Structure-function analysis of mouse Sry reveals dual essential roles of the C-terminal polyglutamine tract in sex determination

Proc Natl Acad Sci U S A. 2014 Aug 12;111(32):11768-73. doi: 10.1073/pnas.1400666111. Epub 2014 Jul 29.

Abstract

The mammalian sex-determining factor SRY comprises a conserved high-mobility group (HMG) box DNA-binding domain and poorly conserved regions outside the HMG box. Mouse Sry is unusual in that it includes a C-terminal polyglutamine (polyQ) tract that is absent in nonrodent SRY proteins, and yet, paradoxically, is essential for male sex determination. To dissect the molecular functions of this domain, we generated a series of Sry mutants, and studied their biochemical properties in cell lines and transgenic mouse embryos. Sry protein lacking the polyQ domain was unstable, due to proteasomal degradation. Replacing this domain with irrelevant sequences stabilized the protein but failed to restore Sry's ability to up-regulate its key target gene SRY-box 9 (Sox9) and its sex-determining function in vivo. These functions were restored only when a VP16 transactivation domain was substituted. We conclude that the polyQ domain has important roles in protein stabilization and transcriptional activation, both of which are essential for male sex determination in mice. Our data disprove the hypothesis that the conserved HMG box domain is the only functional domain of Sry, and highlight an evolutionary paradox whereby mouse Sry has evolved a novel bifunctional module to activate Sox9 directly, whereas SRY proteins in other taxa, including humans, seem to lack this ability, presumably making them dependent on partner proteins(s) to provide this function.

Keywords: TESCO; Y chromosome; sex development; testis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Evolution, Molecular
  • Female
  • Genes, Reporter
  • Genes, sry*
  • Male
  • Mice
  • Mice, Transgenic
  • Mutagenesis
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Peptides / chemistry
  • Pregnancy
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Denaturation
  • Protein Stability
  • Protein Structure, Tertiary
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism
  • Sequence Deletion
  • Sex Determination Processes*
  • Sex-Determining Region Y Protein / chemistry
  • Sex-Determining Region Y Protein / genetics*
  • Sex-Determining Region Y Protein / metabolism*
  • Transcriptional Activation

Substances

  • Peptide Fragments
  • Peptides
  • SOX9 Transcription Factor
  • Sex-Determining Region Y Protein
  • Sox9 protein, mouse
  • Sry protein, mouse
  • polyglutamine
  • Proteasome Endopeptidase Complex