Sex differences in antinociceptive tolerance to delta-9-tetrahydrocannabinol in the rat

Drug and Alcohol Dependence

Volumn 143, Issue 1, 2014, Pages 22-28

  Wakley, Alexa A ^a   Wiley, Jenny L ^b   Craft, Rebecca M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b RTI INTERNATIONAL   (United States)

Author keywords

Antinociception; Cannabinoid; Estrous cycle; Locomotion; Pain; Sex differences

Indexed keywords

ALCOHOL; CANNABINOID; CREMOPHOR; DRONABINOL; ANALGESIC AGENT;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CATALEPSY; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG DEPENDENCE; DRUG POTENCY; DRUG TOLERANCE; ESTRUS; ESTRUS CYCLE; EXPERIMENTAL TEST; FEMALE; LATENT PERIOD; LOCOMOTION; MALE; NONHUMAN; PAIN; PAW PRESSURE TEST; PROESTRUS; RAT; SEDATION; SEX DIFFERENCE; TAIL WITHDRAWAL TEST; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; PAIN MEASUREMENT; SEXUAL DEVELOPMENT;

RATTUS; RODENTIA;

ANALGESICS; ANIMALS; CATALEPSY; DOSE-RESPONSE RELATIONSHIP, DRUG; DRONABINOL; DRUG TOLERANCE; ESTROUS CYCLE; FEMALE; LOCOMOTION; MALE; PAIN MEASUREMENT; RATS; SEX CHARACTERISTICS;

EID: 84922403461     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2014.07.029     Document Type: Article

References (46)

