Oxidative Stress-Induced Brain Damage Triggered by Voluntary Ethanol Consumption during Adolescence: A Potential Target for Neuroprotection?

Author(s): Gustavo E. Buján, Hector A. Serra, Sonia J. Molina, Laura R. Guelman*.

Journal Name: Current Pharmaceutical Design

Volume 25 , Issue 45 , 2019

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Abstract:

Alcohol consumption, in particular ethanol (EtOH), typically begins in human adolescence, often in a “binge like” manner. However, although EtOH abuse has a high prevalence at this stage, the effects of exposure during adolescence have been less explored than prenatal or adult age exposure.

Several authors have reported that EtOH intake during specific periods of development might induce brain damage. Although the mechanisms are poorly understood, it has been postulated that oxidative stress may play a role. In fact, some of these studies revealed a decrease in brain antioxidant enzymes’ level and/or an increase in reactive oxygen species (ROS) production. Nevertheless, although existing literature shows a number of studies in which ROS were measured in developing animals, fewer reported the measurement of ROS levels after EtOH exposure in adolescence. Importantly, neuroprotective agents aimed to these potential targets may be relevant tools useful to reduce EtOH-induced neurodegeneration, restore cognitive function and improve treatment outcomes for alcohol use disorders (AUDs).

The present paper reviews significant evidences about the mechanisms involved in EtOH-induced brain damage, as well as the effect of different potential neuroprotectants that have shown to be able to prevent EtOH-induced oxidative stress. A selective inhibitor of the endocannabinoid anandamide metabolism, a flavonol present in different fruits (quercetin), an antibiotic with known neuroprotective properties (minocycline), a SOD/catalase mimetic, a potent antioxidant and anti-inflammatory molecule (resveratrol), a powerful ROS scavenger (melatonin), an isoquinoline alkaloid (berberine), are some of the therapeutic strategies that could have some clinical relevance in the treatment of AUDs. As most of these works were performed in adult animal models and using EtOH-forced paradigms, the finding of neuroprotective tools that could be effective in adolescent animal models of voluntary EtOH intake should be encouraged.

Keywords: Ethanol, behavior, oxidative stress, neuroprotection, development, adolescence.

[1]
Tan CH, Denny CH, Cheal NE, Sniezek JE, Kanny D. Alcohol use and binge drinking among women of childbearing age - United States, 2011-2013. MMWR Morb Mortal Wkly Rep 2015; 64(37): 1042-6.
[http://dx.doi.org/10.15585/mmwr.mm6437a3] [PMID: 26401713]
[2]
Hoyme HE, Kalberg WO, Elliott AJ, et al. Updated clinical guidelines for diagnosing fetal alcohol spectrum disorders. Pediatrics 2016; 138(2): e20154256.
[http://dx.doi.org/10.1542/peds.2015-4256] [PMID: 27464676]
[3]
Riley EP, Infante MA, Warren KR. Fetal alcohol spectrum disorders: an overview. Neuropsychol Rev 2011; 21(2): 73-80.
[http://dx.doi.org/10.1007/s11065-011-9166-x] [PMID: 21499711]
[4]
Murawski NJ, Moore EM, Thomas JD, Riley EP. Advances in diagnosis and treatment of fetal alcohol spectrum disorders: from animal models to human studies. Alcohol Res 2015; 37(1): 97-108.
[PMID: 26259091]
[5]
Riley EP, McGee CL. Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp Biol Med (Maywood) 2005; 230(6): 357-65.
[http://dx.doi.org/10.1177/15353702-0323006-03] [PMID: 15956765]
[6]
Squeglia LM, Pulido C, Wetherill RR, Jacobus J, Brown GG, Tapert SF. Brain response to working memory over three years of adolescence: influence of initiating heavy drinking. J Stud Alcohol Drugs 2012; 73(5): 749-60.
[http://dx.doi.org/10.15288/jsad.2012.73.749] [PMID: 22846239]
[7]
Crews F, He J, Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 2007; 86(2): 189-99.
[http://dx.doi.org/10.1016/j.pbb.2006.12.001] [PMID: 17222895]
[8]
Townshend JM, Kambouropoulos N, Griffin A, Hunt FJ, Milani RM. Binge drinking, reflection impulsivity, and unplanned sexual behavior: impaired decision-making in young social drinkers. Alcohol Clin Exp Res 2014; 38(4): 1143-50.
[http://dx.doi.org/10.1111/acer.12333] [PMID: 24428268]
[9]
Patrick ME, Terry-McElrath YM. Prevalence of high-intensity drinking from adolescence through young adulthood: national data from 2016-2017. Subst Abuse 2019; 13: 1178221818822976.
