Tumor necrosis factor-alpha increases reactive oxygen species by inducing spermine oxidase in human lung epithelial cells: a potential mechanism for inflammation-induced carcinogenesis

Cancer Res. 2006 Dec 1;66(23):11125-30. doi: 10.1158/0008-5472.CAN-06-3174.

Abstract

Inflammation has been implicated in the development of many human epithelial cancers, including those of the stomach, lung, colon, and prostate. Tumor necrosis factor-alpha (TNF-alpha) is a potent pleiotropic, proinflammatory cytokine produced by many cells in response to injury and inflammation. Here, we show that TNF-alpha exposure results in increased production of reactive oxygen species (ROS), with a concomitant increase in the production of 8-oxo-deoxyguanosine, a marker for oxidative DNA damage, in human lung bronchial epithelial cells. The source of the ROS in TNF-alpha-treated cells was determined by both pharmacologic and small interfering RNA (siRNA) strategies to be spermine oxidase (SMO/PAOh1). SMO/PAOh1 oxidizes spermine into spermidine, 3-aminopropanal, and H(2)O(2). Inhibition of TNF-alpha-induced SMO/PAOh1 activity with MDL 72,527 or with a targeted siRNA prevented ROS production and oxidative DNA damage. Further, similar induction in SMO/PAOh1 is observed with treatment of another inflammatory cytokine, interleukin-6. The data are consistent with a model that directly links inflammation and DNA damage through the production of H(2)O(2) by SMO/PAOh1. Further, these results suggest a common mechanism by which inflammation from multiple sources can lead to the mutagenic changes necessary for the development and progression of epithelial cancers.

Publication types

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

MeSH terms

  • Acetyltransferases / genetics
  • Acetyltransferases / metabolism
  • Aged
  • Amino Acid Sequence
  • Blotting, Western
  • Cell Line
  • Cell Line, Transformed
  • DNA Damage
  • Dose-Response Relationship, Drug
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects*
  • Epithelial Cells / metabolism
  • Female
  • Humans
  • Hydrogen Peroxide / metabolism
  • Inflammation / complications
  • Inflammation / genetics
  • Inflammation / metabolism
  • Lung / cytology
  • Molecular Sequence Data
  • Neoplasms / etiology
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Oxidation-Reduction / drug effects
  • Oxidoreductases Acting on CH-NH Group Donors / genetics
  • Oxidoreductases Acting on CH-NH Group Donors / metabolism*
  • Polyamine Oxidase
  • RNA, Small Interfering / genetics
  • Reactive Oxygen Species / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Spermine / metabolism
  • Transfection
  • Tumor Necrosis Factor-alpha / pharmacology*

Substances

  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • Spermine
  • Hydrogen Peroxide
  • Oxidoreductases Acting on CH-NH Group Donors
  • Acetyltransferases
  • diamine N-acetyltransferase