Impairment of Angiogenesis by Fatty Acid Synthase Inhibition Involves mTOR Malonylation

Cell Metab. 2018 Dec 4;28(6):866-880.e15. doi: 10.1016/j.cmet.2018.07.019. Epub 2018 Aug 23.

Abstract

The role of fatty acid synthesis in endothelial cells (ECs) remains incompletely characterized. We report that fatty acid synthase knockdown (FASNKD) in ECs impedes vessel sprouting by reducing proliferation. Endothelial loss of FASN impaired angiogenesis in vivo, while FASN blockade reduced pathological ocular neovascularization, at >10-fold lower doses than used for anti-cancer treatment. Impaired angiogenesis was not due to energy stress, redox imbalance, or palmitate depletion. Rather, FASNKD elevated malonyl-CoA levels, causing malonylation (a post-translational modification) of mTOR at lysine 1218 (K1218). mTOR K-1218 malonylation impaired mTOR complex 1 (mTORC1) kinase activity, thereby reducing phosphorylation of downstream targets (p70S6K/4EBP1). Silencing acetyl-CoA carboxylase 1 (an enzyme producing malonyl-CoA) normalized malonyl-CoA levels and reactivated mTOR in FASNKD ECs. Mutagenesis unveiled the importance of mTOR K1218 malonylation for angiogenesis. This study unveils a novel role of FASN in metabolite signaling that contributes to explaining the anti-angiogenic effect of FASN blockade.

Keywords: angiogenesis; endothelial cell; fatty acid synthase; lipids; mTOR; mTORC1; malonyl-CoA; metabolism; post-translational modifications; protein malonylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetyl-CoA Carboxylase / antagonists & inhibitors
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Fatty Acid Synthase, Type I / antagonists & inhibitors
  • Fatty Acid Synthase, Type I / genetics
  • Fatty Acid Synthase, Type I / physiology*
  • Human Umbilical Vein Endothelial Cells / cytology
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Malonyl Coenzyme A / metabolism*
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Orlistat / therapeutic use
  • Protein Processing, Post-Translational
  • Retinal Neovascularization / drug therapy
  • Retinal Neovascularization / pathology*
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Malonyl Coenzyme A
  • Orlistat
  • FASN protein, human
  • Fatty Acid Synthase, Type I
  • MTOR protein, human
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases
  • ACACA protein, human
  • Acetyl-CoA Carboxylase