Mechanisms of allergen-specific immunotherapy and immune tolerance to allergens

Abstract

Substantial progress in understanding mechanisms of immune regulation in allergy, asthma, autoimmune diseases, tumors, organ transplantation and chronic infections has led to a variety of targeted therapeutic approaches. Allergen-specific immunotherapy (AIT) has been used for 100 years as a desensitizing therapy for allergic diseases and represents the potentially curative and specific way of treatment. The mechanisms by which allergen-AIT has its mechanisms of action include the very early desensitization effects, modulation of T- and B-cell responses and related antibody isotypes as well as inhibition of migration of eosinophils, basophils and mast cells to tissues and release of their mediators. Regulatory T cells (Treg) have been identified as key regulators of immunological processes in peripheral tolerance to allergens. Skewing of allergen-specific effector T cells to a regulatory phenotype appears as a key event in the development of healthy immune response to allergens and successful outcome in AIT. Naturally occurring FoxP3(+) CD4(+)CD25(+) Treg cells and inducible type 1 Treg (Tr1) cells contribute to the control of allergen-specific immune responses in several major ways, which can be summarized as suppression of dendritic cells that support the generation of effector T cells; suppression of effector Th1, Th2 and Th17 cells; suppression of allergen-specific IgE, and induction of IgG4; suppression of mast cells, basophils and eosinophils and suppression of effector T cell migration to tissues. New strategies for immune intervention will likely include targeting of the molecular mechanisms of allergen tolerance and reciprocal regulation of effector and regulatory T cell subsets.

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    Nograles KE, Zaba LC, Shemer A, Fuentes-Duculan J, Cardinale I, Kikuchi T, et al. IL-22-producing “T22” T cells account for upregulated IL-22 in atopic dermatitis despite reduced IL-17-producing TH17 T cells. J Allergy Clin Immunol. 2009;123:1244-52.

    Not in our library10.1016/j.jaci.2009.03.041

95. 95.

    Akdis CA, Akdis M. Mechanisms and treatment of allergic disease in the big picture of regulatory T cells. J Allergy Clin Immunol. 2009;123:735-46.

    Not in our library10.1016/j.jaci.2009.02.030

96. 96.

    Akdis CA, Bachert C, Cingi C, Dykewicz MS, Hellings PW, Naclerio RM, et al. Endotypes and phenotypes of chronic rhinosinusitis: a PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol. 2013;131:1479-90.

    Not in our library10.1016/j.jaci.2013.02.036

97. 97.

    Rebane A, Akdis CA. MicroRNAs: essential players in the regulation of inflammation. J Allergy Clin Immunol. 2013;132:15-26.

    Not in our library10.1016/j.jaci.2013.04.011

98. 98.

    Nicodemus-Johnson J, Laxman B, Stern RK, Sudi J, Tierney CN, Norwick L, et al. Maternal asthma and microRNA regulation of soluble HLA-G in the airway. J Allergy Clin Immunol. 2013;131:1496-503.

    Not in our library10.1016/j.jaci.2013.01.037

99. 99.

    Lu TX, Rothenberg ME. Diagnostic, functional, and therapeutic roles of microRNA in allergic diseases. J Allergy Clin Immunol. 2013;132:3-13.

    Not in our library10.1016/j.jaci.2013.04.039

100. 100.

     Rebane A, Runnel T, Aab A, Maslovskaja J, Rückert B, Zimmermann M, et al. MicroRNA-146a alleviates chronic skin inflammation in atopic dermatitis through suppression of innate immune responses in keratinocytes. J Allergy Clin Immunol. 2014;134:836-47.

     Not in our library10.1016/j.jaci.2014.05.022

101. 101.

     Tarzi M, Klunker S, Texier C, Verhoef A, Stapel SO, Akdis CA, et al. Induction of interleukin-10 and suppressor of cytokine signalling-3 gene expression following peptide immunotherapy. Clin Exp Allergy. 2006;36:465-74.

     Not in our library10.1111/j.1365-2222.2006.02469.x

102. 102.

