Resveratrol Prevents Ammonia Toxicity in Astroglial Cells

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Bobermin, Larissa Daniele ^a   Quincozes Santos, André ^a   Guerra, Maria Cristina ^a   Leite, Marina Concli ^a   Souza, Diogo Onofre ^a   Gonçalves, Carlos Alberto ^a   Gottfried, Carmem ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; ASCORBIC ACID; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMATE AMMONIA LIGASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; N(G) NITROARGININE METHYL ESTER; PROTEIN S100B; REACTIVE OXYGEN METABOLITE; RESVERATROL; TROLOX C; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; IN VITRO STUDY; INTRACELLULAR SIGNALING; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PROTEIN SECRETION; RAT;

AMMONIA; ANIMALS; ASTROCYTES; CELL LINE; CELLS, CULTURED; GLUTAMATE-AMMONIA LIGASE; INTERLEUKIN-1BETA; INTERLEUKIN-6; NF-KAPPA B; NITRIC OXIDE; RATS; STILBENES; TUMOR NECROSIS FACTOR-ALPHA;

VITACEAE;

EID: 84871353606     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052164     Document Type: Article

References (88)

1. Albrecht J, Jones EA, (1999) Hepatic encephalopathy: molecular mechanisms underlying the clinical syndrome. J Neurol Sci 170: 138-146.
2. Buzanska L, Zablocka B, Dybel A, Domanska-Janik K, Albrecht J, (2000) Delayed induction of apoptosis by ammonia in C6 glioma cells. Neurochem Int 37: 287-297.
3. Felipo V, Butterworth RF, (2002) Neurobiology of ammonia. Prog Neurobiol 67: 259-279.
4. Felipo V, Hermenegildo C, Montoliu C, Llansola M, Minana MD, (1998) Neurotoxicity of ammonia and glutamate: molecular mechanisms and prevention. Neurotoxicology 19: 675-681.
5. Monfort P, Kosenko E, Erceg S, Canales JJ, Felipo V, (2002) Molecular mechanism of acute ammonia toxicity: role of NMDA receptors. Neurochem Int 41: 95-102.
6. Monfort P, Munoz MD, ElAyadi A, Kosenko E, Felipo V, (2002) Effects of hyperammonemia and liver failure on glutamatergic neurotransmission. Metab Brain Dis 17: 237-250.
7. Hillmann P, Kose M, Sohl K, Muller CE, (2008) Ammonium-induced calcium mobilization in 1321N1 astrocytoma cells. Toxicol Appl Pharmacol 227: 36-47.
8. Norenberg MD, (2003) Oxidative and nitrosative stress in ammonia neurotoxicity. Hepatology 37: 245-248.
9. Zielinska M, Zablocka B, Dybel A, Albrecht J, (2005) The role of protein kinase C and cyclic AMP in the ammonia-induced shift of the taurine uptake/efflux balance towards efflux in C6 cells. Neurochem Res 30: 349-354.
10. Jayakumar AR, Panickar KS, Murthy Ch R, Norenberg MD, (2006) Oxidative stress and mitogen-activated protein kinase phosphorylation mediate ammonia-induced cell swelling and glutamate uptake inhibition in cultured astrocytes. J Neurosci 26: 4774-4784.
11. Jayakumar AR, Rao KV, Murthy Ch R, Norenberg MD, (2006) Glutamine in the mechanism of ammonia-induced astrocyte swelling. Neurochem Int 48: 623-628.
12. Haussinger D, Gorg B, (2010) Interaction of oxidative stress, astrocyte swelling and cerebral ammonia toxicity. Curr Opin Clin Nutr Metab Care 13: 87-92.
13. Norenberg MD, Rama Rao KV, Jayakumar AR, (2009) Signaling factors in the mechanism of ammonia neurotoxicity. Metab Brain Dis 24: 103-117.
14. Rothermundt M, Peters M, Prehn JH, Arolt V, (2003) S100B in brain damage and neurodegeneration. Microsc Res Tech 60: 614-632.
15. Schroeter ML, Steiner J, Mueller K, (2011) Glial pathology is modified by age in mood disorders-a systematic meta-analysis of serum S100B in vivo studies. J Affect Disord 134: 32-38.
16. Leite MC, Brolese G, de Almeida LM, Pinero CC, Gottfried C, et al. (2006) Ammonia-induced alteration in S100B secretion in astrocytes is not reverted by creatine addition. Brain Res Bull 70: 179-185.
17. He F, Sun YE, (2007) Glial cells more than support cells? Int J Biochem Cell Biol 39: 661-665.
18. Markiewicz I, Lukomska B, (2006) The role of astrocytes in the physiology and pathology of the central nervous system. Acta Neurobiol Exp (Wars) 66: 343-358.
19. Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, et al. (2004) A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 47: 263-274.
20. Belanger M, Allaman I, Magistretti PJ, (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14: 724-738.
21. McKenna MC, (2007) The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J Neurosci Res 85: 3347-3358.
22. Mates JM, Perez-Gomez C, Nunez de Castro I, Asenjo M, Marquez J, (2002) Glutamine and its relationship with intracellular redox status, oxidative stress and cell proliferation/death. Int J Biochem Cell Biol 34: 439-458.
23. Lemberg A, Fernandez MA, (2009) Hepatic encephalopathy, ammonia, glutamate, glutamine and oxidative stress. Ann Hepatol 8: 95-102.
24. Benda P, Lightbody J, Sato G, Levine L, Sweet W, (1968) Differentiated rat glial cell strain in tissue culture. Science 161: 370-371.
25. Funchal C, Latini A, Jacques-Silva MC, Dos Santos AQ, Buzin L, et al. (2006) Morphological alterations and induction of oxidative stress in glial cells caused by the branched-chain alpha-keto acids accumulating in maple syrup urine disease. Neurochem Int 49: 640-650.
26. Quincozes-Santos A, Andreazza AC, Nardin P, Funchal C, Goncalves CA, et al. (2007) Resveratrol attenuates oxidative-induced DNA damage in C6 Glioma cells. Neurotoxicology 28: 886-891.
27. dos Santos AQ, Nardin P, Funchal C, de Almeida LM, Jacques-Silva MC, et al. (2006) Resveratrol increases glutamate uptake and glutamine synthetase activity in C6 glioma cells. Arch Biochem Biophys 453: 161-167.
28. Quincozes-Santos A, Andreazza AC, Goncalves CA, Gottfried C, (2010) Actions of redox-active compound resveratrol under hydrogen peroxide insult in C6 astroglial cells. Toxicol In Vitro 24: 916-920.
29. Steiner J, Schroeter ML, Schiltz K, Bernstein HG, Muller UJ, et al. (2010) Haloperidol and clozapine decrease S100B release from glial cells. Neuroscience 167: 1025-1031.
30. Tanabe K, Kozawa O, Iida H, (2011) Midazolam suppresses interleukin-1beta-induced interleukin-6 release from rat glial cells. J Neuroinflammation 8: 68.
31. Gutteridge JM, Halliwell B, (2010) Antioxidants: Molecules, medicines, and myths. Biochem Biophys Res Commun 393: 561-564.
32. Baur JA, Sinclair DA, (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5: 493-506.
33. Delmas D, Jannin B, Latruffe N, (2005) Resveratrol: preventing properties against vascular alterations and ageing. Mol Nutr Food Res 49: 377-395.
34. Vang O, Ahmad N, Baile CA, Baur JA, Brown K, et al. (2011) What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS One 6: e19881.
35. de Almeida LM, Leite MC, Thomazi AP, Battu C, Nardin P, et al. (2008) Resveratrol protects against oxidative injury induced by H2O2 in acute hippocampal slice preparations from Wistar rats. Arch Biochem Biophys 480: 27-32.
36. de Almeida LM, Pineiro CC, Leite MC, Brolese G, Tramontina F, et al. (2007) Resveratrol increases glutamate uptake, glutathione content, and S100B secretion in cortical astrocyte cultures. Cell Mol Neurobiol 27: 661-668.
37. Vieira de Almeida LM, Pineiro CC, Leite MC, Brolese G, Leal RB, et al. (2008) Protective effects of resveratrol on hydrogen peroxide induced toxicity in primary cortical astrocyte cultures. Neurochem Res 33: 8-15.
38. Quincozes-Santos A, Nardin P, de Souza DF, Gelain DP, Moreira JC, et al. (2009) The janus face of resveratrol in astroglial cells. Neurotox Res 16: 30-41.
39. Quincozes-Santos A, Gottfried C, (2011) Resveratrol modulates astroglial functions: neuroprotective hypothesis. Ann N Y Acad Sci 1215: 72-78.
40. Tiwari V, Chopra K, (2011) Resveratrol prevents alcohol-induced cognitive deficits and brain damage by blocking inflammatory signaling and cell death cascade in neonatal rat brain. J Neurochem 117: 678-690.
41. Lee EO, Park HJ, Kang JL, Kim HS, Chong YH, (2010) Resveratrol reduces glutamate-mediated monocyte chemotactic protein-1 expression via inhibition of extracellular signal-regulated kinase 1/2 pathway in rat hippocampal slice cultures. J Neurochem 112: 1477-1487.
