Histone methyltransferase Setd2 is critical for the proliferation and differentiation of myoblasts

Biochim Biophys Acta Mol Cell Res. 2017 Apr;1864(4):697-707. doi: 10.1016/j.bbamcr.2017.01.012. Epub 2017 Jan 24.

Abstract

Skeletal muscle cell proliferation and differentiation are tightly regulated. Epigenetic regulation is a major component of the regulatory mechanism governing these processes. Histone modification is part of the epigenetic code used for transcriptional regulation of chromatin through the establishment of an active or repressive state for genes involved in myogenesis in a temporal manner. Here, we uncovered the function of SET domain containing 2 (Setd2), an essential histone 3 lysine 36 trimethyltransferase, in regulating the proliferation and differentiation of myoblasts. Setd2 was silenced in the skeletal muscle myoblast cell line, C2C12, using the CRISPR/CAS9 system. The mutant cells exhibited defect in myotube formation. The myotube formation marker, myosin heavy chain (MHC), was downregulated earlier in Setd2 silenced cells compared to wild-type myoblasts during differentiation. The deficiency in Setd2 also resulted in repression of Myogenin (MyoG) expression, a key myogenic regulator during differentiation. In addition to the myoblast differentiation defect, decreased proliferation rate with significantly reduced levels of histone 3 phosphorylation, indicative of cell proliferation defect, were observed in the Setd2 silenced cells; suggesting an impaired proliferation phenotype. Furthermore, compromised G1/S- and G2/M-phase transition and decreased expression levels of major regulators of cell cycle G1/S checkpoints, cyclin D1, CDK4, CDK6, and cyclin E2 were detected in Setd2 silenced cells. Consistent with the cell cycle arrested phenotype, cyclin-dependent kinase inhibitor p21 was upregulated in Setd2 silenced cells. Together, this study demonstrates an essential role of Setd2 in myoblast proliferation and differentiation, and uncovers Setd2-mediated molecular mechanism through regulating MyoG and p21.

Keywords: C2C12 myoblasts; Epigenetics; H3K36me3; Proliferation and differentiation; Setd2.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • CRISPR-Cas Systems
  • Cell Cycle Checkpoints
  • Cell Differentiation
  • Cell Line
  • Cell Proliferation
  • Chromatin / chemistry
  • Chromatin / metabolism
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • Cyclin-Dependent Kinase 4 / genetics
  • Cyclin-Dependent Kinase 4 / metabolism
  • Cyclin-Dependent Kinase 6 / genetics
  • Cyclin-Dependent Kinase 6 / metabolism
  • Cyclin-Dependent Kinase Inhibitor p21 / genetics*
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism
  • Cyclins / genetics
  • Cyclins / metabolism
  • Gene Editing
  • Gene Silencing
  • Histone-Lysine N-Methyltransferase / deficiency
  • Histone-Lysine N-Methyltransferase / genetics*
  • Histones / genetics*
  • Histones / metabolism
  • Mice
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / metabolism*
  • Myoblasts / cytology
  • Myoblasts / metabolism*
  • Myogenin / genetics*
  • Myogenin / metabolism
  • Myosin Heavy Chains / genetics
  • Myosin Heavy Chains / metabolism
  • Phosphorylation

Substances

  • Ccnd1 protein, mouse
  • Ccne2 protein, mouse
  • Chromatin
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins
  • Histones
  • Myog protein, mouse
  • Myogenin
  • Cyclin D1
  • Histone-Lysine N-Methyltransferase
  • SETD2 protein, mouse
  • Cdk4 protein, mouse
  • Cdk6 protein, mouse
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • Myosin Heavy Chains