     Alexander C, Ying S, B Kay A, Larche M. Fel d 1-derived T cell peptide therapy induces recruitment of CD4+ CD25+; CD4+ interferon-gamma + T helper type 1 cells to sites of allergen-induced late-phase skin reactions in cat-allergic subjects. Clin Exp Allergy. 2005;35:52-8.

     Not in our library10.1111/j.1365-2222.2005.02143.x

103. 103.

     Woo HY, Kim YS, Kang NI, Chung WC, Song CH, Choi IW, et al. Mechanism for acute oral desensitization to antibiotics. Allergy. 2006;61:954-8.

     Not in our library10.1111/j.1398-9995.2006.01147.x

104. 104.

     Eberlein-Konig B, Ullmann S, Thomas P, Przybilla B. Tryptase and histamine release due to a sting challenge in bee venom allergic patients treated successfully or unsuccessfully with hyposensitization. Clin Exp Allergy. 1995;25:704-12.

     Not in our library10.1111/j.1365-2222.1995.tb00007.x

105. 105.

     Jutel M, Muller UR, Fricker M, Rihs S, Pichler WJ, Dahinden C. Influence of bee venom immunotherapy on degranulation and leukotriene generation in human blood basophils. Clin Exp Allergy. 1996;26:1112-8.

     Not in our library10.1111/j.1365-2222.1996.tb00496.x

106. 106.

     Plewako H, Wosinska K, Arvidsson M, Bjorkander J, Skov PS, Håkansson L, et al. Basophil interleukin 4 and interleukin 13 production is suppressed during the early phase of rush immunotherapy. Int Arch Allergy Immunol. 2006;141:346-53.

     Not in our library10.1159/000095461

107. 107.

     Jutel M, Akdis M, Akdis CA. Histamine, histamine receptors and their role in immune pathology. Clin Exp Allergy. 2009;39:1786-800.

     Not in our library10.1111/j.1365-2222.2009.03374.x

108. 108.

     Muller UR, Jutel M, Reimers A, Zumkehr J, Huber C, Kriegel C, et al. Clinical and immunologic effects of H1 antihistamine preventive medication during honeybee venom immunotherapy. J Allergy Clin Immunol. 2008;122:1001-7.

     Not in our library10.1016/j.jaci.2008.08.007

109. 109.

     Akdis CA, Simons FE. Histamine receptors are hot in immunopharmacology. Eur J Pharmacol. 2006;533:69-76.

     Not in our library10.1016/j.ejphar.2005.12.044

110. 110.

     Meiler F, Zumkehr J, Klunker S, Ruckert B, Akdis CA, Akdis M. In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J Exp Med. 2008;205:2887-98.

     Not in our library10.1084/jem.20080193

111. 111.

     Bussmann C, Xia J, Allam JP, Maintz L, Bieber T, Novak N. Early markers for protective mechanisms during rush venom immunotherapy. Allergy. 2010;65(12):1558-65.

     Not in our library10.1111/j.1398-9995.2010.02430.x

112. 112.

     Schmid JM, Wurtzen PA, Dahl R, Hoffmann HJ. Early improvement in basophil sensitivity predicts symptom relief with grass pollen immunotherapy. J Allergy Clin Immunol. 2014;134:741-4.

     Not in our library10.1016/j.jaci.2014.04.029

113. 113.

     Shamji MH, Layhadi JA, Scadding GW, Cheung DK, Calderon MA, Turka LA et al. Basophil expression of diamine oxidase: A novel biomarker of allergen immunotherapy response. J Allergy Clin Immunol 2014;Nov 22. Published online ahead of print. (doi:10.1016/j.jaci.2014.09.049)

     Not in our library10.1016/j.jaci.2014.09.049

114. 114.

     Crameri R, Rhyner C. Novel vaccines and adjuvants for allergen-specific immunotherapy. Curr Opin Immunol. 2006;18:761-8.

     Not in our library10.1016/j.coi.2006.09.001

115. 115.

