Binge ethanol-induced neurodegeneration in rat organotypic brain slice cultures: Effects of PLA2 inhibitor mepacrine and Docosahexaenoic Acid (DHA)

Neurochemical Research

Volumn 34, Issue 2, 2009, Pages 260-267

  Brown III, James ^a   Achille, Nicholas ^a   Neafsey, Edward J ^a   Collins, Michael A ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Alcohol; Arachidonic acid; Entorhinal cortex; Hippocampus; Neuroprotection; Phospholipase A2; Withdrawal

Indexed keywords

ADRENIC ACID; ALCOHOL; ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; LACTATE DEHYDROGENASE; MEPACRINE; PHOSPHOLIPASE A2; PROPIDIUM IODIDE; TRITIUM;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ENTORHINAL CORTEX; HIPPOCAMPUS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; DOCOSAHEXAENOIC ACIDS; ENTORHINAL CORTEX; ENZYME INHIBITORS; ETHANOL; HIPPOCAMPUS; INFLAMMATION; NEUROPROTECTIVE AGENTS; PHOSPHOLIPASES A2; QUINACRINE; RATS;

HIPPOCAMPUS (FISH); RATTUS;

EID: 58849120031     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-008-9765-y     Document Type: Article

References (72)

1. WA Hunt 1993 Are binge drinkers more at risk of developing brain damage? Alcohol 10 559 561 10.1016/0741-8329(93)90083-Z
2. BR Harris DA Gibson MA Prendergast JA Blanchard RC Holley SR Hart 2003 The neurotoxicity induced by ethanol withdrawal in mature organotypic hippocampal slices might involve cross-talk between metabotropic glutamate type 5 receptors and N-methyl-D-aspartate receptors Alcohol Clin Exp Res 27 1724 1735 10.1097/01.ALC.0000093601.33119.E3
3. MA Prendergast BR Harris PJ Mullholland JA Blanchard 2nd DA Gibson RC Holley 2004 Hippocampal CA1 region neurodegeneration produced by ethanol withdrawal requires activation of intrinsic polysynaptic hippocampal pathways and function of N-methyl-D-aspartate receptors Neuroscience 124 869 877 10.1016/j.neuroscience.2003.12.013
4. MA Collins TD Corso EJ Neafsey 1996 Neuronal degeneration in rat cerebrocortical and olfactory regions during subchronic "binge" intoxication with ethanol: possible explanation for olfactory deficits in alcoholics Alcohol Clin Exp Res 20 284 292 10.1111/j.1530-0277.1996.tb01641.x
5. RC Switzer E Majchrowicz F Weight 1982 Ethanol-induced argyrophilia in entorhinal cortex of rat Anat Rec 202 186A
6. FT Crews CJ Braun B Hoplight RC Switzer 3rd DJ Knapp 2000 Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats Alcohol Clin Exp Res 24 1712 1723 10.1111/j.1530-0277.2000. tb01973.x
7. MA Collins JY Zou EJ Neafsey 1998 Brain damage due to episodic alcohol exposure in vivo and in vitro: furosemide neuroprotection implicates edema-based mechanism FASEB J 12 221 230
8. C Hamelink A Hampson DA Wink LE Eiden RL Eskay 2005 Comparison of cannabidiol, antioxidants, and diuretics in reversing binge ethanol-induced neurotoxicity J Pharmacol Exp Ther 314 780 788 10.1124/jpet.105.085779
9. TD Corso HM Mostafa MA Collins EJ Neafsey 1998 Brain neuronal degeneration caused by episodic alcohol intoxication in rats: effects of nimodipine, 6, 7-dinitro-quinoxaline-2, 3-dione, and MK-801 Alcohol Clin Exp Res 22 217 224
10. JC Brown III A Belmadani S Kumar EJ Neafsey MA Collins 2005 Neuroinflammatory-like mechanisms in alcohol-induced brain damage J Neurochem 94 90
11. IH Lambert SF Pedersen KA Poulsen IH Lambert SF Pedersen KA Poulsen 2006 Activation of PLA2 isoforms by cell swelling and ischaemia/hypoxia Acta Physiol (Oxf) 187 75 85 10.1111/j.1748-1716.2006.01557.x
12. GY Sun J Xu MD Jensen A Simonyi 2004 Phospholipase A2 in the central nervous system: implications for neurodegenerative diseases J Lipid Res 45 205 213 10.1194/jlr.R300016-JLR200
13. GY Sun LA Horrocks AA Farooqui 2007 The roles of NADPH oxidase and phospholipases A2 in oxidative and inflammatory responses in neurodegenerative diseases J Neurochem 103 1 16 10.1111/j.1471-4159.2007.05003.x
