A probiotic has differential effects on allergic airway inflammation in A/J and C57BL/6 mice and is correlated with the gut microbiome

Willian R Ribeiro,Wothan Tavares-De-Lima,Niels Olsen Saraiva Câmara ,Caroline M Ferreira,Gilson Masahiro Murata ,Amanda R Crisma,Erasmo Garcia Mendes ,Rui Curi,Bruna Bizzarro,Anderson Sá-Nunes,Márcia Pinto Alves Mayer ,Ana Tada Fonseca Brasil Antiorio ,João Carlos Setúbal ,Flaviano S Martins,Mateus B Casaro,Fernando A Oliveira,Angélica T Vieira,Claudio Fukumori,Andrew Maltez Thomas ,Emmanuel Dias-Neto

doi:10.1186/s40168-021-01081-2

Abstract

The phenotypes of allergic airway diseases are influenced by the interplay between host genetics and the gut microbiota, which may be modulated by probiotics. We investigated the probiotic effects on allergic inflammation in A/J and C57BL/6 mice. C57BL/6 mice had increased gut microbiota diversity compared to A/J mice at baseline. Acetate producer probiotics differentially modulated and altered the genus abundance of specific bacteria, such as Akkermansia and Allistipes, in mouse strains. We induced airway inflammation followed by probiotic treatment and found that only A/J mice exhibited decreased inflammation, and the beneficial effects of probiotics in A/J mice were partially due to acetate production. To understand the relevance of microbial composition colonization in the development of allergic diseases, we implanted female C57BL/6 mice with A/J embryos to naturally modulate the microbial composition of A/J mice, which increased gut microbiota diversity and reduced eosinophilic inflammation in A/J. These data demonstrate the central importance of microbiota to allergic phenotype severity.3HgJewfMcf3oVqbgvbkYNZVideo

Highlights

Asthma is an airway inflammatory disease that exhibits quite heterogenous severity and treatment responsiveness, which are likely due to the diverse mechanisms underlying this disease
We investigated the role of specific probiotics in the two different hosts, A/J and C57BL/6 mice, and the relevance of the gut microbiota composition in experimental allergic disease
Preventive effects of oral Bifidobacterium longum 51A supplementation on OVA-induced allergic airway inflammation in A/J mice In a previous work, we showed that B. longum 51A is an important acetate producer which confers antiinflammatory effects on the host

Summary

Introduction

Asthma is an airway inflammatory disease that exhibits quite heterogenous severity and treatment responsiveness, which are likely due to the diverse mechanisms underlying this disease. An established approach to asthma treatment involves the categorization of patients into so-called phenotypes, which are defined by observable characteristics that result from a combination of hereditary and environmental influences [1]. Some researchers used different inbred strains of mice under the same controlled environments to estimate the influence of genetic background on the allergic airway inflammation phenotype [4,5,6]. These researchers observed that some mouse strains, such as A/J mice, showed greater eosinophilia after 24 h of a challenge with ovalbumin (OVA) than other mouse strains, such as C57BL/6 mice [7, 8]. Animal and clinical studies on the relevance of host genetics

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