A cis-acting structural variation at the ZNF558 locus controls a gene regulatory network in human brain development

Cell Stem Cell. 2022 Jan 6;29(1):52-69.e8. doi: 10.1016/j.stem.2021.09.008. Epub 2021 Oct 7.

Abstract

The human forebrain has expanded in size and complexity compared to chimpanzees despite limited changes in protein-coding genes, suggesting that gene expression regulation is an important driver of brain evolution. Here, we identify a KRAB-ZFP transcription factor, ZNF558, that is expressed in human but not chimpanzee forebrain neural progenitor cells. ZNF558 evolved as a suppressor of LINE-1 transposons but has been co-opted to regulate a single target, the mitophagy gene SPATA18. ZNF558 plays a role in mitochondrial homeostasis, and loss-of-function experiments in cerebral organoids suggests that ZNF558 influences developmental timing during early human brain development. Expression of ZNF558 is controlled by the size of a variable number tandem repeat that is longer in chimpanzees compared to humans, and variable in the human population. Thus, this work provides mechanistic insight into how a cis-acting structural variation establishes a regulatory network that affects human brain evolution.

Keywords: CRISPRi; KRAB-ZNFs; brain development; chimpanzee; evolution; forebrain neural progenitors; human; transposable elements.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain / metabolism
  • DNA-Binding Proteins
  • Gene Expression Regulation
  • Gene Regulatory Networks*
  • Humans
  • Organoids* / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • DNA-Binding Proteins
  • Transcription Factors
  • ZNF558 protein, human