Blockade of Nicotine and Cannabinoid Reinforcement and Relapse by a Cannabinoid CB1-Receptor Neutral Antagonist AM4113 and Inverse Agonist Rimonabant in Squirrel Monkeys.
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Nicotine, the main psychoactive component of tobacco, and (-)-Δ(9)-tetrahydrocannabinol (THC), the main psychoactive ingredient in cannabis, play major roles in tobacco and marijuana dependence as reinforcers of drug-seeking and drug-taking behavior. Drugs that act as inverse agonists of cannabinoid CB1 receptors in the brain can attenuate the rewarding and abuse-related effects of nicotine and THC, but their clinical use is hindered by potentially serious side effects. The recently developed CB1-receptor neutral antagonists may provide an alternative therapeutic approach to nicotine and cannabinoid dependence. Here we compare attenuation of nicotine and THC reinforcement and reinstatement in squirrel monkeys by the CB1-receptor inverse agonist rimonabant and by the recently developed CB1-receptor neutral antagonist AM4113. Both rimonabant and AM4113 reduced two effects of nicotine and THC that play major roles in tobacco and marijuana dependence: (1) maintenance of high rates of drug-taking behavior, and (2) priming- or cue-induced reinstatement of drug-seeking behavior in abstinent subjects (models of relapse). In contrast, neither rimonabant nor AM4113 modified cocaine-reinforced or food-reinforced operant behavior under similar experimental conditions. However, both rimonabant and AM4113 reduced cue-induced reinstatement in monkeys trained to self-administer cocaine, suggesting the involvement of a common cannabinoid-mediated mechanism in the cue-induced reinstatement for different drugs of abuse. These findings point to CB1-receptor neutral antagonists as a new class of medications for treatment of both tobacco dependence and cannabis dependence.
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A neutral CB1 antagonist (AM4113) may retain the therapeutic potential of inverse agonists, possibly without the neuropsychiatric side effects.
“The recent report that a neutral CB1 antagonist (AM4113) may retain the therapeutic potential of inverse agonists 66, 67, possibly without the neuropsychiatric side effects 67”
From Psychosocial and pharmacological interventions for the treatment of cannabis use disorder (2018) · cites this paper as [66]
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Gaal, L. F. V., Rissanen, A., Scheen, A. J., Ziegler, O., & Rössner, S. (2005) · The Lancet · doi:10.1016/s0140-6736(05)66374-x · Cited by 1,500 · see citing works
Pi-Sunyer, X., Aronne, L. J., Heshmati, H. M., Devin, J., Rosenstock, J., & for the RIO-North America Study Group (2006) · JAMA · doi:10.1001/jama.295.7.761 · Cited by 1,209 · see citing works
Tanda, G., Pontieri, F. E., & Chiara, G. D. (1997) · Science · doi:10.1126/science.276.5321.2048 · Cited by 1,079 · see citing works
A cannabinoid mechanism in relapse to cocaine seeking
Vries, T. J. D., Shaham, Y., Homberg, J. R., Crombag, H. S., Schuurman, K. G., Dieben, J., Vanderschuren, L. J. M. J., & Schoffelmeer, A. N. M. (2001) · Nature Medicine · doi:10.1038/nm1001-1151 · Cited by 433 · see citing works
Cohen, C., Perrault, G., Voltz, C., Steinberg, R., & Soubrié, P. (2002) · Behavioural Pharmacology · doi:10.1097/00008877-200209000-00018 · Cited by 396 · see citing works
Tanda, G., Munzar, P., & Goldberg, S. R. (2000) · Nature Neuroscience · doi:10.1038/80577 · Cited by 347 · see citing works
Self-citationPersistent Behavior at High Rates Maintained by Intravenous Self-Administration of Nicotine
Goldberg, S. R., Spealman, R. D., & Goldberg, D. M. (1981) · Science · doi:10.1126/science.7291998 · Cited by 343 · see citing works
Self-citationThe validity of the reinstatement model of craving and relapse to drug use
Katz, J. L., & Higgins, S. T. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1441-y · Cited by 273 · see citing works
SR141716A is an inverse agonist at the human cannabinoid CB1 receptor
Landsman, R. S., Burkey, T. H., Consroe, P. F., Roeske, W. R., & Yamamura, H. I. (1997) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01160-6 · Cited by 263 · see citing works
Nicotine self-administration in rats: strain and nicotine pre-exposure effects on acquisition
