Naltrexone does not attenuate the effects of intravenous Δ9-tetrahydrocannabinol in healthy humans

International Journal of Neuropsychopharmacology

Volumn 15, Issue 9, 2012, Pages 1251-1264

  Ranganathan, Mohini ^a,b,c   Carbuto, Michelle ^a,b,c   Braley, Gabriel ^a,b   Elander, Jaqueline ^a,b   Perry, Edward ^a,b   Pittman, Brian ^a,c   Radhakrishnan, Rajiv ^a,b   Sewell, Richard A ^a,b   D'Souza, Deepak C ^a,b,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c Yale Medical Group   (United States)

Author keywords

opioid receptors; Cannabinoids; CB1 receptors; naltrexone; opioids; tetrahydrocannabinol; THC

Indexed keywords

DRONABINOL; NALTREXONE; PLACEBO;

ADULT; ANXIETY; ARTICLE; BEHAVIOR; COGNITION; COGNITIVE DEFECT; DRUG ANTAGONISM; DRUG EFFECT; EUPHORIA; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PERCEPTION DISORDER; PREMEDICATION; PRIORITY JOURNAL; SIDE EFFECT;

ADOLESCENT; ADULT; ATTENTION; BEHAVIOR; COGNITION; COGNITION DISORDERS; DOUBLE-BLIND METHOD; DRUG INTERACTIONS; EUPHORIA; FEMALE; HALLUCINOGENS; HUMANS; INHIBITION (PSYCHOLOGY); INJECTIONS, INTRAVENOUS; MALE; MARIJUANA ABUSE; MEMORY; MENTAL RECALL; MIDDLE AGED; NALTREXONE; NARCOTIC ANTAGONISTS; ORIENTATION; PERCEPTION; PSYCHOSES, SUBSTANCE-INDUCED; RECOGNITION (PSYCHOLOGY); REWARD; TETRAHYDROCANNABINOL; YOUNG ADULT;

EID: 84871520610     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145711001830     Document Type: Article

References (82)

