Ammonia triggers exocytotic release of L-glutamate from cultured rat astrocytes

GLIA

Volumn 58, Issue 6, 2010, Pages 691-705

  Görg, Boris ^a   Morwinsky, Anke ^a   Keitel, Verena ^a   Qvartskhava, Natalia ^a   Schrör, Karsten ^a   Häussinger, Dieter ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Hepatic encephalopathy; Nmda receptors; Oxidative stress; Prostanoids; VAMP2; Vesicle exocytosis

Indexed keywords

AMMONIA; AMMONIUM CHLORIDE; CALCIUM ION; COLCHICINE; GLUTAMIC ACID; INDOMETACIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROSTAGLANDIN E2; PROSTANOID; SMALL INTERFERING RNA; SYNAPTOBREVIN 2; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ASTROCYTE; BRAIN; CALCIUM CELL LEVEL; CULTURE MEDIUM; EXOCYTOSIS; HEPATIC ENCEPHALOPATHY; MEMBRANE VESICLE; MICROSCOPY; NERVE CELL CULTURE; NEUROTRANSMITTER RELEASE; OXIDATIVE STRESS; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; TOTAL INTERNAL REFLECTION MICROSCOPY; WESTERN BLOTTING;

AMMONIA; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BACTERIAL PROTEINS; BRAIN; CALCIUM; CELLS, CULTURED; CHELATING AGENTS; CYCLOOXYGENASE INHIBITORS; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; EXOCYTOSIS; FLUOROMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; INDOMETHACIN; LUMINESCENT PROTEINS; PROSTAGLANDINS; PROTEIN TRANSPORT; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RATS; RATS, WISTAR; RNA; RNA, SMALL INTERFERING; TRANSFECTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 77950898706     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20955     Document Type: Article

References (64)

