Activation-derepression synergy enables a bHLH network to coordinate a signal-specific fate response

Cell Rep. 2024 Dec 24;43(12):115077. doi: 10.1016/j.celrep.2024.115077. Epub 2024 Dec 12.

Abstract

Stem cells integrate multiple environmental signals to activate appropriate fate programs. To ensure coherent responses, alternative fates must be concomitantly inactivated. However, mechanisms that coordinate fates in a signal-specific manner are not fully understood. Here, we investigate the role of a network of basic-helix-loop-helix (bHLH) transcription factors in neural stem cells, which integrate leukemia inhibitory factor (LIF) and bone morphogenetic protein (BMP) signaling to synergistically induce glial fibrillary acidic protein (GFAP), a key astrocyte-fate determinant. Using quantitative RNA-fluorescence in situ hybridization (FISH) and ectopic expression, we find that multiple bHLHs that promote alternative fates also repress GFAP but are all suppressed by BMP and, to a lesser extent, LIF. Mathematical modeling shows that synergy arises from this coordinated derepression of GFAP combined with its activation by LIF signaling. Finally, we determine how coordinated and tunable derepression results from extensive cross-regulation among bHLHs. Activation-derepression synergy could be broadly utilized to couple signaling and fate, particularly across the numerous developmental systems regulated by bHLH factors.

Keywords: CP: Molecular biology; GFAP; astrocyte; bHLH; cell fate; gene regulatory network; neural stem cell; signal integration; stem cell differentiation; synergy; transcription factor network.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors* / genetics
  • Basic Helix-Loop-Helix Transcription Factors* / metabolism
  • Bone Morphogenetic Proteins* / metabolism
  • Cell Differentiation
  • Glial Fibrillary Acidic Protein* / genetics
  • Glial Fibrillary Acidic Protein* / metabolism
  • Leukemia Inhibitory Factor* / metabolism
  • Mice
  • Neural Stem Cells* / cytology
  • Neural Stem Cells* / metabolism
  • Signal Transduction*

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Leukemia Inhibitory Factor
  • Glial Fibrillary Acidic Protein
  • Bone Morphogenetic Proteins