µ-opioid receptor activation at the dorsal reticular nucleus shifts diffuse noxious inhibitory controls to hyperalgesia in chronic joint pain in male rats.


Journal

Anesthesiology
ISSN: 1528-1175
Titre abrégé: Anesthesiology
Pays: United States
ID NLM: 1300217

Informations de publication

Date de publication:
21 Feb 2024
Historique:
medline: 21 2 2024
pubmed: 21 2 2024
entrez: 21 2 2024
Statut: aheadofprint

Résumé

The dorsal reticular nucleus is a pain facilitatory area involved in the diffuse noxious inhibitory controls (DNIC), through opioidergic mechanisms that are poorly understood. We hypothesized that signaling of µ-opioid receptors is altered in this area at prolonged chronic inflammatory pain and that this accounts for the loss of DNIC occurring in this condition. Monoarthritis was induced in male Wistar rats (n=5-9/group) by tibiotarsal injection of complete Freund's adjuvant. We quantified the immunolabeling of µ-opioid receptors and the phosphorylated forms of µ-opioid receptors and cAMP response element-binding protein. Pharmacological manipulation of µ-opioid receptors at the dorsal reticular nucleus was assessed in DNIC, through the Randall-Selitto test. At 42 days of monoarthritis, µ-opioid receptor labeling decreased at the dorsal reticular nucleus, while its phosphorylated form and the phosphorylated cAMP response element-binding protein increased. D-ALA2,N-ME-PHE4,GLY5-OL)-enkephalin acetate (DAMGO) enhanced DNIC analgesia in normal animals ([Mean ± SD]: pre-DNIC: 126.9 ± 7.0g; DNIC - DAMGO: 147.5 ± 8.0g vs. DNIC + DAMGO: 198.1 ± 19.3g, p < 0.001), whereas it produced hyperalgesia in monoarthritis (pre-DNIC: 67.8 ± 7.5g; DNIC - DAMGO: 70.6 ± 7.7g vs. DNIC + DAMGO: 32.2 ± 2.6g, p < 0.001). An ultra-low dose of naloxone, which prevents the excitatory signaling of the µ-opioid receptor, restored DNIC analgesia in monoarthritis (DNIC - Naloxone: 60.0 ± 6.1g vs. DNIC + Naloxone: 98.0 ± 13.5g, p < 0.001), compared to saline (DNIC - Saline: 62.5 ± 5.2g vs. DNIC + Saline: 64.2 ± 3.8g). When injected prior to DAMGO, it restored DNIC analgesia and decreased the phosphorylated cAMP response element-binding protein in monoarthritis. The dorsal reticular nucleus is likely involved in a facilitatory pathway responsible for DNIC hyperalgesia. The shift of µ-opioid receptor signaling to excitatory in this pathway likely accounts for the loss of DNIC analgesia in monoarthritis.

Sections du résumé

BACKGROUND BACKGROUND
The dorsal reticular nucleus is a pain facilitatory area involved in the diffuse noxious inhibitory controls (DNIC), through opioidergic mechanisms that are poorly understood. We hypothesized that signaling of µ-opioid receptors is altered in this area at prolonged chronic inflammatory pain and that this accounts for the loss of DNIC occurring in this condition.
METHODS METHODS
Monoarthritis was induced in male Wistar rats (n=5-9/group) by tibiotarsal injection of complete Freund's adjuvant. We quantified the immunolabeling of µ-opioid receptors and the phosphorylated forms of µ-opioid receptors and cAMP response element-binding protein. Pharmacological manipulation of µ-opioid receptors at the dorsal reticular nucleus was assessed in DNIC, through the Randall-Selitto test.
RESULTS RESULTS
At 42 days of monoarthritis, µ-opioid receptor labeling decreased at the dorsal reticular nucleus, while its phosphorylated form and the phosphorylated cAMP response element-binding protein increased. D-ALA2,N-ME-PHE4,GLY5-OL)-enkephalin acetate (DAMGO) enhanced DNIC analgesia in normal animals ([Mean ± SD]: pre-DNIC: 126.9 ± 7.0g; DNIC - DAMGO: 147.5 ± 8.0g vs. DNIC + DAMGO: 198.1 ± 19.3g, p < 0.001), whereas it produced hyperalgesia in monoarthritis (pre-DNIC: 67.8 ± 7.5g; DNIC - DAMGO: 70.6 ± 7.7g vs. DNIC + DAMGO: 32.2 ± 2.6g, p < 0.001). An ultra-low dose of naloxone, which prevents the excitatory signaling of the µ-opioid receptor, restored DNIC analgesia in monoarthritis (DNIC - Naloxone: 60.0 ± 6.1g vs. DNIC + Naloxone: 98.0 ± 13.5g, p < 0.001), compared to saline (DNIC - Saline: 62.5 ± 5.2g vs. DNIC + Saline: 64.2 ± 3.8g). When injected prior to DAMGO, it restored DNIC analgesia and decreased the phosphorylated cAMP response element-binding protein in monoarthritis.
CONCLUSIONS CONCLUSIONS
The dorsal reticular nucleus is likely involved in a facilitatory pathway responsible for DNIC hyperalgesia. The shift of µ-opioid receptor signaling to excitatory in this pathway likely accounts for the loss of DNIC analgesia in monoarthritis.

Identifiants

pubmed: 38381969
pii: 139850
doi: 10.1097/ALN.0000000000004956
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 American Society of Anesthesiologists. All Rights Reserved.

Déclaration de conflit d'intérêts

Conflicts of Interest: The authors declare no conflict of interests.

Auteurs

Raquel Pereira-Silva (R)

Instituto de Investigação e Inovação em Saúde da Universidade do Porto (I3S). Rua Alfredo Allen 208, 4200 393 Porto, Portugal.
Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto. Rua Alfredo Allen 208, 4200-393 Porto, Portugal.
Departamento de Biomedicina - Unidade de Biologia Experimental, Faculdade de Medicina, Universidade do Porto. Alameda Prof. Hernâni Monteiro 4200-319 Porto, Portugal.

Armando Teixeira-Pinto (A)

Sydney School of Public Health, Faculty of Medicine and Health, The University of Sydney, Australia.
Centre for Kidney Research, Kids Research Institute, The Children's Hospital at Westmead, Sydney, NSW, Australia.

Fani L Neto (FL)

Instituto de Investigação e Inovação em Saúde da Universidade do Porto (I3S). Rua Alfredo Allen 208, 4200 393 Porto, Portugal.
Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto. Rua Alfredo Allen 208, 4200-393 Porto, Portugal.
Departamento de Biomedicina - Unidade de Biologia Experimental, Faculdade de Medicina, Universidade do Porto. Alameda Prof. Hernâni Monteiro 4200-319 Porto, Portugal.

Isabel Martins (I)

Instituto de Investigação e Inovação em Saúde da Universidade do Porto (I3S). Rua Alfredo Allen 208, 4200 393 Porto, Portugal.
Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto. Rua Alfredo Allen 208, 4200-393 Porto, Portugal.
Departamento de Biomedicina - Unidade de Biologia Experimental, Faculdade de Medicina, Universidade do Porto. Alameda Prof. Hernâni Monteiro 4200-319 Porto, Portugal.

Classifications MeSH