Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way
Exposure to adverse events in early life increases the risk of chronic metabolic disease in adulthood. The objective of this study was to determine the significance of milk fat globule membrane (MFGM)-mediated alterations in the gut microbiome to the metabolic health of offspring in the long-term. F...
Autores principales: | , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8017235/ https://www.ncbi.nlm.nih.gov/pubmed/33816333 http://dx.doi.org/10.3389/fcimb.2021.621957 |
_version_ | 1783674021247713280 |
---|---|
author | Ye, Lin Zhang, Qianren Xin, Fengzhi Cao, Baige Qian, Linxi Dong, Yan |
author_facet | Ye, Lin Zhang, Qianren Xin, Fengzhi Cao, Baige Qian, Linxi Dong, Yan |
author_sort | Ye, Lin |
collection | PubMed |
description | Exposure to adverse events in early life increases the risk of chronic metabolic disease in adulthood. The objective of this study was to determine the significance of milk fat globule membrane (MFGM)-mediated alterations in the gut microbiome to the metabolic health of offspring in the long-term. Female C57BL/6 mice were fed either a high-fat diet (HFD) or a control diet for 3 weeks before pregnancy and throughout pregnancy and lactation. During lactation, pups from the HFD group were breast-fed with or without 1,000 mg/kg BW/day MFGM supplementation (HFD and HFD-MS group, respectively). After weaning, the offspring in each group were divided into male and female subgroups. The weaned mice were then shifted to a control diet for 8 weeks. At the eleventh week, stool samples were collected for 16S rRNA gene sequencing. Serum biochemical parameters were analyzed, and intraperitoneal glucose and insulin tolerance tests were performed. Neonatal supplementation with MFGM ameliorated metabolic disorder and improved glucose tolerance in offspring exposed to maternal HFD in a sex-specific manner. Furthermore, maternal HFD induced gut microbiota perturbation in offspring in adulthood. Neonatal MFGM supplementation significantly enriched g-Parabacteroides, g-Bifidobacterium, g-Faecalibaculum, and g-Lactobacillus in male offspring exposed to maternal HFD, while significantly enriched g-Parabacteroides and g-Alistipes in female offspring exposed to maternal HFD. These bacteria may be associated with the favorable changes in metabolism that occur in adulthood. Sex differences in the changes of metagenomic pathways related to oxidative phosphorylation, citrate cycle, electron transfer carries, and ubiquinone biosynthesis were also observed in the offspring. Maternal HFD has an adverse effect on the metabolism of offspring in later life. Neonatal MFGM supplementation could modulate the structure of gut microbiota communities and may have long-term protective effects on lipid and glucose metabolism, but these effects are sex dimorphic. |
format | Online Article Text |
id | pubmed-8017235 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-80172352021-04-03 Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way Ye, Lin Zhang, Qianren Xin, Fengzhi Cao, Baige Qian, Linxi Dong, Yan Front Cell Infect Microbiol Cellular and Infection Microbiology Exposure to adverse events in early life increases the risk of chronic metabolic disease in adulthood. The objective of this study was to determine the significance of milk fat globule membrane (MFGM)-mediated alterations in the gut microbiome to the metabolic health of offspring in the long-term. Female C57BL/6 mice were fed either a high-fat diet (HFD) or a control diet for 3 weeks before pregnancy and throughout pregnancy and lactation. During lactation, pups from the HFD group were breast-fed with or without 1,000 mg/kg BW/day MFGM supplementation (HFD and HFD-MS group, respectively). After weaning, the offspring in each group were divided into male and female subgroups. The weaned mice were then shifted to a control diet for 8 weeks. At the eleventh week, stool samples were collected for 16S rRNA gene sequencing. Serum biochemical parameters were analyzed, and intraperitoneal glucose and insulin tolerance tests were performed. Neonatal supplementation with MFGM ameliorated metabolic disorder and improved glucose tolerance in offspring exposed to maternal HFD in a sex-specific manner. Furthermore, maternal HFD induced gut microbiota perturbation in offspring in adulthood. Neonatal MFGM supplementation significantly enriched g-Parabacteroides, g-Bifidobacterium, g-Faecalibaculum, and g-Lactobacillus in male offspring exposed to maternal HFD, while significantly enriched g-Parabacteroides and g-Alistipes in female offspring exposed to maternal HFD. These bacteria may be associated with the favorable changes in metabolism that occur in adulthood. Sex differences in the changes of metagenomic pathways related to oxidative phosphorylation, citrate cycle, electron transfer carries, and ubiquinone biosynthesis were also observed in the offspring. Maternal HFD has an adverse effect on the metabolism of offspring in later life. Neonatal MFGM supplementation could modulate the structure of gut microbiota communities and may have long-term protective effects on lipid and glucose metabolism, but these effects are sex dimorphic. Frontiers Media S.A. 2021-03-19 /pmc/articles/PMC8017235/ /pubmed/33816333 http://dx.doi.org/10.3389/fcimb.2021.621957 Text en Copyright © 2021 Ye, Zhang, Xin, Cao, Qian and Dong http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Cellular and Infection Microbiology Ye, Lin Zhang, Qianren Xin, Fengzhi Cao, Baige Qian, Linxi Dong, Yan Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way |
title | Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way |
title_full | Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way |
title_fullStr | Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way |
title_full_unstemmed | Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way |
title_short | Neonatal Milk Fat Globule Membrane Supplementation During Breastfeeding Ameliorates the Deleterious Effects of Maternal High-Fat Diet on Metabolism and Modulates Gut Microbiota in Adult Mice Offspring in a Sex-Specific Way |
title_sort | neonatal milk fat globule membrane supplementation during breastfeeding ameliorates the deleterious effects of maternal high-fat diet on metabolism and modulates gut microbiota in adult mice offspring in a sex-specific way |
topic | Cellular and Infection Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8017235/ https://www.ncbi.nlm.nih.gov/pubmed/33816333 http://dx.doi.org/10.3389/fcimb.2021.621957 |
work_keys_str_mv | AT yelin neonatalmilkfatglobulemembranesupplementationduringbreastfeedingamelioratesthedeleteriouseffectsofmaternalhighfatdietonmetabolismandmodulatesgutmicrobiotainadultmiceoffspringinasexspecificway AT zhangqianren neonatalmilkfatglobulemembranesupplementationduringbreastfeedingamelioratesthedeleteriouseffectsofmaternalhighfatdietonmetabolismandmodulatesgutmicrobiotainadultmiceoffspringinasexspecificway AT xinfengzhi neonatalmilkfatglobulemembranesupplementationduringbreastfeedingamelioratesthedeleteriouseffectsofmaternalhighfatdietonmetabolismandmodulatesgutmicrobiotainadultmiceoffspringinasexspecificway AT caobaige neonatalmilkfatglobulemembranesupplementationduringbreastfeedingamelioratesthedeleteriouseffectsofmaternalhighfatdietonmetabolismandmodulatesgutmicrobiotainadultmiceoffspringinasexspecificway AT qianlinxi neonatalmilkfatglobulemembranesupplementationduringbreastfeedingamelioratesthedeleteriouseffectsofmaternalhighfatdietonmetabolismandmodulatesgutmicrobiotainadultmiceoffspringinasexspecificway AT dongyan neonatalmilkfatglobulemembranesupplementationduringbreastfeedingamelioratesthedeleteriouseffectsofmaternalhighfatdietonmetabolismandmodulatesgutmicrobiotainadultmiceoffspringinasexspecificway |