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Insights into membrane association of the SMP domain of extended synaptotagmin

Author

Listed:
  • Yunyun Wang

    (Frontiers Science Center for Cell Responses, Nankai University)

  • Zhenni Li

    (Frontiers Science Center for Cell Responses, Nankai University)

  • Xinyu Wang

    (Nankai University)

  • Ziyuan Zhao

    (Nankai University)

  • Li Jiao

    (Nankai University)

  • Ruming Liu

    (Nankai University)

  • Keying Wang

    (Zhejiang University)

  • Rui Ma

    (Xiamen University)

  • Yang Yang

    (Renji Hospital, School of Medicine, Shanghai Jiao Tong University)

  • Guo Chen

    (Frontiers Science Center for Cell Responses, Nankai University)

  • Yong Wang

    (Zhejiang University
    International Campus of Zhejiang University)

  • Xin Bian

    (Frontiers Science Center for Cell Responses, Nankai University)

Abstract

The Synaptotagmin-like Mitochondrial-lipid-binding Protein (SMP) domain is a newly identified lipid transfer module present in proteins that regulate lipid homeostasis at membrane contact sites (MCSs). However, how the SMP domain associates with the membrane to extract and unload lipids is unclear. Here, we performed in vitro DNA brick-assisted lipid transfer assays and in silico molecular dynamics simulations to investigate the molecular basis of the membrane association by the SMP domain of extended synaptotagmin (E-Syt), which tethers the tubular endoplasmic reticulum (ER) to the plasma membrane (PM). We demonstrate that the SMP domain uses its tip region to recognize the extremely curved subdomain of tubular ER and the acidic-lipid-enriched PM for highly efficient lipid transfer. Supporting these findings, disruption of these mechanisms results in a defect in autophagosome biogenesis contributed by E-Syt. Our results suggest a model that provides a coherent picture of the action of the SMP domain at MCSs.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37202-8
    DOI: 10.1038/s41467-023-37202-8
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    References listed on IDEAS

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    1. 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.
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    3. Rajesh Ghai & Ximing Du & Huan Wang & Jiangqing Dong & Charles Ferguson & Andrew J. Brown & Robert G. Parton & Jia-Wei Wu & Hongyuan Yang, 2017. "ORP5 and ORP8 bind phosphatidylinositol-4, 5-biphosphate (PtdIns(4,5)P 2) and regulate its level at the plasma membrane," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    4. Yael Elbaz-Alon & Yuting Guo & Nadav Segev & Michal Harel & Daniel E. Quinnell & Tamar Geiger & Ori Avinoam & Dong Li & Jodi Nunnari, 2020. "PDZD8 interacts with Protrudin and Rab7 at ER-late endosome membrane contact sites associated with mitochondria," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. Curtis M. Schauder & Xudong Wu & Yasunori Saheki & Pradeep Narayanaswamy & Federico Torta & Markus R. Wenk & Pietro De Camilli & Karin M. Reinisch, 2014. "Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer," Nature, Nature, vol. 510(7506), pages 552-555, June.
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