Persistent pain model reveals sex difference in morphine potency

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 291, Issue 2, 2006, Pages

  Wang, Xiaoya ^a   Traub, Richard J ^b,c   Murphy, Anne Z ^a,c  

^a GEORGIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Antihyperalgesic; Antinociception; Inflammation; Opioids

Indexed keywords

MORPHINE;

ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG POTENCY; FEMALE; MALE; NONHUMAN; PAIN; PAIN ASSESSMENT; PRIORITY JOURNAL; RAT; SEX DIFFERENCE;

ANALGESIA; ANALGESICS, OPIOID; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FREUND'S ADJUVANT; HYPERALGESIA; MALE; MORPHINE; PAIN; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SEX CHARACTERISTICS; SODIUM CHLORIDE;

EID: 33745858630     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00022.2006     Document Type: Article

References (60)

1. Bartok RE and Craft RM. Sex differences in opioid antinociception. J Pharmacol Exp Ther 282: 769-778, 1997.
2. Basbaum AI, Clanton CH, and Fields HL. Three bulbospinal pathways from the rostral medulla of the cat: an autoradiographic study of pain-modulating systems. J Comp Neurol 178: 209-224, 1978.
3. Basbaum AI and Fields HL. Endogenous pain control mechanisms: review and hypothesis. Ann Neurol 4: 451-462, 1978.
4. Basbaum AI and Fields HL. Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7: 309-338, 1984.
5. Bodnar RJ, Romero MT, and Kramer E. Organismic variables and pain inhibition: roles of gender and aging. Brain Res Bull 21: 947-953, 1988.
6. Boyer JS, Morgan MM, and Craft RM. Microinjection of morphine into the rostral ventromedial medulla produces greater antinociception in male compared to female rats. Brain Res 796: 315-318, 1998.
7. Brookoff D. Chronic pain: 1. A new disease? Hosp Pract (Off Ed) 35: 45-52, 59, 2000.
8. Brookoff D. Chronic pain: 2. The case for opioids. Hosp Pract (Off Ed) 35: 69-72, 75-66, 81-64, 2000.
9. Cepeda MS and Carr DB. Women experience more pain and require more morphine than men to achieve a similar degree of analgesia. Anesth Analg 97: 1464-1468, 2003.
10. Cicero TJ, Nock B, and Meyer ER. Gender-related differences in the antinociceptive properties of morphine. J Pharmacol Exp Ther 279: 767-773, 1996.
11. Cicero TJ, Nock B, and Meyer ER. Sex-related differences in morphine's antinociceptive activity: relationship to serum and brain morphine concentrations. J Pharmacol Exp Ther 282: 939-944, 1997.
12. Cook CD and Nickerson MD. Nociceptive sensitivity and opioid antinociception and antihyperalgesia in Freund's adjuvant-induced arthritic male and female rats. J Pharmacol Exp Ther 313: 449-459, 2005.
13. Craft RM. Sex differences in drug- and non-drug-induced analgesia. Life Sci 72: 2675-2688, 2003.
14. Craft RM. Sex differences in opioid analgesia: "from mouse to man". Clin J Pain 19: 175-186, 2003.
15. Craft RM and Bernal SA. Sex differences in opioid antinociception: kappa and 'mixed action' agonists. Drug Alcohol Depend 63: 215-228, 2001.
16. Craft RM, Kruzich PJ, Boyer JS, Harding JW, and Hanesworth JM. Sex differences in discriminative stimulus and diuretic effects of the kappa opioid agonist U69,593 in the rat. Pharmacol Biochem Behav 61: 395-403, 1998.
17. Craft RM, Mogil JS, and Aloisi AM. Sex differences in pain and analgesia: the role of gonadal hormones. Eur J Pain 8: 397-411, 2004.
18. Dubner R and Ruda MA. Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15: 96-103, 1992.
19. Duncan KA and Murphy AZ. Sex-linked differences in mu opiate receptor distribution in the rat brain. Soc Neuroscience Abstr, 592.3 2005.
20. Eckersell CB, Popper P, and Micevych PE. Estrogen-induced alteration of mu-opioid receeptor immunoreactivity in the medial preoptic nucleus and medial amygdala. J Neurosci 18: 3967-3976, 1998.
21. Flores CM and Mogil JS. The pharmacogenetics of analgesia: toward a genetically-based approach to pain management. Pharmacogenomics 2: 177-194, 2001.
