Cannabinoids and the Microbiota-Gut-Brain Axis: Emerging Effects of Cannabidiol and Potential Applications to Alcohol Use Disorders.


Journal

Alcoholism, clinical and experimental research
ISSN: 1530-0277
Titre abrégé: Alcohol Clin Exp Res
Pays: England
ID NLM: 7707242

Informations de publication

Date de publication:
02 2020
Historique:
received: 22 08 2019
accepted: 25 11 2019
pubmed: 6 12 2019
medline: 5 2 2021
entrez: 6 12 2019
Statut: ppublish

Résumé

The endocannabinoid system (ECS) has emerged in recent years as a potential treatment target for alcohol use disorders (AUD). In particular, the nonpsychoactive cannabinoid cannabidiol (CBD) has shown preclinical promise in ameliorating numerous clinical symptoms of AUD. There are several proposed mechanism(s) through which cannabinoids (and CBD in particular) may confer beneficial effects in the context of AUD. First, CBD may directly impact specific brain mechanisms underlying AUD to influence alcohol consumption and the clinical features of AUD. Second, CBD may influence AUD symptoms through its actions across the digestive, immune, and central nervous systems, collectively known as the microbiota-gut-brain axis (MGBA). Notably, emerging work suggests that alcohol and cannabinoids exert opposing effects on the MGBA. Alcohol is linked to immune dysfunction (e.g., chronic systemic inflammation in the brain and periphery) as well as disturbances in gut microbial species (microbiota) and increased intestinal permeability. These MGBA disruptions have been associated with AUD symptoms such as craving and impaired cognitive control. Conversely, existing preclinical data suggest that cannabinoids may confer beneficial effects on the gastrointestinal and immune system, such as reducing intestinal permeability, regulating gut bacteria, and reducing inflammation. Thus, cannabinoids may exert AUD harm-reduction effects, at least in part, through their beneficial actions across the MGBA. This review will provide a brief introduction to the ECS and the MGBA, discuss the effects of cannabinoids (particularly CBD) and alcohol in the brain, gut, and immune system (i.e., across the MGBA), and put forth a theoretical framework to inform future research questions.

Identifiants

pubmed: 31803950
doi: 10.1111/acer.14256
doi:

Substances chimiques

Cannabinoids 0
Cannabidiol 19GBJ60SN5

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

340-353

Informations de copyright

© 2019 by the Research Society on Alcoholism.

