Modeling uniquely human gene regulatory function via targeted humanization of the mouse genome

Nat Commun. 2022 Jan 13;13(1):304. doi: 10.1038/s41467-021-27899-w.

Abstract

The evolution of uniquely human traits likely entailed changes in developmental gene regulation. Human Accelerated Regions (HARs), which include transcriptional enhancers harboring a significant excess of human-specific sequence changes, are leading candidates for driving gene regulatory modifications in human development. However, insight into whether HARs alter the level, distribution, and timing of endogenous gene expression remains limited. We examined the role of the HAR HACNS1 (HAR2) in human evolution by interrogating its molecular functions in a genetically humanized mouse model. We find that HACNS1 maintains its human-specific enhancer activity in the mouse embryo and modifies expression of Gbx2, which encodes a transcription factor, during limb development. Using single-cell RNA-sequencing, we demonstrate that Gbx2 is upregulated in the limb chondrogenic mesenchyme of HACNS1 homozygous embryos, supporting that HACNS1 alters gene expression in cell types involved in skeletal patterning. Our findings illustrate that humanized mouse models provide mechanistic insight into how HARs modified gene expression in human evolution.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Cell Differentiation / genetics
  • Chondrocytes / cytology
  • Chondrogenesis / genetics
  • Embryo, Mammalian / metabolism
  • Enhancer Elements, Genetic / genetics
  • Epigenesis, Genetic
  • Extremities / embryology
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Gene Knock-In Techniques
  • Genome*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Homozygote
  • Humans
  • Mesoderm / embryology
  • Mesoderm / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Models, Genetic*
  • Pan troglodytes
  • Promoter Regions, Genetic / genetics
  • Time Factors

Substances

  • Gbx2 protein, mouse
  • Homeodomain Proteins