KRAB-Induced Heterochromatin Effectively Silences PLOD2 Gene Expression in Somatic Cells and is Resilient to TGFβ1 Activation

Int J Mol Sci. 2020 May 21;21(10):3634. doi: 10.3390/ijms21103634.

Abstract

Epigenetic editing, an emerging technique used for the modulation of gene expression in mammalian cells, is a promising strategy to correct disease-related gene expression. Although epigenetic reprogramming results in sustained transcriptional modulation in several in vivo models, further studies are needed to develop this approach into a straightforward technology for effective and specific interventions. Important goals of current research efforts are understanding the context-dependency of successful epigenetic editing and finding the most effective epigenetic effector(s) for specific tasks. Here we tested whether the fibrosis- and cancer-associated PLOD2 gene can be repressed by the DNA methyltransferase M.SssI, or by the non-catalytic Krüppel associated box (KRAB) repressor directed to the PLOD2 promoter via zinc finger- or CRISPR-dCas9-mediated targeting. M.SssI fusions induced de novo DNA methylation, changed histone modifications in a context-dependent manner, and led to 50%-70% reduction in PLOD2 expression in fibrotic fibroblasts and in MDA-MB-231 cancer cells. Targeting KRAB to PLOD2 resulted in the deposition of repressive histone modifications without DNA methylation and in almost complete PLOD2 silencing. Interestingly, both long-term TGFβ1-induced, as well as unstimulated PLOD2 expression, was completely repressed by KRAB, while M.SssI only prevented the TGFβ1-induced PLOD2 expression. Targeting transiently expressed dCas9-KRAB resulted in sustained PLOD2 repression in HEK293T and MCF-7 cells. Together, these findings point to KRAB outperforming DNA methylation as a small potent targeting epigenetic effector for silencing TGFβ1-induced and uninduced PLOD2 expression.

Keywords: KRAB; PLOD2; cancer; epigenetic editing; fibrosis; gene repression.

MeSH terms

  • Adult
  • Cells, Cultured
  • DNA-Cytosine Methylases / genetics
  • DNA-Cytosine Methylases / metabolism
  • Epigenesis, Genetic
  • Gene Silencing*
  • HEK293 Cells
  • Heterochromatin / metabolism*
  • Humans
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism*
  • MCF-7 Cells
  • Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase / genetics*
  • Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase / metabolism
  • Promoter Regions, Genetic
  • Transcriptional Activation
  • Transforming Growth Factor beta / metabolism

Substances

  • Heterochromatin
  • Kruppel-Like Transcription Factors
  • Transforming Growth Factor beta
  • PLOD2 protein, human
  • Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase
  • DNA modification methylase SssI
  • DNA-Cytosine Methylases