Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice

Recent studies demonstrate that paternal nutrition prior to conception may determine offspring development and health through epigenetic modification. This study aims to investigate the effects of paternal supplementation of n-3 polyunsaturated fatty acids (n-3 PUFAs) on the brain development and fu...

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Main Authors: Muhan Li, Qiaoyu Shi, Xueyi Jiang, Xuanyi Liu, Wei Han, Xiuqin Fan, Ping Li, Kemin Qi
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Nutrition
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnut.2022.969848/full
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author Muhan Li
Qiaoyu Shi
Xueyi Jiang
Xuanyi Liu
Wei Han
Xiuqin Fan
Ping Li
Kemin Qi
author_facet Muhan Li
Qiaoyu Shi
Xueyi Jiang
Xuanyi Liu
Wei Han
Xiuqin Fan
Ping Li
Kemin Qi
author_sort Muhan Li
collection DOAJ
description Recent studies demonstrate that paternal nutrition prior to conception may determine offspring development and health through epigenetic modification. This study aims to investigate the effects of paternal supplementation of n-3 polyunsaturated fatty acids (n-3 PUFAs) on the brain development and function, and associated gene imprinting in the offspring. Three to four-week-old male C57BL/6J mice (founder) were fed with an n-3 PUFA-deficient diet (n-3 D), and two n-3 PUFA supplementation diets – a normal n-3 PUFA content diet (n-3 N) and a high n-3 PUFA content diet (n-3 H) for 12 weeks. Then they were mated to 10-week-old virgin female C57BL/6J mice to generate the offspring. The results showed that paternal n-3 PUFA supplementation in preconception reduced the anxiety- and depressive-like behavior, and improved sociability, learning and memory in the offspring, along with increased synaptic number, upregulated expressions of neuron specific enolase, myelin basic protein, glial fibrillary acidic protein, brain-derived neurotrophic factor in the hippocampus and cerebral cortex, and altered expressions of genes associated with mitochondria biogenesis, fusion, fission and autophagy. Furthermore, with paternal n-3 PUFA supplementation, the expression of imprinted gene Snrpn was downregulated both in testes of the founder mice and their offspring, but upregulated in the cerebral cortex and hippocampus, with altered DNA methylation in its differentially methylated region. The data suggest that higher paternal intake of n-3 PUFAs in preconception may help to maintain optimal brain development and function in the offspring, and further raise the possibility of paternal nutritional intervention for mental health issues in subsequent generations.
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spelling doaj.art-f8445d3cb8ce410db9332f72b6d363f12022-12-22T03:22:20ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2022-10-01910.3389/fnut.2022.969848969848Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in miceMuhan LiQiaoyu ShiXueyi JiangXuanyi LiuWei HanXiuqin FanPing LiKemin QiRecent studies demonstrate that paternal nutrition prior to conception may determine offspring development and health through epigenetic modification. This study aims to investigate the effects of paternal supplementation of n-3 polyunsaturated fatty acids (n-3 PUFAs) on the brain development and function, and associated gene imprinting in the offspring. Three to four-week-old male C57BL/6J mice (founder) were fed with an n-3 PUFA-deficient diet (n-3 D), and two n-3 PUFA supplementation diets – a normal n-3 PUFA content diet (n-3 N) and a high n-3 PUFA content diet (n-3 H) for 12 weeks. Then they were mated to 10-week-old virgin female C57BL/6J mice to generate the offspring. The results showed that paternal n-3 PUFA supplementation in preconception reduced the anxiety- and depressive-like behavior, and improved sociability, learning and memory in the offspring, along with increased synaptic number, upregulated expressions of neuron specific enolase, myelin basic protein, glial fibrillary acidic protein, brain-derived neurotrophic factor in the hippocampus and cerebral cortex, and altered expressions of genes associated with mitochondria biogenesis, fusion, fission and autophagy. Furthermore, with paternal n-3 PUFA supplementation, the expression of imprinted gene Snrpn was downregulated both in testes of the founder mice and their offspring, but upregulated in the cerebral cortex and hippocampus, with altered DNA methylation in its differentially methylated region. The data suggest that higher paternal intake of n-3 PUFAs in preconception may help to maintain optimal brain development and function in the offspring, and further raise the possibility of paternal nutritional intervention for mental health issues in subsequent generations.https://www.frontiersin.org/articles/10.3389/fnut.2022.969848/fulln-3 polyunsaturated fatty acidspaternal nutritionoffspring braingene imprintingmouse
spellingShingle Muhan Li
Qiaoyu Shi
Xueyi Jiang
Xuanyi Liu
Wei Han
Xiuqin Fan
Ping Li
Kemin Qi
Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice
Frontiers in Nutrition
n-3 polyunsaturated fatty acids
paternal nutrition
offspring brain
gene imprinting
mouse
title Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice
title_full Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice
title_fullStr Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice
title_full_unstemmed Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice
title_short Paternal preconceptional diet enriched with n-3 polyunsaturated fatty acids affects offspring brain function in mice
title_sort paternal preconceptional diet enriched with n 3 polyunsaturated fatty acids affects offspring brain function in mice
topic n-3 polyunsaturated fatty acids
paternal nutrition
offspring brain
gene imprinting
mouse
url https://www.frontiersin.org/articles/10.3389/fnut.2022.969848/full
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