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

Dimitrii Pogorelov, Sebastian Felix Nepomuk Bode, Xin He, Javier Ramiro-Garcia, Fanny Hedin, Wim Ammerlaan, Maria Konstantinou, Christophe M. Capelle, Ni Zeng, Aurélie Poli, Olivia Domingues, Guillem Montamat, Oliver Hunewald, Séverine Ciré, Alexandre Baron, Joseph Longworth, Agnieszka Demczuk, Murilo Luiz Bazon, Ingrid Casper, Ludger Klimek, Lorie Neuberger-Castillo, Dominique Revets, Lea Guyonnet, Sylvie Delhalle, Jacques Zimmer, Vladimir Benes, Françoise Codreanu-Morel, Christiane Lehners-Weber, Ilse Weets, Pinar Alper, Dirk Brenner, Jan Gutermuth, Coralie Guerin, Martine Morisset, François Hentges, Reinhard Schneider, Mohamed H. Shamji, Fay Betsou, Paul Wilmes, Enrico Glaab, Antonio Cosma, Jorge Goncalves, Feng Q. Hefeng () and Markus Ollert ()
Additional contact information
Dimitrii Pogorelov: Luxembourg Institute of Health (LIH)
Sebastian Felix Nepomuk Bode: Luxembourg Institute of Health (LIH)
Xin He: University of Luxembourg
Javier Ramiro-Garcia: University of Luxembourg
Fanny Hedin: Luxembourg Institute of Health
Wim Ammerlaan: Luxembourg Institute of Health
Maria Konstantinou: Luxembourg Institute of Health
Christophe M. Capelle: Luxembourg Institute of Health (LIH)
Ni Zeng: Luxembourg Institute of Health (LIH)
Aurélie Poli: Luxembourg Institute of Health (LIH)
Olivia Domingues: Luxembourg Institute of Health (LIH)
Guillem Montamat: Luxembourg Institute of Health (LIH)
Oliver Hunewald: Luxembourg Institute of Health (LIH)
Séverine Ciré: Luxembourg Institute of Health (LIH)
Alexandre Baron: Luxembourg Institute of Health (LIH)
Joseph Longworth: Luxembourg Institute of Health (LIH)
Agnieszka Demczuk: Luxembourg Institute of Health (LIH)
Murilo Luiz Bazon: Luxembourg Institute of Health (LIH)
Ingrid Casper: Center for Rhinology and Allergology
Ludger Klimek: Center for Rhinology and Allergology
Lorie Neuberger-Castillo: Luxembourg Institute of Health
Dominique Revets: Luxembourg Institute of Health
Lea Guyonnet: Luxembourg Institute of Health (LIH)
Sylvie Delhalle: Luxembourg Institute of Health (LIH)
Jacques Zimmer: Luxembourg Institute of Health (LIH)
Vladimir Benes: European Molecular Biology Laboratory
Françoise Codreanu-Morel: Centre Hospitalier de Luxembourg
Christiane Lehners-Weber: Centre Hospitalier de Luxembourg
Ilse Weets: Universitair Ziekenhuis Brussel
Pinar Alper: University of Luxembourg
Dirk Brenner: Luxembourg Institute of Health (LIH)
Jan Gutermuth: Universitair Ziekenhuis Brussel
Coralie Guerin: Luxembourg Institute of Health (LIH)
Martine Morisset: Centre Hospitalier de Luxembourg
François Hentges: Centre Hospitalier de Luxembourg
Reinhard Schneider: University of Luxembourg
Mohamed H. Shamji: Imperial College London
Fay Betsou: Luxembourg Institute of Health
Paul Wilmes: University of Luxembourg
Enrico Glaab: University of Luxembourg
Antonio Cosma: Luxembourg Institute of Health
Jorge Goncalves: University of Luxembourg
Feng Q. Hefeng: Luxembourg Institute of Health (LIH)
Markus Ollert: Luxembourg Institute of Health (LIH)

Nature Communications, 2024, vol. 15, issue 1, 1-22

Abstract: 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. The primary outcome of this observational study is the comprehensive immunological cellular characterization during the AIT initiation phase, whereas the secondary outcomes are the serological and Th2-cell-type-specific transcriptomic analyses. Here we apply a multilayer-omics approach to reveal dynamic peripheral immune landscapes during the AIT-initiation phase in venom allergy patients (VAP) versus pollen-allergic and healthy controls. Already at baseline, VAP exhibit altered abundances of several cell types, including classical monocytes (cMono), CD4+ hybrid type 1-type 17 cells (Th1-Th17 or Th1/17) and CD8+ counterparts (Tc1-Tc17 or Tc1/17). At 8-24 h following AIT launch in VAP, we identify 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 occur. A disequilibrium between serum IL-6 and cMono in VAP baseline is restored at day seven following AIT launch. Our longitudinal analysis discovers molecular switches during initiation-phase insect-venom AIT that secure long-term outcomes. Trial number: NCT02931955.

Date: 2024
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DOI: 10.1038/s41467-024-54684-2

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