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CNS & Neurological Disorders - Drug Targets

Author(s): Mitra-Sadat Sadat-Shirazi, Mahsa Sadeghi-Adl, Ardeshir Akbarabadi, Ghorbangol Ashabi, Azarakhsh Mokri and Mohammad-Reza Zarrindast*

DOI: 10.2174/1871527321666220429122819

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Inter/Transgenerational Effects of Drugs of Abuse: A Scoping Review

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Abstract

Drug addiction is a chronic relapsing disorder that makes it a global problem. Genetics and environmental factors are the two most important factors that make someone vulnerable to drug addiction. Investigations in the past decade highlighted the role of epigenetics in the inter/transgenerational inheritance of drug addiction. A growing body of evidence showed that parental (paternal, maternal, and biparental) drug exposure before conception changes the phenotype of the offspring, which is correlated with neurochemical and neurostructural changes in the brain. The current paper reviews the effects of parental (maternal, paternal, and biparental) exposure to drugs of abuse (opioids, cocaine, nicotine, alcohol, and cannabis) before gestation in animal models.

Keywords: Transgeneration, opioid, cocaine, cannabis, nicotine, ethanol, parental.

Graphical Abstract

[1]
Strang J, Volkow ND, Degenhardt L, et al. Opioid use disorder. Nat Rev Dis Primers 2020; 6(1): 3.
[http://dx.doi.org/10.1038/s41572-019-0137-5] [PMID: 31919349]
[2]
Takahashi TT, Ornello R, Quatrosi G, et al. European Headache Federation School of Advanced Studies (EHF-SAS). Medication overuse and drug addiction: A narrative review from addiction perspective. J Headache Pain 2021; 22(1): 32.
[http://dx.doi.org/10.1186/s10194-021-01224-8] [PMID: 33910499]
[3]
Dai W, Qiu E, Chen Y, et al. Enhanced functional connectivity between habenula and salience network in medication-overuse headache complicating chronic migraine positions it within the addiction disorders: An ICA-based resting-state fMRI study. J Headache Pain 2021; 22(1): 107.
[http://dx.doi.org/10.1186/s10194-021-01318-3] [PMID: 34503441]
[4]
Balsa AI, Homer JF, French MT. The health effects of parental problem drinking on adult children. J Ment Health Policy Econ 2009; 12(2): 55-66.
[PMID: 19567931]
[5]
Vassoler F M, Byrnes E M, Pierce R C. The impact of exposure to addictive drugs on future generations: Physiological and behavioral effects. Neuropharmacology 2014; 76(Pt B): 269-75.
[6]
Jaenisch R, Bird A. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33 (Suppl.): 245-54.
[http://dx.doi.org/10.1038/ng1089] [PMID: 12610534]
[7]
Skinner MK. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 2011; 6(7): 838-42.
[http://dx.doi.org/10.4161/epi.6.7.16537] [PMID: 21637037]
[8]
Bošković A, Rando OJ. Transgenerational epigenetic inheritance. Annu Rev Genet 2018; 52: 21-41.
[http://dx.doi.org/10.1146/annurev-genet-120417-031404] [PMID: 30160987]
[9]
Maze I, Covington HE III, Dietz DM, et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 2010; 327(5962): 213-6.
[http://dx.doi.org/10.1126/science.1179438] [PMID: 20056891]
[10]
Sharma U, Rando OJ. Metabolic inputs into the epigenome. Cell Metab 2017; 25(3): 544-58.
[http://dx.doi.org/10.1016/j.cmet.2017.02.003] [PMID: 28273477]
[11]
Yohn NL, Bartolomei MS, Blendy JA. Multigenerational and transgenerational inheritance of drug exposure: The effects of alcohol, opiates, cocaine, marijuana, and nicotine. Prog Biophys Mol Biol 2015; 118(1-2): 21-33.
[http://dx.doi.org/10.1016/j.pbiomolbio.2015.03.002] [PMID: 25839742]
[12]
Akbarabadi A, Sadat-Shirazi MS, Kabbaj M, et al. Effects of morphine and maternal care on behaviors and protein expression of male offspring. Neuroscience 2021; 466: 58-76.
[http://dx.doi.org/10.1016/j.neuroscience.2021.04.011] [PMID: 33915201]
[13]
Hempel BJ, Crissman ME, Imanalieva A, Melkumyan M, Winston CA, Riley AL. Cross-generational THC exposure weakly attenuates cocaine’s rewarding effects in adult male offspring. Physiol Behav 2020; 227: 113164.
