Sex differences in opioid analgesia, hyperalgesia, tolerance and withdrawal: Central mechanisms of action and roles of gonadal hormones

Hormones and Behavior

Volumn 58, Issue 1, 2010, Pages 72-81

  Bodnar, Richard J ^a,c   Kest, Benjamin ^b,c  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Activational effects of gonadal hormones; Delta opioid receptor; Kappa opioid receptor; Morphine; Mu opioid receptor; Organizational effects of gonadal hormones; Ovariectomy

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; 3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE METHANESULFONATE; BUPRENORPHINE; BUTORPHANOL; DECAHYDRO 6 PHOSPHONOMETHYL 3 ISOQUINOLINECARBOXYLIC ACID; DELTA OPIATE RECEPTOR; DEXTROMETHORPHAN; DIZOCILPINE; ESTRADIOL; KAPPA OPIATE RECEPTOR; KETAMINE; MORPHINE; MU OPIATE RECEPTOR; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; NALBUPHINE; NALTREXONE; NARCOTIC ANALGESIC AGENT; OXYCODONE; PENTAZOCINE; PROGESTERONE; SEX HORMONE; SPIRADOLINE; STEROID HORMONE; TESTOSTERONE;

ANALGESIA; ARTHRITIS; ARTICLE; DISEASE MODEL; DRUG EFFICACY; DRUG EXPOSURE; DRUG POTENCY; DRUG POTENTIATION; DRUG TOLERANCE; DRUG WITHDRAWAL; ESTRUS; GENETIC VARIABILITY; GONADECTOMY; HORMONE ACTION; HUMAN; HYPERALGESIA; NONHUMAN; OPIATE ADDICTION; PAIN; POSTOPERATIVE PAIN; PRIORITY JOURNAL; SEX DIFFERENCE; ANIMAL; METABOLISM; PHYSIOLOGY; WITHDRAWAL SYNDROME;

ANALGESICS, OPIOID; ANIMALS; DRUG TOLERANCE; GONADAL HORMONES; HUMANS; PAIN; SEX FACTORS; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 77953479985     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.09.012     Document Type: Article

References (145)

1. Ali B., Sharif S., Elkadi A. Sex differences and the effect of gonadectomy on morphine-induced antinociception and dependence in rats and mice. Clin. Exp. Pharmacol. Physiol. 1995, 22:342-344.
2. Arvidsson U., Dado R.J., Riedl M., Lee J.H., Law P.Y., Loh H.H., Elde R., Wessendorf M.W. Delta-opioid immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J. Neurosci. 1995, 15:1215-1235.
3. Arvidsson U., Riedl M., Chakrabati S., Vulchanova L., Lee J.H., Nakano A.H., Lin X., Loh H.H., Law P.Y., Wessendorf M.W. The kappa-opioid receptor is primarily postsynaptic: combined immunohistochemical localization of the receptor and endogenous opioids. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:5062-5066.
4. Baamonde A.I., Hidalgo A., Andres-Trelles F. Sex-related differences in the effects of morphine and stress on visceral pain. Neuropharmacology 1989, 28:967-970.
5. Badillo-Martinez D., Kirchgessner A.L., Butler P.D., Bodnar R.J. Monosodium glutamate and morphine analgesia: test-specific effects. Neuropharmacology 1984, 23:1141-1149.
6. Banerjee T., Chatterjee T., Ghosh J.J. Ovarian steroids and modulation of morphine-induced analgesia and catalepsy in female rats. Eur. J. Pharmacol. 1983, 96:291-294.
7. Barrett A.C. Low efficacy opioids: implications for sex differences in opioid antinociception. Exp. Clin. Psychopharmacol. 2006, 14:1-11.
8. Barrett A.C., Cook C.D., Terner J.M., Craft R.M., Picker M.J. The importance of sex and relative efficacy at the mu opioid receptor in the development of tolerance and cross-tolerance to the antinociceptive effects of opioids. Psychopharmacology 2001, 158:154-164.
9. Barrett A.C., Cook C.D., Terner J.M., Roach E.L., Syvanthong C., Picker M.J. Sex and rat strain determine sensitivity to kappa opioid-induced antinociception. Psychopharmacology 2002, 160:170-181.
10. Barrett A.C., Smith E.S., Picker M.J. Sex-related differences in mechanical nociception and antinociception produced by mu and kappa opioids in rats. Eur. J. Pharmacol. 2002, 452:163-173.
