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

European Journal of Pharmacology

Volumn 556, Issue 1-3, 2007, Pages 55-61

  Nascimento, Carlos G O ^a   Branco, Luiz G S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

(Rat); Carbon monoxide; cGMP; Formalin; Nociception

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; CYCLIC GMP; DEFEROXAMINE; FORMALDEHYDE; GUANYLATE CYCLASE INHIBITOR; HEME LYSINATE; HEME OXYGENASE; HEME OXYGENASE INHIBITOR; METHYLENE BLUE; UNCLASSIFIED DRUG; ZINC DEUTEROPORPHYRIN 2,4 BISGLYCOL;

ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG EFFECT; EVOLUTIONARY ADAPTATION; EXPERIMENTAL MODEL; MALE; NONHUMAN; PAIN; PAIN ASSESSMENT; PAW EDEMA; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

ANIMALS; BILIVERDINE; CARBON MONOXIDE; CYCLIC GMP; DEFEROXAMINE; DEUTEROPORPHYRINS; HEME; HEME OXYGENASE (DECYCLIZING); IRON CHELATING AGENTS; LYSINE; MALE; PAIN; PAIN MEASUREMENT; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 33846066738     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2006.10.009     Document Type: Article

References (42)

1. Abbott F.V., and Teng C.J. The formalin test: a dose-response analysis at three developmental stages. Pain 76 (1998) 337-347
2. Abbott F.V., Franklin K.B.J., and Westbrook R.F. The formalin test: scoring properties of the first and second phases of the pain response in rats. Pain 60 (1995) 91-102
3. Anning P.B., Chen Y., Lamb N.J., Mumby S., Quinlan G.J., Evans T.W., Coderre T.J., Vaccarino A.L., and Melzack R. Central nervous system plasticity in the tonic pain response to subcutaneous formalin injection. Brain Res. 535 (1990) 155-158
4. Coderre T.J., Fundytus M.E., Mckenna J.E., Dalal S., and Melzack R. The formalin test: a validation of the weighted-scores method of behavioural pain rating. Pain 54 (1993) 43-50
5. Cunha F.Q., Teixeira M.M., and Ferreira S.H. Pharmacological modulation of secondary mediator systems - cyclic AMP and cyclic GMP - on inflammatory hyperalgesia. Br. J. Pharmacol. 127 (1999) 671-678
6. Dawson T.M., and Snyder S.H. Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J. Neurosci. 14 9 (1994) 5147-5159
7. Dickenson A.H., and Sullivan A.F. Subcutaneous formalin-induced activity of dorsal horn neurones in the rat: differential response to an intrathecal opiate administered pre or post formalin. Pain 30 (1987) 349-360
8. Duarte I.D., Dos Santos I.R., Lorenzetti B.B., and Ferreira S.H. Analgesia by direct antagonism of nociceptor sensitization involves the arginine-nitric oxide-cGMP pathway. Eur. J. Pharmacol. 217 (1992) 225-227
9. Dubuisson D., and Dennis S.G. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 4 (1977) 161-174
10. Ewing J.F., and Maines M.D. In situ hybridization immunohistochemical localization of heme oxygenase-2 mRNA and protein in normal rat brain: differential distribution of isoenzyme 1 and 2. Mol. Cell. Neurosci. 3 (1992) 559-570
11. Ferreira S.H., Duarte I.D.G., and Lorenzetti B.B. The molecular mechanism of action of periferal morphine analgesia: stimulation of the cGMP system via nitric oxide release. Eur. J. Pharmacol. 201 (1991) 121-122
12. Johnson R.A., Lavessa M., Deseyn K., Scholer M.J., and Nasjletti A. Heme oxygenase substrates acutely lower blood pressure in hypertensive rats. Am. J. Physiol. 271 (1996) H1132-H1138
13. Johnson R.A., Kozma F., and Colombari E. Carbon monoxide: from toxin to endogenous modulator of cardiovascular functions. Braz. J. Med. Biol. Res. 32 (1999) 1-14
14. Li X., and Clark J.D. Heme oxygenase type 2 plays a role in formalin-induced nociception. Pain 86 1-2 (2000) 75-80
15. Li X., and Clark J.D. Spinal cord nitric oxide synthase and heme oxygenase limit morphine induced analgesia. Mol. Brain Res. 95 (2001) 96-102
16. Li X., and Clark J.D. Spinal cord heme oxygenase participates in glutamate-induced pain behavior. Eur. J. Pharmacol. 450 1 (2002) 43-48
