IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37202-8.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37202-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37202-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    2. 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.
    3. Michiko Shirane & Mariko Wada & Keiko Morita & Nahoki Hayashi & Reina Kunimatsu & Yuki Matsumoto & Fumiko Matsuzaki & Hirokazu Nakatsumi & Keisuke Ohta & Yasushi Tamura & Keiichi I. Nakayama, 2020. "Protrudin and PDZD8 contribute to neuronal integrity by promoting lipid extraction required for endosome maturation," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    4. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37202-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.