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Mild Thiamine Deficiency and Chronic Ethanol Consumption Modulate Acetylcholinesterase Activity Change and Spatial Memory Performance in a Water Maze Task

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Abstract

Chronic thiamine deficiency may be responsible for pathologic changes in the brains of alcoholics, and subclinical episodes of this vitamin deficiency may cause cumulative brain damage. In the present work, the chronic effects of ethanol and its association to a mild thiamine deficiency episode (subclinical model) on neocortical and hippocampal acetylcholinesterase activity were assessed along with their possible association to spatial cognitive dysfunction. The results indicate that in the beginning of the neurodegenerative process, before the appearance of brain lesions, chronic ethanol consumption reverses the effects of mild thiamine deficiency on both spatial cognitive performance and acetylcholinesterase activity without having significant effects on any morphometric parameter.

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References

  • Alexander-Kaufman K, Harper C (2009) Transketolase: observations in alcohol-related brain damage research. Int J Biochem Cell Biol 41:717–720

    Article  CAS  PubMed  Google Scholar 

  • Arendt T, Allen Y, Marchbanks RM, Schugens MM, Sinden J, Lantos PL, Gray JA (1989) Cholinergic system and memory in the rat: effects of chronic ethanol, embryonic basal forebrain brain transplants and excitotoxic lesions of cholinergic basal forebrain projection system. Neuroscience 33:435–462

    Article  CAS  PubMed  Google Scholar 

  • Bâ A, Seri BV, Aka KJ, Glin L, Tako A (1999) Comparative effects of developmental thiamine deficiencies and ethanol exposure on the morphometry of the CA3 pyramidal cells. Neurotoxicol Teratol 21:579–586

    Article  PubMed  Google Scholar 

  • Bizon-Zygmańska D, Jankowska-Kulawy A, Bielarczyk H, Pawełczyk T, Ronowska A, Marszałł M, Szutowicz A (2011) Acetyl-CoA metabolism in amprolium-evoked thiamine pyrophosphate deficits in cholinergic SN56 neuroblastoma cells. Neurochem Int 59:208–216

    Article  PubMed  Google Scholar 

  • Bowden SC (1990) Separating cognitive impairment in neurologically asymptomatic alcoholism from Wernicke-Korsakoff-Syndrome: is the neuropsychological distinction justified? Psychol Bull 107:355–366

    Article  CAS  PubMed  Google Scholar 

  • Butterworth RF (1986) Cerbral thiamine-dependent enzyme changes in experimental Wernicke’s encephalopathy. Metab Brain Dis 1(3):165–175

    Article  CAS  PubMed  Google Scholar 

  • Carvalho FM, Pereira SR, Pires RG, Ferraz VP, Romano-Silva MA, Oliveira-Silva IF, Ribeiro AM (2006) Thiamine deficiency decreases glutamate uptake in the prefrontal cortex and impairs spatial memory performance in a water maze test. Pharmacol Biochem Behav 83:481–489

    Article  CAS  PubMed  Google Scholar 

  • Casamenti F, Scali C, Vannucchi MG, Bartolini L, Pepeu G (1993) Long-term ethanol-consumption by rats—effect on acetylcholine-release in-vivo, choline-acetyltransferase activity, and behavior. Neuroscience 56:465–471

    Article  CAS  PubMed  Google Scholar 

  • Caulo M, Van Hecke J, Toma L, Ferretti A, Tartaro A, Colosimo C, Romani GL, Uncini A (2005) Functional MRI study of diencephalic amnesia in Wernicke-Korsakoff syndrome. Brain 128:1584–1594

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Okada S, Okeda R (1997) Causality of parenchymal and vascular changes in rats with experimental thiamine deficiency encephalopathy. Pathol Int 47:748–756

    Article  CAS  PubMed  Google Scholar 

  • Ciccia RM, Langlais PJ (2000) An examination of the synergistic interaction of ethanol and thiamine deficiency in the development of neurological signs and long-term cognitive and memory impairments. Alcohol Clin Exp Res 24:622–634

    Article  CAS  PubMed  Google Scholar 

  • Darreh-Shori T, Almkvist O, Guan ZZ, Garlind A, Strandberg B, Svensson AL, Soreq H, Hellström-Lindahl E, Nordberg A (2002) Sustained cholinesterase inhibition in AD patients receiving rivastigmine for 12 months. Neurology 59:563–572

