Guanosine protects C6 astroglial cells against azide-induced oxidative damage: A putative role of heme oxygenase 1

Journal of Neurochemistry

Volumn 130, Issue 1, 2014, Pages 61-74

  Quincozes Santos, André ^a   Bobermin, Larissa Daniele ^a   Souza, Débora Guerini ^a   Bellaver, Bruna ^a   Gonçalves, Carlos Alberto ^a   Souza, Diogo Onofre ^a  

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

Author keywords

azide; C6 astroglial cells; glioprotective molecule; guanosine; heme oxygenase 1

Indexed keywords

AZIDE; CATALASE; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GUANOSINE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; HEME OXYGENASE; HMOX1 PROTEIN, RAT; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; CELL ACTIVITY; CELL LEVEL; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; MALE; MITOCHONDRION; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL LINE; DRUG EFFECTS; ENZYMOLOGY; PATHOLOGY; PHYSIOLOGY; TOXICITY; WISTAR RAT;

ANIMALS; ASTROCYTES; AZIDES; CELL LINE; CELLS, CULTURED; GUANOSINE; HEME OXYGENASE (DECYCLIZING); MALE; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 84902991801     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12694     Document Type: Article

References (106)

1. Abid M. R., Spokes K. C., Shih S. C., and, Aird W. C., (2007) NADPH oxidase activity selectively modulates vascular endothelial growth factor signaling pathways. J. Biol. Chem. 282, 35373-35385. (Pubitemid 350232487)
2. Aebi H., (1984) Catalase in vitro. Methods Enzymol. 105, 121-126.
3. Albrecht P., Henke N., Tien M. L., Issberner A., Bouchachia I., Maher P., Lewerenz J., and, Methner A., (2013) Extracellular cyclic GMP and its derivatives GMP and guanosine protect from oxidative glutamate toxicity. Neurochem. Int. 62, 610-619.
4. Anderson C. M., and, Swanson R. A., (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32, 1-14.
5. Arredondo F., Echeverry C., Abin-Carriquiry J. A., Blasina F., Antunez K., Jones D. P., Go Y. M., Liang Y. L., and, Dajas F., (2010) After cellular internalization, quercetin causes Nrf2 nuclear translocation, increases glutathione levels, and prevents neuronal death against an oxidative insult. Free Radic. Biol. Med. 49, 738-747.
6. Banerjee R., Vitvitsky V., and, Garg S. K., (2008) The undertow of sulfur metabolism on glutamatergic neurotransmission. Trends Biochem. Sci. 33, 413-419.
7. Bastianetto S., and, 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.
8. Bau C., Middlemiss P. J., Hindley S., Jiang S., Ciccarelli R., Caciagli F., Diiorio P., Werstiuk E. S., and, Rathbone M. P., (2005) Guanosine stimulates neurite outgrowth in PC12 cells via activation of heme oxygenase and cyclic GMP. Purinergic Signal. 1, 161-172. (Pubitemid 40466901)
9. Belanger M., Allaman I., and, Magistretti P. J., (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14, 724-738.
10. Bellaver B., de Souza D. G., Souza D. O., and, Quincozes-Santos A., (2014) Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicol. In Vitro, 28, 479-484.
11. Bennett M. C., Mlady G. W., Fleshner M., and, Rose G. M., (1996a) Synergy between chronic corticosterone and sodium azide treatments in producing a spatial learning deficit and inhibiting cytochrome oxidase activity. Proc. Natl Acad. Sci. USA 93, 1330-1334. (Pubitemid 26052889)
12. Bennett M. C., Mlady G. W., Kwon Y. H., and, Rose G. M., (1996b) Chronic in vivo sodium azide infusion induces selective and stable inhibition of cytochrome c oxidase. J. Neurochem. 66, 2606-2611. (Pubitemid 26159099)
