Follistatin drives neuropathic pain in mice through IGF1R signaling in nociceptive neurons

Sci Transl Med. 2024 Oct 16;16(769):eadi1564. doi: 10.1126/scitranslmed.adi1564. Epub 2024 Oct 16.

Abstract

Neuropathic pain is a debilitating chronic condition that lacks effective treatment. The role of cytokine- and chemokine-mediated neuroinflammation in its pathogenesis has been well documented. Follistatin (FST) is a secreted protein known to antagonize the biological activity of cytokines in the transforming growth factor-β (TGF-β) superfamily. The involvement of FST in neuropathic pain and the underlying mechanism remain largely unknown. Here, we report that FST was up-regulated in A-fiber sensory neurons after spinal nerve ligation (SNL) in mice. Inhibition or deletion of FST alleviated neuropathic pain and reduced the nociceptive neuron hyperexcitability induced by SNL. Conversely, intrathecal or intraplantar injection of recombinant FST, or overexpression of FST in the dorsal root ganglion (DRG) neurons, induced pain hypersensitivity. Furthermore, exogenous FST increased neuronal excitability in nociceptive neurons. The biolayer interferometry (BLI) assay and coimmunoprecipitation (co-IP) demonstrated direct binding of FST to the insulin-like growth factor-1 receptor (IGF1R), and IGF1R inhibition reduced FST-induced activation of extracellular signal-regulated kinase (ERK) and protein kinase B (AKT), as well as neuronal hyperexcitability. Further co-IP analysis revealed that the N-terminal domain of FST exhibits the highest affinity for IGF1R, and blocking this interaction with a peptide derived from FST attenuated Nav1.7-mediated neuronal hyperexcitability and neuropathic pain after SNL. In addition, FST enhanced neuronal excitability in human DRG neurons through IGF1R. Collectively, our findings suggest that FST, released from A-fiber neurons, enhances Nav1.7-mediated hyperexcitability of nociceptive neurons by binding to IGF1R, making it a potential target for neuropathic pain treatment.

MeSH terms

  • Animals
  • Follistatin* / metabolism
  • Ganglia, Spinal* / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuralgia* / metabolism
  • Nociceptors* / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor, IGF Type 1* / metabolism
  • Signal Transduction*
  • Spinal Nerves / metabolism

Substances

  • Receptor, IGF Type 1
  • Follistatin
  • Proto-Oncogene Proteins c-akt
  • Igf1r protein, mouse