Involvement of high mobility group box 1 in the development and maintenance of chemotherapy-induced peripheral neuropathy in rats

Toxicology. 2016 Jul 15:365:48-58. doi: 10.1016/j.tox.2016.07.016. Epub 2016 Jul 27.

Abstract

Given that high mobility group box 1 (HMGB1), a nuclear protein, once released to the extracellular space, promotes nociception, we asked if inactivation of HMGB1 prevents or reverses chemotherapy-induced painful neuropathy in rats and also examined possible involvement of Toll-like receptor 4 (TLR4) and the receptor for advanced glycation endproduct (RAGE), known as targets for HMGB1. Painful neuropathy was produced by repeated i.p. administration of paclitaxel or vincristine in rats. Nociceptive threshold was determined by the paw pressure method and/or von Frey test in the hindpaw. Tissue protein levels were determined by immunoblotting. Repeated i.p. administration of the anti-HMGB1-neutralizing antibody or recombinant human soluble thrombomodulin (rhsTM), known to inactivate HMGB1, prevented the development of hyperalgesia and/or allodynia induced by paclitaxel or vincristine in rats. A single i.p. or intraplantar (i.pl.) administration of the antibody or rhsTM reversed the chemotherapy-induced neuropathy. A single i.pl. administration of a TLR4 antagonist or low molecular weight heparin, known to inhibit RAGE, attenuated the hyperalgesia caused by i.pl. HMGB1 and also the chemotherapy-induced painful neuropathy. Paclitaxel or vincristine treatment significantly decreased protein levels of HMGB1 in the dorsal root ganglia, but not sciatic nerves. HMGB1 thus participates in both development and maintenance of chemotherapy-induced painful neuropathy, in part through RAGE and TLR4. HMGB1 inactivation is considered useful to prevent and treat the chemotherapy-induced painful neuropathy.

Keywords: Chemotherapy-induced painful neuropathy; High mobility group box 1; Neuropathic pain; Thrombomodulin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Neutralizing / pharmacology
  • Antineoplastic Agents / administration & dosage
  • Antineoplastic Agents / adverse effects*
  • Disease Models, Animal
  • Ganglia, Spinal / drug effects
  • Ganglia, Spinal / metabolism
  • HMGB1 Protein / antagonists & inhibitors
  • HMGB1 Protein / genetics*
  • HMGB1 Protein / metabolism
  • Hyperalgesia / genetics
  • Hyperalgesia / prevention & control
  • Male
  • Paclitaxel / administration & dosage
  • Paclitaxel / adverse effects*
  • Pain / chemically induced
  • Pain / genetics*
  • Peripheral Nervous System Diseases / chemically induced
  • Peripheral Nervous System Diseases / genetics*
  • Peripheral Nervous System Diseases / therapy
  • Rats
  • Rats, Wistar
  • Receptor for Advanced Glycation End Products / genetics
  • Receptor for Advanced Glycation End Products / metabolism
  • Recombinant Proteins / pharmacology
  • Sciatic Nerve / drug effects
  • Sciatic Nerve / metabolism
  • Thrombomodulin / genetics
  • Thrombomodulin / metabolism
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / metabolism
  • Vincristine / administration & dosage
  • Vincristine / adverse effects*

Substances

  • Ager protein, rat
  • Antibodies, Neutralizing
  • Antineoplastic Agents
  • HMGB1 Protein
  • Hbp1 protein, rat
  • Receptor for Advanced Glycation End Products
  • Recombinant Proteins
  • THBD protein, human
  • Thrombomodulin
  • Tlr4 protein, rat
  • Toll-Like Receptor 4
  • Vincristine
  • Paclitaxel

Supplementary concepts

  • Neuropathy, Painful