     Senti G, Graf N, Haug S, Rüedi N, von Moos S, Sonderegger T, et al. Epicutaneous allergen administration as a novel method of allergen-specific immunotherapy. J Allergy Clin Immunol. 2009;124:997-1002.

     Not in our library10.1016/j.jaci.2009.07.019

116. 116.

     Allam JP, Wurtzen PA, Reinartz M, Winter J, Vrtala S, Chen KW, et al. Phl p 5 resorption in human oral mucosa leads to dose-dependent and time-dependent allergen binding by oral mucosal Langerhans cells, attenuates their maturation, and enhances their migratory and TGF-beta1 and IL-10-producing properties. J Allergy Clin Immunol. 2010;126:638-45.

     Not in our library10.1016/j.jaci.2010.04.039

117. 117.

     Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med. 2007;204:1757-64.

     Not in our library10.1084/jem.20070590

118. 118.

     Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M, Mora JR, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med. 2007;204:1775-85.

     Not in our library10.1084/jem.20070602

119. 119.

     McGuirk P, McCann C, Mills KH. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J Exp Med. 2002;195:221-31.

     Not in our library10.1084/jem.20011288

120. 120.

     Csoka B, Himer L, Selmeczy Z, Vizi ES, Pacher P, Ledent C, et al. Adenosine A2A receptor activation inhibits T helper 1 and T helper 2 cell development and effector function. FASEB J. 2008;22:3491-9.

     Not in our library10.1096/fj.08-107458

121. 121.

     Urry Z, Xystrakis E, Richards DF, McDonald J, Sattar Z, Cousins DJ, et al. Ligation of TLR9 induced on human IL-10-secreting Tregs by 1alpha,25-dihydroxyvitamin D3 abrogates regulatory function. J Clin Invest. 2009;119(2):387-98.

     Not in our library10.1172/jci32354

122. 122.

     Mucida D, Park Y, Kim G, Scott I, Kronenberg M, Cheroutre H. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317:256-60.

     Not in our library10.1126/science.1145697

123. 123.

     Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol. 2001;2:725-31.

     Not in our library10.1038/90667

124. 124.

     de Heer HJ, Hammad H, Soullie T, Hijdra D, Vos N, Willart MA, et al. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med. 2004;200:89-98.

     Not in our library10.1084/jem.20040035

125. 125.

     Leb VM, Jahn-Schmid B, Kueng HJ, Schmetterer KG, Haiderer D, Neunkirchner A, et al. Modulation of allergen-specific T-lymphocyte function by virus-like particles decorated with HLA class II molecules. J Allergy Clin Immunol. 2009;124:121-8.

     Not in our library10.1016/j.jaci.2009.04.008

126. 126.

     Schmitz N, Dietmeier K, Bauer M, Maudrich M, Utzinger S, Muntwiler S, et al. Displaying Fel d1 on virus-like particles prevents reactogenicity despite greatly enhanced immunogenicity: a novel therapy for cat allergy. J Exp Med. 2009;206:1941-55.

     Not in our library10.1084/jem.20090199

127. 127.

     Bartemes KR, Kephart GM, Fox SJ, Kita H. Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J Allergy Clin Immunol. 2014;134:671-8.

     Not in our library10.1016/j.jaci.2014.06.024

128. 128.

     Annunziato F, Romagnani C, Romagnani S. The 3 major types of innate and adaptive cell-mediated effector immunity. J Allergy Clin Immunol. 2014.

     Not in our library10.1016/j.jaci.2014.11.001

129. 129.

     Lao-Araya M, Steveling E, Scadding GW, Durham SR, Shamji MH. Seasonal increases in peripheral innate lymphoid type 2 cells are inhibited by subcutaneous grass pollen immunotherapy. J Allergy Clin Immunol. 2014;134:1193-5.

     Not in our library10.1016/j.jaci.2014.07.029

130. 130.