11. Bartok R.E., Craft R.M. Sex differences in opioid antinociception. J. Pharmacol. Exp. Ther. 1997, 282:769-778.
12. Basbaum A.I., Fields H.L. Endogenous pain control mechanisms: review and hypothesis. Ann. Neurol. 1978, 4:451-462.
13. Berkley K.J. Sex differences in pain. Behav. Brain Sci. 1997, 20:371-380.
14. Berkley K.J., Zalcman S.S., Simon V.R. Sex and gender differences in pain and inflammation: a rapidly maturing field. Am. J. Physiol., Regul. Integr. Comp. Physiol. 2006, 291:R241-R244.
15. Bernal S.A., Morgan M.M., Craft R.M. PAG mu opioid receptor activation underlies sex differences in morphine antinociception. Behav. Brain Res. 2007, 177:126-133.
16. Bijur P.E., Esses D., Birnbaum A., Chang A.K., Schechter C., Gallagher E.J. Response to morphine in male and female patients: analgesia and adverse events. Clin. J. Pain 2008, 24:192-198.
17. Bodnar R.J., Commons K., Pfaff D.W. Central neural states relating sex and pain 2002, 258. Johns Hopkins University Press, Baltimore, MD.
18. Borzan J., Fuchs P.N. Organizational and activational effects of testosterone on carrageenan-induced inflammatory pain and morphine analgesia. Neuroscience 2006, 143:885-893.
19. Boyer J.S., Morgan M.M., Craft R.M. Microinjection of morphine into the rostral-ventromedial medulla produces greater antinociception in male compared to female rats. Brain Res. 1998, 796:315-318.
20. Bryant C.D., Eitan S., Sinchak K., Fanselow M.S., Evans C.J. NMDA receptor antagonism disrupts the development of morphine analgesic tolerance in male, but not female C57BL/6J mice. Am. J. Physiol., Regul. Integr. Comp. Physiol. 2006, 291:R315-R326.
21. Candido J., Lufty K., Billings B., Sierra V., Duttaroy A., Inturrisi C.E. Effect of adrenal and sex hormones on opioid analgesia and opioid receptor regulation. Pharmacol. Biochem. Behav. 1992, 42:685-692.
22. Cataldo G., Bernal S.Y., Markowitz A., Ogawa S., Ragnauth A., Pfaff D.W., Bodnar R.J. Organizational manipulation of gonadal hormones and systemic morphine analgesia in female rats: effects of adult ovariectomy and estradiol replacement. Brain Res. 2005, 1059:13-19.
23. Cataldo G., Pytte C., Bodnar R.J. Ibotenic acid lesions placed in the ventromedial or medial pre-optic hypothalamic nuclei enhance systemic morphine analgesia in female, but not male rats. Soc. Neurosci. Abstr. 2009, (abstract #458.21).
24. Cataldo, G., Medina, K., Bernal, S.Y., Rozengurtel, S., Bodnar, R.J., in press. Neonatal and adult gonadal hormone manipulations enhance morphine analgesia elicited from the ventrolateral periaqueductal gray in female rats. Int. J. Neurosci.
25. Cepeda M.S., Carr D.B. Women experience more pain and require more morphine than men to achieve a similar degree of analgesia. Anesth. Analg. 2003, 97:1464-1468.
26. Chen C.K., Shu L.W., Liang P.L., Hung T.M., Lin S.K. Drug use patterns and gender differences among heroin addicts hospitalized for detoxification. Changgeng Yixue Zazhi 1998, 21:172-178.
27. Chia Y.Y., Chow L.H., Hung C.C., Liu K., Ger L.P., Wang P.N. Gender and pain upon movement are associated with the requirements for postoperative patient-controlled iv analgesia: a prospective survey of 2298 Chinese patients. Can. J. Anaesth. 2002, 49:249-255.
28. Cicero T.J., Nock B., Meyer E.R. Gender-related differences in the antinociceptive properties of morphine. J. Pharmacol. Exp. Ther. 1996, 279:767-773.
29. Cicero T.J., Nock B., Meyer E.R. Sex-related differences in morphine's antinociceptive activity: relationship to serum and brain morphine concentrations. J. Pharmacol. Exp. Ther. 1997, 282:939-944.
30. Cicero T.J., Nock B., Meyer E.R. Gender-linked differences in the expression of physical dependence in the rat. Pharmacol. Biochem. Behav. 2002, 72:691-697.
