Glutathione production is regulated via distinct pathways in stressed and non-stressed cortical neurons

Brain Research

Volumn 1189, Issue 1, 2008, Pages 12-22

  Burdo, Joseph ^a   Schubert, David ^a   Maher, Pamela ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

c Myc; ERK; Fisetin; Nrf2; Peroxynitrite; Raf1

Indexed keywords

FISETIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; LINSIDOMINE; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PEROXYNITRITE; TRANSCRIPTION FACTOR NRF2; 3 MORPHOLINO SYDNONIMINE; 3-MORPHOLINO-SYDNONIMINE; DRUG DERIVATIVE; FLAVONOID; MOLSIDOMINE; NEUROPROTECTIVE AGENT; NFE2L2 PROTEIN, RAT; NITRIC OXIDE DONOR; NITRO DERIVATIVE; PEROXYNITROUS ACID;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SYNTHESIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; BRAIN CORTEX; CELL CULTURE; CELL SURVIVAL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; GLUTATHIONE; MAP KINASE SIGNALING SYSTEM; MOLSIDOMINE; NEURONS; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; NITRIC OXIDE DONORS; NITRO COMPOUNDS; OXIDATIVE STRESS; PEROXYNITROUS ACID; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 44449133306     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.10.077     Document Type: Article

References (77)

