Alcohol
Volume 31, Issue 1 , Pages 1-10 , August 2003

Opposing effects of ethanol and nicotine on hippocampal calbindin-D28k expression

  • Patrick J Mulholland

      Affiliations

    • Department of Psychology, University of Kentucky, 115 Kastle Hall, Lexington, KY 40506-0044, USA
  • ,
  • Barton R Harris

      Affiliations

    • Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, A. B. Chandler Medical Center MS 305, Lexington, KY 40536-0298, USA
  • ,
  • Lincoln H Wilkins Jr.

      Affiliations

    • Department of Behavioral Science, University of Kentucky College of Medicine, College of Medicine Office Building, Lexington, KY 40536-0086, USA
  • ,
  • Rachel L Self

      Affiliations

    • Department of Psychology, University of Kentucky, 115 Kastle Hall, Lexington, KY 40506-0044, USA
  • ,
  • John A Blanchard II

      Affiliations

    • Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, A. B. Chandler Medical Center MS 305, Lexington, KY 40536-0298, USA
  • ,
  • Robert C Holley

      Affiliations

    • Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, A. B. Chandler Medical Center MS 305, Lexington, KY 40536-0298, USA
  • ,
  • John M Littleton

      Affiliations

    • Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, A. B. Chandler Medical Center MS 305, Lexington, KY 40536-0298, USA
  • ,
  • Mark A Prendergast

      Affiliations

    • Department of Psychology, University of Kentucky, 115 Kastle Hall, Lexington, KY 40506-0044, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1-859-257-6120; fax: +1-859-323-1979.

Received 24 March 2003 ,Revised 4 August 2003 ,Accepted 12 September 2003.

