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

Volumn 228, Issue 3, 2013, Pages 463-477

  Hervera, Arnau ^a   Gou, Gemma ^a   Leánez, Sergi ^a   Pol, Olga ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Allodynia; Antinociception; Carbon monoxide; Hyperalgesia; Morphine; Nitric oxide; Visceral pain

Indexed keywords

CARBON MONOXIDE; FREUND ADJUVANT; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; MORPHINE; NEURONAL NITRIC OXIDE SYNTHASE; PROTOPORPHYRIN COBALT; RUTHENIUM; TRICARBONYLDICHLORORUTHENIUM; UNCLASSIFIED DRUG;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTHRITIS; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; HYPERALGESIA; INFLAMMATORY PAIN; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; SCIATIC NERVE INJURY; TREATMENT RESPONSE; VISCERAL PAIN; WRITHING TEST;

ACUTE PAIN; ANALGESICS; ANIMALS; BEHAVIOR, ANIMAL; CARBON MONOXIDE; CHRONIC PAIN; DISEASE MODELS, ANIMAL; DRUG THERAPY, COMBINATION; HEME OXYGENASE-1; MICE; MICE, KNOCKOUT; MORPHINE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; ORGANOMETALLIC COMPOUNDS; PROTOPORPHYRINS;

EID: 84880262863     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-3053-5     Document Type: Article

References (43)