    Article  CAS  PubMed  Google Scholar 

  • De Jaeger X, Cammarota M, Prado Marco AM, Izquierdo I, Prado VF, Pereira GS (2013) Decreased acetylcholine release delays the consolidation of object recognition memory. Behav Brain Res 238:62–68

    Article  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (1997) Central cholinergic systems and cognition. Annu Rev Psychol 48:649–684

    Article  CAS  PubMed  Google Scholar 

  • Fadda F, Cocco S, Stancampiano R, Rossetti ZL (1999) Long-term voluntary ethanol consumption affects neither spatial nor passive avoidance learning, nor hippocampal acetylcholine release in alcohol-preferring rats. Behav Brain Res 103:71–76

    Article  CAS  PubMed  Google Scholar 

  • Farchi N, Shoham S, Hochner B, Soreq H (2007) Impaired hippocampal plasticity and erros in cognitive performance in mice with maladaptative AChE splice site selection. Eur J Neurosci 25:87–98

  • Fehr KA, Kalant H, LeBlanc AE (1976) Residual learning deficit after heavy exposure to cannabis or alcohol in rats. Science 192:1249–1251

    Article  CAS  PubMed  Google Scholar 

  • Gubler CJ (1961) The effects of thiamine deficiency and thiamine antagonists on the oxidation of α-keto acids by rat tissues. J Biol Chem 236(12):3112–3120

    CAS  PubMed  Google Scholar 

  • Hakim AM, Pappius HM (1983) Sequence of metabolic, clinical, and histological events in experimental thiamine-deficiency. Ann Neurol 13:365–375

    Article  CAS  PubMed  Google Scholar 

  • Harding AJ, Wong A, Svoboda M, Kril JJ, Halliday GM (1997) Chronic alcohol consumption does not cause hippocampal neuron loss in humans. Hippocampus 7:78–87

    Article  CAS  PubMed  Google Scholar 

  • Heinrich CP, Stadler H, Weiser H (1973) Effect of thiamine-deficiency on acetylcoenzyme-a and acetylcholine levels in rat-brain. J Neurochem 21:1273–1281

    Article  CAS  PubMed  Google Scholar 

  • Homewood J, Bond NW, MacKenzie A (1997) The effects of single and repeated episodes of thiamin deficiency on memory in alcohol-consuming rats. Alcohol 14:81–91

    Article  CAS  PubMed  Google Scholar 

  • Hoyumpa AMJ (1980) Mechanisms of thiamin deficiency in chronic alcoholism. Am J Clin Nutr 33:2750–2761

    CAS  PubMed  Google Scholar 

  • Langlais PJ, Mandel RJ, Mair RG (1992) Diencephalic lesions, learning impairments, and intact retrograde memory following acute thiamine-deficiency in the rat. Behav Brain Res 48:177–185

    Article  CAS  PubMed  Google Scholar 

  • Lockridge O, Schopfer LM, Winger G, Woods JH (2005) Large scale purification of butyrylcholinesterase from human plasma suitable for infection into monkeys; a potential new therapeutic for protection against cocaine and nerve agent toxicity. J Med Chem Biol radiol Def 3:nihms5095

  • Martin PR, Singleton CK, Hiller-Sturmhöfel S (2003) The role of thiamine deficiency in alcoholic brain disease. Alcohol Res Health 27(2):134–142

    PubMed  Google Scholar 

  • Massoulie J, Pezzementi L, Bon S, Krejci E, Vallette FM (1993) Molecular and cellular biology of cholinesterases. Prog Neurobiol 41:31–91

    Article  CAS  PubMed  Google Scholar 

  • Mesulam MM, Guillozet A, Shaw P, Levey A, Duysen EG, Lockridge O (2002) Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 110(4):627–639

    Article  CAS  PubMed  Google Scholar 

  • Molina PE, Myers N, Smith RM, Lang CH, Yousef KA, Tepper PG, Abumrad NN (1994) Nutritional and metabolic characterization of a thiamine-deficient rat model. J Parenter Enter Nutr 18:104–111