     Akdis CA, Akdis M, Blesken T, Wymann D, Alkan SS, Müller U, et al. Epitope specific T cell tolerance to phospholipase A2 in bee venom immunotherapy and recovery by IL-2 and IL-15 in vitro. J Clin Invest. 1996;98:1676-83.

     Not in our library10.1172/jci118963

131. 131.

     Akdis CA, Blesken T, Akdis M, Wuthrich B, Blaser K. Role of interleukin 10 in specific immunotherapy. J Clin Invest. 1998;102:98-106.

     Not in our library10.1172/jci2250

132. 132.

     Jutel M, Akdis M, Budak F, Aebischer-Casaulta C, Wrzyszcz M, Blaser K, 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. 2003;33:1205-14.

     Not in our library10.1002/eji.200322919

133. 133.

     Suarez-Fueyo A, Ramos T, Galan A, Jimeno L, Wurtzen PA, Marin A. Grass tablet sublingual immunotherapy downregulates the TH2 cytokine response followed by regulatory T-cell generation. J Allergy Clin Immunol. 2014;133:130-8.

     Not in our library10.1016/j.jaci.2013.09.043

134. 134.

     Francis JN, Till SJ, Durham SR. Induction of IL-10 + CD4 + CD25+ T cells by grass pollen immunotherapy. J Allergy Clin Immunol. 2003;111:1255-61.

     Not in our library10.1067/mai.2003.1570

135. 135.

     Akdis M, Blaser K, Akdis CA. T regulatory cells in allergy: novel concepts in the pathogenesis, prevention, and treatment of allergic diseases. J Allergy Clin Immunol. 2005;116:961-8.

     Not in our library10.1016/j.jaci.2005.09.004

136. 136.

     Ling EM, Smith T, Nguyen XD, Pridgeon C, Dallman M, Arbery J, 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. 2004;363:608-15.

     Not in our library10.1016/s0140-6736(04)15592-x

137. 137.

     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. 2008;121:1467-72.

     Not in our library10.1016/j.jaci.2008.03.013

138. 138.

     Aslam A, Chan H, Warrell DA, Misbah S, Ogg GS. Tracking antigen-specific T-cells during clinical tolerance induction in humans. PLoS One. 2010;5:e11028.

     Not in our library10.1371/journal.pone.0011028

139. 139.

     Campbell JD, Buckland KF, McMillan SJ, Kearley J, Oldfield WL, Stern LJ, et al. Peptide immunotherapy in allergic asthma generates IL-10-dependent immunological tolerance associated with linked epitope suppression. J Exp Med. 2009;: –.

     Not in our library10.1084/jem.20082901

140. 140.

     Tsai YG, Lai JC, Yang KD, Hung CH, Yeh YJ, Lin CY. Enhanced CD46-induced regulatory T cells suppress allergic inflammation after Dermatophagoides pteronyssinus-specific immunotherapy. J Allergy Clin Immunol. 2014;134:1206-9.

     Not in our library10.1016/j.jaci.2014.06.005

141. 141.

     Fox EM, Torrero MN, Evans H, Mitre E. Immunologic characterization of 3 murine regimens of allergen-specific immunotherapy. J Allergy Clin Immunol 2014; Oct 2. Published online ahead of print. (doi:10.1016/j.jaci.2014.07.052)

     Not in our library10.1016/j.jaci.2014.07.052

142. 142.

     Mauri C, Gray D, Mushtaq N, Londei M. Prevention of athritis by interleukin 10-producing B cells. J Exp Med. 2003;197:489-501.

     Not in our library10.1084/jem.20021293

143. 143.

     Akdis M, Verhagen J, Taylor A, Karamloo F, Karagiannidis C, Crameri R, et al. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J Exp Med. 2004;199:1567-75.

     Not in our library10.1084/jem.20032058

144. 144.

     Taylor A, Akdis M, Joss A, Akkoç T, Wenig R, Colonna M, et al. IL-10 inhibits CD28 and ICOS costimulations of T cells via src homology 2 domain-containing protein tyrosine phosphatase 1. J Allergy Clin Immunol. 2007;120:76-83.

