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Alcohol and Cocaine Exposure Modulates ABCB1 and ABCG2 Transporters in Male Alcohol-Preferring Rats

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Abstract

Two efflux transporters, ATP-binding cassettes B1 (ABCB1) and G2 (ABCG2), are highly expressed in the endothelial cells of the brain, where they regulate the bioavailability and distribution of several endogenous and xenobiotic compounds. However, whether ABCB1 or ABCG2 has any link with drug dependence, drug withdrawal effects, or the incidence of adverse effects in drug abuser is not known. In this study, we determined the effects of voluntary ethanol consumption following repeated exposure to cocaine or vehicle on the relative mRNA and protein expression of Abcg2/ABCG2 and Abcb1/ABCB1 in the nucleus accumbens (NAc) and medial prefrontal cortex (mPFC) of male alcohol-preferring (P) rats. Male P rats were allowed free choice access to ethanol (15 and 30% v/v) and water for 5 weeks to establish baseline drinking behavior. The following week, rats were either injected with 20 mg/kg i.p. of cocaine or saline, once a day, for 7 days. The relative mRNA and protein expression of Abcb1/ABCB1 and Abcg2/ABCG2 in the NAc and mPFC were significantly decreased in ethanol-saline- and ethanol-cocaine-exposed rats compared to control rats that received neither ethanol nor cocaine. Thus, prolonged exposure to commonly abused drugs, ethanol and cocaine, alters the expression of Abcb1/ABCB1 and Abcg2/ABCG2 mRNA and protein levels in brain areas that play a role in drug dependence.

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References

  1. Pal D, Mitra AK (2006) MDR-and CYP3A4-mediated drug–drug interactions. J NeuroImmune Pharmacol 1(3):323–339

    Article  PubMed  Google Scholar 

  2. Gottesman MM, Fojo T, Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2(1):48–58

    Article  CAS  PubMed  Google Scholar 

  3. Chan LM, Lowes S, Hirst BH (2004) The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability. Eur J Pharm Sci 21(1):25–51

    Article  CAS  PubMed  Google Scholar 

  4. Goldsmith D, Jayawardene S, Ackland P (2013) ABC of kidney disease. 2nd Edition, Vol. 76. Wiley.

  5. Planas JM, Alfaras I, Colom H, Juan ME (2012) The bioavailability and distribution of trans-resveratrol are constrained by ABC transporters. Arch Biochem Biophys 527(2):67–73

    Article  CAS  PubMed  Google Scholar 

  6. Löscher W, Potschka H (2005) Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2(1):86–98

    Article  PubMed  PubMed Central  Google Scholar 

  7. Uhr M, Steckler T, Yassouridis A, Holsboer F (2000) Penetration of amitriptyline, but not of fluoxetine, into brain is enhanced in mice with blood-brain barrier deficiency due to mdr1a P-glycoprotein gene disruption. Neuropsychopharmacology 22(4):380–387

    Article  CAS  PubMed  Google Scholar 

  8. Antoniou T, Tseng AL-i (2002) Interactions between recreational drugs and antiretroviral agents. Ann Pharmacother 36(10):1598–1613

    Article  CAS  PubMed  Google Scholar 

  9. Bouër R, Barthe L, Philibert C, Tournaire C, Woodley J, Houin G (1999) The roles of P-glycoprotein and intracellular metabolism in the intestinal absorption of methadone: in vitro studies using the rat everted intestinal sac. Fundam Clin Pharmacol 13(4):494–500

    Article  PubMed  Google Scholar 

  10. Tournier N, Chevillard L, Megarbane B, Pirnay S, Scherrmann JM, Declèves X (2010) Interaction of drugs of abuse and maintenance treatments with human P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2). Int J Neuropsychopharmacol 13(7):905–915

    Article  CAS  PubMed  Google Scholar 

  11. Wandel C, Kim R, Wood M, Wood A (2002) Interaction of morphine, fentanyl, sufentanil, alfentanil, and loperamide with the efflux drug transporter P-glycoprotein. Anesthesiology 96(4):913–920

    Article  CAS  PubMed  Google Scholar 

  12. Suzuki T, Zaima C, Moriki Y, Fukami T, Tomono K (2007) P-glycoprotein mediates brain-to-blood efflux transport of buprenorphine across the blood–brain barrier. J Drug Target 15(1):67–74

    Article  CAS  PubMed  Google Scholar 

  13. Störmer E et al (2001) Methadone inhibits rhodamine123 transport in Caco-2 cells. Drug Metab Dispos 29(7):954–956

    PubMed  Google Scholar 

  14. Dagenais C, Graff CL, Pollack GM (2004) Variable modulation of opioid brain uptake by P-glycoprotein in mice. Biochem Pharmacol 67(2):269–276

