Treatment with a heme oxygenase 1 inducer enhances the antinociceptive effects of α-opioid, δ-opioid, and cannabinoid 2 receptors during inflammatory pain

Journal of Pharmacology and Experimental Therapeutics

Volumn 351, Issue 1, 2014, Pages 224-232

  Carcolé, Mireia ^a   Castany, Sílvia ^a   Leánez, Sergi ^a   Pol, Olga ^a  

^a BIOMEDICAL RESEARCH INSTITUTE SANT PAU IIB SANT PAU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYL 3 (1 NAPHTHOYL) 1 PROPYLINDOLE; CANNABINOID 2 RECEPTOR; DELTA OPIATE RECEPTOR; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; HEME OXYGENASE 1; MORPHINE; MU OPIATE RECEPTOR; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN TIN; ANALGESIC AGENT; PROTOPORPHYRIN; SIGMA OPIATE RECEPTOR;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; DRUG MEGADOSE; DRUG POTENTIATION; HYPERALGESIA; INFLAMMATORY PAIN; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SPINAL GANGLION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; GENETICS; METABOLISM; NOCICEPTION; NOCICEPTIVE PAIN;

ANALGESICS; ANIMALS; ENKEPHALIN, D-PENICILLAMINE (2,5)-; GANGLIA, SPINAL; HEME OXYGENASE-1; MALE; MICE; MICE, INBRED C57BL; MORPHINE; NOCICEPTION; NOCICEPTIVE PAIN; PROTOPORPHYRINS; RECEPTOR, CANNABINOID, CB2; RECEPTORS, OPIOID, MU; RECEPTORS, SIGMA;

EID: 84907164517     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.215681     Document Type: Article

References (26)