31. Cicero T.J., Nock B., O'Connor L., Meyer E.R. Role of steroids in sex differences in morphine-induced analgesia: activational and organizational effects. J. Pharmacol. Exp. Ther. 2002, 300:695-701.
32. Claiborne J., Nag S., Mokha S.S. Activation of opioid receptor like-1 receptor in the spinal cord produces sex-specific antinociception in the rat: estrogen attenuates antinociception in the female, whereas testosterone is required for the expression of antinociception in the male. J. Neurosci. 2006, 26:13048-13053.
33. Clemente J.T., Parada C.A., Veiga M.C., Gear R.W., Tambeli C.H. Sexual dimorphism in the antinociception mediated by kappa opioid receptors in the rat temporomandibular joint. Neurosci. Lett. 2004, 372:250-255.
34. Commons K.G., Aicher S.A., Kow L.M., Pfaff D.W. Presynaptic and postsynaptic relations of mu-opioid receptors to gamma-aminobutyric acid-immunoreactive and medullary-projecting periaqueductal gray neurons. J. Comp. Neurol. 2000, 419:532-542.
35. Cook C.D., Nickerson M.D. Nociceptive sensitivity and opioid antinociception and antihyperalgesia in Freund's adjuvant-induced arthritic male and female rats. J. Pharmacol. Exp. Ther. 2005, 313:449-459.
36. Cook C.D., Barrett A.C., Roach E.L., Bowman J.R., Picker M.J. Sex-related differences in the antinociceptive effects of opioids: importance of rat genotype, nociceptive stimulus intensity, and efficacy at the mu opioid receptor. Psychopharmacology 2000, 150:430-442.
37. Craft R.M. Sex differences in opioid analgesia: "from mouse to man". Clin. J. Pain 2003, 19:175-186.
38. Craft R.M., Bernal S.A. Sex differences in opioid antinociception: kappa and mixed action agonists. Drug Alcohol Depend. 2001, 63:215-228.
39. Craft R.M., Lee D.A. NMDA antagonist modulation of morphine antinociception in female vs. male rats. Pharmacol. Biochem. Behav. 2005, 80:639-649.
40. Craft R.M., Leitl M.D. Potentiation of morphine antinociception by pentobarbital in female vs male rats. Pain 2006, 121:115-125.
41. Craft R.M., Stratmann J.A., Bartok R.E., Walpole T.I., King S.J. Sex differences in development of morphine tolerance and dependence in the rat. Psychopharmacology 1999, 143:1-7.
42. Craft R.M., Mogil J.S., Aloisi A.M. Sex differences in pain and analgesia: the role of gonadal hormones. Eur. J. Pain 2004, 8:397-411.
43. Diaz S.L., Kemmling A.K., Rubio M.C., Balerio G.N. Lack of sex-related differences in the prevention by baclofen of the morphine withdrawal syndrome in mice. Behav. Pharmacol. 2001, 12:75-79.
44. Diaz S.L., Kemmling A.K., Bonavita C.D., Rubio M.C., Balerio G.N. Baclofen reestablishes micro-opioid receptor levels modified by morphine withdrawal syndrome in either sex. Synapse 2004, 54:24-29.
45. Diaz S.L., Kemmling A.K., Rubio M.C., Balerio G.N. Morphine withdrawal syndrome: involvement of the dopaminergic system in prepubertal male and female mice. Pharmacol. Biochem. Behav. 2005, 82:601-607.
46. Drake C.T., DeOliveira A.X., Harris J.A., Connor D.M., Winkler C.W., Aicher S.A. Kappa opioid receptors in the rostral ventromedial medulla of male and female rats. J. Comp. Neurol. 2007, 500:465-476.
47. El-Kadi A.O., Sharif S.I. The influence of various experimental conditions on the expression of naloxone-influenced withdrawal symptoms in mice. Gen. Pharmacol. 1994, 25:1505-1510.
48. Elliott J.C., Picker M.J., Nelson C.J., Carrigan K.A., Lysle D.T. Sex differences in opioid-induced enhancement of contact hypersensitivity. J. Invest. Dermatol. 2003, 121:1053-1059.
49. Elliott J.C., Picker M.J., Sparrow A.J., Lysle D.T. Dissociation between sex differences in the immunological, behavioral and physiological effects of kappa- and delta-opioids in Fischer rats. Psychopharmacology 2006, 185:66-75.
