Discovery of biclonal origin and a novel oncogene SLC12A5 in colon cancer by single-cell sequencing

Cell Res. 2014 Jun;24(6):701-12. doi: 10.1038/cr.2014.43. Epub 2014 Apr 4.

Abstract

Single-cell sequencing is a powerful tool for delineating clonal relationship and identifying key driver genes for personalized cancer management. Here we performed single-cell sequencing analysis of a case of colon cancer. Population genetics analyses identified two independent clones in tumor cell population. The major tumor clone harbored APC and TP53 mutations as early oncogenic events, whereas the minor clone contained preponderant CDC27 and PABPC1 mutations. The absence of APC and TP53 mutations in the minor clone supports that these two clones were derived from two cellular origins. Examination of somatic mutation allele frequency spectra of additional 21 whole-tissue exome-sequenced cases revealed the heterogeneity of clonal origins in colon cancer. Next, we identified a mutated gene SLC12A5 that showed a high frequency of mutation at the single-cell level but exhibited low prevalence at the population level. Functional characterization of mutant SLC12A5 revealed its potential oncogenic effect in colon cancer. Our study provides the first exome-wide evidence at single-cell level supporting that colon cancer could be of a biclonal origin, and suggests that low-prevalence mutations in a cohort may also play important protumorigenic roles at the individual level.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenomatous Polyposis Coli Protein / genetics
  • Adenomatous Polyposis Coli Protein / metabolism
  • Apc3 Subunit, Anaphase-Promoting Complex-Cyclosome / genetics
  • Apc3 Subunit, Anaphase-Promoting Complex-Cyclosome / metabolism
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology
  • Genotype
  • High-Throughput Nucleotide Sequencing*
  • Humans
  • K Cl- Cotransporters
  • Male
  • Middle Aged
  • Mutation
  • Oncogenes
  • Poly(A)-Binding Proteins / genetics
  • Poly(A)-Binding Proteins / metabolism
  • Principal Component Analysis
  • Sequence Analysis, DNA
  • Symporters / chemistry
  • Symporters / genetics
  • Symporters / metabolism*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • APC protein, human
  • Adenomatous Polyposis Coli Protein
  • Apc3 Subunit, Anaphase-Promoting Complex-Cyclosome
  • CDC27 protein, human
  • PABPC1L protein, human
  • Poly(A)-Binding Proteins
  • Symporters
  • Tumor Suppressor Protein p53