Lymphoma cell-derived extracellular vesicles inhibit autophagy and apoptosis to promote lymphoma cell growth via the microRNA-106a/Beclin1 axis

Cell Cycle. 2022 Jun;21(12):1280-1293. doi: 10.1080/15384101.2022.2047335. Epub 2022 Mar 13.

Abstract

Lymphoma is a common malignant tumor globally. Tumor-derived extracellular vesicles (Evs) participate in genetic information exchange between tumor cells. We investigated the role and mechanism of human Burkitt lymphoma cells Raji-derived Evs (Raji-Evs) in lymphoma cells. Effects of Evs on lymphoma cell proliferation, invasion, autophagy, and apoptosis were assessed using Cell Counting Kit-8 method, Transwell assay, laser confocal microscopy, Western blotting, and flow cytometry. microRNA (miR)-106a expression in lymphoma cells was determined using reverse transcription-quantitative polymerase chain reaction and then downregulated in Raji cells and then Evs were isolated (Evs-in-miR-106a) to evaluate its role in lymphoma cell growth. The binding relationship between miR-106a and Beclin1 was verified using RNA pull-down and dual-luciferase assays. Beclin1 was overexpressed in SU-DHL-4 and Farage cells and SU-DHL-4 cell autophagy and apoptosis were detected. The levels of miR-106a and Beclin1 in SU-DHL-4 cells were detected after adding autophagy inhibitors. The tumorigenicity assay in nude mice was performed to validate the effects of Raji-Evs in vivo. Raji-Evs promoted lymphoma cell proliferation and invasion and increased miR-106a. miR-106a knockdown reversed Evs-promoted lymphoma cell proliferation and invasion. miR-106a carried by Raji-Evs targeted Beclin1 expression. Beclin1 overexpression or miR-106a inhibitor reversed the effects of Evs on lymphoma cell autophagy and apoptosis. Autophagy inhibitors elevated miR-106a expression and lowered Beclin1 expression. Raji-Evs-carried miR-106a inhibited Beclin1-dependent autophagy and apoptosis in lymphoma cells, which were further verified in vivo, together with promoted tumor growth. We proved that Raji-Evs inhibited lymphoma cell autophagy and apoptosis and promoted cell growth via the miR-106a/Beclin1 axis.

Keywords: Beclin1; Lymphoma cells; apoptosis; autophagy; extracellular vesicles; microRNA-106a.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Autophagy / genetics
  • Beclin-1 / genetics
  • Beclin-1 / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Extracellular Vesicles* / metabolism
  • Lymphoma* / genetics
  • Lymphoma* / metabolism
  • Mice
  • Mice, Nude
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism

Substances

  • Beclin-1
  • MicroRNAs

Grants and funding

This work was supported by Sichuan Science and Technology Program (No. 2019YFS0301); Doctor Research Foundation of The Affiliated Hospital of Southwest Medical University (No. 19032; No. 19079); The Key Research Project from Health and Family Planning Commission of Sichuan Province (No. 18ZD014);Applied Basic Research Project of Luzhou Science and Technology Bureau(2019LZXNYDJ54; 2020LZXNYDJ48; 2020-JYJ-50).