mTORC2 links growth factor signaling with epigenetic regulation of iron metabolism in glioblastoma

J Biol Chem. 2019 Dec 20;294(51):19740-19751. doi: 10.1074/jbc.RA119.011519. Epub 2019 Nov 11.

Abstract

In cancer, aberrant growth factor receptor signaling reprograms cellular metabolism and global gene transcription to drive aggressive growth, but the underlying mechanisms are not well-understood. Here we show that in the highly lethal brain tumor glioblastoma (GBM), mTOR complex 2 (mTORC2), a critical core component of the growth factor signaling system, couples acetyl-CoA production with nuclear translocation of histone-modifying enzymes including pyruvate dehydrogenase and class IIa histone deacetylases to globally alter histone acetylation. Integrated analyses in orthotopic mouse models and in clinical GBM samples reveal that mTORC2 controls iron metabolisms via histone H3 acetylation of the iron-related gene promoter, promoting tumor cell survival. These results nominate mTORC2 as a critical epigenetic regulator of iron metabolism in cancer.

Keywords: acetyl coenzyme A (acetyl-CoA); glioblastoma; glucose metabolism; histone acetylation; iron metabolism; mammalian target of rapamycin (mTOR).

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Brain Neoplasms / metabolism*
  • Cell Line, Tumor
  • Cell Survival
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma / metabolism*
  • Histones / chemistry
  • Humans
  • Immediate-Early Proteins / metabolism
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Iron / metabolism*
  • Mechanistic Target of Rapamycin Complex 2 / metabolism*
  • Metabolome
  • Mice
  • Neoplasm Transplantation
  • Promoter Regions, Genetic
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Pyruvate Dehydrogenase (Lipoamide) / metabolism
  • Signal Transduction

Substances

  • Histones
  • Immediate-Early Proteins
  • Intercellular Signaling Peptides and Proteins
  • Iron
  • Pyruvate Dehydrogenase (Lipoamide)
  • AKT1 protein, human
  • Mechanistic Target of Rapamycin Complex 2
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • serum-glucocorticoid regulated kinase