[http://dx.doi.org/10.1016/j.physbeh.2020.113164] [PMID: 32891609]
[14]
Akbarabadi A, Niknamfar S, Vousooghi N, Sadat-Shirazi MS, Toolee H, Zarrindast MR. Effect of rat parental morphine exposure on passive avoidance memory and morphine conditioned place preference in male offspring. Physiol Behav 2018; 184: 143-9.
[http://dx.doi.org/10.1016/j.physbeh.2017.11.024] [PMID: 29174820]
[15]
Sadat-Shirazi MS, Karimi F, Kaka G, et al. Parental morphine exposure enhances morphine (but not methamphetamine) preference and increases monoamine oxidase-B level in the nucleus accumbens. Behav Pharmacol 2019; 30(5): 435-45.
[http://dx.doi.org/10.1097/FBP.0000000000000465] [PMID: 30694818]
[16]
Li CQ, Luo YW, Bi FF, et al. Development of anxiety-like behavior via hippocampal IGF-2 signaling in the offspring of parental morphine exposure: Effect of enriched environment. Neuropsychopharmacology 2014; 39(12): 2777-87.
[17]
Azadi M, Azizi H, Haghparast A. Paternal exposure to morphine during adolescence induces reward-resistant phenotype to morphine in male offspring. Brain Res Bull 2019; 147: 124-32.
[http://dx.doi.org/10.1016/j.brainresbull.2019.02.004] [PMID: 30769129]
[18]
Cicero TJ, Adams ML, Giordano A, Miller BT, O’Connor L, Nock B. Influence of morphine exposure during adolescence on the sexual maturation of male rats and the development of their offspring. J Pharmacol Exp Ther 1991; 256(3): 1086-93.
[PMID: 2005573]
[19]
Sadat-Shirazi MS, Asgari P, Mahboubi S, et al. Effect of morphine exposure on novel object memory of the offspring: The role of histone H3 and ΔFosB. Brain Res Bull 2020; 156: 141-9.
[http://dx.doi.org/10.1016/j.brainresbull.2020.01.011] [PMID: 31958477]
[20]
Vassoler FM, Toorie AM, Teceno DN, et al. Paternal morphine exposure induces bidirectional effects on cocaine versus opioid self-administration. Neuropharmacology 2020; 162: 107852.
[http://dx.doi.org/10.1016/j.neuropharm.2019.107852] [PMID: 31726075]
[21]
Moulaei N, Mondanizadeh M, Salmani ME, Palizvan MR, Khansarinejad B, Sadegh M. Transgenerational consequences of prepregnancy chronic morphine use on spatial learning and hippocampal Mecp2 and Hdac2 expression. Neuroreport 2018; 29(9): 739-44.
[http://dx.doi.org/10.1097/WNR.0000000000001025] [PMID: 29634586]
[22]
Johnson NL, Carini L, Schenk ME, Stewart M, Byrnes EM. Adolescent opiate exposure in the female rat induces subtle alterations in maternal care and transgenerational effects on play behavior. Front Psychiatry 2011; 2: 29.
[http://dx.doi.org/10.3389/fpsyt.2011.00029] [PMID: 21713113]
[23]
Byrnes EM. Transgenerational consequences of adolescent morphine exposure in female rats: Effects on anxiety-like behaviors and morphine sensitization in adult offspring. Psychopharmacology (Berl) 2005; 182(4): 537-44.
[http://dx.doi.org/10.1007/s00213-005-0122-4] [PMID: 16163528]
[24]
Byrnes JJ, Babb JA, Scanlan VF, Byrnes EM. Adolescent opioid exposure in female rats: Transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav Brain Res 2011; 218(1): 200-5.
[http://dx.doi.org/10.1016/j.bbr.2010.11.059] [PMID: 21138744]
[25]
Bodi CM, Vassoler FM, Byrnes EM. Adolescent experience affects postnatal ultrasonic vocalizations and gene expression in future offspring. Dev Psychobiol 2016; 58(6): 714-23.
[http://dx.doi.org/10.1002/dev.21411] [PMID: 26999300]
[26]
Vassoler FM, Johnson-Collins NL, Carini LM, Byrnes EM. Next generation effects of female adolescent morphine exposure: Sex-specific alterations in response to acute morphine emerge before puberty. Behav Pharmacol 2014; 25(2): 173-81.
[http://dx.doi.org/10.1097/FBP.0000000000000032] [PMID: 24561499]
[27]
Farah Naquiah MZ, James RJ, Suratman S, et al. Transgenerational effects of paternal heroin addiction on anxiety and aggression behavior in male offspring. Behav Brain Funct 2016; 12(1): 23.
[http://dx.doi.org/10.1186/s12993-016-0107-y] [PMID: 27582026]
[28]
Slamberová R, Szilágyi B, Vathy I. Repeated morphine administration during pregnancy attenuates maternal behavior. Psychoneuroendocrinology 2001; 26(6): 565-76.
