Alcohol self-administration and nicotine withdrawal alter biomarkers of stress and inflammation and prefrontal cortex changes in Gβ subunits

References

• Anthony JC, Echeagaray-Wagner F. Epidemiologic analysis of alcohol and tobacco use. Alcohol Res Health. 2000;24:201–08.
   PubMedGoogle Scholar
• Tarren JR, Bartlett SE. Alcohol and nicotine interactions: pre-clinical models of dependence. Am J Drug Alcohol Abuse. 2017;43:146–54. doi:10.1080/00952990.2016.1197232.
   PubMed Web of Science ®Google Scholar
• Adams S. Psychopharmacology of tobacco and alcohol comorbidity: a review of current evidence. Curr Addict Rep. 2017;4:25–34. doi:10.1007/s40429-017-0129-z.
   PubMedGoogle Scholar
• Littleton J, Barron S, Prendergast M, Nixon SJ. Smoking kills (alcoholics)! shouldn’t we do something about it? Alcohol Alcohol. 2007;42:167–73. doi:10.1093/alcalc/agm019.
   PubMed Web of Science ®Google Scholar
• Morel C, Montgomery S, Han MH. Nicotine and alcohol: the role of midbrain dopaminergic neurons in drug reinforcement. Eur J Neurosci. 2019;50:2180–200. doi:10.1111/ejn.14160.
   PubMed Web of Science ®Google Scholar
• Ostroumov A, Thomas AM, Dani JA, Doyon WM. Cigarettes and alcohol: the influence of nicotine on operant alcohol self-administration and the mesolimbic dopamine system. Biochem Pharmacol. 2015;97:550–57. doi:10.1016/j.bcp.2015.07.038.
   PubMed Web of Science ®Google Scholar
• Waeiss RA, Knight CP, Engleman EA, Hauser SR, Rodd ZA. Co-administration of ethanol and nicotine heightens sensitivity to ethanol reward within the nucleus accumbens (NAc) shell and increasing NAc shell BDNF is sufficient to enhance ethanol reward in naïve Wistar rats. J Neurochem. 2020;152:556–69. doi:10.1111/jnc.14914.
   PubMed Web of Science ®Google Scholar
• Tizabi Y, Copeland RL Jr, Louis VA, Taylor RE. Effects of combined systemic alcohol and central nicotine administration into ventral tegmental area on dopamine release in the nucleus accumbens. Alcohol Clin Exp Res. 2002;26:394–9. 25. doi:10.1111/j.1530-0277.2002.tb02551.x.
   PubMed Web of Science ®Google Scholar
• Tizabi Y, Bai L, Copeland RL Jr, Taylor RE. Combined effects of systemic alcohol and nicotine on dopamine release in the nucleus accumbens shell. Alcohol Alcohol. 2007;42:413–16. doi:10.1093/alcalc/agm057.
   PubMed Web of Science ®Google Scholar
• Song C, Lin A, De Jong R, Vandoolaeghe E, Kenis G, Bosmans E, Whelan A, Scharpe S, Maes M. Cytokines in detoxified patients with chronic alcoholism without liver disease: increased monocytic cytokine production. Biol Psychiatry. 1999;45:1212–16. doi:10.1016/S0006-3223(98)00083-3.
   PubMed Web of Science ®Google Scholar
• Aguiar-Nemer AS, Toffolo MC, da Silva CJ, Laranjeira R, Silva-Fonseca VA. Leptin influence in craving and relapse of alcoholics and smokers. J Clin Med Res. 2013;5:164–67. doi:10.4021/jocmr1159w.
   PubMedGoogle Scholar
• Nikou T, Ioannidis A, Zoga M, Tzavellas E, Paparrigopoulos T, Magana M, Pliatsika P, Nikolaou C, Chatzipanagiotou S. Alteration in the concentrations of Interleukin-7 (IL-7), Interleukin-10 (IL-10) and Granulocyte Colony Stimulating Factor (G-CSF) in alcohol-dependent individuals without liver disease, during detoxification therapy. Drug Alcohol Depend. 2016;163:77–83. doi:10.1016/j.drugalcdep.2016.03.022.
