Mechanisms of ammonia-induced cell death in rat cortical neurons: Roles of NMDA receptors and glutathione

Neurochemistry International

Volumn 47, Issue 1-2 SPEC. ISS., 2005, Pages 51-57

  Klejman, Agata ^a   Wȩgrzynowicz, Michał ^b   Szatmari, Erzsebet M ^c   Mioduszewska, Barbara ^a   Hetman, Michał ^a,c   Albrecht, Jan ^b  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Akt; Ammonia; Apoptosis; Cortical neurons; Excitotoxicity; Glutathione

Indexed keywords

4 AMINOBUTYRIC ACID; AMMONIA; AMMONIUM CHLORIDE; BUTHIONINE SULFOXIMINE; DIZOCILPINE; GLUTATHIONE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIPECOTIC ACID; TAURINE; TETRAZOLIUM;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL ASSAY; CELL CULTURE; CELL DEATH; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; INCUBATION TIME; NERVE CELL DEGENERATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

AMMONIA; AMMONIUM CHLORIDE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; GLUTATHIONE; HEPATIC ENCEPHALOPATHY; HYPERAMMONEMIA; NEURONS; NEUROTOXINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 20544457990     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2005.04.006     Document Type: Article

References (49)

1. J. Albrecht Astrocytes and ammonia neurotoxicity M. Aschner H.K. Kimelberg The Role of Glia in Neurotoxicity 1996 CRC Press Boca Raton 137 153
2. M.A. Baker, G.J. Cerniglia, and A. Zaman Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples Anal. Biochem. 190 1990 360 365
3. A.A. Boldyrev, P. Johnson, Y. Wei, Y. Tan, and D.O. Carpenter Carnosine and taurine protect rat cerebellar granular cells from free radical damage Neurosci. Lett. 263 1999 169 172
4. E. Bonfoco, D. Krainc, M. Ankarcrona, P. Nicotera, and S.A. Lipton Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures Proc. Natl. Acad. Sci. U.S.A. 92 1995 7162 7166
5. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
6. H.O. Conn, and J. Bircher Hepatic Encephalopathy: Syndromes and Therapies 1994 Medi-Ed Press Bloomington
7. S.R. Datta, A. Brunet, and M.E. Greenberg Cellular survival: a play in three Akts Genes Dev. 13 1999 2905 2927
8. S.R. Datta, H. Dudek, X. Tao, S. Masters, H.A. Fu, Y. Gotoh, and M.E. Greenberg Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 91 1997 231 241
9. M. Dolińska, W. Hilgier, and J. Albrecht Ammonia stimulates glutamine uptake to nonsynaptic cerebral mitochondria of the rat Neurosci. Lett. 11 1996 175 184
10. L.R. Drewes, and R.L. Leino Neuron-specific mitochondrial degeneration induced by hyperammonemia and octanoic acidemia Brain Res. 340 1985 211 218
11. R. Dringen Metabolism and functions of glutathione in the brain Prog. Neurobiol. 62 2000 649 671
12. R. Dringen, B. Pfeiffer, and B. Hamprecht Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione J. Neurosci. 19 1999 562 569
13. A. El Idrissi, and E. Trenkner Growth factors and taurine protect against excitotoxicity by stabilizing calcium homeostasis and energy metabolism J. Neurosci. 19 1999 9459 9468
14. L. Faff-Michalak, and J. Albrecht Aspartate aminotransferase, malate dehydrogenase, and pyruvate-carboxylase activities in rat cerebral synaptic and nonsynaptic mitochondria: effects of in vitro treatment with ammonia, hyperammonemia and hepatic encephalopathy Metab. Brain Dis. 6 1991 187 197
15. V. Felipo, and R.F. Butterworth Mitochondrial dysfunction in acute hyperammonemia Neurochem. Int. 40 2002 487 491
16. F. Fonnum, and E.A. Lock The contribution of excitotoxicty, glutathione depletion and DNA repair in chemically induced injury to neurons: exemplified with toxic effects on cerebellar granule cells J. Neurochem. 88 2004 513 531
17. K. Fukunaga, and T. Kawano Akt is a molecular target for signal transduction therapy in brain ischemic insult J. Pharmacol. Sci. 2003 317 327
18. O.W. Griffith Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine Anal. Biochem. 106 1980 207 212
19. M.B. Hansen, S.E. Nielsen, and K. Berg Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill J. Immunol. Methods 119 1989 203 210
20. S.J. Heales, A.A. Lam, A.J. Duncan, and J.M. Land Neurodegeneration or neuroprotection: the pivotal role of astrocytes Neurochem. Res. 29 2004 513 519
21. C. Hermenegildo, G. Marcaida, C. Montoliu, S. Grisolia, M.D. Miňana, and V. Felipo NMDA receptor antagonists prevent acute ammonia toxicity in mice Neurochem. Res. 21 1996 1237 1244
22. C. Hermenegildo, P. Monfort, and V. Felipo Activation of N-methyl-d-aspartate receptors in rat brain in vivo following acute ammonia intoxication: characterization by in vivo brain microdialysis Hepatology 31 2000 709 715
23. L. Hertz, A.C. Yu, G. Kala, and A. Schousboe Neuronal-astrocytic and cytosolic-mitochondrial metabolite trafficking during brain activation, hyperammonemia and energy deprivation Neurochem. Int. 37 2000 83 102
