PAG mu opioid receptor activation underlies sex differences in morphine antinociception

Akil, 1976, Antagonism of stimulation-produced analgesia by naloxone, a narcotic antagonist, Science, 191, 961, 10.1126/science.1251210 Baamonde, 1989, Sex-related differences in the effects of morphine and stress on visceral pain, Neuropharmacology, 28, 967, 10.1016/0028-3908(89)90197-4 Banerjee, 1983, Ovarian steroids and modulation of morphine-induced analgesia and catalepsy in female rats, Eur J Pharmacol, 96, 291, 10.1016/0014-2999(83)90319-9 Barrett, 2002, Sex and rat strain determine sensitivity to kappa opioid-induced antinociception, Psychopharmacology, 160, 170, 10.1007/s00213-001-0949-2 Berglund, 1988, Alterations in brain opiate receptor mechanisms on proestrous afternoon, Neuroendocrinology, 48, 394, 10.1159/000125040 Boyer, 1998, Microinjection of morphine into the rostral ventromedial medulla produces greater antinociception in male compared to female rats, Brain Res, 796, 315, 10.1016/S0006-8993(98)00353-9 Candido, 1992, Effect of adrenal and sex hormones on opioid analgesia and opioid receptor regulation, Pharmacol Biochem Behav, 42, 685, 10.1016/0091-3057(92)90015-8 Cicero, 2000, Gender differences in the reinforcing properties of morphine, Pharmacol Biochem Behav, 65, 91, 10.1016/S0091-3057(99)00174-4 Cicero, 1996, Gender-related differences in the antinociceptive properties of morphine, J Pharmacol Exp Ther, 279, 767 Cicero, 1997, Sex-related differences in morphine's antinociceptive activity: relationship to serum and brain morphine concentrations, J Pharmacol Exp Ther, 282, 939 Cook, 2000, Sex-related differences in the antinociceptive effects of opioids: importance of rat genotype, nociceptive stimulus intensity, and efficacy at the rat mu opioid receptor, Psychopharmacology, 150, 430, 10.1007/s002130000453 Craft, 2003, Sex differences in opioid analgesia: “From mouse to man”, Clin J Pain, 19, 175, 10.1097/00002508-200305000-00005 Craft, 2006, Potentiation of morphine antinociception by pentobarbital in female vs. male rats, Pain, 121, 115, 10.1016/j.pain.2005.12.009 Craft, 1996, Sex differences in discriminative stimulus effects of morphine in the rat, Behav Pharm, 7, 764 Craft, 2004, Sex differences in pain and analgesia: the role of gonadal hormones, Eur J Pain, 8, 397, 10.1016/j.ejpain.2004.01.003 Craft, 2001, Receptor-selective antagonism of opioid antinociception in female vs. male rats, Behav Pharm, 12, 591, 10.1097/00008877-200112000-00003 Dickenson, 1979, Role of the nucleus raphe magnus in opiate analgesia as studied by the microinjection technique in the rat, Brain Res, 170, 95, 10.1016/0006-8993(79)90943-0 Freeman, 1988, The ovarian cycle in the rat, 1893 Gear, 1996, Gender difference in analgesic response to the kappa-opioid pentazocine, Neurosci Lett, 205, 207, 10.1016/0304-3940(96)12402-2 Gear, 1996, Kappa-opioids produce significantly greater analgesia in women than in men, Nat Med, 2, 1248, 10.1038/nm1196-1248 Gear, 1999, The kappa opioid nalbuphine produces gender- and dose-dependent analgesia and antianalgesia in patients with postoperative pain, Pain, 83, 339, 10.1016/S0304-3959(99)00119-0 Hammer, 1990, Mu-opiate receptor binding in the medial preoptic area is cyclical and sexually dimorphic, Brain Res, 515, 187, 10.1016/0006-8993(90)90595-3 Hosobuchi, 1977, Pain relief by electrical stimulation of the central gray matter in humans and its reversal by naloxone, Science, 197, 183, 10.1126/science.301658 Jacquet, 1974, Paradoxical effects after microinjection of morphine in the periaqueductal gray matter in the rat, Science, 185, 1055, 10.1126/science.185.4156.1055 Jensen, 1986, 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 the microinjection technique, Brain Res, 372, 301, 10.1016/0006-8993(86)91138-8 Jensen, 1986, Examination of spinal monoamine receptors through which brainstem opiate-sensitive systems act in the rat, Brain Res, 363, 114, 10.1016/0006-8993(86)90663-3 Kanarek, 2001, Chronic sucrose intake augments antinociception induced by injections of mu but not kappa opioid receptor agonists into the periaqueductal gray matter in male and female rats, Brain Res, 920, 97, 10.1016/S0006-8993(01)03039-6 Kepler, 1989, Roles of gender, gonadectomy and estrous phase in the analgesic effects of intracerebroventricular morphine in rats, Pharmacol Biochem Behav, 34, 119, 10.1016/0091-3057(89)90363-8 Kepler, 1991, Gender effects and central opioid analgesia, Pain, 45, 87, 10.1016/0304-3959(91)90168-W Krzanowska, 2000, Sex differences in locomotor activity following beta-endorphin in the ventrolateral periaqueductal gray, Physiol Behav, 68, 595, 