50. Fields H.L., Basbaum A.I. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Ann. Rev. Neurosci. 1984, 7:309-338.
51. Fillingim R.B., Ness T.J., Glover T.L., Campbell C.M., Hastie B.A., Price D.D., Staud R. Morphine responses and experimental pain: sex differences in side effects and cardiovascular responses but not analgesia. J. Pain 2005, 2:116-124.
52. Gaumond I., Spooner M.F., Marchand S. Sex differences in opioid-mediated pain inhibitory mechanisms during the interphase in the formalin test. Neuroscience 2007, 46:366-374.
53. Gear R.W., Gordon N.C., Heller P.H., Paul S., Miaskowski C., Levine J.D. Gender difference in analgesic response to the kappa opioid pentazocine. Neurosci. Lett. 1996, 205:207-209.
54. Gear R.W., Miaskowski C., Gordon N.C., Paul S.M., Heller P.M., Levine J.D. Kappa-opioids produce significantly greater analgesia in women than in men. Nat. Med. 1996, 2:1248-1250.
55. Gear R.W., Miaskowski C., Gordon N.C., Paul S.M., Heller P.H., Levine J.D. The kappa opioid nalbuphine produces gender- and dose-dependent analgesia and antianalgesia in patients with postoperative pain. Pain 1999, 83:339-345.
56. Gijsbers K., Nicholson F. Experimental pain thresholds influenced by sex of experimenter. Percept. Mot. Skills 2005, 101:803-807.
57. Gintzler A.R., Schnell S.A., Gupta D.S., Liu N.J., Wessendorf M.W. Relationship of spinal dynorphin neurons to delta-opioid receptors and estrogen receptor alpha: anatomical basis for ovarian sex steroid opioid antinociception. J. Pharmacol. Exp. Ther. 2008, 326:725-731.
58. Gordon N.C., Gear R.W., Heller P.H., Paul S., Miaskowski C., Levine J.D. Enhancement of morphine analgesia by GABA B agonist baclofen. Neuroscience 1995, 69:345-349.
59. Greenfield S.F., Manwani S.G., Nargiso J.E. Epidemiology of substance use disorders in women. Obstet. Gynecol. Clin. North Am. 2003, 30:413-446.
60. Greenspan J.D., Craft R.M., LeResche L., Berkley K.J., Fillingim R.B., Gold M.S., Holdcroft A., Lautenbacher S., Mayer E.A., Mogil J.S., Murphy A.Z., Traub R.J., Aloisi A.M., Arendt-Neilsen L., Arnold A., Bereiter D., Blaustein J., Bodnar R.J., Chang L., Gintzler A., Hallin R., Hargreaves K., Keogh E., McCarthy P., Naliboff B., Robinson M., Steiner M., Stohler C., Wesselmann U., Xu X., Young E. Studying sex and gender differences in pain and analgesia: a consensus report. Pain 2007, 132:S26-S45.
61. Grisel J.E., Allen S., Nemmani K.V., Fee J.R., Carliss R. The influence of dextromethorphan on morphine analgesia in Swiss Webster mice is sex-specific. Pharmacol. Biochem. Behav. 2005, 81:131-138.
62. Hamann S.R., Malik H., Sloan J.W., Wala E.P. Interactions of "ultra-low" doses of naltrexone and morphine in mature and young male and female rats. Recept Channels 2004, 10:73-81.
63. Harris J.A., Chang P.C., Drake C.T. Kappa opioid receptors in rat spinal cord: sex-linked distribution differences. Neuroscience 2004, 124:879-890.
64. Hoffman G.E., Dohanics J., Watson R.E., Wiegand S.J. The hypothalamic ventromedial nucleus sends a met-enkephalin projection to the preoptic area's periventricular zone in the female rat. Mol. Brain Res. 1996, 36:201-210.
65. Holtman J.R., Wala E.P. Characterization of morphine-induced hyperalgesia in male and female rats. Pain 2005, 114:62-70.
66. Holtman J.R., Wala E.P. Characterization of the antinociceptive effect of oxycodone in male and female rats. Pharmacol. Biochem. Behav. 2006, 83:100-108.
67. Holtman J.R., Jing X., Wala E.P. Sex-related differences in the enhancement of morphine antinociception by NMDA receptor antagonists in rats. Pharmacol. Biochem. Behav. 2003, 76:285-293.
68. Holtman J.R., Sloan J.W., Wala E.P. Morphine tolerance in male and female rats.Pharmacol. Biochem. Behav. 2004, 77:517-523.
