Mitochondrial dysfunction related to cell damage induced by 3-hydroxykynurenine and 3-hydroxyanthranilic acid: Non-dependent-effect of early reactive oxygen species production

NeuroToxicology

Volumn 50, Issue , 2015, Pages 81-91

  Reyes Ocampo, J ^a,b   Ramirez Ortega D ^a   Vazquez Cervantes G I ^a   Pineda, B ^a   Montes de Oca Balderas, Pavel ^a   Gonzalez Esquivel D ^a   Sanchez Chapul L ^c   Lugo Huitron R ^a   Silva Adaya, D ^a   Rios C ^a   Jimenez Anguiano A ^b   Perez de la Cruz V ^a  

^a NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^b DEPARTAMENTO DE QUÍMICA   (Mexico)

^c Laboratorio de Bioquímica Muscular Instituto Nacional de Rehabilitación S S A   (Mexico)

Author keywords

3 Hydroxyanthranilic acid; 3 Hydroxykynurenine; Kynurenines; Mitochondria dysfunction; Oxidative damage

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; 3 HYDROXYANTHRANILIC ACID; 3 HYDROXYKYNURENINE; REACTIVE OXYGEN METABOLITE; 3-HYDROXYKYNURENINE; KYNURENINE; SCAVENGER; SUCCINATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE CULTURE; BRAIN CELL CULTURE; BRAIN TISSUE; CELL DAMAGE; CELL DEATH; CELL ENERGY; CELL FUNCTION; CELL METABOLISM; CIRCLING BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; CYTOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; ANALOGS AND DERIVATIVES; ANIMAL; ASTROCYTE; BRAIN; BRAIN CORTEX; CELL CULTURE; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFECTS; ENERGY METABOLISM; METABOLISM; OXIDATION REDUCTION REACTION; STEREOTYPY; WISTAR RAT;

ANIMALIA; RATTUS;

3-HYDROXYANTHRANILIC ACID; ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FREE RADICAL SCAVENGERS; KYNURENINE; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIAL DISEASES; OXIDATION-REDUCTION; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; STEREOTYPED BEHAVIOR; SUCCINATE DEHYDROGENASE;

EID: 84939230085     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2015.08.003     Document Type: Article

References (54)

