Oxidative Stress and the Combined Use of Tetrahydrocannabinol and Alcohol: Is There a Need for Further Research?

  1. López-Malo, Daniel 1
  2. Sanchez-Martinez, Juan 1
  3. Romero, Francisco 1
  4. Barcia, Jorge 1
  5. Villar, Vincent 2
  1. 1 Universidad Católica de Valencia San Vicente Mártir
    info

    Universidad Católica de Valencia San Vicente Mártir

    Valencia, España

    ROR https://ror.org/03d7a9c68

  2. 2 Universidad CEU Cardenal Herrera
    info

    Universidad CEU Cardenal Herrera

    Valencia, España

    ROR https://ror.org/01tnh0829

Revista:
Reactive Oxygen Species

Año de publicación: 2016

Volumen: 2

Número: 6

Páginas: 388–395

Tipo: Artículo

DOI: 10.20455/ROS.2016.869 GOOGLE SCHOLAR lock_openAcceso abierto editor

Resumen

Cannabis sativa is a plant that produces, among other cannabinoids, the psychoactive Δ-9-tetrahydrocannabinol (THC), whose adverse health effects have been recently reviewed. Repeated doses of THC lead to the development of tolerance to its own effects and the effects of other cannabinoids, and affect the same reward systems as alcohol, cocaine, and opioids. Enhanced brain oxidative stress usually correlates with cognitive impairment and a higher risk of development of neurodegenerative diseases, which has been repeatedly reported for many conditions. THC-induced cognitive effects are aggravated by the combined use of alcohol. Some research suggests similar mechanistic aspects of THC and alcohol on brain mitochondrial oxidative damage. Taking THC and ethanol together represents a greater risk for cognitive and attention impairment than taking either drug separately. While THC and ethanol exposure elevates reactive oxygen species in many tissues including the brain, further research is needed to establish a deleterious role of oxidative stress in the nervous system subjected to both compounds.

