Skip to main content

Advertisement

SpringerLink
Log in

Effects of Systemic Nicotine, Alcohol or Their Combination on Cholinergic Markers in the Frontal Cortex and Hippocampus of Rat

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Acute alcohol (Alc) intoxication has been shown to decrease choline acetyltransferase (ChAT) in the rat brain. The present study extends that finding by examining the effects of nicotine (Nic), Alc, and their combination on ChAT and acetylcholinesterase (AChE) in the frontal cortex and hippocampus of rat. The samples were collected at 30 and 120 min after intraperitoneal administration of saline (0.9%, control), Nic (1 mg/kg), Alc (1 g/kg), and Nic + Alc and analyzed by RT-PCR, Western blot and colorimetry. Alc alone considerably reduced ChAT mRNA expression, whereas Nic alone decreased AChE mRNA expression. In contrast, Nic + Alc exposure had resulted in no significant change in the parameters. These findings are consistent with the results of the Western blot and AChE activity analysis. The results, therefore, indicate that Nic and Alc alone may interact with the central cholinergic system. This interactive effect may contribute to a frequent association of tobacco and Alc consumption.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Prendergast MA, Harris BR, Mayer S et al (2000) Chronic, but not acute, nicotine exposure attenuates ethanol withdrawal-induced hippocampal damage in vitro. Alcohol Clin Exp Res 24:1583–1592

    Article  CAS  PubMed  Google Scholar 

  2. Tizabi Y, Manaye KF, Taylor RE (2005) Nicotine blocks ethanol-induced apoptosis in primary cultures of rat cerebral cortical and cerebellar granule cells. Neurotoxicol Res 7:319–322

    Article  CAS  Google Scholar 

  3. Korkosz A, Zatorski P, Taracha E et al (2006) Ethanol blocks nicotine-induced seizures in mice: comparison with midazolam and baclofen. Alcohol 40:151–157

    Article  CAS  PubMed  Google Scholar 

  4. Tizabi Y, Bai L, Copeland RL Jr et al (2007) Combined effects of systemic alcohol and nicotine on dopamine release in the nucleus accumbens shell. Alcohol Alcohol 42:413–416

    CAS  PubMed  Google Scholar 

  5. Vizi ES, Lendvai B (1999) Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res Rev 30:219–235

    Article  CAS  PubMed  Google Scholar 

  6. Tomkins DM, Sellers EM (2001) Addiction and the brain: the role of neurotransmitters in the cause and treatment of drug dependence. Canadian Med Asso J 164:817–821

    CAS  Google Scholar 

  7. Picciotto MR, Zoli M, Rimondini R et al (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173–177

    Article  CAS  PubMed  Google Scholar 

  8. Kamens HM, Andersen J, Picciotto MR (2010) Modulation of ethanol consumption by genetic and pharmacological manipulation of nicotinic acetylcholine receptors in mice. Psychopharmacology 208:613–626

    Article  CAS  Google Scholar 

  9. Farook JM, Lewis B, Gaddis JG et al (2009) Effects of mecamylamine on alcohol consumption and preference in male C57BL/6J mice. Pharmacology 83:379–384

    Article  CAS  PubMed  Google Scholar 

  10. Nadal R, Chappell AM, Samson HH (1998) Effects of nicotine and mecamylamine microinjections into the nucleus accumbens on ethanol and sucrose self-administration. Alcohol Clin Exp Res 22:1190–1198

    CAS  PubMed  Google Scholar 

  11. Steensland P, Simms JA, Holgate J et al (2007) Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, selectively decreases ethanol consumption and seeking. Proc Natl Acad Sci USA 104:12518–12523

    Article  CAS  PubMed  Google Scholar 

  12. McKee SA, Harrison EL, O’Malley SS et al (2009) Varenicline reduces alcohol self-administration in heavy-drinking smokers. Biol Psychiat 66:185–190

    Article  CAS  PubMed  Google Scholar 

  13. Ceballos NA (2006) Tobacco use, alcohol dependence, and cognitive performance. J Gen Psycho 133:375–388

    Article  Google Scholar 

  14. Castellsagué X, Muñoz N, De Stefani E et al (1999) Independent and joint effects of tobacco smoking and alcohol drinking on the risk of esophageal cancer in men and women. Int J Cancer 82:657–664

