p53 and cell cycle independent dysregulation of autophagy in chronic lymphocytic leukaemia

Br J Cancer. 2013 Oct 29;109(9):2434-44. doi: 10.1038/bjc.2013.601. Epub 2013 Oct 3.

Abstract

Background: Activation of wild-type p53 with the small molecule sirtuin inhibitor Tenovin-6 (Tnv-6) induces p53-dependent apoptosis in many malignant cells. In contrast, Tnv-6 reduces chronic lymphocytic leukaemia (CLL) cell viability with dysregulation of autophagy, without increasing p53-pathway activity.

Methods: Here, we have investigated whether a quiescent phenotype (unique to CLL) determines the Tnv-6 response, by comparing the effects of Tnv-6 on activated and proliferating CLL. We further studied if these responses are p53-dependent.

Results: Unlike quiescent cells, cell death in activated cultures treated with Tnv-6 was consistently associated with p53 upregulation. However, p53 acetylation remained unchanged, without caspase-3 cleavage or apoptosis on electron microscopy. Instead, cellular ultrastructure and protein profiles indicated autophagy inhibition, with reduced ubiquitin-proteasome activity. In specimens with mutant TP53 cultured with Tnv-6, changes in the autophagy-associated protein LC3 occurred independently of p53. Cells treated with Tnv-6 analogues lacking sirtuin inhibitory activity had attenuated LC3 lipidation compared with Tnv-6 (P0.01), suggesting that autophagy dysregulation occurs predominantly through an effect on sirtuins.

Conclusion: These cell cycle and p53-independent anti-leukaemic mechanisms potentially offer novel therapeutic approaches to target leukaemia-sustaining cells in CLL, including in disease with p53-pathway dysfunction. Whether targets in addition to sirtuins contribute to autophagy dysregulation by Tnv-6, requires further investigation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Autophagy / drug effects
  • Autophagy / genetics
  • Autophagy / physiology*
  • Benzamides / pharmacology
  • Caspase 3 / genetics
  • Cell Cycle / drug effects
  • Cell Cycle / genetics
  • Cell Cycle / physiology
  • Cell Proliferation / drug effects
  • Humans
  • Interleukin-2 / pharmacology
  • Leukemia, Lymphocytic, Chronic, B-Cell / genetics
  • Leukemia, Lymphocytic, Chronic, B-Cell / metabolism*
  • Leukemia, Lymphocytic, Chronic, B-Cell / pathology*
  • Microtubule-Associated Proteins / genetics
  • Middle Aged
  • Proteasome Endopeptidase Complex / drug effects
  • Proteasome Endopeptidase Complex / genetics
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*
  • Ubiquitin / genetics
  • Up-Regulation / drug effects
  • Up-Regulation / genetics

Substances

  • Benzamides
  • Interleukin-2
  • MAP1LC3A protein, human
  • Microtubule-Associated Proteins
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Ubiquitin
  • tenovin-6
  • Caspase 3
  • Proteasome Endopeptidase Complex