A recurrent p.Arg92Trp variant in steroidogenic factor-1 (NR5A1) can act as a molecular switch in human sex development

Hum Mol Genet. 2016 Aug 15;25(16):3446-3453. doi: 10.1093/hmg/ddw186. Epub 2016 Jul 4.

Abstract

Cell lineages of the early human gonad commit to one of the two mutually antagonistic organogenetic fates, the testis or the ovary. Some individuals with a 46,XX karyotype develop testes or ovotestes (testicular or ovotesticular disorder of sex development; TDSD/OTDSD), due to the presence of the testis-determining gene, SRY Other rare complex syndromic forms of TDSD/OTDSD are associated with mutations in pro-ovarian genes that repress testis development (e.g. WNT4); however, the genetic cause of the more common non-syndromic forms is unknown. Steroidogenic factor-1 (known as NR5A1) is a key regulator of reproductive development and function. Loss-of-function changes in NR5A1 in 46,XY individuals are associated with a spectrum of phenotypes in humans ranging from a lack of testis formation to male infertility. Mutations in NR5A1 in 46,XX women are associated with primary ovarian insufficiency, which includes a lack of ovary formation, primary and secondary amenorrhoea as well as early menopause. Here, we show that a specific recurrent heterozygous missense mutation (p.Arg92Trp) in the accessory DNA-binding region of NR5A1 is associated with variable degree of testis development in 46,XX children and adults from four unrelated families. Remarkably, in one family a sibling raised as a girl and carrying this NR5A1 mutation was found to have a 46,XY karyotype with partial testicular dysgenesis. These unique findings highlight how a specific variant in a developmental transcription factor can switch organ fate from the ovary to testis in mammals and represents the first missense mutation causing isolated, non-syndromic 46,XX testicular/ovotesticular DSD in humans.

MeSH terms

  • Adult
  • Androgen-Insensitivity Syndrome / genetics
  • Androgen-Insensitivity Syndrome / pathology
  • Cell Lineage / genetics
  • Child
  • DNA-Binding Proteins / genetics*
  • Disorder of Sex Development, 46,XY / genetics*
  • Disorder of Sex Development, 46,XY / pathology
  • Female
  • Gonads / growth & development
  • Gonads / pathology
  • Humans
  • Karyotype
  • Male
  • Mutation, Missense
  • Ovary / growth & development
  • Ovary / pathology
  • Pedigree
  • Primary Ovarian Insufficiency / genetics*
  • Primary Ovarian Insufficiency / pathology
  • Sex Determination Processes
  • Sexual Development / genetics*
  • Steroidogenic Factor 1 / genetics*
  • Testis / growth & development
  • Testis / pathology

Substances

  • DNA-Binding Proteins
  • NR5A1 protein, human
  • Steroidogenic Factor 1