SCML2 establishes the male germline epigenome through regulation of histone H2A ubiquitination

Dev Cell. 2015 Mar 9;32(5):574-88. doi: 10.1016/j.devcel.2015.01.014. Epub 2015 Feb 19.

Abstract

Gametogenesis is dependent on the expression of germline-specific genes. However, it remains unknown how the germline epigenome is distinctly established from that of somatic lineages. Here we show that genes commonly expressed in somatic lineages and spermatogenesis-progenitor cells undergo repression in a genome-wide manner in late stages of the male germline and identify underlying mechanisms. SCML2, a germline-specific subunit of a Polycomb repressive complex 1 (PRC1), establishes the unique epigenome of the male germline through two distinct antithetical mechanisms. SCML2 works with PRC1 and promotes RNF2-dependent ubiquitination of H2A, thereby marking somatic/progenitor genes on autosomes for repression. Paradoxically, SCML2 also prevents RNF2-dependent ubiquitination of H2A on sex chromosomes during meiosis, thereby enabling unique epigenetic programming of sex chromosomes for male reproduction. Our results reveal divergent mechanisms involving a shared regulator by which the male germline epigenome is distinguished from that of the soma and progenitor cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Biomarkers / metabolism
  • Blotting, Western
  • Cell Cycle Proteins
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • Chromosomal Proteins, Non-Histone
  • Epigenomics*
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental*
  • Gene Silencing
  • Germ Cells
  • Histones / metabolism*
  • Immunoenzyme Techniques
  • Intracellular Signaling Peptides and Proteins / physiology
  • Male
  • Meiosis / genetics
  • Mice
  • Mice, Knockout
  • Oligonucleotide Array Sequence Analysis
  • Polycomb Repressive Complex 1 / genetics
  • Polycomb Repressive Complex 1 / metabolism*
  • Polycomb Repressive Complex 1 / physiology
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Repressor Proteins / physiology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sex Chromosomes / genetics
  • Spermatogenesis
  • Testis / cytology
  • Testis / metabolism*
  • Ubiquitin / metabolism*
  • Ubiquitin-Protein Ligases / physiology
  • Ubiquitination

Substances

  • Adaptor Proteins, Signal Transducing
  • Biomarkers
  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Dppa3 protein, mouse
  • Histones
  • Intracellular Signaling Peptides and Proteins
  • MDC1 protein, mouse
  • RNA, Messenger
  • Repressor Proteins
  • Ubiquitin
  • Polycomb Repressive Complex 1
  • Rnf2 protein, mouse
  • Ubiquitin-Protein Ligases

Associated data

  • GEO/GSE55060