Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets

Maternal malnutrition during pregnancy may give rise to female offspring with disrupted ovary functions in adult age. Neonatal ovary development predisposes adult ovary function, yet the effect of maternal nutrition on the neonatal ovary has not been described. Therefore, here we show the impact of...

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Main Authors: Shiyan Sui, Yimin Jia, Bin He, Runsheng Li, Xian Li, Demin Cai, Haogang Song, Rongkui Zhang, Ruqian Zhao
Format: Article
Language:English
Published: Asian-Australasian Association of Animal Production Societies 2014-12-01
Series:Asian-Australasian Journal of Animal Sciences
Subjects:
Online Access:http://www.ajas.info/upload/pdf/ajas-27-12-1695.pdf
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spelling doaj-a516272cfc2f480098dce6bf756bbf182020-11-24T21:07:56ZengAsian-Australasian Association of Animal Production SocietiesAsian-Australasian Journal of Animal Sciences1011-23671976-55172014-12-0127121695170410.5713/ajas.2014.1433522980Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal PigletsShiyan Sui0Yimin Jia1Bin He2Runsheng Li3Xian Li4Demin Cai5Haogang Song6Rongkui Zhang7Ruqian Zhao8 Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China Shanghai Farm of Bright Food (Group) Co., Ltd, Dafeng 224100, .China Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, ChinaMaternal malnutrition during pregnancy may give rise to female offspring with disrupted ovary functions in adult age. Neonatal ovary development predisposes adult ovary function, yet the effect of maternal nutrition on the neonatal ovary has not been described. Therefore, here we show the impact of maternal protein restriction on the expression of folliculogenic and steroidogenic genes, their regulatory microRNAs and promoter DNA methylation in the ovary of neonatal piglets. Sows were fed either standard-protein (SP, 15% crude protein) or low-protein (LP, 7.5% crude protein) diets throughout gestation. Female piglets born to LP sows showed significantly decreased ovary weight relative to body weight (p<0.05) at birth, which was accompanied with an increased serum estradiol level (p<0.05). The LP piglets demonstrated higher ratio of bcl-2 associated X protein/B cell lymphoma/leukemia-2 mRNA (p<0.01), which was associated with up-regulated mRNA expression of bone morphogenic protein 4 (BMP4) (p<0.05) and proliferating cell nuclear antigen (PCNA) (p<0.05). The steroidogenic gene, cytochrome P450 aromatase (CYP19A1) was significantly down-regulated (p<0.05) in LP piglets. The alterations in ovarian gene expression were associated with a significant down-regulation of follicle-stimulating hormone receptor mRNA expression (p<0.05) in LP piglets. Moreover, three microRNAs, including miR-423-5p targeting both CYP19A1 and PCNA, miR-378 targeting CYP19A1 and miR-210 targeting BMP4, were significantly down-regulated (p<0.05) in the ovary of LP piglets. These results suggest that microRNAs are involved in mediating the effect of maternal protein restriction on ovarian function through regulating the expression of folliculogenic and steroidogenic genes in newborn piglets.http://www.ajas.info/upload/pdf/ajas-27-12-1695.pdfFolliculogenesisSteroidogenesisMaternal Dietary ProteinMicroRNAOvaryNeonatal Piglet
collection DOAJ
language English
format Article
sources DOAJ
author Shiyan Sui
Yimin Jia
Bin He
Runsheng Li
Xian Li
Demin Cai
Haogang Song
Rongkui Zhang
Ruqian Zhao
spellingShingle Shiyan Sui
Yimin Jia
Bin He
Runsheng Li
Xian Li
Demin Cai
Haogang Song
Rongkui Zhang
Ruqian Zhao
Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets
Asian-Australasian Journal of Animal Sciences
Folliculogenesis
Steroidogenesis
Maternal Dietary Protein
MicroRNA
Ovary
Neonatal Piglet
author_facet Shiyan Sui
Yimin Jia
Bin He
Runsheng Li
Xian Li
Demin Cai
Haogang Song
Rongkui Zhang
Ruqian Zhao
author_sort Shiyan Sui
title Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets
title_short Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets
title_full Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets
title_fullStr Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets
title_full_unstemmed Maternal Low-protein Diet Alters Ovarian Expression of Folliculogenic and Steroidogenic Genes and Their Regulatory MicroRNAs in Neonatal Piglets
title_sort maternal low-protein diet alters ovarian expression of folliculogenic and steroidogenic genes and their regulatory micrornas in neonatal piglets
publisher Asian-Australasian Association of Animal Production Societies
series Asian-Australasian Journal of Animal Sciences
issn 1011-2367
1976-5517
publishDate 2014-12-01
description Maternal malnutrition during pregnancy may give rise to female offspring with disrupted ovary functions in adult age. Neonatal ovary development predisposes adult ovary function, yet the effect of maternal nutrition on the neonatal ovary has not been described. Therefore, here we show the impact of maternal protein restriction on the expression of folliculogenic and steroidogenic genes, their regulatory microRNAs and promoter DNA methylation in the ovary of neonatal piglets. Sows were fed either standard-protein (SP, 15% crude protein) or low-protein (LP, 7.5% crude protein) diets throughout gestation. Female piglets born to LP sows showed significantly decreased ovary weight relative to body weight (p<0.05) at birth, which was accompanied with an increased serum estradiol level (p<0.05). The LP piglets demonstrated higher ratio of bcl-2 associated X protein/B cell lymphoma/leukemia-2 mRNA (p<0.01), which was associated with up-regulated mRNA expression of bone morphogenic protein 4 (BMP4) (p<0.05) and proliferating cell nuclear antigen (PCNA) (p<0.05). The steroidogenic gene, cytochrome P450 aromatase (CYP19A1) was significantly down-regulated (p<0.05) in LP piglets. The alterations in ovarian gene expression were associated with a significant down-regulation of follicle-stimulating hormone receptor mRNA expression (p<0.05) in LP piglets. Moreover, three microRNAs, including miR-423-5p targeting both CYP19A1 and PCNA, miR-378 targeting CYP19A1 and miR-210 targeting BMP4, were significantly down-regulated (p<0.05) in the ovary of LP piglets. These results suggest that microRNAs are involved in mediating the effect of maternal protein restriction on ovarian function through regulating the expression of folliculogenic and steroidogenic genes in newborn piglets.
topic Folliculogenesis
Steroidogenesis
Maternal Dietary Protein
MicroRNA
Ovary
Neonatal Piglet
url http://www.ajas.info/upload/pdf/ajas-27-12-1695.pdf
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