   PubMed Web of Science ®Google Scholar
• Patel RR, Khom S, Steinman MQ, Varodayan FP, Kiosses WB, Hedges DM, Vlkolinsky R, Nadav T, Polis I, Bajo M, et al. IL-1β expression is increased and regulates GABA transmission following chronic ethanol in mouse central amygdala. Brain Behav Immun. 2019;75:208–19. doi:10.1016/j.bbi.2018.10.009.
   PubMed Web of Science ®Google Scholar
• Rosa MLP, Machado CA, Oliveira BDS, Toscano ECB, Asth L, de Barros JLVM, Teixeira AL, Moreira FA, de Miranda AS. Role of cytokine and neurotrophic factors in nicotine addiction in the conditioned place preference paradigm. Neurosci Lett. 2021;764:136235. doi:10.1016/j.neulet.2021.136235.
   PubMed Web of Science ®Google Scholar
• Otaka M, Konishi N, Odashima M, Jin M, Wada I, Matsuhashi T, Ohba R, Watanabe S. Effect of alcohol consumption on leptin level in serum, adipose tissue, and gastric mucosa. Dig Dis Sci. 2007;52:3066–69. doi:10.1007/s10620-006-9635-x.
   PubMed Web of Science ®Google Scholar
• Li MD, Kane JK. Effect of nicotine on the expression of leptin and forebrain leptin receptors in the rat. Brain Res. 2003;991:222–31. doi:10.1016/j.brainres.2003.08.024.
   PubMed Web of Science ®Google Scholar
• Robins MT, Chiang T, Mores KL, Alongkronrusmee D, van Rijn RM. Critical role for Gi/o-protein activity in the dorsal striatum in the reduction of voluntary alcohol intake in C57Bl/6 mice. Front Psychiatry. 2018;9:112. doi:10.3389/fpsyt.2018.00112.
   PubMed Web of Science ®Google Scholar
• Kononoff J, Kallupi M, Kimbrough A, Conlisk D, de Guglielmo G, George O. Systemic and intra-habenular activation of the orphan G protein-coupled receptor GPR139 decreases compulsive-like alcohol drinking and hyperalgesia in alcohol-dependent rats. eNeuro. 2018;5: 153-18. doi:10.1523/ENEURO.0153-18.2018.
   PubMed Web of Science ®Google Scholar
• Bowers MS, Woodward Hopf F, Chou JK, Guillory AM, Chang S-J, Janak PH, Bonci A, Diamond I. Nucleus accumbens AGS3 expression drives ethanol seeking through Gβγ. Proc Natl Acad Sci U S A. 2008;105:12533–38. doi:10.1073/pnas.0706999105.
   PubMed Web of Science ®Google Scholar
• Antolin-Fontes B, Li K, Ables JL, Riad MH, Görlich A, Williams M, Wang C, Lipford SM, Dao M, Liu J, et al. The habenular G-protein-coupled receptor 151 regulates synaptic plasticity and nicotine intake. Proc Natl Acad Sci U S A. 2020;117:5502–09. doi:10.1073/pnas.1916132117.
   PubMed Web of Science ®Google Scholar
• Inoue Y, Yao LF, Hopf W, Fan P, Zhan J, Bonci A, Diamond I. Nicotine and ethanol activate protein kinase a synergistically via Gi bg subunits in nuleus accumbens/ventral tegmental cocultures: the role of dopamine D1/D2 and adenosine A2A receptors. J Pharmacol Exp Ther. 2007;322:23–29. doi:10.1124/jpet.107.120675.