69. Hopkins E., Rossi G., Kest B. Sex differences in systemic morphine analgesic tolerance following intrathecal morphine injections. Brain Res. 2004, 1014:244-246.
70. Islam A.K., Cooper M.L., Bodnar R.J. Interactions among aging, gender and gonadectomy effects upon morphine antinociception in rats. Physiol. Behav. 1993, 54:45-53.
71. Ji Y., Murphy A.Z., Traub R.J. Sex differences in morphine analgesia of visceral pain are supraspinally and peripherally mediated. Am. J. Physiol., Regul. Integr. Comp. Physiol. 2006, 291:R307-R314.
72. Ji Y., Murphy A.Z., Traub R.J. Estrogen modulation of morphine analgesia of visceral pain in female rats is supraspinally and peripherally mediated. J. Pain 2007, 8:494-502.
73. Juni A., Klein G., Kowalczyk B., Ragnauth A., Kest B. Sex differences in hyperalgesia during morphine infusion: effect of gonadectomy and estrogen treatment. Neuropharmacology 2008, 54:1264-1270.
74. Kalinichev M., Easterling K.W., Holtzman S.G. Early neonatal experience of Long-Evans rats resulted in long-lasting changes in morphine tolerance and dependence. Psychopharmacology 2001, 157:305-312.
75. Kalyuzhny A.E., Arvidsson U., Wu W., Wessendorf M.W. Mu-opioid and delta-opioid receptors are expressed in brainstem antinociceptive circuits: studies using immunohistochemistry and retrograde tract-tracing. J. Neurosci. 1996, 16:6490-6503.
76. Kasson B.G., George R. Endocrine influences on the action of morphine: IV. effects of sex and strain. Life Sci. 1984, 34:1627-1634.
77. Kavaliers M., Innes D.G.L. Sex and day/night differences in opiate-induced responses of insular wild deer mice, Peromyscus maniculatis triangularis. Pharmacol. Biochem. Behav. 1987, 27:477-482.
78. Kavaliers M., Innes D.G.L. Developmental changes in opiate-induced analgesia in deer mice: sex and population differences. Brain Res. 1990, 516:326-331.
79. Kepler K.L., Kest B., Kiefel J.M., Cooper M.L., Bodnar R.J. Roles of gender, gonadectomy and estrus phase in the analgesic effects of intracrebroventricular morphine in rats. Pharmacol. Biochem. Behav. 1989, 34:119-127.
80. Kepler K.L., Standifer K.M., Paul D., Pasternak G.W., Kest B., Bodnar R.J. Differential gender effects upon central opioid analgesia. Pain 1991, 45:87-95.
81. Kest B., Hopkins E. Morphine tolerance after chronic intra-cerebroventricular injection in male and female mice. Brain Res. 2001, 892:208-210.
82. Kest B., Brodsky M., Sadowski B., Mogil J.S., Inturrisi C.E. Mu opioid receptor (MOR-1) mRNA levels are altered in mice with differential analgesic sensitivity to the mu opioid DAMGO. Analgesia 1995, 1:498-501.
83. Kest B., Wilson S.G., Mogil J.S. Genetic mediation of supraspinal morphine analgesia: Strain and sex differences. J. Pharmacol. Exp. Ther. 1999, 289:1370-1375.
84. Kest B., Palmese C., Hopkins E. A comparison of morphine analgesic tolerance in male and female mice. Brain Res. 2000, 879:17-22.
85. Kest B., Palmese C.A., Hopkins E., Adler M., Juni A. Assessment of acute and chronic morphine dependence in male and female mice. Pharmacol. Biochem. Behav. 2001, 70:149-156.
86. Kow L.M., Commons K.G., Ogawa S., Pfaff D.W. Potentiation of the excitatory action of NMDA in ventrolateral periaqueductal gray by the mu-opioid receptor agonist, DAMGO. Brain Res. 2002, 935:87-102.
87. Kowalczyk W.J., Juni A., Klein G., Hruby V., Mogil J.S., Kest B. Female-specific mediation of morphine hyperalgesia by the melanocortin-1 receptor. Soc. Neurosci. Abstr. 2006, (abstract #444.20).
88. Krzanowska E.K., Bodnar R.J. Morphine antinociception elicited from the ventrolateral periaqueductal gray is sensitive to sex and gonadectomy differences in rats. Brain Res. 1999, 821:224-230.
