Transcription Factor GLIS3: A New and Critical Regulator of Postnatal Stages of Mouse Spermatogenesis

Stem Cells. 2016 Nov;34(11):2772-2783. doi: 10.1002/stem.2449. Epub 2016 Jul 11.

Abstract

In this study, we identify a novel and essential role for the Krüppel-like zinc finger transcription factor GLI-similar 3 (GLIS3) in the regulation of postnatal spermatogenesis. We show that GLIS3 is expressed in gonocytes, spermatogonial stem cells (SSCs) and spermatogonial progenitors (SPCs), but not in differentiated spermatogonia and later stages of spermatogenesis or in somatic cells. Spermatogenesis is greatly impaired in GLIS3 knockout mice. Loss of GLIS3 function causes a moderate reduction in the number of gonocytes, but greatly affects the generation of SSCs/SPCs, and as a consequence the development of spermatocytes. Gene expression profiling demonstrated that the expression of genes associated with undifferentiated spermatogonia was dramatically decreased in GLIS3-deficient mice and that the cytoplasmic-to-nuclear translocation of FOXO1, which marks the gonocyte-to-SSC transition and is necessary for SSC self-renewal, is inhibited. These observations suggest that GLIS3 promotes the gonocyte-to-SSC transition and is a critical regulator of the dynamics of early postnatal spermatogenesis. Stem Cells 2016;34:2772-2783.

Keywords: GLIS3; Gene expression; Spermatogenesis; Spermatogonial stem cell.

MeSH terms

  • Animals
  • Cell Differentiation
  • DNA-Binding Proteins
  • Forkhead Box Protein O1 / genetics
  • Forkhead Box Protein O1 / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Protein Transport
  • Repressor Proteins / deficiency
  • Repressor Proteins / genetics*
  • Spermatocytes / cytology
  • Spermatocytes / metabolism*
  • Spermatogenesis / genetics*
  • Spermatogonia / cytology
  • Spermatogonia / metabolism*
  • Stem Cells / cytology
  • Stem Cells / metabolism*
  • Testis / cytology
  • Testis / metabolism*
  • Trans-Activators / deficiency
  • Trans-Activators / genetics*

Substances

  • DNA-Binding Proteins
  • Forkhead Box Protein O1
  • Foxo1 protein, mouse
  • Glis3 protein, mouse
  • Repressor Proteins
  • Trans-Activators