1. Agurell S, Halldin M, Lindgren JE, Ohlsson A, et al. (1986). Pharmacokinetics and metabolism of delta 1-tetrahydrocannabinol and other cannabinoids with emphasis on man. Pharmacological Reviews 38, 21-43.
2. Azorlosa JL, Greenwald MK, Stitzer ML (1995). Marijuana smoking: effects of varying puff volume and breathhold duration. Journal of Pharmacology and Experimental Therapeutics 272, 560-569.
3. Azorlosa JL, Heishman SJ, Stitzer ML, Mahaffey JM (1992). Marijuana smoking: effect of varying delta 9-tetrahydrocannabinol content and number of puffs. Journal of Pharmacology and Experimental Therapeutics 261, 114-122.
4. Beardsley PM, Balster RL, Harris LS (1986). Dependence on tetrahydrocannabinol in rhesus monkeys. Journal of Pharmacology and Experimental Therapeutics 239, 311-319.
5. Bhargava HN, Rahmani NH, Villar VM, Larsen AK (1993). Effects of naltrexone on pharmacodynamics and pharmacokinetics of intravenously administered morphine in the rat. Pharmacology 46, 66-74.
6. Braida D, Iosue S, Pegorini S, Sala M (2004). Delta9- tetrahydrocannabinol-induced conditioned place preference and intracerebroventricular self-administration in rats. European Journal of Pharmacology 506, 63-69.
7. Braida D, Pozzi M, Cavallini R, Sala M (2001). Conditioned place preference induced by the cannabinoid agonist CP 55,940 : interaction with the opioid system. Neuroscience 104, 923-926.
8. Brandt J (1991). The Hopkins Verbal Learning Test. Development of a new memory test with 6 equivalent forms. Clinical Neuropsychologist 5, 125-142.
9. Brandt J, Benedict RHB (1991). Hopkins Verbal Learning Test-Revised. Professional manual. Florida: PAR Inc.
10. Bremner JD, Krystal JH, Putnam FW, Southwick SM, et al. (1998). Measurement of dissociative states with the Clinician-Administered Dissociative States Scale (CADSS). Journal of Traumatic Stress 11, 125-136.
11. Brunner E, Domhof S, Langer F (2002). Nonparametric Analysis of Longitudinal Data in Factorial Experiments. New York: John Wiley and Sons.
12. Cadoni C, Pisanu A, Solinas M, Acquas E, et al. (2001). Behavioural sensitization after repeated exposure to Delta 9-tetrahydrocannabinol and cross-sensitization with morphine. Psychopharmacology 158, 259-266.
13. Cadoni C, Valentini V, di Chiara G (2008). Behavioral sensitization to delta 9-tetrahydrocannabinol and cross-sensitization with morphine: differential changes in accumbal shell and core dopamine transmission. Journal of Neurochemistry 106, 1586-1593.
14. Chen JP, Paredes W, Li J, Smith D, et al. (1990). Delta 9-tetrahydrocannabinol produces naloxone-blockable enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology 102, 156-162.
15. Cooper ZD, Haney M (2010). Opioid antagonism enhances marijuana's effects in heavy marijuana smokers. Psychopharmacology 211, 141-148.
16. Corchero J, Avila MA, Fuentes JA, Manzanares J (1997). delta-9-Tetrahydrocannabinol increases prodynorphin and proenkephalin gene expression in the spinal cord of the rat. Life Sciences 61, 39-43.
17. Corchero J, Fuentes JA, Manzanares J (2002). Gender differences in proenkephalin gene expression response to delta9-tetrahydrocannabinol in the hypothalamus of the rat. Journal of Psychopharmacology 16, 283-289.
18. Corchero J, Garcia-Gil L, Manzanares J, Fernandez-Ruiz JJ, et al. (1998a). Perinatal delta9-tetrahydrocannabinol exposure reduces proenkephalin gene expression in the caudate-putamen of adult female rats. Life Sciences 63, 843-850.
19. Corchero J, Garcia-Gil L, Manzanares J, Fernandez-Ruiz JJ, et al. (1998b). Perinatal delta9-tetrahydrocannabinol exposure reduces proenkephalin gene expression in the caudate-putamen of adult female rats. Life Sciences 63, 843-850.
20. Corchero J, Manzanares J, Fuentes JA (1999a). Repeated administration of delta9-tetrahydrocannabinol produces a differential time related responsiveness on proenkephalin, proopiomelanocortin and corticotropin releasing factor gene expression in the hypothalamus and pituitary gland of the rat. Neuropharmacology 38, 433-439.