13. Bianchi M. G., Rotoli B. M., Dall'Asta V., Gazzola G. C., Gatti R., and, Bussolati O., (2006) PKC-dependent stimulation of EAAT3 glutamate transporter does not require the integrity of actin cytoskeleton. Neurochem. Int. 48, 341-349. (Pubitemid 43327273)
14. Bidmon H. J., Gorg B., Palomero-Gallagher N., Schleicher A., Haussinger D., Speckmann E. J., and, Zilles K., (2008) Glutamine synthetase becomes nitrated and its activity is reduced during repetitive seizure activity in the pentylentetrazole model of epilepsy. Epilepsia 49, 1733-1748.
15. Bobermin L. D., Quincozes-Santos A., Guerra M. C., Leite M. C., Souza D. O., Goncalves C. A., and, Gottfried C., (2012) Resveratrol prevents ammonia toxicity in astroglial cells. PLoS ONE 7, e52164.
16. Bowler M. W., Montgomery M. G., Leslie A. G., and, Walker J. E., (2006) How azide inhibits ATP hydrolysis by the F-ATPases. Proc. Natl Acad. Sci. USA 103, 8646-8649. (Pubitemid 43878074)
17. Bramanti V., Bronzi D., Tomassoni D., Costa A., Raciti G., Avitabile M., Amenta F., and, Avola R., (2008) Growth factors and steroid mediated regulation of cytoskeletal protein expression in serum-deprived primary astrocyte cultures. Neurochem. Res. 33, 2593-2600.
18. Bramanti V., Tomassoni D., Grasso S., et al,. (2012) Cholinergic precursors modulate the expression of heme oxigenase-1, p21 during astroglial cell proliferation and differentiation in culture. Neurochem. Res. 37, 2795-2804.
19. Brennan A. M., Suh S. W., Won S. J., Narasimhan P., Kauppinen T. M., Lee H., Edling Y., Chan P. H., and, Swanson R. A., (2009) NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12, 857-863.
20. Browne R. W., and, Armstrong D., (1998) Reduced glutathione and glutathione disulfide. Methods Mol. Biol. 108, 347-352.
21. Burnstock G., (2009) Purines and sensory nerves. Handb. Exp. Pharmacol., 194, 333-392.
22. Calabrese V., Mancuso C., Calvani M., Rizzarelli E., Butterfield D. A., and, Stella A. M., (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 8, 766-775. (Pubitemid 47462116)
23. Calabrese V., Cornelius C., Mancuso C., et al,. (2008) Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem. Res. 33, 2444-2471.
24. Calkins M. J., Johnson D. A., Townsend J. A., et al,. (2009) The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid. Redox Signal. 11, 497-508.
25. Chang R., Algird A., Bau C., Rathbone M. P., and, Jiang S., (2008) Neuroprotective effects of guanosine on stroke models in vitro and in vivo. Neurosci. Lett. 431, 101-105.
26. Ciccarelli R., Di Iorio P., Giuliani P., D'Alimonte I., Ballerini P., Caciagli F., and, Rathbone M. P., (1999) Rat cultured astrocytes release guanine-based purines in basal conditions and after hypoxia/hypoglycemia. Glia 25, 93-98. (Pubitemid 28554059)
27. Ciccarelli R., Ballerini P., Sabatino G., Rathbone M. P., D'Onofrio M., Caciagli F., and, Di Iorio P., (2001) Involvement of astrocytes in purine-mediated reparative processes in the brain. Int. J. Dev. Neurosci. 19, 395-414. (Pubitemid 32500336)
28. Connell B. J., Di Iorio P., Sayeed I., et al,. (2013) Guanosine protects against reperfusion injury in rat brains after ischemic stroke. J. Neurosci. Res. 91, 262-272.
29. Coulter D. A., and, Eid T., (2012) Astrocytic regulation of glutamate homeostasis in epilepsy. Glia 60, 1215-1226.
30. Coyle J. T., and, Puttfarcken P., (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695. (Pubitemid 23350687)
31. Dal-Cim T., Martins W. C., Santos A. R., and, Tasca C. I., (2011) Guanosine is neuroprotective against oxygen/glucose deprivation in hippocampal slices via large conductance Ca(2)+-activated K+ channels, phosphatidilinositol- 3 kinase/protein kinase B pathway activation and glutamate uptake. Neuroscience 183, 212-220.
