Influence of estrous cycle and gonadal hormone depletion on nociception and opioid antinociception in female rats of four strains

Journal of Pain

Volumn 6, Issue 6, 2005, Pages 372-383

  Terner, Jolan M ^a   Lomas, Lisa M ^a   Picker, Mitchell J ^a  

^a University of North Carolina at Chapel Hill   (United States)

Author keywords

Antinociception; Gonadal hormones; Nociception; Opioids; Rat strains

Indexed keywords

BUPRENORPHINE; MORPHINE; OPIATE; SEX HORMONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; ESTRUS CYCLE; FEMALE; HORMONE ACTION; MENSTRUAL CYCLE; METESTRUS; NOCICEPTION; NONHUMAN; OVARIECTOMY; PROESTRUS; RAT; RAT STRAIN; THERMOREGULATION;

ANALGESICS, OPIOID; ANIMALS; BUPRENORPHINE; DOWN-REGULATION; DRUG RESISTANCE; ESTROUS CYCLE; FEMALE; GONADAL STEROID HORMONES; MORPHINE; OVARIECTOMY; OVARY; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; RATS; RATS, INBRED F344; RATS, INBRED LEW; RATS, LONG-EVANS; RATS, WISTAR; SEX CHARACTERISTICS; SPECIES SPECIFICITY; TEMPERATURE SENSE;

EID: 20444397451     PISSN: 15265900     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jpain.2005.01.354     Document Type: Article

References (79)

