A natural "GA" insertion mutation in the sequence encoding the 3'UTR of CXCL12/SDF-1α: Identification, characterization, and functional impact on mRNA splicing

Gene. 2019 Jan 10:681:36-44. doi: 10.1016/j.gene.2018.09.045. Epub 2018 Sep 28.

Abstract

The CXCL12 gene produces a series of transcript variants through alternative splicing at the 3' end of its pre-mRNA. This study explores the biological activities of these alternative transcripts and the mechanisms involved in the regulation of CXCL12 transcription and RNA splicing. We identified a "GA" insertion mutation in the region of CXCL12α DNA encoding the conserved 3'UTR. This variant transcript was named CXCL12-3'GA+. The mutation occurred at a frequency of 13.2% in healthy Chinese individuals. However, its frequency in healthy Caucasians was 22.6%, significantly higher than what was observed in the Chinese. Genomic analysis indicated that the GA+ mutation likely encodes a G-quadruplex structure in close proximity to a cluster of important AU-rich elements (AREs) that are well-established regulators of mRNA stability at the 3'UTR. Experiments using molecular constructs encoding the 3'UTR of CXCL12 revealed that the GA+ allele can significantly increase gene expression compared to the WT allele. Further studies uncovered that the WT allele was associated with the production of a 225-bp minor transcript isoform (MTI) through alternative splicing resulting in the deletion of exon 2. ARMS-PCR using samples collected from cultured PBMCs of WT/GA+ genotype carriers indicated that the GA+ allele was preferentially transcribed compared to the WT allele. In summary, the study demonstrates that a GA insertion in the region encoding the 3'UTR of CXCL12α may affect gene expression through alternative mRNA splicing. This finding provides a basis for understanding how multiple elements in the sequence encoding the 3'UTR of the CXCL12 gene regulates its transcription and may lead to insights about diseases involving abnormal CXCL12α expression.

Keywords: 3′ untranslated region (3′UTR); Chemokine CXCL12; G-quadruplexes; Minor transcript isoform (MTI); Mutation; Transcription.

MeSH terms

  • 3' Untranslated Regions / genetics*
  • Alternative Splicing / genetics
  • Animals
  • Asian People / genetics
  • Base Sequence
  • Cells, Cultured
  • Chemokine CXCL12 / genetics*
  • Cloning, Molecular
  • DNA Mutational Analysis
  • Gene Frequency
  • HeLa Cells
  • Humans
  • Mice
  • Mutagenesis, Insertional*
  • Protein Isoforms / genetics
  • RNA Splicing / genetics*
  • RNA Stability / genetics
  • White People / genetics

Substances

  • 3' Untranslated Regions
  • CXCL12 protein, human
  • Chemokine CXCL12
  • Protein Isoforms