89. Krzanowska E.K., Bodnar R.J. Analysis of sex and gonadectomy differences in beta-endorphin antinociception elicited from the ventrolateral periaqueductal gray in rats. Eur. J. Pharmacol. 2000, 392:157-161.
90. Krzanowska E.K., Ogawa S., Pfaff D.W., Bodnar R.J. Reversal of sex differences in morphine analgesia elicited from the ventrolateral periaqueductal gray in rats by neonatal hormone manipulations. Brain Res. 2002, 929:1-9.
91. Lehman K.A., Paral F., Sabatowski R. Postoperative schmerztherapie mit hydromorphone und metamizol. Anaesthesia 2001, 2001(50):750-756.
92. Levine F.M., De Simone L.L. The effects of experimenter gender on pain report in male and female subjects. Pain 1991, 44:69-72.
93. Liu N.J., von Gizycki H., Gintzler A.R. Sexually dimorphic recruitment of spinal opioid analgesic pathways by the spinal application of morphine. J. Pharmacol. Exp. Ther. 2007, 322:654-660.
94. Lomas L.M., Picker M.J. Behavioral assessment of temporal summation in the rat: sensitivity to sex, opioids and modulation by NMDA receptor antagonists. Psychopharmacology 2005, 180:84-94.
95. Lomas L.M., Barrett A.C., Terner J.M., Lysle D.T., Picker M.J. Sex differences in the potency of kappa opioids and mixed-action opioids administered systemically and at the site of inflammation against capsaicin-induced hyperalgesia in rats. Psychopharmacology 2007, 191:273-285.
96. Loyd D.R., Murphy A.Z. Sex differences in the anatomical and functional organization of the periaqueductal gray-rostral ventromedial medullary pathway in the rat: a potential circuit mediating the sexually dimorphic actions of morphine. J. Comp. Neurol. 2006, 496:723-738.
97. Loyd D.R., Murphy A.Z. Androgen and estrogen (alpha) receptor localization on periaqueductal gray neurons projecting to the rostral ventromedial medulla in the male and female rat. J. Chem. Neuroanat. 2008, 36:216-226.
98. Loyd D.R., Morgan M.M., Murphy A.Z. Morphine preferentially activates the periaqueductal gray-rostral ventromedial medullary pathway in the male rat: a potential mechanism for sex differences in antinociception. Neuroscience 2007, 147:456-468.
99. Loyd D.R., Morgan M.M., Murphy A.Z. Sexually dimorphic activation of the periaqueductal gray-rostral ventromedial medullary circuit during the development of tolerance to morphine in the rat. Eur. J. Neurosci. 2008, 27:1517-1524.
100. Loyd D.R., Wang X., Murphy A.Z. Sex differences in mu-opioid receptor expression in the rat midbrain periaqueductal gray are essential for eliciting sex differences in morphine analgesia. J. Neurosci. 2008, 28:14007-14017.
101. Mannino C.A., South S.M., Inturrisi C.E., Quinones-Jenab V. Pharmacokinetics and effects of 17beta-estradiol and progesterone implants in ovariectomized rats. J. Pain 2005, 6:809-816.
102. Mansour A., Fox C.A., Akil H., Watson S.J. Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 1995, 18:22-29.
103. Mansour A., Fox C.A., Burke S., Akil H., Watson S.J. Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J. Chem. Neuroanat. 1995, 8:283-305.
104. Miaskowski C., Levine J.D. Does opioid analgesia show a gender preference for females?. Pain Forum 1999, 8:48-50.
105. Mitrovic I., Margeta-Mitrovic M., Bader S., Stoffel M., Jan L.Y., Basbaum A.I. Contribution of GIRK2-mediated postsynaptic signaling to opiate and alpha 2-adrenergic analgesia and analgesic sex differences. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:271-276.
106. Mogil J.S., Chanda M.L. The case for the inclusion of female subjects in basic science studies of pain. Pain 2005, 117:1-5.
107. Mogil J.S., Chesler E.J., Wilson S.G., Juraska J.M., Sternberg W.F. Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype. Neurosci. Biobehav. Rev. 2000, 24:375-389.
108. Mogil J.S., Wilson S.G., Chesler E.J., Rankin A.L., Nemmani K.V., Lariviere W.R., Groce K.M., Wallace M.R., Kaplan L., Staud R., Ness T.J., Glover T.L., Stankova M., Mayorov A., Hruby V.J., Grisel J.E., Fillingim R.B. The melanocortin-1 receptor gene mediates female-specific mechanisms of analgesia in mice and humans. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4867-4872.