32. Dal-Cim T., Molz S., Egea J., et al,. (2012) Guanosine protects human neuroblastoma SH-SY5Y cells against mitochondrial oxidative stress by inducing heme oxigenase-1 via PI3K/Akt/GSK-3beta pathway. Neurochem. Int. 61, 397-404.
33. Dal-Cim T., Ludka F. K., Martins W. C., Reginato C., Parada E., Egea J., Lopez M. G., and, Tasca C. I., (2013) Guanosine controls inflammatory pathways to afford neuroprotection of hippocampal slices under oxygen and glucose deprivation conditions. J. Neurochem. 126, 437-450.
34. D'Alimonte I., Flati V., D'Auro M., et al,. (2007) Guanosine inhibits CD40 receptor expression and function induced by cytokines and beta amyloid in mouse microglia cells. J. Immunol. 178, 720-731. (Pubitemid 46095144)
35. Danbolt N. C., (2001) Glutamate uptake. Prog. Neurobiol. 65, 1-105. (Pubitemid 32479155)
36. Davis K. E., Straff D. J., Weinstein E. A., Bannerman P. G., Correale D. M., Rothstein J. D., and, Robinson M. B., (1998) Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of Glu transporter in C6 glioma. J. Neurosci. 18, 2475-2485. (Pubitemid 28141796)
37. Desjardins P., Rao K. V., Michalak A., Rose C., and, Butterworth R. F., (1999) Effect of portacaval anastomosis on glutamine synthetase protein and gene expression in brain, liver and skeletal muscle. Metab. Brain Dis. 14, 273-280. (Pubitemid 30337701)
38. Dore S., (2005) Unique properties of polyphenol stilbenes in the brain: more than direct antioxidant actions; gene/protein regulatory activity. Neurosignals 14, 61-70. (Pubitemid 40868984)
39. Droge W., (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95. (Pubitemid 34654215)
40. Escartin C., Won S. J., Malgorn C., 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.
41. Fukui M., Choi H. J., and, Zhu B. T., (2010) Mechanism for the protective effect of resveratrol against oxidative stress-induced neuronal death. Free Radic. Biol. Med. 49, 800-813.
42. Ganzella M., de Oliveira E. D., Comassetto D. D., et al,. (2012) Effects of chronic guanosine treatment on hippocampal damage and cognitive impairment of rats submitted to chronic cerebral hypoperfusion. Neurol. Sci. 33, 985-997.
43. Gloire G., Legrand-Poels S., and, Piette J., (2006) NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 72, 1493-1505. (Pubitemid 44666727)
44. Gutteridge J. M., and, Halliwell B., (2000) Free radicals and antioxidants in the year 2000. A historical look to the future. Ann. N. Y. Acad. Sci. 899, 136-147. (Pubitemid 30352782)
45. Halliwell B., (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18, 685-716. (Pubitemid 32948277)
46. Halliwell B., (2006) Oxidative stress and neurodegeneration: where are we now? J. Neurochem. 97, 1634-1658. (Pubitemid 43873658)
47. Halliwell B., (2007) Biochemistry of oxidative stress. Biochem. Soc. Trans. 35, 1147-1150.
48. Hamby M. E., Gragnolati A. R., Hewett S. J., and, Hewett J. A., (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. (Pubitemid 351418053)
49. Hertz L., and, Zielke H. R., (2004) Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci. 27, 735-743. (Pubitemid 39488077)
50. Huang T. C., Lu K. T., Wo Y. Y., Wu Y. J., and, Yang Y. L., (2011) Resveratrol protects rats from Abeta-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation. PLoS ONE 6, e29102.
51. Kleinkauf-Rocha J., Bobermin L. D., Machado Pde M., Goncalves C. A., Gottfried C., and, Quincozes-Santos A., (2013) Lipoic acid increases glutamate uptake, glutamine synthetase activity and glutathione content in C6 astrocyte cell line. Int. J. Dev. Neurosci. 31, 165-170.
