Genetic alterations associated with progression from pancreatic intraepithelial neoplasia to invasive pancreatic tumor

Gastroenterology. 2013 Nov;145(5):1098-1109.e1. doi: 10.1053/j.gastro.2013.07.049. Epub 2013 Aug 2.

Abstract

Background & aims: Increasing grade of pancreatic intraepithelial neoplasia (PanIN) has been associated with progression to pancreatic ductal adenocarcinoma (PDAC). However, the mechanisms that control progression from PanINs to PDAC are not well understood. We investigated the genetic alterations involved in this process.

Methods: Genomic DNA samples from laser-capture microdissected PDACs and adjacent PanIN2 and PanIN3 lesions from 10 patients with pancreatic cancer were analyzed by exome sequencing.

Results: Similar numbers of somatic mutations were identified in PanINs and tumors, but the mutational load varied greatly among cases. Ten of the 15 isolated PanINs shared more than 50% of somatic mutations with associated tumors. Mutations common to tumors and clonally related PanIN2 and PanIN3 lesions were identified as genes that could promote carcinogenesis. KRAS and TP53 frequently were altered in PanINs and tumors, but few other recurrently modified genes were detected. Mutations in DNA damage response genes were prevalent in all samples. Genes that encode proteins involved in gap junctions, the actin cytoskeleton, the mitogen-activated protein kinase signaling pathway, axon guidance, and cell-cycle regulation were among the earliest targets of mutagenesis in PanINs that progressed to PDAC.

Conclusions: Early stage PanIN2 lesions appear to contain many of the somatic gene alterations required for PDAC development.

Keywords: AAF; ATM; LCM; P; PDAC; PanIN; Pancreas; PxT; SNV; T; Tumorigenesis; WGA; Whole-Genome Amplification; alternate allele frequency; ataxia telangiectasia mutated; laser capture microdissection; pancreatic ductal adenocarcinoma; pancreatic intraepithelial neoplasia; pancreatic intraepithelial neoplasia alone; single-nucleotide variant; tumor; tumors and adjacent pancreatic intraepithelial neoplasia; whole-genome amplification.

Publication types

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

MeSH terms

  • Adenocarcinoma / genetics*
  • Adenocarcinoma / pathology
  • Carcinogenesis / genetics
  • Carcinogenesis / pathology
  • Carcinoma in Situ / genetics*
  • Carcinoma in Situ / pathology
  • DNA, Neoplasm / genetics
  • Disease Progression*
  • Humans
  • Mutation / genetics
  • Neoplasm Invasiveness / genetics*
  • Neoplasm Invasiveness / pathology
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / pathology
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins p21(ras)
  • Retrospective Studies
  • Tumor Suppressor Protein p53 / genetics
  • ras Proteins / genetics

Substances

  • DNA, Neoplasm
  • KRAS protein, human
  • Proto-Oncogene Proteins
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Proto-Oncogene Proteins p21(ras)
  • ras Proteins