Références

Abrahao KP, Salinas AG, Lovinger DM (2017) Alcohol and the brain: neuronal molecular targets, synapses, and circuits. Neuron 96:1223-1238.
Acharya N, Penukonda S, Shcheglova T, Hagymasi AT, Basu S, Srivastava PK (2017) Endocannabinoid system acts as a regulator of immune homeostasis in the gut. Proc Natl Acad Sci 114:5005-5010.
Adejumo AC, Ajayi TO, Adegbala OM, Adejumo KL, Alliu S, Akinjero AM, Onyeakusi NE, Ojelabi O, Bukong TN (2018) Cannabis use is associated with reduced prevalence of progressive stages of alcoholic liver disease. Liver Int 38:1475-1486.
Adermark L, Jonsson S, Ericson M, Söderpalm B (2011) Intermittent ethanol consumption depresses endocannabinoid-signaling in the dorsolateral striatum of rat. Neuropharmacology 61:1160-1165.
Al-Ghezi ZZ, Busbee PB, Alghetaa H, Nagarkatti PS, Nagarkatti M (2019) Combination of cannabinoids, delta-9-tetrahydrocannabinol (THC) and cannabidiol (CBD), mitigates experimental autoimmune encephalomyelitis (EAE) by altering the gut microbiome. Brain Behav Immun 82:25-35.
Alhamoruni A, Lee AC, Wright KL, Larvin M, O’Sullivan SE (2010) Pharmacological effects of cannabinoids on the Caco-2 cell culture model of intestinal permeability. J Pharmacol Exp Ther 335:92-102.
Alhamoruni A, Wright KL, Larvin M, O’Sullivan SE (2012) Cannabinoids mediate opposing effects on inflammation-induced intestinal permeability. Br J Pharmacol 165:2598-2610.
Alonso C, Guilarte M, Vicario M, Ramos L, Rezzi S, Martínez C, Lobo B, Martin F-P, Pigrau M, González-Castro AM, Gallart M, Malagelada JR, Azpiroz F, Kochhar S, Santos J (2012) Acute experimental stress evokes a differential gender-determined increase in human intestinal macromolecular permeability. Neurogastroenterol Motil 24:740-e349.
Amato KR (2016) An introduction to microbiome analysis for human biology applications. Am J Hum Biol 29:e22931.
Andreae MH, Carter GM, Shaparin N, Suslov K, Ellis RJ, Ware MA, Abrams DI, Prasad H, Wilsey B, Indyk D, Johnson M, Sacks HS (2015) Inhaled cannabis for chronic neuropathic pain: a meta-analysis of individual patient data. J Pain 16:1221-1232.
Avraham Y, Grigoriadis N, Poutahidis T, Vorobiev L, Magen I, Ilan Y, Mechoulam R, Berry E (2011) Cannabidiol improves brain and liver function in a fulminant hepatic failure-induced model of hepatic encephalopathy in mice. Br J Pharmacol 162:1650-1658.
Bailey MT, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35:146-155.
Bajaj JS, Ridlon JM, Hylemon PB, Thacker LR, Heuman DM, Smith S, Sikaroodi M, Gillevet PM (2012) Linkage of gut microbiome with cognition in hepatic encephalopathy. Am J Physiol Gastrointest Liver Physiol 302:G168-G175.
Ballard ME, de Wit H (2011) Combined effects of acute, very-low-dose ethanol and delta(9)-tetrahydrocannabinol in healthy human volunteers. Pharmacol Biochem Behav 97:627-631.
Banks WA, Erickson MA (2010) The blood-brain barrier and immune function and dysfunction. Neurobiol Dis 37:26-32.
Basavarajappa BS, Ninan I, Arancio O (2008) Acute ethanol suppresses glutamatergic neurotransmission through endocannabinoids in hippocampal neurons. J Neurochem 107:1001-1013.
Belgrave BE, Bird KD, Chesher GB, Jackson DM, Lubbe KE, Starmer GA, Teo RK (1979) The effect of cannabidiol, alone and in combination with ethanol, on human performance. Psychopharmacology 64:243-246.
Bidwell LC, Mueller R, Yorkwilliams SL, Hagerty S, Bryan AD, Hutchison KE (2018) A novel observational method for assessing acute responses to cannabis: preliminary validation using legal market strains. Cannabis Cannabinoid Res 3:35-44.
Bird KD, Boleyn T, Chesher GB, Jackson DM, Starmer GA, Teo RKC (1980) Intercannabinoid and cannabinoid-ethanol interactions and their effects on human performance. Psychopharmacology 71:181-188.
Blednov YA, Harris RA (2009) Deletion of vanilloid receptor (TRPV1) in mice alters behavioral effects of ethanol. Neuropharmacology 56:814-820.
Bode C, Christian Bode J (2003) Effect of alcohol consumption on the gut. Best Pract Res Clin Gastroenterol 17:575-592.
Borrelli F, Aviello G, Romano B, Orlando P, Capasso R, Maiello F, Guadagno F, Petrosino S, Capasso F, Di Marzo V, Izzo AA (2009) Cannabidiol, a safe and non-psychotropic ingredient of the marijuana plant Cannabis sativa, is protective in a murine model of colitis. J Mol Med 87:1111-1121.
Brown AJ (2007) Novel cannabinoid receptors. Br J Pharmacol 152:567-575.
Burstein S (2015) Cannabidiol (CBD) and its analogs: a review of their effects on inflammation. Bioorg Med Chem 23:1377-1385.
Burstein SH, Zurier RB (2009) Cannabinoids, endocannabinoids, and related analogs in inflammation. AAPS J 11:109-119.
Cabral GA, Griffin-Thomas L (2009) Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation. Expert Rev Mol Med 11:e3.
Cabral GA, Rogers TJ, Lichtman AH (2015) Turning over a new leaf: cannabinoid and endocannabinoid modulation of immune function. J Neuroimmune Pharmacol 10:193-203.
