Vertical transmission of maternal DNA through extracellular vesicles associates with altered embryo bioenergetics during the periconception period

The transmission of DNA through extracellular vesicles (EVs) represents a novel genetic material transfer mechanism that may impact genome evolution and tumorigenesis. We aimed to investigate the potential for vertical DNA transmission within maternal endometrial EVs to the pre-implantation embryo a...

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Detalhes bibliográficos
Autores: Bolumar, D, Moncayo-Arlandi, J, Gonzalez-Fernandez, J, Ochando, A, Moreno, I, Monteagudo-Sanchez, A, Marin, C, Diez, A, Fabra, P, Checa, MA, Espinos, JJ, Gardner, DK, Simon, C, Vilella, F
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:INCLIVA
Repositorio:r-INCLIVA. Repositorio Institucional de Producción Científica de INCLIVA
OAI Identifier:oai:incliva.fundanetsuite.com:p19616
Acesso em linha:https://incliva.portalinvestigacion.com/publicaciones/19616
Access Level:acceso abierto
Palavra-chave:maternal-embryonic crosstalk
endometrium
exosomes
extracellular vesicles
metabolism
mitochondrial DNA
Human
Mouse
Descrição
Resumo:The transmission of DNA through extracellular vesicles (EVs) represents a novel genetic material transfer mechanism that may impact genome evolution and tumorigenesis. We aimed to investigate the potential for vertical DNA transmission within maternal endometrial EVs to the pre-implantation embryo and describe any effect on embryo bioenergetics. We discovered that the human endometrium secretes all three general subtypes of EV - apoptotic bodies (ABs), microvesicles (MVs), and exosomes (EXOs) - into the human endometrial fluid (EF) within the uterine cavity. EVs become uniformly secreted into the EF during the menstrual cycle, with the proportion of different EV populations remaining constant; however, MVs contain significantly higher levels of mitochondrial (mt)DNA than ABs or EXOs. During the window of implantation, MVs contain an eleven-fold higher level of mtDNA when compared to cells-of-origin within the receptive endometrium, which possesses a lower mtDNA content and displays the upregulated expression of mitophagy-related genes. Furthermore, we demonstrate the internalization of EV-derived nuclear-encoded (n)DNA/mtDNA by trophoblast cells of murine embryos, which associates with a reduction in mitochondrial respiration and ATP production. These findings suggest that the maternal endometrium suffers a reduction in mtDNA content during the preconceptional period, that nDNA/mtDNA become packaged into secreted EVs that the embryo uptakes, and that the transfer of DNA to the embryo within EVs occurs alongside the modulation of bioenergetics during implantation.