    Article  CAS  PubMed  Google Scholar 

  15. Wang J-S, Ruan Y, Taylor RM, Donovan JL, Markowitz JS, DeVane CL (2004) Brain penetration of methadone (R)- and (S)-enantiomers is greatly increased by P-glycoprotein deficiency in the blood–brain barrier of Abcb1a gene knockout mice. Psychopharmacology 173(1–2):132–138

    Article  CAS  PubMed  Google Scholar 

  16. Santillano DR, Kumar LS, Prock TL, Camarillo C, Tingling JD, Miranda RC (2005) Ethanol induces cell-cycle activity and reduces stem cell diversity to alter both regenerative capacity and differentiation potential of cerebral cortical neuroepithelial precursors. BMC Neurosci 6(1):59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Sauna ZE, Peng XH, Nandigama K, Tekle S, Ambudkar SV (2004) The molecular basis of the action of disulfiram as a modulator of the multidrug resistance-linked ATP binding cassette transporters MDR1 (ABCB1) and MRP1 (ABCC1). Mol Pharmacol 65(3):675–684

    Article  CAS  PubMed  Google Scholar 

  18. Bradbury MW (1985) The blood-brain barrier. Transport across the cerebral endothelium. Circ Res 57(2):213–222

    Article  CAS  PubMed  Google Scholar 

  19. Zhang HF, Lin XH, Yang H, Zhou LC, Guo YL, Barnett JV, Guo ZM (2012) Regulation of the activity and expression of aryl hydrocarbon receptor by ethanol in mouse hepatic stellate cells. Alcohol Clin Exp Res 36(11):1873–1881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Qin L, Crews FT (2012) Chronic ethanol increases systemic TLR3 agonist-induced neuroinflammation and neurodegeneration. J Neuroinflammation 9(1):130

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Evseenko DA, Paxton JW, Keelan JA (2007) Independent regulation of apical and basolateral drug transporter expression and function in placental trophoblasts by cytokines, steroids, and growth factors. Drug Metab Dispos 35(4):595–601

    Article  CAS  PubMed  Google Scholar 

  22. Riezzo I, Fiore C, de Carlo D, Pascale N, Neri M, Turillazzi E, Fineschi V (2012) Side effects of cocaine abuse: multiorgan toxicity and pathological consequences. Curr Med Chem 19(33):5624–5646

    Article  CAS  PubMed  Google Scholar 

  23. Chapy H et al (2014) Carrier-mediated cocaine transport at the blood-brain barrier as a putative mechanism in addiction liability. Int J Neuropsychopharmacol 18(1):pyu001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. André P, Debray M, Scherrmann JM, Cisternino S (2009) Clonidine transport at the mouse blood–brain barrier by a new H+ antiporter that interacts with addictive drugs. J Cereb Blood Flow Metab 29(7):1293–1304

    Article  PubMed  CAS  Google Scholar 

  25. Hammad AM, Alasmari F, Althobaiti YS, Sari Y (2017) Modulatory effects of ampicillin/sulbactam on glial glutamate transporters and metabotropic glutamate receptor 1 as well as reinstatement to cocaine-seeking behavior. Behav Brain Res 332:288–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Volkow ND, Fowler JS, Wolf AP, Schlyer D, Shiue CY, Alpert R, Dewey SL, Logan J et al (1990) Effects of chronic cocaine abuse on postsynaptic dopamine receptors. Am J Psychiatry 147(6):719–724

    Article  CAS  PubMed  Google Scholar 

  27. Lasoñ Waa (2001) Neurochemical and pharmacological aspects of cocaine-induced seizures. Pol J Pharmacol 53(1):57–60

    Article  PubMed  Google Scholar 

  28. López-Pedrajas R, Ramírez-Lamelas DT, Muriach B, Sánchez-Villarejo MV, Almansa I, Vidal-Gil L, Romero FJ, Barcia JM, Muriach M (2015) Cocaine promotes oxidative stress and microglial-macrophage activation in rat cerebellum. Front Cell Neurosci 9, 279

  29. Hu S, Cheeran MC, Sheng WS, Ni HT, Lokensgard JR, Peterson PK (2006) Cocaine alters proliferation, migration, and differentiation of human fetal brain-derived neural precursor cells. J Pharmacol Exp Ther 318(3):1280–1286

