High-resolution profiles of gene expression and DNA methylation highlight mitochondrial modifications during early embryonic development

Well-organized mitochondrial functions and dynamics are critical for early embryonic development and are operated via a large number of mitochondria-related genes (MtGs) encoded by both the nuclear and the mitochondrial genome. However, the mechanisms underlying mitochondrial modifications during th...

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Bibliographic Details
Published in:Journal of Reproduction and Development 2017, Vol.63(3), pp.247-261
Main Authors: REN, Likun, ZHANG, Chao, TAO, Li, HAO, Jing, TAN, Kun, MIAO, Kai, YU, Yong, SUI, Linlin, WU, Zhonghong, TIAN, Jianhui, AN, Lei
Format: Article
Language:English
Subjects:
Apoptosis
Cellular stress response
Deoxyribonucleic acid
DNA
DNA biosynthesis
DNA methylation
DNMT1 protein
Early embryos
Embryogenesis
Gene expression
Genomes
Glutathione
Mitochondria
Mitochondrial DNA
Organogenesis
Original
Reactive oxygen species
Stress response
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Summary:Well-organized mitochondrial functions and dynamics are critical for early embryonic development and are operated via a large number of mitochondria-related genes (MtGs) encoded by both the nuclear and the mitochondrial genome. However, the mechanisms underlying mitochondrial modifications during the critical window between blastocyst implantation and postimplantation organogenesis are poorly understood. Herein, we performed high-resolution dynamic profiling of MtGs to acquire a more detailed understanding of mitochondrial modifications during early development. Our data suggest that the resumption of mitochondrial mass growth is not only facilitated by increased mitochondrial biogenesis and mitochondrial DNA (mtDNA) replication, but also by the appropriate balance between mitochondrial fission and fusion. In addition, increased levels of reactive oxygen species (ROS) resulting from enhanced mitochondrial functions may be the critical inducer for activating the glutathione (GSH)-based stress response system in early embryos. The appropriate balance between the mitochondrial stress response and apoptosis appears to be significant for cell differentiation and early organogenesis. Furthermore, we found that most MtGs undergo de novo promoter methylation, which may have functional consequences on mitochondrial functions and dynamics during early development. We also report that mtDNA methylation can be observed as early as soon after implantation. DNMT1, the predominant enzyme for maintaining DNA methylation, localized to the mitochondria and bound to mtDNA by the implantation stage. Our study provides a new insight into the involvement of mitochondria in early mammalian embryogenesis. We also propose that the epigenetic modifications during early development are significant for modulating mitochondrial functions and dynamics.
ISSN:0916-8818
1348-4400
DOI:10.1262/jrd.2016-168