l-2-Hydroxyglutarate remodeling of the epigenome and epitranscriptome creates a metabolic vulnerability in kidney cancer models

J Clin Invest. 2024 May 14;134(13):e171294. doi: 10.1172/JCI171294.

Abstract

Tumor cells are known to undergo considerable metabolic reprogramming to meet their unique demands and drive tumor growth. At the same time, this reprogramming may come at a cost with resultant metabolic vulnerabilities. The small molecule l-2-hydroxyglutarate (l-2HG) is elevated in the most common histology of renal cancer. Similarly to other oncometabolites, l-2HG has the potential to profoundly impact gene expression. Here, we demonstrate that l-2HG remodels amino acid metabolism in renal cancer cells through combined effects on histone methylation and RNA N6-methyladenosine. The combined effects of l-2HG result in a metabolic liability that renders tumors cells reliant on exogenous serine to support proliferation, redox homeostasis, and tumor growth. In concert with these data, high-l-2HG kidney cancers demonstrate reduced expression of multiple serine biosynthetic enzymes. Collectively, our data indicate that high-l-2HG renal tumors could be specifically targeted by strategies that limit serine availability to tumors.

Keywords: Metabolism; Oncology; Urology.

MeSH terms

  • Adenosine / analogs & derivatives
  • Animals
  • Carcinoma, Renal Cell / genetics
  • Carcinoma, Renal Cell / metabolism
  • Carcinoma, Renal Cell / pathology
  • Cell Line, Tumor
  • Epigenesis, Genetic
  • Epigenome
  • Gene Expression Regulation, Neoplastic
  • Glutarates* / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Kidney Neoplasms* / genetics
  • Kidney Neoplasms* / metabolism
  • Kidney Neoplasms* / pathology
  • Mice
  • RNA, Neoplasm / genetics
  • RNA, Neoplasm / metabolism
  • Serine / metabolism
  • Transcriptome

Substances

  • alpha-hydroxyglutarate
  • Glutarates
  • Serine
  • Histones
  • N-methyladenosine
  • RNA, Neoplasm
  • Adenosine