    Article  CAS  PubMed  Google Scholar 

  30. Liu H et al. (2016) CXCR4 promotes growth and sphere formation of hypoxic breast cancer side 7 population cells via activation of c-Jun/ABCG2 pathway. Oncol Res

  31. Liptrott N, Penny M, Bray PG, Sathish J, Khoo SH, Back DJ, Owen A (2009) The impact of cytokines on the expression of drug transporters, cytochrome P450 enzymes and chemokine receptors in human PBMC. Br J Pharmacol 156(3):497–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Alasmari F, Abuhamdah S, Sari Y (2015) Effects of ampicillin on cystine/glutamate antiporter and glutamate transporter 1 isoforms as well as ethanol drinking in male P rats. Neurosci Lett 600:148–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hammad AM, Althobaiti YS, Das SC, Sari Y (2017) Effects of repeated cocaine exposure and withdrawal on voluntary ethanol drinking, and the expression of glial glutamate transporters in mesocorticolimbic system of P rats. Mol Cell Neurosci 82:58–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sari Y, Sakai M, Weedman JM, Rebec GV, Bell RL (2011) Ceftriaxone, a beta-lactam antibiotic, reduces ethanol consumption in alcohol-preferring rats. Alcohol Alcohol 46(3):239–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Paxinos G, Watson C (1997) The rat brain atlas in stereotaxic coordinates, compact. Academic Press, New York

    Google Scholar 

  36. Sari Y, Sreemantula S (2012) Neuroimmunophilin GPI-1046 reduces ethanol consumption in part through activation of GLT1 in alcohol-preferring rats. Neuroscience 227:327–335

    Article  CAS  PubMed  Google Scholar 

  37. Alasmari F, Crotty Alexander LE, Nelson JA, Schiefer IT, Breen E, Drummond CA, Sari Y (2017) Effects of chronic inhalation of electronic cigarettes containing nicotine on glial glutamate transporters and α-7 nicotinic acetylcholine receptor in female CD-1 mice. Prog Neuro-Psychopharmacol Biol Psychiatry 77:1–8

    Article  CAS  Google Scholar 

  38. Li J, Olinger AB, Dassow MS, Abel MS (2003) Up-regulation of GABAB receptor mRNA and protein in the hippocampus of cocaine-and lidocaine-kindled rats. Neuroscience 118(2):451–462

    Article  CAS  PubMed  Google Scholar 

  39. Zhang Q, Tan Y (2011) Nerve growth factor augments neuronal responsiveness to noradrenaline in cultured dorsal root ganglion neurons of rats. Neuroscience 193:72–79

    Article  CAS  PubMed  Google Scholar 

  40. Simões AP, Duarte JA, Agasse F, Canas PM, Tomé AR, Agostinho P, Cunha RA (2012) Blockade of adenosine A 2A receptors prevents interleukin-1β-induced exacerbation of neuronal toxicity through a p38 mitogen-activated protein kinase pathway. J Neuroinflammation 9(1):204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Devoto VP, Bogetti ME, de Plazas SF (2013) Developmental and hypoxia-induced cell death share common ultrastructural and biochemical apoptotic features in the central nervous system. Neuroscience 252:190–200

    Article  CAS  Google Scholar 

  42. Reichel V, Burghard S, John I, Huber O (2011) P-glycoprotein and breast cancer resistance protein expression and function at the blood–brain barrier and blood–cerebrospinal fluid barrier (choroid plexus) in streptozotocin-induced diabetes in rats. Brain Res 1370:238–245

    Article  CAS  PubMed  Google Scholar 

  43. Tawfik VL, Lacroix-Fralish ML, Bercury KK, Nutile-Mcmenemy N, Harris BT, Deleo JA (2006) Induction of astrocyte differentiation by propentofylline increases glutamate transporter expression in vitro: heterogeneity of the quiescent phenotype. Glia 54(3):193–203

    Article  PubMed  Google Scholar 

  44. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  45. Pfaffl MW (2012) Quantification strategies in real-time polymerase chain reaction. Applied microbiology. Caister Academic Press; Norfolk, UK, p. 53–61

  46. Breslin FJ, Johnson BA, Lynch WJ (2010) Effect of topiramate treatment on ethanol consumption in rats. Psychopharmacology 207(4):529–534

    Article  CAS  PubMed  Google Scholar 

  47. Sari Y, Sreemantula SN, Lee MR, Choi DS (2013) Ceftriaxone treatment affects the levels of GLT1 and ENT1 as well as ethanol intake in alcohol-preferring rats. J Mol Neurosci 51(3):779–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Parikh V, Naughton SX, Shi X, Kelley LK, Yegla B, Tallarida CS, Rawls SM, Unterwald EM (2014) Cocaine-induced neuroadaptations in the dorsal striatum: glutamate dynamics and behavioral sensitization. Neurochem Int 75:54–65