Caillé S, Alvarez-Jaimes L, Polis I, Stouffer DG, Parsons LH (2007) Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration. J Neurosci 27:3695-3702.
Campos AC, Guimarães FS (2009) Evidence for a potential role for TRPV1 receptors in the dorsolateral periaqueductal gray in the attenuation of the anxiolytic effects of cannabinoids. Prog Neuro-Psychopharmacol Biol Psychiatry 33:1517-1521.
Cani PD, Plovier H, Van Hul M, Geurts L, Delzenne NM, Druart C, Everard A (2016) Endocannabinoids-at the crossroads between the gut microbiota and host metabolism. Nat Rev Endocrinol 12:133-143.
Carrier EJ, Auchampach JA, Hillard CJ (2006) Inhibition of an equilibrative nucleoside transporter by cannabidiol: a mechanism of cannabinoid immunosuppression. Proc Natl Acad Sci USA 16:7895-7900.
Chait LD, Evans SM, Grant KA, Kamien JB, Johanson CE, Schuster CR (1988) Discriminative stimulus and subjective effects of smoked marijuana in humans. Psychopharmacology 94:206-212.
Chait L, Perry J (1994) Acute and residual effects of alcohol and marijuana, alone and in combination, on mood and performance. Psychopharmacology 115:340-349.
Chait LD, Zacny JP (1992) Reinforcing and subjective effects of oral Δ9-THC and smoked marijuana in humans. Psychopharmacology 107:255-262.
Chang YH, Lee ST, Lin WW (2001) Effects of cannabinoids on LPS-stimulated inflammatory mediator release from macrophages: involvement of eicosanoids. J Cell Biochem 81:715-723.
Clarke RBC, Adermark L (2010) Acute ethanol treatment prevents endocannabinoid-mediated long-lasting disinhibition of striatal output. Neuropharmacology 58:799-805.
Cluny NL, Keenan CM, Reimer RA, Le Foll B, Sharkey KA (2015) Prevention of diet-induced obesity effects on body weight and gut microbiota in mice treated chronically with Δ9-tetrahydrocannabinol. PLoS ONE 10:e0144270.
Consroe P, Carlini EA, Zwicker AP, Lacerda LA (1979) Interaction of cannabidiol and alcohol in humans. Psychopharmacology 66:45-50.
Crews FT, Sarkar DK, Qin L, Zou J, Boyadjieva N, Vetreno RP (2015) Neuroimmune function and the consequences of alcohol exposure. Alcohol Res 37:331-341, 344-351.
Crews FT, Zou J, Qin L (2011) Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 25:S4-S12.
Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701-712.
D’Argenio G, Petrosino S, Gianfrani C, Valenti M, Scaglione G, Grandone I, Nigam S, Sorrentini I, Mazzarella G, Di Marzo V (2007) Overactivity of the intestinal endocannabinoid system in celiac disease and in methotrexate-treated rats. J Mol Med 85:523-530.
D’Argenio G, Valenti M, Scaglione G, Cosenza V, Sorrentini I, Di Marzo V (2006) Up-regulation of anandamide levels as an endogenous mechanism and a pharmacological strategy to limit colon inflammation. FASEB J 20:568-570.
De Filippis D, Esposito G, Cirillo C, Cipriano M, De Winter BY, Scuderi C, Sarnelli G, Cuomo R, Steardo L, De Man JG, Iuvone T (2011) Cannabidiol reduces intestinal inflammation through the control of neuroimmune axis. PLoS ONE 6:e28159.
de Mello SchierR, de Oliveira Ribeiro NP, Coutinho SD, Machado S, Arias-Carrion O, Crippa JA, Zuardi AW, Nardi AE, Silva A (2014) Antidepressant-like and anxiolytic-like effects of cannabidiol: a chemical compound of Cannabis sativa. CNS Neurol Disord Drug Targets 13:953-960.
de Ternay J, Naassila M, Nourredine M, Louvet A, Bailly F, Sescousse G, Maurage P, Cottencin O, Carrieri P, RollandB (2019) Therapeutic prospects of cannabidiol for alcohol use disorder and alcohol-related damages on the liver and the brain. Front Pharmacol 10:1-11.
Deutsch DG (2016) A personal retrospective: elevating anandamide (AEA) by targeting fatty acid amide hydrolase (FAAH) and the fatty acid binding proteins (FABPs). Front Pharmacol 7:1-7.
Donvito G, Nass SR, Wilkerson JL, Curry ZA, Schurman LD, Kinsey SG, Lichtman AH (2018) The endogenous cannabinoid system: a budding source of targets for treating inflammatory and neuropathic pain. Neuropsychopharmacology 43:52-79.
dos Santos RG, Hallak JEC, Zuardi AW, de Souza Crippa JA (2017) Cannabidiol for the treatment of drug use disorders. In Handbook of Cannabis and Related Pathologies: Biology, Pharmacology, Diagnosis, and Treatment (Preedy VR), Elsevier Inc, Cambridge, MA.
Dutra L, Stathopoulou G, Basden SL, Leyro TM, Powers MB, Otto MW (2008) A meta-analytic review of psychosocial interventions for substance use disorders. Am J Psychiatry 165:179-187.
Elmes MW, Kaczocha M, Berger WT, Leung K, Ralph BP, Wang L, Sweeney JM, Miyauchi JT, Tsirka SE, Ojima I, Deutsch DG (2015) Fatty acid-binding proteins (FABPs) are intracellular carriers for Δ9-tetrahydrocannabinol (THC) and cannabidiol (CBD). J Biol Chem 290:8711-8721.
Engen PA, Green SJ, Voigt RM, Forsyth CB, Keshavarzian A (2015) The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res 37:223-36.