22. Flores JA, El Banoua F, Galan-Rodriguez B, and Fernandez-Espejo E. Opiate anti-nociception is attenuated following lesion of large dopamine neurons of the periaqueductal grey: critical role for D1 (not D2) dopamine receptors. Pain 110: 205-214, 2004.
23. Freeman M. The neuroendcroine control of the ovarian cycle of the rat. In: The Physiology of Reproduction, edited by Knobil E and Neill J. New York: Raven Press, 1988, p. 1893-1928.
24. Guan Y, Guo W, Zou SP, Dubner R, and Ren K. Inflammation-induced upregulation of AMPA receptor subunit expression in brain stem pain modulatory circuitry. Pain 104: 401-413, 2003.
25. Guan Y, Terayama R, Dubner R, and Ren K. Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. J Pharmacol Exp Ther 300: 513-520, 2002.
26. Hurley RW and Hammond DL. The analgesic efects of supraspinal mu and delta opioid receptor agonists are potentiated during persistent inflammation. J Neurosci 20: 1249-1259, 2000.
27. Hurley RW and Hammond DL. Contribution of endogenous enkephalins to the enhanced analgesic effects of supraspinal mu opioid receptor agonists after inflammatory injury. J Neurosci 21: 2536-2545, 2001.
28. Islam AK, Cooper ML, and Bodnar RJ. Interactions among aging, gender, and gonadectomy effects upon morphine antinociception in rats. Physiol Behav 54: 45-53, 1993.
29. Jensen TS and Yaksh TL III. Comparison of the antinociceptive action of mu and delta opioid receptor ligands in the periaqueductal gray matter, medial and paramedial ventral medulla in the rat as studied by microinjection technique. Brain Res 372: 301-312, 1986.
30. Ji Y, Murphy AZ, and Traub RJ. Estrogen modulates the visceromotor reflex and responses of spinal dorsal horn neurons to colorectal stimulation in the rat. J Neurosci 23: 3908-3915, 2003.
31. Kavaliers M and Innes D. Stress-induced opioid analgesia and activity in deer mice: sex and population differences. Brain Res 425: 49-56, 1987.
32. Kavaliers M and Innes DG. Sex and day-night differences in opiate-induced responses of insular wild deer mice, Peromyscus maniculatus triangularis. Pharmacol Biochem Behav 27: 477-482, 1987.
33. Kayser V and Guilbaud G. The analgesic effects of morphine, but not those of the enkephalinase inhibitor thiorphan, are enhanced in arthritic rats. Brain Res 267: 131-138, 1983.
34. Kelly MJ, Qiu J, and Ronnekleiv OK. Estrogen modulation of G-protein-coupled receptor activation of potassium channels in the central nervous system. Ann NY Acad Sci 1007: 6-16, 2003.
35. Kepler KL, Kest B, Kiefel JM, Cooper ML, and Bodnar RJ. Roles of gender, gonadectomy and estrous phase in the analgesic effects of intracerebroventricular morphine in rats. Pharmacol Biochem Behav 34: 119-127, 1989.
36. Kepler KL, Standifer KM, Paul D, Kest B, Pasternak GW, and Bodnar RJ. Gender effects and central opioid analgesia. Pain 45: 87-94, 1991.
37. Kest B, Wilson SG, and Mogil JS. Sex differences in supraspinal morphine analgesia are dependent on genotype. J Pharmacol Exp Ther 289: 1370-1375, 1999.
38. Komisaruk BR. Antinociceptive effects of vaginal stimulation in rats: neurophysiological and behavioral studies. Brain Res 137: 85-107, 1977.
39. Krzanowska EK and Bodnar RJ. Analysis of sex and gonadectomy differences in B-endorphin antinociception elicted from the ventrolateral periaqueductal gray in rats. Eur J Pharm 392: 157-161, 2000.
40. Krzanowska EK and Bodnar RJ. Morphine antinociception elicted from the ventrolateral periaqueductal gray is sensitive to sex and gonadectomy differences in rats. Brain Res 821: 224-230, 1999.
41. Lane DA, Patel PA, and Morgan MM. Evidence for an intrinsic mechanism of antinociceptive tolerance within the ventrolateral periaqueductal gray of rats. Neuroscience 135: 227-234, 2005.
42. Lariviere WR, Wilson SG, Laughlin TM, Kokayeff A, West EE, Adhikari SM, Wan Y, and Mogil JS. Heritability of nociception. III Genetic relationships among commonly used assays of nociception and hypersensitivity. Pain 97: 75-86, 2002.
