Transcription Factor KLF5 Binds a Cyclin E1 Polymorphic Intronic Enhancer to Confer Increased Bladder Cancer Risk

Mol Cancer Res. 2016 Nov;14(11):1078-1086. doi: 10.1158/1541-7786.MCR-16-0123. Epub 2016 Aug 11.

Abstract

It is well established that environmental toxins, such as exposure to arsenic, are risk factors in the development of urinary bladder cancer, yet recent genome-wide association studies (GWAS) provide compelling evidence that there is a strong genetic component associated with disease predisposition. A single-nucleotide polymorphism (SNP), rs8102137, was identified on chromosome 19q12, residing 6 kb upstream of the important cell-cycle regulator and proto-oncogene, Cyclin E1 (CCNE1). However, the functional role of this variant in bladder cancer predisposition has been unclear because it lies within a non-coding region of the genome. Here, it is demonstrated that bladder cancer cells heterozygous for this SNP exhibit biased allelic expression of CCNE1 with 1.5-fold more transcription occurring from the risk allele. Furthermore, using chromatin immunoprecipitation assays, a novel enhancer element was identified within the first intron of CCNE1 that binds Kruppel-like Factor 5 (KLF5), a known transcriptional activator in bladder cancer. Moreover, the data reveal that the presence of rs200996365, a SNP in high-linkage disequilibrium with rs8102137 residing in the center of a KLF5 motif, alters KLF5 binding to this genomic region. Through luciferase assays and CRISPR-Cas9 genome editing, a novel polymorphic intronic regulatory element controlling CCNE1 transcription is characterized. These studies uncover how a cancer-associated polymorphism mechanistically contributes to an increased predisposition for bladder cancer development.

Implications: A polymorphic KLF5 binding site near the CCNE1 gene explains genetic risk identified through GWAS. Mol Cancer Res; 14(11); 1078-86. ©2016 AACR.

MeSH terms

  • Cell Line, Tumor
  • Cyclin E / genetics*
  • Enhancer Elements, Genetic
  • Gene Expression Regulation, Neoplastic
  • Genetic Predisposition to Disease
  • Genome-Wide Association Study
  • Humans
  • Kruppel-Like Transcription Factors / metabolism*
  • Oncogene Proteins / genetics*
  • Polymorphism, Single Nucleotide*
  • Proto-Oncogene Mas
  • Urinary Bladder Neoplasms / genetics*

Substances

  • CCNE1 protein, human
  • Cyclin E
  • KLF5 protein, human
  • Kruppel-Like Transcription Factors
  • MAS1 protein, human
  • Oncogene Proteins
  • Proto-Oncogene Mas