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A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes

Author

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  • Joachim Moser von Filseck

    (CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université de Nice Sophia-Antipolis, 660 rte des lucioles, Valbonne 06560, France)

  • Stefano Vanni

    (CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université de Nice Sophia-Antipolis, 660 rte des lucioles, Valbonne 06560, France)

  • Bruno Mesmin

    (CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université de Nice Sophia-Antipolis, 660 rte des lucioles, Valbonne 06560, France)

  • Bruno Antonny

    (CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université de Nice Sophia-Antipolis, 660 rte des lucioles, Valbonne 06560, France)

  • Guillaume Drin

    (CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université de Nice Sophia-Antipolis, 660 rte des lucioles, Valbonne 06560, France)

Abstract

Lipids are unevenly distributed within eukaryotic cells, thus defining organelle identity. How non-vesicular transport mechanisms generate these lipid gradients between membranes remains a central question. Here using quantitative, real-time lipid transport assays, we demonstrate that Osh4p, a sterol/phosphatidylinositol-4-phosphate (PI(4)P) exchanger of the ORP/Osh family, transports sterol against its gradient between two membranes by dissipating the energy of a PI(4)P gradient. Sterol transport is sustained through the maintenance of this PI(4)P gradient by the PI(4)P-phosphatase Sac1p. Differences in lipid packing between membranes can stabilize sterol gradients generated by Osh4p and modulate its lipid exchange capacity. The ability of Osh4p to recognize sterol and PI(4)P via distinct modalities and the dynamics of its N-terminal lid govern its activity. We thus demonstrate that an intracellular lipid transfer protein actively functions to create a lipid gradient between membranes.

Suggested Citation

  • Joachim Moser von Filseck & Stefano Vanni & Bruno Mesmin & Bruno Antonny & Guillaume Drin, 2015. "A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes," Nature Communications, Nature, vol. 6(1), pages 1-12, May.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7671
    DOI: 10.1038/ncomms7671
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    Cited by:

    1. Jan-Hannes Schäfer & Carolin Körner & Bianca M. Esch & Sergej Limar & Kristian Parey & Stefan Walter & Dovile Januliene & Arne Moeller & Florian Fröhlich, 2023. "Structure of the ceramide-bound SPOTS complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Yunyun Wang & Zhenni Li & Xinyu Wang & Ziyuan Zhao & Li Jiao & Ruming Liu & Keying Wang & Rui Ma & Yang Yang & Guo Chen & Yong Wang & Xin Bian, 2023. "Insights into membrane association of the SMP domain of extended synaptotagmin," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Darshini Jeyasimman & Bilge Ercan & Dennis Dharmawan & Tomoki Naito & Jingbo Sun & Yasunori Saheki, 2021. "PDZD-8 and TEX-2 regulate endosomal PI(4,5)P2 homeostasis via lipid transport to promote embryogenesis in C. elegans," Nature Communications, Nature, vol. 12(1), pages 1-21, December.

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