[http://dx.doi.org/10.1177/1178221818822976] [PMID: 30718957]
[10]
Crews FT, Robinson DL, Chandler LJ, et al. Mechanisms of persistent neurobiological changes following adolescent alcohol exposure: NADIA Consortium findings. Alcohol Clin Exp Res 2019; 43(9): 1806-22.
[http://dx.doi.org/10.1111/acer.14154] [PMID: 31335972]
[11]
White AM. What happened? Alcohol, memory blackouts, and the brain. Alcohol Res Health 2003; 27(2): 186-96.
[PMID: 15303630]
[12]
Crews FT, Buckley T, Dodd PR, et al. Alcoholic neurobiology: changes in dependence and recovery Alcohol Clin Exp Res 2005; 29(8): 1504-3.
[http://dx.doi.org/ 10.1097/01.alc.0000175013.50644.61] [PMID: 16156047]
[13]
[14]
Crews FT, Braun CJ, Hoplight B, Switzer RC III, Knapp DJ. Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 2000; 24(11): 1712-23.
[http://dx.doi.org/10.1111/j.1530-0277.2000.tb01973.x] [PMID: 11104119]
[15]
Wille-Bille A, de Olmos S, Marengo L, Chiner F, Pautassi RM. Long-term ethanol self-administration induces ΔFosB in male and female adolescent, but not in adult, Wistar rats. Prog Neuropsychopharmacol Biol Psychiatry 2017; 74: 15-30.
[http://dx.doi.org/10.1016/j.pnpbp.2016.11.008] [PMID: 27919738]
[16]
Simms JA, Steensland P, Medina B, et al. Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol Clin Exp Res 2008; 32(10): 1816-23.
[http://dx.doi.org/10.1111/j.1530-0277.2008.00753.x] [PMID: 18671810]
[17]
Amodeo LR, Kneiber D, Wills DN, Ehlers CL. Alcohol drinking during adolescence increases consumptive responses to alcohol in adulthood in Wistar rats. Alcohol 2017; 59: 43-51.
[http://dx.doi.org/10.1016/j.alcohol.2016.12.002] [PMID: 28187948]
[18]
National Institute on Alcohol And Alcoholism. Alcohol Use Disorder : A Comparison Between DSM - IV and DSM - 5 In. NIH publication 2013; 13-7999.Available at: . https://www.niaaa.nih.gov/publications/brochures-and-fact-sheets/alcohol-use-disorder-comparison-between-dsm
[19]
Waszkiewicz N, Galińska-Skok B, Nestsiarovich A, et al. Neurobiological effects of binge drinking help in its detection and differential diagnosis from alcohol dependence. Dis Markers 2018; 2018: 5623683.
[http://dx.doi.org/10.1155/2018/5623683] [PMID: 30069273]
[20]
Windle M, Spear LP, Fuligni AJ, et al. Transitions into underage and problem drinking: developmental processes and mechanisms between 10 and 15 years of age. Pediatrics 2008; 121(Suppl. 4): S273-89.
[http://dx.doi.org/10.1542/peds.2007-2243C 21]
[21]
Mental Health United States 2010. Substance Abuse and Mental Health Services Administration (US) 2012; 12-4681.
[22]
Patrick ME, Schulenberg JE, Martz ME, Maggs JL, O’Malley PM, Johnston LD. Extreme binge drinking among 12th-grade students in the United States: prevalence and predictors. JAMA Pediatr 2013; 167(11): 1019-25.
[http://dx.doi.org/10.1001/jamapediatrics.2013.2392] [PMID: 24042318]
[23]
Nguyen-Louie TT, Buckman JF, Ray S, Bates ME. Drinkers’ memory bias for alcohol picture cues in explicit and implicit memory tasks. Drug Alcohol Depend 2016; 160: 90-6.
[http://dx.doi.org/10.1016/j.drugalcdep.2015.12.033] [PMID: 26811126]
[24]
Fowler A-K, Thompson J, Chen L, et al. Differential sensitivity of prefrontal cortex and hippocampus to alcohol-induced toxicity. PLoS One 2014; 9(9): e106945.
[http://dx.doi.org/10.1371/journal.pone.0106945] [PMID: 25188266]
[25]
Stavro K, Pelletier J, Potvin S. Widespread and sustained cognitive deficits in alcoholism: a meta-analysis. Addict Biol 2013; 18(2): 203-13.
