Schwann cell transient receptor potential ankyrin 1 (TRPA1) ortholog in zebrafish larvae mediates chemotherapy-induced peripheral neuropathy

Br J Pharmacol. 2024 Dec;181(23):4859-4873. doi: 10.1111/bph.17318. Epub 2024 Sep 5.

Abstract

Background and purpose: The oxidant sensor transient receptor potential ankyrin 1 (TRPA1) channel expressed by Schwann cells (SCs) has recently been implicated in several models of neuropathic pain in rodents. Here we investigate whether the pro-algesic function of Schwann cell TRPA1 is not limited to mammals by exploring the role of TRPA1 in a model of chemotherapy-induced peripheral neuropathy (CIPN) in zebrafish larvae.

Experimental approach: We used zebrafish larvae and a mouse model to test oxaliplatin-evoked nociceptive behaviours. We also performed a TRPA1 selective silencing in Schwann cells both in zebrafish larvae and mice to study their contribution in oxaliplatin-induced CIPN model.

Key results: We found that zebrafish larvae and zebrafish TRPA1 (zTRPA1)-transfected HEK293T cells respond to reactive oxygen species (ROS) with nociceptive behaviours and intracellular calcium increases, respectively. TRPA1 was found to be co-expressed with the Schwann cell marker, SOX10, in zebrafish larvae. Oxaliplatin caused nociceptive behaviours in zebrafish larvae that were attenuated by a TRPA1 antagonist and a ROS scavenger. Oxaliplatin failed to produce mechanical allodynia in mice with Schwann cell TRPA1 selective silencing (Plp1+-Trpa1 mice). Comparable results were observed in zebrafish larvae where TRPA1 selective silencing in Schwann cells, using the specific Schwann cell promoter myelin basic protein (MBP), attenuated oxaliplatin-evoked nociceptive behaviours.

Conclusion and implications: These results indicate that the contribution of the oxidative stress/Schwann cell/TRPA1 pro-allodynic pathway to neuropathic pain models seems to be conserved across the animal kingdom.

Keywords: Schwann cells; nociceptive behaviours; oxaliplatin; oxidative stress; transient receptor potential ankyrin 1 (TRPA1).

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / toxicity
  • HEK293 Cells
  • Humans
  • Larva*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Oxaliplatin* / toxicity
  • Peripheral Nervous System Diseases / chemically induced
  • Peripheral Nervous System Diseases / metabolism
  • Reactive Oxygen Species / metabolism
  • Schwann Cells* / drug effects
  • Schwann Cells* / metabolism
  • TRPA1 Cation Channel* / genetics
  • TRPA1 Cation Channel* / metabolism
  • Zebrafish Proteins* / genetics
  • Zebrafish Proteins* / metabolism
  • Zebrafish*

Substances

  • TRPA1 Cation Channel
  • Oxaliplatin
  • Zebrafish Proteins
  • Antineoplastic Agents
  • Reactive Oxygen Species
  • trpa1a protein, zebrafish
  • Trpa1 protein, mouse