Peripheral estradiol induces temporomandibular joint antinociception in rats by activating the nitric oxide/cyclic guanosine monophosphate signaling pathway

Neuroscience

Volumn 164, Issue 2, 2009, Pages 724-732

  Favaro Moreira N C ^a   Torres Chavez K E ^a   Fischer, L ^b   Tambeli, C H ^a  

^a Faculty of Dentistry of Piracicaba   (Brazil)

^b Division of Biological Sciences   (Brazil)

Author keywords

cGMP; estradiol; formalin; nitric oxide; nociception; temporomandibular joint pain

Indexed keywords

1H (1,2,4) OXADIASOLO[4,2A]QUINOXALIN 1 ONE; BOVINE SERUM ALBUMIN; CYCLIC GMP; ESTRADIOL; FORMALDEHYDE; FULVESTRANT; GUANYLATE CYCLASE INHIBITOR; N(G) NITROARGININE; NALOXONE; NITRIC OXIDE; OPIATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTHRALGIA; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DIESTRUS; DRUG EFFICACY; DRUG MECHANISM; ESTRADIOL BLOOD LEVEL; FEMALE; MALE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROESTRUS; RAT; SIGNAL TRANSDUCTION; TEMPOROMANDIBULAR JOINT DISORDER;

ANALGESICS; ANIMALS; CYCLIC GMP; DIESTRUS; ESTRADIOL; FEMALE; FORMALDEHYDE; GUANYLATE CYCLASE; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OVARIECTOMY; PAIN; PROESTRUS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TEMPOROMANDIBULAR JOINT;

EID: 70349757165     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.08.012     Document Type: Article

References (48)