1. B.H. Ali, S.I. Sharif, A. Elkadi Sex differences and the effect of gonadectomy on morphine-induced antinociception and dependence in rats and mice Clin Exp Pharmacol 22 1995 324 344
2. A.M. Aloisi, I. Ceccarelli Role of gonadal hormones in formalin-induced pain responses of male rats Modulation by estradiol and naloxone administration Neuroscience 95 2000 559 566
3. P. Banerjee, T.K. Chatterjee, J.J. Ghosh Ovarian steroids and modulation of morphine-induced analgesia and catalepsy in female rats Eur J Pharmacol 96 1983 291 294
4. R.E. Bartok, R.M. Craft Sex differences in opioid antinociception J Pharmacol Exp Ther 282 1997 769 778
5. L.A. Berglund, H. Derendorf, J.W. Simpkins Desensitization of brain opiate receptor mechanisms Gonadal steroid treatments that stimulate luteinizing hormone secretion Endocrinology 122 1988 2718 2726
6. L.A. Berglund, J.W. Simpkins Alterations in brain opiate receptor mechanisms on proestrus afternoon Neuroendocrinology 48 1988 394 400
7. H.B. Bradshaw, J.L. Temple, E. Wood, K.J. Berkley Estrous variations in behavioral responses to vaginal and uterine distention in the rat Pain 82 1999 187 197
8. R.L. Butcher, W.E. Collins, N.W. Fugo Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrous cycle of the rat Endocrinology 94 1974 1704 1708
9. J.C. Chen, E.R. Smith, M. Cahill, R. Cohen, J.B. Fishman The opioid receptor binding of dezocine, morphine, fentanyl, butorphanol, and nalbuphine Life Sci 52 1992 389 396
10. T.J. Cicero, B. Nock, E.R. Meyer Gender-related differences in the antinociceptive properties of morphine J Pharmacol Exp Ther 279 1996 767 773
11. T.J. Cicero, B. Nock, L. O'Connor, E.R. Meyer Role of steroids in sex differences in morphine-induced analgesia Activational and organizational effects J Pharmacol Exp Ther 300 2002 695 701
12. Committee for Research and Ethical Issues of the IASP Ethical standards for investigations of experimental pain in animals Pain 16 1983 109 110
13. C.D. Cook, A.C. Barrett, E.L. Roach, J.R. Bowman, M.J. Picker Sex-related differences in the antinociceptive effects of opioids Importance of rat genotype, nociceptive stimulus intensity, and efficacy at the mu opioid receptor Psychopharmacology 150 2000 430 442
14. R.M. Craft, L.M. Heideman, R.E. Bartok Effect of gonadectomy on discriminative stimulus effects of morphine in female versus male rats Drug Alcohol Depend 53 1999 95 109
15. R.M. Craft, S.A. Bernal Sex differences in opioid antinociception κ and 'mixed action' agonists Drug Alcohol Depend 63 2001 215 228
16. R.M. Craft, J.S. Mogil, A.M. Aloisi Sex differences in pain and analgesia the role of gonadal hormones Eur J Pain 8 2004 397 411
17. M.B. Dawson-Basoa, A.R. Gintzler 17-Beta-estradiol and progesterone modulate an intrinsic opioid analgesic system Brain Res 601 1993 241 245
18. F.S. Dhabhar, B.S. McEwen, R.L. Spencer Adaptation to prolonged or repeated stress Comparison between rat strains showing intrinsic differences in reactivity to acute stress Neuroendocrinology 65 1997 360 368
19. G.I. Elmer, J.O. Pieper, S.S. Negus, J.H. Woods Genetic variance in nociception and its relationship to the potency of morphine-induced analgesia in thermal and chemical assays Pain 75 1998 129 140
20. 6 glioma cell line expressing the μ opioid receptor J Pharmacol Exp Ther 278 1996 1121 1127
21. H.C. Evrard, J. Balthazart Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons J Neurosci 24 2004 7225 7229
22. J.S. Feine, M.C. Bushnell, D. Miron, G.H. Duncan Sex differences in the perception of noxious heat stimuli Pain 44 1991 255 262
23. R.B. Fillingim, W. Maixner, S.S. Girdler, K.C. Light, M.B. Harris, D.S. Sheps, G.A. Mason Ischemic but not thermal pain sensitivity varies across the menstrual cycle Psychosom Med 59 1997 512 520
24. R.B. Fillingim, R.R. Edwards, T. Powell The relationship of sex and clinical pain to experimental pain responses Pain 83 1999 419 425
25. M.E. Freeman The ovarian cycle of the rat E. Knobil J. Neill The physiology of reproduction 1988 Raven Press New York, NY 1893 1928
26. C.A. Frye, B.C. Bock, R.B. Kanarek Hormonal milieu affects tailflick latency in female rats and may be attenuated by access to sucrose Physiol Behav 52 1992 699 706
27. C.A. Frye, J.E. Duncan Estradiol benzoate potentiates neuroactive steroids' effects on pain sensitivity Pharmacol Biochem Behav 53 1996 27 32
28. R.W. Gear, N.C. Gordon, P.H. Heller, S.M. Paul, C. Miaskowski, J.D. Levine Gender difference in analgesic response to the κ-opioid pentazocine Neurosci Lett 205 1996 207 209