1. Abarca-Rojano E., Muniz-Hernandez S., Moreno-Altamirano M.M., Mondragon-Flores R., Enriquez-Rincon F., Sanchez-Garcia F.J. Re-organization of mitochondria at the NK cell immune synapse. Immunol. Lett. 2009, 122:18-25.
2. Almeida A., Almeida J., Bolanos J.P., Moncada S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:15294-15299.
3. Amori L., Wu H.Q., Marinozzi M., Pellicciari R., Guidetti P., Schwarcz R. Specific inhibition of kynurenate synthesis enhances extracellular dopamine levels in the rodent striatum. Neuroscience 2009, 159:196-203.
4. Baran H., Staniek K., Kepplinger B., Stur J., Draxler M., Nohl H. Kynurenines and the respiratory parameters on rat heart mitochondria. Life Sci. 2003, 72:1103-1115.
5. Beckman J.S., Chen J., Ischiropoulos H., Crow J.P. Oxidative chemistry of peroxynitrite. Methods Enzymol. 1994, 233:229-240.
6. Beggiato S., Antonelli T., Tomasini M.C., Tanganelli S., Fuxe K., Schwarcz R., et al. Kynurenic acid, by targeting alpha7 nicotinic acetylcholine receptors, modulates extracellular GABA levels in the rat striatum in vivo. Eur. J. Neurosci. 2013, 37:1470-1477.
7. Beggiato S., Tanganelli S., Fuxe K., Antonelli T., Schwarcz R., Ferraro L. Endogenous kynurenic acid regulates extracellular GABA levels in the rat prefrontal cortex. Neuropharmacology 2014, 82:11-18.
8. Belanger M., Allaman I., Magistretti P.J. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 2011, 14:724-738.
9. Belanger M., Magistretti P.J. The role of astroglia in neuroprotection. Dial. Clin. Neurosci. 2009, 11:281-295.
10. Christen S., Peterhans E., Stocker R. Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:2506-2510.
11. Dringen R., Gutterer J.M., Hirrlinger J. Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur. J. Biochem./FEBS 2000, 267:4912-4916.
12. Eastman C.L., Guilarte T.R. Cytotoxicity of 3-hydroxykynurenine in a neuronal hybrid cell line. Brain Res. 1989, 495:225-231.
13. Eastman C.L., Guilarte T.R. The role of hydrogen peroxide in the in vitro cytotoxicity of 3-hydroxykynurenine. Neurochem. Res. 1990, 15:1101-1107.
14. Erhardt S., Schwieler L., Emanuelsson C., Geyer M. Endogenous kynurenic acid disrupts prepulse inhibition. Biol. Psychiatry 2004, 56:255-260.
15. Floriano-Sanchez E., Villanueva C., Medina-Campos O.N., Rocha D., Sanchez-Gonzalez D.J., Cardenas-Rodriguez N., et al. Nordihydroguaiaretic acid is a potent in vitro scavenger of peroxynitrite, singlet oxygen, hydroxyl radical, superoxide anion and hypochlorous acid and prevents in vivo ozone-induced tyrosine nitration in lungs. Free Radic. Res. 2006, 40:523-533.
16. Fontana M., Mosca L., Rosei M.A. Interaction of enkephalins with oxyradicals. Biochem. Pharmacol. 2001, 61:1253-1257.
17. Giles G.I., Collins C.A., Stone T.W., Jacob C. Electrochemical and in vitro evaluation of the redox-properties of kynurenine species. Biochem. Biophys. Res. Commun. 2003, 300:719-724.
18. Guidetti P., Luthi-Carter R.E., Augood S.J., Schwarcz R. Neostriatal and cortical quinolinate levels are increased in early grade Huntington's disease. Neurobiol. Dis. 2004, 17:455-461.
19. Guidetti P., Schwarcz R. 3-Hydroxykynurenine potentiates quinolinate but not NMDA toxicity in the rat striatum. Eur. J. Neurosci. 1999, 11:3857-3863.
20. Guillemin G.J., Kerr S.J., Smythe G.A., Smith D.G., Kapoor V., Armati P.J., et al. Kynurenine pathway metabolism in human astrocytes: a paradox for neuronal protection. J. Neurochem. 2001, 78:842-853.
21. Halliwell B., Gutteridge J.M., Aruoma O.I. The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 1987, 165:215-219.
22. Hiraku Y., Inoue S., Oikawa S., Yamamoto K., Tada S., Nishino K., et al. Metal-mediated oxidative damage to cellular and isolated DNA by certain tryptophan metabolites. Carcinogenesis 1995, 16:349-356.
23. Jhamandas K., Boegman R.J., Beninger R.J., Bialik M. Quinolinate-induced cortical cholinergic damage: modulation by tryptophan metabolites. Brain Res. 1990, 529:185-191.
24. Kun E., Abood L.G. Colorimetric estimation of succinic dehydrogenase by triphenyltetrazolium chloride. Science 1949, 109:144-146.
25. Lapin I.P. Kynurenines and seizures. Epilepsia 1981, 22:257-265.
26. Leipnitz G., Schumacher C., Dalcin K.B., Scussiato K., Solano A., Funchal C., et al. In vitro evidence for an antioxidant role of 3-hydroxykynurenine and 3-hydroxyanthranilic acid in the brain. Neurochem. Int. 2007, 50:83-94.
27. Long L.H., Evans P.J., Halliwell B. Hydrogen peroxide in human urine: implications for antioxidant defense and redox regulation. Biochem. Biophys. Res. Commun. 1999, 262:605-609.
28. Lugo-Huitron R., Blanco-Ayala T., Ugalde-Muniz P., Carrillo-Mora P., Pedraza-Chaverri J., Silva-Adaya D., et al. On the antioxidant properties of kynurenic acid: free radical scavenging activity and inhibition of oxidative stress. Neurotoxicol. Teratol. 2011, 33:538-547.
29. Magana-Maldonado R., Manoutcharian K., Hernandez-Pedro N.Y., Rangel-Lopez E., Perez-De la Cruz V., Rodriguez-Balderas C., et al. Concomitant treatment with pertussis toxin plus temozolomide increases the survival of rats bearing intracerebral RG2 glioma. J. Cancer Res. Clin. Oncol. 2014, 140:291-301.
