Oxidative stress-inducible truncated serine/arginine-rich splicing factor 3 regulates interleukin-8 production in human colon cancer cells

Am J Physiol Cell Physiol. 2014 Feb 1;306(3):C250-62. doi: 10.1152/ajpcell.00091.2013. Epub 2013 Nov 27.

Abstract

Serine/arginine-rich splicing factor 3 (SRSF3) is a member of the SR protein family and plays wide-ranging roles in gene expression. The human SRSF3 gene generates two alternative splice transcripts, a major mRNA isoform (SRSF3-FL) encoding functional full-length protein and a premature termination codon (PTC)-containing isoform (SRSF3-PTC). The latter is degraded through nonsense-mediated mRNA decay (NMD). Treatment of a human colon cancer cell line (HCT116) with 100 μM sodium arsenite increased SRSF3-PTC mRNA levels without changing SRSF3-FL mRNA levels. A chemiluminescence-based NMD reporter assay system demonstrated that arsenite treatment inhibited NMD activity and increased SRSF3-PTC mRNA levels in the cytoplasm, facilitating translation of a truncated SRSF3 protein (SRSF3-TR) from SRSF3-PTC mRNA. SRSF3-TR lacked two-thirds of the Arg/Ser-rich (RS) domain whose phosphorylation state is known to be crucial for subcellular distribution. SRSF3-FL was localized in the nucleus, while overexpressed SRSF3-TR was diffusely distributed in the cytoplasm and the nucleus. A part of SRSF3-TR was also associated with stress granules in the cytoplasm. Interestingly, treatment of HCT116 cells with a small interference RNA specifically targeting SRSF3-PTC mRNA significantly attenuated arsenite-stimulated induction of c-JUN protein, its binding activity to the AP-1 binding site (-126 to 120 bp) in the interleukin (IL)-8 gene promoter, and AP-1 promoter activity, resulting in significant reduction of arsenite-stimulated IL-8 production. Our results suggest that SRSF3-TR may function as a positive regulator of oxidative stress-initiated inflammatory responses in colon cancer cells.

Keywords: IL-8; SRSF3 gene; alternative splicing; nonsense-mediated mRNA decay; oxidative stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing / genetics
  • Arsenites
  • Binding Sites
  • Cell Line, Tumor
  • Codon, Nonsense
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / metabolism*
  • Gene Expression Regulation, Neoplastic*
  • HCT116 Cells
  • Humans
  • Interleukin-8 / genetics*
  • Nonsense Mediated mRNA Decay / drug effects
  • Oxidative Stress / genetics*
  • Promoter Regions, Genetic
  • Protein Binding / genetics
  • Protein Isoforms / biosynthesis
  • Protein Isoforms / drug effects
  • Protein Isoforms / genetics
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins c-jun / biosynthesis
  • Proto-Oncogene Proteins c-jun / genetics
  • Proto-Oncogene Proteins c-jun / metabolism
  • RNA Interference
  • RNA, Small Interfering
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism*
  • Serine-Arginine Splicing Factors
  • Sodium Compounds
  • Transcription Factor AP-1 / metabolism

Substances

  • Arsenites
  • Codon, Nonsense
  • Interleukin-8
  • Protein Isoforms
  • Proto-Oncogene Proteins c-jun
  • RNA, Small Interfering
  • RNA-Binding Proteins
  • SRSF3 protein, human
  • Sodium Compounds
  • Transcription Factor AP-1
  • Serine-Arginine Splicing Factors
  • sodium arsenite