Neonatal and Adult Gonadal Hormone Manipulations Enhance Morphine Analgesia Elicited from the Ventrolateral Periaqueductal Gray in Female Rats

REFERENCES

• Ali, B., Sharif, S., & Elkadi, A. (1995). Sex differences and the effect of gonadectomy on morphine-induced antinociception and dependence in rats and mice. Clinical and Experimental Pharmacology and Physiology, 22, 342–344.
   PubMedGoogle Scholar
• Baamonde, A. I., Hidalgo, A., & Andres-Trelles, F. (1989). Sex-related differences in the effects of morphine and stress on visceral pain. Neuropharmacology, 28, 967–970.
   PubMed Web of Science ®Google Scholar
• Badillo-Martinez, D., Kirchgessner, A. L., Butler, P. D., & Bodnar, R. J. (1984). Monosodium glutamate and morphine analgesia: Test-specific effects. Neuropharmacology, 23, 1141–1149.
   Google Scholar
• Banerjee, T., Chatterjee, T., & Ghosh, J. J. (1983). Ovarian steroids and modulation of morphine-induced analgesia and catalepsy in female rats. European Journal of Pharmacology, 96, 291–294.
   Google Scholar
• Bartok, R. E., & Craft, R. M. (1997). Sex differences in opioid antinociception. Journal of Pharmacology and Experimental Therapeutics, 282, 769–778.
   PubMed Web of Science ®Google Scholar
• Bernal, S. A., Morgan, M. M., & Craft, R. M. (2007). PAG mu opioid receptor activation underlies sex differences in morphine antinociception. Behavioral Brain Research, 177, 126–133.
   Google Scholar
• Borzan, J., & Fuchs, P. N. (2006). Organizational and activational effects of testosterone on carrageenan-induced inflammatory pain and morphine analgesia. Neuroscience, 143, 885–893.
   Google Scholar
• Boyer, J. S., Morgan, M. M., & Craft, R. M. (1998). Microinjection of morphine into the rostral-ventromedial medulla produces greater antinociception in male compared to female rats. Brain Research, 796, 315–318.
   PubMed Web of Science ®Google Scholar
• Candido, J., Lufty, K., Billings, B., Sierra, V., Duttaroy, A., & Inturrisi, C. E. (1992). Effect of adrenal and sex hormones on opioid analgesia and opioid receptor regulation. Pharmacology Biochemistry and Behavior, 42, 685–692.
   Google Scholar
• Cataldo, G., Bernal, S. Y., Markowitz, A., Ogawa, S., Ragnauth, A., Pfaff, D. W., (2005). Organizational manipulation of gonadal hormones and systemic morphine analgesia in female rats: Effects of adult ovariectomy and estradiol replacement. Brain Research, 1059, 13–19.
   Google Scholar
• Cicero, T. J., Nock, B., & Meyer, E. R. (1996). Gender-related differences in the antinociceptive properties of morphine. Journal of Pharmacology and Experimental Therapeutics, 279, 767–773.
   PubMed Web of Science ®Google Scholar
• Cicero, T. J., Nock, B., & Meyer, E. R. (1997). Sex-related differences in morphine's antinociceptive activity: Relationship to serum and brain morphine concentrations. Journal of Pharmacology and Experimental Therapeutics, 282, 939–944.
   PubMed Web of Science ®Google Scholar
• Cicero, T. J., Nock, B., O’Connor, L., & Meyer, E. R. (2002). Role of steroids in sex differences in morphine-induced analgesia: Activational and organizational effects. Journal of Pharmacology and Experimental Therapeutics, 300, 695–701.
   PubMed Web of Science ®Google Scholar
• Commons, K. G., Aicher, S. A., Kow, L. M., & Pfaff, D. W. (2000). Presynaptic and postsynaptic relations of mu-opioid receptors to gamma-aminobutyric acid-immunoreactive and medullary-projecting periaqueductal gray neurons. Journal of Comparative Neurology, 419, 532–542.
   Google Scholar
• Cook, C. D., Barrett, A. C., Roach, E. L., Bowman, J. R., & Picker, M. J. (2000). 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, 430–442.
   Google Scholar
• Craft, R. M., & Bernal, S. A. (2001). Sex differences in opioid antinociception: Kappa and mixed action agonists. Drug Alcohol Dependence, 63, 215–228.
   PubMedGoogle Scholar
• Crowley, W. R., Jacobs, R., Volpe, J., Rodriguez-Sierra, J. F., & Komisaruk, B. R. (1976). Analgesic effect of vaginal stimulation in rats: Modulation by graded stimulus intensity and hormones. Physiology and Behavior, 16, 483–488.
   PubMed Web of Science ®Google Scholar
• Hoffman, G. E., Dohanics, J., Watson, R. E., & Wiegand, S. J. (1996). The hypothalamic ventromedial nucleus sends a met-enkephalin projection to the preoptic area's periventricular zone in the female rat. Molecular Brain Research, 36, 201–210.
   Google Scholar
• Islam, A. K., Cooper, M. L., & Bodnar, R. J. (1993). Interactions among aging, gender and gonadectomy effects upon morphine antinociception in rats. Physiology and Behavior, 54, 45–53.
   Google Scholar
• Kasson, B. G., & George, R. (1984). Endocrine influences on the action of morphine: IV. Effects of sex and strain. Life Sciences, 34, 1627–1634.