43. Loyd D and Murphy AZ. Sex differences in the anatomical and functional organization of the periaqueductal gray-rostral ventromedial medullary pathway in the rat: A potential circuit mediateing the sexually dimorphic actions of morphine. J Comp Neurol 496: 723-728, 2006.
44. Malyala A, Kelly MJ, and Ronnekleiv OK. Estrogen modulation of hypothalamic neurons: Activation of multiple signaling pathways and gene expression changes. Steroids 70: 397-406, 2005.
45. Martin PR. Headaches. In: Health Care: A Behavioral Approach, edited by King NJ and Remenyi A. Sydney, Australia: Grune & Stratton, 1986, p. 145-157.
46. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, Le Meur M, Dolle P, Tzavara E, Hanoune J, Roques BP, and Kieffer BL. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383: 819-823, 1996.
47. Mogil JS, Chesler EJ, Wilson SG, Juraska JM, and Sternberg WF. Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype. Neurosci Biobehav Rev 24: 375-389, 2000.
48. Negus SS and Mello NK. Opioid antinociception in ovariectomized monkeys: comparison with antinociception in males and effects of estradiol replacement. J Pharmacol Exp Ther 290: 1132-1140, 1999.
49. Ossipov MH, Kovelowski CJ, and Porreca F. The increase in morphine antinociceptive potency produced by carrageenan-induced hindpaw inflammation is blocked by naltrindole, a selective delta-opioid antagonist. Neurosci Lett 184: 173-176, 1995.
50. Parra MC, Nguyen TN, Hurley RW, and Hammond DL. Persistent inflammatory nociception increases levels of dynorphin 1-17 in the spinal cord, but not in supraspinal nuclei involved in pain modulation. J Pain 3: 330-336, 2002.
51. Shaqura MA, Zollner C, Mousa SA, Stein C, and Schafer M. Characterization of mu opioid receptor binding and G protein coupling in rat hypothalamus, spinal cord, and primary afferent neurons during inflammatory pain. J Pharmacol Exp Ther 308: 712-718, 2004.
52. Sora I, Takahashi N, Funada M, Ujike H, Revay RS, Donovan DM, Miner LL, and Uhl GR. Opiate receptor knockout mice define mu receptor roles in endogenous nociceptive responses and morphine-induced analgesia. Proc Natl Acad Sci USA 94: 1544-1549, 1997.
53. Spetea M, Rydelius G, Nylander I, Ahmed M, Bileviciute-Ljungar I, Lundeberg T, Svensson S, and Kreicbergs A. Alteration in endogenous opioid systems due to chronic inflammatory pain conditions. Eur J Pharmacol 435: 245-252, 2002.
54. Stein C, Millan MJ, and Herz A. Unilateral inflammation of the hindpaw in rats as a model of prolonged noxious stimulation: alterations in behavior and nociceptive thresholds. Pharmacol Biochem Behav 31: 455-451, 1988.
55. Stein C, Millan MJ, Yassouridis A, and Herz A. Antinociceptive effects of mu- and kappa-agonists in inflammation are enhanced by a peripheral opioid receptor-specific mechanism. Eur J Pharmacol 155: 255-264, 1988.
56. Stoffel EC, Ulibarri CM, and Craft RM. Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain 103: 285-302, 2003.
57. Stoffel EC, Ulibarri CM, Folk JE, Rice KC, and Craft RM. Gonadal hormone modulation of mu, kappa, and delta opioid antinociception in male and female rats. J Pain 6: 261-274, 2005.
58. Terner JM, Lomas LM, and Picker MJ. Influence of estrous cycle and gonadal hormone depletion on nociception and opioid antinociception in female rats of four strains. J Pain 6: 372-383, 2005.
59. Williams FG, Mullet MA, and Beitz AJ. Basal release of Met-enkephalin and neurotensin in the ventrolateral periaqueductal gray matter of the rat: a microdialysis study of antinociceptive circuits. Brain Res 690: 207-216, 1995.
60. Zollner C, Shaqura MA, Bopaiah CP, Mousa S, Stein C, and Schafer M. Painful inflammation-induced increase in mu-opioid receptor binding and G-protein coupling in primary afferent neurons. Mol Pharmacol 64: 202-210, 2003.