1. Chaplan SR, Bach FW, Pogrel JW, Chung JM, and Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
2. Cunha TM, Roman-Campos D, Lotufo CM, Duarte HL, Souza GR, Verri WA, Jr, Funez MI, Dias QM, Schivo IR, and Domingues AC, et al. (2010) Morphine peripheral analgesia depends on activation of the PI3Kgamma/AKT/nNOS/NO/KATP signaling pathway. Proc Natl Acad Sci USA 107:4442-4447.
3. Egea J, Rosa AO, Lorrio S, del Barrio L, Cuadrado A, and López MG (2009) Haeme oxygenase-1 overexpression via nAChRs and the transcription factor Nrf2 has antinociceptive effects in the formalin test. Pain 146:75-83.
4. Fan W, Huang F, Wu Z, Zhu X, Li D, and He H (2011) Carbon monoxide: a gas that modulates nociception. J Neurosci Res 89:802-807.
5. Ferrándiz ML, Maicas N, Garcia-Arnandis I, Terencio MC, Motterlini R, Devesa I, Joosten LA, van den Berg WB, and Alcaraz MJ (2008) Treatment with a COreleasing molecule (CORM-3) reduces joint inflammation and erosion in murine collagen-induced arthritis. Ann Rheum Dis 67:1211-1217.
6. Gavériaux-Ruff C and Kieffer BL (2011) Delta opioid receptor analgesia: recent contributions from pharmacology and molecular approaches. Behav Pharmacol 22: 405-414.
7. Guillén MI, Megías J, Clérigues V, Gomar F, and Alcaraz MJ (2008) The CO-releasing molecule CORM-2 is a novel regulator of the inflammatory process in osteoarthritic chondrocytes. Rheumatology (Oxford) 47:1323-1328.
8. Hargreaves K, Dubner R, Brown F, Flores C, and Joris J (1988) A new and sensitive method formeasuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
9. Hervera A, Gou G, Leánez S, and Pol O (2013b) Effects of treatment with a carbon monoxide-releasing molecule and a heme oxygenase 1 inducer in the antinociceptive effects of morphine in different models of acute and chronic pain in mice. Psychopharmacology (Berl) 228:463-477.
10. Hervera A, Leánez S,Motterlini R, and Pol O (2013a) Treatment with carbon monoxidereleasing molecules and an HO-1 inducer enhances the effects and expression of m-opioid receptors during neuropathic pain. Anesthesiology 118:1180-1197.
11. Hervera A, Leánez S, Negrete R, and Pol O (2009) The peripheral administration of a nitric oxide donor potentiates the local antinociceptive effects of a DOR agonist during chronic inflammatory pain in mice. Naunyn Schmiedebergs Arch Pharmacol 380:345-352.
12. Hervera A, Negrete R, Leánez S, Martín-Campos J, and Pol O (2010) The role of nitric oxide in the local antiallodynic and antihyperalgesic effects and expression of delta-opioid and cannabinoid-2 receptors during neuropathic pain in mice. J Pharmacol Exp Ther 334:887-896.
13. Hervera A, Negrete R, Leánez S, Martín-Campos JM, and Pol O (2011) Peripheral effects of morphine and expression of m-opioid receptors in the dorsal root ganglia during neuropathic pain: nitric oxide signaling. Mol Pain 7:25.
14. Jiménez N, Puig MM, and Pol O (2006) Antiexudative effects of opioids and expression of kappa- and delta-opioid receptors during intestinal inflammation in mice: involvement of nitric oxide. J Pharmacol Exp Ther 316:261-270.
15. Leánez S, Hervera A, and Pol O (2009) Peripheral antinociceptive effects of mu- and delta-opioid receptor agonists in NOS2 and NOS1 knockout mice during chronic inflammatory pain. Eur J Pharmacol 602:41-49.
16. Maicas N, Ferrándiz ML, Devesa I, Motterlini R, Koenders MI, van den Berg WB, and Alcaraz MJ (2010) The CO-releasing molecule CORM-3 protects against articular degradation in the K/BxN serum transfer arthritis model. Eur J Pharmacol 634:184-191.
17. Megías J, Guillén MI, Clérigues V, Rojo AI, Cuadrado A, Castejón MA, Gomar F, and Alcaraz MJ (2009) Heme oxygenase-1 induction modulates microsomal prostaglandin E synthase-1 expression and prostaglandin E(2) production in osteoarthritic chondrocytes. Biochem Pharmacol 77:1806-1813.
18. Nascimento CG and Branco LG (2007) Role of the peripheral heme oxygenase-carbon monoxide pathway on the nociceptive response of rats to the formalin test: evidence for a cGMP signaling pathway. Eur J Pharmacol 556:55-61.
19. Negrete R, Hervera A, Leánez S, Martín-Campos JM, and Pol O (2011) The antinociceptive effects of JWH-015 in chronic inflammatory pain are produced by nitric oxide-cGMP-PKG-KATP pathway activation mediated by opioids. PLoS ONE 6: e26688.
20. Negrete R, Hervera A, Leánez S, and Pol O (2014) Treatment with a carbon monoxide-releasing molecule inhibits chronic inflammatory pain in mice: nitric oxide contribution. Psychopharmacology (Berl) 231:853-861.
21. Obara I, Parkitna JR, Korostynski M, Makuch W, Kaminska D, Przewlocka B, and Przewlocki R (2009) Local peripheral opioid effects and expression of opioid genes in the spinal cord and dorsal root ganglia in neuropathic and inflammatory pain. Pain 141:283-291.
22. Pacheco DF and Duarte ID (2005) Delta-opioid receptor agonist SNC80 induces peripheral antinociception via activation of ATP-sensitive K1 channels. Eur J Pharmacol 512:23-28.
23. Pol O, Sasaki M, Jiménez N, Dawson VL, Dawson TM, and Puig MM (2005) The involvement of nitric oxide in the enhanced expression of mu-opioid receptors during intestinal inflammation in mice. Br J Pharmacol 145:758-766.
24. Puehler W, Zöllner C, Brack A, Shaqura MA, Krause H, Schäfer M, and Stein C (2004) Rapid upregulation of mu opioid receptor mRNA in dorsal root ganglia in response to peripheral inflammation depends on neuronal conduction. Neuroscience 129:473-479.
25. Rosa AO, Egea J, Lorrio S, Rojo AI, Cuadrado A, and López MG (2008) Nrf2-mediated haeme oxygenase-1 up-regulation induced by cobalt protoporphyrin has antinociceptive effects against inflammatory pain in the formalin test in mice. Pain 137:332-339.
26. Steiner AA, Branco LG, Cunha FQ, and Ferreira SH (2001) Role of the haeme oxygenase/carbon monoxide pathway in mechanical nociceptor hypersensitivity. Br J Pharmacol 132:1673-1682.