1. Alessi D.R., Cohen P., Dudley D.T., and Saltiel A.R. PD98059 is a specific inhibitor of the mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270 (1995) 27489-27494
2. Andreadi C.K., Howells L.M., Atherfold P.A., and Manson M.M. Involvement of Nrf2, p38, B-Raf, and nuclear factor-kappaB, but not phosphatidylinositol 3-kinase, in induction of hemeoxygenase-1 by dietary polyphenols. Mol. Pharmacol. 69 (2006) 1033-1040
3. Arnold H.K., and Sears R.C. Protein phosphatase 2A regulatory subunit B56alpha associates with c-myc and negatively regulates c-myc accumulation. Mol. Cell. Biol. 26 (2006) 2832-2844
4. Bapat S., Verkleij A., and Post J.A. Peroxynitrite activates mitogen-activated protein kinase (MAPK) via a MEK-independent pathway: role for protein kinase C. FEBS Lett. 499 (2001) 21-26
5. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., and Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 1620-1624
6. Beckman J.S., Ischiropoulos H., Zhu L., van der Woerd M., Smith C., Chen J., Harrison J., Martin J.C., and Tsai M. Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298 (1992) 438-445
7. Benassi B., Fanciulli M., Fiorentino F., Porrello A., Chiorino G., Loda M., Zupi G., and Biroccio A. c-Myc phosphorylation is required for cellular response to oxidative stress. Mol. Cell 21 (2006) 509-519
8. Bolanos J.P., Heales S.J.R., Land J.M., and Clark J.B. Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurones and astrocytes in primary culture. J. Neurochem. 64 (1995) 1965-1972
9. Brito P.M., Mariano A., Almeida L.M., and Dinis T.C.P. Resveratrol affords protection against peroxynitrite-mediated endothelial cell death: a role for intracellular glutathione. Chem. Biol. Interact. 164 (2006) 157-166
10. Chen C., and Kong A.-N.T. Dietary chemopreventive compounds and ARE/EpRE signaling. Free Radic. Biol. Med. 36 (2004) 1505-1516
11. Chen T.J., Jeng J.Y., Lin C.W., Wu C.Y., and Chen Y.C. Quercetin inhibition of ROS-dependent and -independent apoptosis in rat glioma C6 cells. Toxicology 223 (2006) 113-126
12. Chen Y.C., Chow J.M., Lin C.W., Wu C.Y., and Shen S.C. Baicalein inhibition of oxidative stress-induced apoptosis via modulation of ERKs activation and induction of HO-1 gene expression in rat glioma cells C6. Toxicol. Appl. Pharmacol. 216 (2006) 263-273
13. Choi Y.J., Jeong Y.J., Lee Y.J., Kwon H.M., and Kang Y.H. (-) Epigallocatechin gallate and quercetin enhance survival signaling in response to oxidant-induced human endothelial apoptosis. J. Nutr. 135 (2005) 707-713
14. Chong H., Vikis H.G., and Guan K.L. Mechanisms of regulating the Raf kinase family. Cell. Signal. 15 (2003) 463-469
15. Dajas F., Rivera F., Blasina F., Arredondo F., Echeverry C., Lafon L., Morquio A., and Heizen H. Cell culture protection and in vivo neuroprotective capacity of flavonoids. Neurotox. Res. 5 (2003) 425-432
16. de Bernardo S., Canals S., Casarejos M.J., Solano R.M., Menendez J., and Mena M.A. Role of extracellular signal-regulated protein kinase in neuronal cell death induced by glutathione depletion in neuron/glia mesencephalic cultures. J. Neurochem. 91 (2004) 667-682
17. Dickinson D.A., Levonen A.-L., Moellering D.R., Arnold E.K., Zhang H., Darley-Usmar V.M., and Forman H.J. Human glutamate cysteine ligase gene regulation through the electrophile response element. Free Radic. Biol. Med. 37 (2004) 1152-1159
18. Dringen R. Oxidative and antioxidative potential of brain microglial cells. Antioxid. Redox Signal. 7 (2005) 1223-1233
19. El-Remessy A.B., Ali Behzadian M., Abou-Mohamed G., Franklin T., Caldwell R.W., and Caldwell R.B. Experimental diabetes causes a breakdown of the blood-retina barrier by a mechanism involving tyrosine nitration and increases in expression of vascular endothelial growth factor and urokinase plasminogen activator receptor. Am. J. Pathol. 162 (2003) 1995-2004
20. Eliasson M.J.L., Huang Z., Ferrante R.J., Sasamata M., Molliver M.E., Snyder S.H., and Moskowitz M.A. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neuronal damage. J. Neurosci. 19 (1999) 5910-5918
21. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., Van Dyk D.E., Pitts W.J., Earl R.A., Hobbs F., Copeland R.A., Magolda R.L., Scherle P.A., and Trzaskos J.M. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273 (1998) 18623-18632
22. Hanneken A., Lin F.-F., Johnson J., and Maher P. Flavonoids protect human pigmented retinal epithelial cells from oxidative stress-induced death. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3164-3177
23. Hansen M.B., Nielsen S.E., and Berg K. 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
24. Heim K.E., Tagliaferro A.R., and Bobilya D.J. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J. Nutr. Biochem 13 (2002) 572-584