14. J Martinez JJ Moreno 2001 Role of Ca2+-independent phospholipase A2 on arachidonic acid release induced by reactive oxygen species Arch Biochem Biophys 392 257 262 10.1006/abbi.2001.2439
15. AA Caro AI Cederbaum 2006 Role of cytochrome P450 in phospholipase A2- and arachidonic acid-mediated cytotoxicity Free Radic Biol Med 40 364 375 10.1016/j.freeradbiomed.2005.10.044
16. RC Maia CA Culver SM Laster RC Maia CA Culver SM Laster 2006 Evidence against calcium as a mediator of mitochondrial dysfunction during apoptosis induced by arachidonic acid and other free fatty acids J Immunol 177 6398 6404
17. KM Fang WL Chang SM Wang MJ Su ML Wu 2008 Arachidonic acid induces both Na+ and Ca2+ entry resulting in apoptosis J Neurochem 104 1177 1189 10.1111/j.1471-4159.2007.05022.x
18. F Crews K Nixon D Kim J Joseph B Shukitt-Hale L Qin 2006 BHT blocks NF-kappaB activation and ethanol-induced brain damage Alcohol Clin Exp Res 30 1938 1949 10.1111/j.1530-0277.2006.00239.x
19. NG Bazan 2007 Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection Curr Opin Clin Nutr Metab Care 10 136 141 10.1097/MCO. 0b013e32802b7030
20. RJ Pawlosky N Salem Jr 1995 Ethanol exposure causes a decrease in docosahexaenoic acid and an increase in docosapentaenoic acid in feline brains and retinas Am J Clin Nutr 61 1284 1289
21. L Gustavsson 1990 Brain lipid changes after ethanol exposure Ups J Med Sci Suppl 48 245 266
22. RJ Pawlosky J Bacher N Salem Jr 2001 Ethanol consumption alters electroretinograms and depletes neural tissues of docosahexaenoic acid in rhesus monkeys: nutritional consequences of a low n-3 fatty acid diet Alcohol Clin Exp Res 25 1758 1765 10.1111/j.1530-0277.2001.tb02187.x
23. J Noraberg BW Kristensen J Zimmer 1999 Markers for neuronal degeneration in organotypic slice cultures Brain Res Brain Res Protoc 3 278 290 10.1016/S1385-299X(98)00050-6
24. S Diekmann R Nitsch TG Ohm 1994 The organotypic entorhinal-hippocampal complex slice culture of adolescent rats. A model to study transcellular changes in a circuit particularly vulnerable in neurodegenerative disorders J Neural Transm Suppl 44 61 71
25. L Stoppini PA Buchs D Muller 1991 A simple method for organotypic cultures of nervous tissue J Neurosci Methods 37 173 182 10.1016/0165-0270(91) 90128-M
26. AW Jones 1999 The drunkest drinking driver in Sweden: blood alcohol concentration 0.545% w/v J Stud Alcohol 60 400 406
27. J Adachi Y Mizoi T Fukunaga Y Ogawa Y Ueno H Imamichi 1991 Degrees of alcohol intoxication in 117 hospitalized cases J Stud Alcohol 52 448 453
28. PJ Mulholland RL Self BR Harris HJ Little JM Littleton MA Prendergast 2005 Corticosterone increases damage and cytosolic calcium accumulation associated with ethanol withdrawal in rat hippocampal slice cultures Alcohol Clin Exp Res 29 871 881 10.1097/01.ALC.0000163509.27577.DA
29. J Zimmer BW Kristensen B Jakobsen J Noraberg 2000 Excitatory amino acid neurotoxicity and modulation of glutamate receptor expression in organotypic brain slice cultures Amino Acids 19 7 21 10.1007/s007260070029
30. A Belmadani JY Zou MJ Schipma EJ Neafsey MA Collins 2001 Ethanol pre-exposure suppresses HIV-1 glycoprotein 120-induced neuronal degeneration by abrogating endogenous glutamate/Ca2+-mediated neurotoxicity Neuroscience 104 769 781 10.1016/S0306-4522(01)00139-7
31. H Ushijima O Nishio R Klocking S Perovic WE Muller 1995 Exposure to gp120 of HIV-1 induces an increased release of arachidonic acid in rat primary neuronal cell culture followed by NMDA receptor-mediated neurotoxicity Eur J Neurosci 7 1353 1359 10.1111/j.1460-9568.1995.tb01126.x
32. EB Dreyer SA Lipton 1995 The coat protein gp120 of HIV-1 inhibits astrocyte uptake of excitatory amino acids via macrophage arachidonic acid Eur J Neurosci 7 2502 2507 10.1111/j.1460-9568.1995.tb01048.x