29. R.W. Gear, C. Miaskowski, N.C. Gordon, S.M. Paul, P.H. Heller, J.D. Levine κ-Opioids produce significantly greater analgesia in women than in men Nat Med 2 1996 1248 1250
30. R.W. Gear, C. Miaskowski, N.C. Gordon, S.M. Paul, P.H. Heller, J.D. Levine The κ opioid nalbuphine produces gender- and dose-dependent analgesia and antianalgesia in patients with postoperative pain Pain 83 1999 339 345
31. F.T. Gordon, M.R. Soliman The effects of estradiol and progesterone on pain sensitivity and brain opioid receptors in ovariectomized rats Horm Behav 30 1996 244 250
32. R.P. Hammer μ-Opiate receptor binding in the medial preoptic area is cyclical and sexually dimorphic Brain Res 515 1990 187 192
33. A.K. Islam, M.L. Cooper, R.J. Bodnar Interactions among aging, gender, and gonadectomy effects upon morphine antinociception in rats Physiol Behav 54 1993 45 53
34. V. Kayser, K.J. Berkley, H. Keita, M. Gautron, G. Guilbaud Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat Brain Res 742 1996 352 354
35. K.L. Kepler, B. Kest, J.M. Kiefel, M.L. Cooper, R.J. Bodnar Roles of gender, gonadectomy and estrous phase in the analgesic effects of intracerebroventricular morphine in rats Pharmacol Biochem Behav 34 1989 119 127
36. B. Kest, S.G. Wilson, J.S. Mogil Sex differences in supraspinal morphine analgesia are dependent on genotype J Pharmacol Exp Ther 289 1999 1370 1375
37. B. Kest, E. Sarton, A. Dahan Gender differences in opioid-mediated analgesia animal and human studies Anesthesiology 93 2000 539 547
38. E.K. Krzanowska, R.J. Bodnar Analysis of sex and gonadectomy differences in β-endorphin antinociception elicited from the ventrolateral periaqueductal grey in rats Eur J Pharmacol 392 2000 157 161
39. E.K. Krzanowska, S. Ogawa, D.W. Pfaff, R.J. Bodnar Reversal of sex differences in morphine analgesia elicited from the ventrolateral periaqueductal gray in rats by neonatal hormone manipulations Brain Res 929 2002 1 9
40. W.R. Lariviere, S.G. Wilson, T.M. Laughlin, A. Kokayeff, E.E. West, S.M. Adhikari, Y. Wan, J.S. Mogil Heritability of nociception. III. Genetic relationships among commonly used assays of nociception and hypersensitivity Pain 97 2002 75 86
41. R.E. Leipheimer, R.V. Gallo Acute and long-term changes and pituitary mechanisms regulating pulsatile luteinizing hormone secretion after ovariectomy in the rat Neuroendocrinology 37 1983 421 426
42. W. Maixner, C. Humphrey Gender differences in pain and cardiovascular responses to forearm ischemia Clin J Pain 9 1993 16 25
43. M. Martinez-Gomez, Y. Cruz, M. Salas, R. Hudson, P. Pacheco Assessing pain threshold in the rat Changes with estrus and time of day Physiol Behav 55 1994 651 657
44. M.Y. McGinnis, L.C. Krey, N.J. MacLusky, B.S. McEwen Steroid receptor levels in intact and ovariectomized estrogen-treated rats An examination of quantitative, temporal and endocrine factors influencing the efficacy of an estradiol stimulus Neuroendocrinology 33 1981 158 165
45. P.E. Micevych, E.F. Rissman, J.A. Gustafsson, K. Sinchak Estrogen receptor-α is required for estrogen-induced μ-opioid receptor internalization J Neurosci Res 71 2003 802 810
46. 1 receptor activation in the arcuate nucleus of female rats J Neurosci 24 2004 947 955
47. J.S. Mogil, J.K. Belknap Sex and genotype differences determine the selective activation of neurochemically-distinct mechanisms of swim stress-induced analgesia Pharmacol Biochem Behav 56 1997 61 66
48. J.S. Mogil, S.G. Wilson, K. Bon, S.E. Lee, K. Chung, P. Raber, J.O. Pieper, H.S. Hain, J.K. Belknap, L. Hubert, G.I. Elmer, J.M. Chung, M. Devor Heritability of nociception I responses of 11 inbred mouse strains on 12 measures of nociception Pain 80 1999 67 82
49. J.S. Mogil, E.J. Chesler, S.G. Wilson, J.M. Juraska, W.F. Sternberg Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype Neurosci Biobehav Rev 24 2000 375 389
50. G.S. Montes, E.H. Luque Effects of ovarian steroids on vaginal smears Acta Anat 133 1988 192 199
51. D. Morgan, C.D. Cook, M.A. Smith, M.J. Picker An examination of the interactions between the antinociceptive effects of morphine and various mu-opioids The role of intrinsic efficacy and stimulus intensity Anesth Analg 88 1999 407 413
52. D. Morgan, C.D. Cook, M.J. Picker Sensitivity to the discriminative stimulus and antinociceptive effects of μ opioids Role of rat strain, stimulus intensity and intrinsic efficacy at the μ opioid receptor J Pharmacol Exp Ther 289 1999 965 975
