Bi-fated tendon-to-bone attachment cells are regulated by shared enhancers and KLF transcription factors

Elife. 2021 Jan 15:10:e55361. doi: 10.7554/eLife.55361.

Abstract

The mechanical challenge of attaching elastic tendons to stiff bones is solved by the formation of a unique transitional tissue. Here, we show that murine tendon-to-bone attachment cells are bi-fated, activating a mixture of chondrocyte and tenocyte transcriptomes, under regulation of shared regulatory elements and Krüppel-like factors (KLFs) transcription factors. High-throughput bulk and single-cell RNA sequencing of humeral attachment cells revealed expression of hundreds of chondrogenic and tenogenic genes, which was validated by in situ hybridization and single-molecule ISH. ATAC sequencing showed that attachment cells share accessible intergenic chromatin areas with either tenocytes or chondrocytes. Epigenomic analysis revealed enhancer signatures for most of these regions. Transgenic mouse enhancer reporter assays verified the shared activity of some of these enhancers. Finally, integrative chromatin and motif analyses and transcriptomic data implicated KLFs as regulators of attachment cells. Indeed, blocking expression of both Klf2 and Klf4 in developing limb mesenchyme impaired their differentiation.

Keywords: cartilage; developmental biology; enthesis; mouse; musculoskeletal system; tendon.

Publication types

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

MeSH terms

  • Animals
  • Bone and Bones
  • Chondrocytes / metabolism*
  • Female
  • Kruppel-Like Factor 4 / genetics
  • Kruppel-Like Factor 4 / metabolism
  • Kruppel-Like Transcription Factors / genetics*
  • Kruppel-Like Transcription Factors / metabolism
  • Mice
  • Regulatory Sequences, Nucleic Acid
  • Tendons
  • Tenocytes / metabolism*
  • Transcriptome*

Substances

  • Klf2 protein, mouse
  • Klf4 protein, mouse
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors

Associated data

  • GEO/GSE144306
  • GEO/GSE160090