     Not in our library10.1016/j.jaci.2007.04.004

145. 145.

     Taylor A, Verhagen J, Akkoc T, Wenig R, Flory E, Blaser K, et al. IL-10 suppresses CD2-mediated T cell activation via SHP-1. Mol Immunol. 2009;46(4):622-9.

     Not in our library10.1016/j.molimm.2008.07.031

146. 146.

     Akdis CA, Joss A, Akdis M, Faith A, Blaser K. A molecular basis for T cell suppression by IL-10: CD28-associated IL-10 receptor inhibits CD28 tyrosine phosphorylation and phosphatidylinositol 3-kinase binding. FASEB J. 2000;14:1666-8.

     Not in our library10.1096/fj.99-0874fje

147. 147.

     Oral HB, Kotenko SV, Yilmaz M, Mani O, Zumkehr J, Blaser K, et al. Regulation of T cells and cytokines by the interleukin-10 (IL-10)-family cytokines IL-19, IL-20, IL-22, IL-24 and IL-26. Eur J Immunol. 2006;36:380-8.

     Not in our library10.1002/eji.200425523

148. 148.

     de Waal MR, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med. 1991;174:1209-20.

     Not in our library10.1084/jem.174.5.1209

149. 149.

     Moore KW, de Waal MR, Coffman RL, O’Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001;19:683-765.

     Not in our library10.1146/annurev.immunol.19.1.683

150. 150.

     Ito S, Ansari P, Sakatsume M, Dickensheets H, Vazquez N, Donnelly RP, et al. Interleukin-10 inhibits expression of both interferon alpha- and interferon gamma- induced genes by suppressing tyrosine phosphorylation of STAT1. Blood. 1999;93:1456-63.

     Not in our library

151. 151.

     Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol. 1998;16:137-61.

     Not in our library10.1146/annurev.immunol.16.1.137

152. 152.

     Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, et al. Conversion of peripheral CD4 + CD25- naive T cells to CD4 + CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875-86.

     Not in our library10.1084/jem.20030152

153. 153.

     Huber S, Schramm C, Lehr HA, Mann A, Schmitt S, Becker C, et al. Cutting edge: TGF-beta signaling is required for the in vivo expansion and immunosuppressive capacity of regulatory CD4 + CD25+ T cells. J Immunol. 2004;173:6526-31.

     Not in our library10.4049/jimmunol.173.11.6526

154. 154.

     Klunker S, Chong MM, Mantel PY, Palomares O, Bassin C, Ziegler M, et al. Transcription factors RUNX1 and RUNX3 in the induction and suppressive function of Foxp3+ inducible regulatory T cells. J Exp Med. 2009;206:2701-15.

     Not in our library10.1084/jem.20090596

155. 155.

     Custovic A, Simpson BM, Simpson A, Hallam CL, Marolia H, Walsh D, et al. Current mite, cat, and dog allergen exposure, pet ownership, and sensitization to inhalant allergens in adults. J Allergy Clin Immunol. 2003;111:402-7.

     Not in our library10.1067/mai.2003.55

156. 156.

     Jartti T, Burmeister KA, Seroogy CM, Jennens-Clough ML, Tisler CJ, Salazar LP, et al. Association between CD4(+)CD25(high) T cells and atopy in children. J Allergy Clin Immunol. 2007;120:177-83.

     Not in our library10.1016/j.jaci.2007.03.008

157. 157.

     Maggi L, Santarlasci V, Liotta F, Frosali F, Angeli R, Cosmi L, et al. Demonstration of circulating allergen-specific CD4 + CD25highFoxp3+ T-regulatory cells in both nonatopic and atopic individuals. J Allergy Clin Immunol. 2007;120:429-36.

     Not in our library10.1016/j.jaci.2007.05.002

158. 158.

     Orihara K, Narita M, Tobe T, Akasawa A, Ohya Y, Matsumoto K, et al. Circulating Foxp3 + CD4+ cell numbers in atopic patients and healthy control subjects. J Allergy Clin Immunol. 2007;120:960-2.

