The impact of gonadal hormones on cannabinoid dependence

Experimental and Clinical Psychopharmacology

Volumn 23, Issue 4, 2015, Pages 206-216

  Marusich, Julie A ^a   Craft, Rebecca M ^b   Lefever, Timothy W ^a   Wiley, Jenny L ^a  

^a RTI INTERNATIONAL   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Dependence; Estradiol; Rimonabant; Testosterone; 9 tetrahydrocannabinol

Indexed keywords

DRONABINOL; ESTRADIOL; PROGESTERONE; RIMONABANT; SEX HORMONE; TESTOSTERONE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CANNABIS ADDICTION; CONTROLLED STUDY; FEMALE; GONADECTOMY; HORMONE ACTION; HYPOTHERMIA; LOCOMOTION; MALE; MASTICATION; NONHUMAN; PATHOGENESIS; RAT; SEX DIFFERENCE; SNIFFING; WITHDRAWAL SYNDROME; ANIMAL; BODY WEIGHT; CASTRATION; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; DRUG TOLERANCE; ESTRUS CYCLE; HORMONE SUBSTITUTION; MARIJUANA ABUSE; MOTOR ACTIVITY; PAIN MEASUREMENT; PROCEDURES; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT; STARTLE REFLEX; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTOR;

ANIMALS; BODY WEIGHT; CASTRATION; DISEASE MODELS, ANIMAL; DRONABINOL; DRUG TOLERANCE; ESTROUS CYCLE; FEMALE; GONADAL HORMONES; HORMONE REPLACEMENT THERAPY; MALE; MARIJUANA ABUSE; MOTOR ACTIVITY; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; REFLEX, STARTLE; SEX CHARACTERISTICS; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTORS;

EID: 84938585767     PISSN: 10641297     EISSN: 19362293     Source Type: Journal    
DOI: 10.1037/pha0000027     Document Type: Article

References (38)