25. Ho H.Y., Wei T.T., Cheng M.L., and Chiu D.T. Green tea polyphenol epigallocatechin-3-gallate protects cells against peroxynitrite-induced cytotoxicity: modulatory effect of cellular G6PD status. J. Agric. Food Chem. 54 (2006) 1638-1645
26. Hoeldtke R.D., Bryner K.D., McNeill D.R., Hobbs G.R., and Baylis C. Peroxynitrite versus nitric oxide in early diabetes. Am. J. Hypertens 16 (2003) 761-766
27. Hou D.-X., Fukuda M., Johnson J.A., Miyamori K., Ushikai M., and Fujii M. Fisetin induces transcription of NADPH:quinone oxidoreductase gene through an antioxidant responsive element-involved activation. Int. J. Oncol. 18 (2001) 1175-1179
28. Iravani M.M., Haddon C.O., Rose S., and Jenner P. 3-Nitrotyrosine-dependent dopaminergic neurotoxicity following direct nigral administration of a peroxynitrite but not a nitric oxide donor. Brain Res. 1067 (2006) 256-262
29. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D., and Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298 (1992) 431-437
30. Ishige K., Schubert D., and Sagara Y. Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic. Biol. Med. 30 (2001) 433-446
31. Ishii N., Patel K.P., Lane P.H., Taylor T., Bian K., Murad F., Pollock J.S., and Carmines P.K. Nitric oxide synthesis and oxidative stress in the renal cortex of rats with diabetes mellitus. J. Am. Soc. Nephrol. 12 (2001) 1630-1639
32. Kensler T.W., Wakabayashi N., and Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 89-116
33. Klejman A., Wegrzynowicz M., Szatmari E.M., Mioduszewska B., Hetman M., and Albrecht J. Mechanisms of ammonia-induced cell death in rat cortical neurons: roles of NMDA receptors and glutathione. Neurochem. Int. 47 (2005) 51-57
34. Klotz L.-O. Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol. Chem. 383 (2002) 443-456
35. Klotz L.-O., and Sies H. Defenses against peroxynitrite: selenocompounds and flavonoids. Toxicol. Lett. 140-141 (2003) 125-132
36. Kuperstein F., and Yavin E. ERK activation and nuclear translocation in amyloid-beta peptide- and iron-stressed neuronal cell cultures. Eur. J. Neurosci. 16 (2002) 44-54
37. Lau F.C., Shukitt-Hale J., and Joseph J. The beneficial effects of fruits polyphenols on brain aging. Neurobiol. Aging 26 (2005) 128-132
38. Levinthal D.J., and DeFranco D.B. Transient phosphatidylinositol 3-kinase inhibition protects immature primary cortical neurons from oxidative toxicity via suppression of extracellular signal-regulated kinase activation. J. Biol. Chem. 279 (2004) 11206-11213
39. Levrand S., Pesse B., Feihl F., Waeber B., Pacher P., Rolli J., Schaller M.-D., and Liaudet L. Peroxynitrite is a potent inhibitor of NF-kB activation triggered by inflammatory stimuli in cardiac and endothelial cell lines. J. Biol. Chem. 280 (2005) 34878-34887
40. Li Y., Maher P., and Schubert D. A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion. Neuron 19 (1997) 453-463
41. Lim S.Y., Jang J.H., Na H.K., Lu S.C., Rahman I., and Surh Y.J. 15-Deoxy-delta 12,14-prostaglandin J(2) protects against nitrosative PC12 cell death through up-regulation of intracellular glutathione synthesis. J. Biol. Chem. 279 (2004) 46263-46270
42. Lin H.C., Cheng T.H., Chen Y.C., and Juan S.H. Mechanism of heme oxygenase-1 gene induction by quercetin in rat aortic smooth muscle cells. Pharmacology 71 (2004) 107-112
43. Maher P. A comparison of the neurotrophic activities of the flavonoid fisetin and some of its derivatives. Free Radic. Res. 40 (2006) 1105-1111
44. Maher P., and Hanneken A. Flavonoids protect retinal ganglion cells from oxidative stress-induced death. Invest. Ophthalmol. Vis. Sci. 46 (2005) 4796-4803
45. Maher P., Akaishi T., and Abe K. The flavonoid fisetin promotes ERK-dependent long-term potentiation and enhances memory. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 16568-16573
46. Maher P., Salgado K.F., Zivin J.A., and Lapchak P.A. A novel approach to screening for new neuroprotective compounds for the treatment of stroke. Brain Res. 1173 (2007) 117-125
47. Manabe Y., Wang J.M., Murakami T., Warita H., Hayashi T., Shoji M., and Abe K. Expressions of nitrotyrosine and TUNEL immunoreactivities in cultured rat spinal cord neurons after exposure to glutamate, nitric oxide, or peroxynitrite. J. Neurosci. Res. 65 (2001) 371-377
48. Middleton E., Kandaswami C., and Theoharides T.C. The effects of flavonoids on mammalian cells: implications for inflammation, heart disease and cancer. Pharmacol. Rev. 52 (2000) 673-751
49. Misko T.P., Highkin M.K., Veenhuizen A.W., Manning P.T., Stern M.K., Currie M.G., and Salvemini D. Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. J. Biol. Chem. 273 (1998) 15646-15653
50. Myhrstad M.C.W., Carlsen H., Nordstrom O., Blomhoff R., and Moskaug J.O. Flavonoids increase the intracellular glutathione level by transactivation of the γ-glutamylcysteine synthetase catalytical subunit promoter. Free Radic. Biol. Med. 32 (2002) 386-393