[http://dx.doi.org/10.1016/S0306-4530(01)00012-9] [PMID: 11403978]
[29]
Martins SS, Fenton MC, Keyes KM, Blanco C, Zhu H, Storr CL. Mood and anxiety disorders and their association with non-medical prescription opioid use and prescription opioid-use disorder: Longitudinal evidence from the National Epidemiologic Study on Alcohol and Related Conditions. Psychol Med 2012; 42(6): 1261-72.
[http://dx.doi.org/10.1017/S0033291711002145] [PMID: 21999943]
[30]
Vassoler FM, Byrnes EM. Transgenerational effects on anxiety-like behavior following adolescent morphine exposure in female rats. Behav Brain Res 2021; 406: 113239.
[http://dx.doi.org/10.1016/j.bbr.2021.113239] [PMID: 33731277]
[31]
Sabzevari S, Rohbani K, Sadat-Shirazi MS, et al. Morphine exposure before conception affects anxiety-like behavior and CRF level (in the CSF and plasma) in the adult male offspring. Brain Res Bull 2019; 144: 122-31.
[http://dx.doi.org/10.1016/j.brainresbull.2018.11.022] [PMID: 30503221]
[32]
Vousooghi N, Sadat-Shirazi MS, Safavi P, et al. Adult rat morphine exposure changes morphine preference, anxiety, and the brain expression of dopamine receptors in male offspring. Int J Dev Neurosci 2018; 69: 49-59.
[http://dx.doi.org/10.1016/j.ijdevneu.2018.06.008] [PMID: 29966738]
[33]
Cicero TJ, Nock B, O’Connor L, Adams M, Meyer ER. Adverse effects of paternal opiate exposure on offspring development and sensitivity to morphine-induced analgesia. J Pharmacol Exp Ther 1995; 273(1): 386-92.
[PMID: 7714793]
[34]
Pachenari N, Azizi H, Ghasemi E, Azadi M, Semnanian S. Exposure to opiates in male adolescent rats alters pain perception in the male offspring. Behav Pharmacol 2018; 29(2): 255-60.
[http://dx.doi.org/10.1097/FBP.0000000000000388]
[35]
Ashabi G, Sadat-Shirazi MS, Akbarabadi A, et al. Is the nociception mechanism altered in offspring of morphine-abstinent rats? J Pain 2018; 19(5): 529-41.
[http://dx.doi.org/10.1016/j.jpain.2017.12.268] [PMID: 29355609]
[36]
Ahmadian-Moghadam H, Sadat-Shirazi MS, Seifi F, et al. Transgenerational influence of parental morphine exposure on pain perception, anxiety-like behavior and passive avoidance memory among male and female offspring of Wistar rats. EXCLI J 2019; 18: 1019-36.
[PMID: 31762726]
[37]
Kamboj SK, Tookman A, Jones L, Curran VH. The effects of immediate-release morphine on cognitive functioning in patients receiving chronic opioid therapy in palliative care. Pain 2005; 117(3): 388-95.
[http://dx.doi.org/10.1016/j.pain.2005.06.022] [PMID: 16198201]
[38]
Schultz W. Dopamine signals for reward value and risk: Basic and recent data. Behav Brain Funct 2010; 6: 24.
[http://dx.doi.org/10.1186/1744-9081-6-24] [PMID: 20416052]
[39]
Ashabi G, Matloob M, Monfared Neirizi N, et al. Activation of D1-like dopamine receptors is involved in the impairment of spatial memory in the offspring of morphine-abstinent rats. Neurosci Res 2020; 158: 37-46.
[PMID: 31629794]
[40]
Vassoler FM, Wright SJ, Byrnes EM. Exposure to opiates in female adolescents alters mu opiate receptor expression and increases the rewarding effects of morphine in future offspring. Neuropharmacology 2016; 103: 112-21.
[http://dx.doi.org/10.1016/j.neuropharm.2015.11.026] [PMID: 26700246]
[41]
Vassoler F M, Oliver D J, Wyse C, et al. Transgenerational attenuation of opioid self-administration as a consequence of adolescent morphine exposure. Neuropharmacology 2017; 113(Pt A): 271-80.
[http://dx.doi.org/10.1016/j.neuropharm.2016.10.006]
[42]
Vassoler FM, Toorie AM, Byrnes EM. Increased cocaine reward in offspring of females exposed to morphine during adolescence. Psychopharmacology (Berl) 2019; 236(4): 1261-72.
[http://dx.doi.org/10.1007/s00213-018-5132-0] [PMID: 30506236]
[43]
Byrnes JJ, Johnson NL, Carini LM, Byrnes EM. Multigenerational effects of adolescent morphine exposure on dopamine D2 receptor function. Psychopharmacology (Berl) 2013; 227(2): 263-72.
