochrane systematic review and meta-analysis. Clin Exp Allergy 2011; 41:1263-1272. The study gives new insights into the efficacy of SLIT in allergic conjunctivitis.
20. Gardner LM, O'Hehir RE, Rolland JM. High dose allergen stimulation of T cells from house dust mite-allergic subjects induces expansion of IFNgamma+ T cells, apoptosis of CD4+IL-4+ T cells and T cell anergy. Int Arch Allergy Immunol 2004; 133:1-13. (Pubitemid 38199394)
21. Antúnez C, Mayorga C, Corzo JL, et al. Two year follow-up of immunological response in mite-allergic children treated with sublingual immunotherapy: comparison with subcutaneous administration. Pediatr Allergy Immunol 2008; 19:210-218. (Pubitemid 351499165)
22. Rolland J, Gardner LM, O'Heir RE. Allergen-related approaches to immunotherapy. Pharmacol Ther 2009; 121:273-284.
23. Jutel M, Akdis CA. Immunological mechanisms of allergen-specific immunotherapy. Allergy 2011; 66:725-732. This review demonstrates that the mechanism of tolerance in SCIT is mainly due to Tr1 cells.
24. Guerra F, Carracedo J, Solana-Lara R, et al. TH2 lymphocytes from atopic patients treated with immunotherapy undergo rapid apoptosis after culture with specific allergens. J Allergy Clin Immunol 2001; 107:647-653. (Pubitemid 32397752)
25. Ciprandi G, Sormani MP, Filaci G, Fenoglio D. Carry-over effect on IFNgamma production induced by allergen-specific immunotherapy. Int Immunopharmacol 2008; 8:1622-1625.
26. Sel S, Wegmann M, Sel S, et al. Immunomodulatory effects of viral TLR ligands on experimental asthma depend on the additive effects of IL-12 and IL-10. J Immunol 2007; 178:7805-7813. (Pubitemid 46898052)
27. Wei W, Liu Y, Zhao Y, et al. Induction of CD4+CD25Foxp3+IL-10+ T cells in HDM-allergic asthmatic children with or without SIT. Int Arch Allergy Immunol 2010; 153:19-26. This study confirms an immunodeviating machanism during immunotherapy of asthma.
28. Rolinck-Werninghaus C, Kopp M, Liebke C, et al. Lack of detectable alterations in immune responses during sublingual immunotherapy in children with seasonal allergic rhinoconjunctivitis to grass pollen. Int Arch Allergy Immunol 2005; 136:134-141. (Pubitemid 40463237)
29. Radulovic S, Jacobson MR, Durham SR, Nouri-Aria KT. Grass pollen immunotherapy induces Foxp3-expressing CD4+ CD25+ cells in the nasal mucosa. J Allergy Clin Immunol 2009; 121:1467-1472.
30. Plewako H, Wosinska K, Arvidsson M, et al. Production of interleukin-12 by monocytes and interferon-gamma by natural killer cells in allergic patients during rush immunotherapy. Ann Allergy Asthma Immunol 2006; 97:464-468. (Pubitemid 44595093)
31. Alexander C, Tarzi M, Larché M, Kay AB. The effect of Fel d 1-derived T-cell peptides on upper and lower airway outcome measurements in cat-allergic subjects. Allergy 2005; 60:1269-1274. (Pubitemid 41297523)
32. Lloyd CM, Hawrylowicz CM. Regulatory T cells in asthma. Immunity 2009; 31:438-449.
33. Hall BM, Verma ND, Tran GT, Hodgkinson SJ. Distinct regulatory CD4(+)T cell subsets: differences between naive and antigen specific T regulatory cells. Curr Opin Immunol 2011; 23:641-647. This study shows that Treg cells are produced and adapt to the specific immune inflammatory environment they are activated in. Activated Tregs produce different molecules to mediate suppression which are tailored to the immune response they are activated by and control.
34. Meiler F, Zumkehr J, Klunker S, et al. In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J Exp Med 2008; 205:2887-2898.
