Evidence for oxidative/nitrosative stress in the pathogenesis of hepatic encephalopathy

Metabolic Brain Disease

Volumn 25, Issue 1, 2010, Pages 3-9

  Bemeur, Chantal ^a   Desjardins, Paul ^a   Butterworth, Roger F ^a  

^a UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Antioxidants; Hepatic encephalopathy; Liver failure; Oxidative stress

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; AMMONIA; ASCORBIC ACID; AZOXYMETHANE; BUTYLATED HYDROXYANISOLE; CARNITINE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; DEFEROXAMINE; DIMETHYL SULFOXIDE; DIMETHYLTHIOUREA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; INDOMETACIN; MANGANESE; MELATONIN; MESSENGER RNA; MINOCYCLINE; NITRATE; NITRITE; SUPEROXIDE DISMUTASE; THIOACETAMIDE;

BRAIN EDEMA; CONFERENCE PAPER; FRONTAL CORTEX; HEPATIC ENCEPHALOPATHY; HUMAN; HYPERAMMONEMIA; IMMUNOHISTOCHEMISTRY; INTRACRANIAL PRESSURE; LIPID PEROXIDATION; LIVER FAILURE; LIVER PROTECTION; MITOCHONDRIAL PERMEABILITY; NEUROTOXICITY; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN EXPRESSION;

ANIMALS; BRAIN; CYTOKINES; FREE RADICAL SCAVENGERS; FREE RADICALS; HEPATIC ENCEPHALOPATHY; HUMANS; HYPERAMMONEMIA; LIVER FAILURE; NITRATES; NITROSATION; OXIDATIVE STRESS;

ANIMALIA;

EID: 77954143165     PISSN: 08857490     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11011-010-9177-y     Document Type: Conference Paper

References (71)