1. Aceto, M.D., Scates, S.M., Lowe, J.A., & Martin, B.R. (1996). Dependence on delta 9-tetrahydrocannabinol: Studies on precipitated and abrupt withdrawal. The Journal of Pharmacology and Experimental Therapeutics, 278, 1290-1295.
2. Barrett, A.C., Cook, C.D., Terner, J.M., Craft, R.M., & Picker, M.J. (2001). 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, 158, 154-164. http://dx.doi.org/10.1007/s002130100821.
3. Bass, C.E., & Martin, B.R. (2000). Time course for the induction and maintenance of tolerance to Delta(9)-tetrahydrocannabinol in mice. Drug and Alcohol Dependence, 60, 113-119. http://dx.doi.org/10.1016/S0376-8716(99)00150-7.
4. Bowen, S.E., Wiley, J.L., Evans, E.B., Tokarz, M.E., & Balster, R.L. (1996). Functional observational battery comparing effects of ethanol, 1,1,1-trichloroethane, ether, and flurothyl. Neurotoxicology and Teratology, 18, 577-585. http://dx.doi.org/10.1016/0892-0362(96)00064-5.
5. Burston, J.J., Wiley, J.L., Craig, A.A., Selley, D.E., & Sim-Selley, L.J. (2010). Regional enhancement of cannabinoid CB1 receptor desensitization in female adolescent rats following repeated Δ-tetrahydrocannabinol exposure. British Journal of Pharmacology, 161, 103-112. http://dx.doi.org/10.1111/j.1476-5381.2010.00870.x.
6. Compton, D.R., Dewey, W.L., & Martin, B.R. (1990). Cannabis dependence and tolerance production. Advances in Alcohol & Substance Abuse, 9, 129-147. http://dx.doi.org/10.1300/J251v09n01_08.
7. Cook, S.A., Lowe, J.A., & Martin, B.R. (1998). CB1 receptor antagonist precipitates withdrawal in mice exposed to Delta9-tetrahydrocannabinol. The Journal of Pharmacology and Experimental Therapeutics, 285, 1150-1156.
8. Cooper, Z.D., & Haney, M. (2014). Investigation of sex-dependent effects of cannabis in daily cannabis smokers. Drug and Alcohol Dependence, 136, 85-91. http://dx.doi.org/10.1016/j.drugalcdep.2013.12.013.
9. Craft, R.M., & Leitl, M.D. (2008). Gonadal hormone modulation of the behavioral effects of Delta9-tetrahydrocannabinol in male and female rats. European Journal of Pharmacology, 578, 37-42. http://dx.doi.org/10.1016/j.ejphar.2007.09.004.
10. Craft, R.M., Wakley, A.A., Tsutsui, K.T., & Laggart, J.D. (2012). Sex differences in cannabinoid 1 vs. cannabinoid 2 receptor-selective antagonism of antinociception produced by delta9-tetrahydrocannabinol and CP55,940 in the rat. The Journal of Pharmacology and Experimental Therapeutics, 340, 787-800. http://dx.doi.org/10.1124/jpet.111.188540.
11. Daniel, J.M., Winsauer, P.J., Brauner, I.N., & Moerschbaecher, J.M. (2002). Estrogen improves response accuracy and attenuates the disruptive effects of delta9-THC in ovariectomized rats responding under a multiple schedule of repeated acquisition and performance. Behavioral Neuroscience, 116, 989-998. http://dx.doi.org/10.1037/0735-7044.116.6.989.
12. Fattore, L., Spano, M.S., Altea, S., Fadda, P., & Fratta, W. (2010). Drugand cue-induced reinstatement of cannabinoid-seeking behaviour in male and female rats: Influence of ovarian hormones. British Journal of Pharmacology, 160, 724-735. http://dx.doi.org/10.1111/j.1476-5381.2010.00734.x.
13. Feder, H.H. (1981). Estrous cyclicity in mammals. In N. T. Adler (Ed.), Neuroendocrinology of reproduction (pp. 279-348). New York, NY: Plenum Press.
14. Freeman, M.E. (1988). The ovarian cycle of the rat. In E. Knobil & J. Neill (Eds.), The physiology of reproduction (pp. 1893-1928). New York, NY: Raven Press.
15. Harte-Hargrove, L.C., & Dow-Edwards, D.L. (2012). Withdrawal from THC during adolescence: Sex differences in locomotor activity and anxiety. Behavioural Brain Research, 231, 48-59. http://dx.doi.org/10.1016/j.bbr.2012.02.048.
16. Hasin, D.S., Keyes, K.M., Alderson, D., Wang, S., Aharonovich, E., & Grant, B.F. (2008). Cannabis withdrawal in the United States: Results from NESARC. Journal of Clinical Psychiatry, 69, 1354-1363. http://dx.doi.org/10.4088/JCP.v69n0902.
17. Huang, P., Liu-Chen, L.Y., & Kirby, L.G. (2010). Anxiety-like effects of SR 141716-precipitated delta9-tetrahydrocannabinol withdrawal in mice in the elevated plus-maze. Neuroscience Letters, 475, 165-168. http://dx.doi.org/10.1016/j.neulet.2010.03.071.
18. Kalbasi Anaraki, D., Sianati, S., Sadeghi, M., Ghasemi, M., Paydar, M.J., Ejtemaei Mehr, S., & Dehpour, A.R. (2008). Modulation by female sex hormones of the cannabinoid-induced catalepsy and analgesia in ovariectomized mice. European Journal of Pharmacology, 586, 189-196. http://dx.doi.org/10.1016/j.ejphar.2008.02.055.
19. Kellert, B.A., Nguyen, M.C., Nguyen, C., Nguyen, Q.H., & Wagner, E.J. (2009). Estrogen rapidly attenuates cannabinoid-induced changes in energy homeostasis. European Journal of Pharmacology, 622, 15-24. http://dx.doi.org/10.1016/j.ejphar.2009.09.001.