    Article  CAS  PubMed  Google Scholar 

  49. Oh JH, Lee DK, Shim YB, Ryu IS, Seo SY, Kim J, Yang JH, Cho HW et al (2015) Dopamine D4 receptors linked to protein kinase G are required for changes in dopamine release followed by locomotor activity after repeated cocaine administration. Exp Brain Res 233(5):1511–1518

    Article  CAS  PubMed  Google Scholar 

  50. Alasmari F, Bell RL, Rao PSS, Hammad AM, Sari Y (2018) Peri-adolescent drinking of ethanol and/or nicotine modulates astroglial glutamate transporters and metabotropic glutamate receptor-1 in female alcohol-preferring rats. Pharmacol Biochem Behav 170:44–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bell RL, Rodd ZA, Sable HJK, Schultz JA, Hsu CC, Lumeng L, Murphy JM, McBride WJ (2006) Daily patterns of ethanol drinking in peri-adolescent and adult alcohol-preferring (P) rats. Pharmacol Biochem Behav 83(1):35–46

    Article  CAS  PubMed  Google Scholar 

  52. Doremus TL, Brunell SC, Rajendran P, Spear LP (2005) Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 29(10):1796–1808

    Article  PubMed  Google Scholar 

  53. García-Burgos D, González F, Manrique T, Gallo M (2009) Patterns of ethanol intake in preadolescent, adolescent, and adult Wistar rats under acquisition, maintenance, and relapse-like conditions. Alcohol Clin Exp Res 33(4):722–728

    Article  PubMed  CAS  Google Scholar 

  54. Miller DS (2015) Regulation of ABC transporters blood–brain barrier: the good, the bad, and the ugly. In Advances in cancer research. Elsevier. p. 43–70

  55. Mahringer A, Ott M, Reimold I, Reichel V, Fricker G (2011) The ABC of the blood-brain barrier-regulation of drug efflux pumps. Curr Pharm Des 17(26):2762–2770

    Article  CAS  PubMed  Google Scholar 

  56. Dauchy S, Dutheil F, Weaver RJ, Chassoux F, Daumas-Duport C, Couraud PO, Scherrmann JM, de Waziers I et al (2008) ABC transporters, cytochromes P450 and their main transcription factors: expression at the human blood–brain barrier. J Neurochem 107(6):1518–1528

    Article  CAS  PubMed  Google Scholar 

  57. Lemmen J, Tozakidis IEP, Bele P, Galla HJ (2013) Constitutive androstane receptor upregulates Abcb1 and Abcg2 at the blood–brain barrier after CITCO activation. Brain Res 1501:68–80

    Article  CAS  PubMed  Google Scholar 

  58. Ott M, Fricker G, Bauer B (2009) Pregnane X receptor (PXR) regulates P-glycoprotein at the blood-brain barrier: functional similarities between pig and human PXR. J Pharmacol Exp Ther 329(1):141–149

    Article  CAS  PubMed  Google Scholar 

  59. Lin X, Yang H, Zhang H, Zhou LC, Guo ZM (2013) A novel transcription mechanism activated by ethanol induction of Slc7a11 gene expression via inhibition of the DNA-binding activity of transcriptional repressor octamer-binding transcription factor 1 (OCT-1). J Biol Chem 288(21):14815–14823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wang J-P, Xu DX, Sun MF, Chen YH, Wang H, Wei W (2005) Chronic ethanol exposure downregulates hepatic expression of pregnane X receptor and P450 3A11 in female ICR mice. Toxicology 215(3):234–244

    Article  CAS  PubMed  Google Scholar 

  61. Marshall SA, Geil CR, Nixon K (2016) Prior binge ethanol exposure potentiates the microglial response in a model of alcohol-induced neurodegeneration. Brain Sci 6(2):16

    Article  PubMed Central  CAS  Google Scholar 

  62. Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT (2008) Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 5(1):10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Walther W et al (2015) Chemosensitization by diverging modulation by short-term and long-term TNF-α action on ABCB1 expression and NF-κB signaling in colon cancer. Int J Oncol 47(6):2276–2285