42. Fukui M, Choi HJ, Zhu BT, (2010) Mechanism for the protective effect of resveratrol against oxidative stress-induced neuronal death. Free Radic Biol Med 49: 800-813.
43. Kwon KJ, Kim JN, Kim MK, Lee J, Ignarro LJ, et al. (2011) Melatonin synergistically increases resveratrol-induced heme oxygenase-1 expression through the inhibition of ubiquitin-dependent proteasome pathway: a possible role in neuroprotection. J Pineal Res 50: 110-123.
44. Leite MC, Galland F, de Souza DF, Guerra MC, Bobermin L, et al. (2009) Gap junction inhibitors modulate S100B secretion in astrocyte cultures and acute hippocampal slices. J Neurosci Res 87: 2439-2446.
45. Hu J, Castets F, Guevara JL, Van Eldik LJ, (1996) S100 beta stimulates inducible nitric oxide synthase activity and mRNA levels in rat cortical astrocytes. J Biol Chem 271: 2543-2547.
46. Leite MC, Galland F, Brolese G, Guerra MC, Bortolotto JW, et al. (2008) A simple, sensitive and widely applicable ELISA for S100B: Methodological features of the measurement of this glial protein. J Neurosci Methods 169: 93-99.
47. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
48. Nardin P, Tramontina F, Leite MC, Tramontina AC, Quincozes-Santos A, et al. (2007) S100B content and secretion decrease in astrocytes cultured in high-glucose medium. Neurochem Int 50: 774-782.
49. King CC, Sastri M, Chang P, Pennypacker J, Taylor SS, (2011) The rate of NF-kappaB nuclear translocation is regulated by PKA and A kinase interacting protein 1. PLoS One 6: e18713.
50. Liskowsky DR, Norenberg LO, Norenberg MD, (1986) Effect of ammonia on cyclic AMP production in primary astrocyte cultures. Brain Res 386: 386-388.
51. Svoboda N, Zierler S, Kerschbaum HH, (2007) cAMP mediates ammonia-induced programmed cell death in the microglial cell line BV-2. Eur J Neurosci 25: 2285-2295.
52. Fernandes A, Falcao AS, Silva RF, Brito MA, Brites D, (2007) MAPKs are key players in mediating cytokine release and cell death induced by unconjugated bilirubin in cultured rat cortical astrocytes. Eur J Neurosci 25: 1058-1068.
53. Kosenko E, Kaminsky Y, Kaminsky A, Valencia M, Lee L, et al. (1997) Superoxide production and antioxidant enzymes in ammonia intoxication in rats. Free Radic Res 27: 637-644.
54. Kosenko E, Felipo V, Montoliu C, Grisolia S, Kaminsky Y, (1997) Effects of acute hyperammonemia in vivo on oxidative metabolism in nonsynaptic rat brain mitochondria. Metab Brain Dis 12: 69-82.
55. Haghighat N, McCandless DW, Geraminegad P, (2000) Responses in primary astrocytes and C6-glioma cells to ammonium chloride and dibutyryl cyclic-AMP. Neurochem Res 25: 277-284.
56. Rose C, Felipo V, (2005) Limited capacity for ammonia removal by brain in chronic liver failure: potential role of nitric oxide. Metab Brain Dis 20: 275-283.
57. Westergaard N, Sonnewald U, Schousboe A, (1995) Metabolic trafficking between neurons and astrocytes: the glutamate/glutamine cycle revisited. Dev Neurosci 17: 203-211.
58. Pellerin L, Bonvento G, Chatton JY, Pierre K, Magistretti PJ (2002) Role of neuron-glia interaction in the regulation of brain glucose utilization. Diabetes Nutr Metab 15: 268-273; discussion 273.
59. Bastianetto S, Quirion R, (2010) Heme oxygenase 1: another possible target to explain the neuroprotective action of resveratrol, a multifaceted nutrient-based molecule. Exp Neurol 225: 237-239.
60. Sakata Y, Zhuang H, Kwansa H, Koehler RC, Dore S, (2010) Resveratrol protects against experimental stroke: putative neuroprotective role of heme oxygenase 1. Exp Neurol 224: 325-329.
61. Quincozes-Santos A, Bobermin L, Goncalves C, Gottfried C, Souza D, (2011) Resveratrol modulates astroglial functions. Supplement to GLIA 59(S1): S80.
62. Hertz L, Zielke HR, (2004) Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 27: 735-743.
63. Dringen R, Hirrlinger J, (2003) Glutathione pathways in the brain. Biol Chem 384: 505-516.
64. Allaman I, Belanger M, Magistretti PJ, (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34: 76-87.
65. Escartin C, Won SJ, Malgorn C, Auregan G, Berman AE, et al. (2011) Nuclear factor erythroid 2-related factor 2 facilitates neuronal glutathione synthesis by upregulating neuronal excitatory amino acid transporter 3 expression. J Neurosci 31: 7392-7401.
