IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31160-3.html
   My bibliography  Save this article

T-cell trans-synaptic vesicles are distinct and carry greater effector content than constitutive extracellular vesicles

Author

Listed:
  • Pablo F. Céspedes

    (The University of Oxford)

  • Ashwin Jainarayanan

    (The University of Oxford)

  • Lola Fernández-Messina

    (Universidad Autónoma de Madrid
    Centro Nacional de Investigaciones Cardiovasculares (CNIC))

  • Salvatore Valvo

    (The University of Oxford)

  • David G. Saliba

    (The University of Oxford)

  • Elke Kurz

    (The University of Oxford)

  • Audun Kvalvaag

    (The University of Oxford)

  • Lina Chen

    (The University of Oxford)

  • Charity Ganskow

    (The University of Oxford)

  • Huw Colin-York

    (The University of Oxford
    The University of Oxford)

  • Marco Fritzsche

    (The University of Oxford
    The University of Oxford)

  • Yanchun Peng

    (The University of Oxford
    University of Oxford)

  • Tao Dong

    (The University of Oxford
    University of Oxford)

  • Errin Johnson

    (The University of Oxford)

  • Jesús A. Siller-Farfán

    (The University of Oxford)

  • Omer Dushek

    (The University of Oxford)

  • Erdinc Sezgin

    (Karolinska Institutet)

  • Ben Peacock

    (NanoFCM, MediCity)

  • Alice Law

    (NanoFCM, MediCity)

  • Dimitri Aubert

    (NanoFCM, MediCity)

  • Simon Engledow

    (The University of Oxford)

  • Moustafa Attar

    (The University of Oxford
    The University of Oxford)

  • Svenja Hester

    (The University of Oxford)

  • Roman Fischer

    (The University of Oxford)

  • Francisco Sánchez-Madrid

    (Universidad Autónoma de Madrid
    Centro Nacional de Investigaciones Cardiovasculares (CNIC))

  • Michael L. Dustin

    (The University of Oxford)

Abstract

The immunological synapse is a molecular hub that facilitates the delivery of three activation signals, namely antigen, costimulation/corepression and cytokines, from antigen-presenting cells (APC) to T cells. T cells release a fourth class of signaling entities, trans-synaptic vesicles (tSV), to mediate bidirectional communication. Here we present bead-supported lipid bilayers (BSLB) as versatile synthetic APCs to capture, characterize and advance the understanding of tSV biogenesis. Specifically, the integration of juxtacrine signals, such as CD40 and antigen, results in the adaptive tailoring and release of tSV, which differ in size, yields and immune receptor cargo compared with steadily released extracellular vesicles (EVs). Focusing on CD40L+ tSV as model effectors, we show that PD-L1 trans-presentation together with TSG101, ADAM10 and CD81 are key in determining CD40L vesicular release. Lastly, we find greater RNA-binding protein and microRNA content in tSV compared with EVs, supporting the specialized role of tSV as intercellular messengers.

