ATM and P53 differentially regulate pancreatic beta cell survival in Ins1E cells

PLoS One. 2020 Aug 18;15(8):e0237669. doi: 10.1371/journal.pone.0237669. eCollection 2020.

Abstract

Pancreatic beta cell death is a hallmark of type 1 and 2 diabetes (T1D/T2D), but the underlying molecular mechanisms are incompletely understood. Key proteins of the DNA damage response (DDR), including tumor protein P53 (P53, also known as TP53 or TRP53 in rodents) and Ataxia Telangiectasia Mutated (ATM), a kinase known to act upstream of P53, have been associated with T2D. Here we test and compare the effect of ATM and P53 ablation on beta cell survival in the rat beta cell line Ins1E. We demonstrate that ATM and P53 differentially regulate beta cell apoptosis induced upon fundamentally different types of diabetogenic beta cell stress, including DNA damage, inflammation, lipotoxicity and endoplasmic reticulum (ER) stress. DNA damage induced apoptosis by treatment with the commonly used diabetogenic agent streptozotocin (STZ) is regulated by both ATM and P53. We show that ATM is a key STZ induced activator of P53 and that amelioration of STZ induced cell death by inhibition of ATM mainly depends on P53. While both P53 and ATM control lipotoxic beta cell apoptosis, ATM but not P53 fails to alter inflammatory beta cell death. In contrast, tunicamycin induced (ER stress associated) apoptosis is further increased by ATM knockdown or inhibition, but not by P53 knockdown. Our results reveal differential roles for P53 and ATM in beta cell survival in vitro in the context of four key pathophysiological types of diabetogenic beta cell stress, and indicate that ATM can use P53 independent signaling pathways to modify beta cell survival, dependent on the cellular insult.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Ataxia Telangiectasia Mutated Proteins / antagonists & inhibitors
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Cell Line
  • Cell Survival / drug effects
  • Cell Survival / genetics*
  • DNA Damage / drug effects
  • Diabetes Mellitus / pathology
  • Endoplasmic Reticulum Stress / drug effects
  • Endoplasmic Reticulum Stress / genetics
  • Gene Knockdown Techniques
  • Humans
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / pathology*
  • Protease Inhibitors / pharmacology
  • Protein Processing, Post-Translational / drug effects
  • RNA, Small Interfering / metabolism
  • Rats
  • Signal Transduction / genetics*
  • Streptozocin / toxicity
  • Tumor Suppressor Protein p53 / metabolism*
  • Tunicamycin / toxicity

Substances

  • Protease Inhibitors
  • RNA, Small Interfering
  • Tp53 protein, rat
  • Tumor Suppressor Protein p53
  • Tunicamycin
  • Streptozocin
  • Ataxia Telangiectasia Mutated Proteins

Grants and funding

The author(s) received no specific funding for this work.