1. Almeida R.T., and Duarte I.D. Nitric oxide/cGMP pathway mediates orofacial antinociception induced by electroacupuncture at the St36 acupoint. Brain Res 1188 (2007) 54-60
2. Arthuri M.T., Gameiro G.H., Tambeli C.H., and de Arruda Veiga M.C. Peripheral effect of a kappa opioid receptor antagonist on nociception evoked by formalin injected in TMJ of pregnant rats. Life Sci 76 (2005) 1177-1188
3. Bereiter D.A. Sex differences in brainstem neural activation after injury to the TMJ region. Cells Tissues Organs 169 (2001) 226-237
4. Brown C.H., Brunton P.J., and Russell J.A. Rapid estradiol-17beta modulation of opioid actions on the electrical and secretory activity of rat oxytocin neurons in vivo. Neurochem Res 33 (2007) 614-623
5. Butcher R.L., Collins W.E., and Fugo N.W. Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17beta throughout the 4-day estrous cycle of the rat. Endocrinology 94 (1974) 1704-1708
6. Cairns B.E., Sim Y., Bereiter D.A., Sessle B.J., and Hu J.W. Influence of sex on reflex jaw muscle activity evoked from the rat temporomandibular joint. Brain Res 957 (2002) 338-344
7. Ceccarelli I., Fiorenzani P., Grasso G., Lariviere W.R., Massafra C., Massai L., Muscettola M., and Aloisi A.M. Estrogen and mu-opioid receptor antagonists counteract the 17 beta-estradiol-induced licking increase and interferon-gamma reduction occurring during the formalin test in male rats. Pain 111 (2004) 181-190
8. Ceccarelli I., Fiorenzani P., Massafra C., and Aloisi A.M. Long-term ovariectomy changes formalin-induced licking in female rats: the role of estrogens. Reprod Biol Endocrinol 1 (2003) 24
9. Chaban V.V., Mayer E.A., Ennes H.S., and Micevych P.E. Estradiol inhibits ATP-induced intracellular calcium concentration increase in dorsal root ganglia neurons. Neuroscience 118 (2003) 941-948
10. Chen Z., Yuhanna I.S., Galcheva-Gargova Z., Karas R.H., Mendelsohn M.E., and Shaul P.W. Estrogen receptor alpha mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest 103 (1999) 401-406
11. Clemente J.T., Parada C.A., Veiga M.C., Gear R.W., and Tambeli C.H. Sexual dimorphism in the antinociception mediated by kappa opioid receptors in the rat temporomandibular joint. Neurosci Lett 372 (2004) 250-255
12. 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
13. Durate I.D., Lorenzetti B.B., and Ferreira S.H. Peripheral analgesia and activation of the nitric oxide-cyclic GMP pathway. Eur J Pharmacol 186 (1990) 289-293
14. Dworkin S.F., Huggins K.H., LeResche L., Von Korff M., Howard J., Truelove E., and Sommers E. Epidemiology of signs and symptoms in temporomandibular disorders: clinical signs in cases and controls. J Am Dent Assoc 120 (1990) 273-281
15. Eisenberg E., Vos B.P., and Strassman A.M. The peripheral antinociceptive effect of morphine in a rat model of facial pain. Neuroscience 72 (1996) 519-525
16. Evrard H.C., and Balthazart J. Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons. J Neurosci 24 (2004) 7225-7229
17. Fiorelli G., Gori F., Frediani U., Franceschelli F., Tanini A., Tosti-Guerra C., Benvenuti S., Gennari L., Becherini L., and Brandi M.L. Membrane binding sites and non-genomic effects of estrogen in cultured human pre-osteoclastic cells. J Steroid Biochem Mol Biol 59 (1996) 233-240
18. Fischer L., Clemente J.T., and Tambeli C.H. The protective role of testosterone in the development of temporomandibular joint pain. J Pain 8 (2007) 437-442
19. Fischer L., Torres-Chavez K.E., Clemente-Napimoga J.T., Jorge D., Arsati F., de Arruda Veiga M.C., and Tambeli C.H. The influence of sex and ovarian hormones on temporomandibular joint nociception in rats. J Pain 9 (2008) 630-638
20. Flake N.M., Hermanstyne T.O., and Gold M.S. Testosterone and estrogen have opposing actions on inflammation-induced plasma extravasation in the rat temporomandibular joint. Am J Physiol Regul Integr Comp Physiol 291 (2006) R343-R348
21. Gaumond I., Arsenault P., and Marchand S. The role of sex hormones on formalin-induced nociceptive responses. Brain Res 958 (2002) 139-145
22. Gordon F.T., and Soliman M.R. Diurnal variation in the acute effects of estradiol and progesterone on beta-endorphin and Met-enkephalin levels in specific brain regions of ovariectomized rats. Pharmacology 49 (1994) 192-198
23. Granados-Soto V., Rufino M.O., Gomes Lopes L.D., and Ferreira S.H. Evidence for the involvement of the nitric oxide-cGMP pathway in the antinociception of morphine in the formalin test. Eur J Pharmacol 340 (1997) 177-180
24. Haas D.A., Nakanishi O., MacMillan R.E., Jordan R.C., and Hu J.W. Development of an orofacial model of acute inflammation in the rat. Arch Oral Biol 37 (1992) 417-422
25. Jost A. Genetic and hormonal factors in sex differentiation of the brain. Psychoneuroendocrinology 8 (1983) 183-193
26. Keith Jr. J.C., Albert L.M., Leathurby Y., Follettie M., Wang L., Borges-Marcucci L., Chadwick C.C., Steffan R.J., and Harnish D.C. The utility of pathway selective estrogen receptor ligands that inhibit nuclear factor-kappa B transcriptional activity in models of rheumatoid arthritis. Arthritis Res Ther 7 (2005) R427-R438
27. Kelly M.J., and Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol Metab 12 (2001) 152-156
28. Kuba T., Wu H.B., Nazarian A., Festa E.D., Barr G.A., Jenab S., Inturrisi C.E., and Quinones-Jenab V. Estradiol and progesterone differentially regulate formalin-induced nociception in ovariectomized female rats. Horm Behav 49 (2006) 441-449
29. Lagrange A.H., Ronnekleiv O.K., and Kelly M.J. Estradiol-17 beta and mu-opioid peptides rapidly hyperpolarize GnRH neurons: a cellular mechanism of negative feedback?. Endocrinology 136 (1995) 2341-2344
30. Lee D.Y., Chai Y.G., Lee E.B., Kim K.W., Nah S.Y., Oh T.H., and Rhim H. 17Beta-estradiol inhibits high-voltage-activated calcium channel currents in rat sensory neurons via a non-genomic mechanism. Life Sci 70 (2002) 2047-2059
31. LeResche L., Mancl L., Sherman J.J., Gandara B., and Dworkin S.F. Changes in temporomandibular pain and other symptoms across the menstrual cycle. Pain 106 (2003) 253-261
32. LeResche L., Sherman J.J., Huggins K., Saunders K., Mancl L.A., Lentz G., and Dworkin S.F. Musculoskeletal orofacial pain and other signs and symptoms of temporomandibular disorders during pregnancy: a prospective study. J Orofac Pain 19 (2005) 193-201
33. Mannino C.A., South S.M., Quinones-Jenab V., and Inturrisi C.E. Estradiol replacement in ovariectomized rats is antihyperalgesic in the formalin test. J Pain 8 (2007) 334-342
34. McEwen B.S. Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J Appl Physiol 91 (2001) 2785-2801
35. Okamoto K., Hirata H., Takeshita S., and Bereiter D.A. Response properties of TMJ units in superficial laminae at the spinomedullary junction of female rats vary over the estrous cycle. J Neurophysiol 89 (2003) 1467-1477
36. Pajot J., Ressot C., Ngom I., and Woda A. Gonadectomy induces site-specific differences in nociception in rats. Pain 104 (2003) 367-373
37. Pol O. The involvement of the nitric oxide in the effects and expression of opioid receptors during peripheral inflammation. Curr Med Chem 14 (2007) 1945-1955
38. Qian Y., Chao D.S., Santillano D.R., Cornwell T.L., Nairn A.C., Greengard P., Lincoln T.M., and Bredt D.S. cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J Neurosci 16 (1996) 3130-3138
39. Rittner H.L., Brack A., and Stein C. Pain and the immune system. Br J Anaesth 101 (2008) 40-44
40. Rosland J.H. The formalin test in mice: the influence of ambient temperature. Pain 45 (1991) 211-216
41. Roughan J.V., and Flecknell P.A. Effects of surgery and analgesic administration on spontaneous behaviour in singly housed rats. Res Vet Sci 69 (2000) 283-288
42. Roveroni R.C., Parada C.A., Cecilia M., Veiga F.A., and Tambeli C.H. Development of a behavioral model of TMJ pain in rats: the TMJ formalin test. Pain 94 (2001) 185-191
43. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., and Liao J.K. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407 (2000) 538-541
44. Smith Y.R., Stohler C.S., Nichols T.E., Bueller J.A., Koeppe R.A., and Zubieta J.K. Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women. J Neurosci 26 (2006) 5777-5785
45. Stefano G.B., Prevot V., Beauvillain J.C., Cadet P., Fimiani C., Welters I., Fricchione G.L., Breton C., Lassalle P., Salzet M., and Bilfinger T.V. Cell-surface estrogen receptors mediate calcium-dependent nitric oxide release in human endothelia. Circulation 101 (2000) 1594-1597
46. Toda N., Ayajiki K., and Okamura T. Neural mechanism underlying basilar arterial constriction by intracisternal l-NNA in anesthetized dogs. Am J Physiol 265 (1993) H103-H107
47. Unruh A.M. Gender variations in clinical pain experience. Pain 65 (1996) 123-167
48. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110