The BH3-only proteins BIM and PUMA are not critical for the reticulocyte apoptosis caused by loss of the pro-survival protein BCL-XL

Cell Death Dis. 2017 Jul 6;8(7):e2914. doi: 10.1038/cddis.2017.304.

Abstract

Anaemia is a major global health problem arising from diverse causes and for which improved therapeutic strategies are needed. Erythroid cells can undergo apoptotic cell death and loss of pro-survival BCL-XL is known to trigger apoptosis during late-stage erythroid development. However, the mechanism by which loss or pharmacological blockade of BCL-XL leads to erythroid cell apoptosis remains unclear. Here we sought to identify the precise stage of erythropoiesis that depends on BCL-XL. We also tested whether deficiency of BIM or PUMA, the two main pro-apoptotic antagonists of BCL-XL, could prevent reticulocyte death and anaemia caused by BCL-XL loss. Using an in vivo mouse model of tamoxifen-inducible Bclx gene deletion and in vitro assays with a BCL-XL-selective inhibitor, we interrogated each stage of erythrocyte differentiation for BCL-XL dependency. This revealed that reticulocytes, but not orthochromatic erythroblasts, require BCL-XL for their survival. Surprisingly, concurrent loss of BIM or PUMA had no significant impact on the development of anemia following acute BCL-XL deletion in vivo. However, analysis of mixed bone marrow chimaeric mice revealed that loss of PUMA, but not loss of BIM, partially alleviated impaired erythropoiesis caused by BCL-XL deficiency. Insight into how the network of pro-survival and pro-apoptotic proteins works will assist the development of strategies to mitigate the effects of abnormal cell death during erythropoiesis and prevent anaemia in patients treated with BCL-XL-specific BH3-mimetic drugs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anemia / genetics*
  • Anemia / metabolism
  • Anemia / pathology
  • Animals
  • Apoptosis / genetics*
  • Apoptosis Regulatory Proteins / deficiency
  • Apoptosis Regulatory Proteins / genetics*
  • Bcl-2-Like Protein 11 / deficiency
  • Bcl-2-Like Protein 11 / genetics*
  • Benzothiazoles / pharmacology
  • Cell Survival
  • Disease Models, Animal
  • Erythroblasts / metabolism
  • Erythroblasts / pathology
  • Erythropoiesis / genetics
  • Gene Deletion
  • Gene Expression Regulation*
  • Humans
  • Isoquinolines / pharmacology
  • Mice
  • Mice, Knockout
  • Organ Specificity
  • Protein Domains
  • Reticulocytes / metabolism
  • Reticulocytes / pathology
  • Signal Transduction
  • Tamoxifen / pharmacology
  • Tumor Suppressor Proteins / deficiency
  • Tumor Suppressor Proteins / genetics*
  • bcl-X Protein / antagonists & inhibitors
  • bcl-X Protein / deficiency
  • bcl-X Protein / genetics*

Substances

  • A-1331852
  • Apoptosis Regulatory Proteins
  • BCL2L1 protein, human
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • Benzothiazoles
  • Isoquinolines
  • PUMA protein, mouse
  • Tumor Suppressor Proteins
  • bcl-X Protein
  • Tamoxifen