References 

  1. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci. 2000;20:2896–2903
  2. Akaike A, Tamura Y, Yokota T, Shimohama S, Kimura J. Nicotine-induced protection of cultured cortical neurons against N-methyl-d-aspartate receptor–mediated glutamate cytotoxicity. Brain Res. 1994;644:181–187
  3. Albuquerque EX, Alkondon M, Pereira EFR, Castro NG, Schrattenholz A, Barbosa CTF, et al. Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther. 1997;280:1117–1136
  4. Baimbridge KG, Celio MR, Rogers JH. Calcium-binding proteins in the nervous system. Trends Neurosci. 1992;15:303–308
  5. Baimbridge KG, Miller JJ, Parkes CO. Calcium-binding protein distribution in the rat brain. Brain Res. 1982;239:519–525
  6. Becker HC, Veatch LM, Diaz-Granados JL. Repeated ethanol withdrawal experience selectively alters sensitivity to different chemoconvulsant drugs in mice. Psychopharmacology (Berl). 1998;139:145–153
  7. Blaustein MP. Calcium transport and buffering in neurons. Trends Neurosci. 1988;11:438–443
  8. Choi DW. Excitotoxic cell death. J Neurobiol. 1992;23:1261–1276
  9. Christakos S, Rhoten WB, Feldman SC. Rat calbindin D28K: purification, quantitation, immunocytochemical localization, and comparative aspects. Methods Enzymol. 1987;139:534–551
  10. Collins MA, Zou J-Y, Neafsey EJ. Brain damage due to episodic alcohol exposure in vivo and in vitro: furosemide neuroprotection implicates edema-based mechanism. FASEB J. 1998;12:221–230
  11. Davies ARL, Hardick DJ, Blagbrough IS, Potter BVL, Wolstenholme AJ, Wonnacott S. Characterisation of the binding of [3H]methyllycaconitine: a new radioligand for labelling α7-type neuronal nicotinic acetylcholine receptors. Neuropharmacology. 1999;38:679–690
  12. Devaud LL, Morrow AL. Gender-selective effects of ethanol dependence on NMDA receptor subunit expression in cerebral cortex, hippocampus and hypothalamus. Eur J Pharmacol. 1999;369:331–334
  13. Foulds J, Stapleton J, Swettenham J, Bell N, McSorley K, Russel MA. Cognitive performance effects of subcutaneous nicotine in smokers and never-smokers. Psychopharmacology (Berl). 1996;127:31–38
  14. Gonzalez LP, Veatch LM, Ticku MK, Becker HC. Alcohol withdrawal kindling: mechanisms and implications for treatment. Alcohol Clin Exp Res (5 Suppl ISBRA). 2001;25:197S–201S
  15. Gross MD, Gosnell M, Tsarbopoulos A, Hunziker W. A functional and degenerate pair of EF hands contains the very high affinity calcium-binding site of calbindin-D28K. J Biol Chem. 1993;268:20917–20922
  16. Guo Q, Christakos S, Robinson N, Mattson MP. Calbindin D28k blocks the proapoptotic actions of mutant presenilin 1: reduced oxidative stress and preserved mitochondrial function. Proc Natl Acad Sci U S A. 1998;95:3227–3232
  17. Harper CG, Kril JJ, Holloway RL. Brain shrinkage in chronic alcoholics: a pathological study. Br Med J (Clin Res Ed). 1985;290:501–504
  18. Henningfield JE, Stapleton JM, Benowitz NL, Grayson RF, London ED. Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug Alcohol Depend. 1993;33:23–29
  19. Institute of Laboratory Animal Resources , Commission on Life Sciences , National Research Council . Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press; 1996;
  20. Jande SS, Maler L, Lawson DE. Immunohistochemical mapping of vitamin D–dependent calcium-binding protein in brain. Nature. 1981;294:765–767
  21. Kaneko S, Maeda T, Kume T, Kochiyama H, Akaike A, Shimohama S, et al. Nicotine protects cultured cortical neurons against glutamate-induced cytotoxicity via α7-neuronal receptors and neuronal CNS receptors. Brain Res. 1997;765:135–140
  22. le Novère N, Changeux J-P. Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells. J Mol Evol. 1995;40:155–172
  23. Littleton J, Little H. Current concepts of ethanol dependence. Addiction. 1994;89:1397–1412
  24. Littleton JM, Little HJ, Laverty R. Role of neuronal calcium channels in ethanol dependence: from cell cultures to the intact animal. Ann N Y Acad Sci. 1992;654:324–334
  25. Littleton JM, Little HJ, Whittington MA. Effects of dihydropyridine calcium channel antagonists in ethanol withdrawal; doses required, stereospecificity and actions of Bay K 8644. Psychopharmacology (Berl). 1990;100:387–392
  26. Lukas RJ, Changeux J-P, le Novère N, Albuquerque EX, Balfour DJK, Berg DK, et al. International Union of Pharmacology. XX. Current status of the nomenclature for nicotinic acetylcholine receptors and their subunits. Pharmacol Rev. 1999;51:397–401
  27. Marin P, Maus M, Desagher S, Glowinski J, Premont J. Nicotine protects cultured striatal neurones against N-methyl-d-aspartate receptor–mediated neurotoxicity. Neuroreport. 1994;5:1977–1980
  28. Marks JL, Hill EM, Pomerleau CS, Mudd SA, Blow FC. Nicotine dependence and withdrawal in alcoholic and nonalcoholic ever-smokers. J Subst Abuse Treat. 1997;14:521–527
  29. Mattson MP, Rychlik B, Chu C, Christakos S. Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron. 1991;6:41–51
  30. Mayer S, Harris BR, Gibson DA, Blanchard JA, Prendergast MA, Holley RC, et al. Acamprosate, MK-801, and ifenprodil inhibit neurotoxicity and calcium entry induced by ethanol withdrawal in organotypic slice cultures from neonatal rat hippocampus. Alcohol Clin Exp Res. 2002;26:1468–1478
  31. McAlhany RE, West JR, Miranda RC. Glial-derived neurotrophic factor rescues calbindin-D28k-immunoreactive neurons in alcohol-treated cerebellar explant cultures. J Neurobiol. 1997;33:835–847
  32. Meier TJ, Ho DY, Park TS, Sapolsky RM. Gene transfer of calbindin D28k cDNA via herpes simplex virus amplicon vector decreases cytoplasmic calcium ion response and enhances neuronal survival following glutamatergic challenge but not following cyanide. J Neurochem. 1998;71:1013–1023
  33. Meier TJ, Ho DY, Sapolsky RM. Increased expression of calbindin D28k via herpes simplex virus amplicon vector decreases calcium ion mobilization and enhances neuronal survival after hypoglycemic challenge. J Neurochem. 1997;69:1039–1047