   Google Scholar
• Kavaliers, M., & Innes, D. G. L. (1987). Sex and day/night differences in opiate-induced responses of insular wild deer mice, Peromyscus maniculatis triangularis. Pharmacology Biochemistry and Behavior, 27, 477–482.
   PubMed Web of Science ®Google Scholar
• Kepler, K. L., Kest, B., Kiefel, J. M., Cooper, M. L., & Bodnar, R. J. (1989). Roles of gender, gonadectomy and estrus phase in the analgesic effects of intracrebroventricular morphine in rats. Pharmacology Biochemistry and Behavior, 34, 119–127.
   PubMed Web of Science ®Google Scholar
• Kepler, K. L., Standifer, K. M., Paul, D., Pasternak, G. W., Kest, B., & Bodnar, R. J. (1991). Differential gender effects upon central opioid analgesia. Pain, 45, 87–95.
   Google Scholar
• Kow, L. M., Commons, K. G., Ogawa, S., & Pfaff, D. W. (2002). Potentiation of the excitatory action of NMDA in ventrolateral periaqueductal gray by the mu-opioid receptor agonist, DAMGO. Brain Research, 935, 87–102.
   Google Scholar
• Krzanowska, E. K., & Bodnar, R. J. (1999). Morphine antinociception elicited from the ventrolateral periaqueductal gray is sensitive to sex and gonadectomy differences in rats. Brain Research, 821, 224–230.
   PubMed Web of Science ®Google Scholar
• Krzanowska, E. K., & Bodnar, R. J. (2000). Analysis of sex and gonadectomy differences in beta-endorphin antinociception elicited from the ventrolateral periaqueductal gray in rats. European Journal of Pharmacology, 392, 157–161.
   Google Scholar
• Krzanowska, E. K., Ogawa, S., Pfaff, D. W., & Bodnar, R. J. (2002). Reversal of sex differences in morphine analgesia elicited from the ventrolateral periaqueductal gray in rats by neonatal hormone manipulations. Brain Research, 929, 1–9.
   PubMed Web of Science ®Google Scholar
• LaCroix-Fralish, M. L., Tawfik, V. L., & DeLeo, J. A. (2005). The organizational and activational effects of sex hormones on tactile and thermal hypersensitivity following lumbar nerve root injury in male and female rats. Pain, 114, 71–80.
   Google Scholar
• Loyd, D. R., & Murphy, A. Z. (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. Journal of Comparative Neurology, 496, 723–738.
   Google Scholar
• Negus, S. S., & Mello, N. K. (1999). Opioid antinociception in ovariectomized monkeys: Comparison with antinociception in males and effects of estradiol replacement. Journal of Pharmacology and Experimental Therapeutics, 290, 1132–1140.
   PubMed Web of Science ®Google Scholar
• Paxinos, G., & Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates, 4th ed. Knoxville, TN: Neuroscience Associates.
   Google Scholar
• Priest, C. A., Eckersell, C. B., & Micevych, P. E. (1995). Estrogen regulates preproenkephalin-A mRNA levels in the rat ventromedial nucleus: Temporal and cellular aspects. Molecular Brain Research, 28, 251–262.
   Google Scholar
• Romano, G. J., Harlan, R. E., Shivers, B. D., Howells, R. D., & Pfaff, D. W. (1988). Estrogen increases proenkephalin messenger ribonucleic acid levels in the ventromedial hypothalamus of the rat. Molecular Endocrinology, 2, 1320–1328.
   Google Scholar
• Romano, G. J., Mobbs, C. V., Howells, R. D., & Pfaff, D. W. (1989). Estrogen regulation of proenkephalin gene expression in the ventromedial hypothalamus of the rat: Temporal qualities and synergism with progesterone. Molecular Brain Research, 5, 51–58.
   PubMedGoogle Scholar
• Romano, G. J., Mobbs, C. V., Lauber, A., Howells, R. D., & Pfaff, D. W. (1990). 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 Research, 536, 63–68.
   PubMed Web of Science ®Google Scholar
• Shane, R., Bernal, S. Y., Rozengurtel, S., & Bodnar, R. J. (2007). Estrus phase differences in female rats in morphine antinociception elicited from the ventrolateral periaqueductal gray. International Journal of Neuroscience, 117, 811–822.
   Web of Science ®Google Scholar
• Stoffel, E. C., Ulibarri, C. M., & Craft, R. M. (2003). Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain, 103, 285–302.
   PubMed Web of Science ®Google Scholar
• Terner, J. M., Barrett, A. C., Cook, C. D., & Picker, M. J. (2003). Sex differences in (-)-pentazocine antinociception: Comparison to morphine and spiradoline in four rat strains using a thermal nociceptive assay. Behavioral Pharmacology, 14, 77–85.
   Google Scholar
• Terner, J. M., Barrett, A. C., Grossell, E., & Picker, M. J. (2002). Influence of gonadectomy on the antinociceptive effects of opioids in male and female rats. Psychopharmacology, 163, 183–193.
   Google Scholar
• Turcotte, J. C., & Blaustein, J. D. (1999). Projections of the estrogen receptor-immunoreactive ventrolateral hypothalamus to other estrogen receptor-immunoreactive sites in female guinea pig brain. Neuroendocrinology, 69, 63–76.
   Google Scholar