Effect of repetitive daily ethanol intoxication on adult rat brain: Significant changes in phospholipase A2 enzyme levels in association with increased PARP-1 indicate neuroinflammatory pathway activation

Alcohol

Volumn 47, Issue 1, 2013, Pages 39-45

  Tajuddin, Nuzhath F ^a   Przybycien Szymanska, Magdalena M ^a   Pak, Toni R ^a   Neafsey, Edward J ^a   Collins, Michael A ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Alcohol; AQP4; Arachidonic acid; Neurodegeneration; Neuroinflammation; PARP 1; Parthanatos; PLA2

Indexed keywords

ALCOHOL; AQUAPORIN 4; CASPASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 GROUP IV; PHOSPHOLIPASE A2 GROUP VI;

ALCOHOL BLOOD LEVEL; ALCOHOL INTOXICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENTORHINAL CORTEX; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; IMMUNOBLOTTING; MALE; NERVE CELL DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NONHUMAN; RAT; SIGNAL TRANSDUCTION;

AGING; ALCOHOLIC INTOXICATION; ANIMALS; AQUAPORIN 4; CASPASE 3; ENTORHINAL CORTEX; GROUP VI PHOSPHOLIPASES A2; HIPPOCAMPUS; MALE; PHOSPHOLIPASES A2, CYTOSOLIC; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

ANIMALIA; IVA; RATTUS; RATTUS NORVEGICUS;

EID: 84872419905     PISSN: 07418329     EISSN: 18736823     Source Type: Journal    
DOI: 10.1016/j.alcohol.2012.09.003     Document Type: Article

References (63)