Referencias bibliográficas

  • European Monitoring Centre for Drugs and Drug Addiction. European Drug Report 2016: Trends and Developments. Luxembourg. 2016.
  • Volkow ND, Baler RD, Compton WM, Weiss SR. Adverse health effects of marijuana use. N Engl J Med 2014; 370(23):2219‒27. doi: 10.1056/NEJMra1402309.
  • Mechoulam R, Gaoni Y. The absolute configuration of delta-1-tetrahydrocannabinol, the major active constituent of hashish. Tetrahedron Lett 1967; 12:1109‒11.
  • McLaren J, Swift W, Dillon P, Allsop S. Cannabis potency and contamination: a review of the literature. Addiction 2008; 103(7):1100‒9. doi: 10.1111/j.1360-0443.2008.02230.x.
  • Pertwee RG. The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9-tetrahydrocannabivarin. Br J Pharmacol 2008; 153(2):199‒215. doi: 10.1038/sj.bjp.0707442.
  • Glass M, Dragunow M, Faull RL. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1997; 77(2):299‒318.
  • Cadet JL, Bisagno V, Milroy CM. Neuropathology of substance use disorders. Acta Neuropathol 2014; 127(1):91‒107. doi: 10.1007/s00401-013-1221-7.
  • Hall W, Solowij N. Adverse effects of cannabis. Lancet 1998; 352(9140):1611‒6. doi: 10.1016/S0140-6736(98)05021-1.
  • Fouad AA, Albuali WH, Al-Mulhim AS, Jresat I. Cardioprotective effect of cannabidiol in rats exposed to doxorubicin toxicity. Environ Toxicol Pharmacol 2013; 36(2):347‒57. doi: 10.1016/j.etap.2013.04.018.
  • Mecha M, Torrao AS, Mestre L, Carrillo-Salinas FJ, Mechoulam R, Guaza C. Cannabidiol protects oligodendrocyte progenitor cells from inflammation-induced apoptosis by attenuating endoplasmic reticulum stress. Cell Death Dis 2012; 3:e331. doi: 10.1038/cddis.2012.71.
  • Wolff V, Schlagowski AI, Rouyer O, Charles AL, Singh F, Auger C, et al. Tetrahydrocannabinol induces brain mitochondrial respiratory chain dysfunction and increases oxidative stress: a potential mechanism involved in cannabis-related stroke. Biomed Res Int 2015; 2015:323706. doi: 10.1155/2015/323706.
  • The World Health Organization. Alcohol: Fact Sheet. 2015. http://www.who.int/mediacentre/factsheets/fs349/en/ (accessed on June 29, 2016).
  • Roman PM. Seventy-five years of policy on alcohol problems: an American perspective. J Stud Alcohol Drugs Suppl 2014; 75 Suppl 17:116‒24.
  • Guo R, Ren J. Alcohol and acetaldehyde in public health: from marvel to menace. Int J Environ Res Public Health 2010; 7(4):1285‒301. doi: 10.3390/ijerph7041285.
  • Parolini M, Binelli A. Oxidative and genetic responses induced by Delta-9-tetrahydrocannabinol (Delta-9-THC) to Dreissena polymorpha. Sci Total Environ 2014; 468‒469:68‒76. doi: 10.1016/j.scitotenv.2013.08.024.
  • Muntoni AL, Pillolla G, Melis M, Perra S, Gessa GL, Pistis M. Cannabinoids modulate spontaneous neuronal activity and evoked inhibition of locus coeruleus noradrenergic neurons. Eur J Neurosci 2006; 23(9):2385‒94. doi: 10.1111/j.1460-9568.2006.04759.x.
  • Robledo P, Trigo JM, Panayi F, de la Torre R, Maldonado R. Behavioural and neurochemical effects of combined MDMA and THC administration in mice. Psychopharmacology (Berl) 2007; 195(2):255‒64. doi: 10.1007/s00213-007-0879-8.
  • Bossong MG, van Berckel BN, Boellaard R, Zuurman L, Schuit RC, Windhorst AD, et al. Delta 9-tetrahydrocannabinol induces dopamine release in the human striatum. Neuropsychopharmacology 2009; 34(3):759‒66. doi: 10.1038/npp.2008.138.
  • Antunes F, Han D, Rettori D, Cadenas E. Mitochondrial damage by nitric oxide is potentiated by dopamine in PC12 cells. Biochim Biophys Acta 2002; 1556(2‒3):233‒8.
  • Juarez Olguin H, Calderon Guzman D, Hernandez Garcia E, Barragan Mejia G. The Role of dopamine and its dysfunction as a consequence of oxidative stress. Oxid Med Cell Longev 2016; 2016:9730467. doi: 10.1155/2016/9730467.
  • Rubino T, Parolaro D. Long lasting consequences of cannabis exposure in adolescence. Mol Cell Endocrinol 2008; 286(1‒2 Suppl 1):S108‒13. doi: 10.1016/j.mce.2008.02.003.
  • Realini N, Rubino T, Parolaro D. Neurobiological alterations at adult age triggered by adolescent exposure to cannabinoids. Pharmacol Res 2009; 60(2):132‒8. doi: 10.1016/j.phrs.2009.03.006.
