Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner
The healthy growth of infants during early life is associated with lifelong consequences. Breastfeeding has positive impacts on reducing obesity risk, which is likely due to the varied components of breast milk, such as N-acetylneuraminic acid (Neu5Ac). However, the effect of breast milk Neu5Ac on i...
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-07-01
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| Series: | Metabolites |
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| Online Access: | https://www.mdpi.com/2218-1989/13/7/846 |
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| author | Runze Ouyang Sijia Zheng Xiaolin Wang Qi Li Juan Ding Xiao Ma Zhihong Zhuo Zhen Li Qi Xin Xin Lu Lina Zhou Zhigang Ren Surong Mei Xinyu Liu Guowang Xu |
| author_facet | Runze Ouyang Sijia Zheng Xiaolin Wang Qi Li Juan Ding Xiao Ma Zhihong Zhuo Zhen Li Qi Xin Xin Lu Lina Zhou Zhigang Ren Surong Mei Xinyu Liu Guowang Xu |
| author_sort | Runze Ouyang |
| collection | DOAJ |
| description | The healthy growth of infants during early life is associated with lifelong consequences. Breastfeeding has positive impacts on reducing obesity risk, which is likely due to the varied components of breast milk, such as N-acetylneuraminic acid (Neu5Ac). However, the effect of breast milk Neu5Ac on infant growth has not been well studied. In this study, targeted metabolomic and metagenomic analyses were performed to illustrate the association between breast milk Neu5Ac and infant growth. Results demonstrated that Neu5Ac was significantly abundant in breast milk from infants with low obesity risk in two independent Chinese cohorts. Neu5Ac from breast milk altered infant gut microbiota and bile acid metabolism, resulting in a distinct fecal bile acid profile in the high-Neu5Ac group, which was characterized by reduced levels of primary bile acids and elevated levels of secondary bile acids. Taurodeoxycholic acid 3-sulfate and taurochenodeoxycholic acid 3-sulfate were correlated with high breast milk Neu5Ac and low obesity risk in infants, and their associations with healthy growth were reproduced in mice colonized with infant-derived microbiota. <i>Parabacteroides</i> might be linked to bile acid metabolism and act as a mediator between Neu5Ac and infant growth. These results showed the gut microbiota-dependent crosstalk between breast milk Neu5Ac and infant growth. |
| first_indexed | 2024-03-11T00:51:10Z |
| format | Article |
| id | doaj.art-c67657582b154d59995674330c977713 |
| institution | Directory Open Access Journal |
| issn | 2218-1989 |
| language | English |
| last_indexed | 2024-03-11T00:51:10Z |
| publishDate | 2023-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Metabolites |
| spelling | doaj.art-c67657582b154d59995674330c9777132023-11-18T20:28:03ZengMDPI AGMetabolites2218-19892023-07-0113784610.3390/metabo13070846Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent MannerRunze Ouyang0Sijia Zheng1Xiaolin Wang2Qi Li3Juan Ding4Xiao Ma5Zhihong Zhuo6Zhen Li7Qi Xin8Xin Lu9Lina Zhou10Zhigang Ren11Surong Mei12Xinyu Liu13Guowang Xu14CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaDepartment of Quality Control, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, ChinaDepartment of Nursing, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, ChinaDepartment of Pediatric, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, ChinaDepartment of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, ChinaAcademy of Medical Sciences, Zhengzhou University, Zhengzhou 450052, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaDepartment of Infectious Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, ChinaState Key Laboratory of Environment Health (Incubation), Key Laboratory of Environment and Health, Ministry of Education, Key Laboratory of Environment and Health (Wuhan), Ministry of Environmental Protection, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaCAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, ChinaThe healthy growth of infants during early life is associated with lifelong consequences. Breastfeeding has positive impacts on reducing obesity risk, which is likely due to the varied components of breast milk, such as N-acetylneuraminic acid (Neu5Ac). However, the effect of breast milk Neu5Ac on infant growth has not been well studied. In this study, targeted metabolomic and metagenomic analyses were performed to illustrate the association between breast milk Neu5Ac and infant growth. Results demonstrated that Neu5Ac was significantly abundant in breast milk from infants with low obesity risk in two independent Chinese cohorts. Neu5Ac from breast milk altered infant gut microbiota and bile acid metabolism, resulting in a distinct fecal bile acid profile in the high-Neu5Ac group, which was characterized by reduced levels of primary bile acids and elevated levels of secondary bile acids. Taurodeoxycholic acid 3-sulfate and taurochenodeoxycholic acid 3-sulfate were correlated with high breast milk Neu5Ac and low obesity risk in infants, and their associations with healthy growth were reproduced in mice colonized with infant-derived microbiota. <i>Parabacteroides</i> might be linked to bile acid metabolism and act as a mediator between Neu5Ac and infant growth. These results showed the gut microbiota-dependent crosstalk between breast milk Neu5Ac and infant growth.https://www.mdpi.com/2218-1989/13/7/846breast milkN-acetylneuraminic acidgut microbiotabile acidsinfant growthgerm-free mice |
| spellingShingle | Runze Ouyang Sijia Zheng Xiaolin Wang Qi Li Juan Ding Xiao Ma Zhihong Zhuo Zhen Li Qi Xin Xin Lu Lina Zhou Zhigang Ren Surong Mei Xinyu Liu Guowang Xu Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner Metabolites breast milk N-acetylneuraminic acid gut microbiota bile acids infant growth germ-free mice |
| title | Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner |
| title_full | Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner |
| title_fullStr | Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner |
| title_full_unstemmed | Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner |
| title_short | Crosstalk between Breast Milk N-Acetylneuraminic Acid and Infant Growth in a Gut Microbiota-Dependent Manner |
| title_sort | crosstalk between breast milk n acetylneuraminic acid and infant growth in a gut microbiota dependent manner |
| topic | breast milk N-acetylneuraminic acid gut microbiota bile acids infant growth germ-free mice |
| url | https://www.mdpi.com/2218-1989/13/7/846 |
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