109. Mogil J.S., Ritchie J., Smith S.B., Strasburg K., Kaplan L., Wallace M.R., Romberg R.R., Bijl H., Sarton E.Y., Fillingim R.B., Dahan A. Melanocortin-1 receptor gene variants affect pain and mu-opioid analgesia in mice and humans. J. Med. Genet. 2005, 42:583-587.
110. Mousavi Z., Shafaghi B., Kobarfard F., Jorjani M. Sex differences and role of gonadal hormones on glutamate level in the nucleus accumbens in morphine tolerant rats: a microdialysis study. Eur. J. Pharmacol. 2007, 554:145-149.
111. Murphy A.Z., Suckow S.K., Johns M., Traub R.J. Sex differences in the activation of the spinoparabrachial circuit by visceral pain. Physiol. Behav. 2009, 97:205-212.
112. Negus S.S., Mello N.K. Opioid antinociception in ovariectomized monkeys: comparison with antinociception in males and effects of estradiol replacement. J. Pharmacol. Exp. Ther. 1999, 290:1132-1140.
113. Nemmani K.V., Grisel J.E., Stowe J.R., Smith-Carliss R., Mogil J.S. Modulation of morphine analgesia by site-specific N-methyl-d-aspartate receptor antagonists: dependence on sex, site of antagonism, morphine dose, and time. Pain 2004, 109:274-283.
114. Okamoto K., Tashiro A., Hirata H., Bereiter D.A. Differential modulation of TMJ neurons in superficial laminae of trigeminal subnucleus caudalis/upper cervical cord junction region of male and cycling female rats by morphine. Pain 2005, 114:203-211.
115. Olofsen E., Romberg R., Bijl H., Mooren R., Engbers F., Kest B., Dahan A. Alfentanil and placebo analgesia: absence of sex differences. Anesthesiology 2005, 103:130-139.
116. Ossipov M.H., Lai J., King T., Vanderah T.W., Malan T.P., Hruby V.J., Porreca F.J. Antinociceptive and nociceptive actions of opioids. J. Neurobiol. 2004, 61:126-148.
117. Papaleo F., Contarino A. Gender- and morphine dose-linked expression of spontaneous somatic opiate withdrawal in mice. Behav. Brain Res. 2006, 170:110-118.
118. Patrick C.A., Ko M.-C., Woods J.H. Comparison of the antinociceptive effects induced by kappa opioid agonists in male and female mice. Analgesia 1999, 4:397-404.
119. Peckham E.M., Barkley L.M., Divin M.F., Cicero T.J., Traynor J.R. Comparison of the antinociceptive effect of acute morphine in female and male Sprague-Dawley rats using the long-lasting mu-antagonist methocinnamox. Brain Res. 2005, 1058:137-147.
120. Priest C.A., Eckersell C.B., Micevych P.E. Estrogen regulates preproenkephalin-A mRNA levels in the rat ventromedial nucleus: temporal and cellular aspects. Mol. Brain Res. 1995, 28:251-262.
121. Romano G.J., Harlan R.E., Shivers B.D., Howells R.D., Pfaff D.W. Estrogen increases proenkephalin messenger ribonucleic acid levels in the ventromedial hypothalamus of the rat. Mol. Endocrinol. 1988, 2:1320-1328.
122. Romano G.J., Mobbs C.V., Howells R.D., Pfaff D.W. Estrogen regulation of proenkephalin gene expression in the ventromedial hypothalamus of the rat: temporal qualities and synergism with progesterone. Mol. Brain Res. 1989, 5:51-58.
123. Romano G.J., Mobbs C.V., Lauber A., Howells R.D., Pfaff D.W. Differential regulation of proenkephalin gene expression by estrogen in the ventromedial hypothalamus of male and female rats: implications for the molecular basis of a sexually differentiated behavior. Brain Res. 1990, 536:63-68.
124. Romberg R., Olofsen E., Sarton E., den Hartigh J., Taschner P., Dahan A. Pharmacokinetic/pharmacodynamic modeling of morphine-6-glucuronide-induced analgesia in healthy volunteers: absence of sex differences. Anesthesiology 2004, 100:120-133.
