Immunometabolic coevolution defines unique microenvironmental niches in ccRCC

Cell Metab. 2023 Aug 8;35(8):1424-1440.e5. doi: 10.1016/j.cmet.2023.06.005. Epub 2023 Jul 5.

Abstract

Tumor cell phenotypes and anti-tumor immune responses are shaped by local metabolite availability, but intratumoral metabolite heterogeneity (IMH) and its phenotypic consequences remain poorly understood. To study IMH, we profiled tumor/normal regions from clear cell renal cell carcinoma (ccRCC) patients. A common pattern of IMH transcended all patients, characterized by correlated fluctuations in the abundance of metabolites and processes associated with ferroptosis. Analysis of intratumoral metabolite-RNA covariation revealed that the immune composition of the microenvironment, especially the abundance of myeloid cells, drove intratumoral metabolite variation. Motivated by the strength of RNA-metabolite covariation and the clinical significance of RNA biomarkers in ccRCC, we inferred metabolomic profiles from the RNA sequencing data of ccRCC patients enrolled in 7 clinical trials, and we ultimately identifyied metabolite biomarkers associated with response to anti-angiogenic agents. Local metabolic phenotypes, therefore, emerge in tandem with the immune microenvironment, influence ongoing tumor evolution, and are associated with therapeutic sensitivity.

Keywords: cancer metabolism; immune microenvironment; immunometabolism; imputation; intratumoral heterogeneity; metabolites; metabolomics; renal cell carcinoma; transcriptomics.

Publication types

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

MeSH terms

  • Biomarkers, Tumor
  • Carcinoma*
  • Carcinoma, Renal Cell*
  • Humans
  • Kidney Neoplasms*
  • Myeloid Cells
  • RNA
  • Tumor Microenvironment

Substances

  • RNA
  • Biomarkers, Tumor