   PubMed Web of Science ®Google Scholar
• Tavares ER, Silva-Gotay A, Riad WV, Bengston L, Richardson HN. Sex differences in the effect of alcohol drinking on myelinated axons in the anterior cingulate cortex of adolescent rats. Brain Sci. 2019;9:167. doi:10.3390/brainsci9070167.
   PubMed Web of Science ®Google Scholar
• 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:e31466. doi:10.1371/journal.pone.0031466.
   PubMed Web of Science ®Google Scholar
• Richardson HN, Lee SY, O’Dell LE, Koob GF, Rivier CL. Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur J Neurosci. 2008;28:1641–53. doi:10.1111/j.1460-9568.2008.06455.x.
   PubMed Web of Science ®Google Scholar
• Kenny PJ, Markou A. Neurobiology of the nicotine withdrawal syndrome. Pharmacol Biochem Behav. 2001;70:531–49. doi:10.1016/S0091-3057(01)00651-7.
   PubMed Web of Science ®Google Scholar
• Malin DH. Nicotine dependence: studies with a laboratory model. Pharmacol Biochem Behav. 2001;70:551–59. doi:10.1016/S0091-3057(01)00699-2.
   PubMed Web of Science ®Google Scholar
• O’Dell LE, Roberts AJ, Smith RT, Koob GF. Enhanced alcohol self-administration after intermittent versus continuous alcohol vapor exposure. Alcohol Clin Exp Res. 2004;28:1676–82. doi:10.1097/01.ALC.0000145781.11923.4E.
   PubMed Web of Science ®Google Scholar
• Torres OV, Gentil LG, Natividad LA, Carcoba LM, O’Dell LE. Behavioral, biochemical, and molecular indices of stress are enhanced in female versus male rats experiencing nicotine withdrawal. Front Psychiatry. 2013;4:38. doi:10.3389/fpsyt.2013.00038.
   PubMedGoogle Scholar
• Weinland C, Tanovska P, Kornhuber J, Mühle C, Lenz B. Serum lipids, leptin, and soluble leptin receptor in alcohol dependence: a cross-sectional and longitudinal study. Drug Alcohol Depend. 2020;209:107898. doi:10.1016/j.drugalcdep.2020.107898.
   PubMed Web of Science ®Google Scholar
• Patel RR, Varodayan FP, Herman MA, Jimenez V, Agnore R, Gao L, Bajo M, Cuzon Carlson VC, Walter NA, Fei SS, et al. Synaptic effects of IL-1β and CRF in the central amygdala after protracted alcohol abstinence in male rhesus macaques. Neuropsychopharmacology. 2022;47:847–56. doi:10.1038/s41386-021-01231-y.
   PubMed Web of Science ®Google Scholar
• von der Goltz C, Koopmann A, Dinter C, Richter A, Rockenbach C, Grosshans M, Nakovics H, Wiedemann K, Mann K, Winterer G, et al. Orexin and leptin are associated with nicotine craving: a link between smoking, appetite and reward. Psychoneuroendocrinology. 2010;35:570–77. doi:10.1016/j.psyneuen.2009.09.005.
   PubMed Web of Science ®Google Scholar
• Flores RJ, Cruz B, Uribe KP, Correa VL, Arreguin MC, Carcoba LM, Mendez IA, O’Dell LE. Estradiol promotes and progesterone reduces anxiety-like behavior produced by nicotine withdrawal in female rats. Psychoneuroendocrinology. 2020;119:104694. doi:10.1016/j.psyneuen.2020.104694.
   PubMed Web of Science ®Google Scholar
• Roberts AJ, Cole M, Koob GF. Intra-amygdala muscimol decreases operant ethanol self-administration in dependent rats. Alcohol Clin Exp Res. 1996;20:1289–98. doi:10.1111/j.1530-0277.1996.tb01125.x.
   PubMed Web of Science ®Google Scholar
• Roberts AJ, Heyser CJ, Koob GF. Operant self-administration of sweetened versus unsweetened ethanol: effects on blood alcohol levels. Alcohol Clin Exp Res. 1999;23:1151–57.