[http://dx.doi.org/10.1007/s00213-012-2960-1] [PMID: 23314440]
[44]
Bruijnzeel AW, Repetto M, Gold MS. Neurobiological mechanisms in addictive and psychiatric disorders. Psychiatr Clin North Am 2004; 27(4): 661-74.
[http://dx.doi.org/10.1016/j.psc.2004.06.005] [PMID: 15550286]
[45]
Nouri Zadeh-Tehrani S, Sadat-Shirazi MS, Akbarabadi A, et al. Beneficial effects of physical activity on depressive and OCD-like behaviors in the male offspring of morphine-abstinent rats. Brain Res 2020; 1744: 146908.
[http://dx.doi.org/10.1016/j.brainres.2020.146908] [PMID: 32473256]
[46]
Torkaman-Boutorabi A, Seifi F, Akbarabadi A, et al. Morphine exposure and enhanced depression-like behaviour confronting chronic stress in adult male offspring rat. Basic Clin Neurosci 2019; 10(4): 323-32.
[PMID: 32231769]
[47]
Rohbani K, Sabzevari S, Sadat-Shirazi MS, et al. Parental morphine exposure affects repetitive grooming actions and marble burying behavior in the offspring: Potential relevance for obsessive-compulsive like behavior. Eur J Pharmacol 2019; 865: 172757.
[http://dx.doi.org/10.1016/j.ejphar.2019.172757] [PMID: 31693870]
[48]
Soltani H, Sadat-Shirazi MS, Pakpour B, Ashabi G, Zarrindast MR. Toxic effect of calcium/calmodulin kinase II on anxiety behavior, neuronal firing and plasticity in the male offspring of morphine-abstinent rats. Behav Brain Res 2020; 395: 112877.
[http://dx.doi.org/10.1016/j.bbr.2020.112877] [PMID: 32841609]
[49]
Sarkaki A, Assaei R, Motamedi F, Badavi M, Pajouhi N. Effect of parental morphine addiction on hippocampal long-term potentiation in rats offspring. Behav Brain Res 2008; 186(1): 72-7.
[http://dx.doi.org/10.1016/j.bbr.2007.07.041] [PMID: 17868930]
[50]
Toorie AM, Vassoler FM, Qu F, et al. A history of opioid exposure in females increases the risk of metabolic disorders in their future male offspring. Addict Biol 2021; 26(1): e12856.
[http://dx.doi.org/10.1111/adb.12856] [PMID: 31782234]
[51]
Vassoler FM, Toorie AM, Byrnes EM. Transgenerational blunting of morphine-induced corticosterone secretion is associated with dysregulated gene expression in male offspring. Brain Res 2018; 1679: 19-25.
[http://dx.doi.org/10.1016/j.brainres.2017.11.004] [PMID: 29129606]
[52]
Amri J, Sadegh M, Moulaei N, Palizvan MR. Transgenerational modification of hippocampus TNF-α and S100B levels in the offspring of rats chronically exposed to morphine during adolescence. Am J Drug Alcohol Abuse 2018; 44(1): 95-102.
[http://dx.doi.org/10.1080/00952990.2017.1348509] [PMID: 28750172]
[53]
Strathearn L, Mayes LC. Cocaine addiction in mothers: Potential effects on maternal care and infant development. Ann N Y Acad Sci 2010; 1187: 172-83.
[http://dx.doi.org/10.1111/j.1749-6632.2009.05142.x] [PMID: 20201853]
[54]
Fischer DK, Rice RC, Martinez Rivera A, Donohoe M, Rajadhyaksha AM. Altered reward sensitivity in female offspring of cocaine-exposed fathers. Behav Brain Res 2017; 332: 23-31.
[http://dx.doi.org/10.1016/j.bbr.2017.05.054] [PMID: 28552600]
[55]
Wimmer ME, Briand LA, Fant B, et al. Paternal cocaine taking elicits epigenetic remodeling and memory deficits in male progeny. Mol Psychiatry 2017; 22(11): 1641-50.
[http://dx.doi.org/10.1038/mp.2017.8] [PMID: 28220045]
[56]
Yaw AM, Woodruff RW, Prosser RA, Glass JD. Paternal cocaine disrupts offspring circadian clock function in a sex-dependent manner in mice. Neuroscience 2018; 379: 257-68.
[http://dx.doi.org/10.1016/j.neuroscience.2018.03.012] [PMID: 29567492]
[57]
Yaw AM, Prosser RA, Jones PC, Garcia BJ, Jacobson DA, Glass JD. Epigenetic effects of paternal cocaine on reward stimulus behavior and accumbens gene expression in mice. Behav Brain Res 2019; 367: 68-81.