1. Adachi J., Mizoi Y., Fukunaga T., Ogawa Y., Ueno Y., Imamichi H. Degrees of alcohol intoxication in 117 hospitalized cases. Journal of Studies on Alcohol 1991, 52:448-453.
2. Adibhatla R.M., Hatcher J.F. Secretory phospholipase A2 IIA is up-regulated by TNF-alpha and IL-1alpha/beta after transient focal cerebral ischemia in rat. Brain Research 2007, 1134:199-205.
3. Adibhatla R.M., Hatcher J.F. Phospholipase A(2), reactive oxygen species, and lipid peroxidation in CNS pathologies. Biochemistry and Molecular Biology Reports 2008, 41:560-567.
4. Alfonso-Loeches S., Pascual-Lucas M., Blanco A.M., Sanchez-Vera I., Guerri C. Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. Journal of Neuroscience 2010, 30:8285-8295.
5. Andrabi S.A., Kang H.C., Haince J.F., Lee Y.I., Zhang J., Chi Z., et al. Iduna protects the brain from glutamate excitotoxicity and stroke by interfering with poly(ADP-ribose) polymer-induced cell death. Nature Medicine 2011, 17:692-699.
6. Basavarajappa B.S., Cooper T.B., Hungund B.L. Effect of chronic ethanol exposure on mouse brain arachidonic acid specific phospholipase A2. Biochemical Pharmacology 1998, 55:515-521.
7. Basavarajappa B.S., Saito M., Cooper T.B., Hungund B.L. Activation of arachidonic acid-specific phospholipase A2 in human neuroblastoma cells after chronic alcohol exposure: prevention by GM1 ganglioside. Alcoholism: Clinical & Experimental Research 1997, 21:1199-1203.
8. Bazan N.G., Molina M.F., Gordon W.C. Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. Annual Review of Nutrition 2011, 31:321-351.
9. Bobba A., Atlante A., Petragallo V.A., Marra E. Different sources of reactive oxygen species contribute to low potassium-induced apoptosis in cerebellar granule cells. International Journal of Molecular Medicine 2008, 21:737-745.
10. Brown J., Achille N., Neafsey E.J., Collins M.A. Binge ethanol-induced neurodegeneration in rat organotypic brain slice cultures: effects of PLA2 inhibitor mepacrine and docosahexaenoic acid (DHA). Neurochemical Research 2009, 34:260-267.
11. Carlen P.L., McAndrews M.P., Weiss R.T., Dongier M., Hill J.M., Menzano E., et al. Alcohol-related dementia in the institutionalized elderly. Alcoholism: Clinical & Experimental Research 1994, 18:1330-1334.
12. Chaitanya G.V., Steven A.J., Babu P.P. PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Communication and Signaling 2010, 8:31.
13. Cippitelli A., Zook M., Bell L., Damadzic R., Eskay R.L., Schwandt M., et al. Reversibility of object recognition but not spatial memory impairment following binge-like alcohol exposure in rats. Neurobiology of Learning and Memory 2010, 94:538-546.
14. Collins M.A., Corso T.D., Neafsey E.J. Neuronal degeneration in rat cerebrocortical and olfactory regions during subchronic "binge" intoxication with ethanol: possible explanation for olfactory deficits in alcoholics. Alcoholism: Clinical & Experimental Research 1996, 20:284-292.
15. Collins M.A., Neafsey E.J. Ethanol and adult CNS neurodamage: oxidative stress, but possibly not excitotoxicity. Frontiers in Bioscience 2012, 4:1358-1367.
16. Collins M.A., Neafsey E.J. Neuroinflammatory pathways in binge alcohol-induced neuronal degeneration: oxidative stress cascade involving aquaporin, brain edema, and phospholipase A2 activation. Neurotoxicity Research 2012, 21:70-78.
17. Collins M.A., Zou J.Y., Neafsey E.J. Brain damage due to episodic alcohol exposure in vivo and in vitro: furosemide neuroprotection implicates edema-based mechanism. FASEB Journal 1998, 12:221-230.
18. Crews F.T., Zou J., Qin L. Induction of innate immune genes in brain create the neurobiology of addiction. Brain, Behavior, and Immunity 2011, 25(Suppl. 1):S4-S12.
19. Dana R., Leto T.L., Malech H.L., Levy R. Essential requirement of cytosolic phospholipase A2 for activation of the phagocyte NADPH oxidase. Journal of Biological Chemistry 1998, 273:441-445.
20. David K.K., Andrabi S.A., Dawson T.M., Dawson V.L. Parthanatos, a messenger of death. Frontiers in Bioscience 2009, 14:1116-1128.
21. Eckardt M.J., Martin P.R. Clinical assessment of cognition in alcoholism. Alcoholism: Clinical & Experimental Research 1986, 10:123-127.
22. Floreani N.A., Rump T.J., Muneer P.M., Alikunju S., Morsey B.M., Brodie M.R., et al. Alcohol-induced interactive phosphorylation of Src and toll-like receptor regulates the secretion of inflammatory mediators by human astrocytes. Journal of Neuroimmune Pharmacology 2010, 5:533-545.
23. Friis M.B., Vorum K.G., Lambert I.H. Volume-sensitive NADPH oxidase activity and taurine efflux in NIH3T3 mouse fibroblasts. American Journal of Physiology. Cell Physiology 2008, 294:C1552-C1565.
24. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death and Differentiation 2012, 19:107-120.
25. Goracci G., Ferrini M., Nardicchi V. Low molecular weight phospholipases A2 in mammalian brain and neural cells: roles in functions and dysfunctions. Molecular Neurobiology 2010, 41:274-289.
26. Gotz M.E., Janetzky B., Pohli S., Gottschalk A., Gsell W., Tatschner T., et al. Chronic alcohol consumption and cerebral indices of oxidative stress: is there a link?. Alcoholism: Clinical & Experimental Research 2001, 25:717-725.
27. Gunnarson E., Zelenina M., Aperia A. Regulation of brain aquaporins. Neuroscience 2004, 129:947-955.
28. Gupta S., Warner J. Alcohol-related dementia: a 21st-century silent epidemic?. British Journal of Psychiatry 2008, 193:351-353.
29. Hassa P.O., Hottiger M.O. The functional role of poly(ADP-ribose)polymerase 1 as novel coactivator of NF-kappaB in inflammatory disorders. Cellular and Molecular Life Sciences 2002, 59:1534-1553.
30. Hernandez M., Burillo S.L., Crespo M.S., Nieto M.L. Secretory phospholipase A2 activates the cascade of mitogen-activated protein kinases and cytosolic phospholipase A2 in the human astrocytoma cell line 1321N1. Journal of Biological Chemistry 1998, 273:606-612.