   PubMed Web of Science ®Google Scholar
• Samson HH. Initiation of ethanol reinforcement using a sucrose-substitution procedure in food- and water-sated rats. Alcohol Clin Exp Res. 1986;10:436–42. doi:10.1111/j.1530-0277.1986.tb05120.x.
   PubMed Web of Science ®Google Scholar
• Funk CK, O’Dell LE, Crawford EF, Koob GF. Corticotropin-releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats. J Neurosci. 2006;26:11324–32. doi:10.1523/JNEUROSCI.3096-06.2006.
   PubMed Web of Science ®Google Scholar
• Watkins SS, Stinus L, Koob GF, Markou A. Reward and somatic changes during precipitated nicotine withdrawal in rats: centrally and peripherally mediated effects. J Pharmacol Exp Ther. 2000;292:1053–64.
   PubMed Web of Science ®Google Scholar
• Clark A, Lindgren S, Brooks SP, Watson WP, Little HJ. Chronic infusion of nicotine can increase operant self-administration of alcohol. Neuropharmacology. 2001;41:108–17. doi:10.1016/S0028-3908(01)00037-5.
   PubMed Web of Science ®Google Scholar
• Nadal R, Samson HH. Operant ethanol self-administration after nicotine treatment and withdrawal. Alcohol. 1999;7:139–47. doi:10.1016/S0741-8329(98)00045-7.
   Google Scholar
• Lê AD, Lo S, Harding S, Juzytsch W, Marinelli PW, Funk D. Coadministration of intravenous nicotine and oral alcohol in rats. Psychopharmacology (Berl). 2010;208:475–86. doi:10.1007/s00213-009-1746-6.
   PubMed Web of Science ®Google Scholar
• Sharpe AL, Samson HH. Repeated nicotine injections decrease operant ethanol self-administration. Alcohol. 2002;28:1–7. doi:10.1016/S0741-8329(02)00238-0.
   PubMed Web of Science ®Google Scholar
• Montanari C, Secci ME, Driskell A, McDonald KO, Schratz CL, Gilpin NW. Chronic nicotine increases alcohol self-administration in adult male Wistar rats. Psychopharmacology (Berl). 2021;238:201–13. doi:10.1007/s00213-020-05669-8.
   PubMed Web of Science ®Google Scholar
• Lopez-Moreno JA, Trigo-Diaz JM, de Rodriguez FF, Gonzalez CG, de Gomez HR, Crespo GI, Navarro M. Nicotine in alcohol deprivation increases alcohol operant self-administration during reinstatement. Neuropharmacology. 2004;47:1036–44. doi:10.1016/j.neuropharm.2004.08.002.
   PubMed Web of Science ®Google Scholar
• Lê AD, Wang A, Harding S, Juzytsch W, Shaham Y. Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology (Berl). 2003;168:216–21. doi:10.1007/s00213-002-1330-9.
   PubMed Web of Science ®Google Scholar
• Smith BR, Horan JT, Gaskin S, Amit Z. Exposure to nicotine enhances acquisition of ethanol drinking by laboratory rats in a limited access paradigm. Psychopharmacology (Berl). 1999;142:408–12. doi:10.1007/s002130050906.
   PubMed Web of Science ®Google Scholar
• Doyon WM, Dong Y, Ostroumov A, Thomas AM, Zhang TA, Dani JA. Nicotine decreases ethanol-induced dopamine signaling and increases self-administration via stress hormones. Neuron. 2013;79:530–40. doi:10.1016/j.neuron.2013.06.006.
   PubMed Web of Science ®Google Scholar
• Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation. 2008;18:10. doi:10.1186/1742-2094-5-10.
   Google Scholar
• Al’Absi M, Hooker S, Fujiwara K, Kiefer F, von der Goltz C, Cragin T, Wittmers LE. Circulating leptin levels are associated with increased craving to smoke in abstinent smokers. Pharmacol Biochem Behav. 2011;97:509–13. doi:10.1016/j.pbb.2010.10.004.
