Abstract
Chemokine (C-C motif) ligand 17 (CCL17) is a pro-allergic factor: high CCL17 levels in cord blood (CB) precede later allergic predisposition. Short-chain fatty acid (SCFA) treatment during pregnancy has been shown to protect mouse pups against allergic diseases. The maternal microbial metabolome during pregnancy may affect fetal allergic immune responses. We therefore examined the associations between CB CCL17 and gut SCFA levels in healthy pregnant Japanese women. CB CCL17 serum levels at birth, and maternal non-specific IgE levels in maternal sera at 32 weeks of gestation were measured. Maternal stool samples were collected at 12 (n = 59) and 32 (n = 58) weeks of gestation for gut microbiota analysis, based on barcoded 16S rRNA sequencing and metabolite levels. The CB CCL17 levels correlated negatively with butyrate concentrations and positively with isobutyrate at 12 weeks; CB CCL17 correlated positively with valerate and lactate at 32 weeks. Similarly, butyrate levels correlated negatively with maternal non-specific IgE levels, whereas the lactate concentration correlated positively with IgE levels. At 32 weeks, the Shannon diversity index (SDI) of Firmicutes and Proteobacteria correlated negatively with CB CCL17 levels, while those of the total microbiota correlated positively with the CB CCL17 levels. These metabolites may alter fetal immune responses. This study provides the first link between maternal metabolites during pregnancy and the risk of allergic diseases in human offspring.
Highlights
Recent studies have revealed that allergies in infants begin in utero, and are influenced by maternal environmental factors during the pregnancy [1]; notably, a healthy microbiome during the prenatal period appears to be especially important in reducing the risks of asthma and allergic diseases [2]
The gestational ages of the neonates who were delivered by caesarean section (C-section) were 38 to 40 weeks, all analyzed mothers including C-section were healthy, we did not exclude the data from the participants of the C-section for the analyses
In addition to the role of the mother-baby vertical transmission of vaginal microbes at the moment of birth, our results suggest that maternal intestinal microbiota and Short-chain fatty acid (SCFA) during pregnancy may influence the offspring’s fetal allergic immune response
Summary
Recent studies have revealed that allergies in infants begin in utero, and are influenced by maternal environmental factors during the pregnancy [1]; notably, a healthy microbiome during the prenatal period appears to be especially important in reducing the risks of asthma and allergic diseases [2]. Maternal contact with farm animals and cats that exposes the mother to several microbial populations, during pregnancy, exert distinct effects on regulatory T (Treg) cells, the type-1 helper T cell (Th1)/type-2 helper T cell (Th2) ratio, and FoxP3 demethylation in the offspring [3], thereby influencing the expression of innate immune receptors at birth [4]. Thorburn et al found that the offspring of pregnant mice treated with SCFA acetates were protected against allergic disease through epigenetic effects: increase H4 acetylation in the FoxP3 promoter region, correlated with increased
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