Shoaib, M., Schindler, C. W., & Goldberg, S. R. (1997) · Psychopharmacology · doi:10.1007/s002130050159 · Cited by 233 · see citing works
Self-citationNicotine induces conditioned place preferences over a large range of doses in rats
Foll, B. L., & Goldberg, S. R. (2004) · Psychopharmacology · doi:10.1007/s00213-004-2021-5 · Cited by 229 · see citing works
Self-citationCannabinoid CB1 receptors control conditioned drug seeking
Vries, T. J. D., & Schoffelmeer, A. N. M. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.06.002 · Cited by 219 · see citing works
Nicotine as a reinforcer in human subjects and laboratory animals
Henningfield, J. E., & Goldberg, S. R. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90405-7 · Cited by 214 · see citing works
Self-citationGoldberg, S. R. (1973) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)29561-1 · Cited by 214 · see citing works
Self-citationEffects of Nicotine in Experimental Animals and Humans: An Update on Addictive Properties
Foll, B. L., & Goldberg, S. R. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-69248-5_12 · Cited by 194 · see citing works
Self-citationNicotine receptor partial agonists for smoking cessation
Cahill, K., Stead, L. F., & Lancaster, T. (2011) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006103.pub5 · Cited by 187 · see citing works
Janero, D. R., & Makriyannis, A. (2009) · Expert Opinion on Emerging Drugs · doi:10.1517/14728210902736568 · Cited by 186 · see citing works
Self-citationRimonabant, a CB1 antagonist, blocks nicotine-conditioned place preferences
Foll, B. L., & Goldberg, S. R. (2004) · Neuroreport · doi:10.1097/00001756-200409150-00028 · Cited by 174 · see citing works
Self-citationXi, Z., Gilbert, J. G., Peng, X., Pak, A. C., Li, X., & Gardner, E. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0726-06.2006 · Cited by 162 · see citing works
Sink, K. S., McLaughlin, P. J., Wood, J. A. T., Brown, C., Fan, P., Vemuri, K. V., Pang, Y., Olzewska, T., Thakur, G. A., Makriyannis, A., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301476 · Cited by 161 · see citing works
Self-citationSalamone, J. D., McLaughlin, P. J., Sink, K. S., Makriyannis, A., & Parker, L. A. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.04.013 · Cited by 130 · see citing works
Self-citationForget, B., Coen, K. M., & Foll, B. L. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1569-5 · Cited by 118 · see citing works
Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats
Forget, B., Hamon, M., & Thiébot, M.-H. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0015-6 · Cited by 115 · see citing works
Sink, K. S., Vemuri, K. V., Olszewska, T., Makriyannis, A., & Salamone, J. D. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0988-4 · Cited by 115 · see citing works
Self-citationPavón, F. J., Bilbao, A., Hernández‐Folgado, L., Cippitelli, A., Jagerovic, N., Abellán, G., Rodrı́guez-Franco, M. I., Serrano, A., Macías, M., de Heras, R. G., et al. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.03.029 · Cited by 113 · see citing works
Medicinal chemistry of cannabinoids
Vemuri, K., & Makriyannis, A. (2015) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt.115 · Cited by 108 · see citing works
Self-citationJustinová, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0951-05.2005 · Cited by 104 · see citing works
Fattore, L. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00059-5 · Cited by 100 · see citing works
Vemuri, K. V., Janero, D. R., & Makriyannis, A. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.012 · Cited by 100 · see citing works
Self-citationJustinová, Z., Mascia, P., Wu, H., Secci, M. E., Redhi, G. H., Panlilio, L. V., Scherma, M., Barnes, C., Parashos, A., Zara, T., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3540 · Cited by 99 · see citing works
Self-citationCB1 receptor agonist and heroin, but not cocaine, reinstate cannabinoid‐seeking behaviour in the rat
Spano, M. S., Fattore, L., Cossu, G., Deiana, S., Fadda, P., & Fratta, W. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705932 · Cited by 95 · see citing works
A neutral CB1 receptor antagonist reduces weight gain in rat
Chambers, A. P., Vemuri, K. V., Peng, Y., Wood, J. T., Olszewska, T., Pittman, Q. J., Makriyannis, A., & Sharkey, K. A. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00663.2007 · Cited by 93 · see citing works