   PubMed Web of Science ®Google Scholar
• Browning BD, Schwandt ML, Farokhnia M, Deschaine SL, Hodgkinson CA, Leggio L. Leptin gene and leptin receptor gene polymorphisms in alcohol use disorder: findings related to psychopathology. Front Psychiatry. 2021;12:723059. doi:10.3389/fpsyt.2021.723059.
   PubMed Web of Science ®Google Scholar
• Mehta S, Baruah A, Das S, Avinash P, Chetia D, Gupta D. Leptin levels in alcohol dependent patients and their relationship with withdrawal and craving. Asian J Psychiatr. 2020;51:101967. doi:10.1016/j.ajp.2020.101967.
   PubMed Web of Science ®Google Scholar
• Hiney JK, Dearth RK, Lara F 3rd, Wood S, Srivastava V, Les Dees W. Effects of ethanol on leptin secretion and the leptin-induced luteinizing hormone (LH) release from late juvenile female rats. Alcohol Clin Exp Res. 1999;23:1785–92. doi:10.1111/j.1530-0277.1999.tb04074.x.
   PubMed Web of Science ®Google Scholar
• Pravdova E, Macho L, Fickova M. Alcohol intake modifies leptin, adiponectin and resistin serum levels and their mRNA expressions in adipose tissue of rats. Endocr Regul. 2009;43:117–25.
   PubMedGoogle Scholar
• Jope RS, Song L, Grimes CA, Pacheco MA, Dilley GE, Li X, Meltzer HY, Overholser JC, Stockmeier CA. Selective increases in phosphoinositide signaling activity and G protein levels in postmortem brain from subjects with schizophrenia or alcohol dependence. J Neurochem. 1998;70:763–71. doi:10.1046/j.1471-4159.1998.70020763.x.
   PubMed Web of Science ®Google Scholar
• Neasta J, Darcq E, Jeanblanc J, Carnicella S, Ben Hamida S. GPCR and alcohol-related behaviors in genetically modified mice. Neurotherapeutics. 2020;17:17–42. doi:10.1007/s13311-019-00828-y.
   PubMed Web of Science ®Google Scholar
• Sierra-Fonseca JA, Najera O, Martinez-Jurado J, Walker EM, Varela-Ramirez A, Khan AM, Miranda M, Lamango NS, Roychowdhury S. Nerve growth factor induces neurite outgrowth of PC12 cells by promoting Gβγ-microtubule interaction. BMC Neurosci. 2014;31:132. doi:10.1186/s12868-014-0132-4.
   Google Scholar
• Sierra-Fonseca JA, Miranda M, Das S, Roychowdhury S. The βγ subunit of heterotrimeric G proteins interacts with actin filaments during neuronal differentiation. Biochem Biophys Res Commun. 2021;16:98–104. doi:10.1016/j.bbrc.2021.02.095.
   Google Scholar
• Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Malenka RC, Nestler EJ. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 2010;33:267–76. doi:10.1016/j.tins.2010.02.002.
   PubMed Web of Science ®Google Scholar
• Rothenfluh A, Cowan CW. Emerging roles of actin cytoskeleton regulating enzymes in drug addiction: actin or reactin’? Curr Opin Neurobiol. 2013;23:507–12. doi:10.1016/j.conb.2013.01.027.
   PubMed Web of Science ®Google Scholar
• Deehan GA Jr, Hauser SR, Waeiss RA, Knight CP, Toalston JE, Truitt WA, McBride WJ, Rodd ZA. Co-administration of ethanol and nicotine: the enduring alterations in the rewarding properties of nicotine and glutamate activity within the mesocorticolimbic system of female alcohol-preferring (P) rats. Psychopharmacology (Berl). 2015;232:4293–302. doi:10.1007/s00213-015-4056-1.