Englund A, Morrison PD, Nottage J, Hague D, Kane F, Bonaccorso S, Stone JM, Reichenberg A, Brenneisen R, Holt D, Feilding A, Walker L, Murray RM, Kapur S (2013) Cannabidiol inhibits THC-elicited paranoid symptoms and hippocampal-dependent memory impairment. J Psychopharmacol 27:19-27.
Esposito G, Scuderi C, Savani C, Steardo L, De Filippis D, Cottone P, Iuvone T, Cuomo V (2007) Cannabidiol in vivo blunts b-amyloid induced neuroinflammation by suppressing IL-1b and iNOS expression. Br J Pharmacol 151:1272-1279.
Fernández Ó (2016) THC:CBD in daily practice: available data from UK, Germany and Spain. Eur Neurol 75:1-3.
Fernández-Ruiz J, Pazos MR, García-Arencibia M, Sagredo O, Ramos JA (2008) Role of CB 2 receptors in neuroprotective effects of cannabinoids. Mol Cell Endocrinol 286:91-96.
Fitzcharles M-A, Ste-Marie PA, Häuser W, Clauw DJ, Jamal S, Karsh J, Landry T, Leclercq S, Mcdougall JJ, Shir Y, Shojania K, Walsh Z (2016) Efficacy, tolerability, and safety of cannabinoid treatments in the rheumatic diseases: a systematic review of randomized controlled trials. Arthritis Care Res (Hoboken) 68:681-688.
Forsythe P, Bienenstock J, Kunze WA (2014) Vagal Pathways for Microbiome-Brain-Gut Axis Communication, pp 115-133. Springer, New York, NY.
Foster JA, Mcvey Neufeld K-A (2013) Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305-312.
Fouad AA, Jresat I (2011) Therapeutic potential of cannabidiol against ischemia/reperfusion liver injury in rats. Eur J Pharmacol 670:216-223.
Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066.
Glass M,Dragunow M, Faull RLM (1997) Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 77:299-318.
Gonzalez-Cuevas G, Martin-Fardon R, Kerr TM, Stouffer DG, Parsons LH, Hammell DC, Banks SL, Stinchcomb AL, Weiss F (2018) Unique treatment potential of cannabidiol for the prevention of relapse to drug use: preclinical proof of principle. Neuropsychopharmacology 43:2036-2045.
Gorky J, Schwaber J (2016) The role of the gut-brain axis in alcohol use disorders. Prog Neuropsychopharmacol Biol Psychiatry 65:234-241.
Goyal H, Guerreso K, Smith B, Harper K, Patel S, Patel A, Parikh P (2017) Severity and outcomes of acute alcoholic pancreatitis in cannabis users. Transl Gastroenterol Hepatol 2:1-8.
Grant BF, Chou SP, Saha TD, Pickering RP, Kerridge BT, Ruan WJ, Huang B, Jung J, Zhang H, Fan A, Hasin DS (2017) Prevalence of 12-month alcohol use, high-risk drinking, and DSM-IV alcohol use disorder in the United States, 2001-2002 to 2012-2013. JAMA Psychiatry 74:911-923.
Guindon J, Hohmann AG (2009) The endocannabinoid system and pain. CNS Neurol Disord Drug Targets 8:403-421.
Gyires K, Zádori ZS (2016) Role of cannabinoids in gastrointestinal mucosal defense and inflammation. Curr Neuropharmacol 14:935-951.
Hamelink C, Hampson A, Wink DA, Eiden LE, Eskay RL (2005) Comparison of cannabidiol, antioxidants, and diuretics in reversing binge ethanol-induced neurotoxicity. J Pharmacol Exp Ther 314:780-788.
Heishman SJ, Huestis MA, Henningfield JE, Cone EJ (1990) Acute and residual effects of marijuana: profiles of plasma THC levels, physiological, subjective, and performance measures. Pharmacol Biochem Behav 37:561-565.
Hinds NM, Ullrich K, Smid SD (2006) Cannabinoid 1 (CB1) receptors coupled to cholinergic motorneurones inhibit neurogenic circular muscle contractility in the human colon. Br J Pharmacol 148:191-199.
Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
Hungund BL, Szakall I, Adam A, Basavarajappa BS, Vadasz C (2003) Cannabinoid CB1 receptor knockout mice exhibit markedly reduced voluntary alcohol consumption and lack alcohol-induced dopamine release in the nucleus accumbens. J Neurochem 84:698-704.
Hurd YL (2017) Cannabidiol: swinging the marijuana pendulum from ‘Weed’ to medication to treat the opioid epidemic. Trends Neurosci 40:124-127.
Hurd YL, Yoon M, Manini AF, Hernandez S, Olmedo R, Ostman M, Jutras-Aswad D (2015) Early phase in the development of cannabidiol as a treatment for addiction: opioid relapse takes initial center stage. Neurotherapeutics 12:807-815.
Ilgen MA, Bohnert K, Kleinberg F, Jannausch M, Bohnert ASB, Walton M, Blow FC (2013) Characteristics of adults seeking medical marijuana certification. Drug Alcohol Depend 132:654-659.
Izzo AA, Borrelli F, Capasso R, Di Marzo V, Mechoulam R (2009) Non-psychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb. Trends Pharmacol Sci 30:515-527.
Izzo AA, Fezza F, Capasso R, Bisogno T, Pinto L, Iuvone T, Esposito G, Mascolo N, Di Marzo V, Capasso F (2001b) Cannabinoid CB1-receptor mediated regulation of gastrointestinal motility in mice in a model of intestinal inflammation. Br J Pharmacol 134:563-570.
Izzo A, Mascolo N, Capasso F (2001a) The gastrointestinal pharmacology of cannabinoids. Curr Opin Pharmacol 1:597-603.
Izzo AA, Sharkey KA (2010) Cannabinoids and the gut: New developments and emerging concepts. Pharmacol Ther 126:21-38.
Jonas DE, Amick HR, Feltner C, Bobashev G, Thomas K, Wines R, Kim MM, Shanahan E, Gass CE, Rowe CJ, Garbutt JC (2014) Pharmacotherapy for adults with alcohol use disorders in outpatient settings. JAMA 311:1889-1900.