125. Sadeghi M., Sianati S., Anaraki D.K., Ghasemi M., Paydar M.J., Sharif B., Mehr S.E., Dehpour A.R. Study of morphine-induced dependence in gonadectomized male and female mice. Pharmacol. Biochem. Behav 2009, 91:604-609.
126. Sarton E., Olofsen E., Romberg R., den Hartigh J., Kest B., Nieuwenhuijs D., Burm A., Teppema L., Dahan A. Sex differences in morphine analgesia: an experimental study in healthy volunteers. Anesthesiology 2000, 93:1245-1254.
127. Shane R., Bernal S.Y., Rozengurtel S., Bodnar R.J. Estrus phase differences in female rats in morphine antinociception elicited from the ventrolateral periaqueductal gray. Int. J. Neurosci. 2007, 117:811-822.
128. Shekunova E.V., Bespalov A.Y. Estrous cycle stage-dependent expression of acute tolerance to morphine analgesia in rats. Eur. J. Pharmacol. 2004, 486:259-264.
129. Shekunova E.V., Bespalov A.Y. Effects of memantine on estrogen-dependent acute tolerance to the morphine analgesia in female rats. Eur. J. Pharmacol. 2006, 535:78-85.
130. South S.M., Wright A.W., Lau M., Mather L.E., Smith M.T. Sex-related differences in antinociception and tolerance development following chronic intravenous infusion of morphine in the rat: modulatory role of testosterone via morphine clearance. J. Pharmacol. Exp. Ther. 2001, 297:446-457.
131. Stoffel E.C., Ulibarri C.M., Craft R.M. Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain 2003, 103:285-302.
132. Stoffel E.C., Ulibarri C.M., Folk J.E., Rice K.C., Craft R.M. Gonadal hormone modulation of mu, kappa, and delta opioid antinociception in male and female rats. J. Pain 2005, 6:261-274.
133. Terner J.M., Barrett A.C., Grossell E., Picker M.J. Influence of gonadectomy on the antinociceptive effects of opioids in male and female rats. Psychopharmacology 2002, 163:183-193.
134. Terner J.M., Barrett A.C., Cook C.D., Picker M.J. Sex differences in (-)-pentazocine antinociception: comparison to morphine and spiradoline in four rat strains using a thermal nociceptive assay. Behav. Pharmacol. 2003, 14:77-85.
135. Terner J.M., Lomas L.M., Smith E.S., Barrett A.C., Picker M.J. Pharmacogenetic analysis of sex differences in opioid antinociception in rats. Pain 2003, 106:381-391.
136. Terner J.M., Lomas L.M., Picker M.J. Influence of estrus cycle and gonadal hormone depletion on nociception and opioid antinociception in female rats of four strains. J. Pain 2005, 6:372-383.
137. Terner J.M., Barrett A.C., Lomas L.M., Negus S.S., Picker M.J. Influence of low doses of naltrexone on morphine antinociception and morphine tolerance in male and female rats of four strains. Pain 2006, 122:90-101.
138. Thornton S.R., Wang A.F., Smith F.L. Characterization of neonatal rat morphine tolerance and dependence. Eur. J. Pharmacol. 1997, 340:161-167.
139. Turcotte J.C., Blaustein J.D. Projections of the estrogen receptor-immunoreactive ventrolateral hypothalamus to other estrogen receptor-immunoreactive sites in female guinea pig brain. Neuroendocrinology 1999, 69:63-76.
140. Unruh A.M. Gender variations in clinical pain experience. Pain 1996, 65:123-167.
141. Unruh A.M., Ritchie J., Merskey H. Does gender affect appraisal of pain and pain coping strategies?. Clin. J. Pain 1999, 15:31-40.
142. Wagner C.K., Morrell J.I. Distribution of steroid hormone regulation of aramatase mRNA expression in the forebrain of adult male and female rats: a cellular-level analysis using in situ hybridization. J. Comp. Neurol. 1996, 370:71-84.
143. Wang X., Traub R.J., Murphy A.Z. Persistent pain model reveals sex difference in morphine potency. Am. J. Physiol., Regul. Integr. Comp. Physiol. 2006, 291:R300-R306.
144. Yates P., Dewar A., Edwards H., Fentiman B., Majman J., Nash R., Richardson V., Fraser J. The prevalence and perception of pain amongst hospital in-patients. J. Clin. Nurs. 1998, 7:521-530.
145. Zacny J.P. Gender differences in opioid analgesia in human volunteers: cold pressor and mechanical pain. NIDA Res. Monog. 2002, 182:22-23.