   PubMed Web of Science ®Google Scholar
• Barker JM, Zhang H, Villafane JJ, Wang TL, Torregrossa MM, Taylor JR. Epigenetic and pharmacological regulation of 5HT3 receptors controls compulsive ethanol seeking in mice. Eur J Neurosci. 2014;39:999–1008. doi:10.1111/ejn.12477.
   PubMed Web of Science ®Google Scholar
• Lovinger DM. Serotonin’s role in alcohol’s effects on the brain. Alcohol Health Res World. 1997;21:114–20.
   PubMedGoogle Scholar
• Lovinger DM. 5-HT3 receptors and the neural actions of alcohols: an increasingly exciting topic. Neurochem Int. 1999;35:125–30. doi:10.1016/S0197-0186(99)00054-6.
   PubMed Web of Science ®Google Scholar
• Davis TJ, de Fiebre CM. Alcohol’s actions on neuronal nicotinic acetylcholine receptors. Alcohol Res Health. 2006;29:179–85.
   PubMedGoogle Scholar
• Miller CN, Kamens HM. The role of nicotinic acetylcholine receptors in alcohol-related behaviors. Brain Res Bull. 2020;163:135–42. doi:10.1016/j.brainresbull.2020.07.017.
   PubMed Web of Science ®Google Scholar
• Rodd ZA, Hauser SR, Swartzwelder HS, Waeiss RA, Lahiri DK, Bell RL. Regulation of the deleterious effects of binge-like exposure to alcohol during adolescence by α7 nicotinic acetylcholine receptor agents: prevention by pretreatment with a α7 negative allosteric modulator and emulation by a α7 agonist in alcohol-preferring (P) male and female rats. Psychopharmacology (Berl). 2020;237:2601–11. doi:10.1007/s00213-020-05557-1.
   PubMed Web of Science ®Google Scholar
• Waeiss RA, Knight CP, Hauser SR, Pratt LA, McBride WJ, Rodd ZA. Therapeutic challenges for concurrent ethanol and nicotine consumption: naltrexone and varenicline fail to alter simultaneous ethanol and nicotine intake by female alcohol-preferring (P) rats. Psychopharmacology (Berl). 2019;236:1887–900. doi:10.1007/s00213-019-5174-y.
   PubMed Web of Science ®Google Scholar
• Chandler CM, Maggio SE, Peng H, Nixon K, Bardo MT. Effects of ethanol, naltrexone, nicotine and varenicline in an ethanol and nicotine co-use model in Sprague-Dawley rats. Drug Alcohol Depend. 2020;212:107988. doi:10.1016/j.drugalcdep.2020.107988.
   PubMed Web of Science ®Google Scholar
• Lopez-Castejon G, Brough D. Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev. 2011;22:189–95. doi:10.1016/j.cytogfr.2011.10.001.
   PubMed Web of Science ®Google Scholar
• Loram LC, Themistocleous AC, Fick LG, Kamerman PR. The time course of inflammatory cytokine secretion in a rat model of postoperative pain does not coincide with the onset of mechanical hyperalgesia. Can J Physiol Pharmacol. 2007;85:613–20. doi:10.1139/Y07-054.
   PubMed Web of Science ®Google Scholar
• Barrett ST, Thompson BM, Emory JR, Larsen CE, Pittenger ST, Harris EN, Bevins RA. Sex differences in the reward-enhancing effects of nicotine on ethanol reinforcement: a reinforcer demand analysis. Nicotine Tob Res. 2020;22:238–47. doi:10.1093/ntr/ntz056.
   PubMed Web of Science ®Google Scholar
• Ozturk B, Pogun S, Kanit L. Increased alcohol preference and intake in nicotine-preferring rats. Am J Drug Alcohol Abuse. 2020 3;46:408–20. doi:10.1080/00952990.2019.1695808.
   PubMed Web of Science ®Google Scholar