Julien B, Ichigotani Y, Zimmer A, Tran-Van-Nhieu J, Teixeira-Clerc F, Lotersztajn S, Karsak M, Mallat A, Manin S, Deveaux V (2007) CB2 receptors as new therapeutic targets for liver diseases. Br J Pharmacol 153:286-289.
Karoly HC, Bidwell LC, Mueller RL, Hutchison KE (2018) Investigating the relationships between alcohol consumption, cannabis use, and circulating cytokines: a preliminary analysis. Alcohol Clin Exp Res 42:531-539.
Kelaï S, Hanoun N, Aufrère G, Beaugé F, Hamon M, Lanfumey L (2006) Cannabinoid-serotonin interactions in alcohol-preferring vs. alcohol-avoiding mice. J Neurochem 99:308-320.
Kelly JR, Kennedy PJ, Cryan JF, Dinan TG, Clarke G, Hyland NP (2015) Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci 9:1-20.
Kimball ES, Schneider CR, Wallace NH, Hornby PJ (2006) Agonists of cannabinoid receptor 1 and 2 inhibit experimental colitis induced by oil of mustard and by dextran sulfate sodium. Am J Physiol Liver Physiol 291:G364-G371.
Klein TW, Cabral GA (2006) Cannabinoid-induced immune suppression and modulation of antigen-presenting cells. J Neuroimmune Pharmacol 1:50-64.
Klein TW, Newton CA, Widen R, Friedman H (1985) The effect of delta-9-tetrahydrocannabinol and 11-hydroxy-delta-9-tetrahydrocannabinol on T-lymphocyte and B-lymphocyte mitogen responses. J Immunopharmacol 7:451-466.
Koob GF (1992) Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13:177-184.
Laprairie RB, Bagher AM, Kelly MEM, Denovan-Wright EM, Denovan-Wright EM (2015) Cannabidiol is a negative allosteric modulator of the cannabinoid CB 1 receptor. Br J Pharmacol 172:4790-4805.
Larsson A, Engel JA (2004) Neurochemical and behavioral studies on ethanol and nicotine interactions. Neurosci Biobehav Rev 27:713-720.
Leclercq S, Cani PD, Neyrinck AM, Stärkel P, Jamar F, Mikolajczak M, Delzenne NM, de Timary P (2012) Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects. Brain Behav Immun 26:911-918.
Leclercq S, de Timary P, Delzenne NM, Stärkel P (2017) The link between inflammation, bugs, the intestine and the brain in alcohol dependence. Transl Psychiatry 7:e1048-e1048.
Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, Windey K, Tremaroli V, Bäckhed F, Verbeke K (2014a) Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci 111:E4485-E4493.
Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, Windey K, Tremaroli V, Bäckhed F, Verbeke K, de Timary P, Delzenne NM (2014b) Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci USA 111:E4485-E4493.
Lee Y-K, Park S-W, Kim Y-K, Kim D-J, Jeong J, Myrick H, Kim Y-H (2005) Effects of naltrexone on the ethanol-induced changes in the rat central dopaminergic system. Alcohol Alcohol 40:297-301.
Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, Pierre JF, Heneghan AF, Nadimpalli A, Hubert N, Zale E, Wang Y, Huang Y, Theriault B, Dinner AR, Musch MW, Kudsk KA, Prendergast BJ, Gilbert JA, Chang EB (2015) Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17:681-689.
Li Y, Hao Y, Fan F, Zhang B (2018) The role of microbiome in insomnia, circadian disturbance and depression. Front Psychiatry 9:1-11.
Lim MP, Devi LA, Rozenfeld R (2011) Cannabidiol causes activated hepatic stellate cell death through a mechanism of endoplasmic reticulum stress-induced apoptosis. Cell Death Dis 2:e170.
Liput DJ, Hammell DC, Stinchcomb AL, Nixon K (2013) Transdermal delivery of cannabidiol attenuates binge alcohol-induced neurodegeneration in a rodent model of an alcohol use disorder. Pharmacol Biochem Behav 111:120-127.
Liu J, Bátkai S, Pacher P, Harvey-White J, Wagner JA, Cravatt BF, Gao B, Kunos G (2003) Lipopolysaccharide induces anandamide synthesis in macrophages via CD14/MAPK/phosphoinositide 3-kinase/NF-κB independently of platelet-activating factor. J Biol Chem 278:45034-45039.
Liu Z, Zhou J, Li Y, Hu F, Lu Y, Ma M, Feng Q, Zhang J, Wang D, Zeng J, Bao J, Kim J-Y, Chen Z-F, El Mestikawy S, Luo M (2014) Dorsal raphe neurons signal reward through 5-HT and glutamate. Neuron 81:1360-1374.
Lukas SE, Orozco S (2001) Ethanol increases plasma Δ9-tetrahydrocannabinol (THC) levels and subjective effects after marihuana smoking in human volunteers. Drug Alcohol Depend 64:143-149.
Mackie K (2005) Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb Exp Pharmacol 168:299-325.
Maes M, Kubera M, Leunis J-C, Berk M (2012) Increased IgA and IgM responses against gut commensals in chronic depression: Further evidence for increased bacterial translocation or leaky gut. J Affect Disord 141:55-62.
Malaguarnera G, Giordano M, Nunnari G, Bertino G, Malaguarnera M (2014) Gut microbiota in alcoholic liver disease: pathogenetic role and therapeutic perspectives. World J Gastroenterol 20:16639-16648.
Malan-Muller S, Valles-Colomer M, Raes J, Lowry CA, Seedat S, Hemmings SMJ (2018) The gut microbiome and mental health: implications for anxiety- and trauma-related disorders. Omi A J Integr Biol 22:90-107.
