Clonal Expansion and Diversification of Cancer-Associated Mutations in Endometriosis and Normal Endometrium

Cell Rep. 2018 Aug 14;24(7):1777-1789. doi: 10.1016/j.celrep.2018.07.037.

Abstract

Endometriosis is characterized by ectopic endometrial-like epithelium and stroma, of which molecular characteristics remain to be fully elucidated. We sequenced 107 ovarian endometriotic and 82 normal uterine endometrial epithelium samples isolated by laser microdissection. In both endometriotic and normal epithelium samples, numerous somatic mutations were identified within genes frequently mutated in endometriosis-associated ovarian cancers. KRAS is frequently mutated in endometriotic epithelium, with a higher mutant allele frequency (MAF) accompanied by arm-level allelic imbalances. Analyses of MAF, combined with multiregional sequencing, illuminated spatiotemporal evolution of the endometriosis and uterine endometrium genomes. We sequenced 109 single endometrial glands and found that each gland carried distinct cancer-associated mutations, demonstrating the heterogeneity of the genomic architecture of endometrial epithelium. Remarkable increases in MAF of mutations in cancer-associated genes in endometriotic epithelium suggest retrograde flow of endometrial cells already harboring cancer-associated mutations, with selective advantages at ectopic sites, leading to the development of endometriosis.

Keywords: clonal evolution; endometrial gland; endometriosis; epithelial cell; genomic heterogeneity; multiregional sequencing; next-generation sequencing; ovarian cancer; somatic mutation; uterine endometrium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Carcinogenesis / genetics
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Class I Phosphatidylinositol 3-Kinases / genetics
  • Class I Phosphatidylinositol 3-Kinases / metabolism
  • Class Ia Phosphatidylinositol 3-Kinase
  • Clone Cells
  • Endometrial Neoplasms / genetics*
  • Endometrial Neoplasms / metabolism
  • Endometrial Neoplasms / pathology
  • Endometriosis / genetics*
  • Endometriosis / metabolism
  • Endometriosis / pathology
  • Endometrium / metabolism
  • Endometrium / pathology
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • F-Box-WD Repeat-Containing Protein 7 / genetics
  • F-Box-WD Repeat-Containing Protein 7 / metabolism
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic*
  • Gene Frequency
  • Genome, Human
  • Humans
  • Laser Capture Microdissection
  • Middle Aged
  • Mutation*
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Phosphatase 2 / genetics
  • Protein Phosphatase 2 / metabolism
  • Proto-Oncogene Proteins p21(ras) / genetics*
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • Whole Genome Sequencing

Substances

  • F-Box-WD Repeat-Containing Protein 7
  • FBXW7 protein, human
  • KRAS protein, human
  • PPP2R1A protein, human
  • PIK3R1 protein, human
  • Class I Phosphatidylinositol 3-Kinases
  • Class Ia Phosphatidylinositol 3-Kinase
  • PIK3CA protein, human
  • Protein Phosphatase 2
  • Proto-Oncogene Proteins p21(ras)