31. Kim H.-W., Cheon Y., Modi H.R., Rapoport S.I., Rao J.S. Effects of chronic clozapine administration on markers of arachidonic acid cascade and synaptic integrity in rat brain. Psychopharmacology 2012, 222:663-674.
32. Kinsey G.R., Blum J.L., Covington M.D., Cummings B.S., McHowat J., Schnellmann R.G. Decreased iPLA2gamma expression induces lipid peroxidation and cell death and sensitizes cells to oxidant-induced apoptosis. Journal of Lipid Research 2008, 49:1477-1487.
33. Koivusalo M., Kapus A., Grinstein S. Sensors, transducers, and effectors that regulate cell size and shape. Journal of Biological Chemistry 2009, 284:6595-6599.
34. Kolko M., Rodriguez de Turco E.B., Diemer N.H., Bazan N.G. Neuronal damage by secretory phospholipase A2: modulation by cytosolic phospholipase A2, platelet-activating factor, and cyclooxygenase-2 in neuronal cells in culture. Neuroscience Letters 2003, 338:164-168.
35. Kramer R.M., Stephenson D.T., Roberts E.F., Clemens J.A. Cytosolic phospholipase A2 (cPLA2) and lipid mediator release in the brain. Journal of Lipid Mediators and Cell Signalling 1996, 14:3-7.
36. Lambert I.H., Pedersen S.F., Poulsen K.A. Activation of PLA2 isoforms by cell swelling and ischaemia/hypoxia. Acta Physiologica (Oxford) 2006, 187:75-85.
37. Lehtonen J.Y., Kinnunen P.K. Phospholipase A2 as a mechanosensor. Biophysical Journal 1995, 68:1888-1894.
38. Li L., Zhang H., Varrin-Doyer M., Zamvil S.S., Verkman A.S. Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation. FASEB Journal 2011, 25:1556-1566.
39. Luo J., Lindstrom C.L., Donahue A., Miller M.W. Differential effects of ethanol on the expression of cyclo-oxygenase in cultured cortical astrocytes and neurons. Journal of Neurochemistry 2001, 76:1354-1363.
40. Ma M.T., Yeo J.F., Farooqui A.A., Ong W.Y. Role of calcium independent phospholipase A2 in maintaining mitochondrial membrane potential and preventing excessive exocytosis in PC12 cells. Neurochemical Research 2011, 36:347-354.
41. Majchrowicz E. Induction of physical dependence upon ethanol and the associated behavioral changes in rats. Psychopharmacologia 1975, 43:245-254.
42. Manley G.T., Fujimura M., Ma T., Noshita N., Filiz F., Bollen A.W., et al. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nature Medicine 2000, 6:159-163.
43. Moses G.S., Jensen M.D., Lue L.F., Walker D.G., Sun A.Y., Simonyi A., et al. Secretory PLA2-IIA: a new inflammatory factor for Alzheimer's disease. Journal of Neuroinflammation 2006, 3.
44. Obernier J.A., Bouldin T.W., Crews F.T. Binge ethanol exposure in adult rats causes necrotic cell death. Alcoholism: Clinical & Experimental Research 2002, 26:547-557.
45. Obernier J.A., White A.M., Swartzwelder H.S., Crews F.T. Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats. Pharmacology Biochemistry & Behavior 2002, 72:521-532.
46. Ong W.Y., Farooqui T., Farooqui A.A. Involvement of cytosolic phospholipase A(2), calcium independent phospholipase A(2) and plasmalogen selective phospholipase A(2) in neurodegenerative and neuropsychiatric conditions. Current Medicinal Chemistry 2010, 17:2746-2763.
47. Pacher P., Szabo C. Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. American Journal of Pathology 2008, 173:2-13.
48. Przybycien-Szymanska M.M., Mott N.N., Paul C.R., Gillespie R.A., Pak T.R. Binge-pattern alcohol exposure during puberty induces long-term changes in HPA axis reactivity. PLoS ONE 2011, 6:e18350.
49. Rao J.S., Ertley R.N., DeMar J.C., Rapoport S.I., Bazinet R.P., Lee H.J. Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex. Molecular Psychiatry 2007, 12:151-157.
50. Roberta A., Rossella B. Aquaporins and glia. Current Neuropharmacology 2010, 8:84-91.
51. Saadoun S., Papadopoulos M.C. Aquaporin-4 in brain and spinal cord oedema. Neuroscience 2010, 168:1036-1046.
52. Seleznev K., Zhao C., Zhang X.H., Song K., Ma Z.A. Calcium-independent phospholipase A2 localizes in and protects mitochondria during apoptotic induction by staurosporine. Journal of Biological Chemistry 2006, 281:22275-22288.
53. Shinzawa K., Sumi H., Ikawa M., Matsuoka Y., Okabe M., Sakoda S., et al. Neuroaxonal dystrophy caused by group VIA phospholipase A2 deficiency in mice: a model of human neurodegenerative disease. Journal of Neuroscience 2008, 28:2212-2220.
54. Simonyi A., Woods D., Sun A.Y., Sun G.Y. Grape polyphenols inhibit chronic ethanol-induced COX-2 mRNA expression in rat brain. Alcoholism: Clinical & Experimental Research 2002, 26:352-357.
55. Sripathirathan K., Brown J., Neafsey E.J., Collins M.A. Linking binge alcohol-induced neurodamage to brain edema and potential aquaporin-4 upregulation: evidence in rat organotypic brain slice cultures and in vivo. Journal of Neurotrauma 2009, 26:261-273.
56. Strokin M., Chechneva O., Reymann K.G., Reiser G. 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 2006, 140:547-553.
57. Sun G.Y., Shelat P.B., Jensen M.B., He Y., Sun A.Y., Simonyi A. Phospholipases A2 and inflammatory responses in the central nervous system. NeuroMolecular Medicine 2010, 12:133-148.
58. Switzer R.C., Majchrowicz E., Weight F. Ethanol-induced argyrophilia in entorhinal cortex of rat. Anatomical Record 1982, 202:186A.
59. Tomas-Camardiel M., Venero J.L., de Pablos R.M., Rite I., Machado A., Cano J. In vivo expression of aquaporin-4 by reactive microglia. Journal of Neurochemistry 2004, 91:891-899.
60. Wang Y., Dawson V.L., Dawson T.M. Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Experimental Neurology 2009, 218:193-202.
61. Wu A., Ying Z., Gomez-Pinilla F. The salutary effects of DHA dietary supplementation on cognition, neuroplasticity, and membrane homeostasis after brain trauma. Journal of Neurotrauma 2011, 28:2113-2122.
62. Yang H.C., Mosior M., Ni B., Dennis E.A. Regional distribution, ontogeny, purification, and characterization of the Ca2+-independent phospholipase A2 from rat brain. Journal of Neurochemistry 1999, 73:1278-1287.
63. Zou J., Crews F. Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-kappaB and proinflammatory cytokines. Alcoholism: Clinical & Experimental Research 2010, 34:777-789.