[http://dx.doi.org/10.1016/j.bbr.2019.02.043] [PMID: 30910707]
[58]
Fant B, Wimmer ME, Swinford-Jackson SE, Maurer J, Van Nest D, Pierce RC. Preconception maternal cocaine self-administration increases the reinforcing efficacy of cocaine in male offspring. Psychopharmacology (Berl) 2019; 236(12): 3429-37.
[http://dx.doi.org/10.1007/s00213-019-05307-y] [PMID: 31236644]
[59]
Sasaki A, Constantinof A, Pan P, Kupferschmidt DA, McGowan PO, Erb S. Cocaine exposure prior to pregnancy alters the psychomotor response to cocaine and transcriptional regulation of the dopamine D1 receptor in adult male offspring. Behav Brain Res 2014; 265: 163-70.
[http://dx.doi.org/10.1016/j.bbr.2014.02.017] [PMID: 24583058]
[60]
Paine TA, Jackman SL, Olmstead MC. Cocaine-induced anxiety: Alleviation by diazepam, but not buspirone, dimenhydrinate or diphenhydramine. Behav Pharmacol 2002; 13(7): 511-23.
[http://dx.doi.org/10.1097/00008877-200211000-00001] [PMID: 12409990]
[61]
White SL, Vassoler FM, Schmidt HD, Pierce RC, Wimmer ME. Enhanced anxiety in the male offspring of sires that self-administered cocaine. Addict Biol 2016; 21(4): 802-10.
[http://dx.doi.org/10.1111/adb.12258] [PMID: 25923597]
[62]
Kutlu MG, Gould TJ. Effects of drugs of abuse on hippocampal plasticity and hippocampus-dependent learning and memory: Contributions to development and maintenance of addiction. Learn Mem 2016; 23(10): 515-33.
[http://dx.doi.org/10.1101/lm.042192.116] [PMID: 27634143]
[63]
Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC. Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 2013; 16(1): 42-7.
[http://dx.doi.org/10.1038/nn.3280] [PMID: 23242310]
[64]
Wimmer ME, Vassoler FM, White SL, et al. Impaired cocaine-induced behavioral plasticity in the male offspring of cocaine-experienced sires. Eur J Neurosci 2019; 49(9): 1115-26.
[http://dx.doi.org/10.1111/ejn.14310] [PMID: 30565761]
[65]
Rounsaville BJ. Treatment of cocaine dependence and depression. Biol Psychiatry 2004; 56(10): 803-9.
[http://dx.doi.org/10.1016/j.biopsych.2004.05.009] [PMID: 15556126]
[66]
Sobrian SK, Marr L, Ressman K. Prenatal cocaine and/or nicotine exposure produces depression and anxiety in aging rats. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27(3): 501-18.
[http://dx.doi.org/10.1016/S0278-5846(03)00042-3] [PMID: 12691787]
[67]
Renaud SM, Fountain SB. Transgenerational effects of adolescent nicotine exposure in rats: Evidence for cognitive deficits in adult female offspring. Neurotoxicol Teratol 2016; 56: 47-54.
[http://dx.doi.org/10.1016/j.ntt.2016.06.002] [PMID: 27286749]
[68]
Hawkey AB, White H, Pippen E, et al. Paternal nicotine exposure in rats produces long-lasting neurobehavioral effects in the offspring. Neurotoxicol Teratol 2019; 74: 106808.
[http://dx.doi.org/10.1016/j.ntt.2019.05.001] [PMID: 31103693]
[69]
Zhang M, Xu W, He G, et al. Maternal nicotine exposure has severe cross-generational effects on offspring behavior. Behav Brain Res 2018; 348: 263-6.
[http://dx.doi.org/10.1016/j.bbr.2018.04.033] [PMID: 29698694]
[70]
Murphy PJ, Guo J, Jenkins TG, et al. NRF2 loss recapitulates heritable impacts of paternal cigarette smoke exposure. PLoS Genet 2020; 16(6): e1008756.
[http://dx.doi.org/10.1371/journal.pgen.1008756] [PMID: 32520939]
[71]
Vallaster MP, Kukreja S, Bing XY, et al. Paternal nicotine exposure alters hepatic xenobiotic metabolism in offspring. eLife 2017; 6: 6.
[http://dx.doi.org/10.7554/eLife.24771] [PMID: 28196335]
[72]
Morissette SB, Tull MT, Gulliver SB, Kamholz BW, Zimering RT. Anxiety, anxiety disorders, tobacco use, and nicotine: A critical review of interrelationships. Psychol Bull 2007; 133(2): 245-72.