  • Chandra LC, Kumar V, Torben W, Vande Stouwe C, Winsauer P, Amedee A, et al. Chronic administration of Delta9-tetrahydrocannabinol induces intestinal anti-inflammatory microRNA expression during acute simian immunodeficiency virus infection of rhesus macaques. J Virol 2015; 89(2):1168‒81. doi: 10.1128/JVI.01754-14.
  • Yamaori S, Ishii H, Chiba K, Yamamoto I, Watanabe K. Delta-Tetrahydrocannabinol induces cytotoxicity in macrophage J774-1 cells: involvement of cannabinoid receptor 2 and p38 MAPK. Toxicology 2013; 314(2‒3):254‒61. doi: 10.1016/j.tox.2013.10.007.
  • Rajesh M, Mukhopadhyay P, Hasko G, Liaudet L, Mackie K, Pacher P. Cannabinoid-1 receptor activation induces reactive oxygen species-dependent and -independent mitogen-activated protein kinase activation and cell death in human coronary artery endothelial cells. Br J Pharmacol 2010; 160(3):688‒700. doi: 10.1111/j.1476-5381.2010.00712.x.
  • Juknat A, Pietr M, Kozela E, Rimmerman N, Levy R, Gao F, et al. Microarray and pathway analysis reveal distinct mechanisms underlying cannabinoid-mediated modulation of LPS-induced activation of BV-2 microglial cells. PLoS One 2013; 8(4):e61462. doi: 10.1371/journal.pone.0061462.
  • Clausen A, Doctrow S, Baudry M. Prevention of cognitive deficits and brain oxidative stress with superoxide dismutase/catalase mimetics in aged mice. Neurobiol Aging 2010; 31(3):425‒33. doi: 10.1016/j.neurobiolaging.2008.05.009.
  • Bishop NA, Lu T, Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature 2010; 464(7288):529‒35. doi: 10.1038/nature08983.
  • Grimm S, Hoehn A, Davies KJ, Grune T. Protein oxidative modifications in the ageing brain: consequence for the onset of neurodegenerative disease. Free Radic Res 2011; 45(1):73‒88. doi: 10.3109/10715762.2010.512040.
  • Gowran A, Campbell VA. A role for p53 in the regulation of lysosomal permeability by delta 9-tetrahydrocannabinol in rat cortical neurones: implications for neurodegeneration. J Neurochem 2008; 105(4):1513‒24. doi: 10.1111/j.1471-4159.2008.05278.x.
  • Costa B, Colleoni M. Changes in rat brain energetic metabolism after exposure to anandamide or Delta(9)-tetrahydrocannabinol. Eur J Pharmacol 2000; 395(1):1‒7.
  • Cederbaum AI. Introduction-serial review: alcohol, oxidative stress and cell injury. Free Radic Biol Med 2001; 31(12):1524‒6.
  • Cederbaum AI. Alcohol metabolism. Clin Liver Dis 2012; 16(4):667‒85. doi: 10.1016/j.cld.2012.08.002.
  • Bondy SC, Guo SX. Regional selectivity in ethanol-induced pro-oxidant events within the brain. Biochem Pharmacol 1995; 49(1):69‒72.
  • Bosch-Morell F, Martinez-Soriano F, Colell A, Fernandez-Checa JC, Romero FJ. Chronic ethanol feeding induces cellular antioxidants decrease and oxidative stress in rat peripheral nerves: effect of S-adenosyl-L-methionine and N-acetyl-L-cysteine. Free Radic Biol Med 1998; 25(3):365‒8.
  • Ramachandran V, Watts LT, Maffi SK, Chen J, Schenker S, Henderson G. Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons. J Neurosci Res 2003; 74(4):577‒88. doi: 10.1002/jnr.10767.
  • Sun AY, Chen YM, James-Kracke M, Wixom P, Cheng Y. Ethanol-induced cell death by lipid peroxidation in PC12 cells. Neurochem Res 1997; 22(10):1187‒92.
  • Crabb DW. Ethanol oxidizing enzymes: roles in alcohol metabolism and alcoholic liver disease. Prog Liver Dis 1995; 13:151‒72.
  • Edenberg HJ. The genetics of alcohol metabolism: role of alcohol dehydrogenase and aldehyde dehydrogenase variants. Alcohol Res Health 2007; 30(1):5‒13.
  • Riveros-Rosas H, Julian-Sanchez A, Pina E. Enzymology of ethanol and acetaldehyde metabolism in mammals. Arch Med Res 1997; 28(4):453‒71.
  • Raskin NH, Sokoloff L. Alcohol dehydrogenase activity in rat brain and liver. J Neurochem 1970; 17(12):1677‒87.
  • Zimatkin SM, Liopo AV, Deitrich RA. Distribution and kinetics of ethanol metabolism in rat brain. Alcohol Clin Exp Res 1998; 22(8):1623‒7.
  • Thurman RG, Handler JA. New perspectives in catalase-dependent ethanol metabolism. Drug Metab Rev 1989; 20(2‒4):679‒88. doi: 10.3109/03602538909103570.
  • Koop DR. Alcohol metabolism's damaging effects on the cell: a focus on reactive oxygen generation by the enzyme cytochrome P450 2E1. Alcohol Res Health 2006; 29(4):274‒80.
  • Herrera DG, Yague AG, Johnsen-Soriano S, Bosch-Morell F, Collado-Morente L, Muriach M, et al. Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci USA 2003; 100(13):7919‒24. doi: 10.1073/pnas.1230907100.
