Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp

ABSTRACT The maternal milk glycobiome is crucial for shaping the gut microbiota of infants. Although high core fucosylation catalyzed by fucosyltransferase 8 (Fut8) is a general feature of human milk glycoproteins, its role in the formation of a healthy microbiota has not been evaluated. In this stu...

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Autores principales: Ming Li, Yaqiang Bai, Jiaorui Zhou, Wei Huang, Jingyu Yan, Jia Tao, Qingjie Fan, Yang Liu, Di Mei, Qiulong Yan, Jieli Yuan, Patrice Malard, Zhongfu Wang, Jianguo Gu, Naoyuki Tanigchi, Wenzhe Li
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:ac86f877e6264314a9f7f9c1beadf8922021-11-15T15:55:26ZCore Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp10.1128/mBio.00128-192150-7511https://doaj.org/article/ac86f877e6264314a9f7f9c1beadf8922019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00128-19https://doaj.org/toc/2150-7511ABSTRACT The maternal milk glycobiome is crucial for shaping the gut microbiota of infants. Although high core fucosylation catalyzed by fucosyltransferase 8 (Fut8) is a general feature of human milk glycoproteins, its role in the formation of a healthy microbiota has not been evaluated. In this study, we found that the core-fucosylated N-glycans in milk of Chinese mothers selectively promoted the colonization of specific gut microbial groups, such as Bifidobacterium spp. and Lactobacillus spp. in their breast-fed infants during lactation. Compared with Fut8+/+ (WT) mouse-fed neonates, the offspring fed by Fut8+/− maternal mice had a distinct gut microbial profile, which was featured by a significant reduction of Lactobacillus spp., Bacteroides spp., and Bifidobacterium spp. and increased abundance of members of the Lachnospiraceae NK4A136 group and Akkermansia spp. Moreover, these offspring mice showed a lower proportion of splenic CD19+ CD69+ B lymphocytes and attenuated humoral immune responses upon ovalbumin (OVA) immunization. In vitro studies demonstrated that the chemically synthesized core-fucosylated oligosaccharides possessed the ability to promote the growth of tested Bifidobacterium and Lactobacillus strains in minimal medium. The resulting L-fucose metabolites, lactate and 1,2-propanediol, could promote the activation of B cells via the B cell receptor (BCR)-mediated signaling pathway. IMPORTANCE This study provides novel evidence for the critical role of maternal milk protein glycosylation in shaping early-life gut microbiota and promoting B cell activation of neonates. The special core-fucosylated oligosaccharides might be promising prebiotics for the personalized nutrition of infants.Ming LiYaqiang BaiJiaorui ZhouWei HuangJingyu YanJia TaoQingjie FanYang LiuDi MeiQiulong YanJieli YuanPatrice MalardZhongfu WangJianguo GuNaoyuki TanigchiWenzhe LiAmerican Society for MicrobiologyarticleB cellsBifidobacteriumLactobacilluscore fucosylationinfantsmilk N-glycanMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution DOAJ
collection DOAJ
language EN
topic B cells
Bifidobacterium
Lactobacillus
core fucosylation
infants
milk N-glycan
Microbiology
QR1-502
spellingShingle B cells
Bifidobacterium
Lactobacillus
core fucosylation
infants
milk N-glycan
Microbiology
QR1-502
Ming Li
Yaqiang Bai
Jiaorui Zhou
Wei Huang
Jingyu Yan
Jia Tao
Qingjie Fan
Yang Liu
Di Mei
Qiulong Yan
Jieli Yuan
Patrice Malard
Zhongfu Wang
Jianguo Gu
Naoyuki Tanigchi
Wenzhe Li
Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp
description ABSTRACT The maternal milk glycobiome is crucial for shaping the gut microbiota of infants. Although high core fucosylation catalyzed by fucosyltransferase 8 (Fut8) is a general feature of human milk glycoproteins, its role in the formation of a healthy microbiota has not been evaluated. In this study, we found that the core-fucosylated N-glycans in milk of Chinese mothers selectively promoted the colonization of specific gut microbial groups, such as Bifidobacterium spp. and Lactobacillus spp. in their breast-fed infants during lactation. Compared with Fut8+/+ (WT) mouse-fed neonates, the offspring fed by Fut8+/− maternal mice had a distinct gut microbial profile, which was featured by a significant reduction of Lactobacillus spp., Bacteroides spp., and Bifidobacterium spp. and increased abundance of members of the Lachnospiraceae NK4A136 group and Akkermansia spp. Moreover, these offspring mice showed a lower proportion of splenic CD19+ CD69+ B lymphocytes and attenuated humoral immune responses upon ovalbumin (OVA) immunization. In vitro studies demonstrated that the chemically synthesized core-fucosylated oligosaccharides possessed the ability to promote the growth of tested Bifidobacterium and Lactobacillus strains in minimal medium. The resulting L-fucose metabolites, lactate and 1,2-propanediol, could promote the activation of B cells via the B cell receptor (BCR)-mediated signaling pathway. IMPORTANCE This study provides novel evidence for the critical role of maternal milk protein glycosylation in shaping early-life gut microbiota and promoting B cell activation of neonates. The special core-fucosylated oligosaccharides might be promising prebiotics for the personalized nutrition of infants.
format article
author Ming Li
Yaqiang Bai
Jiaorui Zhou
Wei Huang
Jingyu Yan
Jia Tao
Qingjie Fan
Yang Liu
Di Mei
Qiulong Yan
Jieli Yuan
Patrice Malard
Zhongfu Wang
Jianguo Gu
Naoyuki Tanigchi
Wenzhe Li
author_facet Ming Li
Yaqiang Bai
Jiaorui Zhou
Wei Huang
Jingyu Yan
Jia Tao
Qingjie Fan
Yang Liu
Di Mei
Qiulong Yan
Jieli Yuan
Patrice Malard
Zhongfu Wang
Jianguo Gu
Naoyuki Tanigchi
Wenzhe Li
author_sort Ming Li
title Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp
title_short Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp
title_full Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp
title_fullStr Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp
title_full_unstemmed Core Fucosylation of Maternal Milk N-Glycan Evokes B Cell Activation by Selectively Promoting the <sc>l</sc>-Fucose Metabolism of Gut <italic toggle="yes">Bifidobacterium</italic> spp. and <italic toggle="yes">Lactobacillus</italic> spp
title_sort core fucosylation of maternal milk n-glycan evokes b cell activation by selectively promoting the <sc>l</sc>-fucose metabolism of gut <italic toggle="yes">bifidobacterium</italic> spp. and <italic toggle="yes">lactobacillus</italic> spp
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/ac86f877e6264314a9f7f9c1beadf892
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