33. J Brown III N Achille EJ Neafsey MA Collins 2006 Identification of phospholipase A2 isoforms which contribute to binge alcohol-mediated neurodegeneration Alcohol 39 112 10.1016/j.alcohol.2006.09.010
34. FT Crews MA Collins C Dlugos J Littleton L Wilkins EJ Neafsey 2004 Alcohol-induced neurodegeneration: when, where and why? Alcohol Clin Exp Res 28 350 364 10.1097/01.ALC.0000113416.65546.01
35. S Basavappa SF Pedersen NK Jorgensen JC Ellory EK Hoffmann 1998 Swelling-induced arachidonic acid release via the 85-kDa cPLA2 in human neuroblastoma cells J Neurophysiol 79 1441 1449
36. JY Lehtonen PK Kinnunen 1995 Phospholipase A2 as a mechanosensor Biophys J 68 1888 1894
37. F Staub A Winkler J Peters O Kempski A Baethmann 1994 Mechanisms of glial swelling by arachidonic acid Acta Neurochir Suppl (Wien) 60 20 23
38. F Staub A Winkler J Peters O Kempski V Kachel A Baethmann 1994 Swelling, acidosis, and irreversible damage of glial cells from exposure to arachidonic acid in vitro J Cereb Blood Flow Metab 14 1030 1039
39. AA Farooqui LA Horrocks T Farooqui 2007 Modulation of inflammation in brain: a matter of fat J Neurochem 101 577 599 10.1111/j.1471-4159.2006.04371.x
40. X Wang X Zhao ZY Mao XM Wang ZL Liu 2003 Neuroprotective effect of docosahexaenoic acid on glutamate-induced cytotoxicity in rat hippocampal cultures Neuroreport 14 2457 2461 10.1097/00001756-200312190-00033
41. E Kishida M Tajiri Y Masuzawa E Kishida M Tajiri Y Masuzawa 2006 Docosahexaenoic acid enrichment can reduce L929 cell necrosis induced by tumor necrosis factor Biochim Biophys Acta 1761 454 462
42. Y Wu M Tada K Takahata K Tomizawa H Matsui 2007 Inhibitory effect of polyunsaturated fatty acids on apoptosis induced by etoposide, okadaic acid and AraC in Neuro2a cells Acta Med Okayama 61 147 152
43. S Florent C Malaplate-Armand I Youssef B Kriem V Koziel MC Escanye 2006 Docosahexaenoic acid prevents neuronal apoptosis induced by soluble amyloid-beta oligomers J Neurochem 96 385 395 10.1111/j.1471-4159.2005.03541.x
44. M Strokin O Chechneva KG Reymann G Reiser M Strokin O Chechneva 2006 Neuroprotection of rat hippocampal slices exposed to oxygen-glucose deprivation by enrichment with docosahexaenoic acid and by inhibition of hydrolysis of docosahexaenoic acid-containing phospholipids by calcium independent phospholipase A2 Neuroscience 140 547 553 10.1016/j.neuroscience.2006.02.026
45. D Cao R Xue J Xu Z Liu 2005 Effects of docosahexaenoic acid on the survival and neurite outgrowth of rat cortical neurons in primary cultures J Nutr Biochem 16 538 546 10.1016/j.jnutbio.2005.02.002
46. F Calderon HY Kim 2004 Docosahexaenoic acid promotes neurite growth in hippocampal neurons J Neurochem 90 979 988 10.1111/j.1471-4159.2004.02520.x
47. C Young PW Gean LC Chiou YZ Shen 2000 Docosahexaenoic acid inhibits synaptic transmission and epileptiform activity in the rat hippocampus Synapse 37 90 94 10.1002/1098-2396(200008)37:2=90::AID-SYN2≥3.0.CO;2-Z
48. M Martinez I Mougan 1998 Fatty acid composition of human brain phospholipids during normal development J Neurochem 71 2528 2533
49. Salem N Jr, Kim H-Y, Yergey JA Docosahexaenoic acid in membrane function and metabolism. In: Simopoulos A, Martin R, Kifer R (eds) The health effects of polyunsaturated fatty acids in seafoods. Academic Press, New York, pp 263-317
50. R Wilson MV Bell 1993 Molecular species composition of glycerophospholipids from white matter of human brain Lipids 28 13 17 10.1007/BF02536353
51. PS Sastry 1985 Lipids of nervous tissue: composition and metabolism Prog Lipid Res 24 69 176 10.1016/0163-7827(85)90011-6
52. M Akbar F Calderon Z Wen HY Kim 2005 Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival Proc Natl Acad Sci USA 102 10858 10863 10.1073/pnas.0502903102