[http://dx.doi.org/10.1111/j.1369-1600.2011.00418.x] [PMID: 22264351]
[26]
Vetreno RP, Hall JM, Savage LM. Alcohol-related amnesia and dementia: animal models have revealed the contributions of different etiological factors on neuropathology, neurochemical dysfunction and cognitive impairment. Neurobiol Learn Mem 2011; 96(4): 596-608.
[http://dx.doi.org/10.1016/j.nlm.2011.01.003] [PMID: 21256970]
[27]
May PA, Chambers CD, Kalberg WO, et al. Prevalence of fetal alcohol spectrum disorders in 4 US communities. JAMA 2018; 319(5): 474-82.
[http://dx.doi.org/10.1001/jama.2017.21896] [PMID: 29411031]
[28]
Memo L, Gnoato E, Caminiti S, Pichini S, Tarani L. Fetal alcohol spectrum disorders and fetal alcohol syndrome: the state of the art and new diagnostic tools. Early Hum Dev 2013; 89(Suppl. 1): S40-3.
[http://dx.doi.org/10.1016/S0378-3782(13)70013-6] [PMID: 23809349]
[29]
Chen SY, Dehart DB, Sulik KK. Protection from ethanol-induced limb malformations by the superoxide dismutase/catalase mimetic, EUK-134. FASEB J 2004; 18(11): 1234-6.
[http://dx.doi.org/10.1096/fj.03-0850fje] [PMID: 15208273]
[30]
White AM, Swartzwelder HS. Age-related effects of alcohol on memory and memory-related brain function in adolescents and adults Recent Dev Alcohol. 2005; 17: pp. 161-76.
[http://dx.doi.org/10.1007/0-306-48626-1_8] [PMID: 15789865]
[31]
Mundt MP, Zakletskaia LI, Brown DD, Fleming MF. Alcohol-induced memory blackouts as an indicator of injury risk among college drinkers. Inj Prev 2012; 18(1): 44-9.
[http://dx.doi.org/10.1136/ip.2011.031724] [PMID: 21708813]
[32]
Zorumski CF, Mennerick S, Izumi Y. Acute and chronic effects of ethanol on learning-related synaptic plasticity. Alcohol 2014; 48(1): 1-17.
[http://dx.doi.org/10.1016/j.alcohol.2013.09.045] [PMID: 24447472]
[33]
Obernier JA, Bouldin TW, Crews FT. Binge ethanol exposure in adult rats causes necrotic cell death. Alcohol Clin Exp Res 2002; 26(4): 547-57.
[http://dx.doi.org/10.1111/j.1530-0277.2002.tb02573.x] [PMID: 11981132]
[34]
Swartzwelder HS, Risher M-L, Miller KM, Colbran RJ, Winder DG, Wills TA. Changes in the Adult GluN2B Associated Proteome following Adolescent Intermittent Ethanol Exposure. PLoS One 2016; 11(5): e0155951.
[http://dx.doi.org/10.1371/journal.pone.0155951] [PMID: 27213757]
[35]
Ojeda ML, Carreras O, Sobrino P, Murillo ML, Nogales F. Biological implications of selenium in adolescent rats exposed to binge drinking: oxidative, immunologic and apoptotic balance. Toxicol Appl Pharmacol 2017; 329(329): 165-72.
[http://dx.doi.org/10.1016/j.taap.2017.05.037] [PMID: 28579252]
[36]
Miceli M, Molina SJ, Forcada A, Acosta GB, Guelman LR. Voluntary alcohol intake after noise exposure in adolescent rats: hippocampal-related behavioral alterations. Brain Res 2018; 1679: 10-8.
[http://dx.doi.org/10.1016/j.brainres.2017.11.001] [PMID: 29113737]
[37]
Fabio MC, Nizhnikov ME, Spear NE, Pautassi RM. Binge ethanol intoxication heightens subsequent ethanol intake in adolescent, but not adult, rats. Dev Psychobiol 2014; 56(3): 574-83.
[http://dx.doi.org/10.1002/dev.21101] [PMID: 23341340]
[38]
Hermens DF, Lagopoulos J. Binge drinking and the young brain: a mini review of the neurobiological underpinnings of alcohol-induced blackout. Front Psychol 2018; 9: 12.
[http://dx.doi.org/10.3389/fpsyg.2018.00012] [PMID: 29403418]
[39]
Spear L. Modeling adolescent development and alcohol use in animals. Alcohol Res Health 2000; 24(2): 115-23.
[PMID: 11199278]
[40]
Spear LP. Effects of adolescent alcohol consumption on the brain and behaviour. Nat Rev Neurosci 2018; 19(4): 197-214.
