AMPK-PERK axis represses oxidative metabolism and enhances apoptotic priming of mitochondria in acute myeloid leukemia

Cell Rep. 2022 Jan 4;38(1):110197. doi: 10.1016/j.celrep.2021.110197.

Abstract

AMP-activated protein kinase (AMPK) regulates the balance between cellular anabolism and catabolism dependent on energy resources to maintain proliferation and survival. Small-compound AMPK activators show anti-cancer activity in preclinical models. Using the direct AMPK activator GSK621, we show that the unfolded protein response (UPR) is activated by AMPK in acute myeloid leukemia (AML) cells. Mechanistically, the UPR effector protein kinase RNA-like ER kinase (PERK) represses oxidative phosphorylation, tricarboxylic acid (TCA) cycle, and pyrimidine biosynthesis and primes the mitochondrial membrane to apoptotic signals in an AMPK-dependent manner. Accordingly, in vitro and in vivo studies reveal synergy between the direct AMPK activator GSK621 and the Bcl-2 inhibitor venetoclax. Thus, selective AMPK-activating compounds kill AML cells by rewiring mitochondrial metabolism that primes mitochondria to apoptosis by BH3 mimetics, holding therapeutic promise in AML.

Keywords: AML; AMPK; GSK621; PERK; mitochondrial apoptosis; unfolded protein response; venetoclax.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / metabolism*
  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / physiology
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology*
  • Cell Line, Tumor
  • Citric Acid Cycle / drug effects
  • Drug Evaluation, Preclinical
  • Female
  • HEK293 Cells
  • HL-60 Cells
  • Humans
  • Imidazoles / pharmacology*
  • Leukemia, Myeloid, Acute / drug therapy*
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / metabolism
  • Male
  • Mice
  • Middle Aged
  • Mitochondria / metabolism
  • Oxidative Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-bcl-2 / antagonists & inhibitors
  • Pyrimidinones / pharmacology*
  • Sulfonamides / pharmacology*
  • THP-1 Cells
  • U937 Cells
  • Unfolded Protein Response / physiology*
  • Young Adult
  • eIF-2 Kinase / metabolism*

Substances

  • Antineoplastic Agents
  • Bridged Bicyclo Compounds, Heterocyclic
  • GSK621
  • Imidazoles
  • Proto-Oncogene Proteins c-bcl-2
  • Pyrimidinones
  • Sulfonamides
  • EIF2AK3 protein, human
  • eIF-2 Kinase
  • AMP-Activated Protein Kinases
  • venetoclax