Malfait AM, Gallily R, Sumariwalla PF, Malik AS, Andreakos E, Mechoulam R, Feldmann M (2000) The nonpsychoactive cannabis constituent cannabidiol is an oral anti-arthritic therapeutic in murine collagen-induced arthritis. Proc Natl Acad Sci 97:9561-9566.
Martín-Moreno AM, Reigada D, Ramírez BG, Mechoulam R, Innamorato N, Cuadrado A, de Ceballos ML (2011) Cannabidiol and other cannabinoids reduce microglial activation in vitro and in vivo: relevance to Alzheimer’s disease. Mol Pharmacol 79:964-973.
Massa F, Marsicano G, Hermann H, Cannich A, Monory K, Cravatt BF, Ferri G-L, Sibaev A, Storr M, Lutz B (2004) The endogenous cannabinoid system protects against colonic inflammation. J Clin Invest 113:1202-1229.
Massa F, Monory K (2006) Endocannabinoids and the gastrointestinal tract. J Endocrinol Invest 29:47-57.
Mayer EA, Tillisch K, Gupta A (2015) Gut/brain axis and the microbiota. J Clin Invest 125:926-938.
Mayfield J, Ferguson L, Harris RA (2013) Neuroimmune signaling: a key component of alcohol abuse. Curr Opin Neurobiol 23:513-520.
McCoy KL (2016) Interaction between cannabinoid system and toll-like receptors controls inflammation. Mediators Inflamm 2016:1-18.
McCoy KL, Gainey D, Cabral GA (1995) delta 9-Tetrahydrocannabinol modulates antigen processing by macrophages. J Pharmacol Exp Ther 273:1216-1223.
Mecha M, Feliú A, Iñigo PM, Mestre L, Carrillo-Salinas FJ, Guaza C (2013) Cannabidiol provides long-lasting protection against the deleterious effects of inflammation in a viral model of multiple sclerosis: A role for A 2A receptors. Neurobiol Dis 59:141-150.
Mehrpouya-Bahrami P, Chitrala KN, Ganewatta MS, Tang C, Murphy EA, Enos RT, Velazquez KT, McCellan J, Nagarkatti M, Nagarkatti P (2017) Blockade of CB1 cannabinoid receptor alters gut microbiota and attenuates inflammation and diet-induced obesity. Sci Rep 7:1-16.
Montesinos J, Alfonso-Loeches S, Guerri C (2016) Impact of the innate immune response in the actions of ethanol on the central nervous system. Alcohol Clin Exp Res 40:2260-2270.
Morgan CJA, Gardener C, Schafer G, Swan S, Demarchi C, Freeman TP, Warrington P, Rupasinghe I, Ramoutar A, Tan N, Wingham G, Lewis S, Curran HV (2012) Sub-chronic impact of cannabinoids in street cannabis on cognition, psychotic-like symptoms and psychological well-being. Psychol Med 42:391-400.
Muccioli GG, Naslain D, Bäckhed F, Reigstad CS, Lambert DM, Delzenne NM, Cani PD (2010) The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol 6:1-15.
Mukhopadhyay P, Rajesh M, Horváth B, Bátkai S, Park O, Tanchian G, Gao RY, Patel V, Wink DA, Liaudet L, Haskó G, Mechoulam R, Pacher P (2011) Cannabidiol protects against hepatic ischemia/reperfusion injury by attenuating inflammatory signaling and response, oxidative/nitrative stress, and cell death. Free Radic Biol Med 50:1368-1381.
Musella A, Fresegna D, Rizzo FR, Gentile A, Bullitta S, De Vito F, Guadalupi L, Centonze D, Mandolesi G (2017) A novel crosstalk within the endocannabinoid system controls GABA transmission in the striatum. Sci Rep 7:1-8.
Mutlu EA, Gillevet PM, Rangwala H, Sikaroodi M, Naqvi A, Engen PA, Kwasny M, Lau CK, Keshavarzian A (2012) Colonic microbiome is altered in alcoholism. Am J Physiol Liver Physiol 302:G966-G978.
Naftali T, Schleider LB-L, Dotan I, Lansky EP, Sklerovsky Benjaminov F, Konikoff FM (2013) Cannabis induces a clinical response in patients with Crohn’s disease: a prospective placebo-controlled study. Clin Gastroenterol Hepatol 11:1276-1280.e1.
Nagarkatti P, Pandey R, Rieder SA, Hegde VL, Nagarkatti M (2009) Cannabinoids as novel anti-inflammatory drugs. Futur Med Chem 1:1333-1349.
Neelakantan H, Tallarida RJ, Reichenbach ZW, Tuma RF, Ward SJ, Walker EA (2015) Distinct interactions of cannabidiol and morphine in three nociceptive behavioral models in mice. Behav Pharmacol 26:304-314.
Niesink RJM, van Laar MW (2013) Does cannabidiol protect against adverse psychological effects of THC? Front Psychiatry 4:1-8.
Oláh A, Szekanecz Z, Bíró T (2017) Targeting cannabinoid signaling in the immune system: “High”-ly exciting questions, possibilities, and challenges. Front Immunol 8:1-14.
Oliva JM, Ortiz S, Pérez-Rial S, Manzanares J (2008) Time dependent alterations on tyrosine hydroxylase, opioid and cannabinoid CB1 receptor gene expressions after acute ethanol administration in the rat brain. Eur Neuropsychopharmacol 18:373-382.
Ortiz J, Fitzgerald LW, Charlton M, Lane S, Trevisan L, Guitart X, Shoemaker W, Duman RS, Nestler EJ (1995) Biochemical actions of chronic ethanol exposure in the mesolimbic dopamine system. Synapse 21:289-298.
Pandey R, Mousawy K, Nagarkatti M, Nagarkatti P (2009) Endocannabinoids and immune regulation. Pharmacol Res 60:85-92.
Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, Collins SM (2013) Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil 25:733-e575.
