Aspartate is a limiting metabolite for cancer cell proliferation under hypoxia and in tumours

Nat Cell Biol. 2018 Jul;20(7):775-781. doi: 10.1038/s41556-018-0118-z. Epub 2018 Jun 25.

Abstract

As oxygen is essential for many metabolic pathways, tumour hypoxia may impair cancer cell proliferation1-4. However, the limiting metabolites for proliferation under hypoxia and in tumours are unknown. Here, we assessed proliferation of a collection of cancer cells following inhibition of the mitochondrial electron transport chain (ETC), a major metabolic pathway requiring molecular oxygen5. Sensitivity to ETC inhibition varied across cell lines, and subsequent metabolomic analysis uncovered aspartate availability as a major determinant of sensitivity. Cell lines least sensitive to ETC inhibition maintain aspartate levels by importing it through an aspartate/glutamate transporter, SLC1A3. Genetic or pharmacologic modulation of SLC1A3 activity markedly altered cancer cell sensitivity to ETC inhibitors. Interestingly, aspartate levels also decrease under low oxygen, and increasing aspartate import by SLC1A3 provides a competitive advantage to cancer cells at low oxygen levels and in tumour xenografts. Finally, aspartate levels in primary human tumours negatively correlate with the expression of hypoxia markers, suggesting that tumour hypoxia is sufficient to inhibit ETC and, consequently, aspartate synthesis in vivo. Therefore, aspartate may be a limiting metabolite for tumour growth, and aspartate availability could be targeted for cancer therapy.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Antineoplastic Agents / pharmacology
  • Aspartic Acid / metabolism*
  • Biological Transport
  • Cell Line, Tumor
  • Cell Proliferation* / drug effects
  • Electron Transport Chain Complex Proteins / metabolism
  • Energy Metabolism* / drug effects
  • Excitatory Amino Acid Transporter 1 / genetics
  • Excitatory Amino Acid Transporter 1 / metabolism
  • Humans
  • Metabolomics / methods
  • Mice, Inbred NOD
  • Mice, SCID
  • Middle Aged
  • Mitochondria / metabolism
  • Neoplasms / drug therapy
  • Neoplasms / genetics
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Signal Transduction
  • Time Factors
  • Tumor Burden
  • Tumor Hypoxia*
  • Tumor Microenvironment*
  • Xenograft Model Antitumor Assays
  • Young Adult

Substances

  • Antineoplastic Agents
  • Electron Transport Chain Complex Proteins
  • Excitatory Amino Acid Transporter 1
  • SLC1A3 protein, human
  • Aspartic Acid