52. Krizman-Genda E., Gonzalez M. I., Zelenaia O., and, Robinson M. B., (2005) Evidence that Akt mediates platelet-derived growth factor-dependent increases in activity and surface expression of the neuronal glutamate transporter, EAAC1. Neuropharmacology 49, 872-882. (Pubitemid 41483893)
53. Lalo U., Pankratov Y., Kirchhoff F., North R. A., and, Verkhratsky A., (2006) NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J. Neurosci. 26, 2673-2683. (Pubitemid 43357850)
54. Lara D. R., Schmidt A. P., Frizzo M. E., Burgos J. S., Ramirez G., and, Souza D. O., (2001) Effect of orally administered guanosine on seizures and death induced by glutamatergic agents. Brain Res. 912, 176-180. (Pubitemid 32800672)
55. Leary S. C., Hill B. C., Lyons C. N., Carlson C. G., Michaud D., Kraft C. S., Ko K., Glerum D. M., and, Moyes C. D., (2002) Chronic treatment with azide in situ leads to an irreversible loss of cytochrome c oxidase activity via holoenzyme dissociation. J. Biol. Chem. 277, 11321-11328. (Pubitemid 34952897)
56. Lee M., Cho T., Jantaratnotai N., Wang Y. T., McGeer E., and, McGeer P. L., (2010) Depletion of GSH in glial cells induces neurotoxicity: relevance to aging and degenerative neurological diseases. FASEB J. 24, 2533-2545.
57. Lewerenz J., Klein M., and, Methner A., (2006) Cooperative action of glutamate transporters and cystine/glutamate antiporter system Xc- protects from oxidative glutamate toxicity. J. Neurochem. 98, 916-925. (Pubitemid 44051291)
58. Lowry O. H., Rosebrough N. J., Farr A. L., and, Randall R. J., (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
59. Maragakis N. J., and, Rothstein J. D., (2006) Mechanisms of Disease: astrocytes in neurodegenerative disease. Nat. Clin. Pract. Neurol. 2, 679-689. (Pubitemid 44782682)
60. Mates J. M., Perez-Gomez C., Nunez de Castro I., Asenjo M., and, 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. (Pubitemid 34242758)
61. McKenna M. C., (2007) The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J. Neurosci. Res. 85, 3347-3358. (Pubitemid 350058523)
62. Moncada S., and, Bolanos J. P., (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J. Neurochem. 97, 1676-1689. (Pubitemid 43873660)
63. Moretto M. B., Arteni N. S., Lavinsky D., Netto C. A., Rocha J. B., Souza D. O., and, Wofchuk S., (2005) Hypoxic-ischemic insult decreases glutamate uptake by hippocampal slices from neonatal rats: prevention by guanosine. Exp. Neurol. 195, 400-406. (Pubitemid 41297791)
64. Moretto M. B., Boff B., Lavinsky D., Netto C. A., Rocha J. B., Souza D. O., and, Wofchuk S. T., (2009) Importance of schedule of administration in the therapeutic efficacy of guanosine: early intervention after injury enhances glutamate uptake in model of hypoxia-ischemia. J. Mol. Neurosci. 38, 216-219.
65. Nedergaard M., Ransom B., and, Goldman S. A., (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26, 523-530. (Pubitemid 37176906)
66. Ogura H., Evans J. P., Peng D., Satterlee J. D., Ortiz de Montellano P. R., and, La Mar G. N., (2009) The orbital ground state of the azide-substrate complex of human heme oxygenase is an indicator of distal H-bonding: implications for the enzyme mechanism. Biochemistry 48, 3127-3137.
67. Oleskovicz S. P., Martins W. C., Leal R. B., and, Tasca C. I., (2008) Mechanism of guanosine-induced neuroprotection in rat hippocampal slices submitted to oxygen-glucose deprivation. Neurochem. Int. 52, 411-418.
68. Parpura V., Heneka M. T., Montana V., et al,. (2012) Glial cells in (patho)physiology. J. Neurochem. 121, 4-27.
69. Pettifer K. M., Kleywegt S., Bau C. J., Ramsbottom J. D., Vertes E., Ciccarelli R., Caciagli F., Werstiuk E. S., and, Rathbone M. P., (2004) Guanosine protects SH-SY5Y cells against beta-amyloid-induced apoptosis. NeuroReport 15, 833-836. (Pubitemid 38453468)