Suggested Citation

  • Pablo F. Céspedes & Ashwin Jainarayanan & Lola Fernández-Messina & Salvatore Valvo & David G. Saliba & Elke Kurz & Audun Kvalvaag & Lina Chen & Charity Ganskow & Huw Colin-York & Marco Fritzsche & Yan, 2022. "T-cell trans-synaptic vesicles are distinct and carry greater effector content than constitutive extracellular vesicles," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31160-3
    DOI: 10.1038/s41467-022-31160-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31160-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31160-3?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. María Mittelbrunn & Cristina Gutiérrez-Vázquez & Carolina Villarroya-Beltri & Susana González & Fátima Sánchez-Cabo & Manuel Ángel González & Antonio Bernad & Francisco Sánchez-Madrid, 2011. "Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells," Nature Communications, Nature, vol. 2(1), pages 1-10, September.
    2. Di Li & Huw Colin-York & Liliana Barbieri & Yousef Javanmardi & Yuting Guo & Kseniya Korobchevskaya & Emad Moeendarbary & Dong Li & Marco Fritzsche, 2021. "Astigmatic traction force microscopy (aTFM)," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    3. Liliana Barbieri & Huw Colin-York & Kseniya Korobchevskaya & Di Li & Deanna L. Wolfson & Narain Karedla & Falk Schneider & Balpreet S. Ahluwalia & Tore Seternes & Roy A. Dalmo & Michael L. Dustin & Do, 2021. "Two-dimensional TIRF-SIM–traction force microscopy (2D TIRF-SIM-TFM)," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Kaushik Choudhuri & Jaime Llodrá & Eric W. Roth & Jones Tsai & Susana Gordo & Kai W. Wucherpfennig & Lance C. Kam & David L. Stokes & Michael L. Dustin, 2014. "Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse," Nature, Nature, vol. 507(7490), pages 118-123, March.
    5. Hye-Ran Kim & YeVin Mun & Kyung-Sik Lee & Yoo-Jin Park & Jeong-Su Park & Jin-Hwa Park & Bu-Nam Jeon & Chang-Hyun Kim & Youngsoo Jun & Young-Min Hyun & Minsoo Kim & Sang-Myeong Lee & Chul-Seung Park & , 2018. "T cell microvilli constitute immunological synaptosomes that carry messages to antigen-presenting cells," Nature Communications, Nature, vol. 9(1), pages 1-19, 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. Jeong-Su Park & Jun-Hyeong Kim & Won-Chang Soh & Na-Young Kim & Kyung-Sik Lee & Chang-Hyun Kim & Ik-Joo Chung & Sunjae Lee & Hye-Ran Kim & Chang-Duk Jun, 2023. "Trogocytic molting of T cell microvilli upregulates T cell receptor surface expression and promotes clonal expansion," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Sarah Renaud & Anthony Lefebvre & Olivier Moralès & Nadira Delhem, 2019. "Mini Review - Exosomes from Discovery to Isolation," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 15(2), pages 11286-11293, February.
    3. Jinhong Xu & Le Cui & Jiaqi Wang & Shasha Zheng & Huahua Zhang & Shuo Ke & Xiaoqin Cao & Yanteng Shi & Jing Li & Ke Zen & Antonio Vidal-Puig & Chen-Yu Zhang & Liang Li & Xiaohong Jiang, 2023. "Cold-activated brown fat-derived extracellular vesicle-miR-378a-3p stimulates hepatic gluconeogenesis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Johannes W Blumberg & Ulrich S Schwarz, 2022. "Comparison of direct and inverse methods for 2.5D traction force microscopy," PLOS ONE, Public Library of Science, vol. 17(1), pages 1-25, January.
    5. Christopher Szeto & Pirooz Zareie & Rushika C. Wirasinha & Justin B. Zhang & Andrea T. Nguyen & Alan Riboldi-Tunnicliffe & Nicole L. Gruta & Stephanie Gras & Stephen R. Daley, 2022. "Covalent TCR-peptide-MHC interactions induce T cell activation and redirect T cell fate in the thymus," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Sophie L Wardle & Mark E S Bailey & Audrius Kilikevicius & Dalia Malkova & Richard H Wilson & Tomas Venckunas & Colin N Moran, 2015. "Plasma MicroRNA Levels Differ between Endurance and Strength Athletes," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-15, April.
    7. Dingxi Zhou & Mariana Borsa & Daniel J. Puleston & Susanne Zellner & Jesusa Capera & Sharon Sanderson & Martina Schifferer & Svenja S. Hester & Xin Ge & Roman Fischer & Luke Jostins & Christian Behren, 2022. "Mapping autophagosome contents identifies interleukin-7 receptor-α as a key cargo modulating CD4+ T cell proliferation," Nature Communications, Nature, vol. 13(1), pages 1-15, 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:13:y:2022:i:1:d:10.1038_s41467-022-31160-3. 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.