Clonal evolution in paired endometrial intraepithelial neoplasia/atypical hyperplasia and endometrioid adenocarcinoma

Hum Pathol. 2017 Sep:67:69-77. doi: 10.1016/j.humpath.2017.07.003. Epub 2017 Jul 14.

Abstract

Endometrial intraepithelial neoplasia (EIN) and atypical endometrial hyperplasia (AH) are histomorphologically defined precursors to endometrioid adenocarcinoma, which are unified as EIN/AH by the World Health Organization. EIN/AH harbors a constellation of molecular alterations similar to those found in endometrioid adenocarcinoma. However, the process of clonal evolution from EIN/AH to carcinoma is poorly characterized. To investigate, we performed next-generation sequencing, copy number alteration (CNA) analysis, and immunohistochemistry for mismatch repair protein expression on EIN/AH and endometrioid adenocarcinoma samples from 6 hysterectomy cases with spatially distinct EIN/AH and carcinoma. In evaluating all samples, EIN/AH and carcinoma did not differ in mutational burden, CNA burden, or specific genes mutated (all P>.1). All paired EIN/AH and carcinoma samples shared at least one identical somatic mutation, frequently in PI(3)K pathway members. Large CNAs (>10 genes in length) were identified in 83% of cases; paired EIN/AH and carcinoma samples shared at least one identical CNA in these cases. Mismatch repair protein expression matched in all paired EIN/AH and carcinoma samples. All paired EIN/AH and carcinoma samples had identical The Cancer Genome Atlas subtype, with 3 classified as "copy number low endometrioid" and 3 classified as "microsatellite instability hypermutated." Although paired EIN/AH and carcinoma samples were clonal, private mutations (ie, present in only one sample) were identified in EIN/AH and carcinoma in all cases, frequently in established cancer-driving genes. These findings indicate that EIN/AH gives rise to endometrioid adenocarcinoma by a complex process of subclone evolution, not a linear accumulation of molecular events.

Keywords: Clonal evolution; Endometrial hyperplasia; Endometrial intraepithelial neoplasia; Endometrioid adenocarcinoma; Next generation sequencing.

Publication types

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

MeSH terms

  • Aged
  • Aged, 80 and over
  • Biomarkers, Tumor / analysis
  • Biomarkers, Tumor / genetics*
  • Biopsy
  • Carcinoma in Situ / enzymology
  • Carcinoma in Situ / genetics*
  • Carcinoma in Situ / pathology
  • Carcinoma in Situ / surgery
  • Carcinoma, Endometrioid / enzymology
  • Carcinoma, Endometrioid / genetics*
  • Carcinoma, Endometrioid / pathology
  • Carcinoma, Endometrioid / surgery
  • Cell Proliferation
  • Clonal Evolution*
  • DNA Copy Number Variations
  • DNA Mismatch Repair
  • DNA Repair Enzymes / analysis
  • Disease Progression
  • Endometrial Hyperplasia / enzymology
  • Endometrial Hyperplasia / genetics*
  • Endometrial Hyperplasia / pathology
  • Endometrial Hyperplasia / surgery
  • Endometrial Neoplasms / enzymology
  • Endometrial Neoplasms / genetics*
  • Endometrial Neoplasms / pathology
  • Endometrial Neoplasms / surgery
  • Female
  • Gene Dosage
  • Genetic Predisposition to Disease
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Hysterectomy
  • Immunohistochemistry
  • Microsatellite Instability
  • Middle Aged
  • Mutation
  • Phenotype

Substances

  • Biomarkers, Tumor
  • DNA Repair Enzymes