Hydrogen Peroxide Induces Muscle Nociception via Transient Receptor Potential Ankyrin 1 Receptors

Daisuke Sugiyama; Sinyoung Kang; Nicholas Arpey; Preeyaphan Arunakul; Yuriy M Usachev; Timothy J Brennan

doi:10.1097/aln.0000000000001756

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Hydrogen Peroxide Induces Muscle Nociception via Transient Receptor Potential Ankyrin 1 Receptors

Journal article

Open access

Peer reviewed

Hydrogen Peroxide Induces Muscle Nociception via Transient Receptor Potential Ankyrin 1 Receptors

Daisuke Sugiyama, Sinyoung Kang, Nicholas Arpey, Preeyaphan Arunakul, Yuriy M Usachev and Timothy J Brennan

Anesthesiology (Philadelphia), Vol.127(4), pp.695-708

10/2017

DOI: 10.1097/aln.0000000000001756

PMCID: PMC5605423

PMID: 28640016

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Abstract

H2O2 has a variety of actions in skin wounds but has been rarely studied in deep muscle tissue. Based on response to the transient receptor potential ankyrin 1 antagonists after plantar incision, we hypothesized that H2O2 exerts nociceptive effects via the transient receptor potential ankyrin 1 in muscle. Nociceptive behaviors in rats (n = 269) and mice (n = 16) were evaluated after various concentrations and volumes of H2O2 were injected into the gastrocnemius muscle or subcutaneous tissue. The effects of H2O2 on in vivo spinal dorsal horn neuronal activity and lumbar dorsal root ganglia neurons in vitro were evaluated from 26 rats and 6 mice. Intramuscular (mean ± SD: 1,436 ± 513 s) but not subcutaneous (40 ± 58 s) injection of H2O2 (100 mM, 0.6 ml) increased nociceptive time. Conditioned place aversion was evident after intramuscular (-143 ± 81 s) but not subcutaneous (-2 ± 111 s) injection of H2O2. These H2O2-induced behaviors were blocked by transient receptor potential ankyrin 1 antagonists. Intramuscular injection of H2O2 caused sustained in vivo activity of dorsal horn neurons, and H2O2 activated a subset of dorsal root ganglia neurons in vitro. Capsaicin nerve block decreased guarding after plantar incision and reduced nociceptive time after intramuscular H2O2. Nociceptive time after intramuscular H2O2 in transient receptor potential ankyrin 1 knockout mice was shorter (173 ± 156 s) compared with wild-type mice (931 ± 629 s). The greater response of muscle tissue to H2O2 may help explain why incision that includes deep muscle but not skin incision alone produces spontaneous activity in nociceptive pathways.

Posterior Horn Cells - drug effects

TRPC Cation Channels - drug effects

Anti-Infective Agents, Local - pharmacology

Hydrogen Peroxide - pharmacology

Rats

Male

Rats, Sprague-Dawley

Animals

Muscle, Skeletal - drug effects

TRPA1 Cation Channel

Nociception - drug effects

Female

Ganglia, Spinal - drug effects

TRPC Cation Channels - genetics

Nociceptors - drug effects

Disease Models, Animal

Details

Title: Subtitle: Hydrogen Peroxide Induces Muscle Nociception via Transient Receptor Potential Ankyrin 1 Receptors
Creators: Daisuke Sugiyama - From the Departments of Anesthesia (D.S., S.K., N.A., P.A., T.J.B.) and Pharmacology (Y.M.U., T.J.B.), Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, Iowa
Sinyoung Kang
Nicholas Arpey
Preeyaphan Arunakul
Yuriy M Usachev
Timothy J Brennan
Resource Type: Journal article
Publication Details: Anesthesiology (Philadelphia), Vol.127(4), pp.695-708
DOI: 10.1097/aln.0000000000001756
PMID: 28640016
PMCID: PMC5605423
NLM abbreviation: Anesthesiology
ISSN: 0003-3022
eISSN: 1528-1175
Publisher: United States
Grant note: R21 NS092851 / NINDS NIH HHS
Language: English
Date published: 10/2017
Academic Unit: Iowa Neuroscience Institute; Anesthesia; Neuroscience and Pharmacology
Record Identifier: 9984007293802771

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