1. Barrett A.C., Cook C.D., Terner J.M., Craft R.M., Picker M.J. 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. Psychopharmacologia 2001, 158:154-164.
2. Bass C.E., Martin B.R. Time course for the induction and maintenance of tolerance to Delta(9)-tetrahydrocannabinol in mice. Drug Alcohol Depend. 2000, 60:113-119.
3. Beery A.K., Zucker I. Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 2011, 35:565-572.
4. Bradshaw H., Rimmerman N., Krey J., Walker J. Sex and hormonal cycle differences in rat brain levels of pain-related cannabimimetic lipid mediators. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291. R349-R358-R349-R358.
5. Breivogel C.S., Childers S.R., Deadwyler S.A., Hampson R.E., Vogt L.J., Sim-Selley L.J. Chronic delta9-tetrahydrocannabinol treatment produces a time-dependent loss of cannabinoid receptors and cannabinoid receptor-activated G proteins in rat brain. J. Neurochem. 1999, 73:2447-2459.
6. Breivogel C.S., Lambert J.M., Gerfin S., Huffman J.W., Razdan R.K. Sensitivity to delta9-tetrahydrocannabinol is selectively enhanced in beta-arrestin2 -/- mice. Behav. Pharmacol. 2008, 19:298-307.
7. Burston J.J., Wiley J.L., Craig A.A., Selley D.E., Sim-Selley L.J. Regional enhancement of cannabinoid CB1 receptor desensitization in female adolescent rats following repeated (9-tetrahydrocannabinol exposure. Br. J. Pharmacol. 2010, 161:103-112.
8. Carroll M.E., Lynch W.J., Roth M.E., Morgan A.D., Cosgrove K.P. Sex and estrogen influence drug abuse. Trends Pharmacol. Sci. 2004, 25:273-279.
9. Cha Y.M., Jones K.H., Kuhn C.M., Wilson W.A., Swartzwelder H.S. Sex differences in the effects of delta9-tetrahydrocannabinol on spatial learning in adolescent and adult rats. Behav. Pharmacol. 2007, 18:563-569.
10. Craft R., Leitl M. Gonadal hormone modulation of the behavioral effects of Delta(9)-tetrahydrocannabinol in male and female rats. Eur. J. Pharmacol. 2008, 578:37-42.
11. Craft R.M., Kandasamy R., Davis S.M. Sex differences in anti-allodynic, anti-hyperalgesic and anti-edema effects of ((9)-tetrahydrocannabinol in the rat. Pain 2013, 154:1709-1717.
12. Craft R.M., Wakley A.A., Laggart J.D. Sex differences in CB1 vs. CB2 receptor-selective antagonism of antinociception produced by delta-9-THC and CP55,490 in the rat. J. Pharmacol. Exp. Ther. 2012, 340:787-800.
13. Fattore L., Spano M.S., Altea S., Angius F., Fadda P., Fratta W. Cannabinoid self-administration in rats: sex differences and the influence of ovarian function. Br. J. Pharmacol. 2007, 152:795-804.
14. Feder H.H. Estrous cyclicity in mammals. Neuroendocrinology of Reproduction 1981, 279-348. Plenum Press, New York. N.T. Adler (Ed.).
15. Fillingim R.B., King C.D., Ribeiro-Dasilva M.C., Rahim-Williams B., Riley J.L. Sex, gender, and pain: a review of recent clinical and experimental findings. J. Pain 2009, 10:447-485.
16. Freeman M.E. The ovarian cycle of the rat. The Physiology of Reproduction 1988, 1893-1928. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
17. Haim S., Shakhar G., Rossene E., Taylor A.N., Ben-Eliyahu S. Serum levels of sex hormones and corticosterone throughout 4- and 5-day estrous cycles in Fischer 344 rats and their simulation in ovariectomized females. J. Endocrinol. Invest. 2003, 26:1013-1022.
18. Harte-Hargrove L.C., Dow-Edwards D.L. Withdrawal from THC during adolescence: sex differences in locomotor activity and anxiety. Behav. Brain Res. 2012, 231:48-59.
19. Ibrahim I.A.A.E.-H., Kurose H. β-arrestin-mediated signaling improves the efficacy of therapeutics. J. Pharmacol. Sci. 2012, 118:408-412.
20. Marusich J.A., Lefever T.W., Antonazzo K.R., Craft R.M., Wiley J.L. Evaluation of sex differences in cannabinoid dependence. Drug Alcohol Depend. 2014, 137:20-28.
21. Marusich J.A., Lefever T.W., Novak S.P., Blough B.E., Wiley J.L. Prediction and prevention of prescription drug abuse: role of preclinical assessment of substance abuse liability. Methods Rep. RTI Press 2013.
22. McKinney D.L., Cassidy M.P., Collier L.M., Martin B.R., Wiley J.L., Selley D.E., Sim-Selley L.J. Dose-related differences in the regional pattern of cannabinoid receptor adaptation and in vivo tolerance development to delta9-tetrahydrocannabinol. J. Pharmacol. Exp. Ther. 2008, 324:664-673.
23. Mendelson J.H., Mello N.K., Ellingboe J., Skupny A.S., Lex B.W., Griffin M. Marihuana smoking suppresses luteinizing hormone in women. J. Pharmacol. Exp. Ther. 1986, 237:862-866.
24. 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.