1. S Ahboucha G Pomier-Layrargues O Mamer RF Butterworth 2006 Increased levels of pregnenolone and its neuroactive metabolite allopregnanolone in autopsied brain tissue from cirrhotic patients who died in hepatic coma Neurochem Int 49 372 378 10.1016/j.neuint.2006.02.002 1:CAS:528: DC%2BD28Xns1Smtrs%3D 16563564 (Pubitemid 44119043)
2. M Asanuma S Nishibayashi-Asanuma I Miyazaki M Kohno N Ogawa 2001 Neuroprotective effects of non-steroidal anti-inflammatory drugs by direct scavenging of nitric oxide radicals J Neurochem 76 1895 1904 10.1046/j.1471-4159.2001.00205.x 1:CAS:528:DC%2BD3MXitlSktLo%3D 11259508 (Pubitemid 32221130)
3. G Bai KV Rama Rao CR Murthy KS Panickar AR Jayakumar MD Norenberg 2001 Ammonia induces the mitochondrial permeability transition in primary cultures of rat astrocytes J Neurosci Res 66 981 991 10.1002/jnr.10056 1:CAS:528: DC%2BD3MXpt1SgtLk%3D 11746427 (Pubitemid 33126402)
4. C Bemeur L Ste-Marie P Desjardins L Vachon RF Butterworth AS Hazell J Montgomery 2005 Dehydrascorbic acid normalizes several markers of oxidative stress and inflammation in acute hyperglycemic focal cerebral ischemia in the rat Neurochem Int 46 399 407 10.1016/j.neuint.2004.11.007 1:CAS:528: DC%2BD2MXhvVeksbo%3D 15737438 (Pubitemid 40292720)
5. Bemeur C, Jiang W, Desjardins P, Butterworth RF (2009) Mild hypothermia attenuates oxidative/nitrosative stress and cytotoxic brain edema in experimental acute liver failure. XXIVth International Symposium on Cerebral Blood Flow, Metabolism and Function & IXth International Conference on Quantification of Brain Function with PET, Chicago, IL, USA
6. Bemeur C, Vaquero J, Desjardins P, Butterworth RF (2010a) N-Acetylcysteine attenuates cerebral complications of non-acetaminophen-induced acute liver failure in mice: antioxidant and anti-inflammatory mechanisms. Metab Brain Dis (in press)
7. Bemeur C, Desjardins P, Butterworth RF (2010b) Antioxidant and anti-inflammatory effects of mild hypothermia in the attenuation of liver injury due to azoxymethane toxicity in the mouse. Metab Brain Dis (in press)
8. R Bruck H Aeed H Shirin Z Matas L Zaidel Y Avni Z Halpern 1999 The hydroxyl radical scavengers dimethylsulfoxide and dimethylthiourea protect rats against thioacetamide-induced fulminant hepatic failure J Hepatol 31 27 38 10.1016/S0168-8278(99)80160-3 1:CAS:528:DyaK1MXktlCjtLo%3D 10424280 (Pubitemid 29287606)
9. UT Brunk 1989 On the origin of lipofuscin; the iron content of residual bodies, and the relation of these organelles to the lysosomal vacuome. A study on cultured human glial cells Adv Exp Med Biol 266 313 320 1:CAS:528: DyaK3MXit1KgsL8%3D 2486159
10. SW Brusilow DL Valle M Batshaw 1979 New pathways of nitrogen excretion in inborn errors of urea synthesis Lancet 2 452 254 10.1016/S0140-6736(79)91503-4 1:CAS:528:DyaL3cXls1WgsQ%3D%3D 89510
11. RF Butterworth 2002 Pathophysiology of hepatic encephalopathy: a new look at ammonia Metab Brain Dis 17 221 227 10.1023/A:1021989230535 1:CAS:528:DC%2BD3sXislGksQ%3D%3D 12602499 (Pubitemid 36204752)
12. C Chung J Gottstein AT Blei 2001 Indomethacin prevents the development of experimental ammonia-induced brain edema in rats after portacaval anastomosis Hepatology 34 249 254 10.1053/jhep.2001.26383 1:CAS:528:DC%2BD3MXmtVGqt78%3D 11481608 (Pubitemid 32702336)
13. JO Clemmesen BA Hansen FS Larsen 1997 Indomethacin normalizes intracranial pressure in acute liver failure: a twenty-three-year-old woman treated with indomethacin Hepatology 26 1423 1425 10.1002/hep.510260608 1:STN:280:DyaK1c%2FlvVGqsg%3D%3D 9397981
