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The asynchronous establishment of chromatin 3D architecture between in vitro fertilized and uniparental preimplantation pig embryos.

ABSTRACT: BACKGROUND:Pigs are important animals for agricultural and biomedical research, and improvement is needed for use of the assisted reproductive technologies. Determining underlying mechanisms of epigenetic reprogramming in the early stage of preimplantation embryos derived from in vitro fertilization (IVF), parthenogenesis, and androgenesis will not only contribute to assisted reproductive technologies of pigs but also will shed light into early human development. However, the reprogramming of three-dimensional architecture of chromatin in this process in pigs is poorly understood. RESULTS:We generate three-dimensional chromatin profiles for pig somatic cells, IVF, parthenogenesis, and androgenesis preimplantation embryos. We find that the chromosomes in the pig preimplantation embryos are enriched for superdomains, which are more rare in mice. However, p(s) curves, compartments, and topologically associated domains (TADs) are largely conserved in somatic cells and are gradually established during preimplantation embryogenesis in both mammals. In the uniparental pig embryos, the establishment of chromatin architecture is highly asynchronized at all levels from IVF embryos, and a remarkably strong decompartmentalization is observed during zygotic genome activation (ZGA). Finally, chromosomes originating from oocytes always establish TADs faster than chromosomes originating from sperm, both before and during ZGA. CONCLUSIONS:Our data highlight a potential unique 3D chromatin pattern of enriched superdomains in pig preimplantation embryos, an unusual decompartmentalization process during ZGA in the uniparental embryos, and an asynchronized TAD reprogramming between maternal and paternal genomes, implying a severe dysregulation of ZGA in the uniparental embryos in pigs.

SUBMITTER: Li F

PROVIDER: S-EPMC7418210 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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The asynchronous establishment of chromatin 3D architecture between in vitro fertilized and uniparental preimplantation pig embryos.

Li Feifei F Wang Danyang D Song Ruigao R Cao Chunwei C Zhang Zhihua Z Wang Yu Y Li Xiaoli X Huang Jiaojiao J Liu Qiang Q Hou Naipeng N Xu Bingxiang B Li Xiao X Gao Xiaomeng X Jia Yan Y Zhao Jianguo J Wang Yanfang Y

Genome biology 20200810 1

<h4>Background</h4>Pigs are important animals for agricultural and biomedical research, and improvement is needed for use of the assisted reproductive technologies. Determining underlying mechanisms of epigenetic reprogramming in the early stage of preimplantation embryos derived from in vitro fertilization (IVF), parthenogenesis, and androgenesis will not only contribute to assisted reproductive technologies of pigs but also will shed light into early human development. However, the reprogrammi ...[more]

PMID: 32778155

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Project description:Study questionDoes the oxygen concentration in the culture medium [either physiologic (5%) or atmospheric (20%)] affect mitochondrial ultrastructure and function in preimplantation mouse embryos generated by IVF?Summary answerEmbryos cultured in 20% oxygen show increased mitochondrial abnormalities compared to embryos cultured in 5% oxygen.What is known alreadyART are widely used and have resulted in the birth of more than 8 million children. A variety of media and oxygen concentrations are used to culture embryos. Embryos cultured under physiological O2 tension (5%) reach the blastocyst stage faster and have fewer alterations in gene expression when compared with embryos cultured under atmospheric oxygen conditions (20%). The mechanisms by which oxygen tension affects preimplantation development remain unclear, but mitochondria are believed to play an important role. The aim of this study was to evaluate how mitochondrial ultrastructure and function in IVF embryos were affected by culture under physiologic (5%) or atmospheric (20%) oxygen concentrations.Study design, size, durationZygotes, 2-cell, 4-cell, morula and blastocyst were flushed out of the uterus after natural fertilization and used as controls. IVF was performed in CF1 x B6D2F1 mice and embryos were cultured in Potassium simplex optimized medium (KSOM) with amino acids (KAA) under 5% and 20% O2 until the blastocyst stage. Embryo development with the addition of antioxidants was also tested.Participants/materials, setting, methodsMitochondrial function was assessed by measuring mitochondrial membrane potential, reactive oxygen species (ROS) production, ATP levels, and the expression of selected genes involved in mitochondrial function. Mitochondria ultrastructure was evaluated by transmission electron microscopy (TEM).Main results and the role of chanceEmbryos cultured under 20% O2 had fewer mitochondria and more vacuoles and hooded (abnormal) mitochondria compared to the other groups (P < 0.05). At the blastocyst stage the mitochondria of IVF embryos cultured in 20% O2 had lower mtDNA copy number, a denser matrix and more lamellar cristae than controls. Overall IVF-generated blastocysts had lower mitochondrial membrane potential, higher ROS levels, together with changes in the expression of selected mitochondrial genes (P < 0.05). ATP levels were significantly lower than controls only under 5% O2, with the 20% O2 IVF group having intermediate levels. Unexpectedly, adding antioxidant to the culture medium did not improve development.Large scale dataN/A.Limitations, reasons for cautionFindings in mice embryos might be different from human embryos.Wider implications of the findingsThis study suggests that changes in the mitochondria may be part of the mechanism by which lower oxygen concentration leads to better embryo development and further emphasize the importance of mitochondria as a locus of reprogramming.Study funding/competing interest(s)This study was funded by R01 HD 082039 to PFR, the Department of Life, Health and Environmental Sciences, University of L'Aquila, Italy (RIA 2016-2018) and the Department of Anatomy, Histology, Forensic Medicine and Orthopaedics, La Sapienza University of Rome, Italy (University grants 2016-2017). The authors declare no competing interests.

Dataset Information

The asynchronous establishment of chromatin 3D architecture between in vitro fertilized and uniparental preimplantation pig embryos.

Publications

The asynchronous establishment of chromatin 3D architecture between in vitro fertilized and uniparental preimplantation pig embryos.

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