Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17

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 dur...

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Main Authors: Hiromi Tanabe, Kenichi Sakurai, Yumiko Nakanishi, Tamotsu Kato, Yohei Kawasaki, Taiji Nakano, Fumiya Yamaide, Naoko Taguchi-Atarashi, Yuki Shiko, Ikumi Takashima, Masahiro Watanabe, Shingo Ochiai, Hiroshi Ohno, Hideoki Fukuoka, Naoki Shimojo, Chisato Mori
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Nutrients
Subjects:
Online Access:https://www.mdpi.com/2072-6643/13/8/2837
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spelling doaj-3c76feb432224509a0a5e98f325031402021-08-26T14:11:08ZengMDPI AGNutrients2072-66432021-08-01132837283710.3390/nu13082837Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17Hiromi Tanabe0Kenichi Sakurai1Yumiko Nakanishi2Tamotsu Kato3Yohei Kawasaki4Taiji Nakano5Fumiya Yamaide6Naoko Taguchi-Atarashi7Yuki Shiko8Ikumi Takashima9Masahiro Watanabe10Shingo Ochiai11Hiroshi Ohno12Hideoki Fukuoka13Naoki Shimojo14Chisato Mori15Center for Preventive Medical Sciences, Chiba University, Chiba 263-8522, JapanCenter for Preventive Medical Sciences, Chiba University, Chiba 263-8522, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa 230-0045, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa 230-0045, JapanFaculty of Nursing, Japanese Red Cross College of Nursing, Tokyo 150-0012, JapanDepartment of Pediatrics, Graduate School of Medicine, Chiba University, Chiba 260-8670, JapanDepartment of Pediatrics, Graduate School of Medicine, Chiba University, Chiba 260-8670, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa 230-0045, JapanBiostatistics Section, Clinical Research Center, Chiba University Hospital, Chiba 260-8677, JapanData Science Office, Clinical Research Promotion Center, University of Tokyo Hospital, Tokyo 113-8655, JapanCenter for Preventive Medical Sciences, Chiba University, Chiba 263-8522, JapanDepartment of Bioenvironmental Medicine, Graduate School of Medicine, Chiba University, Chiba 260-8670, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa 230-0045, JapanCenter for Preventive Medical Sciences, Chiba University, Chiba 263-8522, JapanCenter for Preventive Medical Sciences, Chiba University, Chiba 263-8522, JapanCenter for Preventive Medical Sciences, Chiba University, Chiba 263-8522, JapanChemokine (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 (<i>n</i> = 59) and 32 (<i>n</i> = 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.https://www.mdpi.com/2072-6643/13/8/2837cord bloodCCL17/TARCmaternal gut microbiotashort-chain fatty acids
collection DOAJ
language English
format Article
sources DOAJ
author Hiromi Tanabe
Kenichi Sakurai
Yumiko Nakanishi
Tamotsu Kato
Yohei Kawasaki
Taiji Nakano
Fumiya Yamaide
Naoko Taguchi-Atarashi
Yuki Shiko
Ikumi Takashima
Masahiro Watanabe
Shingo Ochiai
Hiroshi Ohno
Hideoki Fukuoka
Naoki Shimojo
Chisato Mori
spellingShingle Hiromi Tanabe
Kenichi Sakurai
Yumiko Nakanishi
Tamotsu Kato
Yohei Kawasaki
Taiji Nakano
Fumiya Yamaide
Naoko Taguchi-Atarashi
Yuki Shiko
Ikumi Takashima
Masahiro Watanabe
Shingo Ochiai
Hiroshi Ohno
Hideoki Fukuoka
Naoki Shimojo
Chisato Mori
Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17
Nutrients
cord blood
CCL17/TARC
maternal gut microbiota
short-chain fatty acids
author_facet Hiromi Tanabe
Kenichi Sakurai
Yumiko Nakanishi
Tamotsu Kato
Yohei Kawasaki
Taiji Nakano
Fumiya Yamaide
Naoko Taguchi-Atarashi
Yuki Shiko
Ikumi Takashima
Masahiro Watanabe
Shingo Ochiai
Hiroshi Ohno
Hideoki Fukuoka
Naoki Shimojo
Chisato Mori
author_sort Hiromi Tanabe
title Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17
title_short Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17
title_full Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17
title_fullStr Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17
title_full_unstemmed Association of the Maternal Gut Microbiota/Metabolome with Cord Blood CCL17
title_sort association of the maternal gut microbiota/metabolome with cord blood ccl17
publisher MDPI AG
series Nutrients
issn 2072-6643
publishDate 2021-08-01
description 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 (<i>n</i> = 59) and 32 (<i>n</i> = 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.
topic cord blood
CCL17/TARC
maternal gut microbiota
short-chain fatty acids
url https://www.mdpi.com/2072-6643/13/8/2837
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