HuR is a post-transcriptional regulator of core metabolic enzymes in pancreatic cancer

RNA Biol. 2013 Aug;10(8):1312-23. doi: 10.4161/rna.25274. Epub 2013 Jun 13.

Abstract

Cancer cell metabolism differs from normal cells, yet the regulatory mechanisms responsible for these differences are incompletely understood, particularly in response to acute changes in the tumor microenvironment. HuR, an RNA-binding protein, acts under acute stress to regulate core signaling pathways in cancer through post-transcriptional regulation of mRNA targets. We demonstrate that HuR regulates the metabolic phenotype in pancreatic cancer cells and is critical for survival under acute glucose deprivation. Using three pancreatic cancer cell line models, HuR-proficient cells demonstrated superior survival under glucose deprivation when compared with isogenic cells with siRNA-silencing of HuR expression (HuR-deficient cells). We found that HuR-proficient cells utilized less glucose, but produced greater lactate, as compared with HuR-deficient cells. Acute glucose deprivation was found to act as a potent stimulus for HuR translocation from the nucleus to the cytoplasm, where HuR stabilizes its mRNA targets. We performed a gene expression array on ribonucleoprotein-immunoprecipitated mRNAs bound to HuR and identified 11 novel HuR target transcripts that encode enzymes central to glucose metabolism. Three (GPI, PRPS2 and IDH1) were selected for validation studies, and confirmed as bona fide HuR targets. These findings establish HuR as a critical regulator of pancreatic cancer cell metabolism and survival under acute glucose deprivation. Further explorations into HuR's role in cancer cell metabolism should uncover novel therapeutic targets that are critical for cancer cell survival in a metabolically compromised tumor microenvironment.

Keywords: HuR; cancer metabolism; pancreatic cancer; post-transcriptional gene regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • Cell Survival / genetics
  • Cell Survival / physiology
  • Cytokines / genetics
  • Cytokines / metabolism
  • ELAV Proteins / genetics
  • ELAV Proteins / metabolism
  • Gene Expression Regulation, Neoplastic
  • Glucose / genetics
  • Glucose / metabolism*
  • Glucose-6-Phosphate Isomerase / genetics
  • Glucose-6-Phosphate Isomerase / metabolism
  • Humans
  • Isocitrate Dehydrogenase / genetics
  • Isocitrate Dehydrogenase / metabolism
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / metabolism*
  • Protein Transport
  • RNA Processing, Post-Transcriptional*
  • RNA, Messenger / metabolism*
  • Reproducibility of Results
  • Stress, Physiological
  • Tumor Microenvironment

Substances

  • Cytokines
  • ELAV Proteins
  • RNA, Messenger
  • Isocitrate Dehydrogenase
  • IDH1 protein, human
  • GPI protein, human
  • Glucose-6-Phosphate Isomerase
  • Glucose