[http://dx.doi.org/10.1037/0033-2909.133.2.245] [PMID: 17338599]
[73]
Zhang M, Zhang D, Dai J, et al. Paternal nicotine exposure induces hyperactivity in next-generation via down-regulating the expression of DAT. Toxicology 2020; 431: 152367.
[http://dx.doi.org/10.1016/j.tox.2020.152367] [PMID: 31945395]
[74]
Valentine G, Sofuoglu M. Cognitive effects of nicotine: Recent progress. Curr Neuropharmacol 2018; 16(4): 403-14.
[http://dx.doi.org/10.2174/1570159X15666171103152136] [PMID: 29110618]
[75]
McCarthy DM, Morgan TJ Jr, Lowe SE, et al. Nicotine exposure of male mice produces behavioral impairment in multiple generations of descendants. PLoS Biol 2018; 16(10): e2006497.
[http://dx.doi.org/10.1371/journal.pbio.2006497] [PMID: 30325916]
[76]
Goldberg LR, Zeid D, Kutlu MG, et al. Paternal nicotine enhances fear memory, reduces nicotine administration, and alters hippocampal genetic and neural function in offspring. Addict Biol 2021; 26(1): e12859.
[http://dx.doi.org/10.1111/adb.12859] [PMID: 31782218]
[77]
Fluharty M, Taylor AE, Grabski M, Munafò MR. The association of cigarette smoking with depression and anxiety: A systematic review. Nicotine Tob Res 2017; 19(1): 3-13.
[http://dx.doi.org/10.1093/ntr/ntw140] [PMID: 27199385]
[78]
Buck JM, O’Neill HC, Stitzel JA. Developmental nicotine exposure elicits multigenerational disequilibria in proBDNF proteolysis and glucocorticoid signaling in the frontal cortices, striata, and hippocampi of adolescent mice. Biochem Pharmacol 2019; 168: 438-51.
[http://dx.doi.org/10.1016/j.bcp.2019.08.003] [PMID: 31404529]
[79]
Meek LR, Myren K, Sturm J, Burau D. Acute paternal alcohol use affects offspring development and adult behavior. Physiol Behav 2007; 91(1): 154-60.
[http://dx.doi.org/10.1016/j.physbeh.2007.02.004] [PMID: 17433387]
[80]
Rompala GR, Finegersh A, Homanics GE. Paternal preconception ethanol exposure blunts hypothalamic-pituitary-adrenal axis responsivity and stress-induced excessive fluid intake in male mice. Alcohol 2016; 53: 19-25.
[http://dx.doi.org/10.1016/j.alcohol.2016.03.006] [PMID: 27286933]
[81]
Abel EL, Lee JA. Paternal alcohol exposure affects offspring behavior but not body or organ weights in mice. Alcohol Clin Exp Res 1988; 12(3): 349-55.
[http://dx.doi.org/10.1111/j.1530-0277.1988.tb00205.x] [PMID: 3044161]
[82]
Kim P, Choi CS, Park JH, et al. Chronic exposure to ethanol of male mice before mating produces attention deficit hyperactivity disor-der-like phenotype along with epigenetic dysregulation of dopamine transporter expression in mouse offspring. J Neurosci Res 2014; 92(5): 658-70.
[http://dx.doi.org/10.1002/jnr.23275] [PMID: 24510599]
[83]
Randall CL, Burling TA, Lochry EA, Sutker PB. The effect of paternal alcohol consumption on fetal development in mice. Drug Alcohol Depend 1982; 9(1): 89-95.
[http://dx.doi.org/10.1016/0376-8716(82)90028-X] [PMID: 7084025]
[84]
Liang F, Diao L, Liu J, et al. Paternal ethanol exposure and behavioral abnormities in offspring: Associated alterations in imprinted gene methylation. Neuropharmacology 2014; 81: 126-33.
[http://dx.doi.org/10.1016/j.neuropharm.2014.01.025] [PMID: 24486713]
[85]
Jamerson PA, Wulser MJ, Kimler BF. Neurobehavioral effects in rat pups whose sires were exposed to alcohol. Brain Res Dev Brain Res 2004; 149(2): 103-11.
[http://dx.doi.org/10.1016/j.devbrainres.2003.12.010] [PMID: 15063090]
[86]
Ceccanti M, Coccurello R, Carito V, et al. Paternal alcohol exposure in mice alters brain NGF and BDNF and increases ethanol-elicited preference in male offspring. Addict Biol 2016; 21(4): 776-87.
[http://dx.doi.org/10.1111/adb.12255] [PMID: 25940002]
[87]
Ledig M, Misslin R, Vogel E, Holownia A, Copin JC, Tholey G. Paternal alcohol exposure: Developmental and behavioral effects on the offspring of rats. Neuropharmacology 1998; 37(1): 57-66.
