Combined steroidogenic characters of fetal adrenal and Leydig cells in childhood adrenocortical carcinoma

J Steroid Biochem Mol Biol. 2016 May:159:86-93. doi: 10.1016/j.jsbmb.2016.02.031. Epub 2016 Mar 3.

Abstract

Although childhood adrenocortical carcinomas (c-ACCs) with a TP53 mutation are known to produce androgens, detailed steroidogenic characters have not been clarified. Here, we examined steroid metabolite profiles and expression patterns of steroidogenic genes in a c-ACC removed from the left adrenal position of a 2-year-old Brazilian boy with precocious puberty, using an atrophic left adrenal gland removed at the time of tumorectomy as a control. The c-ACC produced not only abundant dehydroepiandrosterone-sulfate but also a large amount of testosterone via the Δ5 pathway with Δ5-androstenediol rather than Δ4-androstenedione as the primary intermediate metabolite. Furthermore, the c-ACC was associated with elevated expressions of CYP11A1, CYP17A1, POR, HSD17B3, and SULT2A1, a low but similar expression of CYB5A, and reduced expressions of AKR1C3 (HSD17B5) and HSD3B2. Notably, a Leydig cell marker INSL3 was expressed at a low but detectable level in the c-ACC. Furthermore, molecular studies revealed a maternally inherited heterozygous germline TP53 mutation, and several post-zygotic genetic aberrations in the c-ACC including loss of paternally derived chromosome 17 with a wildtype TP53 and loss of maternally inherited chromosome 11 and resultant marked hyperexpression of paternally expressed growth promoting gene IGF2 and drastic hypoexpression of maternally expressed growth suppressing gene CDKN1C. These results imply the presence of combined steroidogenic properties of fetal adrenal and Leydig cells in this patient's c-ACC with a germline TP53 mutation and several postzygotic carcinogenic events.

Keywords: Adrenocortical carcinoma; Androgen production; Steroidogenesis; TP53; Tumorigenesis.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenal Cortex Neoplasms / diagnosis*
  • Adrenal Cortex Neoplasms / genetics
  • Adrenal Cortex Neoplasms / metabolism
  • Adrenal Glands / pathology
  • Adrenocortical Carcinoma / diagnosis*
  • Adrenocortical Carcinoma / genetics
  • Adrenocortical Carcinoma / metabolism
  • Base Sequence
  • Biomarkers, Tumor / metabolism*
  • Biosynthetic Pathways
  • Cell Line, Tumor
  • Child, Preschool
  • Cholesterol Side-Chain Cleavage Enzyme / metabolism
  • Comparative Genomic Hybridization
  • DNA Mutational Analysis
  • Gene Expression
  • Germ-Line Mutation
  • Humans
  • Insulin / metabolism
  • Leydig Cells / metabolism*
  • Lipid Metabolism
  • Male
  • Pedigree
  • Proteins / metabolism
  • Steroid 17-alpha-Hydroxylase / metabolism
  • Tumor Suppressor Protein p53 / genetics

Substances

  • Biomarkers, Tumor
  • Insulin
  • Leydig insulin-like protein
  • Proteins
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • CYP17A1 protein, human
  • Steroid 17-alpha-Hydroxylase
  • Cholesterol Side-Chain Cleavage Enzyme