Dynamic enlargement and mobilization of lipid droplets in pluripotent cells coordinate morphogenesis during mouse peri-implantation development

King Hang Tommy Mau, Donja Karimlou, David Barneda, Vincent Brochard, Christophe Royer, Bryony Leeke, Roshni A. Souza, Mélanie Pailles, Michelle Percharde, Shankar Srinivas, Alice Jouneau, Mark Christian and Véronique Azuara ()
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King Hang Tommy Mau: Faculty of Medicine, Imperial College London, Hammersmith Hospital
Donja Karimlou: Faculty of Medicine, Imperial College London, Hammersmith Hospital
David Barneda: Faculty of Medicine, Imperial College London, Hammersmith Hospital
Vincent Brochard: Université Paris-Saclay, UVSQ, INRAE, BREED
Christophe Royer: University of Oxford
Bryony Leeke: MRC London Institute of Medical Sciences (LMS), Hammersmith Hospital
Roshni A. Souza: Faculty of Medicine, Imperial College London, Hammersmith Hospital
Mélanie Pailles: Université Paris-Saclay, UVSQ, INRAE, BREED
Michelle Percharde: Faculty of Medicine, Imperial College London, Hammersmith Hospital
Shankar Srinivas: University of Oxford
Alice Jouneau: Université Paris-Saclay, UVSQ, INRAE, BREED
Mark Christian: Faculty of Medicine, Imperial College London, Hammersmith Hospital
Véronique Azuara: Faculty of Medicine, Imperial College London, Hammersmith Hospital

Nature Communications, 2022, vol. 13, issue 1, 1-13

Abstract: Abstract Mammalian pre-implantation embryos accumulate substantial lipids, which are stored in lipid droplets (LDs). Despite the fundamental roles of lipids in many cellular functions, the significance of building-up LDs for the developing embryo remains unclear. Here we report that the accumulation and mobilization of LDs upon implantation are causal in the morphogenesis of the pluripotent epiblast and generation of the pro-amniotic cavity in mouse embryos, a critical step for all subsequent development. We show that the CIDEA protein, found abundantly in adipocytes, enhances lipid storage in blastocysts and pluripotent stem cells by promoting LD enlargement through fusion. The LD-stored lipids are mobilized into lysosomes at the onset of lumenogenesis, but without CIDEA are prematurely degraded by cytosolic lipases. Loss of lipid storage or inactivation of lipophagy leads to the aberrant formation of multiple cavities within disorganised epithelial structures. Thus, our study reveals an unexpected role for LDs in orchestrating tissue remodelling and uncovers underappreciated facets of lipid metabolism in peri-implantation development.

Date: 2022
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DOI: 10.1038/s41467-022-31323-2

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