Lipid droplets in mammalian eggs are utilized during embryonic diapause.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
09 03 2021
Historique:
entrez: 2 3 2021
pubmed: 3 3 2021
medline: 18 8 2021
Statut: ppublish

Résumé

Embryonic diapause (ED) is a temporary arrest of an embryo at the blastocyst stage when it waits for the uterine receptivity signal to implant. ED used by over 100 species may also occur in normally "nondiapausing" mammals when the uterine receptivity signal is blocked or delayed. A large number of lipid droplets (LDs) are stored throughout the preimplantation embryo development, but the amount of lipids varies greatly across different mammalian species. Yet, the role of LDs in the mammalian egg and embryo remains unknown. Here, using a mouse model, we provide evidence that LDs play a crucial role in maintaining ED. By mechanical removal of LDs from zygotes, we demonstrated that delipidated embryos are unable to survive during ED. LDs are not essential for normal prompt implantation, without ED. We further demonstrated that with the progression of ED, the amount of intracellular lipid reduces, and composition changes. This decrease in lipid is caused by a switch from carbohydrate metabolism to lipid catabolism in diapausing blastocysts, which also exhibit increased release of exosomes reflecting elevated embryonic signaling to the mother. We have also shown that presence of LDs in the oocytes of various mammals positively corelates with their species-specific length of diapause. Our results reveal the functional role of LDs in embryonic development. These results can help to develop diagnostic techniques and treatment of recurrent implantation failure and will likely ignite further studies in developmental biology and reproductive medicine fields.

Identifiants

pubmed: 33649221
pii: 2018362118
doi: 10.1073/pnas.2018362118
pmc: PMC7958255
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2021 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Roberta Arena (R)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.
Institute of Genetics and Animal Breeding of the Polish Academy of Sciences, 05-552 Jastrzębiec, Poland.

Simona Bisogno (S)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.
Institute of Genetics and Animal Breeding of the Polish Academy of Sciences, 05-552 Jastrzębiec, Poland.

Łukasz Gąsior (Ł)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.

Joanna Rudnicka (J)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.

Laura Bernhardt (L)

Institute of Human Genetics, Julius Maximilian University, 97074 Würzburg, Germany.

Thomas Haaf (T)

Institute of Human Genetics, Julius Maximilian University, 97074 Würzburg, Germany.

Federica Zacchini (F)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.
Percuros BV, 2333 Leiden, The Netherlands.

Michał Bochenek (M)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.

Kinga Fic (K)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland.

Ewelina Bik (E)

Faculty of Chemistry, Jagiellonian University, 30-387 Krakow, Poland.
Jagiellonian Centre for Experimental Therapeutics, Jagiellonian University, 30-348 Krakow, Poland.

Małgorzata Barańska (M)

Faculty of Chemistry, Jagiellonian University, 30-387 Krakow, Poland.
Jagiellonian Centre for Experimental Therapeutics, Jagiellonian University, 30-348 Krakow, Poland.

Anna Bodzoń-Kułakowska (A)

Department of Biochemistry and Neurobiology, Akademia Górniczo-Hutnicza University of Science and Technology, 30-059 Krakow, Poland.

Piotr Suder (P)

Department of Biochemistry and Neurobiology, Akademia Górniczo-Hutnicza University of Science and Technology, 30-059 Krakow, Poland.

Joanna Depciuch (J)

Institute of Nuclear Physics, Polish Academy of Sciences, 31-342 Krakow, Poland.

Artur Gurgul (A)

University Centre of Veterinary Medicine, University of Agriculture, 30-059 Krakow, Poland.

Zbigniew Polański (Z)

Institute of Zoology and Biomedical Research, Jagiellonian University, 30-387 Krakow, Poland.

Grażyna E Ptak (GE)

Małopolska Centre of Biotechnology, Jagiellonian University, 30-387 Krakow, Poland; g.ptak@uj.edu.pl.
Department of Biosciences, University of Teramo, 64100 Teramo, Italy.

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