    Article  CAS  Google Scholar 

  • Morris RG, Garrud P, Rawlins JN, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683

    Article  CAS  PubMed  Google Scholar 

  • National Research Council (1985) Guide for the care and use of laboratory animals: a report of the institute of laboratory animal resources committee on care and use of laboratory animals

  • Noël X, Paternot J, Van der Linden M, Sferrazza R, Verhas M, Hanak C, Kornreich C, Martin P, De Mol J, Pelc I, Verbanck P (2001) Correlation between inhibition, working memory and delimited frontal area blood flow measured by Tc-99 m-bicisate spect in alcohol-dependent patients. Alcohol Alcohol 36:556–563

    Article  PubMed  Google Scholar 

  • Palencia G, Teixeira F, Ortiz A, Perez R, Rios C, Sotelo J (1994) Detrimental effects of malnutrition on the damage-induced by alcoholism - a study of animal-models that simulate chronic-alcoholism and malnutrition of large human groups. J Stud Alcohol 55:113–120

    CAS  PubMed  Google Scholar 

  • Paula-Barbosa MM, Brandao F, Madeira MD, Cadete-Leite A (1993) Structural changes in the hippocampal formation after long-term alcohol consumption and withdrawal in the rat. Addiction 88:237–247

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G and Watson C (2007) The rat brain in stereotaxic coordinates. 6th,31-33

  • Pekkanen L (1979) Pyrithiamin shortens ethanol-induced narcosis and increases voluntary ethanol drinking in rats. Int J Vitam Nutr Res 49:386–390

    CAS  PubMed  Google Scholar 

  • Pereira SRC, Menezes GA, Franco GC, Costa AEB, Ribeiro AM (1998) Chronic ethanol consumption impairs spatial remote memory in rats but does not affect cortical cholinergic parameters. Pharmacol Biochem Behav 60:305–311

    Article  CAS  PubMed  Google Scholar 

  • Peterson JW, Gubler CJ, Kuby SA (1975) Partial-purification and properties of thiamine pyrophosphokinase from pig brain. Biochim Biophys Acta 397:377–394

    Article  CAS  PubMed  Google Scholar 

  • Picklo MJ (2008) Ethanol intoxication increases hepatic N-lysyl protein acetylation. Biochem Biophys Res Commun 376:615–619

    Article  CAS  PubMed  Google Scholar 

  • Pinto LCM (1996) QUANTIKOV - Um analisador microestrutural para o ambiente Windows. Doctorated thesis. IPEN - USP: São Paulo, p 167

  • Pires RG, Pereira SR, Carvalho FM, Oliveira-Silva IF, Ferraz VP, Ribeiro AM (2007) Correlation between phosphorylation level of a hippocampal 86 kDa protein and extinction of a behaviour in a model of Wernicke-Korsakoff syndrome. Behav Brain Res 180:102–106

    Article  CAS  PubMed  Google Scholar 

  • Pires RGW, Pereira SRC, Pittella JE, Franco GC, Ferreira CL, Fernandes PA, Ribeiro AM (2001) The contribution of mild thiamine deficiency and ethanol consumption to central cholinergic parameter dysfunction and rats’ open-field performance impairment. Pharmacol Biochem Behav 70:227–235

    Article  CAS  PubMed  Google Scholar 

  • Pitel AL, Zahr NM, Jackson K, Sassoon SA, Rosenbloom MJ, Pfefferbaum A, Sullivan EV (2011) Signs of preclinical Wernicke’s encephalopathy and thiamine levels as predictors of neuropsychological deficits in alcoholism without Korsakoff’s syndrome. Neuropsychopharmacology 36:580–588

    Article  PubMed Central  PubMed  Google Scholar 

  • Redish AD (2001) The hippocampal debate: are we asking the right questions? Behav Brain Res 127:81–98

    Article  CAS  PubMed  Google Scholar 

  • Roland JJ, Mark K, Vetreno RP, Savage LM (2008) Increasing hippocampal acetylcholine levels enhance behavioral performance in an animal model of diencephalic amnesia. Brain Res 1234:116–127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Savage LM, Hall JM, Resende LS (2012) Translational rodent models of Korsakoff syndrome reveal the critical neuroanatomical substrates of memory dysfunction and recovery. Neuropsychol Rev 22:195–209

    Article  PubMed  Google Scholar 

  • Schegg KM, Gillespie RP, Prym U, Peacock JH (1990) Changes in membrane-bound and soluble molecular forms of acetylcholinesterase in mouse hippocampus after cholinergic denervation. Neurosci Lett 118:197–200

    Article  CAS  PubMed  Google Scholar 

  • Segal M, Greenberger V, Israeli M, Biegon A (1988) A correlation between regional acetylcholinesterase activity rat brain and performance in a spatial task. Behav Brain Res 30:215–219

    Article  CAS  PubMed  Google Scholar 

  • Shaltiel G, Hanan M, Wolf Y, Barbash S, Kovalev E, Shoham S, Soreq H (2013) Hippocampal microRNA-132 mediates stress-inducible cognitive deficits through its acetylcholinesterase target. Brain Struct Funct 218:59–72

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shenhar-Tsarfaty S, Berliner S, Bornstein NM, Soreq H (2013) Cholinesterases as biomarkers for parasympathetic dysfunction and inflammation-related disease. J Mol Neurosci 1559–1166

  • Takashima A, Nieuwenhuis ILC, Rijpkema M, Petersson KM, Jensen O, Fernandez G (2007) Memory trace stabilization leads to large-scale changes in the retrieval network: a functional MRI study on associative memory. Learn Mem 14:472–479

    Article  PubMed Central  PubMed  Google Scholar 

  • Victor M (1994) Alcoholic dementia. Can J Neurol Sci 21:88–99

    CAS  PubMed  Google Scholar 

  • Vigil FA, Oliveira-Silva IF, Ferreira LF, Pereira SR, Ribeiro AM (2010) Spatial memory deficits and thalamic serotonergic metabolite change in thiamine deficient rats. Behav Brain Res 210:140–142

    Article  CAS  PubMed  Google Scholar 

  • Vorhees CV, Schmidt DE, Barrett RJ, Schenker S (1977) Effects of thiamin deficiency on acetylcholine levels and utilization in vivo in rat brain. J Nutr 107:1902–1908

    CAS  PubMed  Google Scholar 

  • Zimatkin SM, Zimatkina TI (1996) Thiamine deficiency as predisposition to, and consequence of, increased alcohol consumption. Alcohol Alcohol 31:421–427

    Article  CAS  PubMed  Google Scholar 

  • Zimitat C, Kril J, Harper CG, Nixon PF (1990) Progression of neurological disease in thiamin-deficient rats is enhanced by ethanol. Alcohol 7:493–501

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG). The author thanks Aparecida Guerra de Jesus, received recipient of a FAPEMIG scholarship, for her technical assistance.

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Authors and Affiliations

  1. Departamento de Análises Clínicas e Toxicológicas - Faculdade de Farmácia, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-010, Brazil

    Ieda de Fátima Oliveira-Silva & Paula A. Fernandes

  2. Programa de Pós-graduação em Neurociências, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-010, Brazil

    Silvia R. Castanheira Pereira, Andrea F. Ribeiro & Angela Maria Ribeiro

  3. Departamento de Ciências Fisiológicas/Centro Biomédico-Laboratório de Neurobiologia Molecular e Comportamental, Universidade Federal do Espírito Santo, Vitória, 29043-910, Brazil

    Rita G. W. Pires

  4. Departamento de Bioquímica e Imunologia, Laboratório de Neurociências Comportamental e Molecular, LaNeC, Faculdade de Filosofia e Ciências Humanas, FaFiCH, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-010, Brazil

    Angela Maria Ribeiro

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  1. Ieda de Fátima Oliveira-Silva
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  2. Silvia R. Castanheira Pereira
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  6. Angela Maria Ribeiro
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Correspondence to Angela Maria Ribeiro.

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de Fátima Oliveira-Silva, I., Pereira, S.R.C., Fernandes, P.A. et al. Mild Thiamine Deficiency and Chronic Ethanol Consumption Modulate Acetylcholinesterase Activity Change and Spatial Memory Performance in a Water Maze Task. J Mol Neurosci 55, 217–226 (2015). https://doi.org/10.1007/s12031-014-0306-7

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  • DOI: https://doi.org/10.1007/s12031-014-0306-7

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