25. Narimatsu S., Watanabe K., Yamamoto I., Yoshimura H. Sex difference in the oxidative-metabolism of delta-9-tetrahydrocannabinol in the rat. Biochem. Pharmacol. 1991, 41:1187-1194.
26. National Research Council Guide for the Care and Use of Laboratory Animals 2011, The National Academies Press, Washington DC. Eighth Ed.
27. Nguyen P.T., Schmid C.L., Raehal K.M., Selley D.E., Bohn L.M., Sim-Selley L.J. β-arrestin2 regulates cannabinoid CB1 receptor signaling and adaptation in a central nervous system region-dependent manner. Biol. Psychiatry 2012, 71:714-724.
28. O'Connell M.E., Morrill G.A., Fujimoto G.I., Kostellow A.B. Factors affecting the response of the female rat reproductive system to cannabinoids. Toxicol. Appl. Pharmacol. 1987, 88:411-417.
29. Rodriguez De Fonseca F., Cebeira M., Ramos J., Martin M., Fernandez-Ruiz J. Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement. Life Sci. 1994, 54:159-170.
30. Romero E., Fernández B., Sagredo O., Gomez N., Urigüen L., Guaza C., de Miguel R., Ramos J., Viveros M. Antinociceptive, behavioural and neuroendocrine effects of CP 55,940 in young rats. Brain Res. Dev. Brain Res. 2002, 136:85-92.
31. Romero J., Berrendero F., Garcia-Gil L., Ramos J.A., Fernández-Ruiz J.J. Cannabinoid receptor and WIN-55,212-2-stimulated [35S]GTP gamma S binding and cannabinoid receptor mRNA levels in the basal ganglia and the cerebellum of adult male rats chronically exposed to delta 9-tetrahydrocannabinol. J. Mol. Neurosci. 1998, 11:109-119.
32. Romero J., Berrendero F., Manzanares J., Pérez A., Corchero J., Fuentes J.A., Fernández-Ruiz J.J., Ramos J.A. Time-course of the cannabinoid receptor down-regulation in the adult rat brain caused by repeated exposure to delta-9-tetrahydrocannabinol. Synapse 1998, 30:298-308.
33. Romero J., Garcia-Palomero E., Castro J.G., Garcia-Gil L., Ramos J.A., Fernández-Ruiz J.J. Effects of chronic exposure to delta-9-tetrahydrocannabinol on cannabinoid receptor binding and mRNA levels in several rat brain regions. Brain Res. Mol. Brain Res. 1997, 46:100-108.
34. Sandén C., Broselid S., Cornmark L., Andersson K., Daszkiewicz-Nilsson J., Mårtensson U.E.A., Olde B., Leeb-Lundberg L.M.F. G protein-coupled estrogen receptor 1/G protein-coupled receptor 30 localizes in the plasma membrane and traffics intracellularly on cytokeratin intermediate filaments. Mol. Pharmacol. 2011, 79:400-410.
35. Sim-Selley L.J., Martin B.R. Effect of chronic administration of R-(+)-[2,3-Dihydro-5-methyl-3-[(morpholinyl)methyl]pyrrolo[1,2,3-de]-1,4-benzoxazinyl]-(1-naphthalenyl)methanone mesylate (WIN55,212-2) or delta(9)-tetrahydrocannabinol on cannabinoid receptor adaptation in mice. J. Pharmacol. Exp. Ther. 2002, 303:36-44.
36. Smith C.G., Almirez R.G., Berenberg J., Asch R.H. Tolerance develops to the disruptive effects of delta 9-tetrahydrocannabinol on primate menstrual cycle. Science 1983, 219:1453-1455.
37. Tseng A., Craft R. Sex differences in antinociceptive and motoric effects of cannabinoids. Eur. J. Pharmacol. 2001, 430:41-47.
38. Tseng A., Harding J., Craft R. Pharmacokinetic factors in sex differences in Delta(9)-tetrahydrocannabinol-induced behavioral effects in rats. Behav. Brain Res. 2004, 154:77-83.
39. Unruh A.M. Gender variations in clinical pain experience. Pain 1996, 65:123-167.
40. 9-tetrahydrocannabinol in female vs. male rats. Behav. Brain Res. 2011, 216:200-206.
41. Whitlow C.T., Freedland C.S., Porrino L.J. Functional consequences of the repeated administration of Delta9-tetrahydrocannabinol in the rat. Drug Alcohol Depend. 2003, 71:169-177.
42. Wiley J. Sex-dependent effects of Delta(9)-tetrahydrocannabinol on locomotor activity in mice. Neurosci. Lett. 2003, 352:77-80.
43. Wiley J.L., Barrett R.L., Britt D.T., Balster R.L., Martin B.R. Discriminative stimulus effects of delta 9-tetrahydrocannabinol and delta 9-11-tetrahydrocannabinol in rats and rhesus monkeys. Neuropharmacology 1993, 32:359-365.
44. 9-tetrahydrocannabinol metabolism and in vivo pharmacology following acute and repeated dosing in adolescent rats. Neurosci. Lett. 2014, 576:51-55.
45. Wiley J.L., Evans R.L., Grainger D.B., Nicholson K.L. Locomotor activity changes in female adolescent and adult rats during repeated treatment with a cannabinoid or club drug. Pharmacol. Rep. 2011, 63:1085-1092.
46. Wiley J.L., O'connell M.M., Tokarz M.E., Wright M.J. Pharmacological effects of acute and repeated administration of Delta(9)-tetrahydrocannabinol in adolescent and adult rats. J. Pharmacol. Exp. Ther. 2007, 320:1097-1105.