35. Möbs C, Slotosch C, Löffler H, et al. Birch pollen immunotherapy leads to differential induction of regulatory T cells and delayed helper T cell immune deviation. J Immunol 2010; 184:2194-2203. The study shows that peripheral CD25+Foxp3+Treg cells were unchanged in birch pollen SIT compared with birch allergic controls.
36. Maggi L, Santarlasci V, Liotta F, et al. Demonstration of circulating allergenspecific CD4+CD25highFoxp3+ T-regulatory cells in both nonatopic and atopic individuals. J Allergy Clin Immunol 2007; 120:429-436. (Pubitemid 47411530)
37. Pfefferle PI, Sel S, Ege MJ, et al. PASTURE study group. Cord blood allergenspecific IgE is associated with reduced IFN-g production by cord blood cells: the protection against allergy-study in rural environments (PASTURE) study. J Allergy Clin Immunol 2008; 122:711-716.
38. Van Overtvelt L, Wambre E, Maillere B, et al. Assessment of Bet v 1-specific CD4-T cell responses in allergic and nonallergic individuals using MHC class II peptide tetramers. J Immunol 2008; 180:4514-4522.
39. Romagnani S. Coming back to a missing immune deviation as the main explanatory mechanism for the hygiene hypothesis. J Allergy Clin Immunol 2007; 119:1511-1513. (Pubitemid 46855874)
40. McKinstry KK, Strutt TM, Buck A, et al. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J Immunol 2009; 182:7353-7363.
41. Oida T, Xu L, Weiner HL, et al. TGF-beta-mediated suppression by CD4+CD25+ T cells is facilitated by CTLA-4 signaling. J Immunol 2006; 177:2331-2339. (Pubitemid 44200993)
42. James LK, Durham SR. Update on mechanisms of allergen injection immunotherapy. Clin Exp Allergy 2008; 38:1074-1088.
43. Allam JP, Duan Y, Winter J, et al. Tolerogenic T cells, Th1/Th17 cytokines and TLR2/TLR4 expressing dendritic cells predominate the microenvironment within distinct oral mucosal sites. Allergy 2011; 66:532-539. An interesting insight into the tolerogenic milieu of oral mucosal regions compared with skin.
44. Novak N, Bieber T, Allam J-P. Immunological mechanisms of sublingual allergen-specific immunotherapy. Allergy 2011; 66:733-739.
45. Piconi S, Trabattoni D, Rainone V, et al. Immunological effects of sublingual immunotherapy: clinical efficacy is associated with modulation of programmed cell death ligand 1, IL-10, and IgG4. J Immunol 2010; 185:7723-7730. Important study reporting the increased expression of tolerogenic signals induced by SLIT during the pollen season.
46. Savolainen J, Jacobsen L, Valovirta E. Sublingual immunotherapy in children modulates allergen-induced in vitro expression of cytokine mRNA in PBMC. Allergy 2006; 61:1184-1190. (Pubitemid 44326353)
47. Bohle B, Kinaciyan T, Gerstmayr M, et al. Sublingual immunotherapy induces IL-10-producing T regulatory cells, allergen-specific T-cell tolerance, and immune deviation. J Allergy Clin Immunol 2007; 120:707-713. (Pubitemid 47320765)
48. O'Hehir RE, Gardner LM, de Leon MP, et al. House dust mite sublingual immunotherapy: the role for transforming growth factor-beta and functional regulatory T cells. Am J Respir Crit Care Med 2009; 180:936-947.
49. Nieminen K, Valovirta E, Savolainen J. Clinical outcome and IL-17, IL-23, IL-27 and FOXP3 expression in peripheral blood mononuclear cells of pollenallergic children during sublingual immunotherapy. Pediatr Allergy Immunol 2010; 21:174-184. An important insight showing an inverse correlation between the IL-17A/IL-23 axis and the efficacy of SLIT.
50. Incorvaia C, Frati F, Puccinelli P, et al. Effects of sublingual immunotherapy on allergic inflammation. Inflamm Allergy Drug Targets 2008; 7:167-172.
51. Reefer AJ, Carneiro RM, Custis NJ, et al. A role for IL-10-mediated HLA-DR7-restricted T cell-dependent events in development of the modified Th2 response to cat allergen. J Immunol 2004; 172:2763-2772. (Pubitemid 38263659)
52. Worm M, Lee HH, Kleine-Tebbe J, et al. Development and preliminary clinical evaluation of a peptide immunotherapy vaccine for cat allergy. J Allergy Clin Immunol 2011; 127:89-97.