    Article  CAS  PubMed  Google Scholar 

  64. Alfonso-Loeches S, Pascual-Lucas M, Blanco AM, Sanchez-Vera I, Guerri C (2010) Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. J Neurosci 30(24):8285–8295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Marshall SA, Casachahua JD, Rinker JA, Blose AK, Lysle DT, Thiele TE (2016) IL-1 receptor signaling in the basolateral amygdala modulates binge-like ethanol consumption in male C57BL/6J mice. Brain Behav Immun 51:258–267

    Article  CAS  PubMed  Google Scholar 

  66. Hisaeda K, Inokuchi A, Nakamura T, Iwamoto Y, Kohno K, Kuwano M, Uchiumi T (2004) Interleukin-1β represses MRP2 gene expression through inactivation of interferon regulatory factor 3 in HepG2 cells. Hepatology 39(6):1574–1582

    Article  CAS  PubMed  Google Scholar 

  67. Chandler B, Detsika M, Khoo SH, Williams J, Back DJ, Owen A (2007) Factors impacting the expression of membrane-bound proteins in lymphocytes from HIV-positive subjects. J Antimicrob Chemother 60(3):685–689

    Article  CAS  PubMed  Google Scholar 

  68. Pandhare J, Addai AB, Mantri CK, Hager C, Smith RM, Barnett L, Villalta F, Kalams SA et al (2014) Cocaine enhances HIV-1-induced CD4+ T-cell apoptosis: implications in disease progression in cocaine-abusing HIV-1 patients. Am J Pathol 184(4):927–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Uhl GR, Drgon T, Johnson C, Fatusin OO, Liu QR, Contoreggi C, Li CY, Buck K et al (2008) “Higher order” addiction molecular genetics: convergent data from genome-wide association in humans and mice. Biochem Pharmacol 75(1):98–111

    Article  CAS  PubMed  Google Scholar 

  70. Reed B, Butelman ER, Yuferov V, Randesi M, Kreek MJ (2014) Genetics of opiate addiction. Curr Psychiatry Rep 16(11):504

    Article  PubMed  Google Scholar 

  71. Edenberg HJ, Koller DL, Xuei X, Wetherill L, McClintick JN, Almasy L, Bierut LJ, Bucholz KK et al (2010) Genome-wide association study of alcohol dependence implicates a region on chromosome 11. Alcohol Clin Exp Res 34(5):840–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Morozova TV, Anholt RR, Mackay TF (2007) Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster. Genome Biol 8(10):R231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Mulligan MK, Ponomarev I, Hitzemann RJ, Belknap JK, Tabakoff B, Harris RA, Crabbe JC, Blednov YA et al (2006) Toward understanding the genetics of alcohol drinking through transcriptome meta-analysis. Proc Natl Acad Sci U S A 103(16):6368–6373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Liu X, Liu M, Li X, Zhang L, Fan R, Wang J (2015) Prioritizing genes related to nicotine addiction via a multi-source-based approach. Mol Neurobiol 52(1):442–455

    Article  CAS  PubMed  Google Scholar 

  75. Salvatore JE, Edwards AC, McClintick JN, Bigdeli TB, Adkins A, Aliev F, Edenberg HJ, Foroud T et al (2015) Genome-wide association data suggest ABCB1 and immune-related gene sets may be involved in adult antisocial behavior. Transl Psychiatry 5:e558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Spiro AS, Wong A, Boucher AA, Arnold JC (2012) Enhanced brain disposition and effects of Delta9-tetrahydrocannabinol in P-glycoprotein and breast cancer resistance protein knockout mice. PLoS One 7(4):e35937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Alhaddad H, Cisternino S, Declèves X, Tournier N, Schlatter J, Chiadmi F, Risède P, Smirnova M et al (2012) Respiratory toxicity of buprenorphine results from the blockage of P-glycoprotein-mediated efflux of norbuprenorphine at the blood-brain barrier in mice. Crit Care Med 40(12):3215–3223

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Sujan Chandra Das and Yusuf S. Althobaiti for their contribution to the experimental procedures. We thank Dr. Charles R. Ashby Jr. (St. John’s University, Queens, NY) and Ms. Charisse Montgomery (University of Toledo, Toledo, Ohio) for critically reviewing the manuscript.

Funding

This work was supported, in part, by the National Institutes of Health (R01AA019458 to Y.S.) and the University of Toledo start-up grant (F110760) to A.K.T.

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Correspondence to Amit K. Tiwari.

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Hammad, A.M., Alasmari, F., Sari, Y. et al. Alcohol and Cocaine Exposure Modulates ABCB1 and ABCG2 Transporters in Male Alcohol-Preferring Rats. Mol Neurobiol 56, 1921–1932 (2019). https://doi.org/10.1007/s12035-018-1153-2

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