  34. Messi ML, Renganathan M, Grigorenko E, Delbono O. Activation of α7 nicotinic acetylcholine receptor promotes survival of spinal cord motoneurons. FEBS Lett. 1997;411:32–38
  35. Mogg AJ, Whiteaker P, McIntosh JM, Marks M, Collins AC, Wonnacott S. Methyllycaconitine is a potent antagonist of α-conotoxin-MII–sensitive presynaptic nicotinic acetylcholine receptors in rat striatum. J Pharmacol Exp Ther. 2002;302:197–204
  36. Muller D, Buchs PA, Stoppini L. Time course of synaptic development in hippocampal organotypic cultures. Brain Res Dev Brain Res. 1993;71:93–100
  37. Nakao N. An increase in intracellular levels of cyclic AMP produces trophic effects on striatal neurons developing in culture. Neuroscience. 1998;82:1009–1020
  38. Obernier JA, Bouldin TW, Crews FT. Binge ethanol exposure in adult rats causes necrotic cell death. Alcohol Clin Exp Res. 2002;26:547–557
  39. Pfefferbaum A, Rosenbloom M, Serventi KL, Sullivan EV. Corpus callosum, pons, and cortical white matter in alcoholic women. Alcohol Clin Exp Res. 2002;26:400–406
  40. Phillips RG, Meier TJ, Giuli LC, McLaughlin JR, Ho DY, Spolsky RM. Calbindin D28K gene transfer via herpes simplex virus amplicon vector decreases hippocampal damage in vivo following neurotoxic insults. J Neurochem. 1999;73:1200–1205
  41. Prendergast MA, Harris BR, Blanchard JA, Mayer S, Gibson DA, Littleton JM. In vitro effects of ethanol withdrawal and spermidine on viability of hippocampus from male and female rat. Alcohol Clin Exp Res. 2000;24:1855–1861
  42. Prendergast MA, Harris BR, Mayer S, Holley RC, Hauser KF, Littleton JM. Chronic nicotine exposure reduces N-methyl-d-aspartate receptor–mediated damage in the hippocampus without altering calcium accumulation or extrusion: evidence of calbindin-D28K overexpression. Neuroscience. 2001;102:75–85
  43. Prendergast MA, Harris BR, Mayer S, Holley RC, Pauly JR, Littleton JM. Nicotine exposure reduces N-methyl-d-aspartate toxicity in the hippocampus: relation to distribution of the α7 nicotinic acetylcholine receptor subunit. Med Sci Monit. 2001;7:1153–1160
  44. Prendergast MA, Harris BR, Mayer S, Littleton JM. Chronic, but not acute, nicotine exposure attenuates ethanol withdrawal–induced hippocampal damage in vitro. Alcohol Clin Exp Res. 2000;24:1583–1592
  45. Rintoul GL, Raymond LA, Baimbridge KG. Calcium buffering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells. Cell Calcium. 2001;29:277–287
  46. Ruhe CA, Littleton JM. The possible role of voltage-operated calcium channels in the enhancement of excitatory amino acid toxicity following chronic ethanol exposure in vitro. Alcohol Alcohol Suppl. 1994;2:217–221
  47. Satriotomo I, Miki T, Itoh M, Ameno K, Ijiri I, Takeuchi Y. Short-term ethanol exposure alters calbindin D28k and glial fibrillary acidic protein immunoreactivity in hippocampus of mice. Brain Res. 2000;879:55–64
  48. Satriotomo I, Miki T, Itoh M, Xie Q, Ameno K, Takeuchi Y. Effect of short-term ethanol exposure on the suprachiasmatic nucleus of hypothalamus: immunohystochemical study in mice. Brain Res. 1999;847:124–129
  49. Scharfman HE, Goodman JH, Sollas AL. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci. 2000;20:6144–6158
  50. Sharp FR, Liu J, Bernabeu R. Neurogenesis following brain ischemia. Brain Res Dev Brain Res. 2002;134:23–30
  51. Shimohama S, Akaike A, Kimura J. Nicotine-induced protection against glutamate cytotoxicity. Nicotinic cholinergic receptor–mediated inhibition of nitric oxide formation. Ann N Y Acad Sci. 1996;777:356–361
  52. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991;37:173–182
  53. Takasawa K-I, Kitagawa K, Yagita Y, Sasaki T, Tanaka S, Matsushita K, et al. Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 2002;22:299–307
  54. Thomas MP, Monaghan DT, Morrisett RA. Evidence for a causative role of N-methyl-d-aspartate receptors in an in vitro model of alcohol withdrawal hyperexcitability. J Pharmacol Exp Ther. 1998;287:87–97
  55. Thomas MP, Morrisett RA. Dynamics of NMDAR-mediated neurotoxicity during chronic ethanol exposure and withdrawal. Neuropharmacology. 2000;39:218–226
  56. Treinin M, Chalfie M. A mutated acetylcholine receptor subunit causes neuronal degeneration in C. elegans. Neuron. 1995;14:871–877
  57. Tsai G, Coyle JT. The role of glutamatergic neurotransmission in the pathophysiology of alcoholism. Annu Rev Med. 1998;49:173–184
  58. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J, et al. Distribution of α2, α3, α4, and β2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol. 1989;284:314–335
  59. Walton TG. Smoking and alcoholism: a brief report. Am J Psychiatry. 1981;11:139–140
  60. Watson WP, Little HJ. Correlation between increases in dihydropyridine binding in vivo and behavioral signs of ethanol withdrawal in mice. Alcohol Alcohol. 1999;34:35–42
  61. Wernyj RP, Mattson MP, Christakos S. Expression of calbindin-D28k in C6 glial cells stabilizes intracellular calcium levels and protects against apoptosis induced by calcium ionophore and amyloid β-peptide. Brain Res Mol Brain Res. 1999;64:69–79
  62. Wesnes K, Revell A. The separate and combined effects of scopolamine and nicotine on human information processing. Psychopharmacology (Berl). 1984;84:5–11
  63. Wesnes K, Warburton DM. The effects of cigarettes of varying yield on rapid information processing performance. Psychopharmacology (Berl). 1984;82:338–342

 A paper published as a high-priority communication is one that reviewers have identified as being of high scientific significance and have recommended that the study findings should be communicated to the scientific community as soon as possible.

PII: S0741-8329(03)00191-5

doi: 10.1016/j.alcohol.2003.09.001

Alcohol
Volume 31, Issue 1 , Pages 1-10 , August 2003