Arginine methylation of ribose-5-phosphate isomerase A senses glucose to promote human colorectal cancer cell survival

Sci China Life Sci. 2020 Sep;63(9):1394-1405. doi: 10.1007/s11427-019-1562-y. Epub 2020 Mar 6.

Abstract

Cancer cells remodel their metabolic network to adapt to variable nutrient availability. Pentose phosphate pathway (PPP) plays protective and biosynthetic roles by oxidizing glucose to generate reducing power and ribose. How cancer cells modulate PPP activity in response to glucose supply remains unclear. Here we show that ribose-5-phosphate isomerase A (RPIA), an enzyme in PPP, directly interacts with co-activator associated arginine methyltransferase 1 (CARM1) and is methylated at arginine 42 (R42). R42 methylation up-regulates the catalytic activity of RPIA. Furthermore, glucose deprivation strengthens the binding of CARM1 with RPIA to induce R42 hypermethylation. Insufficient glucose supply links to RPIA hypermethylation at R42, which increases oxidative PPP flux. RPIA methylation supports ROS clearance by enhancing NADPH production and fuels nucleic acid synthesis by increasing ribose supply. Importantly, RPIA methylation at R42 significantly potentiates colorectal cancer cell survival under glucose starvation. Collectively, RPIA methylation connects glucose availability to nucleotide synthesis and redox homeostasis.

Keywords: CARM1; arginine methylation; colorectal cancer; pentose phosphate pathway; reactive oxygen species; ribose-5-phosphate isomerase A; ribulose-5-phosphate.

MeSH terms

  • Aldose-Ketose Isomerases / metabolism*
  • Amino Acid Sequence
  • Animals
  • Arginine / chemistry*
  • CRISPR-Cas Systems
  • Catalytic Domain
  • Cell Line, Tumor
  • Cell Survival
  • Colorectal Neoplasms / metabolism*
  • Gene Knockout Techniques
  • Glucose / metabolism*
  • Humans
  • Methylation
  • Mice
  • Mice, Nude
  • NADP / metabolism
  • Oxidation-Reduction
  • Pentose Phosphate Pathway
  • Protein Binding
  • Protein-Arginine N-Methyltransferases / metabolism
  • Reactive Oxygen Species / metabolism
  • Up-Regulation

Substances

  • Reactive Oxygen Species
  • NADP
  • Arginine
  • Protein-Arginine N-Methyltransferases
  • coactivator-associated arginine methyltransferase 1
  • Aldose-Ketose Isomerases
  • ribosephosphate isomerase
  • Glucose