    Article  PubMed  Google Scholar 

  15. Little HJ (2000) Behavioral mechanisms underlying the link between smoking and drinking. Alcohol Res Health 24:215–224

    CAS  PubMed  Google Scholar 

  16. Checkoway H, Powers K, Smith-Weller T et al (2002) Parkinson’s disease risks associated with cigarette smoking, alcohol consumption, and caffeine intake. Am J Epidemio 155:732–738

    Article  Google Scholar 

  17. Weiss S, Nosten-Bertrand M, McIntosh JM et al (2007) Nicotine improves cognitive deficits of dopamine transporter knockout mice without long-term tolerance. Neuropsychopharmacology 32:2465–2478

    Article  CAS  PubMed  Google Scholar 

  18. Pogocki D, Ruman T, Danilczuk M et al (2007) Application of nicotine enantiomers, derivatives and analogues in therapy of neurodegenerative disorders. Eur J Pharmacol 563:18–39

    Article  CAS  PubMed  Google Scholar 

  19. Dani JA, Bertrand D (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47:699–729

    Article  CAS  PubMed  Google Scholar 

  20. Larsson A, Engel JA (2004) Neurochemical and behavioral studies on ethanol and nicotine interactions. Neurosci Biobehav Rev 27:713–720

    Article  CAS  PubMed  Google Scholar 

  21. Chen WJ, Parnell SE, West JR (1999) Effects of alcohol and nicotine on developing olfactory bulb: loss of mitral cells and alterations in neurotransmitter levels. Alcohol Clin Exp Res 23:18–25

    CAS  PubMed  Google Scholar 

  22. Kashkin VA, De Witte P (2005) Nicotine increases microdialysate brain amino acid concentrations and induces conditioned place preference. Eur Neuropsychopharmacol 15:625–632

    Article  CAS  PubMed  Google Scholar 

  23. Moriguchi S, Zhao X, Marszalec W et al (2007) Effects of ethanol on excitatory and inhibitory synaptic transmission in rat cortical neurons. Alcohol Clin Exp Res 31:89–99

    Article  CAS  PubMed  Google Scholar 

  24. Abou-Donia MB, Abdel-Rahman A, Goldstein LB et al (2003) Sensorimotor deficits and increased brain nicotinic acetylcholine receptors following exposure to chlorpyrifos and/or nicotine in rats. Arch Toxicol 77:452–458

    Article  CAS  PubMed  Google Scholar 

  25. Nordberg A, Romanelli L, Sundwall A et al (1989) Effect of acute and subchronic nicotine treatment on cortical acetylcholine release and on nicotinic receptors in rats and guinea-pigs. Br J Pharmacol 98:71–78

    CAS  PubMed  Google Scholar 

  26. Jamal M, Ameno K, Ameno S et al (2007) Changes in cholinergic function in the frontal cortex and hippocampus of rat exposed to ethanol and acetaldehyde. Neuroscience 144:232–238

    Article  CAS  PubMed  Google Scholar 

  27. Wang H, Carlier PR, Ho WL et al (1999) Effects of bis (7)-tacrine, a novel anti-Alzheimer’s agent, on rat brain AChE. Neuroreport 10:789–793

    Article  CAS  PubMed  Google Scholar 

  28. Jamal M, Ameno K, Uekita I et al (2007) Catalase mediates acetaldehyde formation in the striatum of free-moving rats. Neurotoxicology 28:1245–1248

    Article  CAS  PubMed  Google Scholar 

  29. Jamal M, Ameno K, Kumihashi M et al (2004) Failure of ethanol and acetaldehyde to alter in vivo norepinephrine release in the striatum and hippocampus of rats. Arch Toxicol 78:723–727

    Article  CAS  PubMed  Google Scholar 

  30. Ilbäck NG, Stålhandske T (2003) Nicotine accumulation in the mouse brain is age-dependent and is quantitatively different in various segments. Toxicol Lett 143:175–184

    Article  PubMed  CAS  Google Scholar 

  31. Jamal M, Ameno K, Wang W et al (2005) Inhibition of acetaldehyde metabolism decreases acetylcholine release in medial frontal cortex of freely moving rats. Brain Res 1039:90–96

