Abstract

Communication between cells is essential for multicellular life. During cognate immune interactions, T cells communicate with antigen-presenting cells (APC) via direct cell–cell contact or the release of molecules and vesicles containing T cell messages. A wide variety of mechanisms have been reported and among them a process called “trogocytosis” has traditionally been thought to be the fastest way to directly transfer membrane portions containing intact proteins from one cell to another; however, the mechanism is unverified. Trogocytosis has been distinguished from the generation of extracellular vesicles (EVs), a term that encompasses exosomes and microvesicles, as EVs are released via a contact-independent manner and are suggested to potentially send molecular messages over a distance. However, some previous reports regarding EVs in T cells may be misleading in terms of explaining their cellular origins. In addition, there is little evidence on how EVs are generated from T cells in vivo and function to regulate complex immune responses. A recent work demonstrated that T cell microvilli—thin and finger-like membrane protrusions—are highly fragile and easily separated as membrane particles by trogocytosis, forming a new class of EVs. Surprisingly, released T cell microvilli-derived particles act as vectors, transmitting T cell messages to cognate APCs. This review focuses on how T cell microvilli vesicles are connected with immune regulation mechanisms discovered previously.

Highlights

  • Information exchange between T cells and cognate antigen-presenting cells (APCs) dictates the character and scope of immune responses

  • A more striking point is that microvilli are selectively enriched with the membrane sorting complexes such as arrestin domain-containing protein 1 (Arrrdc1), TSG101, and Vps4, which are well-known to mediate microvesicle budding at the cell surface and are known to be involved in the immunological synapse (IS) [3, 43, 44]

  • Choudhuri et al demonstrated that TCR-enriched microvesicles are released from the central supramolecular activation clusters (cSMAC), we identified that TCR-enriched T cell microvilli particles are highly separated during T cell kinapses, suggesting that the generation of TCR-enriched vesicles are not restricted to the cSMAC, but can be separated from microvilli during T cell activation

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Summary

INTRODUCTION

Information exchange between T cells and cognate antigen-presenting cells (APCs) dictates the character and scope of immune responses. Over two decades before the IS was discovered, scientists made surprising in vitro and in vivo observations; proteins thought to be specific for one cell type were found in small amounts on the surfaces of other cell types [6,7,8]. This process has been referred as “absorption” [9], “internalization” [10], or “trogocytosis” [11, 12] (from the ancient Greek “trogo,” meaning “gnaw” or “nibble”) and has characteristics distinct from enzymemediated cleavage or exosomal transfer [12, 13]. We focus on the T cell microvilli and their roles in molecular and cellular aspects, especially in relation to the IS and TCR clusters, trogocytosis, membrane nanotubes, and EVs

Lymphocyte Microvilli
Membrane Tunneling Nanotubes
Immunological Synapses and Kinapses
APCs or Other Immune Cells
TMPs Can Be Categorized as a New Class of EVs
Conclusion and Perspectives
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