RHOX10 drives mouse spermatogonial stem cell establishment through a transcription factor signaling cascade

Cell Rep. 2021 Jul 20;36(3):109423. doi: 10.1016/j.celrep.2021.109423.

Abstract

Spermatogonial stem cells (SSCs) are essential for male fertility. Here, we report that mouse SSC generation is driven by a transcription factor (TF) cascade controlled by the homeobox protein, RHOX10, which acts by driving the differentiation of SSC precursors called pro-spermatogonia (ProSG). We identify genes regulated by RHOX10 in ProSG in vivo and define direct RHOX10-target genes using several approaches, including a rapid temporal induction assay: iSLAMseq. Together, these approaches identify temporal waves of RHOX10 direct targets, as well as RHOX10 secondary-target genes. Many of the RHOX10-regulated genes encode proteins with known roles in SSCs. Using an in vitro ProSG differentiation assay, we find that RHOX10 promotes mouse ProSG differentiation through a conserved transcriptional cascade involving the key germ-cell TFs DMRT1 and ZBTB16. Our study gives important insights into germ cell development and provides a blueprint for how to define TF cascades.

Keywords: DMRT1; RHOX10; SLAM-seq; ZBTB16; gonocyte; homeobox; pro-spermatogonia; single-cell RNA-seq; spermatogonial stem cells; transcription factor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Base Sequence
  • Cell Differentiation / genetics
  • Gene Expression Regulation, Developmental
  • Genome
  • Germ Cells / metabolism
  • HEK293 Cells
  • Homeodomain Proteins / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Promyelocytic Leukemia Zinc Finger Protein / metabolism
  • Signal Transduction*
  • Spermatogonia / cytology*
  • Stem Cells / cytology*
  • Stem Cells / metabolism*
  • Transcription Factors / metabolism*
  • Transcription, Genetic
  • Transcriptional Activation / genetics

Substances

  • DMRT1 protein
  • Homeodomain Proteins
  • Promyelocytic Leukemia Zinc Finger Protein
  • Rhox10 protein, mouse
  • Transcription Factors
  • Zbtb16 protein, mouse