  • Johnsen-Soriano S, Bosch-Morell F, Miranda M, Asensio S, Barcia JM, Roma J, et al. Ebselen prevents chronic alcohol-induced rat hippocampal stress and functional impairment. Alcohol Clin Exp Res 2007; 31(3):486‒92. doi: 10.1111/j.1530-0277.2006.00329.x.
  • Almansa I, Fernandez A, Garcia-Ruiz C, Muriach M, Barcia JM, Miranda M, et al. Brain mitochondrial alterations after chronic alcohol consumption. J Physiol Biochem 2009; 65(3):305‒12. doi: 10.1007/BF03180583.
  • Almansa I, Barcia JM, Lopez-Pedrajas R, Muriach M, Miranda M, Romero FJ. Naltrexone reverses ethanol-induced rat hippocampal and serum oxidative damage. Oxid Med Cell Longev 2013; 2013:296898. doi: 10.1155/2013/296898.
  • Barcia JM, Flores-Bellver M, Muriach M, Sancho-Pelluz J, Lopez-Malo D, Urdaneta AC, et al. Matching diabetes and alcoholism: oxidative stress, inflammation, and neurogenesis are commonly involved. Mediators Inflamm 2015; 2015:624287. doi: 10.1155/2015/624287.
  • Miksys SL, Tyndale RF. Drug-metabolizing cytochrome P450s in the brain. J Psychiatry Neurosci 2002; 27(6):406‒15.
  • Martinez-Gil N, Flores-Bellver M, Atienzar-Aroca S, Lopez-Malo D, Urdaneta AC, Sancho-Pelluz J, et al. CYP2E1 in the human retinal pigment epithelium: expression, activity, and induction by ethanol. Invest Ophthalmol Vis Sci 2015; 56(11):6855‒63. doi: 10.1167/iovs.14-16291.
  • Simons JS, Gaher RM, Correia CJ, Hansen CL, Christopher MS. An affective-motivational model of marijuana and alcohol problems among college students. Psychol Addict Behav 2005; 19(3):326‒34. doi: 10.1037/0893-164X.19.3.326.
  • Weinberger AH, Platt J, Goodwin RD. Is cannabis use associated with an increased risk of onset and persistence of alcohol use disorders? A three-year prospective study among adults in the United States. Drug Alcohol Depend 2016; 161:363‒7. doi: 10.1016/j.drugalcdep.2016.01.014.
  • Wolff K, Johnston A. Cannabis use: a perspective in relation to the proposed UK drug-driving legislation. Drug Test Anal 2014; 6(1‒2):143‒54. doi: 10.1002/dta.1588.
  • Dubois S, Mullen N, Weaver B, Bedard M. The combined effects of alcohol and cannabis on driving: impact on crash risk. Forensic Sci Int 2015; 248:94‒100. doi: 10.1016/j.forsciint.2014.12.018.
  • Jacobus J, Squeglia LM, Meruelo AD, Castro N, Brumback T, Giedd JN, et al. Cortical thickness in adolescent marijuana and alcohol users: a three-year prospective study from adolescence to young adulthood. Dev Cogn Neurosci 2015; 16:101‒9. doi: 10.1016/j.dcn.2015.04.006.
  • Jacobus J, Squeglia LM, Bava S, Tapert SF. White matter characterization of adolescent binge drinking with and without co-occurring marijuana use: a 3-year investigation. Psychiatry Res 2013; 214(3):374‒81. doi: 10.1016/j.pscychresns.2013.07.014.
  • Squeglia LM, Sorg SF, Schweinsburg AD, Wetherill RR, Pulido C, Tapert SF. Binge drinking differentially affects adolescent male and female brain morphometry. Psychopharmacology (Berl) 2012; 220(3):529‒39. doi: 10.1007/s00213-011-2500-4.
  • Schweinsburg AD, Schweinsburg BC, Nagel BJ, Eyler LT, Tapert SF. Neural correlates of verbal learning in adolescent alcohol and marijuana users. Addiction 2011; 106(3):564‒73. doi: 10.1111/j.1360-0443.2010.03197.x.
  • Squeglia LM, Spadoni AD, Infante MA, Myers MG, Tapert SF. Initiating moderate to heavy alcohol use predicts changes in neuropsychological functioning for adolescent girls and boys. Psychol Addict Behav 2009; 23(4):715‒22. doi: 10.1037/a0016516.
  • Mahmood OM, Jacobus J, Bava S, Scarlett A, Tapert SF. Learning and memory performances in adolescent users of alcohol and marijuana: interactive effects. J Stud Alcohol Drugs 2010; 71(6):885‒94.
  • Lipina C, Hundal HS. Modulation of cellular redox homeostasis by the endocannabinoid system. Open Biol 2016; 6(4):150276. doi: 10.1098/rsob.150276.
  • Muniyappa R, Sable S, Ouwerkerk R, Mari A, Gharib AM, Walter M, et al. Metabolic effects of chronic cannabis smoking. Diabetes Care 2013; 36(8):2415‒22. doi: 10.2337/dc12-2303.
  • Borini P, Guimaraes RC, Borini SB. Possible hepatotoxicity of chronic marijuana usage. Sao Paulo Med J 2004; 122(3):110‒6. doi: /S1516-31802004000300007.