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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
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    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. 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.
    3. 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.
    4. 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.
    5. 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.
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