21. Corchero J, Romero J, Berrendero F, Fernandez-Ruiz J, et al. (1999b). Time-dependent differences of repeated administration with Delta9- tetrahydrocannabinol in proenkephalin and cannabinoid receptor gene expression and G-protein activation by mu-opioid and CB1-cannabinoid receptors in the caudate-putamen. Brain Research. Molecular Brain Research 67, 148-157.
22. Da Fonseca Pacheco D, Klein A, Perez AC, Pacheco CM, et al. (2009). Central antinociception induced by mu-opioid receptor agonist morphine, but not delta-or kappa-, is mediated by cannabinoid CB1 receptor. British Journal of Pharmacology 158, 225-231.
23. Del Arco I, Navarro M, Bilbao A, Ferrer B, et al. (2002). Attenuation of spontaneous opiate withdrawal in mice by the anandamide transport inhibitor AM404. European Journal of Pharmacology 454, 103-104.
24. D'Souza DC, Abi-Saab WM, Madonick S, Forselius-Bielen K, et al. (2005). Delta-9-tetrahydrocannabinol effects in schizophrenia : implications for cognition, psychosis, and addiction. Biological Psychiatry 57, 594-608.
25. D'Souza DC, Braley G, Blaise R, Vendetti M, et al. (2008a). Effects of haloperidol on the behavioral, subjective, cognitive, motor, and neuroendocrine effects of Delta-9-tetrahydrocannabinol in humans. Psychopharmacology 198, 587-603.
26. D'Souza DC, Perry E, MacDougall L, Ammerman Y, et al. (2004). The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals : implications for psychosis. Neuropsychopharmacology 29, 1558-1572.
27. D'Souza DC, Perry E, Wray Y, Macdougall L, et al. (2001). Cannabinoid-dopamine interactions and psychosis: haloperidol effects. Cannabinoid Model Psychosis 11th Annual International Cannabinoid Research Society Meeting, San Lorenzo De El Escorial, Madrid, Spain.
28. D'Souza DC, Ranganathan M, Braley G, Gueorguieva R, et al. (2008b). Blunted psychotomimetic and amnestic effects of delta-9-tetrahydrocannabinol in frequent users of cannabis. Neuropsychopharmacology 33, 2505-2516.
29. Fattore L, Cossu G, Spano MS, Deiana S, et al. (2004). Cannabinoids and reward: interactions with the opioid system. Critical Reviews in Neurobiology 16, 147-158.
30. First MB, Spitzer RL, Gibbon M, Williams JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders-Non-patient Edition. Washington, DC: American Psychiatric Association.
31. Folstein MF, Folstein SE, McHugh PR (1975). 'Mini-mental state'. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189-198.
32. Greenwald MK, Stitzer ML (2000). Antinociceptive, subjective and behavioral effects of smoked marijuana in humans. Drug Alcohol Depend 59, 261-275.
33. Grotenhermen F (2003). Pharmacokinetics and pharmacodynamics of cannabinoids. Clinical Pharmacokinetics 42, 327-360.
34. Guthrie S (1990). Pharmacologic interventions for the treatment of opioid dependence and withdrawal. Dalian Institute of Chemical Physics 24, 721-734.
35. Hadjiconstantinou M, Neff NH (2011). Nicotine and endogenous opioids : neurochemical and pharmacological evidence. Neuropharmacology 60, 1209-1220.
36. Haertzen CA (1965). Addiction Research Center Inventory (ARCI): development of a general drug estimation scale. Journal of Nervous and Mental Disease 141, 300-307.
37. Haertzen CA (1966). Development of scales based on patterns of drug effects, using the addiction Research Center Inventory (ARCI). Psychological Reports 18, 163-194.
38. Haney M (2007). Opioid antagonism of cannabinoid effects : differences between marijuana smokers and nonmarijuana smokers. Neuropsychopharmacology 32, 1391-1403.
39. Haney M, Bisaga A, Foltin RW (2003). Interaction between naltrexone and oral THC in heavy marijuana smokers. Psychopharmacology 166, 77-85.
40. Hojo M, Sudo Y, Ando Y, Minami K, et al. (2008). mu-Opioid receptor forms a functional heterodimer with cannabinoid CB1 receptor : electrophysiological and FRET assay analysis. Journal of Pharmacological Sciences 108, 308-319.
41. Hooker WD, Jones RT (1987). Increased susceptibility to memory intrusions and the Stroop interference effect during acute marijuana intoxication. Psychopharmacology 91, 20-24.
42. Howlett AC, Barth F, Bonner TI, Cabral G, et al. (2002). International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacological Reviews 54, 161-202.
