Arginine Methylation of MDH1 by CARM1 Inhibits Glutamine Metabolism and Suppresses Pancreatic Cancer

Mol Cell. 2016 Nov 17;64(4):673-687. doi: 10.1016/j.molcel.2016.09.028. Epub 2016 Nov 10.

Abstract

Distinctive from their normal counterparts, cancer cells exhibit unique metabolic dependencies on glutamine to fuel anabolic processes. Specifically, pancreatic ductal adenocarcinoma (PDAC) cells rely on an unconventional metabolic pathway catalyzed by aspartate aminotransferase, malate dehydrogenase 1 (MDH1), and malic enzyme 1 to rewire glutamine metabolism and support nicotinamide adenine dinucleotide phosphate (NADPH) production. Here, we report that methylation on arginine 248 (R248) negatively regulates MDH1. Protein arginine methyltransferase 4 (PRMT4/CARM1) methylates and inhibits MDH1 by disrupting its dimerization. Knockdown of MDH1 represses mitochondria respiration and inhibits glutamine metabolism, which sensitizes PDAC cells to oxidative stress and suppresses cell proliferation. Meanwhile, re-expression of wild-type MDH1, but not its methylation-mimetic mutant, protects cells from oxidative injury and restores cell growth and clonogenic activity. Importantly, MDH1 is hypomethylated at R248 in clinical PDAC samples. Our study reveals that arginine methylation of MDH1 by CARM1 regulates cellular redox homeostasis and suppresses glutamine metabolism of pancreatic cancer.

Keywords: CARM1; KRAS; MDH1; arginine methylation; glutamine metabolism; mitochondrial respiration; nicotinamide adenine dinucleotide phosphate; pancreatic cancer; reactive oxygen species; redox homeostasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arginine / metabolism
  • Carcinoma, Pancreatic Ductal / genetics*
  • Carcinoma, Pancreatic Ductal / metabolism
  • Carcinoma, Pancreatic Ductal / pathology
  • Cell Line, Tumor
  • Cell Proliferation
  • Gene Expression Regulation, Neoplastic*
  • Glutamine / metabolism*
  • HEK293 Cells
  • Humans
  • Malate Dehydrogenase (NADP+) / antagonists & inhibitors
  • Malate Dehydrogenase (NADP+) / genetics*
  • Malate Dehydrogenase (NADP+) / metabolism
  • Methylation
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Models, Molecular
  • NADP / biosynthesis
  • Oxidation-Reduction
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Protein Multimerization
  • Protein Structure, Secondary
  • Protein-Arginine N-Methyltransferases / genetics*
  • Protein-Arginine N-Methyltransferases / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Signal Transduction

Substances

  • RNA, Small Interfering
  • Glutamine
  • NADP
  • Arginine
  • Malate Dehydrogenase (NADP+)
  • Protein-Arginine N-Methyltransferases
  • coactivator-associated arginine methyltransferase 1