High-throughput detection of clinically relevant mutations in archived tumor samples by multiplexed PCR and next-generation sequencing

Clin Cancer Res. 2014 Apr 15;20(8):2080-91. doi: 10.1158/1078-0432.CCR-13-3114. Epub 2014 Feb 26.

Abstract

Purpose: Tailoring cancer treatment to tumor molecular characteristics promises to make personalized medicine a reality. However, reliable genetic profiling of archived clinical specimens has been hindered by limited sensitivity and high false-positive rates. Here, we describe a novel methodology, MMP-seq, which enables sensitive and specific high-throughput, high-content genetic profiling in archived clinical samples.

Experimental design: We first validated the technical performance of MMP-seq in 66 cancer cell lines and a Latin square cross-dilution of known somatic mutations. We next characterized the performance of MMP-seq in 17 formalin-fixed paraffin-embedded (FFPE) clinical samples using matched fresh-frozen tissue from the same tumors as benchmarks. To demonstrate the potential clinical utility of our methodology, we profiled FFPE tumor samples from 73 patients with endometrial cancer.

Results: We demonstrated that MMP-seq enabled rapid and simultaneous profiling of a panel of 88 cancer genes in 48 samples, and detected variants at frequencies as low as 0.4%. We identified DNA degradation and deamination as the main error sources and developed practical and robust strategies for mitigating these issues, and dramatically reduced the false-positive rate. Applying MMP-seq to a cohort of endometrial tumor samples identified extensive, potentially actionable alterations in the PI3K (phosphoinositide 3-kinase) and RAS pathways, including novel PIK3R1 hotspot mutations that may disrupt negative regulation of PIK3CA.

Conclusions: MMP-seq provides a robust solution for comprehensive, reliable, and high-throughput genetic profiling of clinical tumor samples, paving the way for the incorporation of genomic-based testing into clinical investigation and practice.

MeSH terms

  • Cell Line, Tumor
  • Class I Phosphatidylinositol 3-Kinases
  • Class Ia Phosphatidylinositol 3-Kinase
  • DNA Mutational Analysis / methods
  • DNA, Neoplasm / genetics
  • DNA, Neoplasm / metabolism
  • ErbB Receptors / genetics
  • Genotyping Techniques
  • High-Throughput Nucleotide Sequencing / methods*
  • Humans
  • MCF-7 Cells
  • Multiplex Polymerase Chain Reaction / methods*
  • Mutation*
  • Neoplasms / genetics*
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • PTEN Phosphohydrolase / genetics
  • Paraffin Embedding
  • Phosphatidylinositol 3-Kinases / genetics
  • Proto-Oncogene Proteins B-raf / genetics
  • Reproducibility of Results
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism
  • ras Proteins / genetics

Substances

  • DNA, Neoplasm
  • Tumor Suppressor Proteins
  • PIK3R1 protein, human
  • Class I Phosphatidylinositol 3-Kinases
  • Class Ia Phosphatidylinositol 3-Kinase
  • PIK3CA protein, human
  • ErbB Receptors
  • Proto-Oncogene Proteins B-raf
  • PTEN Phosphohydrolase
  • ras Proteins