43. Justinova Z, Munzar P, Panlilio LV, Yasar S, et al. (2008). Blockade of THC-seeking behavior and relapse in monkeys by the cannabinoid CB(1)-receptor antagonist rimonabant. Neuropsychopharmacology 33, 2870-2877.
44. Justinova Z, Tanda G, Munzar P, Goldberg SR (2004). The opioid antagonist naltrexone reduces the reinforcing effects of Delta 9 tetrahydrocannabinol (THC) in squirrel monkeys. Psychopharmacology 173, 186-194.
45. Kay SR, Opler LA, Lindenmayer JP (1989). The Positive and Negative Syndrome Scale (PANSS): rationale and standardisation. British Journal of Psychiatry (Suppl.) 59-67.
46. Korczyn AD, Eshel Y (1982). Mydriasis induced by tetrahydrocannabinol (THC) in rats. Investigative Ophthalmology and Visual Science 22, 408-410.
47. Krystal JH, Karper LP, Seibyl JP, Freeman GK, et al. (1994). Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Archives of General Psychiatry 51, 199-214.
48. Krystal JH, Madonick S, Perry E, Gueorguieva R, et al. (2006). Potentiation of low dose ketamine effects by naltrexone : potential implications for the pharmacotherapy of alcoholism. Neuropsychopharmacology 31, 1793-1800.
49. Lamarque S, Taghzouti K, Simon H (2001). Chronic treatment with Delta(9)-tetrahydrocannabinol enhances the locomotor response to amphetamine and heroin. Implications for vulnerability to drug addiction. Neuropharmacology 41, 118-129.
50. Le Foll B, Wiggins M, Goldberg SR (2006). Nicotine pre-exposure does not potentiate the locomotor or rewarding effects of Delta-9-tetrahydrocannabinol in rats. Behavioural Pharmacology 17, 195-199.
51. Li JX, McMahon LR, Gerak LR, Becker GL, et al. (2008). Interactions between Delta(9)-tetrahydrocannabinol and mu opioid receptor agonists in rhesus monkeys: discrimination and antinociception. Psychopharmacology 199, 199-208.
52. Lile JA, Kelly TH, Pinsky DJ, Hays LR (2009). Substitution profile of Delta9-tetrahydrocannabinol, triazolam, hydromorphone, and methylphenidate in humans discriminating Delta9-tetrahydrocannabinol. Psychopharmacology 203, 241-250.
53. Lindgren JE, Ohlsson A, Agurell S, Hollister L, et al. (1981). Clinical effects and plasma levels of delta 9-tetrahydrocannabinol (delta 9-THC) in heavy and light users of cannabis. Psychopharmacology 74, 208-212.
54. Manzanares J, Corchero J, Fuentes JA (1999a). Opioid and cannabinoid receptor-mediated regulation of the increase in adrenocorticotropin hormone and corticosterone plasma concentrations induced by central administration of delta(9)-tetrahydrocannabinol in rats. Brain Research 839, 173-179.
55. Manzanares J, Corchero J, Romero J, Fernandez-Ruiz JJ, et al. (1999b). Pharmacological and biochemical interactions between opioids and cannabinoids. Trends in Pharmacological Sciences 20, 287-294.
56. Massi P, Vaccani A, Romorini S, Parolaro D (2001). Comparative characterization in the rat of the interaction between cannabinoids and opiates for their immunosuppressive and analgesic effects. Journal of Neuroimmunology 117, 116-124.
57. Navarro M, Carrera MR, del Arco I, Trigo JM, et al. (2004). Cannabinoid receptor antagonist reduces heroin self-administration only in dependent rats. European Journal of Pharmacology 501, 235-237.
58. Navarro M, Carrera MR, Fratta W, Valverde O, et al. (2001). Functional interaction between opioid and cannabinoid receptors in drug self-administration. Journal of Neuroscience 21, 5344-5350.
59. Navarro M, Chowen J, Rocio ACM, del Arco I, et al. (1998). CB1 cannabinoid receptor antagonist-induced opiate withdrawal in morphine-dependent rats. Neuroreport 9, 3397-3402.
60. O'Brien CPCA, McLellan AT, Ternes J, Ehrman RN (1984). Use of naltrexone to extinguish opioid-conditioned responses. Journal of Clinical Psychiatry 45(9), 53-56.
61. Ohlsson A, Widman M, Carlsson S, Ryman T, et al. (1980). Plasma and brain levels of delta 6-THC and seven monooxygenated metabolites correlated to the cataleptic effect in the mouse. Acta Pharmacologica et Toxicologica 47, 308-317.