[http://dx.doi.org/10.1038/nrn.2018.10] [PMID: 29467469]
[41]
Spear LP, Varlinskaya EI. Adolescence. Alcohol sensitivity, tolerance, and intake. Recent Dev Alcohol 2005.17: 143-59..
[http://dx.doi.org/10.1007/0-306-48626-1_7] [PMID: 15789864]
[42]
Marquardt K, Brigman JL. The impact of prenatal alcohol exposure on social, cognitive and affective behavioral domains: insights from rodent models. Alcohol 2016; 51: 1-15.
[http://dx.doi.org/10.1016/j.alcohol.2015.12.002] [PMID: 26992695]
[43]
Scheidt L, Fries GR, Stertz L, Cabral JCC, Kapczinski F, de Almeida RMM. Ethanol during adolescence decreased the BDNF levels in the hippocampus in adult male Wistar rats, but did not alter aggressive and anxiety-like behaviors. Trends Psychiatry Psychother 2015; 37(3): 143-51.
[http://dx.doi.org/10.1590/2237-6089-2015-0017] [PMID: 26630405]
[44]
Lacaille H, Duterte-Boucher D, Liot D, Vaudry H, Naassila M, Vaudry D. Comparison of the deleterious effects of binge drinking-like alcohol exposure in adolescent and adult mice. J Neurochem 2015; 132(6): 629-41.
[http://dx.doi.org/10.1111/jnc.13020] [PMID: 25556946]
[45]
Little PJ, Kuhn CM, Wilson WA, Swartzwelder HS. Differential effects of ethanol in adolescent and adult rats. Alcohol Clin Exp Res 1996; 20(8): 1346-51.
[http://dx.doi.org/10.1111/j.1530-0277.1996.tb01133.x] [PMID: 8947309]
[46]
Pascual M, Blanco AM, Cauli O, Miñarro J, Guerri C. Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats Eur J Neurosci 2007; 25(2): 541-0.
[http://dx.doi.org/10.1111/j.1460-9568.2006.05298.x] [PMID: 17284196]
[47]
Ros-Simó C, Moscoso-Castro M, Ruiz-Medina J, Ros J, Valverde O. Memory impairment and hippocampus specific protein oxidation induced by ethanol intake and 3, 4-methylenedioxymethamphetamine (MDMA) in mice. J Neurochem 2013; 125(5): 736-46.
[http://dx.doi.org/10.1111/jnc.12247] [PMID: 23521165]
[48]
Risher ML, Fleming RL, Risher WC, et al. Adolescent intermittent alcohol exposure: persistence of structural and functional hippocampal abnormalities into adulthood. Alcohol Clin Exp Res 2015; 39(6): 989-97.
[http://dx.doi.org/10.1111/acer.12725] [PMID: 25916839]
[49]
Mansouri A, Demeilliers C, Amsellem S, Pessayre D, Fromenty B. Acute ethanol administration oxidatively damages and depletes mitochondrial DNA in mouse liver, brain, heart, and skeletal muscles: protective effects of antioxidants. J Pharmacol Exp Ther 2001; 298(2): 737-43.
[PMID: 11454938]
[50]
Vargas WM, Bengston L, Gilpin NW, Whitcomb BW, Richardson HN. Alcohol binge drinking during adolescence or dependence during adulthood reduces prefrontal myelin in male rats. J Neurosci 2014; 29; 34(44): 14777-82.
[http://dx.doi.org/ 10.1523/JNEUROSCI.3189-13.2014]
[51]
Boschen KE, Klintsova AY. Neurotrophins in the Brain: Interaction with alcohol exposure during development. Vitam Horm 2017; 104: 197-242.
[http://dx.doi.org/10.1016/bs.vh.2016.10.008] [PMID: 28215296]
[52]
Criado JR, Ehlers CL. Effects of adolescent onset voluntary drinking followed by ethanol vapor exposure on subsequent ethanol consumption during protracted withdrawal in adult Wistar rats. Pharmacol Biochem Behav 2013; 103(3): 622-30.
[http://dx.doi.org/10.1016/j.pbb.2012.10.016] [PMID: 23128022]
[53]
Gilpin NW, Karanikas CA, Richardson HN. Adolescent binge drinking leads to changes in alcohol drinking, anxiety, and amygdalar corticotropin releasing factor cells in adulthood in male rats. PLoS One 2012; 7(2): e31466.
[http://dx.doi.org/10.1371/journal.pone.0031466] [PMID: 22347484]
[54]
Jung ME, Metzger DB. A sex difference in oxidative stress and behavioral suppression induced by ethanol withdrawal in rats. Behav Brain Res 2016; 314: 199-214.