66. Wiltfang J, Nolte W, Otto M, Wildberg J, Bahn E, et al. (1999) Elevated serum levels of astroglial S100beta in patients with liver cirrhosis indicate early and subclinical portal-systemic encephalopathy. Metab Brain Dis 14: 239-251.
67. Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, et al. (2009) S100B's double life: intracellular regulator and extracellular signal. Biochim Biophys Acta 1793: 1008-1022.
68. Quincozes-Santos A, Rosa RB, Leipnitz G, de Souza DF, Seminotti B, et al. (2010) Induction of S100B secretion in C6 astroglial cells by the major metabolites accumulating in glutaric acidemia type I. Metab Brain Dis. 25: 191-198.
69. Funchal C, Tramontina F, Quincozes dos Santos A, Fraga de Souza D, Goncalves CA, et al. (2007) Effect of the branched-chain alpha-keto acids accumulating in maple syrup urine disease on S100B release from glial cells. J Neurol Sci 260: 87-94.
70. Rose C, Kresse W, Kettenmann H, (2005) Acute insult of ammonia leads to calcium-dependent glutamate release from cultured astrocytes, an effect of pH. J Biol Chem 280: 20937-20944.
71. Davey GE, Murmann P, Heizmann CW, (2001) Intracellular Ca2+ and Zn2+ levels regulate the alternative cell density-dependent secretion of S100B in human glioblastoma cells. J Biol Chem 276: 30819-30826.
72. Goncalves D, Karl J, Leite M, Rotta L, Salbego C, et al. (2002) High glutamate decreases S100B secretion stimulated by serum deprivation in astrocytes. Neuroreport 13: 1533-1535.
73. Tanabe K, Matsushima-Nishiwaki R, Yamaguchi S, Iida H, Dohi S, et al. (2010) Mechanisms of tumor necrosis factor-alpha-induced interleukin-6 synthesis in glioma cells. J Neuroinflammation 7: 16.
74. Santello M, Bezzi P, Volterra A, (2011) TNFalpha controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69: 988-1001.
75. Butterworth RF, (2011) Neuroinflammation in acute liver failure: Mechanisms and novel therapeutic targets. Neurochem Int 59: 830-836.
76. Butterworth RF, (2011) Hepatic encephalopathy: a central neuroinflammatory disorder? Hepatology 53: 1372-1376.
77. Van Eldik LJ, Wainwright MS, (2003) The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci 21: 97-108.
78. Guerra MC, Tortorelli LS, Galland F, Da Re C, Negri E, et al. (2011) Lipopolysaccharide modulates astrocytic S100B secretion: a study in cerebrospinal fluid and astrocyte cultures from rats. J Neuroinflammation 8: 128.
79. Farina C, Aloisi F, Meinl E, (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28: 138-145.
80. Baltimore D, (2011) NF-kappaB is 25. Nat Immunol 12: 683-685.
81. Gerlo S, Kooijman R, Beck IM, Kolmus K, Spooren A, et al. (2011) Cyclic AMP: a selective modulator of NF-kappaB action. Cell Mol Life Sci 68: 3823-3841.
82. Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW (2010) When NRF2 Talks, Who's Listening? Antioxid Redox Signal.
83. Shen HM, Pervaiz S, (2006) TNF receptor superfamily-induced cell death: redox-dependent execution. FASEB J 20: 1589-1598.
84. Hamby ME, Gragnolati AR, Hewett SJ, Hewett JA, (2008) TGF beta 1 and TNF alpha potentiate nitric oxide production in astrocyte cultures by recruiting distinct subpopulations of cells to express NOS-2. Neurochem Int 52: 962-971.
85. Gorg B, Qvartskhava N, Keitel V, Bidmon HJ, Selbach O, et al. (2008) Ammonia induces RNA oxidation in cultured astrocytes and brain in vivo. Hepatology 48: 567-579.
86. Schliess F, Gorg B, Haussinger D, (2009) RNA oxidation and zinc in hepatic encephalopathy and hyperammonemia. Metab Brain Dis 24: 119-134.
87. Csiszar A, (2011) Anti-inflammatory effects of resveratrol: possible role in prevention of age-related cardiovascular disease. Ann N Y Acad Sci 1215: 117-122.
88. Huang TC, Lu KT, Wo YY, Wu YJ, Yang YL, (2011) Resveratrol protects rats from Abeta-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation. PLoS One 6: e29102.