62. Perez-Rosado A, Manzanares J, Fernandez-Ruiz J, Ramos JA (2000). Prenatal Delta(9)-tetrahydrocannabinol exposure modifies proenkephalin gene expression in the fetal rat brain : sex-dependent differences. Brain Research. Developmental Brain Research 120, 77-81.
63. Pickel VM, Chan J, Kash TL, Rodriguez JJ, et al. (2004). Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127, 101-112.
64. Prescott WR, Gold LH, Martin BR (1992). Evidence for separate neuronal mechanisms for the discriminative stimulus and catalepsy induced by delta 9-THC in the rat. Psychopharmacology 107, 117-124.
65. Pugh Jr. G, Smith PB, Dombrowski DS, Welch SP (1996). The role of endogenous opioids in enhancing the antinociception produced by the combination of delta 9-tetrahydrocannabinol and morphine in the spinal cord. Journal of Pharmacology and Experimental Therapeutics 279, 608-616.
66. Rios C, Gomes I, Devi LA (2006). mu opioid and CB1 cannabinoid receptor interactions : reciprocal inhibition of receptor signaling and neuritogenesis. British Journal of Pharmacology 148, 387-395.
67. Rodriguez JJ, Mackie K, Pickel VM (2001). Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat caudate putamen nucleus. Journal of Neuroscience 21, 823-833.
68. Salio C, Fischer J, Franzoni MF, Mackie K, et al. (2001). CB1-cannabinoid and mu-opioid receptor co-localization on postsynaptic target in the rat dorsal horn. Neuroreport 12, 3689-3692.
69. Solinas M, Goldberg SR (2005). Motivational effects of cannabinoids and opioids on food reinforcement depend on simultaneous activation of cannabinoid and opioid systems. Neuropsychopharmacology 30, 2035-2045.
70. Solinas M, Panlilio LV, Goldberg SR (2004). Exposure to delta-9-tetrahydrocannabinol (THC) increases subsequent heroin taking but not heroin's reinforcing efficacy: a self-administration study in rats. Neuropsychopharmacology 29, 1301-1311.
71. Spano MS, Fattore L, Cossu G, Deiana S, et al. (2004). CB1 receptor agonist and heroin, but not cocaine, reinstate cannabinoid-seeking behaviour in the rat. British Journal of Pharmacology 143, 343-350.
72. Tanda G, Pontieri FE, Di Chiara G (1997). Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism[comment]. Science 276, 2048-2050.
73. Tiffany ST, Drobes DJ (1991). The development and initial validation of a questionnaire on smoking urges. British Journal of Addiction 86, 1467-1476.
74. Valverde O, Noble F, Beslot F, Dauge V, et al. (2001). Delta9-tetrahydrocannabinol releases and facilitates the effects of endogenous enkephalins : reduction in morphine withdrawal syndrome without change in rewarding effect. European Journal of Neuroscience 13, 1816-1824.
75. Vaysse PJ, Gardner EL, Zukin RS (1987). Modulation of rat brain opioid receptors by cannabinoids. Journal of Pharmacology and Experimental Therapeutics 241, 534-539.
76. Vigano D, Rubino T, Parolaro D (2005). Molecular and cellular basis of cannabinoid and opioid interactions. Pharmacology Biochemistry and Behavior 81, 360-368.
77. Wachtel SR, de Wit H (2000). Naltrexone does not block the subjective effects of oral Delta(9)-tetrahydrocannabinol in humans. Drug and Alcohol Dependence 59, 251-260.
78. Wakley AA, Craft RM (2011). THC-methadone and THC-naltrexone interactions on discrimination, antinociception, and locomotion in rats. Behavioural Pharmacology 22, 489-497.
79. Webster LR, Johnson FK, Stauffer J, Setnik B, et al. (2011). Impact of intravenous naltrexone on intravenous morphine-induced high, drug liking, and euphoric effects in experienced, nondependent male opioid users. Drugs in R&D 11, 259-275.
80. Welch SP, Eads M (1999). Synergistic interactions of endogenous opioids and cannabinoid systems. Brain Research 848, 183-190.
81. Welch SP, Stevens DL (1992). Antinociceptive activity of intrathecally administered cannabinoids alone, and in combination with morphine, in mice. Journal of Pharmacology and Experimental Therapeutics 262, 10-18.
82. Welch SP, Thomas C, Patrick GS (1995). Modulation of cannabinoid-induced antinociception after intracerebroventricular vs. intrathecal administration to mice: possible mechanisms for interaction with morphine. Journal of Pharmacology and Experimental Therapeutics 272, 310-321.