20. Khan, S.S., Secades-Villa, R., Okuda, M., Wang, S., Pérez-Fuentes, G., Kerridge, B.T., & Blanco, C. (2013). Gender differences in cannabis use disorders: Results from the National Epidemiologic Survey of Alcohol and Related Conditions. Drug and Alcohol Dependence, 130, 101-108. http://dx.doi.org/10.1016/j.drugalcdep.2012.10.015.
21. Levin, K.H., Copersino, M.L., Heishman, S.J., Liu, F., Kelly, D.L., Boggs, D.L., & Gorelick, D.A. (2010). Cannabis withdrawal symptoms in non-treatment-seeking adult cannabis smokers. Drug and Alcohol Dependence, 111, 120-127. http://dx.doi.org/10.1016/j.drugalcdep.2010.04.010.
22. Lichtman, A.H., Fisher, J., & Martin, B.R. (2001). Precipitated cannabinoid withdrawal is reversed by Delta(9)-tetrahydrocannabinol or clonidine. Pharmacology, Biochemistry, and Behavior, 69, 181-188. http://dx.doi.org/10.1016/S0091-3057(01)00514-7.
23. Martin, B.R., Compton, D.R., Thomas, B.F., Prescott, W.R., Little, P.J., Razdan, R.K.,.Ward, S.J. (1991). Behavioral, biochemical, and molecular modeling evaluations of cannabinoid analogs. Pharmacology, Biochemistry and Behavior, 40, 471-478. http://dx.doi.org/10.1016/0091-3057(91)90349-7.
24. Marusich, J.A., Lefever, T.W., Antonazzo, K.R., Craft, R.M., & Wiley, J.L. (2014). Evaluation of sex differences in cannabinoid dependence. Drug and Alcohol Dependence, 137, 20-28. http://dx.doi.org/10.1016/j.drugalcdep.2014.01.019.
25. National Research Council. (2011). Guidelines for the care and use of mammals in neuroscience and behavioral research. Washington, DC: National Academies Press.
26. Rodriguez de Fonseca, F., Cebeira, M., Ramos, J.A., Martín, M., & Fernández-Ruiz, J.J. (1994). Cannabinoid receptors in rat brain areas: Sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement. Life Sciences, 54, 159-170.
27. 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.
28. Substance Abuse and Mental Health Services Administration. (2014). Results from the 2013 National Survey on Drug Use and Health: Summary of National Findings, NSDUH Series H-48, HHS Publication No. (SMA) 14-4863. Rockville, MD: Substance Abuse and Mental Health Services Administration.
29. Tseng, A.H., & Craft, R.M. (2001). Sex differences in antinociceptive and motoric effects of cannabinoids. European Journal of Pharmacology, 430, 41-47. http://dx.doi.org/10.1016/S0014-2999(01)01267-5.
30. Tseng, A.H., Harding, J.W., & Craft, R.M. (2004). Pharmacokinetic factors in sex differences in Delta 9-tetrahydrocannabinol-induced behavioral effects in rats. Behavioural Brain Research, 154, 77-83. http://dx.doi.org/10.1016/j.bbr.2004.01.029.
31. Tsou, K., Patrick, S.L., & Walker, J.M. (1995). Physical withdrawal in rats tolerant to delta 9-tetrahydrocannabinol precipitated by a cannabinoid receptor antagonist. European Journal of Pharmacology, 280, R13-R15. http://dx.doi.org/10.1016/0014-2999(95)00360-W.
32. Wakley, A.A., McBride, A.A., Vaughn, L.K., & Craft, R.M. (2014). Cyclic ovarian hormone modulation of supraspinal Δ9-tetrahydrocannabinol-induced antinociception and cannabinoid receptor binding in the female rat. Pharmacology, Biochemistry, and Behavior, 124, 269-277. http://dx.doi.org/10.1016/j.pbb.2014.06.007.
33. Wakley, A.A., Wiley, J.L., & Craft, R.M. (2014). Sex differences in antinociceptive tolerance to delta-9-tetrahydrocannabinol in the rat. Drug and Alcohol Dependence, 143, 22-28. http://dx.doi.org/10.1016/j.drugalcdep.2014.07.029.
34. Wakley, A.A., Wiley, J.L., & Craft, R.M. (2015). Gonadal hormones do not alter the development of antinociceptive tolerance to delta-9-tetrahydrocannabinol in adult rats. Pharmacology, Biochemistry, and Behavior, 133, 111-121. http://dx.doi.org/10.1016/j.pbb.2015.03.021
35. (9)- tetrahydrocannabinol metabolism and in vivo pharmacology following acute and repeated dosing in adolescent rats. Neuroscience Letters, 576, 51-55. http://dx.doi.org/10.1016/j.neulet.2014.05.057.
36. Wiley, J.L., O'connell, M.M., Tokarz, M.E., & Wright, M.J., Jr. (2007). Pharmacological effects of acute and repeated administration of Delta(9)-tetrahydrocannabinol in adolescent and adult rats. The Journal of Pharmacology and Experimental Therapeutics, 320, 1097-1105. http://dx.doi.org/10.1124/jpet.106.108126.
37. Winsauer, P.J., Daniel, J.M., Filipeanu, C.M., Leonard, S.T., Hulst, J.L., Rodgers, S.P.,.Sutton, J.L. (2011). Long-term behavioral and pharmacodynamic effects of delta-9-tetrahydrocannabinol in female rats depend on ovarian hormone status. Addiction Biology, 16, 64-81. http://dx.doi.org/10.1111/j.1369-1600.2010.00227.x.
38. Winsauer, P.J., & Sutton, J.L. (2014). Chronic ad ministration during early adulthood does not alter the hormonally-dependent disruptive effects of delta-9-tetrahydrocannabinol (Δ9-THC) on complex behavior in female rats. Pharmacology, Biochemistry and Behavior, 117, 118-127. http://dx.doi.org/10.1016/j.pbb.2013.12.014.