24. M. Hetman, K. Kanning, J.E. Cavanaugh, and Z. Xia Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase J. Biol. Chem. 274 1999 22569 22580
25. W. Hilgier, E. Anderzhanova, S.S. Oja, P. Saransaari, and J. Albrecht 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 2003 21 25
26. A.M. Insausti, J.M. Gaztelu, L.M. Gonzalo, M. Romero-Vives, C. Barrenechea, V. Felipo, and R. Insausti Diet induced hyperammonemia decreases neuronal nuclear size in rat entorhinal cortex Neurosci. Lett. 231 1997 179 181
27. E. Kosenko, Y. Kaminsky, I.G. Stavroskaya, and V. Felipo Alteration of mitochondrial calcium homeostasis by ammonia-induced activation of NMDA receptors in rat brain in vivo Brain Res. 880 2000 139 146
28. H.R. Luo, H. Hattori, M.A. Hossain, L. Hester, Y. Huang, W. Lee-Kwon, M. Donowitz, E. Nagata, and S.H. Snyder Akt as a mediator of cell death Proc. Natl. Acad. Sci. U.S.A. 100 2003 11712 11717
29. C. Malcolm, A. Grieve, L. Ritchie, A. Schousboe, and R. Griffiths NMDA receptor-mediated cGMP synthesis in primary cultures of mouse cerebellar granule cells appears to involve neuron-astrocyte communication with NO operating as the intercellular messenger J. Neurosci. Res. 45 1996 129 142
30. P. Monfort, E. Kosenko, S. Erceg, J.J. Canales, and V. Felipo Molecular mechanism of acute ammonia toxicity: role of NMDA receptors Neurochem. Int. 41 2002 95 102
31. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. Methods 65 1983 55 63
32. C.R. Murthy, A.S. Bender, R.S. Dombro, G. Bai, and M.D. Norenberg Elevation of glutathione levels by ammonium ions in primary cultures of rat astrocytes Neurochem. Int. 37 2000 255 268
33. C.R. Murthy, K.V. Rama Rao, G. Bai, and M.D. Norenberg Ammonia-induced production of free radicals in primary cultures of rat astrocytes J. Neurosci. Res. 66 2001 282 288
34. M.D. Norenberg Astroglial dysfunction in hepatic encephalopathy Metab. Brain Dis. 13 1998 319 335
35. Y.B. Ouyang, Y. Tan, M. Comb, C.L. Liu, M.E. Martone, B.K. Siesjo, and B.R. Hu Survival- and death-promoting events after transient cerebral ischemia: phosphorylation of Akt, release of cytochrome C and activation of caspase-like proteases J. Cereb. Blood Flow Metab. 19 1999 1126 1135
36. J.C. Partin, J.S. Partin, W.K. Schubert, and R.L. McLaurin Brain ultrastructure in Reye's syndrome J. Neuropathol. Exp. Neurol. 34 1975 425 444
37. J. Peeling, L. Shoemaker, T. Gauthier, A. Benarroch, G.R. Sutherland, and G.Y. Minuk Cerebral metabolic and histological effects of thioacetamide-induced liver failure Am. J. Physiol. 265 1993 G572 G578
38. C.M. Pilbeam, R.M. Anderson, and P.S. Bhathal The brain in experimental portal-systemic encephalopathy. I. Morphological changes in three animal models J. Pathol. 140 1983 331 345
39. K.V. Rama Rao, M. Chen, J.M. Simard, and M.D. Norenberg Suppression of ammonia-induced astrocyte swelling by cyclosporin A J. Neurosci. Res. 74 2003 891 897
40. F. Schliess, B. Gorg, R. Fischer, P. Desjardins, H.J. Bidmon, A. Herrmann, R.F. Butterworth, K. Zilles, and D. Häussinger Ammonia induces MK-801-sensitive nitration and phosphorylation of protein tyrosine residues in rat astrocytes FASEB J. 16 2002 739 741
41. J.I. Sagara, K. Miura, and S. Bannai Maintenance of neuronal glutathione by glial cells J. Neurochem. 61 1993 1672 1676
42. J.C. Szerb, and R.F. Butterworth Effect of ammonium ions on synaptic transmission in the mammalian central nervous system Prog. Neurobiol. 39 1992 135 153
43. F. Tietze Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues Anal. Biochem. 27 1969 502 522
44. I. Velasco, and R. Tapia High extracellular gamma-aminobutyric acid protects cultured neurons against damage induced by the accumulation of endogenous extracellular glutamate J. Neurosci. Res. 67 2002 406 410
45. U. Wullner, J. Seyfried, P. Groscurth, S. Beinroth, S. Winter, M. Gleichmann, M. Heneka, P. Loschmann, J.B. Schulz, M. Weller, and T. Klockgether Glutathione depletion and neuronal cell death: the role of reactive oxygen intermediates and mitochondrial function Brain Res. 826 1999 53 62
46. L. Yang, K. Omori, K. Omori, H. Otani, J. Suzukawa, and C. Inagaki GABAC receptor agonist suppressed ammonia-induced apoptosis in cultured rat hippocampal neurons by restoring phosphorylated BAD level J. Neurochem. 87 2003 791 800
47. L. Yang, K. Omori, J. Suzukawa, and C. Inagaki Calcineurin-mediated BAD Ser155 dephosphorylation in ammonia-induced apoptosis of cultured rat hippocampal neurons Neurosci. Lett. 357 2004 73 75
48. M. Zielińska, W. Hilgier, H.D. Borkowska, S.S. Oja, P. Saransaari, P. Goryński, and J. Albrecht Ammonia-induced extracellular accumulation of taurine in the rat striatum in vivo: role of ionotropic glutamate receptors Neurochem. Res. 27 2002 37 42
49. M. Zielińska, R.O. Law, and J. Albrecht Excitotoxic mechanism of cell swelling in rat cerebral cortical slices treated acutely with ammonia Neurochem. Int. 43 2003 299 303