Multiomics approaches disclose very-early molecular and cellular switches during insect-venom allergen-specific immunotherapy

Feng Hefeng*, Dimitrii Pogorelov, Sebastian Bode, Xin He, Javier Ramiro-Garcia, Fanny Hedin, Wim Ammerlaan, Maria Konstantinou, Christophe Capelle, Ni Zeng, Aurélie Poli, Olivia Domingues, Guillem Montamat, Oliver Hunewald, Séverine Cire, Alexandre Baron, Joseph Longworth, Lorie Neuberger-Castillo, Dominique Revets, Léa GuyonnetAgnieszka Demczuk, Sylvie Delhalle, Jacques Zimmer, Vladimir Benes, Françoise Codreanu-Morel, Christiane Lehners-Weber, Ilse Weets, Pinar Alper, Dirk Brenner, Jan Gutermuth, Coralie Guérin, Martine Morisset, François Hentges, Reinhard Schneider, Mohamed Shamji, Fay Betsou, Paul Wilmes, Enrico Glaab, Jorge Goncalves, Antonio Cosma, Markus Ollert

*Corresponding author for this work

Research output: Working paperPreprint

Abstract

Allergen-specific immunotherapy (AIT) induces immune tolerance, showing the highest success rate (>95%) for insect venom while a much lower chance for pollen allergy. However, the molecular switches leading to successful durable tolerance restoration remain elusive. Here we applied a multilayer-omics approach to reveal dynamic peripheral immune landscapes during AIT-initiation phase in venom allergy patients (VAP) versus pollen-allergic and healthy controls. Already at baseline, VAP exhibited altered abundances of several cell types, including antigen-presenting cells (APC) and hybrid types, especially pDC-mDC hybrids. At 8-24h following AIT launch in VAP, we identified a uniform AIT-elicited pulse of late-transitional/IL-10-producing B cells, IL-6 signaling within Th2 cells and non-inflammatory serum-IL-6 levels. Sequential induction of activation and survival protein markers also immediately occurred. A disequilibrium between serum IL-6 and APC in VAP baseline was restored at day seven following AIT launch. Our longitudinal analysis discovers molecular switches during initiation-phase insect-venom AIT that secure long-term outcomes.
Original languageEnglish
DOIs
Publication statusPublished - 22 Feb 2024

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