53. C.D. Myers, M.E. Robinson, J.L. Riley, D. Sheffield Sex, gender, and blood pressure Contributions to experimental pain report Psychosom Med 63 2001 545 550
54. S.S. Negus, N.K. Mello Opioid antinociception in ovariectomized monkeys Comparison with antinociception in males and effects of estradiol replacement J Pharmacol Exp Ther 290 1999 1132 1140
55. S.S. Negus, B.A. Wurrey, N.K. Mello Sex differences in thermal nociception and prostaglandin-induced thermal hypersensitivity in rhesus monkeys J Pain 5 2004 92 103
56. G. Nomikos, C. Spyraki, A. Kazandjian, A. Sfikakis Estrogen treatment to ovariectomized rats modifies morphine-induced behavior Pharmacol Biochem Behav 27 1987 611 617
57. J. Pajot, C. Ressot, I. Ngom, A. Woda Gonadectomy induces site-specific differences in nociception in rats Pain 104 2003 367 373
58. M. Pfleeger, P.A. Straneva, R.B. Fillingim, W. Maixner, S.S. Girdler Menstrual cycle, blood pressure and ischemic pain sensitivity in women A preliminary investigation Int J Psychophysiol 27 1997 161 166
59. A. Ratka, J.W. Simpkins Dose-dependent effects of chronic treatment with estradiol or progesterone on LH secretion in ovariectomized rats Endocrine Res 16 1990 165 184
60. A. Ratka, J.W. Simpkins Effects of estradiol and progesterone on the sensitivity to pain and on morphine-induced antinociception in female rats Horm Behav 25 1991 217 228
61. J.L. Riley, M.E. Robinson, E.A. Wise, D.D. Price A meta-analytic review of pain perception across the menstrual cycle Pain 81 1999 225 235
62. M.E. Roth, A.G. Casimir, M.E. Carroll Influence of estrogen in the acquisition of intravenously self-administered heroin in female rats Pharmacol Biochem Behav 72 2002 313 318
63. S.M. Ryan, S.F. Maier The estrous cycle and estrogen modulate stress-induced analgesia Behav Neurosci 102 1988 371 380
64. A. Sandner-Kiesling, J.C. Eisenach Pharmacology of opioid inhibition to noxious uterine cervical distension Anesthesiology 97 2002 966 971
65. D.E. Selley, J.T. Herbert, D. Morgan, C.D. Cook, M.J. Picker, L.J. Sim-Selley Effect of strain and sex on mu opioid receptor-mediated G-protein activation in rat brain Brain Res Bull 60 2003 201 208
66. E.V. Shekunova, A.Y. Bespalov Estrous cycle stage-dependent expression of acute tolerance to morphine analgesia in rats Eur J Pharmacol 486 2004 259 264
67. J.W. Simpkins Effects of age and ovarian steroids on responses to opiates in the female rat Neurobiol Aging 15 1994 545 552
68. J. Stewart, B. Woodside, Y. Shaham Ovarian hormones do not affect the initiation and maintenance of intravenous self-administration of heroin in the female rat Psychobiology 24 1996 154 159
69. E.C. Stoffel, C.M. Ulibarri, R.M. Craft Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats Pain 103 2003 285 302
70. R.J. Tallarida, R.B. Murray Manual of pharmacologic calculations with computer programs 1987 Springer Berlin
71. J.M. Terner, A.C. Barrett, E. Grossell, M.J. Picker Influence of gonadectomy on the antinociceptive effects of opioids in male and female rats Psychopharmacology 163 2002 183 193
72. J.M. Terner, L.M. Lomas, E.S. Smith, A.C. Barrett, M.J. Picker Pharmacogenetic analysis of sex differences in opioid antinociception in rats Pain 106 2003 381 391
73. M. Vincler, W. Maixner, C.J. Vierck, A.R. Light Estrous cycle modulation of nociceptive behaviors elicited by electrical stimulation and formalin Pharmacol Biochem Behav 69 2001 315 324
74. E.P. Vinogradova, D.A. Zhukov, A.S. Batuev The effects of stages of the estrous cycle on pain thresholds in female white rats Neurosci Behav Physiol 33 2003 269 272
75. E.A. Walker, E.R. Butelman, B.R. DeCosta, J.H. Woods Opioid thermal antinociception in rhesus monkeys Receptor mechanisms and temperature dependency J Pharmacol Exp Ther 267 1993 280 286
76. E.A. Walker, M.J. Picker, L.A. Dykstra Three-choice discrimination in pigeons is based on relative efficacy differences among opioids Psychopharmacology 155 2001 389 396
77. N.G. Weiland, P.M. Wise Estrogen and progesterone regulate opiate receptor densities in multiple brain regions Endocrinology 126 1990 804 808
78. S.G. Wilson, S.B. Smith, E.J. Chesler, K.A. Melton, J.J. Haas, B. Mitton, K. Strasburg, L. Hubert, S.L. Rodriguez-Zas, J.S. Mogil The heritability of antinociception Common pharmacogenetic mediation of five neurochemically distinct analgesics J Pharmacol Exp Ther 304 2003 547 559
79. D.R. Woolfolk, S.G. Holtzman Rat strain differences in the potentiation of morphine-induced analgesia by stress Pharmacol Biochem Behav 51 1995 699 703