A conserved transcription factor regulatory program promotes tendon fate

Dev Cell. 2024 Dec 2;59(23):3106-3123.e12. doi: 10.1016/j.devcel.2024.08.006. Epub 2024 Aug 30.

Abstract

Tendons, which transmit force from muscles to bones, are highly prone to injury. Understanding the mechanisms driving tendon fate would impact efforts to improve tendon healing, yet this knowledge is limited. To find direct regulators of tendon progenitor emergence, we performed a zebrafish high-throughput chemical screen. We established forskolin as a tenogenic inducer across vertebrates, functioning through Creb1a, which is required and sufficient for tendon fate. Putative enhancers containing cyclic AMP (cAMP) response elements (CREs) in humans, mice, and fish drove specific expression in zebrafish cranial and fin tendons. Analysis of these genomic regions identified motifs for early B cell factor (Ebf/EBF) transcription factors. Mutation of CRE or Ebf/EBF motifs significantly disrupted enhancer activity and specificity in tendons. Zebrafish ebf1a/ebf3a mutants displayed defects in tendon formation. Notably, Creb1a/CREB1 and Ebf1a/Ebf3a/EBF1 overexpression facilitated tenogenic induction in zebrafish and human pluripotent stem cells. Together, our work identifies the functional conservation of two transcription factors in promoting tendon fate.

Keywords: Creb1a/CREB1; Ebf1a/Ebf3a/EBF1; cAMP; chemical screen; enhancer; forskolin/colforsin; scxa; tendon; zebrafish.

MeSH terms

  • Animals
  • Cell Differentiation* / genetics
  • Colforsin / pharmacology
  • Cyclic AMP / metabolism
  • Cyclic AMP Response Element-Binding Protein* / genetics
  • Cyclic AMP Response Element-Binding Protein* / metabolism
  • Enhancer Elements, Genetic / genetics
  • Gene Expression Regulation, Developmental
  • Humans
  • Mice
  • Pluripotent Stem Cells / cytology
  • Pluripotent Stem Cells / metabolism
  • Tendons* / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Zebrafish Proteins* / genetics
  • Zebrafish Proteins* / metabolism
  • Zebrafish* / genetics
  • Zebrafish* / metabolism

Substances

  • Zebrafish Proteins
  • Transcription Factors
  • Cyclic AMP Response Element-Binding Protein
  • Colforsin
  • Cyclic AMP