Parlesak A, Schäfer C, Schütz T, Bode JC, Bode C (2000) Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol 32:742-747.
Parsons LH, Hurd YL (2015) Endocannabinoid signalling in reward and addiction. Nat Rev Neurosci 16:579-594.
Pascual M, Baliño P, Alfonso-Loeches S, Aragón CMG, Guerri C (2011) Impact of TLR4 on behavioral and cognitive dysfunctions associated with alcohol-induced neuroinflammatory damage. Brain Behav Immun 25:S80-S91.
Pertwee RG (2004a) The pharmacology and therapeutic potential of cannabidiol.
Pertwee RG (2004b) Pharmacological and therapeutic targets for ∆9-tetrahydrocannabinol and cannabidiol. Euphytica 140:73-82.
Pertwee RG (2008) The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: Δ9-tetrahydrocannabinol, cannabidiol and Δ9-tetrahydrocannabivarin. Br J Pharmacol 153:199-215.
Pertwee R (2014) Handbook of Cannabis. Oxford University Press, Oxford.
Petra AI, Panagiotidou S, Hatziagelaki E, Stewart JM, Conti P, Theoharides TC (2015) Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther 37:984-995.
Prud'homme M, Cata R, Jutras-Aswad D (2015) Cannabidiol as an intervention for addictive behaviors: a systematic review of the evidence. Subst Abus Res Treat 9:SART.S25081.
Puffenbarger RA, Boothe AC, Cabral GA (2000) Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia 29:58-69.
Pusceddu MM, Gareau MG (2018) Visceral pain: gut microbiota, a new hope? J Biomed Sci 25:1-8.
Qin L, Crews FT (2012) NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration. J Neuroinflammation 9:1-19.
Ramaekers JG, Theunissen EL, de Brouwer M, Toennes SW, Moeller MR, Kauert G (2011) Tolerance and cross-tolerance to neurocognitive effects of THC and alcohol in heavy cannabis users. Psychopharmacology 214:391-401.
Richards BL, Whittle SL, Buchbinder R (2012) Neuromodulators for pain management in rheumatoid arthritis. Cochrane Database Syst Rev 1:CD008921.
Roberto M, Cruz M, Bajo M, Siggins GR, Parsons LH, Schweitzer P (2010) The endocannabinoid system tonically regulates inhibitory transmission and depresses the effect of ethanol in central amygdala. Neuropsychopharmacology 35:1962-1972.
Roche M, Diamond M, Kelly JP, Finn DP (2006) In vivo modulation of LPS-induced alterations in brain and peripheral cytokines and HPA axis activity by cannabinoids. J Neuroimmunol 181:57-67.
Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, Hauschildt S (2011) LPS-induced cytokine production in human monocytes and macrophages. Crit Rev Immunol 31:379-446.
Russo EB, Burnett A, Hall B, Parker KK (2005) Agonistic properties of cannabidiol at 5-HT1a receptors. Neurochem Res 30:1037-1043.
Russo R, Cristiano C, Avagliano C, De Caro C, La Rana G, Raso GM, Canani RB, Meli R, Calignano A (2018) Gut-brain axis: role of lipids in the regulation of inflammation, pain and CNS diseases. Curr Med Chem 25:3930-3952.
Ryberg E, Larsson N, Sjögren S, Hjorth S, Hermansson N-O, Leonova J, Elebring T, Nilsson K, Drmota T, Greasley PJ (2007) The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152:1092-1101.
Serrano A, Rivera P, Pavon FJ, Decara J, Suárez J, Rodriguez de Fonseca F, Parsons LH (2012) Differential effects of single versus repeated alcohol withdrawal on the expression of endocannabinoid system-related genes in the rat amygdala. Alcohol Clin Exp Res 36:984-994.
Shoskes DA, Wang H, Polackwich AS, Tucky B, Altemus J, Eng C (2016) Analysis of gut microbiome reveals significant differences between men with chronic prostatitis/chronic pelvic pain syndrome and controls. J Urol 196:435-441.
Skewes MC, Gonzalez VM (2013) The biopsychosocial model of addiction. Princ Addict 1:61-70.
Sloan ME, Gowin JL, Ramchandani VA, Le Foll B (2017) The endocannabinoid system as a target for addiction treatment: Trials and tribulations. Neuropharmacology 124:73-83.
Snedecor SJ, Sudharshan L, Cappelleri JC, Sadosky A, Desai P, Jalundhwala YJ, Botteman M (2013) Systematic review and comparison of pharmacologic therapies for neuropathic pain associated with spinal cord injury. J Pain Res 6:539-547.
Söderpalm B, Ericson M (2011) Neurocircuitry Involved in the Development of Alcohol Addiction: The Dopamine System and its Access Points, pp 127-161. Springer, Berlin, Heidelberg.
Spanagel R, Weiss F (1999) The dopamine hypothesis of reward: past and current status. Trends Neurosci 22:521-527.
Stahre M, Roeber J, Kanny D, Brewer RD, Zhang X (2014) Peer reviewed: contribution of excessive alcohol consumption to deaths and years of potential life lost in the United States. Prev Chronic Dis 11:E109.
Storr MA, Keenan CM, Emmerdinger D, Zhang H, Yüce B, Sibaev A, Massa F, Buckley NE, Lutz B, Göke B, Brand S, Patel KD, Sharkey KA (2008a) Targeting endocannabinoid degradation protects against experimental colitis in mice: involvement of CB1 and CB2 receptors. J Mol Med 86:925-936.
Storr MA, Sharkey KA (2007) The endocannabinoid system and gut-brain signalling. Curr Opin Pharmacol 7:575-582.