Self-citationShoaib, M. C. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.10.011 · Cited by 93 · see citing works
The role of CB1 receptors in psychostimulant addiction
Wiskerke, J., Pattij, T., Schoffelmeer, A. N. M., & Vries, T. J. D. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00109.x · Cited by 91 · see citing works
Sink, K. S., Segovia, K. N., Sink, J. R., Randall, P. A., Collins, L. E., Correa, M., Markus, E. J., Vemuri, K. V., Makriyannis, A., & Salamone, J. D. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.11.002 · Cited by 86 · see citing works
Self-citationJustinová, Z., Munzar, P., Panlilio, L. V., Yaşar, S., Redhi, G. H., Tanda, G., & Goldberg, S. R. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.21 · Cited by 86 · see citing works
Self-citationFilip, M., Gołda, A., Zaniewska, M., McCreary, A. C., Nowak, E., Kolasiewicz, W., & Przegaliński, E. (2006) · PubMed · Cited by 83 · see citing works
Mato, S., Pazos, Á., & Valdizán, E. M. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)01575-3 · Cited by 80 · see citing works
Diergaarde, L., de Vries, W., Raasø, H. S., Schoffelmeer, A. N. M., & Vries, T. J. D. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.003 · Cited by 80 · see citing works
Neutral antagonism at the cannabinoid 1 receptor: a safer treatment for obesity
Meye, F. J., Trezza, V, Vanderschuren, L. J. M. J., Ramakers, G. M. J., & Adan, R. A. H. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.145 · Cited by 76 · see citing works
Cannabinoid abuse and addiction: Clinical and preclinical findings
Panlilio, L. V., Goldberg, S. R., & Justinová, Z. (2015) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt.118 · Cited by 74 · see citing works
Self-citationCannabinoid type 1 receptor antagonists for smoking cessation
Cahill, K., & USSHER, M. H. (2011) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005353.pub4 · Cited by 72 · see citing works
Scherma, M., Justinová, Z., Zanettini, C., Panlilio, L. V., Mascia, P., Fadda, P., Fratta, W., Makriyannis, A., Vadivel, S. K., Gamaleddin, I., et al. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01467.x · Cited by 70 · see citing works
Self-citationWard, S. J., Rosenberg, M., Dykstra, L., & Walker, E. A. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.07.002 · Cited by 68 · see citing works
Panlilio, L. V., Solinas, M., Matthews, S. A., & Goldberg, S. R. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301109 · Cited by 68 · see citing works
Self-citationJustinová, Z., Yaşar, S., Redhi, G. H., & Goldberg, S. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6058-10.2011 · Cited by 63 · see citing works
Self-citationJustinová, Z., Panlilio, L. V., Secci, M. E., Redhi, G. H., Schindler, C. W., Cross, A. J., Mrzljak, L., Medd, A. M., Shaham, Y., & Goldberg, S. R. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.01.014 · Cited by 63 · see citing works
Self-citationStorr, M., Bashashati, M., Hirota, C. L., Vemuri, K. V., Keenan, C. M., Duncan, M., Lutz, B., Mackie, K., Makriyannis, A., MacNaughton, W. K., et al. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01478.x · Cited by 59 · see citing works
Self-citationMartín‐García, E., Bourgoin, L., Cathala, A., Kasanetz, F., Mondésir, M., Gutiérrez‐Rodrίguez, A., Reguero, L., Fiancette, J.-F., Grandes, P., Spampinato, U., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.351 · Cited by 55 · see citing works
Cannabinoid Discrimination and Antagonism by CB1 Neutral and Inverse Agonist Antagonists
Kangas, B. D., Delatte, M. S., Vemuri, K. V., Thakur, G. A., Nikas, S. P., Subramanian, K. V., Shukla, V. G., Makriyannis, A., & Bergman, J. (2013) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.201962 · Cited by 47 · see citing works
Self-citationSink, K. S., Segovia, K. N., Collins, L. E., Markus, E. J., Vemuri, K. V., Makriyannis, A., & Salamone, J. D. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.03.011 · Cited by 44 · see citing works
Self-citationSink, K. S., Vemuri, K. V., Wood, J. T., Makriyannis, A., & Salamone, J. D. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.07.013 · Cited by 43 · see citing works
Self-citationJärbe, T. U. C., LeMay, B. J., Olszewska, T., Vemuri, K. V., WOOD, J., & Makriyannis, A. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.06.014 · Cited by 39 · see citing works