1. Bennett GJ, Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107
2. Boettger MK, Uceyler N, Zelenka M, Schmitt A, Reif A, Chen Y, Sommer C (2007) Differences in inflammatory pain in nNOS-, iNOS- and eNOS-deficient mice. Eur J Pain 11:810-818
3. Bura SA, Nadal X, Ledent C, Maldonado R, Valverde O (2008) A 2A adenosine receptor regulates glia proliferation and pain after peripheral nerve injury. Pain 140:95-103
4. Castañé A, Célérier E, Martín M, Ledent C, Parmentier M, Maldonado R, Valverde O (2006) Development and expression of neuropathic pain in CB1 knockout mice. Neuropharmacology 50:111-122
5. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63
6. Chen Y, Boettger MK, Reif A, Schmitt A, Uçeyler N, Sommer C (2010) Nitric oxide synthase modulates CFA-induced thermal hyperalgesia through cytokine regulation in mice. Mol Pain 6:13
7. Cunha TM, Roman-Campos D, Lotufo CM, Duarte HL, Souza GR, Verri WA Jr, Funez MI, Dias QM, Schivo IR, Domingues AC, Sachs D, Chiavegatto S, Teixeira MM, Hothersall JS, Cruz JS, Cunha FQ, Ferreira SH (2010) Morphine peripheral analgesia depends on activation of the PI3Kgamma/AKT/nNOS/NO/KATP signaling pathway. Proc Natl Acad Sci U S A 107:4442-4447
8. Egea J, Rosa AO, Lorrio S, del Barrio L, Cuadrado A, 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
9. Fan W, Huang F, Wu Z, Zhu X, Li D, He H (2011) Carbon monoxide: a gas that modulates nociception. J Neurosci Res 89:802-807
10. Ferrándiz ML, Maicas N, Garcia-Arnandis I, Terencio MC, Motterlini R, Devesa I, Joosten LA, van den Berg WB, Alcaraz MJ (2008) Treatment with a CO-releasing molecule (CORM-3) reduces joint inflammation and erosion in murine collagen-induced arthritis. Ann Rheum Dis 67:1211-1217
11. Gordh T, Sharma HS, Azizi M, Alm P, Westman J (2000) Spinal nerve lesion induces upregulation of constitutive isoform of heme oxygenase in the spinal cord. An immunohistochemical investigation in the rat. Amino Acids 19:373-381
12. Guan Y, Yaster M, Raja SN, Tao YX (2007) Genetic knockout and pharmacologic inhibition of neuronal nitric oxide synthase attenuate nerve injury-induced mechanical hypersensitivity in mice. Mol Pain 3:29
13. Guillén MI, Megías J, Clérigues V, Gomar F, Alcaraz MJ (2008) The CO-releasing molecule CORM-2 is a novel regulator of the inflammatory process in osteoarthritic chondrocytes. Rheumatology 47:1323-1328
14. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88
15. Hervera A, Negrete R, Leánez S, Martín-Campos JM, Pol O (2010a) The spinal cord expression of neuronal and inducible nitric oxide synthases and their contribution in the maintenance of neuropathic pain in mice. PLoS One 13:e14321
16. Hervera A, Negrete R, Leánez S, Martín-Campos J, Pol O (2010b) 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
17. Hervera A, Negrete R, Leánez S, Martín-Campos JM, Pol O (2011) Peripheral effects of morphine and expression of μ-opioid receptors in the dorsal root ganglia during neuropathic pain: nitric oxide signaling. Mol Pain 7:25
18. Hervera A, Leánez S, Negrete R, Motterlini R, Pol O (2012) Carbon monoxide reduces neuropathic pain and spinal microglial activation by inhibiting nitric oxide synthesis in mice. PLoS One 7:e43693
19. Hunskaar S, Fasmer OB, Hole K (1985) Formalin test in mice, a useful technique for evaluating mild analgesics. J Neurosci Methods 14:69-76
20. Keeble J, Blades M, Pitzalis C, Castro da Rocha FA, Brain SD (2005) The role of substance P in microvascular responses in murine joint inflammation. Br J Pharmacol 144:1059-1066
21. Komatsu T, Sakurada C, Sasaki M, Sanai K, Tsuzuki M, Bagetta G, Sakurada S, Sakurada T (2007) Extracellular signal-regulated kinase (ERK) and nitric oxide synthase mediate intrathecal morphine-induced nociceptive behavior. Neuropharmacology 52:1237-1243
22. Koster R, Anderson M, Beer EJ (1959) Acetic acid for analgesic screening. Fed Proceeds 18:412-416
23. Kuboyama K, Tsuda M, Tsutsui M, Toyohara Y, Tozaki-Saitoh H, Shimokawa H, Yanagihara N, Inoue K (2011) Reduced spinal microglial activation and neuropathic pain after nerve injury in mice lacking all three nitric oxide synthase. Mol Pain 14:7-50
24. LaBuda CJ, Koblish M, Tuthill P, Dolle RE, Little PJ (2006) Antinociceptive activity of the selective iNOS inhibitor AR-C102222 in rodent models of inflammatory, neuropathic and post-operative pain. Eur J Pain 10:505-512
25. Leánez S, Hervera A, 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
26. Li X, Clark JD (2000) The role of heme oxygenase in neuropathic and incisional pain. Anesth Analg 90:677-682
27. Li X, Clark JD (2003) Heme oxygenase type 2 participates in the development of chronic inflammatory and neuropathic pain. J Pain 4:101-107
28. Machelska H, Labuz D, Przewłocki R, Przewłocka B (1997) Inhibition of nitric oxide synthase enhances antinociception mediated by mu, delta and kappa opioid receptors in acute and prolonged pain in the rat spinal cord. J Pharmacol Exp Ther 282:977-984
29. Maicas N, Ferrándiz ML, Devesa I, Motterlini R, Koenders MI, van den Berg WB, 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
30. Malmberg AB, Basbaum AI (1998) Partial sciatic nerve injury in the mouse as a model of neuropathic pain: behavioral and neuroanatomical correlates. Pain 76:215-222
31. Mika J, Osikowicz M, Makuch W, Przewlocka B (2007) Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur J Pharmacol 560:142-149
32. Nascimento CG, 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
33. Nascimento CG, Branco LG (2009) Antinociception synergy between the peripheral and spinal sites of the heme oxygenase-carbon monoxide pathway. Braz J Med Biol Res 42:141-147
34. Negrete R, Hervera A, Leánez S, Martín-Campos JM, 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
35. Obara I, Parkitna JR, Korostynski M, Makuch W, Kaminska D, Przewlocka B, 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
36. Rosa AO, Egea J, Lorrio S, Rojo AI, Cuadrado A, 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
37. Ruiz-Medina J, Ledent C, Valverde O (2011) GPR3 orphan receptor is involved in neuropathic pain after peripheral nerve injury and regulates morphine-induced antinociception. Neuropharmacology 61:43-50
38. Sagar DR, Burston JJ, Hathway GJ, Woodhams SG, Pearson RG, Bennett AJ, Kendall DA, Scammell BE, Chapman V (2011) The contribution of spinal glial cells to chronic pain behaviour in the monosodium iodoacetate model of osteoarthritic pain. Mol Pain 7:88
39. Schmidtko A, Gao W, König P, Heine S, Motterlini R, Ruth P, Schlossmann J, Koesling D, Niederberger E, Tegeder I, Friebe A, Geisslinger G (2008) cGMP produced by NO-sensitive guanylyl cyclase essentially contributes to inflammatory and neuropathic pain by using targets different from cGMP-dependent protein kinase I. J Neurosci 28:8568-8576
40. Tanabe M, Nagatani Y, Saitoh K, Takasu K, Ono H (2009) Pharmacological assessments of nitric oxide synthase isoforms and downstream diversity of NO signaling in the maintenance of thermal and mechanical hypersensitivity after peripheral nerve injury in mice. Neuropharmacology 56:702-708
41. Tegeder I, Del Turco D, Schmidtko A, Sausbier M, Feil R, Hofmann F, Deller T, Ruth P, Geisslinger G (2004) Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc Natl Acad Sci U S A 101:3253-3257
42. Tjølsen A, Berge OG, Hunskaar S, Rosland JH, Hole K (1992) The formalin test: an evaluation of the method. Pain 51:5-17
43. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24:450-455