[http://dx.doi.org/10.1016/S0028-3908(97)00185-8] [PMID: 9680259]
[88]
Wozniak DF, Cicero TJ, Kettinger L III, Meyer ER. Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring. Psychopharmacology (Berl) 1991; 105(2): 289-302.
[http://dx.doi.org/10.1007/BF02244324] [PMID: 1796134]
[89]
Jabbar S, Chastain LG, Gangisetty O, Cabrera M A, Sochacki K, Sarkar D K. Preconception alcohol increases offspring vulnerability to stress. Neuropsychopharmacology 2016; 41(11): 2782-93.
[90]
Asimes A, Kim CK, Cuarenta A, Auger AP, Pak TR. Binge drinking and intergenerational implications: Parental preconception alcohol impacts offspring development in rats. J Endocr Soc 2018; 2(7): 672-86.
[http://dx.doi.org/10.1210/js.2018-00051] [PMID: 29946576]
[91]
Asimes A, Torcaso A, Pinceti E, Kim CK, Zeleznik-Le NJ, Pak TR. Adolescent binge-pattern alcohol exposure alters genome-wide DNA methylation patterns in the hypothalamus of alcohol-naïve male offspring. Alcohol 2017; 60: 179-89.
[http://dx.doi.org/10.1016/j.alcohol.2016.10.010] [PMID: 27817987]
[92]
Pepino MY, Abate P, Spear NE, Molina JC. Disruption of maternal behavior by alcohol intoxication in the lactating rat: A behavioral and metabolic analysis. Alcohol Clin Exp Res 2002; 26(8): 1205-14.
[http://dx.doi.org/10.1111/j.1530-0277.2002.tb02657.x] [PMID: 12198395]
[93]
Gilpin NW, Herman MA, Roberto M. The central amygdala as an integrative hub for anxiety and alcohol use disorders. Biol Psychiatry 2015; 77(10): 859-69.
[http://dx.doi.org/10.1016/j.biopsych.2014.09.008] [PMID: 25433901]
[94]
Finegersh A, Homanics GE. Paternal alcohol exposure reduces alcohol drinking and increases behavioral sensitivity to alcohol selectively in male offspring. PLoS One 2014; 9(6): e99078.
[http://dx.doi.org/10.1371/journal.pone.0099078] [PMID: 24896617]
[95]
Beeler E, Nobile ZL, Homanics GE. Paternal preconception every-other-day ethanol drinking alters behavior and ethanol consumption in offspring. Brain Sci 2019; 9(3): E56.
[http://dx.doi.org/10.3390/brainsci9030056] [PMID: 30845665]
[96]
Le Berre AP, Fama R, Sullivan EV. Executive functions, memory, and social cognitive deficits and recovery in chronic alcoholism: A critical review to inform future research. Alcohol Clin Exp Res 2017; 41(8): 1432-43.
[http://dx.doi.org/10.1111/acer.13431] [PMID: 28618018]
[97]
Boden JM, Fergusson DM. Alcohol and depression. Addiction 2011; 106(5): 906-14.
[http://dx.doi.org/10.1111/j.1360-0443.2010.03351.x] [PMID: 21382111]
[98]
Knezovich JG, Ramsay M. The effect of preconception paternal alcohol exposure on epigenetic remodeling of the h19 and rasgrf1 imprinting control regions in mouse offspring. Front Genet 2012; 3: 10.
[http://dx.doi.org/10.3389/fgene.2012.00010] [PMID: 22371710]
[99]
Przybycien-Szymanska MM, Rao YS, Prins SA, Pak TR. Parental binge alcohol abuse alters F1 generation hypothalamic gene expression in the absence of direct fetal alcohol exposure. PLoS One 2014; 9(2): e89320.
[http://dx.doi.org/10.1371/journal.pone.0089320] [PMID: 24586686]
[100]
Byrnes JJ, Johnson NL, Schenk ME, Byrnes EM. Cannabinoid exposure in adolescent female rats induces transgenerational effects on morphine conditioned place preference in male offspring. J Psychopharmacol 2012; 26(10): 1348-54.
[http://dx.doi.org/10.1177/0269881112443745] [PMID: 22516667]
[101]
Hempel BJ, Crissman ME, Imanalieva A, et al. Cross-generational THC exposure alters heroin reinforcement in adult male offspring. Drug Alcohol Depend 2020; 212: 107985.
[http://dx.doi.org/10.1016/j.drugalcdep.2020.107985] [PMID: 32386920]
[102]
Szutorisz H, DiNieri J A, Sweet E, et al. Parental THC exposure leads to compulsive heroin-seeking and altered striatal synaptic plasticity in the subsequent generation. Neuropsychopharmacology 2014; 39(6): 1315-23.
