Contribution of Endogenous Opioids to Gonadal Hormones-Induced Temporomandibular Joint Antinociception

Behavioral Neuroscience

Volumn 123, Issue 5, 2009, Pages 1129-1140

  Fischer, Luana ^a   Arthuri, Mariana T ^b   Torres Chávez, Karla E ^b   Tambeli, Claudia Herrera ^b  

^a Division of Biological Sciences   (Brazil)

^b Faculty of Odontology of Piracicaba   (Brazil)

Author keywords

endogenous opioid system; estradiol; progesterone; temporomandibular joint pain; testosterone

Indexed keywords

ESTRADIOL; FORMALDEHYDE; NALOXONE; OPIATE; PROGESTERONE; TESTOSTERONE PROPIONATE;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HORMONE ACTION; MALE; MYOFASCIAL PAIN; NONHUMAN; ORCHIECTOMY; OVARIECTOMY; PROESTRUS; RAT; TRIGEMINAL NERVE;

ANALGESIA; ANALYSIS OF VARIANCE; ANDROGENS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGENS; ESTROUS CYCLE; FEMALE; FORMALDEHYDE; MALE; NALOXONE; NARCOTIC ANTAGONISTS; OPIOID PEPTIDES; OVARIECTOMY; PAIN; PAIN MEASUREMENT; PROGESTERONE; PROGESTINS; RATS; RATS, WISTAR; TEMPOROMANDIBULAR JOINT; TESTOSTERONE PROPIONATE;

EID: 70350120601     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0017063     Document Type: Article

References (47)

