Arsenite-induced pseudo-hypoxia results in loss of anchorage-dependent growth in BEAS-2B pulmonary epithelial cells

PLoS One. 2014 Dec 16;9(12):e114549. doi: 10.1371/journal.pone.0114549. eCollection 2014.

Abstract

Epidemiology studies have established a strong link between lung cancer and arsenic exposure. Currently, the role of disturbed cellular energy metabolism in carcinogenesis is a focus of scientific interest. Hypoxia inducible factor-1 alpha (HIF-1A) is a key regulator of energy metabolism, and it has been found to accumulate during arsenite exposure under oxygen-replete conditions. We modeled arsenic-exposed human pulmonary epithelial cells in vitro with BEAS-2B, a non-malignant lung epithelial cell line. Constant exposure to 1 µM arsenite (As) resulted in the early loss of anchorage-dependent growth, measured by soft agar colony formation, beginning at 6 weeks of exposure. This arsenite exposure resulted in HIF-1A accumulation and increased glycolysis, similar to the physiologic response to hypoxia, but in this case under oxygen-replete conditions. This "pseudo-hypoxia" response was necessary for the maximal acquisition of anchorage-independent growth in arsenite-exposed BEAS-2B. The HIF-1A accumulation and induction in glycolysis was sustained throughout a 52 week course of arsenite exposure in BEAS-2B. There was a time-dependent increase in anchorage-independent growth during the exposure to arsenite. When HIF-1A expression was stably suppressed, arsenite-induced glycolysis was abrogated, and the anchorage-independent growth was reduced. These findings establish that arsenite exerts a hypoxia-mimetic effect, which plays an important role in the subsequent gain of malignancy-associated phenotypes.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alveolar Epithelial Cells / drug effects
  • Alveolar Epithelial Cells / physiology*
  • Analysis of Variance
  • Arsenites / toxicity*
  • Cell Hypoxia / physiology
  • Cell Line
  • Energy Metabolism / physiology*
  • Fluorescent Antibody Technique
  • Gas Chromatography-Mass Spectrometry
  • Glycolysis / drug effects*
  • Half-Life
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Immunoblotting
  • Lactic Acid / metabolism
  • Metabolomics
  • Oligonucleotides
  • Real-Time Polymerase Chain Reaction

Substances

  • Arsenites
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Oligonucleotides
  • Lactic Acid
  • arsenite