[103]
Levin ED, Hawkey AB, Hall BJ, et al. Paternal THC exposure in rats causes long-lasting neurobehavioral effects in the offspring. Neurotoxicol Teratol 2019; 74: 106806.
[http://dx.doi.org/10.1016/j.ntt.2019.04.003] [PMID: 31028824]
[104]
Holloway ZR, Hawkey AB, Pippin E, et al. Paternal factors in neurodevelopmental toxicology: THC exposure of male rats causes long-lasting neurobehavioral effects in their offspring. Neurotoxicology 2020; 78: 57-63.
[http://dx.doi.org/10.1016/j.neuro.2020.01.009] [PMID: 32045580]
[105]
Crippa JA, Zuardi AW, Martín-Santos R, et al. Cannabis and anxiety: A critical review of the evidence. Hum Psychopharmacol 2009; 24(7): 515-23.
[http://dx.doi.org/10.1002/hup.1048] [PMID: 19693792]
[106]
Ibn Lahmar Andaloussi Z, Taghzouti K, Abboussi O. Behavioural and epigenetic effects of paternal exposure to cannabinoids during adolescence on offspring vulnerability to stress. Int J Dev Neurosci 2019; 72: 48-54.
[http://dx.doi.org/10.1016/j.ijdevneu.2018.11.007] [PMID: 30476535]
[107]
Varvel SA, Hamm RJ, Martin BR, Lichtman AH. Differential effects of delta 9-THC on spatial reference and working memory in mice. Psychopharmacology (Berl) 2001; 157(2): 142-50.
[http://dx.doi.org/10.1007/s002130100780] [PMID: 11594438]
[108]
Pitsilis G, Spyridakos D, Nomikos GG, Panagis G. Adolescent female cannabinoid exposure diminishes the reward-facilitating effects of Δ9-Tetrahydrocannabinol and d-amphetamine in the adult male offspring. Front Pharmacol 2017; 8: 225.
[http://dx.doi.org/10.3389/fphar.2017.00225] [PMID: 28487656]
[109]
Hempel BJ, Melkumyan M, Crissman ME, Winston CA, Madar J, Riley AL. Pre-conception exposure to THC fails to impact nicotine reward in adult offspring. Pharmacol Biochem Behav 2020; 197: 173001.
[http://dx.doi.org/10.1016/j.pbb.2020.173001] [PMID: 32710886]
[110]
Vassoler FM, Johnson NL, Byrnes EM. Female adolescent exposure to cannabinoids causes transgenerational effects on morphine sensitization in female offspring in the absence of in utero exposure. J Psychopharmacol 2013; 27(11): 1015-22.
[http://dx.doi.org/10.1177/0269881113503504] [PMID: 24048098]
[111]
Szutorisz H, Egervári G, Sperry J, Carter JM, Hurd YL. Cross-generational THC exposure alters the developmental sensitivity of ventral and dorsal striatal gene expression in male and female offspring. Neurotoxicol Teratol 2016; 58: 107-14.
[http://dx.doi.org/10.1016/j.ntt.2016.05.005] [PMID: 27221226]
[112]
Watson C T, Szutorisz H, Garg P, et al. Genome-wide DNA methylation profiling reveals epigenetic changes in the rat nucleus accumbens associated with cross-generational effects of adolescent THC exposure. Neuropsychopharmacology 2015; 40(13): 2993-3005.
[113]
Insel TR, Fernald RD. How the brain processes social information: Searching for the social brain. Annu Rev Neurosci 2004; 27: 697-722.
[http://dx.doi.org/10.1146/annurev.neuro.27.070203.144148] [PMID: 15217348]
[114]
Crews D. Epigenetic modifications of brain and behavior: Theory and practice. Horm Behav 2011; 59(3): 393-8.
[http://dx.doi.org/10.1016/j.yhbeh.2010.07.001] [PMID: 20633562]
[115]
Cadet JL, Jayanthi S. Epigenetics of addiction. Neurochem Int 2021; 147: 105069.
[http://dx.doi.org/10.1016/j.neuint.2021.105069] [PMID: 33992741]
[116]
Browne CJ, Godino A, Salery M, Nestler EJ. Epigenetic mechanisms of opioid addiction. Biol Psychiatry 2020; 87(1): 22-33.
[http://dx.doi.org/10.1016/j.biopsych.2019.06.027] [PMID: 31477236]
[117]
Vassoler FM, Toorie AM, Byrnes EM. Multi-, inter-, and transgenerational effects of drugs of abuse on behavior. Curr Top Behav Neurosci 2019; 42: 247-58.
[http://dx.doi.org/10.1007/7854_2019_106] [PMID: 31396893]