The Anti-Warburg Effect Elicited by the cAMP-PGC1α Pathway Drives Differentiation of Glioblastoma Cells into Astrocytes

Cell Rep. 2017 Jan 10;18(2):468-481. doi: 10.1016/j.celrep.2016.12.037.

Abstract

Glioblastoma multiforme (GBM) is among the most aggressive of human cancers. Although differentiation therapy has been proposed as a potential approach to treat GBM, the mechanisms of induced differentiation remain poorly defined. Here, we established an induced differentiation model of GBM using cAMP activators that specifically directed GBM differentiation into astroglia. Transcriptomic and proteomic analyses revealed that oxidative phosphorylation and mitochondrial biogenesis are involved in induced differentiation of GBM. Dibutyryl cyclic AMP (dbcAMP) reverses the Warburg effect, as evidenced by increased oxygen consumption and reduced lactate production. Mitochondrial biogenesis induced by activation of the CREB-PGC1α pathway triggers metabolic shift and differentiation. Blocking mitochondrial biogenesis using mdivi1 or by silencing PGC1α abrogates differentiation; conversely, overexpression of PGC1α elicits differentiation. In GBM xenograft models and patient-derived GBM samples, cAMP activators also induce tumor growth inhibition and differentiation. Our data show that mitochondrial biogenesis and metabolic switch to oxidative phosphorylation drive the differentiation of tumor cells.

Keywords: PGC1α; PPARγ coactivator-1α; Warburg effect; cAMP; cyclic adenosine monophosphate; glioblastoma; glycolysis; induced differentiation; metabolic reprogramming; mitochondrial biogenesis; oxidative phosphorylation.

MeSH terms

  • 8-Bromo Cyclic Adenosine Monophosphate / analogs & derivatives
  • 8-Bromo Cyclic Adenosine Monophosphate / pharmacology
  • Astrocytes / metabolism
  • Astrocytes / pathology*
  • Astrocytes / ultrastructure
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • Brain Neoplasms / ultrastructure
  • Cell Death / drug effects
  • Cell Differentiation* / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cyclic AMP / metabolism*
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Gene Expression Profiling
  • Glial Fibrillary Acidic Protein / metabolism
  • Glioblastoma / genetics
  • Glioblastoma / metabolism*
  • Glioblastoma / pathology*
  • Glioblastoma / ultrastructure
  • Glycolysis* / drug effects
  • Humans
  • Organelle Biogenesis
  • Oxidative Phosphorylation / drug effects
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism*
  • Proteomics
  • Signal Transduction
  • Xenograft Model Antitumor Assays

Substances

  • Cyclic AMP Response Element-Binding Protein
  • Glial Fibrillary Acidic Protein
  • PPARGC1A protein, human
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • 8-Bromo Cyclic Adenosine Monophosphate
  • 8-chloro-cyclic adenosine monophosphate
  • Cyclic AMP