Combinatorial CRISPR/Cas9 Approach to Elucidate a Far-Upstream Enhancer Complex for Tissue-Specific Sox9 Expression

Dev Cell. 2018 Sep 24;46(6):794-806.e6. doi: 10.1016/j.devcel.2018.07.024. Epub 2018 Aug 23.

Abstract

SRY-box 9 (SOX9) is a master transcription factor that regulates cartilage development. SOX9 haploinsufficiency resulting from breakpoints in a ∼1-Mb region upstream of SOX9 was reported in acampomelic campomelic dysplasia (ACD) patients, suggesting that essential enhancer regions of SOX9 for cartilage development are located in this long non-coding sequence. However, the cis-acting enhancer region regulating cartilage-specific SOX9 expression remains to be identified. To identify distant cartilage Sox9 enhancers, we utilized the combination of multiple CRISPR/Cas9 technologies including enrichment of the promoter-enhancer complex followed by next-generation sequencing and mass spectrometry (MS), SIN3A-dCas9-mediated epigenetic silencing, and generation of enhancer deletion mice. As a result, we could identify a critical far-upstream cis-element and Stat3 as a trans-acting factor, regulating cartilage-specific Sox9 expression and subsequent skeletal development. Our strategy could facilitate definitive ACD diagnosis and should be useful to reveal the detailed chromatin conformation and regulation.

Keywords: ACD; CRISPR; SRY-box 9; Sox9; Stat3; acampomelic campomelic dysplasia; cartilage; clustered regularly interspaced short palindromic repeats; enhancer; signal transducer and activator of transcription 3; transcription complex.

Publication types

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

MeSH terms

  • Animals
  • CRISPR-Cas Systems*
  • Cartilage / cytology
  • Cartilage / metabolism*
  • Cells, Cultured
  • Chondrocytes / cytology
  • Chondrocytes / metabolism*
  • Chromatin / metabolism
  • Enhancer Elements, Genetic*
  • Female
  • Gene Expression Regulation*
  • Mice
  • Mice, Inbred C57BL
  • Organ Specificity
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism*
  • STAT3 Transcription Factor / metabolism
  • Sequence Deletion

Substances

  • Chromatin
  • SOX9 Transcription Factor
  • STAT3 Transcription Factor
  • Sox9 protein, mouse
  • Stat3 protein, mouse