70. Quincozes-Santos A., and, Gottfried C., (2011) Resveratrol modulates astroglial functions: neuroprotective hypothesis. Ann. N. Y. Acad. Sci. 1215, 72-78.
71. Quincozes-Santos A., Nardin P., de Souza D. F., Gelain D. P., Moreira J. C., Latini A., Goncalves C. A., and, Gottfried C., (2009) The janus face of resveratrol in astroglial cells. Neurotox. Res. 16, 30-41.
72. Quincozes-Santos A., Bobermin L. D., de Souza D. G., Bellaver B., Goncalves C. A., and, Souza D. O., (2013a) Gliopreventive effects of guanosine against glucose deprivation in vitro. Purinergic Signal. 9, 643-654.
73. Quincozes-Santos A., Bobermin L. D., Latini A., Wajner M., Souza D. O., Goncalves C. A., and, Gottfried C., (2013b) Resveratrol protects C6 astrocyte cell line against hydrogen peroxide-induced oxidative stress through heme oxygenase 1. PLoS ONE 8, e64372.
74. Ransom B. R., and, Ransom C. B., (2012) Astrocytes: multitalented stars of the central nervous system. Methods Mol. Biol. 814, 3-7.
75. Rathbone M. P., Middlemiss P. J., Gysbers J. W., Andrew C., Herman M. A., Reed J. K., Ciccarelli R., Di Iorio P., and, Caciagli F., (1999) Trophic effects of purines in neurons and glial cells. Prog. Neurobiol. 59, 663-690. (Pubitemid 29457587)
76. Rathbone M. P., Saleh T. M., Connell B. J., Chang R., Su C., Worley B., Kim M., and, Jiang S., (2011) Systemic administration of guanosine promotes functional and histological improvement following an ischemic stroke in rats. Brain Res. 1407, 79-89.
77. Reers M., Smiley S. T., Mottola-Hartshorn C., Chen A., Lin M., and, Chen L. B., (1995) Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260, 406-417.
78. Reyes R. C., Brennan A. M., Shen Y., Baldwin Y., and, Swanson R. A., (2012) Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes. J. Neurosci. 32, 12973-12978.
79. Rogawski M. A., (2013) AMPA receptors as a molecular target in epilepsy therapy. Acta Neurol. Scand. Suppl., 197, 9-18.
80. Rousset F., Nguyen M. V., Grange L., Morel F., and, Lardy B., (2013) Heme oxygenase-1 regulates matrix metalloproteinase MMP-1 secretion and chondrocyte cell death via Nox4 NADPH oxidase activity in chondrocytes. PLoS ONE 8, e66478.
81. Rowley S., and, Patel M., (2013) Mitochondrial involvement and oxidative stress in temporal lobe epilepsy. Free Radic. Biol. Med. 62, 121-131.
82. Russo I., Bonini D., Via L. L., Barlati S., and, Barbon A., (2013) AMPA receptor properties are modulated in the early stages following pilocarpine-induced status epilepticus. Neuromolecular Med. 15, 324-338.
83. Sakata Y., Zhuang H., Kwansa H., Koehler R. C., and, Dore S., (2010) Resveratrol protects against experimental stroke: putative neuroprotective role of heme oxygenase 1. Exp. Neurol. 224, 325-329.
84. dos Santos A. Q., Nardin P., Funchal C., de Almeida L. M., Jacques-Silva M. C., Wofchuk S. T., Goncalves C. A., and, Gottfried C., (2006) Resveratrol increases glutamate uptake and glutamine synthetase activity in C6 glioma cells. Arch. Biochem. Biophys. 453, 161-167. (Pubitemid 44344218)
85. Scapagnini G., Butterfield D. A., Colombrita C., Sultana R., Pascale A., and, Calabrese V., (2004) Ethyl ferulate, a lipophilic polyphenol, induces HO-1 and protects rat neurons against oxidative stress. Antioxid. Redox Signal. 6, 811-818. (Pubitemid 39237933)
86. Schmidt A. P., Lara D. R., de Faria Maraschin J., da Silveira Perla A., and, Onofre Souza D., (2000) Guanosine and GMP prevent seizures induced by quinolinic acid in mice. Brain Res. 864, 40-43. (Pubitemid 30227595)