53. RE Martin 1998 Docosahexaenoic acid decreases phospholipase A2 activity in the neurites/nerve growth cones of PC12 cells J Neurosci Res 54 805 813 10.1002/(SICI)1097-4547(19981215)54:6=805::AID-JNR8≥3.0.CO;2-4
54. JS Rao RN Ertley JC DeMar Jr SI Rapoport RP Bazinet HJ Lee 2007 Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex Mol Psychiatry 12 151 157 10.1038/sj.mp. 4001887
55. NG Bazan Jr 1970 Effects of ischemia and electroconvulsive shock on free fatty acid pool in the brain Biochim Biophys Acta 218 1 10
56. M Strokin M Sergeeva G Reiser 2003 Docosahexaenoic acid and arachidonic acid release in rat brain astrocytes is mediated by two separate isoforms of phospholipase A2 and is differently regulated by cyclic AMP and Ca2+ Br J Pharmacol 139 1014 1022 10.1038/sj.bjp. 0705326
57. E Yavin A Brand P Green 2002 Docosahexaenoic acid abundance in the brain: a biodevice to combat oxidative stress Nutr Neurosci 5 149 157 10.1080/10284150290003159
58. MS Hossain M Hashimoto S Gamoh S Masumura 1999 Antioxidative effects of docosahexaenoic acid in the cerebrum versus cerebellum and brainstem of aged hypercholesterolemic rats J Neurochem 72 1133 1138 10.1046/j.1471-4159.1999. 0721133.x
59. M Massaro A Habib L Lubrano S Del Turco G Lazzerini T Bourcier 2006 The omega-3 fatty acid docosahexaenoate attenuates endothelial cyclooxygenase-2 induction through both NADP(H) oxidase and PKC epsilon inhibition Proc Natl Acad Sci USA 103 15184 15189 10.1073/pnas.0510086103
60. M Guo L Stockert M Akbar HY Kim 2007 Neuronal specific increase of phosphatidylserine by docosahexaenoic acid J Mol Neurosci 33 67 73 10.1007/s12031-007-0046-z
61. HY Kim 2007 Novel metabolism of docosahexaenoic acid in neural cells J Biol Chem 282 18661 18665 10.1074/jbc.R700015200
62. Z Wen HY Kim 2004 Alterations in hippocampal phospholipid profile by prenatal exposure to ethanol J Neurochem 89 1368 1377 10.1111/j.1471-4159.2004. 02433.x
63. CN Serhan M Arita S Hong K Gotlinger 2004 Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their endogenous aspirin-triggered epimers Lipids 39 1125 1132 10.1007/s11745-004-1339-7
64. NG Bazan 2005 Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress Brain Pathol 15 159 166
65. WJ Lukiw JG Cui VL Marcheselli M Bodker A Botkjaer K Gotlinger 2005 A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease J Clin Invest 115 2774 2783 10.1172/JCI25420
66. Q Wang AY Sun A Simonyi TJ Kalogeris DK Miller GY Sun 2007 Ethanol preconditioning protects against ischemia/reperfusion-induced brain damage: role of NADPH oxidase-derived ROS Free Radic Biol Med 43 1048 1060 10.1016/j.freeradbiomed.2007.06.018
67. SM Bailey 2003 A review of the role of reactive oxygen and nitrogen species in alcohol-induced mitochondrial dysfunction Free Radic Res 37 585 596 10.1080/1071576031000091711
68. V Ramachandran LT Watts SK Maffi J Chen S Schenker G Henderson 2003 Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons J Neurosci Res 74 577 588 10.1002/jnr.10767
69. GL Milne JD Morrow MJ Picklo Sr 2006 Elevated oxidation of docosahexaenoic acid, 22:6 (n-3), in brain regions of rats undergoing ethanol withdrawal Neurosci Lett 405 172 174 10.1016/j.neulet.2006.06.058
70. SY Kim RA Breslow J Ahn N Salem Jr 2007 Alcohol consumption and fatty acid intakes in the 2001-2002 National Health and Nutrition Examination Survey Alcohol Clin Exp Res 31 1407 1414 10.1111/j.1530-0277.2007.00442.x
71. N Salem Jr B Litman HY Kim K Gawrisch 2001 Mechanisms of action of docosahexaenoic acid in the nervous system Lipids 36 945 959 10.1007/s11745-001-0805-6
72. S Kotani E Sakaguchi S Warashina N Matsukawa Y Ishikura Y Kiso 2006 Dietary supplementation of arachidonic and docosahexaenoic acids improves cognitive dysfunction Neurosci Res 56 159 164 10.1016/j.neures.2006.06.010