51. Nakamura K., Bindokas V.P., Kowlessur D., Elas M., Milstein S., Marks J.D., Halpern H.J., and Kang U.J. Tetrahydrobiopterin scavenges superoxide in dopaminergic neurons. J. Biol. Chem. 276 (2001) 34402-34407
52. Naoi M., Maruyama W., Shamoto-Nagai M., Yi H., Akao Y., and Tanaka M. Oxidative stress in mitochondria. Mol. Neurobiol. 31 (2005) 81-93
53. Nguyen T., Sherratt P.J., and Pickett C.B. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 233-260
54. Nowak P., Olas B., Bald E., Glowacki R., and Wachowicz B. Peroxynitrite-induced changes of thiol groups in human blood platelets. Platelets 14 (2003) 375-379
55. Oh-hashi K., Maruyama W., Yi H., Takahashi T., Naoi M., and Isobe K.-I. Mitogen-activated protein kinase pathway mediates peroxynitrite-induced apoptosis in human dopaminergic neuroblastoma SH-SY5Y cells. Biochem. Biophys. Res. Commun. 263 (1999) 504-509
56. Pannala A., Rice-Evans C.A., Halliwell B., and Singh S. Inhibition of peroxynitrite-mediated tyrosine nitration by catechin polyphenols. Biochem. Biophys. Res. Commun. 232 (1997) 164-168
57. Radi R., Beckman J.S., Bush K.M., and Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266 (1991) 4244-42450
58. Rahman I., Biswas S.K., and Kirkham P.A. Regulation of inflammation and redox signaling by dietary polyphenols. Biochem. Pharmacol. 72 (2006) 1439-1452
59. Ramassamy C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur. J. Pharmacol. 545 (2006) 51-64
60. Sagara Y., Vahnnasy J., and Maher P. Induction of PC12 cell differentiation by flavonoids is dependent upon extracellular signal-regulated kinase activation. J. Neurochem. 90 (2004) 1144-1155
61. Schieke S.M., Briviba K., Klotz L.-O., and Sies H. Activation pattern of mitogen-activated protein kinases elicited by peroxynitrite: attentuation by selenite supplementation. FEBS Lett. 448 (1999) 301-303
62. Schreiber E., Matthias P., Muller M.M., and Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17 (1989) 6419
63. Singh I.N., Sullivan P.G., Deng Y., Mbye L.H., and Hall E.D. Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy. J. Cereb. Blood Flow Metab. 26 (2006) 1407-1418
64. Sun X., Erb H., and Murphy T.H. Coordinate regulation of glutathione metabolism in actrocytes by Nrf2. Biochem. Biophys. Res. Commun. 326 (2005) 371-377
65. Thuraisingham R.C., Nott C.A., Dodd S.M., and Yaqoob M.M. Increased nitrotyrosine staining in kidneys from patients with diabetic nephropathy. Kidney Int. 57 (2000) 1968-1972
66. Torreilles F., Salman-Tabcheh S., Guerin M., and Torreilles J. Neurodegenerative disorders: the role of peroxynitrite. Brain Res. Brain Res. Rev. 30 (1999) 153-163
67. Valerio L.G., Kepa J.K., Pickwell G.V., and Quattrochi L.C. Induction of human NAD(P)H:quinone oxidoreductase (NQO1) gene expression by the flavonol quercetin. Toxicol. Lett. 119 (2001) 49-57
68. van Acker F.A., Schouten O., Haenen G.R., van der Vijgh W.J., and Bast A. Flavonoids can replace alpha-tocopherol as an antioxidant. FEBS Lett. 473 (2000) 145-148
69. White A.R., and Cappai R. Neurotoxicity from glutathione depletion is dependent on extracellular trace copper. J. Neurosci. Res. 71 (2003) 889-897
70. Wild A.C., and Mulcahy R.T. Regulation of γ-glutamylcysteine synthetase subunit gene expression: insights into transcriptional control of antioxidant defenses. Free Radic. Res. 32 (2000) 281-301
71. Wu Z., Wu L., Tashiro S., Onodera S., and Ikejima T. Phosphorylated extracellular signal-regulated kinase up-regulated p53 expression in shikonon-induced HeLa cell apoptosis. Chin. Med. J. (Engl.) 118 (2005) 671-677
72. Wu C.C., Hsu M.C., Hsieh C.W., Lin J.B., Lai P.H., and Wung B.S. Upregulation of heme oxygenase-1 by epigallocatechin-3-gallter via the phosphatidylinositol 3-kinase/Akt and ERK pathways. Life Sci. 78 (2006) 2889-2897
73. Zhang D.D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab. Rev. 38 (2006) 769-789
74. Zhang Y., and Rosenberg P.A. Caspase-1 and poly (ADP-ribose) polymerase inhibitors may protect against peroxynitrite-induced neurotoxicity independent of their enzyme inhibitor activity. Eur. J. Neurosci. 20 (2004) 1727-1736
75. Zhang P., Wang Y.-Z., Kagan E., and Bonner J.C. Peroxynitrite targets the epidermal growth factor receptor, Raf-1, and MEK independently to activate MAPK. J. Biol. Chem. 275 (2000) 22479-22486
76. Zhang Y., Wang H., Li J., Jimenez D.A., Levitan E.S., Aizenman E., and Rosenberg P.A. Peroxynitrite-induced neuronal apoptosis is mediated by intracellular zinc release and 12-lipoxygenase activation. J. Neurosci. 24 (2004) 10616-10627
77. Zouki C., Jozsef L., Ouellet S., Paquette Y., and Filep J.G. Peroxynitrite mediates cytokine-induced IL-8 gene expression and production by human leukocytes. J. Leukoc. Biol. 69 (2001) 815-824