87. Schmidt A. P., Avila T. T., and, Souza D. O., (2005) Intracerebroventricular guanine-based purines protect against seizures induced by quinolinic acid in mice. Neurochem. Res. 30, 69-73. (Pubitemid 40254206)
88. Schmidt A. P., Lara D. R., and, Souza D. O., (2007) Proposal of a guanine-based purinergic system in the mammalian central nervous system. Pharmacol. Ther. 116, 401-416. (Pubitemid 350116938)
89. Schmidt A. P., Bohmer A. E., Schallenberger C., Antunes C., Pereira M. S., Leke R., Wofchuk S. T., Elisabetsky E., and, Souza D. O., (2009) Spinal mechanisms of antinociceptive action caused by guanosine in mice. Eur. J. Pharmacol. 613, 46-53.
90. Schulz J. B., Lindenau J., Seyfried J., and, Dichgans J., (2000) Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem. 267, 4904-4911. (Pubitemid 30641286)
91. Shen H. M., and, Pervaiz S., (2006) TNF receptor superfamily-induced cell death: redox-dependent execution. FASEB J. 20, 1589-1598. (Pubitemid 44943796)
92. Sorce S., and, Krause K. H., (2009) NOX enzymes in the central nervous system: from signaling to disease. Antioxid. Redox Signal. 11, 2481-2504.
93. Souza D. G., Bellaver B., Souza D. O., and, Quincozes-Santos A., (2013) Characterization of adult rat astrocyte cultures. PLoS ONE 8, e60282.
94. Sugishima M., Sakamoto H., Higashimoto Y., Omata Y., Hayashi S., Noguchi M., and, Fukuyama K., (2002) Crystal structure of rat heme oxygenase-1 in complex with heme bound to azide. Implication for regiospecific hydroxylation of heme at the alpha-meso carbon. J. Biol. Chem. 277, 45086-45090. (Pubitemid 36159109)
95. Suh S. W., Shin B. S., Ma H., Van Hoecke M., Brennan A. M., Yenari M. A., and, Swanson R. A., (2008) Glucose and NADPH oxidase drive neuronal superoxide formation in stroke. Ann. Neurol. 64, 654-663.
96. Trotti D., Danbolt N. C., and, Volterra A., (1998) Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol. Sci. 19, 328-334. (Pubitemid 28389731)
97. Tulpule K., and, Dringen R., (2012) Formate generated by cellular oxidation of formaldehyde accelerates the glycolytic flux in cultured astrocytes. Glia 60, 582-593.
98. Vargas M. R., Johnson D. A., Sirkis D. W., Messing A., and, Johnson J. A., (2008) Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J. Neurosci. 28, 13574-13581.
99. Vinade E. R., Schmidt A. P., Frizzo M. E., Izquierdo I., Elisabetsky E., and, Souza D. O., (2003) Chronically administered guanosine is anticonvulsant, amnesic and anxiolytic in mice. Brain Res. 977, 97-102. (Pubitemid 36638698)
100. Vinade E. R., Schmidt A. P., Frizzo M. E., Portela L. V., Soares F. A., Schwalm F. D., Elisabetsky E., Izquierdo I., and, Souza D. O., (2005) Effects of chronic administered guanosine on behavioral parameters and brain glutamate uptake in rats. J. Neurosci. Res. 79, 248-253. (Pubitemid 40116442)
101. Volterra A., Trotti D., Floridi S., and, Racagni G., (1994a) Reactive oxygen species inhibit high-affinity glutamate uptake: molecular mechanism and neuropathological implications. Ann. N. Y. Acad. Sci. 738, 153-162.
102. Volterra A., Trotti D., Tromba C., Floridi S., and, Racagni G., (1994b) Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J. Neurosci. 14, 2924-2932. (Pubitemid 24140915)
103. Wakabayashi N., Slocum S. L., Skoko J. J., Shin S., and, Kensler T. W., (2010) When NRF2 Talks, Who's Listening? Antioxid. Redox Signal. 13, 1649-1663.
104. Waldbaum S., and, Patel M., (2010) Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res. 88, 23-45.
105. Wang D. D., and, Bordey A., (2008) The astrocyte odyssey. Prog. Neurobiol. 86, 342-367.
106. Yoshikawa S., and, Caughey W. S., (1992) Infrared evidence of azide binding to iron, copper, and non-metal sites in heart cytochrome c oxidase. J. Biol. Chem. 267, 9757-9766.