14. J Cordoba J Crespin J Gottstein AT Blei 1999 Mild hypothermia modifies ammonia- induced brain edema in rats after portacaval anastomosis Gastroenterology 116 686 693 10.1016/S0016-5085(99)70191-5 1:STN:280: DyaK1M7lsFarug%3D%3D 10029628
15. P Desjardins RF Butterworth 2002 The "peripheral-type" benzodiazepine (omega 3) receptor in hyperammonemic disorders Neurochem Int 41 109 114 10.1016/S0197-0186(02)00031-1 1:CAS:528:DC%2BD38XjvVejtb4%3D 12020611 (Pubitemid 34521684)
16. MY Globus O Alonso WD Dietrich R Busto MD Ginsberg 1995 Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia J Neurochem 65 1704 1711 1:CAS:528:DyaK2MXotFOks7g%3D 7561868
17. B Görg N Foster R Reinehr HJ Bidmon A Höngen D Häussinger F Schliess 2003 Benzodiazepine-induced protein tyrosine nitration in rat astrocytes Hepatology 37 334 342 10.1053/jhep.2003.50061 12540783 (Pubitemid 36152532)
18. B Görg N Qvartskhava P Voss T Grune D Häussinger F Schliess 2007 Reversible inhibition of mammalian glutamine synthetase by tyrosine nitration FEBS Lett 581 84 90 10.1016/j.febslet.2006.11.081 17174954 (Pubitemid 44960284)
19. VH Guerrini 1994 Effect of antioxidants on ammonia induced CNS-renal pathobiology in sheep Free Radic Res 21 35 43 10.3109/10715769409056553 1:CAS:528:DyaK2cXkvF2ktL8%3D 7951910
20. B Halliwell 1992 Reactive oxygen species and the central nervous system J Neurochem 59 1609 1623 10.1111/j.1471-4159.1992.tb10990.x 1:CAS:528: DyaK38XmsVKlsbk%3D 1402908
21. PM Harrison JA Wendon AE Gimson GJ Alexander R Williams 1991 Improvement by acetylcysteine of hemodynamics and oxygen transport in fulminant hepatic failure N Engl J Med 324 1852 1857 1:STN:280:DyaK3M3ltFyltQ%3D%3D 1904133
22. RF Haseloff IE Blasig H Meffert B Ebert 1990 Hydroxyl radical scavenging and antipsoriatic activity of benzoic acid derivatives Free Radic Biol Med 9 111 115 10.1016/0891-5849(90)90113-W 1:CAS:528:DyaK3MXmt1aktrg%3D 2172097 (Pubitemid 20270679)
23. RA Hawkins J Jessy AM Mans MR De Joseph 1993 Effect of reducing brain glutamine synthesis on metabolic symptoms of hepatic encephalopathy J Neurochem 60 1000 1006 10.1111/j.1471-4159.1993.tb03247.x 1:CAS:528:DyaK3sXksVKltLk%3D 8436955
24. C Hermenegildo G Marcaida C Montoliu S Grisolia MD Minana V Felipo 1996 NMDA receptor antagonists prevent acute ammonia toxicity in mice Neurochem Res 21 1237 1244 10.1007/BF02532401 1:CAS:528:DyaK28XmtlKntbw%3D 8923486 (Pubitemid 26357276)
25. C Hermenegildo P Monfort V Felipo 2000 Activation of N-methyl-D-aspartate receptors in rat brain in vivo following acute ammonia intoxication: characterization by in vivo brain microdialysis Hepatology 31 709 715 10.1002/hep.510310322 1:CAS:528:DC%2BD3cXhvFGjsrc%3D 10706562
26. R Hernández E Martinez-Lara ML Del Moral S Blanco A Cañuelo E Siles FJ Esteban JA Pedrosa MA Peinado 2004 Upregulation of endothelial nitric oxide synthase maintains nitric oxide production in the cerebellum of thioacetamide cirrhotic rats Neuroscience 126 879 887 10.1016/j.neuroscience. 2004.04.010 15207323 (Pubitemid 38780893)
27. W Hilgier E Anderzhanova SS Oja P Saransaari J Albrecht 2003 Taurine reduces ammonia- and N-methyl-D-aspartate-induced accumulation of cyclic GMP and hydroxyl radicals in microdialysates of the rat striatum Eur J Pharmacol 468 21 25 10.1016/S0014-2999(03)01667-4 1:CAS:528:DC%2BD3sXjt1Kgtb0%3D 12729839 (Pubitemid 36555748)
28. R Jalan SW Olde Damink NE Deutz A Lee PC Hayes 1999 Moderate hypothermia for uncontrolled intracranial hypertension in acute liver failure Lancet 354 1164 1168 10.1016/S0140-6736(98)12440-6 1:STN:280:DyaK1MvktFylug%3D%3D 10513710 (Pubitemid 29460446)
