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Lipidomic and biophysical homeostasis of mammalian membranes counteracts dietary lipid perturbations to maintain cellular fitness

Author

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  • Kandice R. Levental

    (Department of Integrative Biology & Pharmacology, University of Texas Health Science Center at Houston)

  • Eric Malmberg

    (Department of Integrative Biology & Pharmacology, University of Texas Health Science Center at Houston)

  • Jessica L. Symons

    (Department of Integrative Biology & Pharmacology, University of Texas Health Science Center at Houston)

  • Yang-Yi Fan

    (Texas A&M University)

  • Robert S. Chapkin

    (Texas A&M University)

  • Robert Ernst

    (Saarland University)

  • Ilya Levental

    (Department of Integrative Biology & Pharmacology, University of Texas Health Science Center at Houston)

Abstract

Proper membrane physiology requires maintenance of biophysical properties, which must be buffered from external perturbations. While homeostatic adaptation of membrane fluidity to temperature variation is a ubiquitous feature of ectothermic organisms, such responsive membrane adaptation to external inputs has not been directly observed in mammals. Here, we report that challenging mammalian membranes by dietary lipids leads to robust lipidomic remodeling to preserve membrane physical properties. Specifically, exogenous polyunsaturated fatty acids are rapidly incorporated into membrane lipids, inducing a reduction in membrane packing. These effects are rapidly compensated both in culture and in vivo by lipidome-wide remodeling, most notably upregulation of saturated lipids and cholesterol, resulting in recovery of membrane packing and permeability. Abrogation of this response results in cytotoxicity when membrane homeostasis is challenged by dietary lipids. These results reveal an essential mammalian mechanism for membrane homeostasis wherein lipidome remodeling in response to dietary lipid inputs preserves functional membrane phenotypes.

Suggested Citation

  • Kandice R. Levental & Eric Malmberg & Jessica L. Symons & Yang-Yi Fan & Robert S. Chapkin & Robert Ernst & Ilya Levental, 2020. "Lipidomic and biophysical homeostasis of mammalian membranes counteracts dietary lipid perturbations to maintain cellular fitness," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15203-1
    DOI: 10.1038/s41467-020-15203-1
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    Cited by:

    1. Alfredo Erazo-Oliveras & Mónica Muñoz-Vega & Mohamed Mlih & Venkataramana Thiriveedi & Michael L. Salinas & Jaileen M. Rivera-Rodríguez & Eunjoo Kim & Rachel C. Wright & Xiaoli Wang & Kerstin K. Landr, 2023. "Mutant APC reshapes Wnt signaling plasma membrane nanodomains by altering cholesterol levels via oncogenic β-catenin," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    2. Gabriele Rocchetti & Marika Vitali & Martina Zappaterra & Laura Righetti & Rubina Sirri & Luigi Lucini & Chiara Dall’Asta & Roberta Davoli & Gianni Galaverna, 2022. "A molecular insight into the lipid changes of pig Longissimus thoracis muscle following dietary supplementation with functional ingredients," PLOS ONE, Public Library of Science, vol. 17(3), pages 1-24, March.
    3. Alexandre Santinho & Maxime Carpentier & Julio Lopes Sampaio & Mohyeddine Omrane & Abdou Rachid Thiam, 2024. "Giant organelle vesicles to uncover intracellular membrane mechanics and plasticity," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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