Adenosine leakage from perforin-burst extracellular vesicles inhibits perforin secretion by cytotoxic T-lymphocytes

PLoS One. 2020 Apr 10;15(4):e0231430. doi: 10.1371/journal.pone.0231430. eCollection 2020.

Abstract

Extracellular vesicles (EVs) in the tumor microenvironment facilitate intercellular communication. Cancer cell-derived EVs act as an immunosuppressor by transporting cargos and presenting transmembrane proteins. By contrast, CD8+ cytotoxic T-lymphocytes (CTLs) exert anti-cancer cytotoxicity via the pore-forming protein perforin. Here, we hypothesize that although EVs are destroyed by perforin, cancer cell-derived EVs might possess mechanisms that enable them to avoid this destruction. We used a breast cancer cell line, MDA-MB-231-luc-D3H2LN (D3H2LN), to generate EVs. Destruction of the EVs by perforin was demonstrated visually using atomic force microscopy. To investigate immunosuppressive metabolites within cancer cell-derived EVs, we performed metabolomic profiling of EVs from D3H2LN cells cultured for 48 h with or without IFN-γ, which induces metabolic changes in the cells. We found that both types of EV from IFN-γ treated D3H2LN cells and non-treated D3H2LN cells contained adenosine, which has immunosuppressive effects. When we exposed cancer cell-derived EVs to CTLs, perforin secretion by CTLs fell significantly. In addition, the decreases in perforin secretion were ameliorated by treatment with adenosine deaminase, which degrades extracellular adenosine. Taken together, these results suggest that after perforin secreted by CTLs disrupts the membrane of EVs, adenosine released from the EVs acts as an immunosuppressive metabolite by binding to the adenosine receptor on the CTL membrane. This mechanism provides a novel survival strategy using cancer cell-derived EVs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / metabolism*
  • Cell Line, Tumor
  • Cells, Cultured
  • Extracellular Vesicles / drug effects
  • Extracellular Vesicles / metabolism*
  • Humans
  • Interferon-gamma / pharmacology
  • Perforin / metabolism*
  • Perforin / pharmacology
  • T-Lymphocytes, Cytotoxic / drug effects
  • T-Lymphocytes, Cytotoxic / metabolism*

Substances

  • Perforin
  • Interferon-gamma
  • Adenosine

Grants and funding

This work was supported by the JSPS Early-Career Scientists KAKENHI grant number: JP18K15258 (to H.T.);https://www.jsps.go.jp/english/index.html, the JSPS Grant-in-Aid for Scientific Research on Innovative Areas KAKENHI grant number: JP18H04804 (to A.H.);https://www.jsps.go.jp/english/index.html, the Research on Development of New Drugs GAPFREE (to A.H.) from the Japan Agency for Medical Research and Development (AMED);https://www.amed.go.jp/en/index.html, and Project for Cancer Research and Therapeutic Evolution (P-CREATE) grant number: 19cm0106402h0004 (to T.O.) from the Japan Agency for Medical Research and Development (AMED);https://www.amed.go.jp/en/index.html. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.