29. R Jalan SW Olde Damink NE Deutz NA Davies OJ Garden KK Machavan PC Hayes A Lee 2003 Moderate hypothermia prevents cerebral hyperemia and increase in intracranial pressure in patients undergoing liver transplantation for acute liver failure Transplantation 75 2034 2039 10.1097/01.TP.0000066240.42113.FF 12829907
30. W Jiang P Desjardins RF Butterworth 2009 Hypothermia attenuates oxidative/nitrosative stress, encephalopathy and brain edema in acute (ischemic) liver failure Neurochem Int 55 124 128 10.1016/j.neuint.2009.02.007 1:CAS:528:DC%2BD1MXltVKrs7w%3D 19428816
31. W Jiang P Desjardins RF Butterworth 2009 Minocycline attenuates oxidative/nitrosative stress and cerebral complications of acute liver failure in rats Neurochem Int 55 601 605 10.1016/j.neuint.2009.06.001 1:CAS:528:DC%2BD1MXhtV2ru7bE 19524003
32. AL Jones 1998 Mechanism of action and value of n-acetylcysteine in the treatment of early and late acetaminophen poisoning: a critical review J Toxicol Clin Toxicol 36 277 285 10.3109/15563659809028022 1:CAS:528:DyaK1cXlsF2nsr4%3D 9711192
33. E Kosenko Y Kaminsky E Grau MD Miñana G Marcaida S Grisolía V Felipo 1994 Brain ATP depletion induced by acute ammonia intoxication in rats is mediated by activation of the NMDA receptor and Na+, K(+)-ATPase J Neurochem 63 2172 2178 1:CAS:528:DyaK2MXit12kurk%3D 7964737
34. E Kosenko Y Kaminsky A Kaminsky M Valencia L Lee C Hermenegildo V Felipo 1997 Superoxide production and antioxidant enzymes in ammonia intoxication in rats Free Radic Res 27 637 644 10.3109/10715769709097867 1:CAS:528: DyaK1cXpslWqtA%3D%3D 9455699
35. E Kosenko Y Kaminski O Lopata N Muravyoy V Felipo 1999 Blocking NMDA receptors prevents the oxidative stress induced by acute ammonia intoxication Free Radic Biol Med 26 1369 1374 10.1016/S0891-5849(98)00339-6 1:STN:280:DyaK1MzivFynsA%3D%3D 10401599 (Pubitemid 29302268)
36. E Kosenko N Venediktova Y Kaminsky C Montoliu V Felipo 2003 Sources of oxygen radicals in brain in acute ammonia intoxication in vivo Brain Res 98 193 200 10.1016/S0006-8993(03)03035-X (Pubitemid 37281235)
37. E Kosenko C Montoliu G Giordano Y Kaminsky N Venediktova Y Buryanov V Felipo 2004 Acute ammonia intoxication induces an NMDA receptor-mediated increase in poly(ADP-ribose) polymerase level and NAD metabolism in nuclei of rat brain cells J Neurochem 89 1101 1110 10.1111/j.1471-4159.2004.02426.x 1:CAS:528:DC%2BD2cXkvFOktb4%3D 15147502 (Pubitemid 38715827)
38. FS Laroux KP Pavlick IN Hines S Kawachi H Harada S Bharwani JM Hoffman MB Grisham 2001 Role of nitric oxide in inflammation Acta Physiol Scand 173 113 118 10.1046/j.1365-201X.2001.00891.x 1:CAS:528:DC%2BD3MXnt1Cnu7o%3D 11678733 (Pubitemid 32948340)
39. FS Larsen J Gottstein AT Blei 2001 Cerebral hyperemia and nitric oxide synthase in rats with ammonia-induced brain edema J Hepatol 34 548 554 10.1016/S0168-8278(00)00069-6 1:CAS:528:DC%2BD3MXjvVertbs%3D 11394654 (Pubitemid 32328511)
40. G Marcaida V Felipo C Hermenegildo MD Manama S Grisolia 1992 Acute ammonia toxicity is mediated by the NMDA type of glutamate receptors FEBS Lett 296 67 68 10.1016/0014-5793(92)80404-5 1:CAS:528:DyaK38XnvVWisw%3D%3D 1346118
41. S Master J Gottstein AT Blei 1999 Cerebral blood flow and the development of ammonia-induced brain edema in rats after portacaval anastomosis Hepatology 30 876 880 10.1002/hep.510300428 1:STN:280:DyaK1MvivVCgsw%3D%3D 10498637 (Pubitemid 29458274)