Self-citationVlachou, S., Stamatopoulou, F., Nomikos, G. G., & Panagis, G. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708008717 · Cited by 39 · see citing works
Wills, K. L., Vemuri, K., Kalmar, A., Lee, A., Limebeer, C. L., Makriyannis, A., & Parker, L. A. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3575-5 · Cited by 29 · see citing works
Self-citationJärbe, T. U. C., LeMay, B. J., Vemuri, K. V., Vadivel, S. K., Zvonok, A. M., & Makriyannis, A. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2226-3 · Cited by 15 · see citing works
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- National Research Council (2003) Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research. The National Academies Press: Washington, DC. [PubMed] [Google Scholar]
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Hua, T., Vemuri, K. V., Pu, M., Qu, L., Han, G. W., Wu, Y., Zhao, S., Shui, W., Li, S., Korde, A., et al. (2016) · Cell · doi:10.1016/j.cell.2016.10.004 · Cited by 693 · see citing works
Self-citationCannabis use and cannabis use disorder
Connor, J. P., Stjepanović, D., Le Foll, B., Hoch, E., Budney, A. J., & Hall, W. D. (2021) · Nature Reviews Disease Primers · doi:10.1038/s41572-021-00247-4 · Cited by 552 · see citing works
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Maccarrone, M., Di Marzo, V., Gertsch, J., Grether, U., Howlett, A. C., Hua, T., Makriyannis, A., Piomelli, D., Ueda, N., & van der Stelt, M. (2023) · Pharmacological Reviews · doi:10.1124/pharmrev.122.000600 · Cited by 183 · see citing works
Self-citationFreels, T. G., Baxter-Potter, L. N., Lugo, J. M., Glodosky, N. C., Wright, H. R., Baglot, S. L., Petrie, G. N., Yu, Z., Clowers, B. H., Cuttler, C., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2416-19.2020 · Cited by 105 · see citing works
Nguyen, T., Thomas, B. F., & Zhang, Y. (2019) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026619666190708164841 · Cited by 103 · see citing works
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Sloan, M. E., Gowin, J. L., Ramchandani, V. A., Hurd, Y. L., & Foll, B. L. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.05.031 · Cited by 90 · see citing works
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Presynaptic G Protein-Coupled Receptors: Gatekeepers of Addiction?
Johnson, K. A., & Lovinger, D. M. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00264 · Cited by 66 · see citing works
Potential of Cannabinoid Receptor Ligands as Treatment for Substance Use Disorders
Galaj, E., & Xi, Z. (2019) · CNS Drugs · doi:10.1007/s40263-019-00664-w · Cited by 65 · see citing works
He, X., Jordan, C. J., Vemuri, K. V., Bi, G., Zhan, J., Gardner, E. L., Makriyannis, A., Wang, Y., & Xi, Z. (2018) · Acta Pharmacologica Sinica · doi:10.1038/s41401-018-0059-x · Cited by 54 · see citing works
Self-citationDelis, F., Polissidis, A., Poulia, N., Justinová, Z., Nomikos, G. G., Goldberg, S. R., & Antoniou, K. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw102 · Cited by 53 · see citing works
Self-citationStern, C. A. J., de Carvalho, C. R., Bertoglio, L. J., & Takahashi, R. N. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.07.018 · Cited by 52 · see citing works
Balla, A., Dong, B., Shilpa, B. M., Vemuri, K. V., Makriyannis, A., Pandey, S. C., Sershen, H. W., Suckow, R. F., & Vinod, K. Y. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.10.040 · Cited by 50 · see citing works
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Psychosocial and pharmacological interventions for the treatment of cannabis use disorder
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Panlilio, L. V., & Justinová, Z. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.193 · Cited by 37 · see citing works
Analysis of natural product regulation of opioid receptors in the treatment of human disease
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Off-label and investigational drugs in the treatment of alcohol use disorder: A critical review
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Soler‐Cedeño, O., & Xi, Z. (2022) · Cells · doi:10.3390/cells11203262 · Cited by 26 · see citing works
Analysis of natural product regulation of cannabinoid receptors in the treatment of human disease
