UV-Induced stabilization of c-fos and other short-lived mRNAs

Mol Cell Biol. 2000 May;20(10):3616-25. doi: 10.1128/MCB.20.10.3616-3625.2000.

Abstract

Irradiation of cells with short-wavelength ultraviolet light (UVC) changes the program of gene expression, in part within less than 15 min. As one of the immediate-early genes in response to UV, expression of the oncogene c-fos is upregulated. This immediate induction is regulated at the transcriptional level and is transient in character, due to the autocatalyzed shutoff of transcription and the rapid turnover of c-fos mRNA. In an experiment analyzing the kinetics of c-fos mRNA expression in murine fibroblasts irradiated with UVC, we found that, in addition to the initial transient induction, c-fos mRNA accumulated in a second wave starting at 4 to 5 h after irradiation, reaching a maximum at 8 h, and persisting for several more hours. It was accompanied by an increase in Fos protein synthesis. The second peak of c-fos RNA was caused by an UV dose-dependent increase in mRNA half-life from about 10 to 60 min. With similar kinetics, the mRNAs of other UV target genes (i.e., the Kin17 gene, c-jun, IkappaB, and c-myc) were stabilized (e.g., Kin17 RNA from 80 min to more than 8 h). The delayed response was not due to autocrine cytokine secretion with subsequent autostimulation of the secreting cells or to UV-induced growth factor receptor activation. Cells unable to repair UVC-induced DNA damage responded to lower doses of UVC with an even greater accumulation of c-fos and Kin17 mRNAs than repair-proficient wild-type cells, suggesting that a process in which a repair protein is involved regulates mRNA stability. Although resembling the induction of p53, a DNA damage-dependent increase in p53 was not a necessary intermediate in the stabilization reaction, since cells derived from p53 knockout mice showed the same pattern of c-fos and Kin17 mRNA accumulation as wild-type cells. The data indicate that the signal flow induced by UV radiation addresses not only protein stability (p53) and transcription but also RNA stability, a hitherto-unrecognized level of UV-induced regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Death
  • Cells, Cultured
  • DNA-Binding Proteins / genetics
  • Dose-Response Relationship, Radiation
  • Fibroblasts / cytology
  • Fibroblasts / radiation effects
  • Genes, Immediate-Early / radiation effects
  • Genes, fos / radiation effects
  • Genes, p53
  • Half-Life
  • Mice
  • Mice, Knockout
  • Nuclear Proteins*
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins c-fos / genetics*
  • Proto-Oncogene Proteins c-mdm2
  • RNA Stability / radiation effects*
  • RNA, Messenger / metabolism*
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Receptors, Growth Factor / metabolism
  • Time Factors
  • Transcription Factor AP-1 / metabolism
  • Transcriptional Activation
  • Ultraviolet Rays*
  • Xeroderma Pigmentosum Group A Protein

Substances

  • DNA-Binding Proteins
  • Nuclear Proteins
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-fos
  • RNA, Messenger
  • Receptors, Growth Factor
  • Transcription Factor AP-1
  • Xeroderma Pigmentosum Group A Protein
  • Xpa protein, mouse
  • Mdm2 protein, mouse
  • Proto-Oncogene Proteins c-mdm2
  • Receptor Protein-Tyrosine Kinases