42. TJ Miller AD Phelka RB Tjalkens LA Dethloff MA Philbert 2003 CI-1010 induced opening of the mitochondrial permeability transition pore precedes oxidative stress and apoptosis in SY5Y neuroblastoma cells Brain Res 963 43 56 10.1016/S0006-8993(02)03838-6 1:CAS:528:DC%2BD3sXmsV2isA%3D%3D 12560110 (Pubitemid 36126285)
43. DD Mousseau RF Butterworth 1994 Current theories on the pathogenesis of hepatic encephalopathy Proc Soc Exp Biol Med 206 329 344 1:CAS:528: DyaK2cXlslKhu7w%3D 7915420
44. CR Murthy KV Rama Rao G Bai MD Norenberg 2001 Ammonia-induced production of free radicals in primary cultures of rat astrocytes J Neurosci Res 66 282 288 10.1002/jnr.1222 1:CAS:528:DC%2BD3MXnsVykur8%3D 11592125 (Pubitemid 32912297)
45. MD Norenberg 1981 The astrocyte in liver disease Adv Cell Neurobiol 2 303 352
46. MD Norenberg Z Huo JT Neary A Roig-Cantesano 1997 The glial glutamate transporter in hyperammonemia and hepatic encephalopathy: relation to energy metabolism and glutamatergic neurotransmission Glia 21 124 133 10.1002/(SICI)1098-1136(199709)21:1<124::AID-GLIA14>3.0.CO;2-U 1:STN:280:DyaK2svkt1ejtA%3D%3D 9298855 (Pubitemid 27389648)
47. MD Norenberg AR Jayakumar KV Rama Rao KS Panickar 2007 New concepts in the mechanism of ammonia-induced astrocyte swelling Metab Brain Dis 22 219 234 10.1007/s11011-007-9062-5 1:CAS:528:DC%2BD2sXht1amurzO 17823859 (Pubitemid 47624314)
48. JE O'Connor M Costell 1990 New roles of carnitine metabolism in ammonia cytotoxicity Adv Exp Med Biol 272 183 195 2103686
49. KV Rama Rao AR Jayakumar MD Norenberg 2003 Ammonia neurotoxicity: role of the mitochondrial permeability transition Metab Brain Dis 18 113 127 10.1023/A:1023858902184 1:STN:280:DC%2BD3s3psFantw%3D%3D 12822830 (Pubitemid 36718124)
50. KV Rama Rao AR Jayakumar MD Norenberg 2005 Role of oxidative stress in the ammonia-induced mitochondrial permeability transition in cultured astrocytes Neurochem Int 47 31 38 10.1016/j.neuint.2005.04.004 1:STN:280: DC%2BD2MzjsFSjtA%3D%3D 15908047 (Pubitemid 40848690)
51. VL Rao 2002 Nitric oxide in hepatic encephalopathy and hyperammonemia Neurochem Int 41 161 170 10.1016/S0197-0186(02)00038-4 1:CAS:528: DC%2BD38XjvVejtbs%3D 12020616 (Pubitemid 34521689)
52. KV Rao MD Norenberg 2001 Cerebral energy metabolism in hepatic encephalopathy and hyperammonemia Metab Brain Dis 16 67 78 10.1023/A: 1011666612822 1:CAS:528:DC%2BD3MXpt1Wnt7c%3D 11726090 (Pubitemid 33064038)
53. VL Rao RM Audet RF Butterworth 1995 Increased nitric oxide synthase activities and L-[3H]arginine uptake in brain following portacaval anastomosis J Neurochem 65 677 678 1:CAS:528:DyaK2MXntFGgsLc%3D 7542313
54. PV Reddy CR Murthy P Reddanna 2004 Fulminant hepatic failure induced oxidative stress in nonsynaptic mitochondria of cerebral cortex in rats Neurosci Lett 368 15 20 10.1016/j.neulet.2004.06.046 1:CAS:528:DC%2BD2cXntlSlsLk%3D 15342125 (Pubitemid 39178739)
55. C Rose A Michalak M Pannunzio N Chatauret A Rambaldi RF Butterworth 2000 Mild hypothermia delays the onset of coma and prevents brain edema and extracellular brain glutamate accumulation in rats with acute liver failure Hepatology 31 872 877 10.1053/he.2000.5923 1:CAS:528:DC%2BD3cXis1Cksrg%3D 10733542
56. KV Sathyasaikumar I Swapna PV Reddy ChR Murthy A Dutta Gupta B Senthilkumaran P Reddanna 2007 Fulminant hepatic failure in rats induces oxidative stress differentially in cerebral cortex, cerebellum and pons medulla Neurochem Res 32 517 524 10.1007/s11064-006-9265-x 1:CAS:528: DC%2BD2sXhslWisLk%3D 17268843 (Pubitemid 46295151)
57. K Sawara P Desjardins N Chatauret A Kato K Suzuki RF Butterworth 2009 Alterations in expression of genes coding for proteins of the neurovascular unit in ischemic liver failure Neurochem Int 55 119 123 10.1016/j.neuint.2009.01.023 1:CAS:528:DC%2BD1MXltVKrs78%3D 19428815
