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Adipose triglyceride lipase promotes prostaglandin-dependent actin remodeling by regulating substrate release from lipid droplets

View ORCID ProfileMichelle S. Giedt, View ORCID ProfileJonathon M. Thomalla, View ORCID ProfileMatthew R. Johnson, Zon Weng Lai, View ORCID ProfileTina L. Tootle, View ORCID ProfileMichael A. Welte
doi: https://doi.org/10.1101/2021.08.02.454724
Michelle S. Giedt
1Anatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA
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Jonathon M. Thomalla
2Department of Biology, University of Rochester, Rochester, NY
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Matthew R. Johnson
2Department of Biology, University of Rochester, Rochester, NY
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Zon Weng Lai
3Harvard T.H. Chan Advanced Multi-omics Platform, Harvard T.H. Chan School of Public Health, Boston, MA
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Tina L. Tootle
1Anatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA
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  • For correspondence: tina-tootle@uiowa.edu michael.welte@rochester.edu
Michael A. Welte
2Department of Biology, University of Rochester, Rochester, NY
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  • For correspondence: tina-tootle@uiowa.edu michael.welte@rochester.edu
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Abstract

A key factor controlling oocyte quality and fertility is lipids. Even though lipid droplets (LDs) are crucial regulators of lipid metabolism, their roles in fertility are poorly understood. During Drosophila oogenesis, LD accumulation in nurse cells coincides with dynamic actin remodeling necessary for late-stage follicle morphogenesis and fertility. Loss of the LD-associated Adipose Triglyceride Lipase (ATGL) disrupts both actin bundle formation and cortical actin integrity, an unusual phenotype also seen when Pxt, the enzyme responsible for prostaglandin (PG) synthesis, is missing. Dominant genetic interactions and PG treatment of follicles in vitro reveal that ATGL and Pxt act in the same pathway to regulate actin remodeling, with ATGL upstream of Pxt. Further, lipidomic analysis detects arachidonic acid (AA) containing triglycerides in ovaries. Because AA is the substrate for Pxt, we propose that ATGL releases AA from LDs to drive PG synthesis necessary for follicle development. We also find that exogenous AA is toxic to follicles in vitro, and LDs modulate this toxicity. This leads to the model that LDs both sequester AA to limit toxicity, and release AA via ATGL to drive PG production. We speculate that the same pathways are conserved across organisms to regulate oocyte development and promote fertility.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The scope of the manuscript has been revised to focus on the role of ATGL in modulating prostaglandin signaling.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 17, 2022.
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Adipose triglyceride lipase promotes prostaglandin-dependent actin remodeling by regulating substrate release from lipid droplets
Michelle S. Giedt, Jonathon M. Thomalla, Matthew R. Johnson, Zon Weng Lai, Tina L. Tootle, Michael A. Welte
bioRxiv 2021.08.02.454724; doi: https://doi.org/10.1101/2021.08.02.454724
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Adipose triglyceride lipase promotes prostaglandin-dependent actin remodeling by regulating substrate release from lipid droplets
Michelle S. Giedt, Jonathon M. Thomalla, Matthew R. Johnson, Zon Weng Lai, Tina L. Tootle, Michael A. Welte
bioRxiv 2021.08.02.454724; doi: https://doi.org/10.1101/2021.08.02.454724

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