[http://dx.doi.org/10.1016/j.bbr.2016.07.054] [PMID: 27503149]
[55]
Truxell EM, Molina JC, Spear NE. Ethanol intake in the juvenile, adolescent, and adult rat: effects of age and prior exposure to ethanol. Alcohol Clin Exp Res 2007; 31(5): 755-65.
[http://dx.doi.org/10.1111/j.1530-0277.2007.00358.x] [PMID: 17386073]
[56]
Amodeo LR, Wills DN, Sanchez-Alavez M, Nguyen W, Conti B, Ehlers CL. Intermittent voluntary ethanol consumption combined with ethanol vapor exposure during adolescence increases drinking and alters other behaviors in adulthood in female and male rats. Alcohol 2018; 73: 57-66.
[http://dx.doi.org/10.1016/j.alcohol.2018.04.003] [PMID: 30293056]
[57]
Li J, Bian W, Dave V, Ye JH. Blockade of GABA(A) receptors in the paraventricular nucleus of the hypothalamus attenuates voluntary ethanol intake and activates the hypothalamic-pituitary-adrenocortical axis. Addict Biol 2011; 16(4): 600-14.
[http://dx.doi.org/10.1111/j.1369-1600.2011.00344.x] [PMID: 21762292]
[58]
Tiwari V, Kuhad A, Chopra K. Neuroprotective effect of vitamin E isoforms against chronic alcohol-induced peripheral neurotoxicity: possible involvement of oxidative-nitrodative stress. Phytother Res 2012; 26(11): 1738-45.
[http://dx.doi.org/10.1002/ptr.4635] [PMID: 22422517]
[59]
Zhong Y, Dong G, Luo H, et al. Induction of brain CYP2E1 by chronic ethanol treatment and related oxidative stress in hippocampus, cerebellum, and brainstemToxicology 2012; 16; 302(2-3): 275-84.
[http://dx.doi.org/10.1016/j.tox.2012.08.009]
[60]
Sey NYA, Gómez-A A, Madayag AC, Boettiger CA, Robinson DL. Adolescent intermittent ethanol impairs behavioral flexibility in a rat foraging task in adulthood. Behav Brain Res 2019; 373112085
[http://dx.doi.org/10.1016/j.bbr.2019.112085] [PMID: 31319133]
[61]
Dahl RE. Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 2004; 1021: 1-22.
[http://dx.doi.org/10.1196/annals.1308.001] [PMID: 15251869]
[62]
Spear LP, Swartzwelder HS. Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neurosci Biobehav Rev 2014; 45: 1-8.
[http://dx.doi.org/10.1016/j.neubiorev.2014.04.012] [PMID: 24813805]
[63]
White AM, Swartzwelder HS. Hippocampal function during adolescence: a unique target of ethanol effects. Ann N Y Acad Sci 2004; 1021: 206-20.
[http://dx.doi.org/10.1196/annals.1308.026] [PMID: 15251891]
[64]
Silvers JM, Tokunaga S, Mittleman G, O’Buckley T, Morrow AL, Matthews DB. Chronic intermittent ethanol exposure during adolescence reduces the effect of ethanol challenge on hippocampal allopregnanolone levels and Morris water maze task performance. Alcohol 2006; 39(3): 151-8.
[http://dx.doi.org/10.1016/j.alcohol.2006.09.001]
[65]
Crews FT, Nixon K. Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 2009; 44(2): 115-27.
[http://dx.doi.org/10.1093/alcalc/agn079] [PMID: 18940959]
[66]
Schramm-Sapyta NL, Kingsley MA, Rezvani AH, Propst K, Swartzwelder HS, Kuhn CM. Early ethanol consumption predicts relapse-like behavior in adolescent male rats. Alcohol Clin Exp Res 2008; 32(5): 754-62.
[http://dx.doi.org/10.1111/j.1530-0277.2008.00631.x] [PMID: 18336637]
[67]
Pelição R, Santos MC, Freitas-Lima LC, et al. URB597 inhibits oxidative stress induced by alcohol binging in the prefrontal cortex of adolescent rats. Neurosci Lett 2016; 624: 17-22.
[http://dx.doi.org/10.1016/j.neulet.2016.04.068] [PMID: 27150075]
[68]
Prendergast MA, Harris BR, Mullholland PJ, et al. Hippocampal CA1 region neurodegeneration produced by ethanol withdrawal requires activation of intrinsic polysynaptic hippocampal pathways and function of N-methyl-D-aspartate receptors. Neuroscience 2004; 124(4): 869-77.