17. Linden I.B., Tokola O., Karlsson M., and Tenhunen R. Fate of haem after parenteral administration of haem arginate to rabbits. J. Pharm. Pharmacol. 39 (1987) 96-102
18. Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2 (1988) 2557-2568
19. Maines M.D. Carbon monoxide: an emerging regulatory of cGMP in the brain. Mol. Cell. Neurosci. 4 (1993) 389-397
20. Maines M.D. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 517-554
21. Mancuso C. Heme oxygenase and its products in the nervous system. Antioxid. Redox Signal. 6 5 (2004) 878-887
22. Marks G.S., Brien J.F., Nakatsu K., and Mclaughlin B.E. Does carbon monoxide have a physiological function?. Trends Pharmacol. Sci. 12 (1991) 185-188
23. Morita T., Perrella M.A., Lee M.E., and Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of cGMP. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 1475-1479
24. Odaka Y., Takahashi T., Yamasaki A., Suzuki T., Fujiwara T., Yamada T., Hirakawa M., Fujita H., Ohmori E., and Akagi R. Prevention of halothane-induced hepatotoxicity by hemin pretreatment: protective hole of heme oxygenase-1 induction. Biochem. Pharmacol. 59 (2000) 871-880
25. Ponka P. Cell biology of heme. Am. J. Med. Sci. 318 (1999) 241-256
26. Prado W.A., Schiavon V.F., and Cunha F.Q. Dual effect of local application of nitric oxide donors in a model of incision pain in rats. Eur. J. Pharmacol. 441 (2002) 57-65
27. Puig S., and Sorkin L.S. Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. Pain 64 (1996) 345-355
28. Rokyta R., Holecek V., Pekarkova I., Krejcova J., Racek J., Trefil L., and Yamamotova A. Free radicals after painful stimulation are influenced by antioxidants and analgesics. Neuro Endocrinol. Lett. 24 (2003) 304-309
29. + channel pathway. PNAS 101 (2004) 3680-3685
30. Shibahara S. Heme oxygenase-regulation of and physiological implication in heme catabolism. In: Fujita H., and Medina O.H. (Eds). Regulation of Heme Protein Synthesis (1994), AlphaMed Press 103-116
31. Steiner A.A., and Branco L.G.S. Central CO-heme oxygenase pathway raises body temperature by a prostaglandin-independent way. J. Appl. Physiol. 88 (2000) 1607-1613
32. Steiner A.A., and Branco L.G.S. Carbon monoxide is the heme oxygenase product with a pyretic action: evidence for a cGMP signaling pathway. Am. J. Physiol. 280 (2001) R448-R457
33. Steiner A.A., Colombari E., and Branco L.G.S. Carbon monoxide as a novel mediator of the febrile response in the central nervous system. Am. J. Physiol. 277 (1999) R499-R507
34. Steiner A.A., Branco L.G.S., Cunha F.Q., and Ferreira S.H. Role of the haeme oxygenase/carbon monoxide pathway in mechanical nociceptor hypersensitivity. Br. J. Pharmacol. 132 (2001) 1673-1682
35. Steiner A.A., Reste G., and Branco L.G.S. Role of the brain heme oxygenase-carbon monoxide pathway in stress fever in rats. Neurosci. Lett. 348 (2003) 193-196
36. Stocker R., Yamamoto Y., Mcdonagh A.F., Glazer A.N., and Ames B.N. Bilirubin is an antioxidant of possible physiological importance. Science 235 4792 (1987) 1043-1046
37. Takahashi K., Hara E., Suzuki H., Sasano H., and Shibahara S. Expression of heme oxygenase isozyme mRNA in the human brain and induction of heme oxygenase-1 by nitric oxide donors. J. Neurochem. 67 (1996) 482-489
38. Tenhumen R., Tokola O., and Linden I.B. Haem arginate: a new stable haem compound. J. Pharm. Pharmacol. 39 (1987) 780-786
39. Tjølsen A., Berg O.G., Hunskaar S., Rosland J.H., and Hole K. The formalin test: an evaluation of the method. Pain 51 (1992) 5-17
40. Wheeler-Aceto H., and Cowan A. Buprenorphine and morphine cause antinociception by different transduction mechanisms. Eur. J. Pharmacol. 195 3 (1991) 411-413
41. Yamamoto T., and Nozaki-Taguchi N. Zn protoporphirin IX, an inhibitor of the enzyme that produces carbon monoxide, blocks spinal nociceptive transmission evoked by formalin injection in the rat. Brain Res. 704 (1995) 256-262
42. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110