     Not in our library10.1016/j.jaci.2007.05.036

159. 159.

     Karlsson MR, Rugtveit J, Brandtzaeg P. Allergen-responsive CD4 + CD25+ regulatory T cells in children who have outgrown cow’s milk allergy. J Exp Med. 2004;199:1679-88.

     Not in our library10.1084/jem.20032121

160. 160.

     Wambre E, DeLong JH, James EA, Torres-Chinn N, Pfützner W, Möbs C, et al. Specific immunotherapy modifies allergen-specific CD4(+) T-cell responses in an epitope-dependent manner. J Allergy Clin Immunol. 2014;133:872-9.

     Not in our library10.1016/j.jaci.2013.10.054

161. 161.

     Zaleska A, Eiwegger T, Soyer O, van de Veen W, Rhyner C, Soyka MB, et al. Immune regulation by intralymphatic immunotherapy with modular allergen translocation MAT vaccine. Allergy. 2014;69:1162-70.

     Not in our library10.1111/all.12461

162. 162.

     Gorelik M, Narisety SD, Guerrerio AL, Chichester KL, Keet CA, Bieneman AP, et al. Suppression of the immunologic response to peanut during immunotherapy is often transient. J Allergy Clin Immunol 2014; Dec 24. Published online ahead of print. (doi:10.1016/j.jaci.2014.11.010)

     Not in our library10.1016/j.jaci.2014.11.010

163. 163.

     Kucuksezer UC, Palomares O, Ruckert B, Jartti T, Puhakka T, Nandy A, et al. Triggering of specific Toll-like receptors and proinflammatory cytokines breaks allergen-specific T-cell tolerance in human tonsils and peripheral blood. J Allergy Clin Immunol. 2013;131:875-85.

     Not in our library10.1016/j.jaci.2012.10.051

164. 164.

     Palomares O, Rückert B, Jartti T, Kücüksezer UC, Puhakka T, Gomez E, et al. Induction and maintenance of allergen-specific FOXP3+ Treg cells in human tonsils as potential first-line organs of oral tolerance. J Allergy Clin Immunol. 2012;129:510-20.

     Not in our library10.1016/j.jaci.2011.09.031

165. 165.

     Jartti T, Palomares O, Waris M, Tastan O, Nieminen R, Puhakka T, et al. Distinct regulation of tonsillar immune response in virus infection. Allergy. 2014;69:658-67.

     Not in our library10.1111/all.12396

166. 166.

     van de Veen W, Stanic B, Yaman G, Wawrzyniak M, Söllner S, Akdis DG, et al. IgG4 production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immunol. 2013;131:1204-12.

     Not in our library10.1016/j.jaci.2013.01.014

167. 167.

     Stanic B, van de Veen W, Wirz OF, Rückert B, Morita H, Söllner S, et al. IL-10-overexpressing B cells regulate innate and adaptive immune responses. J Allergy Clin Immunol. 2014;135(3):771-780.e8.

     Not in our library10.1016/j.jaci.2014.07.041

168. 168.

     Van Ree R, Van Leeuwen WA, Dieges PH, Van Wijk RG, De Jong N, Brewczyski PZ, et al. Measurement of IgE antibodies against purified grass pollen allergens (Lol p 1, 2, 3 and 5) during immunotherapy. Clin Exp Allergy. 1997;27:68-74.

     Not in our library10.1111/j.1365-2222.1997.tb00674.x

169. 169.

     Gleich GJ, Zimmermann EM, Henderson LL, Yunginger JW. Effect of immunotherapy on immunoglobulin E and immunoglobulin G antibodies to ragweed antigens: a six-year prospective study. J Allergy Clin Immunol. 1982;70:261-71.

     Not in our library10.1016/0091-6749(82)90062-8

170. 170.

     Bousquet J, Maasch H, Martinot B, Hejjaoui A, Wahl R, Michel FB. Double-blind, placebo-controlled immunotherapy with mixed grass-pollen allergoids. II. Comparison between parameters assessing the efficacy of immunotherapy. J Allergy Clin Immunol. 1988;82:439-46.

