DICER1 mutations in familial multinodular goiter with and without ovarian Sertoli-Leydig cell tumors

JAMA. 2011 Jan 5;305(1):68-77. doi: 10.1001/jama.2010.1910.

Abstract

Context: Nontoxic multinodular goiter (MNG) is frequently observed in the general population, but little is known about the underlying genetic susceptibility to this disease. Familial cases of MNG have been reported, and published reports describe 5 families that also contain at least 1 individual with a Sertoli-Leydig cell tumor of the ovary (SLCT). Germline mutations in DICER1, a gene that codes for an RNase III endoribonuclease, have been identified in families affected by pleuropulmonary blastoma (PPB), some of whom include cases of MNG and gonadal tumors such as SLCTs.

Objective: To determine whether familial MNG with or without SLCT in the absence of PPB was associated with mutations in DICER1.

Design, setting, and patients: From September 2009 to September 2010, we screened 53 individuals from 2 MNG and 3 MNG/SLCT families at McGill University for mutations in DICER1. We investigated blood lymphocytes and MNG and SLCT tissue from family members for loss of the wild-type DICER1 allele (loss of heterozygosity), DICER1 expression, and microRNA (miRNA) dysregulation.

Main outcome measure: Detection of germline DICER1 gene mutations in familial MNG with and without SLCT.

Results: We identified and characterized germline DICER1 mutations in 37 individuals from 5 families. Two mutations were predicted to be protein truncating, 2 resulted in in-frame deletions, and 1 was a missense mutation. Molecular analysis of the 3 SLCTs showed no loss of heterozygosity of DICER1, and immunohistochemical analysis in 2 samples showed strong expression of DICER1 in Sertoli cells but weak staining of Leydig cells. miRNA profiling of RNA from lymphoblastoid cell lines from both affected and unaffected members of the familial MNG cases revealed miRNA perturbations in DICER1 mutation carriers.

Conclusions: DICER1 mutations are associated with both familial MNG and MNG with SLCT, independent of PPB. These germline DICER1 mutations are associated with dysregulation of miRNA expression patterns.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Child
  • DEAD-box RNA Helicases / genetics*
  • DNA Mutational Analysis
  • Female
  • Genetic Predisposition to Disease*
  • Germ-Line Mutation*
  • Goiter, Nodular / complications
  • Goiter, Nodular / genetics*
  • Humans
  • Male
  • MicroRNAs / metabolism
  • Mutation, Missense
  • Ovarian Neoplasms / complications
  • Ovarian Neoplasms / genetics*
  • Pulmonary Blastoma / complications
  • Pulmonary Blastoma / genetics
  • Ribonuclease III / genetics*
  • Sertoli-Leydig Cell Tumor / complications
  • Sertoli-Leydig Cell Tumor / genetics
  • Young Adult

Substances

  • MicroRNAs
  • DICER1 protein, human
  • Ribonuclease III
  • DEAD-box RNA Helicases

Supplementary concepts

  • Androblastoma of ovary
  • Pleuropulmonary blastoma