The FOXA2 transcription factor is frequently somatically mutated in uterine carcinosarcomas and carcinomas

Cancer. 2018 Jan 1;124(1):65-73. doi: 10.1002/cncr.30971. Epub 2017 Sep 21.

Abstract

Background: Uterine carcinosarcomas (UCSs) are a rare but clinically aggressive form of cancer. They are biphasic tumors consisting of both epithelial and sarcomatous components. The majority of uterine carcinosarcomas are clonal, with the carcinomatous cells undergoing metaplasia to give rise to the sarcomatous component. The objective of the current study was to identify novel somatically mutated genes in UCSs.

Methods: We whole exome sequenced paired tumor and nontumor DNAs from 14 UCSs and orthogonally validated 464 somatic variants using Sanger sequencing. Fifteen genes that were somatically mutated in at least 2 tumor exomes were Sanger sequenced in another 39 primary UCSs.

Results: Overall, among 53 UCSs in the current study, the most frequently mutated of these 15 genes were tumor protein p53 (TP53) (75.5%), phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit alpha (PIK3CA) (34.0%), protein phosphatase 2, regulatory subunit A, alpha (PPP2R1A) (18.9%), F-box and WD repeat domain containing 7 (FBXW7) (18.9%), chromodomain helicase DNA binding protein 4 (CHD4) (17.0%), and forkhead box A2 (FOXA2) (15.1%). FOXA2 has not previously been implicated in UCSs and was predominated by frameshift and nonsense mutations. One UCS with a FOXA2 frameshift mutation expressed truncated FOXA2 protein by immunoblotting. Sequencing of FOXA2 in 160 primary endometrial carcinomas revealed somatic mutations in 5.7% of serous, 22.7% of clear cell, 9% of endometrioid, and 11.1% of mixed endometrial carcinomas, the majority of which were frameshift mutations.

Conclusions: Collectively, the findings of the current study provide compelling genetic evidence that FOXA2 is a pathogenic driver gene in the etiology of primary uterine cancers, including UCSs. Cancer 2018;124:65-73. © 2017 American Cancer Society.

Keywords: carcinosarcoma; endometrial cancer; endometrial carcinoma; exome; mutation; uterine cancer.

MeSH terms

  • Adenocarcinoma, Clear Cell / genetics
  • Autoantigens / genetics
  • Carcinoma / genetics*
  • Carcinoma, Endometrioid / genetics
  • Carcinosarcoma / genetics*
  • Cell Line, Tumor
  • Class I Phosphatidylinositol 3-Kinases / genetics
  • Endometrial Neoplasms / genetics
  • F-Box-WD Repeat-Containing Protein 7 / genetics
  • Female
  • Hepatocyte Nuclear Factor 3-beta / genetics
  • Humans
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex / genetics
  • Microsatellite Instability
  • Mutation
  • Neoplasms, Cystic, Mucinous, and Serous / genetics
  • Polymerase Chain Reaction
  • Protein Phosphatase 2 / genetics
  • Sequence Analysis, DNA
  • Tumor Suppressor Protein p53 / genetics
  • Uterine Neoplasms / genetics*

Substances

  • Autoantigens
  • CHD4 protein, human
  • F-Box-WD Repeat-Containing Protein 7
  • FBXW7 protein, human
  • FOXA2 protein, human
  • PPP2R1A protein, human
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Hepatocyte Nuclear Factor 3-beta
  • Class I Phosphatidylinositol 3-Kinases
  • PIK3CA protein, human
  • Protein Phosphatase 2
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex