Effects of long-term moderate ethanol and cholesterol on cognition, cholinergic neurons, inflammation, and vascular impairment in rats

Neuroscience

Volumn 205, Issue , 2012, Pages 154-166

  Ehrlich, D ^a   Pirchl, M ^a   Humpel, C ^a  

^a Department of Psychiatry and Psychotherapy   (Austria)

Author keywords

Blood brain barrier leakage; Cholinergic dysfunction; Cognitive decline; Ethanol

Indexed keywords

ACETYLCHOLINE; ALCOHOL; AMYLOID BETA PROTEIN; BIOLOGICAL MARKER; CHOLESTEROL; CHOLINE ACETYLTRANSFERASE; IMMUNOGLOBULIN G ANTIBODY; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUROTROPHIN RECEPTOR P75; TISSUE PLASMINOGEN ACTIVATOR;

ACETYLCHOLINE BRAIN LEVEL; ADULT ANIMAL; ALCOHOL BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL AMYGDALA; BLOOD BRAIN BARRIER; BRAIN NERVE CELL; CELL ACTIVATION; CEREBROVASCULAR DISEASE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; COGNITIVE DEFECT; CONTROLLED STUDY; ENCEPHALITIS; HYPERCHOLESTEROLEMIA; LONG TERM EXPOSURE; MALE; MEYNERT BASAL NUCLEUS; MICROGLIA; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RISK FACTOR; SPATIAL MEMORY;

ALCOHOL-INDUCED DISORDERS, NERVOUS SYSTEM; ANIMALS; CHOLINERGIC NEURONS; DEMENTIA, VASCULAR; DISEASE MODELS, ANIMAL; HYPERCHOLESTEROLEMIA; INFLAMMATION MEDIATORS; MALE; RATS; RATS, SPRAGUE-DAWLEY; TIME;

EID: 84858009243     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.12.054     Document Type: Article

References (97)

1. Aho L., Karkola K., Juusela J., Alafuzoff I. Heavy alcohol consumption and neuropathological lesions: a post-mortem human study. J Neurosci Res 2009, 87:2786-2792.
2. Allgaier C. Ethanol sensitivity of NMDA receptors. Neurochem Int 2002, 41:377-382.
3. Aloe L., Tirassa P. The effect of long-term alcohol intake on brain NGF-target cells of aged rats. Alcohol 1992, 9:299-304.
4. Anstey K.J., Mack H.A., Cherbuin N. Alcohol consumption as a risk factor for dementia and cognitive decline: meta-analysis of prospective studies. Am J Geriatr Psychiatry 2009, 17:542-555.
5. Arendt T. Impairment in memory function and neurodegenerative changes in the cholinergic basal forebrain system induced by chronic intake of ethanol. J Neural Transm Suppl 1994, 44:173-187.
6. Arendt T., Brückner M.K., Krell T., Pagliusi S., Kruska L., Heumann R. Degeneration of rat cholinergic basal forebrain neurons and reactive changes in nerve growth factor expression after chronic neurotoxic injury-II. Reactive expression of the nerve growth factor gene in astrocytes. Neuroscience 1995, 65:647-659.
7. Arendt T., Henning D., Gray J.A., Marchbanks R. Loss of neurons in the rat basal forebrain cholinergic projection system after prolonged intake of ethanol. Brain Res Bull 1988, 21:563-569.
8. Aroor A.R., Shukla S.D. MAP kinase signaling in diverse effects of ethanol. Life Sci 2004, 26:2339-2364.
9. Baek J.K., Heaton M.B., Walker D.W. Chronic alcohol ingestion: nerve growth factor gene expression and neurotrophic activity in rat hippocampus. Alcohol Clin Exp Res 1994, 18:1368-1376.
10. Bate C., Williams A. Ethanol protects cultured neurons against amyloid-β and α-synuclein-induced synapse damage. Neuropharmacology 2011, 61:1406-1412.
11. Bell R.D., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol 2009, 118:103-113.
12. Benarroch E.E. Tissue plasminogen activator: beyond thrombolysis. Neurology 2007, 69:799-802.
13. Beracochea D., Micheau J., Jaffard R. Memory deficits following chronic alcohol consumption in mice: relationships with hippocampal and cortical cholinergic activities. Pharmacol Biochem Behav 1992, 42:749-753.
14. Blednov Y.A., Bergeson S.E., Walker D., Ferreira V.M., Kuziel W.A., Harris R.A. Perturbation of chemokine networks by gene deletion alters the reinforcing actions of ethanol. Behav Brain Res 2005, 165:110-125.
15. Bowen D.M., Smith C.B., White P., Davison A.N. Neurotransmitter-related enzymes and indices of hypoxia in senile dementia and other abiotrophies. Brain 1976, 99:459-496.
16. Casamenti F., Corradetti R., Löffelholz K., Mantovani P., Pepeu G. Effects of 4-aminopyridine on acetylcholine output from the cerebral cortex of the rat in vivo. Br J Pharmacol 1982, 76:439-445.
17. Catlin M.C., Guizzetti M., Costa L.G. Effects of ethanol on calcium homeostasis in the nervous system: implications for astrocytes. Mol Neurobiol 1999, 19:1-24.
18. Charness M.E. Brain lesions in alcoholics. Alcohol Clin Exp Res 1993, 17:2-11.
19. Costa L.G., Guizzetti M. Muscarinic cholinergic receptor signal transduction as a potential target for the developmental neurotoxicity of ethanol. Biochem Pharmacol 1999, 57:721-726.
20. Costa L.G., Vitalone A., Guizzetti M. Signal transduction mechanisms involved in the antiproliferative effects of ethanol in glial cells. Toxicol Lett 2004, 149:67-73.
21. Crews F.T., Morrow A.L., Criswell H., Breese G. Effects of ethanol on ion channels. Int Rev Neurobiol 1996, 39:283-367.
22. Crews F.T., Nixon K. Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 2009, 44:115-127.
23. Das S.K., Vasudevan D.M. Alcohol-induced oxidative stress. Life Sci 2007, 81:177-187.
24. Deane R., Zlokovic B.V. Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res 2007, 4:191-197.
25. Deng X.S., Deitrich R.A. Ethanol metabolism and effects: nitric oxide and its interaction. Curr Clin Pharmacol 2007, 2:145-153.
26. Diamond I., Messing R.O. Neurologic effects of alcoholism. West J Med 1994, 161:279-287.
27. Floyd E.A., Young-Seigler A.C., Ford B.D., Reasor J.D., Moore E.L., Townsel J.G., Rucker H.K. Chronic ethanol ingestion produces cholinergic hypofunction in rat brain. Alcohol 1997, 14:93-98.
28. Foddai M., Dosia G., Spiga S., Diana M. Acetaldehyde increases dopaminergic neuronal activity in the VTA. Neuropsychopharmacology 2004, 29:530-536.
29. Gentry T.R. Effect of food on the pharmacokinetics of alcohol absorption. Alcohol Clin Exp Res 2000, 24:403-404.
30. Goldstein G., Tarter R.E., Shelly C., Alterman A.I., Petrarulo E. Withdrawal seizures in black and white alcoholic patients: intellectual and neuropsychological sequelae. Drug Alcohol Depend 1983, 12:349-354.
31. Graves A.B., White E., Koepsell T.D., Reifler B.V., van Belle G., Larson E.B., Raskind M. A case-control study of Alzheimer's disease. Ann Neurol 1990, 28:766-774.
32. Guizzetti M., Costa L.G. Cholesterol homeostasis in the developing brain: a possible new target for ethanol. Hum Exp Toxicol 2007, 26:355-360.
33. Haorah J., Knipe B., Leibhart J., Ghorpade A., Persidsky Y. Alcohol-induced oxidative stress in brain endothelial cells causes blood-brain barrier dysfunction. J Leukoc Biol 2005, 78:1223-1232.
34. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
35. He J., Crews F.T. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 2008, 210:349-358.
36. Hillbom M., Kaste M. Ethanol intoxication: a risk factor for ischemic brain infarction in adolescents and young adults. Stroke 1981, 12:422-425.
37. Humpel C. Chronic mild cerebrovascular dysfunction as a cause for Alzheimer's disease?. Exp Gerontol 2011, 46:225-232.
38. Humpel C., Weis C. Nerve growth factor and cholinergic CNS neurons studied in organotypic brain slices. Implication in Alzheimer's disease?. J Neural Transm Suppl 2002, 62:253-263.
39. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 2004, 5:347-360.
40. Irle E., Markowitsch H.J. Widespread neuroanatomical damage and learning deficits following chronic alcohol consumption or vitamin-B1 (thiamine) deficiency in rats. Behav Brain Res 1983, 9:277-294.
41. Jamal M., Ameno K., Ameno S., Morishita J., Wang W., Kumihashi M., Ikuo U., Miki T., Ijiri I. Changes in cholinergic function in the frontal cortex and hippocampus of rat exposed to ethanol and acetaldehyde. Neuroscience 2007, 144:232-238.
42. Jamal M., Ameno K., Miki T., Wang W., Kumihashi M., Isse T., Kawamoto T., Kitagawa K., Nakayama K., Ijiri I., Kinoshita H. Cholinergic alterations following alcohol exposure in the frontal cortex of Aldh2-deficient mice models. Brain Res 2009, 1295:37-43.
43. Jarrard L.E., Okaichi H., Steward O., Goldschmidt R.B. On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav Neurosci 1984, 98:946-954.
44. Ji K.A., Yang M.S., Jeong H.K., Min K.J., Kang S.H., Jou I., Joe E.H. Resident microglia die and infiltrated neutrophils and monocytes become major inflammatory cells in lipopolysaccharide-injected brain. Glia 2007, 55:1577-1588.
45. Kaul M., Garden G.A., Lipton S.A. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 2001, 410:988-994.
46. Kaur C., Singh J., Lim M.K., Ng B.L., Yap E.P., Ling E.A. The response of neurons and microglia to blast injury in the rat brain. Neuropathol Appl Neurobiol 1995, 21:369-377.
47. Kentroti S., Vernadakis A. Ethanol neurotoxicity in culture: selective loss of cholinergic neurons. J Neurosci Res 1996, 44:577-585.
48. Kim S.R., Jeong H.Y., Yang S., Choi S.P., Seo M.Y., Yun Y.K., Choi Y., Baik S.H., Park J.S., Gwon A.R., Yang D.K., Lee C.H., Lee S.M., Park K.W., Jo D.G. Effects of chronic alcohol consumption on expression levels of APP and Aβ-producing enzymes. BMB Rep 2011, 44:135-139.
49. Ku B.M., Lee Y.K., Jeong J.Y., Mun J., Han J.Y., Roh G.S., Kim H.J., Cho G.J., Choi W.S., Yi G.S., Kang S.S. Ethanol-induced oxidative stress is mediated by p38 MAPK pathway in mouse hippocampal cells. Neurosci Lett 2007, 23:64-67.
50. Lacor P.N., Buniel M.C., Furlow P.W., Sanz Clemente A.S., Velasco P.T., Wood M., Viola K.L., Klein W.L. Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 2007, 27:796-807.
51. Lahiri D.K., Nall C., Chen D., Zaphiriou M., Morgan C., Nurnberger J.I. Developmental expression of the beta-amyloid precursor protein and heat-shock protein 70 in the cerebral hemisphere region of the rat brain. Ann N Y Acad Sci 2002, 965:324-333.
52. Laifenfeld D., Karry R., Grauer E., Klein E., Ben-Shachar D. Antidepressants and prolonged stress in rats modulate CAM-L1, laminin, and pCREB, implicated in neuronal plasticity. Neurobiol Dis 2005, 20:432-441.
53. Little A.R., Benkovic S.A., Miller D.B., O'Callaghan J.P. Chemically induced neuronal damage and gliosis: enhanced expression of the proinflammatory chemokine, monocyte chemoattractant protein (MCP)-1, without a corresponding increase in proinflammatory cytokines. Neuroscience 2002, 115:307-320.
54. Lukoyanov N.V., Pereira P.A., Paula-Barbosa M.M., Cadete-Leite A. Nerve growth factor improves spatial learning and restores hippocampal cholinergic fibers in rats withdrawn from chronic treatment with ethanol. Exp Brain Res 2003, 148:88-94.
55. Luo J., West J.R., Pantazis N.J. Nerve growth factor and basic fibroblast growth factor protect rat cerebellar granule cells in culture against ethanol-induced cell death. Alcohol Clin Exp Res 1997, 21:1108-1120.
56. Marksteiner J., Humpel C. Beta-amyloid expression, release and extracellular deposition in aged rat brain slices. Mol Psychiatry 2008, 13:939-952.
57. McKinney M. Brain cholinergic vulnerability: relevance to behavior and disease. Biochem Pharmacol 2005, 70:1115-1124.
58. McManus C.M., Liu J.S., Hahn M.T., Hua L.L., Brosnan C.F., Berman J.W., Lee S.C. Differential induction of chemokines in human microglia by type I and II interferons. Glia 2000, 29:273-280.
59. Mendenhall C.L., Rouster S.D., Roselle G.A., Grossman C.J., Ghosn S., Gartside P. Impact of chronic alcoholism on the aging rat: changes in nutrition, liver composition, and mortality. Alcohol Clin Exp Res 1993, 17(4):847-853.
60. Mesulam M. The cholinergic lesion of Alzheimer's disease: pivotal factor or side show?. Learn Mem 2010, 11:43-49.
61. Monforte R., Estruch R., Graus F., Nicolas J.M., Urbano-Marquez A. High ethanol consumption as risk factor for intracerebral hemorrhage in young and middle-aged people. Stroke 1990, 21:1529-1532.
62. Mooney S.M., Miller M.W. Nerve growth factor neuroprotection of ethanol-induced neuronal death in rat cerebral cortex is age dependent. Neuroscience 2007, 149:372-381.
63. Mostofsky E., Burger M.R., Schlaug G., Mukamal K.J., Rosamond W.D., Mittleman M.A. Alcohol and acute ischemic stroke onset: the stroke onset study. Stroke 2010, 41:1845-1849.
64. Mufson E.J., Conner J.M., Kordower J.H. Nerve growth factor in Alzheimer's disease: defective retrograde transport to nucleus basalis. Neuroreport 1995, 6:1063-1066.
65. Mufson E.J., Counts S.E., Perez S.E., Binder L. Galanin plasticity in the cholinergic basal forebrain in Alzheimer's disease and transgenic mice. Neuropeptides 2005, 39:233-237.
66. Mufson E.J., Counts S.E., Perez S.E., Ginsberg S.D. Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 2008, 8:1703-1718.
67. Mufson E.J., Ginsberg S.D., Ikonomovic M.D., DeKosky S.T. Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J Chem Neuroanat 2003, 26:233-242.
68. Nakano T., Fujimoto T., Shimooki S., Fukudome T., Uchida T., Tsuji T., Mitsuyama Y., Akimoto H., Furukawa S. Transient elevation of nerve growth factor content in the rat hippocampus and frontal cortex by chronic ethanol treatment. Psychiatry Clin Neurosci 1996, 50:157-160.
69. Noel M., Norris E.H., Strickland S. Tissue plasminogen activator is required for the development of fetal alcohol syndrome in mice. Proc Natl Acad Sci U S A 2011, 108:5069-5074.
70. Nordmann R., Ribière C., Rouach H. Ethanol-induced lipid peroxidation and oxidative stress in extrahepatic tissues. Alcohol Alcohol 1990, 25:231-237.
71. Oda Y. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol Int 1999, 49:921-937.
72. Olton D.S. The use of animal models to evaluate the effects of neurotoxins on cognitive processes. Neurobehav Toxicol Teratol 1983, 5:635-640.
73. Paula-Barbosa M.M., Silva S.M., Andrade J.P., Cadete-Leite A., Madeira M.D. Nerve growth factor restores mRNA levels and the expression of neuropeptides in the suprachiasmatic nucleus of rats submitted to chronic ethanol treatment and withdrawal. J Neurocytol 2001, 30:195-207.
74. Paula-Barbosa M.M., Tavares M.A. Neuritic plaque-like structures in the rat cerebellum following prolonged alcohol consumption. Experientia 1984, 40:110-112.
75. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, New York. 2nd ed.
76. Pirchl M., Ullrich C., Humpel C. Differential effects of short- and long-term hyperhomocysteinaemia on cholinergic neurons, spatial memory and microbleedings in vivo in rats. Eur J Neurosci 2010, 32:1516-1527.
77. Qin L., He J., Hanes R.N., Pluzarev O., Hong J.S., Crews F.T. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 2008, 18:5-10.
78. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., Knapp D.J., Crews F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 255:453-462.
79. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N Engl J Med 2010, 362:329-344.
80. Rosen J., Colantonio A., Becker J.T., Lopez O.L., DeKosky S.T., Moss H.B. Effects of a history of heavy alcohol consumption on Alzheimer's disease. Br J Psychiatry 1993, 163:358-363.
81. Salehi A., Kleshevnikov A., Mobley W.C. Cholinergic neurodegeneration in Alzheimer's disease: basis for nerve growth factor therapy. Pharmacological Mechanisms in Alzheimer's Therapeutics 2007, 64-104. Springer, New York.
82. Sassin I., Schultz C., Thal D.R., Rüb U., Arai K., Braak E., Braak H. Evolution of Alzheimer's disease-related cytoskeletal changes in the basal nucleus of Meynert. Acta Neuropathol 2000, 100:259-269.
83. Schindowski K., Belarbi K., Buée L. Neurotrophic factors in Alzheimer's disease: role of axonal transport. Genes Brain Behav 2008, 1:43-56.
84. Scott S.A., Mufson E.J., Weingartner J.A., Skau K.A., Crutcher K.A. Nerve growth factor in Alzheimer's disease: increased levels throughout the brain coupled with declines in nucleus basalis. J Neurosci 1995, 9:6213-6221.
85. Skrzypiec A.E., Maiya R., Chen Z., Pawlak R., Strickland S. Plasmin-mediated degradation of laminin gamma-1 is critical for ethanol-induced neurodegeneration. Biol Psychiatry 2009, 66:785-794.
86. Stamatovic S.M., Keep R.F., Kunkel S.L., Andjelkovic A.V. Potential role of MCP-1 in endothelial cell tight junction opening: signaling via Rho and Rho kinase. J Cell Sci 2003, 116:4615-4628.
87. Stamatovic S.M., Shakui P., Keep R.F., Moore B.B., Kunkel S.L., Van Rooijen N., Andjelkovic A.V. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J Cereb Blood Flow Metab 2005, 25:593-606.
88. Sun L., Wang X., Liu S., Wang Q., Wang J., Bennecib M., Gong C.X., Sengupta A., Grundke-Iqbal I., Iqbal K. Bilateral injection of isoproterenol into hippocampus induces Alzheimer-like hyperphosphorylation of tau and spatial memory deficit in rat. FEBS Lett 2005, 579:251-258.
89. Tanaka N., Asada T., Kinoshita T., Yamashita F., Uno M. Alcohol consumption and risk of dementia. Lancet 2002, 360:491.
90. Toda N., Ayajiki K. Vascular actions of nitric oxide as affected by exposure to alcohol. Alcohol Alcohol 2010, 45:347-355.
91. Tyas S.L. Are tobacco and alcohol use related to Alzheimer's disease?. A critical assessment of the evidence and its implications. Addict Biol 1996, 1:237-254.
92. Ullrich C., Pirchl M., Humpel C. Hypercholesterolemia in rats impairs the cholinergic system and leads to memory deficits. Mol Cell Neurosci 2010, 45:408-417.
93. Wagner C., Hänsch G.M., Stegmaier S., Denefleh B., Hug F., Schoels M. The complement receptor 3, CR3 (CD11b/CD18), on T lymphocytes: activation-dependent up-regulation and regulatory function. Eur J Immunol 2001, 31:1173-1180.
94. Webb B., Suarez S.S., Heaton M.B., Walker D.W. Cultured postnatal rat septohippocampal neurons change intracellular calcium in response to ethanol and nerve growth factor. Brain Res 1997, 778:354-366.
95. Webb L.E., Lengle E., Izzo R., Woods E. Micromethod for lipid-chromatographic determination of cholesterol in lipemic sera. Clin Chem 1982, 28:1769-1772.
96. Yamamoto M., Horiba M., Buescher J.L., Huang D., Gendelman H.E., Ransohoff R.M., Ikezu T. Overexpression of monocyte chemotactic protein-1/CCL2 in beta-amyloid precursor protein transgenic mice show accelerated diffuse beta-amyloid deposition. Am J Pathol 2005, 166:1475-1485.
97. Zahr N.M., Kaufman K.L., Harper C.G. Clinical and pathological features of alcohol-related brain damage. Nat Rev Neurol 2011, 7:284-294.