1. Allert N, Koller H, Siebler M. 1998. Ammonia-induced depolarization of cultured rat cortical astrocytes. Brain Res 782:261-270. (Pubitemid 28123003)
2. Alvarez-Leefmans FJ, Herrera-Perez JJ, Marquez MS, Blanco VM. 2006. Simultaneous measurement of water volume and pH in single cells using BCECF and fluorescence imaging microscopy. Biophys J 90:608-618.
3. Andersson AK, Adermark L, Persson M, Westerlund A, Olsson T, Hansson E. 2009. Lactate contributes to ammonia-mediated astroglial dysfunction during hyperammonemia. Neurochem Res 34:556-565.
4. Araque A, Li N, Doyle RT, Haydon PG. 2000. SNARE protein-dependent glutamate release from astrocytes. J Neurosci 20:666-673. (Pubitemid 30225569)
5. Bal-Price A, Moneer Z, Brown GC. 2002. Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 40:312-323. (Pubitemid 36010738)
6. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A. 1998. Prostaglandins stimulate calcium-dependent glutamate release in. Nature 391:281-285. (Pubitemid 28099014)
7. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A. 2001. CXCR4-activated astrocyte glutamate release via TNFalpha: Amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702-710.
8. Cauli O, Rodrigo R, Piedrafita B, Boix J, Felipo V. 2007. Inflammation and hepatic encephalopathy: Ibuprofen restores learning ability in rats with portacaval shunts. Hepatology 46:514-519. (Pubitemid 47344787)
9. Cauli O, Rodrigo R, Piedrafita B, Llansola M, Mansouri MT, Felipo V. 2009. Neuroinflammation contributes to hypokinesia in rats with hepatic encephalopathy: Ibuprofen restores its motor activity. J Neurosci Res 87:1369-1374.
10. Chen CJ, Liao SL, Kuo JS. 2000. Gliotoxic action of glutamate on cultured astrocytes. J Neurochem 75:1557-1565.
11. Chen X, Wang L, Zhou Y, Zheng L, Zhou Z. 2005. 'Kiss-and-run' glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J Neurosci 25:9236-9243. (Pubitemid 41500832)
12. Chung C, Gottstein J, Blei AT. 2001. Indomethacin prevents the development of experimental ammonia-induced brain edema in rats after portacaval anastomosis. Hepatology 34:249-254. (Pubitemid 32702336)
13. Cousin MA, Robinson PJ. 1999. Mechanisms of synaptic vesicle recycling illuminated by fluorescent dyes. J Neurochem 73:2227-2239.
14. Crippa D, Schenk U, Francolini M, Rosa P, Verderio C, Zonta M, Pozzan T, Matteoli M, Carmignoto G. 2006. Synaptobrevin2-expressing vesicles in rat astrocytes: Insights into molecular characterization, dynamics and exocytosis. J Physiol 570:567-582.
15. 2+ response in cultured rat astrocytes. Glia 20:51-58.
16. + on synaptosomal membrane potential in the rat brain. Nippon Yakurigaku Zasshi 92:359-364.
17. Görg B, Bidmon HJ, Keitel V, Foster N, Goerlich R, Schliess F, Häussinger D. 2006. Inflammatory cytokines induce protein tyrosine nitration in rat astrocytes. Arch Biochem Biophys 449:104-114.
18. Görg B, Qvartskhava N, Keitel V, Bidmon HJ, Selbach O, Schliess F, Häussinger D. 2008. Ammonia induces RNA oxidation in cultured astrocytes and brain in vivo. Hepatology 48:567-579.
19. Görg B, Qvartskhava N, Voss P, Grune T, Häussinger D, Schliess F. 2007. Reversible inhibition of mammalian glutamine synthetase by tyrosine nitration. FEBS Lett 581:84-90. (Pubitemid 44960284)
20. Harata NC, Choi S, Pyle JL, Aravanis AM, Tsien RW. 2006. Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49:243-256. (Pubitemid 43089641)
21. Häussinger D. 2006. Low grade cerebral edema and the pathogenesis of hepatic encephalopathy in cirrhosis. Hepatology 43:1187-1190. (Pubitemid 43980095)
22. Häussinger D, Blei AT. 2007. Hepatic encephalopathy. In: Rodes J, Benhamou JP, Blei AT, Reichen J, Rizzetto M, editors. Textbook of hepatology. Oxford: Blackwell. pp 728-760.
23. Häussinger D, Laubenberger J, vom Dahl S, Ernst T, Bayer S, Langer M, Gerok W, Hennig J. 1994. Proton magnetic resonance spectroscopy studies on human brain myo-inositol in hypo-osmolarity and hepatic encephalopathy. Gastroenterology 107:1475-1480.
24. Häussinger D, Kircheis G, Fischer R, Schliess F, vom Dahl S. 2000. Hepatic encephalopathy in chronic liver disease: A clinical manifestation of astrocyte swelling and low-grade cerebral edema? J Hepatol 32:1035-1038.
25. Häussinger D, Schliess F. 2008. Pathogenetic mechanisms of hepatic encephalopathy. Gut 57:1156-1165.
26. Hermenegildo C, Marcaida G, Montoliu C, Grisolia S, Minana MD, Felipo V. 1996. NMDA receptor antagonists prevent acute ammonia toxicity in mice. Neurochem Res 21:1237-1244. (Pubitemid 26357276)
27. Hermenegildo C, Monfort P, Felipo V. 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. (Pubitemid 30118640)
28. Kimelberg HK, Goderie SK, Higman S, Pang S, Waniewski RA. 1990. Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 10:1583-1591.
29. Knecht K, Michalak A, Rose C, Rothstein JD, Butterworth RF. 1997. Decreased glutamate transporter (GLT-1) expression in frontal cortex of rats with acute liver failure. Neurosci Lett 229:201-203. (Pubitemid 27316081)
30. 2+ and induces a depolarization in cultured astroglial cells. Brain. 119 (Part 6):2021-2027.
31. Kosenko E, Montoliu C, Giordano G, Kaminsky Y, Venediktova N, Buryanov Y, Felipo V. 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. (Pubitemid 38715827)
32. Kosenko E, Kaminski Y, Lopata O, Muravyov N, Felipo V. 1999. Blocking NMDA receptors prevents the oxidative stress induced by acute ammonia intoxication. Free Radic Biol Med 26:1369-1374. (Pubitemid 29302268)