    Article  CAS  PubMed  Google Scholar 

  32. Stancampiano R, Carta M, Cocco S et al (2004) Biphasic effects of ethanol on acetylcholine release in the rat prefrontal cortex. Brain Res 997:128–132

    Article  CAS  PubMed  Google Scholar 

  33. Owasoyo JO, Iramain CA (1981) Effect of acute ethanol intoxication on the enzymes of the cholinergic system in mouse brain. Toxicol Lett 9:267–270

    Article  CAS  PubMed  Google Scholar 

  34. Floyd EA, Young-Seigler AC, Ford BD (1997) Chronic ethanol ingestion produces cholinergic hypofunction in rat brain. Alcohol 14:93–98

    Article  CAS  PubMed  Google Scholar 

  35. Durkin TP, Hashem-Zadeh H, Mandel P et al (1982) A comparative study of the acute effects of ethanol on the cholinergic system in hippocampus and striatum of inbred mouse strains. J Pharmacol Exp Ther 220:203–208

    CAS  PubMed  Google Scholar 

  36. Hsu LL, Samorajski T, Claghorn JL (1983) Effects of acute and chronic ethanol and dihydroergotoxine (Hydergine) on neurotransmitter enzymes in brain. Alcohol Clin Exp Res 7:249–255

    Article  CAS  PubMed  Google Scholar 

  37. Chang PL, Bhagat B, Taylor JJ (1973) Effect of chronic administration of nicotine on acetylcholinesterase activity in the hypothalamus and medulla oblongata of the rat brain. An ultrastructural study. Brain Res 54:75–84

    Article  CAS  PubMed  Google Scholar 

  38. Trauth JA, McCook EC, Seidler FJ et al (2000) Modeling adolescent nicotine exposure: effects on cholinergic systems in rat brain regions. Brain Res 873:18–25

    Article  CAS  PubMed  Google Scholar 

  39. Ribeiro-Carvalho A, Lima CS, Filgueiras CC et al (2008) Nicotine and ethanol interact during adolescence: effects on the central cholinergic systems. Brain Res 1232:48–60

    Article  CAS  PubMed  Google Scholar 

  40. Tani Y, Saito K, Imoto M et al (1998) Pharmacological characterization of nicotinic receptor-mediated acetylcholine release in rat brain–an in vivo microdialysis study. Eur J Pharmacol 351:181–188

    Article  CAS  PubMed  Google Scholar 

  41. Chen WJ, Harle LK (2005) Interactive effect of alcohol and nicotine on developing cerebellum: an investigation of the temporal pattern of alcohol and nicotine administration. Alcohol Clin Exp Res 29:437–442

    Article  PubMed  Google Scholar 

  42. Bachtell RK, Ryabinin AE (2001) Interactive effects of nicotine and alcohol co-administration on expression of inducible transcription factors in mouse brain. Neuroscience 103:941–954

    Article  CAS  PubMed  Google Scholar 

  43. Jang MH, Shin MC, Jung SB et al (2002) Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. Neuroreport 13:1509–1513

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the Grant-in-Aid for Scientific Research [Grand No. (c) 18590637, 20590681] from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Author information

Authors and Affiliations

  1. Department of Forensic Medicine, Faculty of Medicine, Kagawa University, 1750-1, Ikenobe, Miki, Kita, Kagawa, 761-0793, Japan

    Mostofa Jamal, Kiyoshi Ameno, Naoko Tanaka, Eriko Ohkubo & Hiroshi Kinoshita

  2. Department of Anatomy and Neurobiology, Faculty of Medicine, Kagawa University, Miki, Kita, Kagawa, Japan

    Takanori Miki

Authors
  1. Mostofa Jamal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kiyoshi Ameno
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takanori Miki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naoko Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eriko Ohkubo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroshi Kinoshita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mostofa Jamal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jamal, M., Ameno, K., Miki, T. et al. Effects of Systemic Nicotine, Alcohol or Their Combination on Cholinergic Markers in the Frontal Cortex and Hippocampus of Rat. Neurochem Res 35, 1064–1070 (2010). https://doi.org/10.1007/s11064-010-0155-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-010-0155-x

Keywords

Search

Navigation