NT-3 contributes to chemotherapy-induced neuropathic pain through TrkC-mediated CCL2 elevation in DRG neurons

EMBO Rep. 2024 May;25(5):2375-2390. doi: 10.1038/s44319-024-00133-6. Epub 2024 Apr 9.

Abstract

Cancer patients undergoing treatment with antineoplastic drugs often experience chemotherapy-induced neuropathic pain (CINP), and the therapeutic options for managing CINP are limited. Here, we show that systemic paclitaxel administration upregulates the expression of neurotrophin-3 (Nt3) mRNA and NT3 protein in the neurons of dorsal root ganglia (DRG), but not in the spinal cord. Blocking NT3 upregulation attenuates paclitaxel-induced mechanical, heat, and cold nociceptive hypersensitivities and spontaneous pain without altering acute pain and locomotor activity in male and female mice. Conversely, mimicking this increase produces enhanced responses to mechanical, heat, and cold stimuli and spontaneous pain in naive male and female mice. Mechanistically, NT3 triggers tropomyosin receptor kinase C (TrkC) activation and participates in the paclitaxel-induced increases of C-C chemokine ligand 2 (Ccl2) mRNA and CCL2 protein in the DRG. Given that CCL2 is an endogenous initiator of CINP and that Nt3 mRNA co-expresses with TrkC and Ccl2 mRNAs in DRG neurons, NT3 likely contributes to CINP through TrkC-mediated activation of the Ccl2 gene in DRG neurons. NT3 may be thus a potential target for CINP treatment.

Keywords: C–C Chemokine Ligand 2; Dorsal Root Ganglion; Neurotrophin-3; Paclitaxel-induced Peripheral Neuropathy; TrkC.

MeSH terms

  • Animals
  • Antineoplastic Agents / adverse effects
  • Chemokine CCL2* / genetics
  • Chemokine CCL2* / metabolism
  • Female
  • Ganglia, Spinal* / drug effects
  • Ganglia, Spinal* / metabolism
  • Male
  • Mice
  • Nerve Growth Factors / genetics
  • Nerve Growth Factors / metabolism
  • Neuralgia* / chemically induced
  • Neuralgia* / genetics
  • Neuralgia* / metabolism
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Neurotrophin 3* / genetics
  • Neurotrophin 3* / metabolism
  • Paclitaxel* / adverse effects
  • Paclitaxel* / pharmacology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptor, trkC* / genetics
  • Receptor, trkC* / metabolism

Substances

  • Antineoplastic Agents
  • Chemokine CCL2
  • Neurotrophin 3
  • Paclitaxel
  • Receptor, trkC
  • RNA, Messenger
  • neurotropin 3, mouse
  • Nerve Growth Factors