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Psychosocial and Pharmacological Interventions for the Treatment of Cannabis Use Disorder
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Hayase, T. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000326 · Cited by 11 · see citing works
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Wang, X., Chen, Y., Dong, J., Ge, J., Liu, X., & Liu, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031482 · Cited by 10 · see citing works
Alsaafin, A., Chenoweth, M. J., Sylvestre, M., O’Loughlin, J. L., & Tyndale, R. F. (2022) · Addictive Behaviors · doi:10.1016/j.addbeh.2022.107545 · Cited by 9 · see citing works
Galaj, E., Hempel, B. J., Moore, A. R., Klein, B., Bi, G., Gardner, E. L., Seltzman, H. H., & Xi, Z. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02059-w · Cited by 9 · see citing works
Dulman, R. S., Zhang, H., Banerjee, R., Krishnan, H. R., Dong, B., Hungund, B. L., Vinod, K. Y., & Pandey, S. C. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108623 · Cited by 8 · see citing works
Antiemetic Effects of Cannabinoid Agonists in Nonhuman Primates
Wooldridge, L. M., Ji, L., Liu, Y., Nikas, S. P., Makriyannis, A., Bergman, J., & Kangas, B. D. (2020) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.120.265710 · Cited by 8 · see citing works
Self-citationMartin, E. L., & McRae‐Clark, A. L. (2020) · Current Addiction Reports · doi:10.1007/s40429-020-00342-8 · Cited by 8 · see citing works
Alayoubi, M., Henry, B. A., Cahill, C. M., & Cooper, Z. D. (2024) · Drugs · doi:10.1007/s40265-024-02098-1 · Cited by 7 · see citing works
Butler, K., Forget, B., Heishman, S. J., & Foll, B. L. (2021) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000607 · Cited by 7 · see citing works
Shankar, K., Bonnet-Zahedi, S., & George, O. (2025) · Psychopharmacology · doi:10.1007/s00213-025-06852-5 · Cited by 6 · see citing works
Alkhelb, D. A., Kirunda, A., Ho, T. C., Makriyannis, A., & Desai, R. I. (2022) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2022.109646 · Cited by 6 · see citing works
Self-citationPlescia, F., Plescia, F., Raffa, D., Cavallaro, A., Lavanco, G., Maggio, B., Raimondi, M. V., Daidone, G., Brancato, A., & Cannizzaro, C. (2018) · Pharmacological Reports · doi:10.1016/j.pharep.2018.06.004 · Cited by 5 · see citing works
Plescia, F., Lavanco, G., Zizzo, M. G., D'Amico, C., Bellocchio, L., Malta, G., Vaccaro, F., Cannizzaro, E., Dimino, L., & Plescia, F. (2025) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2025.177973 · Cited by 4 · see citing works
Laprairie, R. B., Vemuri, K. V., Stahl, E. L., Korde, A., Ho, J., Grim, T. W., Hua, T., Wu, Y., Stevens, R. C., Liu, Z., et al. (2019) · Molecular Pharmacology · doi:10.1124/mol.119.116483 · Cited by 4 · see citing works
Self-citationThe Role of the Endocannabinoid System in Addiction
Trigo, J. M., & Foll, B. L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809666-6.00006-x · Cited by 4 · see citing works
Advances in the study of pharmacotherapy for addiction to naturally-derived psychoactive substances
Xie, K., Xiao, D., Xu, P., Shen, H., & Di, B. (2025) · Chinese Journal of Natural Medicines · doi:10.1016/s1875-5364(25)60831-4 · Cited by 3 · see citing works
Chemical Probes for Investigating the Endocannabinoid System
Hanske, A., Nazaré, M., & Grether, U. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_563 · Cited by 3 · see citing works
Animal Models of Cannabis Use Disorder
Justinová, Z. (2018) · Springer eBooks · doi:10.1007/978-3-319-90365-1_8 · Cited by 3 · see citing works
Eiler, W. J. A., Gleason, S. D., Smith, J. L., & Witkin, J. M. (2019) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2019.06.005 · Cited by 3 · see citing works
Cannabinoid-based Pharmacology for the Management of Substance Use Disorders
Luján, M. Á., Kim, Y., Zhang, L., & Cheer, J. F. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_551 · Cited by 2 · see citing works
Janero, D. R., Vemuri, K. V., & Makriyannis, A. (2018) · Springer eBooks · doi:10.1007/978-3-319-90365-1_6 · Cited by 2 · see citing works
Self-citationNeuroanatomical and neurochemical substrates of addiction
Yates, J. R. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90578-7.00001-3 · Cited by 2 · see citing works