33. Maclouf J, Sors H, Rigaud M. 1977. Recent aspects of prostaglandin biosynthesis: A review. Biomedicine 26:362-375.
34. Magistretti PJ. 2006. Neuron-glia metabolic coupling and plasticity. J Exp Biol 209:2304-2311.
35. Malarkey EB, Parpura V. 2008. Mechanisms of glutamate release from astrocytes. Neurochem Int 52:142-154.
36. Master S, Gottstein J, Blei AT. 1999. Cerebral blood flow and the development of ammonia-induced brain edema in rats after portacaval anastomosis. Hepatology 30:876-880. (Pubitemid 29458274)
37. Mattson MP. 2008. Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann N Y Acad Sci 1144:97-112.
38. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
39. Michalak A, Knecht K, Butterworth RF. 1997. Hepatic encephalopathy in acute liver failure: Role of the glutamate system. Adv Exp Med Biol 420:35-43. (Pubitemid 27396099)
40. Mollace V, Colasanti M, Muscoli C, Lauro GM, Iannone M, Rotiroti D, Nistico G. 1998. The effect of nitric oxide on cytokine-induced release of PGE2 by human cultured astroglial cells. Br J Pharmacol 124:742-746. (Pubitemid 28276811)
41. Montana V, Ni Y, Sunjara V, Hua X, Parpura V. 2004. Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 24:2633-2642. (Pubitemid 38380939)
42. Ni Y, Parpura V. 2009. Dual regulation of Ca(2+)-dependent glutamate release from astrocytes: Vesicular glutamate transporters and cytosolic glutamate levels. Glia 57:1296-1305.
43. Nishizaki T. 2004. ATP- and adenosine-mediated signaling in the central nervous system: Adenosine stimulates glutamate release from astrocytes via A2a adenosine receptors. J Pharmacol Sci 94:100-102. (Pubitemid 38405120)
44. O'Connor ER, Kimelberg HK. 1993. Role of calcium in astrocyte volume regulation and in the release of ions and amino acids. J Neurosci 13:2638-2650.
45. Pangrsic T, Potokar M, Haydon PG, Zorec R, Kreft M. 2006. Astrocyte swelling leads to membrane unfolding, not membrane insertion. J Neurochem 99:514-523. (Pubitemid 44477207)
46. 2+-dependent peptide secretion in astrocytes. J Neurochem 110:143-156.
47. Reinehr R, Görg B, Becker S, Qvartskhava N, Bidmon HJ, Selbach O, Haas HL, Schliess F, Häussinger D. 2007. Hypoosmotic swelling and ammonia increase oxidative stress by NADPH oxidase in cultured astrocytes and vital brain slices. Glia 55:758-771. (Pubitemid 46663028)
48. Rose C. 2006. Effect of ammonia on astrocytic glutamate uptake/release mechanisms. J Neurochem 97 (Suppl 1):11-15.
49. Rose C, Kresse W, Kettenmann H. 2005. Acute insult of ammonia leads to calcium-dependent glutamate release from cultured, an effect of pH. J Biol Chem 280:20937-20944. (Pubitemid 40805650)
50. 2+-dependent glutamate release. Neuroscience 158:253-259.
51. Schliess F, Foster N, Görg B, Reinehr R, Häussinger D. 2004. Hypoosmotic swelling increases protein tyrosine nitration in cultured rat astrocytes. Glia 47:21-29. (Pubitemid 38879702)
52. Schliess F, Görg B, Fischer R, Desjardins P, Bidmon HJ, Herrmann A, Butterworth RF, Zilles K, Häussinger D. 2002. Ammonia induces MK-801-sensitive nitration and phosphorylation of protein tyrosine residues in rat. FASEB J 16:739-741.
53. Schliess F, Görg B, Häussinger D. 2009. RNA oxidation and zinc in hepatic encephalopathy and hyperammonemia. Metab Brain Dis 24:119-134.
54. Schliess F, Görg B, Reinehr RM, Bidmon H-J, Häussinger D. 2006. Osmotic and oxidative stress in hepatic encephalopathy. In: Häussinger D, Kircheis G, Schliess F, editors. Hepatic encephalopathy and nitrogen metabolism. Dordrecht: Springer. pp 20-42.
55. Schliess F, Sinning R, Fischer R, Schmalenbach C, Häussinger D. 1996. Calcium-dependent activation of Erk-1 and Erk-2 after hypoosmotic astrocyte swelling. Biochem J 320:167-171. (Pubitemid 26400175)
56. Stigliani S, Zappettini S, Raiteri L, Passalacqua M, Melloni E, Venturi C, Tacchetti C, Diaspro A, Usai C, Bonanno G. 2006. Glia re-sealed particles freshly prepared from adult rat brain are competent for exocytotic release of glutamate. J Neurochem 96:656-668.
57. Suarez I, Bodega G, Fernandez B. 2000. Modulation of glutamate transporters (GLAST, GLT-1 and EAAC1) in the rat cerebellum following portocaval anastomosis. Brain Res 859:293-302. (Pubitemid 30136101)
58. Sun GY, Xu J, Jensen MD, Yu S, Wood WG, Gonzalez FA, Simonyi A, Sun AY, Weisman GA. 2005. Phospholipase A2 in astrocytes: Responses to oxidative stress, inflammation, and G protein-coupled receptor agonists. Mol Neurobiol 31:27-41. (Pubitemid 41271192)
59. Szatkowski M, Barbour B, Attwell D. 1990. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348:443-446. (Pubitemid 120015084)
60. Tofteng F, Larsen FS. 2004. The effect of indomethacin on intracranial pressure, cerebral perfusion and extracellular lactate and glutamate concentrations in patients with fulminant hepatic failure. J Cereb Blood Flow Metab 24:798-804. (Pubitemid 38880225)
61. Vaquero J, Chung C, Blei AT. 2003. Brain edema in acute liver failure. A window to the pathogenesis of hepatic encephalopathy. Ann Hepatol 2:12-22.
62. Xu J, Peng H, Kang N, Zhao Z, Lin JH, Stanton PK, Kang J. 2007. Glutamate-induced exocytosis of glutamate from astrocytes. J Biol Chem 282:24185-24197.
63. Zhang Q, Pangrsic T, Kreft M, Krzan M, Li N, Sul J, Halassa M, Van Bockstaele E, Zorec R, Haydon PG. 2004. Fusion-related release of glutamate from. J Biol Chem 279:12724-12733.
64. Zonta M, Sebelin A, Gobbo S, Fellin T, Pozzan T, Carmignoto G. 2003. Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J Physiol 553:407-414. (Pubitemid 37527544)