Constitutive autophagy contributes to resistance to TP53-mediated apoptosis in Epstein-Barr virus-positive latency III B-cell lymphoproliferations

Autophagy. 2015;11(12):2275-87. doi: 10.1080/15548627.2015.1115939.

Abstract

The Epstein-Barr virus (EBV) is associated with various lymphoproliferative disorders and lymphomas. We have previously demonstrated that treating wild-type TP53-expressing B cell lines with the TP53 pathway activator nutlin-3 induced apoptosis in EBV-negative and EBV-positive latency I cells whereas EBV-positive latency III cells remained much more apoptosis-resistant. Here, we report a constitutively high level of autophagy in these resistant cells which express high levels of the proautophagic protein BECN1/Beclin 1 based, at least in part, on the activation of the NFKB signaling pathway by the viral protein LMP1. Following treatment with nutlin-3, several autophagy-stimulating genes were upregulated both in EBV-negative and EBV-positive latency III cells. However the process of autophagy was only triggered in the latter and was associated with an upregulation of SESN1/sestrin 1 and inhibition of MTOR more rapid than in EBV-negative cells. A treatment with chloroquine, an inhibitor of autophagy, potentiated the apoptotic effect of nutlin-3, particularly in those EBV-positive cells which were resistant to apoptosis induced by nutlin-3 alone, thereby showing that autophagy participates in this resistant phenotype. Finally, using immunohistochemical staining, clinical samples from various B cell lymphoproliferations with the EBV-positive latency II or III phenotype were found to harbor a constitutively active autophagy.

Keywords: BECN1; Burkitt lymphoma; EBV; TP53; autophagy; nulin-3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects*
  • Autophagy* / drug effects
  • B-Lymphocytes / cytology*
  • B-Lymphocytes / virology*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Gene Expression / drug effects
  • Herpesvirus 4, Human*
  • Humans
  • Imidazoles / pharmacology
  • Lymphoma / pathology*
  • Lymphoma / virology
  • Piperazines / pharmacology
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Imidazoles
  • Piperazines
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • nutlin 3