[http://dx.doi.org/10.1016/j.neuroscience.2003.12.013] [PMID: 15026127]
[69]
Haorah J, Ramirez SH, Floreani N, Gorantla S, Morsey B, Persidsky Y. Mechanism of alcohol-induced oxidative stress and neuronal injury. Free Radic Biol Med 2008; 45(11): 1542-50.
[http://dx.doi.org/10.1016/j.freeradbiomed.2008.08.030] [PMID: 18845238]
[70]
Bondy SC. Ethanol toxicity and oxidative stress. Toxicol Lett 1992; 63(3): 231-41.
[http://dx.doi.org/10.1016/0378-4274(92)90086-Y] [PMID: 1488774]
[71]
Thirunavukkarasu V, Anuradha CV, Viswanathan P. Protective effect of fenugreek (Trigonella foenum graecum) seeds in experimental ethanol toxicity. Phytother Res 2003; 17(7): 737-43.
[http://dx.doi.org/10.1002/ptr.1198] [PMID: 12916070]
[72]
Jung ME, Metzger DB. Alcohol withdrawal and brain injuries: beyond classical mechanisms. Molecules 2010; 15(7): 4984-5011.
[http://dx.doi.org/10.3390/molecules15074984] [PMID: 20657404]
[73]
Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. In: Free Radical Biology and Medicine. 2nd ed. Acta Cryst: 2017.
[http://dx.doi.org/10.1016/0891-5849(92)90062-L]
[74]
Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000; 408(6809): 239-47.
[http://dx.doi.org/10.1038/35041687] [PMID: 11089981]
[75]
Gutteridge JMC, Halliwell B. Mini-Review: oxidative stress, redox stress or redox success? Biochem Biophys Res Commun 2018; 502(2): 183-6.
[http://dx.doi.org/10.1016/j.bbrc.2018.05.045] [PMID: 29752940]
[76]
Han J-H, Tian H-Z, Lian Y-Y, et al. Quetiapine mitigates the ethanol-induced oxidative stress in brain tissue, but not in the liver, of the rat. Neuropsychiatr Dis Treat 2015; 11: 1473-82.
[http://dx.doi.org/10.2147/NDT.S80505] [PMID: 26109862]
[77]
Allen RG, Tresini M. Oxidative stress and gene regulation. Free Radic Biol Med 2000; 28(3): 463-99.
[http://dx.doi.org/10.1016/S0891-5849(99)00242-7] [PMID: 10699758]
[78]
Brocardo PS, Gil-Mohapel J, Wortman R, et al. The effects of ethanol exposure during distinct periods of brain development on oxidative stress in the adult rat brain. Alcohol Clin Exp Res 2017; 41(1): 26-37.
[http://dx.doi.org/10.1111/acer.13266] [PMID: 27862017]
[79]
Ahmad A, Rasheed N, Banu N, Palit G. Alterations in monoamine levels and oxidative systems in frontal cortex, striatum, and hippocampus of the rat brain during chronic unpredictable stress. Stress 2010; 13(4): 355-64.
[http://dx.doi.org/10.3109/10253891003667862] [PMID: 20536337]
[80]
Hu M, Zou W, Wang C-Y, et al. Hydrogen Sulfide protects against chronic unpredictable mild stress-induced oxidative stress in hippocampus by upregulation of BDNF-TrkB pathway. Oxid Med Cell Longev 2016; 2016: 2153745.
[http://dx.doi.org/10.1155/2016/2153745] [PMID: 27525050]
[81]
Caceres LG, Rios H, Guelman LR. Long-lasting effects of neonatal ionizing radiation exposure on spatial memory and anxiety-like behavior. Ecotoxicol Environ Saf 2009; 72(3): 895-904.
[http://dx.doi.org/10.1016/j.ecoenv.2008.09.009] [PMID: 18947871]
[82]
Caceres LG, Aon Bertolino L, Saraceno GE, et al. Hippocampal-related memory deficits and histological damage induced by neonatal ionizing radiation exposure. Role of oxidative status. Brain Res 2010; 1312: 67-78.
[http://dx.doi.org/10.1016/j.brainres.2009.11.053] [PMID: 19948150]
[83]
Ehrhart F, Roozen S, Verbeek J, et al. Review and gap analysis: molecular pathways leading to fetal alcohol spectrum disorders. Mol Psychiatry 2019; 24(1): 10-7.
[http://dx.doi.org/10.1038/s41380-018-0095-4] [PMID: 29892052]
[84]
Merad-Boudia M, Nicole A, Santiard-Baron D, Saillé C, Ceballos-Picot I. Mitochondrial impairment as an early event in the process of apoptosis induced by glutathione depletion in neuronal cells: relevance to Parkinson’s disease. Biochem Pharmacol 1998; 56(5): 645-55.
