IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46678-x.html
   My bibliography  Save this article

Rab GTPases and phosphoinositides fine-tune SNAREs dependent targeting specificity of intracellular vesicle traffic

Author

Listed:
  • Seiichi Koike

    (Max Planck Institute for Multidisciplinary Sciences
    Department of Life Sciences and Bioengineering)

  • Reinhard Jahn

    (Max Planck Institute for Multidisciplinary Sciences)

Abstract

In the secretory pathway the destination of trafficking vesicles is determined by specific proteins that, with the notable exception of SNAREs, are recruited from soluble pools. Previously we have shown that microinjected proteoliposomes containing early or late endosomal SNAREs, respectively, are targeted to the corresponding endogenous compartments, with targeting specificity being dependent on the recruitment of tethering factors by some of the SNAREs. Here, we show that targeting of SNARE-containing liposomes is refined upon inclusion of polyphosphoinositides and Rab5. Intriguingly, targeting specificity is dependent on the concentration of PtdIns(3)P, and on the recruitment of PtdIns(3)P binding proteins such as rabenosyn-5 and PIKfyve, with conversion of PtdIns(3)P into PtdIns(3,5)P2 re-routing the liposomes towards late endosomes despite the presence of GTP-Rab5 and early endosomal SNAREs. Our data reveal a complex interplay between permissive and inhibitory targeting signals that sharpen a basic targeting and fusion machinery for conveying selectivity in intracellular membrane traffic.

Suggested Citation

  • Seiichi Koike & Reinhard Jahn, 2024. "Rab GTPases and phosphoinositides fine-tune SNAREs dependent targeting specificity of intracellular vesicle traffic," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46678-x
    DOI: 10.1038/s41467-024-46678-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46678-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46678-x?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. Sudharshan Eathiraj & Xiaojing Pan & Christopher Ritacco & David G. Lambright, 2005. "Structural basis of family-wide Rab GTPase recognition by rabenosyn-5," Nature, Nature, vol. 436(7049), pages 415-419, July.
    2. Gilbert Di Paolo & Pietro De Camilli, 2006. "Phosphoinositides in cell regulation and membrane dynamics," Nature, Nature, vol. 443(7112), pages 651-657, October.
    3. Savvas Christoforidis & Heidi M. McBride & Robert D. Burgoyne & Marino Zerial, 1999. "The Rab5 effector EEA1 is a core component of endosome docking," Nature, Nature, vol. 397(6720), pages 621-625, February.
    4. Takeshi Ohya & Marta Miaczynska & Ünal Coskun & Barbara Lommer & Anja Runge & David Drechsel & Yannis Kalaidzidis & Marino Zerial, 2009. "Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes," Nature, Nature, vol. 459(7250), pages 1091-1097, June.
    5. Kumi Matsuura-Tokita & Masaki Takeuchi & Akira Ichihara & Kenta Mikuriya & Akihiko Nakano, 2006. "Live imaging of yeast Golgi cisternal maturation," Nature, Nature, vol. 441(7096), pages 1007-1010, June.
    6. Seiichi Koike & Reinhard Jahn, 2019. "SNAREs define targeting specificity of trafficking vesicles by combinatorial interaction with tethering factors," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    7. Rudy Behnia & Sean Munro, 2005. "Organelle identity and the signposts for membrane traffic," Nature, Nature, vol. 438(7068), pages 597-604, December.
    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. Yu-Te Yeh & Chandan Sona & Xin Yan & Yunxiao Li & Adrija Pathak & Mark I. McDermott & Zhigang Xie & Liangwen Liu & Anoop Arunagiri & Yuting Wang & Amaury Cazenave-Gassiot & Adhideb Ghosh & Ferdinand v, 2023. "Restoration of PITPNA in Type 2 diabetic human islets reverses pancreatic beta-cell dysfunction," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Yue Huang & Ruipeng Mu & David Wen & Joseph S Grimsby & Meina Liang & Anton I Rosenbaum, 2021. "Differences in levels of phosphatidylinositols in healthy and stable Coronary Artery Disease subjects revealed by HILIC-MRM method with SERRF normalization," PLOS ONE, Public Library of Science, vol. 16(6), pages 1-14, June.
    3. Antonio L Egea-Jiménez & Ángel Pérez-Lara & Senena Corbalán-García & Juan C Gómez-Fernández, 2013. "Phosphatidylinositol 4,5-Bisphosphate Decreases the Concentration of Ca2+, Phosphatidylserine and Diacylglycerol Required for Protein Kinase C α to Reach Maximum Activity," PLOS ONE, Public Library of Science, vol. 8(7), pages 1-8, July.
    4. Maria Thürmer & André Gollowitzer & Helmut Pein & Konstantin Neukirch & Elif Gelmez & Lorenz Waltl & Natalie Wielsch & René Winkler & Konstantin Löser & Julia Grander & Madlen Hotze & Sönke Harder & A, 2022. "PI(18:1/18:1) is a SCD1-derived lipokine that limits stress signaling," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    5. Nilmani Singh & Adriana Reyes-Ordoñez & Michael A. Compagnone & Jesus F. Moreno & Benjamin J. Leslie & Taekjip Ha & Jie Chen, 2021. "Redefining the specificity of phosphoinositide-binding by human PH domain-containing proteins," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Ammu Prasanna Kumar & Suryani Lukman, 2018. "Allosteric binding sites in Rab11 for potential drug candidates," PLOS ONE, Public Library of Science, vol. 13(6), pages 1-46, June.
    7. Di-Ao Liu & Kai Tao & Bin Wu & Ziyan Yu & Malwina Szczepaniak & Matthew Rames & Changsong Yang & Tatyana Svitkina & Yueyao Zhu & Fengyuan Xu & Xiaolin Nan & Wei Guo, 2023. "A phosphoinositide switch mediates exocyst recruitment to multivesicular endosomes for exosome secretion," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Ying Huang & Chenyang Xue & Ruiqian Bu & Cang Wu & Jiachen Li & Jinqiu Zhang & Jinyu Chen & Zhaoying Shi & Yonglong Chen & Yong Wang & Zhongmin Liu, 2024. "Inhibition and transport mechanisms of the ABC transporter hMRP5," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Hankum Park & Frances V. Hundley & Qing Yu & Katherine A. Overmyer & Dain R. Brademan & Lia Serrano & Joao A. Paulo & Julia C. Paoli & Sharan Swarup & Joshua J. Coon & Steven P. Gygi & J. Wade Harper, 2022. "Spatial snapshots of amyloid precursor protein intramembrane processing via early endosome proteomics," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    10. 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.
    11. Salome Funes & Jonathan Jung & Del Hayden Gadd & Michelle Mosqueda & Jianjun Zhong & Shankaracharya & Matthew Unger & Karly Stallworth & Debra Cameron & Melissa S. Rotunno & Pepper Dawes & Megan Fowle, 2024. "Expression of ALS-PFN1 impairs vesicular degradation in iPSC-derived microglia," Nature Communications, Nature, vol. 15(1), pages 1-25, 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:15:y:2024:i:1:d:10.1038_s41467-024-46678-x. 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.