     Not in our library10.1016/0091-6749(88)90017-6

171. 171.

     Golden DB, Meyers DA, Kagey-Sobotka A, Valentine MD, Lichtenstein LM. Clinical relevance of the venom-specific immunoglobulin G antibody level during immunotherapy. J Allergy Clin Immunol. 1982;69:489-93.

     Not in our library10.1016/0091-6749(82)90172-5

172. 172.

     Müller UR, Helbling A, Bischof M. Predictive value of venom-specific IgE, IgG and IgG subclass antibodies in patients on immunotherapy with honey bee venom. Allergy. 1989;44:412-8.

     Not in our library10.1111/j.1398-9995.1989.tb04172.x

173. 173.

     Jutel M, Jaeger L, Suck R, Meyer H, Fiebig H, Cromwell O. Allergen-specific immunotherapy with recombinant grass pollen allergens. J Allergy Clin Immunol. 2005;116:608-13.

     Not in our library10.1016/j.jaci.2005.06.004

174. 174.

     Reisinger J, Horak F, Pauli G, van Hage M, Cromwell O, König F, et al. Allergen-specific nasal IgG antibodies induced by vaccination with genetically modified allergens are associated with reduced nasal allergen sensitivity. J Allergy Clin Immunol. 2005;116:347-54.

     Not in our library10.1016/j.jaci.2005.04.003

175. 175.

     Wachholz PA, Durham SR. Mechanisms of immunotherapy: IgG revisited. Curr Opin Allergy Clin Immunol. 2004;4:313-8.

     Not in our library10.1097/01.all.0000136753.35948.c0

176. 176.

     Till SJ, Francis JN, Nouri-Aria K, Durham SR. Mechanisms of immunotherapy. J Allergy Clin Immunol. 2004;113:1025-34.

     Not in our library10.1016/j.jaci.2004.03.024

177. 177.

     Shamji MH, Francis JN, Wurtzen PA, Lund K, Durham SR, Till SJ. Cell-free detection of allergen-IgE cross-linking with immobilized phase CD23: inhibition by blocking antibody responses after immunotherapy. J Allergy Clin Immunol. 2013;132:1003-5.

     Not in our library10.1016/j.jaci.2013.05.025

178. 178.

     Aalberse RC, Schuurman J. IgG4 breaking the rules. Immunology. 2002;105:9-19.

     Not in our library10.1046/j.0019-2805.2001.01341.x

179. 179.

     van der Neut KM, Schuurman J, Losen M, Bleeker WK, Martínez-Martínez P, Vermeulen E, et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science. 2007;317:1554-7.

     Not in our library10.1126/science.1144603

180. 180.

     Meiler F, Klunker S, Zimmermann M, Akdis CA, Akdis M. Distinct regulation of IgE, IgG4 and IgA by T regulatory cells and toll-like receptors. Allergy. 2008;63:1455-63.

     Not in our library10.1111/j.1398-9995.2008.01774.x

181. 181.

     Radbruch A, Muehlinghaus G, Luger EO, Inamine A, Smith KG, Dörner T, et al. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol. 2006;6:741-50.

     Not in our library10.1038/nri1886

182. 182.

     Akdis CA, Akdis M. Mechanisms of immune tolerance to allergens: role of IL-10 and Tregs. J Clin Invest. 2014;124:4678-80.

     Not in our library10.1172/jci78891

Cited by papers we hold 4

• Mast Cell Desensitization in Allergen Immunotherapy · 2022
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• Targeting Mitochondrial-Derived Reactive Oxygen Species in T Cell-Mediated Autoimmune Diseases · 2021
  No notice
• Clinical efficacy of sublingual immunotherapy is associated with restoration of steady-state serum lipocalin 2 after SLIT: a pilot study · 2018
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• Endotype-driven treatment in chronic upper airway diseases · 2017
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