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T cell microvilli constitute immunological synaptosomes that carry messages to antigen-presenting cells

Author

Listed:
  • Hye-Ran Kim

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • YeVin Mun

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Kyung-Sik Lee

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Yoo-Jin Park

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Jeong-Su Park

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Jin-Hwa Park

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Bu-Nam Jeon

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Chang-Hyun Kim

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

  • Youngsoo Jun

    (Gwangju Institute of Science and Technology (GIST))

  • Young-Min Hyun

    (Yonsei University College of Medicine)

  • Minsoo Kim

    (University of Rochester)

  • Sang-Myeong Lee

    (Chonbuk National University)

  • Chul-Seung Park

    (Gwangju Institute of Science and Technology (GIST))

  • Sin-Hyeog Im

    (Pohang University of Science and Technology
    Pohang University of Science and Technology)

  • Chang-Duk Jun

    (Gwangju Institute of Science and Technology (GIST)
    Gwangju Institute of Science and Technology (GIST))

Abstract

Microvilli on T cells have been proposed to survey surfaces of antigen-presenting cells (APC) or facilitate adhesion under flow; however, whether they serve essential functions during T cell activation remains unclear. Here we show that antigen-specific T cells deposit membrane particles derived from microvilli onto the surface of cognate antigen-bearing APCs. Microvilli carry T cell receptors (TCR) at all stages of T cell activation and are released as large TCR-enriched, T cell microvilli particles (TMP) in a process of trogocytosis. These microvilli exclusively contain protein arrestin-domain-containing protein 1, which is directly involved in membrane budding and, in combination with vacuolar protein-sorting-associated protein 4, transforms large TMPs into smaller, exosome-sized TMPs. Notably, TMPs from CD4+ T cells are enriched with LFA-2/CD2 and various cytokines involved in activating dendritic cells. Collectively, these results demonstrate that T cell microvilli constitute “immunological synaptosomes” that carry T cell messages to APCs.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-06090-8
    DOI: 10.1038/s41467-018-06090-8
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    Cited by:

    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. Leeya Engel & Magda Zaoralová & Momei Zhou & Alexander R. Dunn & Stefan L. Oliver, 2025. "Extracellular filaments revealed by affinity capture cryogenic-electron tomography," Nature Communications, Nature, vol. 16(1), pages 1-11, December.
    3. Hirushi Gunasekara & Yu-Shiuan Cheng & Vanessa Perez-Silos & Alejandro Zevallos-Morales & Daniel Abegg & Alyssa Burgess & Liang-Wei Gong & Richard D. Minshall & Alexander Adibekian & Carlos Murga-Zama, 2025. "Unveiling cellular communications through rapid pan-membrane-protein labeling," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    4. Stephanie F. Rutter & Taeyoung Kang & Gemma F. Ryan & Bo Shi & Caitlin L. Vella & Pradeep Rajasekhar & Sean W. Cutter & Amy L. Hodge & Dilara C. Ozkocak & Ching-Seng Ang & Julian Ratcliffe & Katrina J, 2025. "The formation of the ‘footprint of death’ as a mechanism for generating large substrate-bound extracellular vesicles that mark the site of cell death," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    5. 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.

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