Metabolic and epigenetic dysfunctions underlie the arrest of in vitro fertilized human embryos in a senescent-like state

Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical problem. The mechanisms behind this arrest are unclear. Here, we show that the arrested embryos enter a senescent-like state, marked by cell cycle...

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Published inPLoS biology Vol. 20; no. 6; p. e3001682
Main Authors Yang, Yang, Shi, Liyang, Fu, Xiuling, Ma, Gang, Yang, Zhongzhou, Li, Yuhao, Zhou, Yibin, Yuan, Lihua, Xia, Ye, Zhong, Xiufang, Yin, Ping, Sun, Li, Zhang, Wuwen, Babarinde, Isaac A., Wang, Yongjun, Zhao, Xiaoyang, Hutchins, Andrew P., Tong, Guoqing
Format Journal Article
LanguageEnglish
Published San Francisco Public Library of Science 30.06.2022
Public Library of Science (PLoS)
Subjects
Arrests
Biology and Life Sciences
Cell cycle
Datasets
Embryonic development
Embryos
Epigenetic inheritance
Epigenetics
Gene expression
Genetic aspects
Genetic engineering
Glycolysis
Health aspects
Histones
In vitro fertilization
Metabolism
Morphology
Myc protein
Nicotinamide
Oxidative phosphorylation
Phenotypes
Phosphorylation
Physiological aspects
Resveratrol
Ribosomes
Stem cells
China
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Abstract Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical problem. The mechanisms behind this arrest are unclear. Here, we show that the arrested embryos enter a senescent-like state, marked by cell cycle arrest, the down-regulation of ribosomes and histones and down-regulation of MYC and p53 activity. The arrested embryos can be divided into 3 types. Type I embryos fail to complete the maternal-zygotic transition, and Type II/III embryos have low levels of glycolysis and either high (Type II) or low (Type III) levels of oxidative phosphorylation. Treatment with the SIRT agonist resveratrol or nicotinamide riboside (NR) can partially rescue the arrested phenotype, which is accompanied by changes in metabolic activity. Overall, our data suggests metabolic and epigenetic dysfunctions underlie the arrest of human embryos.
AbstractList Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical problem. The mechanisms behind this arrest are unclear. Here, we show that the arrested embryos enter a senescent-like state, marked by cell cycle arrest, the down-regulation of ribosomes and histones and down-regulation of MYC and p53 activity. The arrested embryos can be divided into 3 types. Type I embryos fail to complete the maternal-zygotic transition, and Type II/III embryos have low levels of glycolysis and either high (Type II) or low (Type III) levels of oxidative phosphorylation. Treatment with the SIRT agonist resveratrol or nicotinamide riboside (NR) can partially rescue the arrested phenotype, which is accompanied by changes in metabolic activity. Overall, our data suggests metabolic and epigenetic dysfunctions underlie the arrest of human embryos.
Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical problem. The mechanisms behind this arrest are unclear. Here, we show that the arrested embryos enter a senescent-like state, marked by cell cycle arrest, the down-regulation of ribosomes and histones and down-regulation of MYC and p53 activity. The arrested embryos can be divided into 3 types. Type I embryos fail to complete the maternal-zygotic transition, and Type II/III embryos have low levels of glycolysis and either high (Type II) or low (Type III) levels of oxidative phosphorylation. Treatment with the SIRT agonist resveratrol or nicotinamide riboside (NR) can partially rescue the arrested phenotype, which is accompanied by changes in metabolic activity. Overall, our data suggests metabolic and epigenetic dysfunctions underlie the arrest of human embryos.Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical problem. The mechanisms behind this arrest are unclear. Here, we show that the arrested embryos enter a senescent-like state, marked by cell cycle arrest, the down-regulation of ribosomes and histones and down-regulation of MYC and p53 activity. The arrested embryos can be divided into 3 types. Type I embryos fail to complete the maternal-zygotic transition, and Type II/III embryos have low levels of glycolysis and either high (Type II) or low (Type III) levels of oxidative phosphorylation. Treatment with the SIRT agonist resveratrol or nicotinamide riboside (NR) can partially rescue the arrested phenotype, which is accompanied by changes in metabolic activity. Overall, our data suggests metabolic and epigenetic dysfunctions underlie the arrest of human embryos.
Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical problem. The mechanisms behind this arrest are unclear. Here, we show that the arrested embryos enter a senescent-like state, marked by cell cycle arrest, the down-regulation of ribosomes and histones and down-regulation of MYC and p53 activity. The arrested embryos can be divided into 3 types. Type I embryos fail to complete the maternal-zygotic transition, and Type II/III embryos have low levels of glycolysis and either high (Type II) or low (Type III) levels of oxidative phosphorylation. Treatment with the SIRT agonist resveratrol or nicotinamide riboside (NR) can partially rescue the arrested phenotype, which is accompanied by changes in metabolic activity. Overall, our data suggests metabolic and epigenetic dysfunctions underlie the arrest of human embryos. Human embryos develop poorly in vitro, and as much as 60% of embryos will irreversibly arrest. This study shows that the arrested embryos enter a senescent-like state, and reveals that several mechanisms related to zygotic genome activation problems and erroneous metabolism can at least partly explain some of the reasons behind this arrest.
Audience Academic
Author Fu, Xiuling
Ma, Gang
Xia, Ye
Zhong, Xiufang
Yang, Yang
Babarinde, Isaac A.
Yang, Zhongzhou
Hutchins, Andrew P.
Sun, Li
Yuan, Lihua
Yin, Ping
Zhou, Yibin
Zhao, Xiaoyang
Tong, Guoqing
Zhang, Wuwen
Shi, Liyang
Wang, Yongjun
Li, Yuhao
AuthorAffiliation Max F Perutz Laboratories Center of Molecular Biology, AUSTRIA
8 Guangzhou Regenerative Medicine and Health Guangdong Laboratory (GRMH-GDL), Guangzhou, Guangdong, China
1 Center for Reproductive Medicine, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, China
6 State Key Laboratory of Organ Failure Research, Department of Developmental Biology, School of Basic Medical Sciences, Southern Medical University, Guangzhou, Guangdong, China
7 Guangdong Key Laboratory of Construction and Detection in Tissue Engineering, Southern Medical University, Guangzhou, Guangdong, China
5 Key Laboratory of Theory and Therapy of Muscles and Bones, Ministry of Education, Shanghai, China
4 Longhua Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai, China
2 Shenzhen Key Laboratory of Gene Regulation and Systems Biology, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, China
3 BGI Genomics, BGI-S
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2022 Yang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 Yang et al 2022 Yang et al
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– notice: 2022 Yang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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These authors are joint senior authors on this work.
The authors have declared that no competing interests exist.
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Snippet Around 60% of in vitro fertilized (IVF) human embryos irreversibly arrest before compaction between the 3- to 8-cell stage, posing a significant clinical...
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SubjectTerms Arrests
Biology and Life Sciences
Cell cycle
Datasets
Embryonic development
Embryos
Epigenetic inheritance
Epigenetics
Gene expression
Genetic aspects
Genetic engineering
Glycolysis
Health aspects
Histones
In vitro fertilization
Metabolism
Morphology
Myc protein
Nicotinamide
Oxidative phosphorylation
Phenotypes
Phosphorylation
Physiological aspects
Resveratrol
Ribosomes
Stem cells
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Title Metabolic and epigenetic dysfunctions underlie the arrest of in vitro fertilized human embryos in a senescent-like state
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https://www.proquest.com/docview/2682783104
https://pubmed.ncbi.nlm.nih.gov/PMC9246109
https://doaj.org/article/50dd3f10766441e8bab60d8a7a5b1b2d
http://dx.doi.org/10.1371/journal.pbio.3001682
Volume 20
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