[http://dx.doi.org/10.1016/S0006-2952(97)00647-3] [PMID: 9783733]
[85]
Balmus IM, Ciobica A, Antioch I, Dobrin R, Timofte D. Oxidative stress implications in the affective disorders: main biomarkers, animal models relevance, genetic perspectives, and antioxidant approaches. Oxid Med Cell Longev 2016; 2016: 3975101.
[http://dx.doi.org/10.1155/2016/3975101] [PMID: 27563374]
[86]
Patil S, Tawari S, Mundhada D, Nadeem S. Protective effect of berberine, an isoquinoline alkaloid ameliorates ethanol-induced oxidative stress and memory dysfunction in rats. Pharmacol Biochem Behav 2015; 136: 13-20.
[http://dx.doi.org/10.1016/j.pbb.2015.07.001] [PMID: 26159088]
[87]
Soleimani E, Goudarzi I, Abrari K, Lashkarbolouki T. Maternal administration of melatonin prevents spatial learning and memory deficits induced by developmental ethanol and lead co-exposure. Physiol Behav 2017; 173: 200-8.
[http://dx.doi.org/10.1016/j.physbeh.2017.02.012] [PMID: 28209536]
[88]
Enache M, Van Waes V, Vinner E, Lhermitte M, Maccari S, Darnaudéry M. Impact of an acute exposure to ethanol on the oxidative stress status in the hippocampus of prenatal restraint stress adolescent male rats. Brain Res 2008; 1191: 55-62.
[http://dx.doi.org/10.1016/j.brainres.2007.11.031] [PMID: 18096141]
[89]
Díaz A, Treviño S, Guevara J, et al. Energy Drink administration in combination with alcohol causes an inflammatory response and oxidative stress in the hippocampus and temporal cortex of rats. Oxid Med Cell Longev 2016; 2016: 8725354.
[http://dx.doi.org/10.1155/2016/8725354] [PMID: 27069534]
[90]
Oyenihi OR, Afolabi BA, Oyenihi AB, Ogunmokun OJ, Oguntibeju OO. Hepato- and neuro-protective effects of watermelon juice on acute ethanol-induced oxidative stress in rats. Toxicol Rep 2016; 3: 288-94.
[http://dx.doi.org/10.1016/j.toxrep.2016.01.003] [PMID: 28959549]
[91]
Ozkol H, Bulut G, Balahoroglu R, Tuluce Y, Ozkol HU. Protective effects of selenium, n-acetylcysteine and vitamin E against acute ethanol intoxication in rats. Biol Trace Elem Res 2017; 175(1): 177-85.
[http://dx.doi.org/10.1007/s12011-016-0762-8] [PMID: 27250492]
[92]
Karadayian AG, Malanga G, Czerniczyniec A, Lombardi P, Bustamante J, Lores-Arnaiz S. Free radical production and antioxidant status in brain cortex non-synaptic mitochondria and synaptosomes at alcohol hangover onset. Free Radic Biol Med 2017; 108: 692-703.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.04.344] [PMID: 28450149]
[93]
Cohen-Kerem R, Koren G. Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicol Teratol 2003; 25(1): 1-9.
[http://dx.doi.org/10.1016/S0892-0362(02)00324-0] [PMID: 12633732]
[94]
Dong J, Sulik KK, Chen SY. The role of NOX enzymes in ethanol-induced oxidative stress and apoptosis in mouse embryos. Toxicol Lett 2010; 193(1): 94-100.
[http://dx.doi.org/10.1016/j.toxlet.2009.12.012] [PMID: 20026259]
[95]
Teixeira FB, Santana LN da S, Bezerra FR, et al. Chronic ethanol exposure during adolescence in rats induces motor impairments and cerebral cortex damage associated with oxidative stress. PLoS One 2014; 9(6)e101074
[http://dx.doi.org/10.1371/journal.pone.0101074] [PMID: 24967633]
[96]
World Health Organization. Global strategy to reduce the harmful use of alcohol 2010.Available at:. https://www.who.int/substance_abuse/publications/global_strategy_reduce_harmful_use_alcohol/en/
[97]
Pamplona-Santos D, Lamarão-Vieira K, Nascimento PC, et al. Aerobic physical exercise as a neuroprotector strategy for ethanol binge-drinking effects in the hippocampus and systemic redox status in rats. Oxid Med Cell Longev 2019; 2019: 2415243.
