Dysregulation of schizophrenia-associated genes and genome-wide hypomethylation in neurons overexpressing DNMT1

Epigenomics. 2021 Oct;13(19):1539-1555. doi: 10.2217/epi-2021-0133. Epub 2021 Oct 14.

Abstract

Aim: To study the effects of DNMT1 overexpression on transcript levels of genes dysregulated in schizophrenia and on genome-wide methylation patterns. Materials & methods: Transcriptome and DNA methylome comparisons were made between R1 (wild-type) and Dnmt1tet/tet mouse embryonic stem cells and neurons overexpressing DNMT1. Genes dysregulated in both Dnmt1tet/tet cells and schizophrenia patients were studied further. Results & conclusions: About 50% of dysregulated genes in patients also showed altered transcript levels in Tet/Tet neurons in a DNA methylation-independent manner. These neurons unexpectedly showed genome-wide hypomethylation, increased transcript levels of Tet1 and Apobec 1-3 genes and increased activity and copy number of LINE-1 elements. The observed similarities between Tet/Tet neurons and schizophrenia brain samples reinforce DNMT1 overexpression as a risk factor.

Keywords: DNMT1 overexpression; LINE-1 burden; genome-wide hypomethylation; schizophrenia; transcript dysregulation.

Plain language summary

Lay abstract DNMT1 controls cytosine methylation, which is often associated with reduced gene expression. Increased levels of DNMT1 is a risk factor for schizophrenia but information on the affected genes is limited. In this study, ∼50% of genes with altered levels of messenger RNAs in schizophrenia patients were also altered in neurons with increased DNMT1. Surprisingly, the neurons with higher DNMT1 levels showed genome-wide decrease in methylation. These findings uncover a new type of gene dysregulation that is independent of DNMT1's catalytic activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Computational Biology / methods
  • DNA (Cytosine-5-)-Methyltransferase 1 / genetics*
  • DNA Copy Number Variations
  • DNA Methylation*
  • Disease Models, Animal
  • Disease Susceptibility
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Genome-Wide Association Study
  • Humans
  • Long Interspersed Nucleotide Elements
  • Mice
  • Mice, Transgenic
  • Mouse Embryonic Stem Cells / metabolism
  • Neurons / metabolism*
  • Reactive Oxygen Species / metabolism
  • Schizophrenia / etiology*
  • Transcriptome

Substances

  • Reactive Oxygen Species
  • DNA (Cytosine-5-)-Methyltransferase 1
  • DNMT1 protein, human