Storr MA, Yüce B, Andrews CN, Sharkey KA (2008b) The role of the endocannabinoid system in the pathophysiology and treatment of irritable bowel syndrome. Neurogastroenterol Motil 20:857-868.
Szabo G (2015) Gut-liver axis in alcoholic liver disease. Gastroenterology 148:30-36.
Talani G, Lovinger DM (2015) Interactions between ethanol and the endocannabinoid system at GABAergic synapses on basolateral amygdala principal neurons. Alcohol 49:781-794.
Thomas A, Baillie GL, Phillips AM, Razdan RK, Ross RA, Pertwee RG (2007) Cannabidiol displays unexpectedly high potency as an antagonist of CB 1 and CB 2 receptor agonists in vitro. Br J Pharmacol 150:613-623.
Trautmann SM, Sharkey KA (2015) The endocannabinoid system and its role in regulating the intrinsic neural circuitry of the gastrointestinal tract. Int Rev Neurobiol 125:85-126.
Turcotte C, Chouinard F, Lefebvre JS, Flamand N (2015) Regulation of inflammation by cannabinoids, the endocannabinoids 2-arachidonoyl-glycerol and arachidonoyl-ethanolamide, and their metabolites. J Leukoc Biol 97:1049-1070.
Turna J, Syan SK, Frey BN, Rush B, Costello MJ, Weiss M, MacKillop J (2019) Cannabidiol as a novel candidate alcohol use disorder pharmacotherapy: a systematic review. Alcohol Clin Exp Res 43:550-563.
Urits I, Borchart M, Hasegawa M, Kochanski J, Orhurhu V, Viswanath O (2019) An update of current cannabis-based pharmaceuticals in pain medicine. Pain Ther 8:41-51.
Vann RE, Gamage TF, Warner JA, Marshall EM, Taylor NL, Martin BR, Wiley JL (2008) Divergent effects of cannabidiol on the discriminative stimulus and place conditioning effects of Δ9-tetrahydrocannabinol. Drug Alcohol Depend 94:191-198.
Vanuytsel T, van Wanrooy S, Vanheel H, Vanormelingen C, Verschueren S, Houben E, Salim Rasoel S, Tόth J, Holvoet L, Farré R, Van Oudenhove L, Boeckxstaens G, Verbeke K, Tack J (2014) Psychological stress and corticotropin-releasing hormone increase intestinal permeability in humans by a mast cell-dependent mechanism. Gut 63:1293-1299.
Varga K, Wagner JA, Bridgen DT, Kunos G (1998) Platelet- and macrophage-derived endogenous cannabinoids are involved in endotoxin-induced hypotension. FASEB J 12:1035-1044.
Viudez-Martínez A, García-Gutiérrez MS, Fraguas-Sánchez AI, Torres-Suárez AI, Manzanares J (2018a) Effects of cannabidiol plus naltrexone on motivation and ethanol consumption. Br J Pharmacol 175:3369-3378.
Viudez-Martínez A, García-Gutiérrez MS, Navarrón CM, Morales-Calero MI, Navarrete F, Torres-Suárez AI, Manzanares J (2018b) Cannabidiol reduces ethanol consumption, motivation and relapse in mice. Addict Biol 23:154-164.
Volkow ND, Baler RD (2014) Addiction science: Uncovering neurobiological complexity. Neuropharmacology 76:235-249.
Wang HJ, Zakhari S, Jung MK (2010) Alcohol, inflammation, and gut-liver-brain interactions in tissue damage and disease development. World J Gastroenterol WJG 16:1304-1313.
Wang Y, Mukhopadhyay P, Cao Z, Wang H, Feng D, Haskó G, Mechoulam R, Gao B, Pacher P (2017) Cannabidiol attenuates alcohol-induced liver steatosis, metabolic dysregulation, inflammation and neutrophil-mediated injury. Sci Rep 7:1-12.
Whiting PF, Wolff RF, Deshpande S, Di Nisio M, Duffy S, Hernandez AV, Keurentjes JC, Lang S, Misso K, Ryder S, Schmidlkofer S, Westwood M, Kleijnen J (2015) Cannabinoids for medical use. JAMA 313:2456-2473.
Wiley NC, Dinan TG, Ross RP, Stanton C, Clarke G, Cryan JF (2017) The microbiota-gut-brain axis as a key regulator of neural function and the stress response: Implications for human and animal health1,2. J Anim Sci 95:3225-3246.
Wright K, Rooney N, Feeney M, Tate J, Robertson D, Welham M, Ward S (2005) Differential expression of cannabinoid receptors in the human colon: cannabinoids promote epithelial wound healing. Gastroenterology 129:437-453.
Yang L, Rozenfeld R, Wu D, Devi LA, Zhang Z, Cederbaum A (2014) Cannabidiol protects liver from binge alcohol-induced steatosis by mechanisms including inhibition of oxidative stress and increase in autophagy. Free Radic Biol Med 68:260-267.
Yuan M, Kiertscher SM, Cheng Q, Zoumalan R, Tashkin DP, Roth MD (2002) D9-tetrahydrocannabinol regulates Th1/Th2 cytokine balance in activated human T cells. J Neuroimmunol 133:124-131.
Zhornitsky S, Potvin S (2012) Cannabidiol in humans-the quest for therapeutic targets. Pharmaceuticals 5:529-552.
Zhu X, Han Y, Du J, Liu R, Jin K, Yi W (2017) Microbiota-gut-brain axis and the central nervous system. Oncotarget 8:53829-53838.

Auteurs

Hollis C Karoly (HC)

Institute of Cognitive Science, University of Colorado Boulder, Boulder, Colorado.

Raeghan L Mueller (RL)

Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, Colorado.

L Cinnamon Bidwell (LC)

Institute of Cognitive Science, University of Colorado Boulder, Boulder, Colorado.
Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, Colorado.

Kent E Hutchison (KE)

Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, Colorado.

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