[http://dx.doi.org/10.1155/2019/2415243] [PMID: 31354903]
[98]
Fernandes LMP, Lopes KS, Santana LNS, et al. Repeated cycles of binge-like ethanol intake in adolescent female rats induce motor function impairment and oxidative damage in motor cortex and liver, but not in blood. Oxid Med Cell Longev 2018; 2018: 3467531.
[http://dx.doi.org/10.1155/2018/3467531] [PMID: 30327712]
[99]
Tapia-Rojas C, Carvajal FJ, Mira RG, et al. Adolescent binge alcohol exposure affects the brain function through mitochondrial impairment. Mol Neurobiol 2018; 55(5): 4473-91.
[http://dx.doi.org/10.1007/s12035-018-1268-5] [PMID: 28674997]
[100]
Anandatheerthavarada HK, Shankar SK, Bhamre S, Boyd MR, Song BJ, Ravindranath V. Induction of brain cytochrome P-450IIE1 by chronic ethanol treatment. Brain Res 1993; 22;601(1-2): 279-85.
[101]
Bell RL, Hauser SR, Liang T, Sari Y, Maldonado-Devincci A, Rodd ZA. Rat animal models for screening medications to treat alcohol use disorders. Neuropharmacology 2017; 122: 201-43.
[http://dx.doi.org/10.1016/j.neuropharm.2017.02.004] [PMID: 28215999]
[102]
Gupta KK, Gupta VK, Shirasaka T. An update on fetal alcohol syndrome-pathogenesis, risks, and treatment. Alcohol Clin Exp Res 2016; 40(8): 1594-602.
[http://dx.doi.org/10.1111/acer.13135] [PMID: 27375266]
[103]
Herrera DG, Yague AG, Johnsen-Soriano S, 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.
[http://dx.doi.org/10.1073/pnas.1230907100] [PMID: 12792022]
[104]
Hamelink C, Hampson A, Wink DA, Eiden LE, Eskay RL. Comparison of cannabidiol, antioxidants, and diuretics in reversing binge ethanol-induced neurotoxicity. J Pharmacol Exp Ther 2005; 314(2): 780-8.
[http://dx.doi.org/10.1124/jpet.105.085779] [PMID: 15878999]
[105]
Liput DJ, Pauly JR, Stinchcomb AL, Nixon K. Binge alcohol exposure transiently changes the endocannabinoid system: a potential target to prevent alcohol-induced neurodegeneration. Brain Sci 2017; 7(12): 158.
[http://dx.doi.org/10.3390/brainsci7120158] [PMID: 29186065]
[106]
Gowran A, Noonan J, Campbell VA. The multiplicity of action of cannabinoids: implications for treating neurodegeneration. CNS Neurosci Ther 2011; 17(6): 637-44.
[http://dx.doi.org/10.1111/j.1755-5949.2010.00195.x] [PMID: 20875047]
[107]
Paloczi J, Varga ZV, Hasko G, Pacher P. Neuroprotection in oxidative stress-related neurodegenerative diseases: role of endocannabinoid system modulation. Antioxid Redox Signal 2018; 29(1): 75-108.
[http://dx.doi.org/10.1089/ars.2017.7144] [PMID: 28497982]
[108]
Ojeda ML, Rua RM, Nogales F, Díaz-Castro J, Murillo ML, Carreras O. The benefits of administering folic acid in order to combat the oxidative damage caused by binge drinking in adolescent rats. Alcohol Alcohol 2016; 51(3): 235-41.
[http://dx.doi.org/10.1093/alcalc/agv111] [PMID: 26433946]
[109]
Oliveira GB, Fontes Ede A Jr, de Carvalho S, et al. Minocycline mitigates motor impairments and cortical neuronal loss induced by focal ischemia in rats chronically exposed to ethanol during adolescence. Brain Res 2014; 1561: 23-34.
[http://dx.doi.org/10.1016/j.brainres.2014.03.005] [PMID: 24637259]
[110]
Tiwari V, Chopra K. Resveratrol abrogates alcohol-induced cognitive deficits by attenuating oxidative-nitrosative stress and inflammatory cascade in the adult rat brain. Neurochem Int 2013; 62(6): 861-9.
[http://dx.doi.org/10.1016/j.neuint.2013.02.012] [PMID: 23422878]
[111]
Simpkins JW, Yang S-H, Liu R, et al. Estrogen-like compounds for ischemic neuroprotection. Stroke 2004; 35(11)(Suppl. 1): 2648-51.
[http://dx.doi.org/10.1161/01.STR.0000143734.59507.88] [PMID: 15472107]


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VOLUME: 25
ISSUE: 45
Year: 2019
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DOI: 10.2174/1381612825666191209121735
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