1. Amandusson A., Hallbeck M., Hallbeck A.L., Hermanson O., and Blomqvist A. Estrogen-induced alterations of spinal cord enkephalin gene expression. Pain 83 (1999) 243-248
2. Amandusson A., Hermanson O., and Blomqvist A. Colocalization of oestrogen receptor immunoreactivity and preproenkephalin mRNA expression to neurons in the superficial laminae of the spinal and medullary dorsal horn of rats. European Journal of Neuroscience 8 (1996) 2440-2445
3. 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 Sciences 76 (2005) 1177-1188
4. Bebo Jr. B.F., Schuster J.C., Vandenbark A.A., and Offner H. Androgens alter the cytokine profile and reduce encephalitogenicity of myelin-reactive T cells. Journal of Immunology 162 (1999) 35-40
5. Bereiter D.A. Sex differences in brainstem neural activation after injury to the TMJ region. Cells Tissues Organs 169 (2001) 226-237
6. Bernardi F., Pluchino N., Pieri M., Begliuomini S., Lenzi E., Puccetti S., and Genazzani A.R. Progesterone and medroxyprogesterone acetate effects on central and peripheral allopregnanolone and beta-endorphin levels. Neuroendocrinology 83 (2006) 348-359
7. 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
8. 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 Research 957 (2002) 338-344
9. Campos M., Morais Pde L., and Pupo A.S. Effects of castration and of testosterone replacement on alpha(1)-adrenoceptor subtypes in the rat vas deferens. European Journal of Pharmacology 471 (2003) 149-155
10. Carlsson G., and LeResche L. Epidemiology of temporomandibular disorders. In: Sessle B.J., Bryant P., and Dionne R. (Eds). Progress in pain research and management (1995), IASP Press, Seattle, WA 211-226
11. Chang P.C., Aicher S.A., and Drake C.T. Kappa opioid receptors in rat spinal cord vary across the estrous cycle. Brain Research 861 (2000) 168-172
12. 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. Neuroscience Letters 372 (2004) 250-255
13. Collins J.G., and Ren K. WDR response profiles of spinal dorsal horn neurons may be unmasked by barbiturate anesthesia. Pain 28 (1987) 369-378
14. Danzebrink R.M., Green S.A., and Gebhart G.F. Spinal mu and delta, but not kappa, opioid-receptor agonists attenuate responses to noxious colorectal distension in the rat. Pain 63 (1995) 39-47
15. Diatchenko L., Slade G.D., Nackley A.G., Bhalang K., Sigurdsson A., Belfer I., and Maixner W. Genetic basis for individual variations in pain perception and the development of a chronic pain condition. Human Molecular Genetics 14 (2005) 135-143
16. 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. Journal of the American Dental Association 120 (1990) 273-281
17. 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
18. Fischer L., Clemente J.T., and Tambeli C.H. The protective role of testosterone in the development of temporomandibular joint pain. Journal of Pain 8 (2007) 437-442
19. Fischer L., Parada C.A., and Tambeli C.H. A novel method for subarachnoid drug delivery in the medullary region of rats. Journal of Neuroscience Methods 148 (2005) 108-112
20. 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. Journal of Pain 9 (2008) 630-638
21. Flake N.M., Bonebreak D.B., and Gold M.S. Estrogen and inflammation increase the excitability of rat temporomandibular joint afferent neurons. Journal of Neurophysiology 93 (2005) 1585-1597
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. Harris J.A., Chang P.C., and Drake C.T. Kappa opioid receptors in rat spinal cord: Sex-linked distribution differences. Neuroscience 124 (2004) 879-890
24. He J., Evans C.O., Hoffman S.W., Oyesiku N.M., and Stein D.G. Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury. Experimental Neurology 189 (2004) 404-412
25. Heym J., Steinfels G.F., and Jacobs B.L. Chloral hydrate anesthesia alters the responsiveness of central serotonergic neurons in the cat. Brain Research 291 (1984) 63-72
26. Johansson P., Ray A., Zhou Q., Huang W., Karlsson K., and Nyberg F. Anabolic androgenic steroids increase beta-endorphin levels in the ventral tegmental area in the male rat brain. Neuroscience Research 27 (1997) 185-189
27. Kawata M. Roles of steroid hormones and their receptors in structural organization in the nervous system. Neuroscience Research 24 (1995) 1-46
28. King A., Gardner L., and Loke Y.W. Evaluation of oestrogen and progesterone receptor expression in uterine mucosal lymphocytes. Human Reproduction 11 (1996) 1079-1082
29. Kuroiwa T., Bonnekoh P., and Hossmann K.A. Therapeutic window of halothane anesthesia for reversal of delayed neuronal injury in gerbils: Relationship to postischemic motor hyperactivity. Brain Research 563 (1991) 33-38
30. 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
31. 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. Journal of Orofacial Pain 19 (2005) 193-201
32. McGaraughty S., Reinis S., and Tsoukatos J. A correlogram analysis of the activity in the rostral ventromedial medulla of awake rats and in rats anesthetized with ketamine or pentobarbital following the administration of morphine. Experimental Brain Research 106 (1995) 283-290
33. Montagne-Clavel J., Oliveras J.L., and Martin G. Single-unit recordings at dorsal raphe nucleus in the awake-anesthetized rat: Spontaneous activity and responses to cutaneous innocuous and noxious stimulations. Pain 60 (1995) 303-310
34. 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. Journal of Neurophysiology 89 (2003) 1467-1477
35. Oliveras J.L., Montagne-Clavel J., and Martin G. Drastic changes of ventromedial medulla neuronal properties induced by barbiturate anesthesia: I. Comparison of the single-unit types in the same awake and pentobarbital-treated rats. Brain Research 563 (1991) 241-250
36. Owen M.D., Unal C.B., Callahan M.F., Trivedi K., York C., and Millington W.R. Glycyl-glutamine inhibits the respiratory depression, but not the antinociception, produced by morphine. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 279 (2000) R1944-R1948
37. Petersen S.L., and LaFlamme K.D. Progesterone increases levels of mu-opioid receptor mRNA in the preoptic area and arcuate nucleus of ovariectomized, estradiol-treated female rats. Molecular Brain Research 52 (1997) 32-37
38. Quinones-Jenab V., Jenab S., Ogawa S., Inturrisi C., and Pfaff D.W. Estrogen regulation of mu-opioid receptor mRNA in the forebrain of female rats. Molecular Brain Research 47 (1997) 134-138
39. Roughan J.V., and Flecknell P.A. Effects of surgery and analgesic administration on spontaneous behaviour in singly housed rats. Research in Veterinary Science 69 (2000) 283-288
40. 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
41. Sander H.W., Portoghese P.S., and Gintzler A.R. Spinal kappa-opiate receptor involvement in the analgesia of pregnancy: Effects of intrathecal nor-binaltorphimine, a kappa-selective antagonist. Brain Research 474 (1988) 343-347
42. Shaw F.Z., Chen R.F., and Yen C.T. Dynamic changes of touch- and laser heat-evoked field potentials of primary somatosensory cortex in awake and pentobarbital-anesthetized rats. Brain Research 911 (2001) 105-115
43. 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. Journal of Neuroscience 26 (2006) 5777-5785
44. Stein C., Schafer M., and Machelska H. Attacking pain at its source: New perspectives on opioids. Nature Medicine 9 (2003) 1003-1008
45. Stoffel E.C., Ulibarri C.M., Folk J.E., Rice K.C., and Craft R.M. Gonadal hormone modulation of mu, kappa, and delta opioid antinociception in male and female rats. Journal of Pain 6 (2005) 261-274
46. Unruh A.M. Gender variations in clinical pain experience. Pain 65 (1996) 123-167
47. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110