Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes

doi:10.1038/s41588-018-0055-6

. 2018 Mar;50(3):432-442.

doi: 10.1038/s41588-018-0055-6. Epub 2018 Feb 19.

Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes

Longsen Han^#¹, Chao Ren^#², Ling Li^#¹, Xiaoyan Li³, Juan Ge¹, Haichao Wang¹, Yi-Liang Miao⁴, Xuejiang Guo¹, Kelle H Moley⁵, Wenjie Shu⁶, Qiang Wang⁷

Affiliations

¹ State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, China.
² Department of Biotechnology, Beijing Institute of Radiation Medicine, Beijing, China.
³ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, China.
⁴ Institute of Stem Cell and Regenerative Biology, College of Animal Science and Technology & College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, China.
⁵ Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO, USA.
⁶ Department of Biotechnology, Beijing Institute of Radiation Medicine, Beijing, China. shuwj@bmi.ac.cn.
⁷ State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, China. qwang2012@njmu.edu.cn.

^# Contributed equally.

PMID: 29459681
DOI: 10.1038/s41588-018-0055-6

Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes

Longsen Han et al. Nat Genet. 2018 Mar.

. 2018 Mar;50(3):432-442.

doi: 10.1038/s41588-018-0055-6. Epub 2018 Feb 19.

Authors

Longsen Han^#¹, Chao Ren^#², Ling Li^#¹, Xiaoyan Li³, Juan Ge¹, Haichao Wang¹, Yi-Liang Miao⁴, Xuejiang Guo¹, Kelle H Moley⁵, Wenjie Shu⁶, Qiang Wang⁷

Affiliations

¹ State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, China.
² Department of Biotechnology, Beijing Institute of Radiation Medicine, Beijing, China.
³ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, China.
⁴ Institute of Stem Cell and Regenerative Biology, College of Animal Science and Technology & College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, China.
⁵ Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO, USA.
⁶ Department of Biotechnology, Beijing Institute of Radiation Medicine, Beijing, China. shuwj@bmi.ac.cn.
⁷ State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, China. qwang2012@njmu.edu.cn.

^# Contributed equally.

PMID: 29459681
DOI: 10.1038/s41588-018-0055-6

Erratum in

Publisher Correction: Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes.
Han L, Ren C, Li L, Li X, Ge J, Wang H, Miao YL, Guo X, Moley KH, Shu W, Wang Q. Han L, et al. Nat Genet. 2018 May;50(5):768. doi: 10.1038/s41588-018-0077-0. Nat Genet. 2018. PMID: 29487399

Abstract

Maternal obesity can impair embryo development and offspring health, yet the mechanisms responsible remain poorly understood. In a high-fat diet (HFD)-based female mouse model of obesity, we identified a marked reduction of Stella (also known as DPPA3 or PGC7) protein in oocytes. Starting with this clue, we found that the establishment of pronuclear epigenetic asymmetry in zygotes from obese mice was severely disrupted, inducing the accumulation of maternal 5-hydroxymethylcytosine modifications and DNA lesions. Furthermore, methylome-wide sequencing analysis detected global hypomethylation across the zygote genome in HFD-fed mice, with a specific enrichment in transposon elements and unique regions. Notably, overexpression of Stella in the oocytes of HFD-fed mice not only restored the epigenetic remodeling in zygotes but also partly ameliorated the maternal-obesity-associated developmental defects in early embryos and fetal growth. Thus, Stella insufficiency in oocytes may represent a critical mechanism that mediates the phenotypic effects of maternal obesity in embryos and offspring.

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Comment in

Obesity: Link between maternal obesity and offspring is STELLA.
Leong I. Leong I. Nat Rev Endocrinol. 2018 Apr;14(4):189. doi: 10.1038/nrendo.2018.26. Epub 2018 Mar 2. Nat Rev Endocrinol. 2018. PMID: 29498374 No abstract available.
Eggs sense high-fat diet.
Leitch HG, Hajkova P. Leitch HG, et al. Nat Genet. 2018 Mar;50(3):318-319. doi: 10.1038/s41588-018-0068-1. Nat Genet. 2018. PMID: 29511285 No abstract available.

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References

1. King, J. C. Maternal obesity, metabolism and pregnancy outcomes. Annu. Rev. Nutr. 26, 271–291 (2006). - DOI - PubMed
1. Tenenbaum-Gavish, K. & Hod, M. Impact of maternal obesity on fetal health. Fetal Diagn. Ther. 34, 1–7 (2013). - DOI - PubMed
1. Neri, C. & Edlow, A. G. Effects of maternal obesity on fetal programming: molecular approaches. Cold Spring Harb. Perspect. Med. 6, a026591 (2015). - DOI - PubMed
1. Mahizir, D. et al. Maternal obesity in females born small: pregnancy complications and offspring disease risk. Mol. Nutr. Food Res. 60, 8–17 (2016). - DOI - PubMed
1. Luzzo, K. M. et al. High-fat-diet-induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation and brain defects. PLoS One 7, e49217 (2012). - DOI - PubMed - PMC

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[1] King, J. C. Maternal obesity, metabolism and pregnancy outcomes. Annu. Rev. Nutr. 26, 271–291 (2006). - DOI - PubMed

[2] King, J. C. Maternal obesity, metabolism and pregnancy outcomes. Annu. Rev. Nutr. 26, 271–291 (2006). - DOI - PubMed

[3] Tenenbaum-Gavish, K. & Hod, M. Impact of maternal obesity on fetal health. Fetal Diagn. Ther. 34, 1–7 (2013). - DOI - PubMed

[4] Tenenbaum-Gavish, K. & Hod, M. Impact of maternal obesity on fetal health. Fetal Diagn. Ther. 34, 1–7 (2013). - DOI - PubMed

[5] Neri, C. & Edlow, A. G. Effects of maternal obesity on fetal programming: molecular approaches. Cold Spring Harb. Perspect. Med. 6, a026591 (2015). - DOI - PubMed

[6] Neri, C. & Edlow, A. G. Effects of maternal obesity on fetal programming: molecular approaches. Cold Spring Harb. Perspect. Med. 6, a026591 (2015). - DOI - PubMed

[7] Mahizir, D. et al. Maternal obesity in females born small: pregnancy complications and offspring disease risk. Mol. Nutr. Food Res. 60, 8–17 (2016). - DOI - PubMed

[8] Mahizir, D. et al. Maternal obesity in females born small: pregnancy complications and offspring disease risk. Mol. Nutr. Food Res. 60, 8–17 (2016). - DOI - PubMed

[9] Luzzo, K. M. et al. High-fat-diet-induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation and brain defects. PLoS One 7, e49217 (2012). - DOI - PubMed - PMC

[10] Luzzo, K. M. et al. High-fat-diet-induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation and brain defects. PLoS One 7, e49217 (2012). - DOI - PubMed - PMC

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Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes

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Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes

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