Eckard, M. L., & Kinsey, S. G. (2024) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2024.173718 · Cited by 2 · see citing works
Medications development for food-based and drug use disorders
de Moura, F. B., Kohut, S. J., & Bergman, J. (2019) · Advances in pharmacology · doi:10.1016/bs.apha.2019.04.005 · Cited by 2 · see citing works
Self-citationMcLaughlin, P. J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.96545-0 · Cited by 2 · see citing works
Involvement of CB1R and CB2R Ligands in Sleep Disorders and Addictive Behaviors in the Last 25 Years
Pérez-Morales, M., Espinoza-Abad, R., & García‐García, F. (2025) · Pharmaceuticals · doi:10.3390/ph18020266 · Cited by 1 · see citing works
Pharmacotherapy for Cannabis Use Disorder: Preclinical and Clinical Models
Bedillion, M. F., Moore, C. F., Weerts, E. M., Arout, C. A., Harris, H. M., & Haney, M. (2025) · Current topics in behavioral neurosciences · doi:10.1007/7854_2025_598 · Cited by 1 · see citing works
Costa, G. P. A., MacLean, R. R., Sofuoglu, M., & Aquino, J. P. D. (2026) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyag030 · Cited by 1 · see citing works
A Study on the Drug Abuse and Crimes Impacts on Youth
Manimugundhan, E. C. (2024) · International Journal of Advanced Research in Science Communication and Technology · doi:10.48175/ijarsct-19185 · Cited by 1 · see citing works
Nicotine Reward and Abstinence: Role of the CB1 Receptors
Tannous, S., & Caillé, S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813035-3.00037-x · Cited by 1 · see citing works
The endocannabinoid system: from the receptors to therapy
Bába, L.-I., Kolcsár, M., Beatrix, H., Gáll, Z., & Zoltán, K. I. (2019) · Orvostudományi Értesítö · doi:10.2478/orvtudert-2019-0002
Role of anandamide in nicotine addiction
Foll, B. L. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-19081-0.00015-9
From Stigma to Therapy: The Evolution of Psychiatry in Substance Use Disorders
Sagheddu, C., Virdis, G., & Melis, M. (2024) · Springer eBooks · doi:10.1007/978-3-031-72219-6_51
Giménez, V. M. M., & Manucha, W. A. (2024) · Springer eBooks · doi:10.1007/978-3-031-72219-6_18
Moore, C. F., Bedillion, M. F., Haney, M., & Weerts, E. M. (2025) · Current Addiction Reports · doi:10.1007/s40429-025-00705-z
Cannabinoid–Nicotine Interactions in Nicotine Addiction: Preclinical Evidence
Rodríguez‐Borillo, O., & Scherma, M. (2026) · Springer eBooks · doi:10.1007/978-3-032-12239-1_13
Morrisson, D., Smith, E. C., Alkhelb, D. A., Ho, T., Ji, L., Sromek, A. W., Makriyannis, A., & Desai, R. I. (2026) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2026.113243
Self-citationCo-use of cannabis and tobacco in the same occasion: Acute effects. A systematic review
Xu, J., Nette, A., Zakala, C., Zhao, S., Matheson, J., Wickens, C. M., Bonato, S., & Ciano, P. D. (2026) · Psychopharmacology · doi:10.1007/s00213-026-07174-w
- Authors
- Schindler, C. W., Redhi, G. H., Vemuri, K., Makriyannis, A., Le Foll, B., Bergman, J., Goldberg, S. R., & Justinova, Z.
- Affiliations
- National Institutes of Health (US)
- Northeastern University (US)
- Harvard University (US)
- Venue
- Neuropsychopharmacology
- Published
- 2016-02-18
- Volume
- 41
- Issue
- 9
- Pages
- 2283-2293
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC4946059
- OpenAlex
- W2331358065
- Cited by
- 73
- References
- 56
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 12 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 6 · 2019: 8 · 2018: 8 · 2017: 10 · 2016: 4
- FWCI
- 8.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (Z99 DA999999)
- National Institute on Drug Abuse (R01DA019205, R01DA007215, Z01DA000003, Z01DA000001, R01DA003801, R37DA023142, R01DA031020, R37DA003801, P01DA009158)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- nicotine reinforcement, CB1 receptor, rimonabant, neutral antagonists, inverse agonists, reinstatement, relapse, cue-induced reinstatement, self-administration, cocaine, food reinforcement, tobacco dependence, cannabis use disorder, squirrel monkey
- MeSH terms
- Rimonabant, Animals, Marijuana Abuse, Conditioning, Operant, Cues, Male, Nicotine, Piperidines, Pyrazoles, Recurrence, Reinforcement, Psychology, Saimiri, Self Administration, Dronabinol, Tobacco Use Disorder, Receptor, Cannabinoid, CB1, Drug-Seeking Behavior
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