58. S Schenker KS Warren 1962 Effect of temperature variation on toxicity and metabolism of ammonia in mice J Lab Clin Med 60 291 301 1:CAS:528: DyaF3sXkt1CrtA%3D%3D 14498233
59. F Schliess B Görg R Fischer P Desjardins HJ Bidmon A Herrmann RF Butterworth K Zilles D Häussinger 2002 Ammonia induces MK-801-sensitive nitration and phosphorylation of protein tyrosine residues in rat astrocytes FASEB J 16 739 741 1:CAS:528:DC%2BD38XjsVeqt74%3D 11923223
60. F Schliess B Görg D Häussinger 2006 Pathogenetic interplay between osmotic and oxidative stress: the hepatic encephalopathy paradigm Biol Chem 387 1363 1370 10.1515/BC.2006.171 1:CAS:528:DC%2BD28XhtFygtLjK 17081108 (Pubitemid 44691416)
61. G Song VK Dhodda AT Blei RJ Dempsey VL Rao 2002 GeneChip analysis shows altered mRNA expression of transcripts of neurotransmitter and signal transduction pathways in the cerebral cortex of portacaval shunted rats J Neurosci Res 68 730 737 10.1002/jnr.10268 1:CAS:528:DC%2BD38XksFGru7g%3D 12111833 (Pubitemid 34594989)
62. I Suárez G Bodega M Rubino V Felipo B Fernández 2005 Neuronal and inducible nitric oxide synthase expression in the rat cerebellum following portacaval anastomosis Brain Res 1047 205 213 10.1016/j.brainres.2005. 04.035 15904901 (Pubitemid 40799315)
63. I Suárez G Bodega E Arilla V Felipo B Fernández 2006 The expression of nNOS, iNOS and nitrotyrosine is increased in the rat cerebral cortex in experimental hepatic encephalopathy Neuropathol Appl Neurobiol 32 594 604 10.1111/j.1365-2990.2006.00768.x 17083474 (Pubitemid 44684645)
64. S Sushma S Dasarathy RK Tandon S Jain S Gupta MS Bhist 1992 Sodium benzoate in the treatment of acute hepatic encephalopathy: a double-blind randomized trial Hepatology 16 138 144 10.1002/hep.1840160123 1:STN:280:DyaK38zhs1ClsQ%3D%3D 1618465
65. JC Szerb RF Butterworth 1992 Effect of ammonium ions on synaptic transmission in the mammalian central nervous system Prog Neurobiol 39 135 153 10.1016/0301-0082(92)90008-3 1:CAS:528:DyaK38XltVyls7Y%3D 1354386
66. H Takahashi RC Koehler SW Brusilow RJ Traystman 1991 Inhibition of brain glutamine accumulation prevents cerebral edema in hyperammonemic rats Am J Physiol 261 H825 H829 1:CAS:528:DyaK3MXmtVGjurs%3D 1679605
67. P Traber M DalCanto D Ganger AT Blei 1989 Effect of body temperature on brain edema and encephalopathy in the rat after hepatic devascularization Gastroenterology 96 885 891 1:STN:280:DyaL1M7itFCisg%3D%3D 2914649
68. I Túnez MC Muñoz FJ Medina M Salcedo M Feijóo P Montilla 2007 Comparison of melatonin, vitamin E and L-carnitine in the treatment of neuro- and hepatoxicity induced by thioacetamide Cell Biochem Funct 25 119 127 10.1002/cbf.1276 16245358 (Pubitemid 46408644)
69. KK Upreti M Das SK Khanna 1991 Role of antioxidants and scavengers on argemone oil-induced toxicity in rats Arch Environ Contam Toxicol 20 531 537 10.1007/BF01065845 1:CAS:528:DyaK3MXisVagsbk%3D 2069426
70. JA Wendon PM Harrison R Keays R Williams 1994 Cerebral blood flow and metabolism in fulminant liver failure Hepatology 19 1407 1413 10.1002/hep.1840190614 1:STN:280:DyaK2c3ksFSqtA%3D%3D 8188170
71. A Zarros S Theocharis N Skandali S Tsakiris 2008 Effects of fulminant hepatic encephalopathy on the adult rat brain antioxidant status and the activities of acetylcholinesterase, (Na(+), K(+))- and Mg (2+)-ATPase: comparison of the enzymes' response to in vitro treatment with ammonia Metab Brain Dis 23 255 264 10.1007/s11011-008-9091-8 1:CAS:528:DC%2BD1cXhtVSrsr3J 18665440