53. Moldaver D, Larchè M. Immunotherapy with peptides. Allergy 2011; 66:784-791.
54. Qian C, An H, Yu Y, et al. TLR agonists induce regulatory dendritic cells to recruit Th1 cells via preferential IP-10 secretion and inhibit Th1 proliferation. Blood 2007; 109:3308-3315. (Pubitemid 46572518)
55. Bozza S, Zelante T, Moretti S, et al. Lack of Toll IL-1R8 exacerbates Th17 cell responses in fungal infection. J Immunol 2008; 180:4022-4031.
56. Mamessier E, Birnbaum J, Dupuy P, et al. Ultra-rush venom immunotherapy induces differential T cell activation and regulatory patterns according to the severity of allergy. Clin Exp Allergy 2006; 36:704-713. (Pubitemid 43972965)
57. Jones SM, Pons L, Roberts JL, et al. Clinical efficacy and immune regulation with peanut oral immunotherapy. J Allergy Clin Immunol 2009; 124:292-300.
58. Cosmi L, Santarlasci V, Angeli R, et al. Sublingual immunotherapy with dermatophagoides monomeric allergoid down-regulates allergen-specific immunoglobulin E and increases both interferon-gamma- and interleukin 10-production. Clin Exp Allergy 2006; 36:261-272. (Pubitemid 43344707)
59. Stock P, Akbari O, Berry G, et al. Induction of T helper type 1-like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat Immunol 2004; 5:1149-1156. (Pubitemid 39549629)
60. Jankovic D, Kullberg MC, Feng CG, et al. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J Exp Med 2007; 204:273-283. (Pubitemid 46294544)
61. Trinchieri G. Interleukin-10 production by effector T cells: Th1 cells show self control. J Exp Med 2007; 204:239-243. (Pubitemid 46294539)
62. Häringer B, Lozza L, Steckel B, Geginat J. Identification and characterization of IL-10/IFN-gamma-producing effector-like T cells with regulatory function in human blood. J Exp Med 2009; 206:1009-1017.
63. Rutz S, Janke M, Kassner N, et al. Notch regulates IL-10 production by Thelper 1 cells. Proc Natl Acad Sci U S A 2008; 105:3497-3502. (Pubitemid 351723581)
64. Stumhofer JS, Silver JS, Laurence A, et al. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol 2007; 8:1363-1371. (Pubitemid 350131173)
65. Tsai YG, Yang KD, Niu DM, et al. TLR2 agonists enhance CD8+Foxp3+ regulatory T cells and suppress Th2 immune responses during allergen immunotherapy. J Immunol 2010; 184:7229-7237. The first demonstration that SLIT upregulates CD8+Foxp3+ Treg cells.
66. Vultaggio A, Nencini F, Pratesi S, et al. The TLR7 ligand 9-benzyl-2-butoxy-8-hydroxy adenine inhibits IL-17 response by eliciting IL-10 and IL-10-inducing cytokines. J Immunol 2011; 186:4707-4715. The study shows that a novel TLR7 agonist induces in vivo both IFN-g and IL-10, thus impairing the Th2 and Th17 responses toward allergen.
67. Lombardi V, Van Overtvelt L, Horiot S, et al. Toll-like receptor 2 agonist Pam3CSK4 enhances the induction of antigen-specific tolerance via the sublingual route. Clin Exp Allergy 2008; 38:1819-1829.
68. Schülke S, Burggraf M, Waibler Z, et al. Fusion protein of flagellin and ovalbumin suppresses the T(H)2 response and prevents murine intestinal allergy. J Allergy Clin Immunol 2011. [Epub ahead of print]
69. Creticos PS, Schroeder JT, Hamilton RG, et al. Immune Tolerance Network Group. Immunotherapy with a ragweed-Toll like receptor 9 agonist vaccine for allergic rhinitis. New Engl J Med 2006; 355:1445-1455. (Pubitemid 44511559)