10.1016/S0031-9384(99)00242-5 Krzanowska, 1999, Morphine antinociception elicited from the ventrolateral periaqueductal gray is sensitive to sex and gonadectomy differences in rats, Brain Res, 821, 224, 10.1016/S0006-8993(98)01364-X Krzanowska, 2002, Reversal of sex differences in morphine analgesia elicited from the ventrolateral periaqueductal gray in rats by neonatal hormone manipulations, Brain Res, 929, 1, 10.1016/S0006-8993(01)03350-9 Lane, 2005, Evidence for an intrinsic mechanism of antinociceptive tolerance within the ventrolateral periaqueductal gray of rats, Neuroscience, 135, 227, 10.1016/j.neuroscience.2005.06.014 Lewis, 1977, Evaluation of the periaqueductal central gray (PAG) as a morphine-specific locus of action and examination of morphine-induced and stimulation-produced analgesia at coincident PAG loci, Brain Res, 124, 283, 10.1016/0006-8993(77)90886-1 Loyd, 2006, 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, 496, 723, 10.1002/cne.20962 Maggi, 1991, Modulation of the binding characteristics of hypothalamic mu opioid receptors in rats by gonadal steroids, J Steroid Biochem Molec Biol, 40, 113, 10.1016/0960-0760(91)90174-4 Manning, 1998, Morphine analgesia in the formalin test: reversal by microinjection of quaternary naloxone into the posterior hypothalamic area or periaqueductal gray, Behav Brain Res, 92, 97, 10.1016/S0166-4328(97)00130-7 Mogil, 2000, Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype, Neurosci Biobehav Rev, 24, 375, 10.1016/S0149-7634(00)00015-4 Morgan, 1998, Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray, Brain Res, 804, 159, 10.1016/S0006-8993(98)00669-6 Negus, 1999, Opioid antinociception in ovariectomized monkeys: comparison with antinociception in males and effects of estradiol replacement, J Pharmacol Exp Ther, 290, 1132 Oliveras, 1974, Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat, Exp Brain Res, 20, 32, 10.1007/BF00239016 Pavlovic, 1996, Opioid antagonists in the periaqueductal gray inhibit morphine and beta-endorphin analgesia elicited from the amygdala of rats, Brain Res, 741, 13, 10.1016/S0006-8993(96)00880-3 Paxinos, 1986, vol. 2 Randich, 1992, Intravenous morphine-induced activation of vagal afferents: peripheral, spinal, and CNS substrates mediating inhibition of spinal nociception and cardiovascular responses, J Neurophys, 68, 1027, 10.1152/jn.1992.68.4.1027 Ryan, 1988, The estrous cycle and estrogen modulate stress-induced analgesia, Behav Neurosci, 102, 371, 10.1037/0735-7044.102.3.371 Sandner, 1987, Mapping of jumping, rearing, squealing and switch-off behaviors elicited by periaqueductal gray stimulation in the rat, Physiol Behav, 39, 333, 10.1016/0031-9384(87)90231-9 Shane R, Bernal SY, Rozengurtel S, Bodnar RJ. Estrus phase differences in female rats in morphine antinociception elicited from the ventrolateral periaqueductal gray. Int J Neurosci; in press. Smith, 1992, Opioid receptors mediating antinociception from beta-endorphin and morphine in the periaqueductal gray, Neuropharmacology, 31, 1137, 10.1016/0028-3908(92)90010-M Stewart, 1999, The effects of gonadal hormones on the development and expression of the stimulant effects of morphine in male and female rats, Behav Brain Res, 102, 89, 10.1016/S0166-4328(99)00002-9 Stoffel, 2003, Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats, Pain, 103, 285, 10.1016/s0304-3959(02)00457-8 Terner, 2005, Influence of estrous cycle and gonadal hormone depletion on nociception and opioid antinociception in female rats of four strains, J Pain, 6, 372, 10.1016/j.jpain.2005.01.354 Terner, 2003, Pharmacogenetic analysis of sex differences in opioid antinociception in rats, Pain, 106, 381, 10.1016/j.pain.2003.08.008 Tershner, 2000, Brainstem pain modulating circuitry is sexually dimorphic with respect to mu and kappa opioid receptor function, Pain, 85, 153, 10.1016/S0304-3959(99)00257-2 Tseng, 1990, Different mechanisms mediate beta-endorphin- and morphine-induced inhibition of the tail-flick response in rats, J Pharmacol Exp Ther, 252, 546 Wang X, Traub RJ, Murphy AZ. Sexually dimorphic mu opioid receptor expression in the midbrain periaqueductal gray may contribute to the observed sex differences in intra-periaqueductal gray morphine in a persistent pain model. Neuroscience; submitted for publication. Yaksh, 1976, Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observation of differential effects within the periaqueductal gray, Brain Res, 114, 83, 10.1016/0006-8993(76)91009-X Zambotti, 1982, Periaqueductal gray matter involvement in the muscimol-induced decrease of morphine antinociception, Naunyn-Sch Arch Pharmacol, 318, 368, 10.1007/BF00501180