30. Morita T., Saito K., Takemura M., Maekawa N., Fujigaki S., Fujii H., et al. 3-Hydroxyanthranilic acid, an L-tryptophan metabolite, induces apoptosis in monocyte-derived cells stimulated by interferon-gamma. Ann. Clin. Biochem. 2001, 38:242-251.
31. Nakagami Y., Saito H., Katsuki H. 3-Hydroxykynurenine toxicity on the rat striatum in vivo. Jpn. J. Pharmacol. 1996, 71:183-186.
32. Okuda S., Nishiyama N., Saito H., Katsuki H. 3-Hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J. Neurochem. 1998, 70:299-307.
33. Perez-De La Cruz V., Elinos-Calderon D., Carrillo-Mora P., Silva-Adaya D., Konigsberg M., Moran J., et al. Time-course correlation of early toxic events in three models of striatal damage: modulation by proteases inhibition. Neurochem. Int. 2010, 56:834-842.
34. Perez-De La Cruz V., Gonzalez-Cortes C., Galvan-Arzate S., Medina-Campos O.N., Perez-Severiano F., Ali S.F., et al. Excitotoxic brain damage involves early peroxynitrite formation in a model of Huntington's disease in rats: protective role of iron porphyrinate 5,10,15,20-tetrakis (4-sulfonatophenyl)porphyrinate iron (III). Neuroscience 2005, 135:463-474.
35. Perez-De La Cruz V., Gonzalez-Cortes C., Pedraza-Chaverri J., Maldonado P.D., Andres-Martinez L., Santamaria A. Protective effect of S-allylcysteine on 3-nitropropionic acid-induced lipid peroxidation and mitochondrial dysfunction in rat brain synaptosomes. Brain Res. Bull. 2006, 68:379-383.
36. Perez-De La Cruz V., Konigsberg M., Pedraza-Chaverri J., Herrera-Mundo N., Diaz-Munoz M., Moran J., et al. Cytoplasmic calcium mediates oxidative damage in an excitotoxic/energetic deficit synergic model in rats. Eur. J. Neurosci. 2008, 27:1075-1085.
37. Potter M.C., Elmer G.I., Bergeron R., Albuquerque E.X., Guidetti P., Wu H.Q., et al. Reduction of endogenous kynurenic acid formation enhances extracellular glutamate, hippocampal plasticity, and cognitive behavior. Neuropsychopharmacol.: Off. Publ. Am. College Neuropsychopharmacol. 2010, 35:1734-1742.
38. Quagliariello E., Papa S., Saccone C., Alifano A. Effect of 3-hydroxyanthranilic acid on the mitochondrial respiratory system. Biochem. J. 1964, 91:137-146.
39. Ramirez Ortega D. Caracterización del efecto de 3-hidroxikinurenina per se y bajo condiciones pro-oxidantes en cerebro de rata: un estudio in vtro e in vivo [Original] 2013, Universidad Nacional Autonoma de Mexico, Mexico City.
40. Ramirez Ortega, D., Vazquez Cervantes, G., Perla, U.M., Lugo Huitrón, R., Rangel Lopez, E., Campos Peña, V., et al., 2013. Chelating, scavenging and antioxidant properties of 3-hydroxykynurenine in brain tissue homogenates of rat exposed to peroxynitrite and FESO4: comparison with 3-hydroxyanthranilic. 2013 Neuroscience Meeting Planner San Diego, Society for Neuroscience, CA.
41. Reinhard J.F. Pharmacological manipulation of brain kynurenine metabolism. Ann. N. Y. Acad. Sci. 2004, 1035:335-349.
42. Reyes Ocampo J., Lugo Huitron R., Gonzalez-Esquivel D., Ugalde-Muniz P., Jimenez-Anguiano A., Pineda B., et al. Kynurenines with neuroactive and redox properties: relevance to aging and brain diseases. Oxidat. Med. Cell. Longevity 2014, 2014:646909.
43. Roberts R.C., McCarthy K.E., Du F., Ottersen O.P., Okuno E., Schwarcz R. 3-Hydroxyanthranilic acid oxygenase-containing astrocytic processes surround glutamate-containing axon terminals in the rat striatum. J. Neurosci.: Off. J. Soc. Neurosci. 1995, 15:1150-1161.
44. Rosenthal R.E., Hamud F., Fiskum G., Varghese P.J., Sharpe S. Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine. J. Cerebral Blood Flow Metab.: Off. J. Int. Soc. Cerebral Blood Flow Metab. 1987, 7:752-758.
45. Schwarcz R., Pellicciari R. Manipulation of brain kynurenines: glial targets, neuronal effects, and clinical opportunities. J. Pharmacol. Exp. Therapeut. 2002, 303:1-10.
46. Shih A.Y., Johnson D.A., Wong G., Kraft A.D., Jiang L., Erb H., et al. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J. Neurosci.: Off. J. Soc. Neurosci. 2003, 23:3394-3406.
47. Silva-Adaya D., Perez-De La Cruz V., Herrera-Mundo M.N., Mendoza-Macedo K., Villeda-Hernandez J., Binienda Z., et al. Excitotoxic damage, disrupted energy metabolism, and oxidative stress in the rat brain: antioxidant and neuroprotective effects of L-carnitine. J. Neurochem. 2008, 105:677-689.
48. Speciale C., Schwarcz R. Uptake of kynurenine into rat brain slices. J. Neurochem. 1990, 54:156-163.
49. Stone T.W., Darlington L.G. Endogenous kynurenines as targets for drug discovery and development. Nat. Rev. Drug Discov. 2002, 1:609-620.
50. Vazquez Cervantes G. Caracterizacion de las propiedades redox del acido 3-hidroxiantranilico: un estudio in vivo e in vitro [Original] 2013, Universidad Nacional Autonoma de México, Mexico DF.
51. Vazquez S., Garner B., Sheil M.M., Truscott R.J. Characterisation of the major autoxidation products of 3-hydroxykynurenine under physiological conditions. Free Rad. Res. 2000, 32:11-23.
52. Widner B., Leblhuber F., Walli J., Tilz G.P., Demel U., Fuchs D. Tryptophan degradation and immune activation in Alzheimer's disease. J. Neural. Transm. 2000, 107:343-353.
53. Wilson J.X. Antioxidant defense of the brain: a role for astrocytes. Can. J. Physiol. Pharmacol. 1997, 75:1149-1163.
54. Zadori D., Klivenyi P., Szalardy L., Fulop F., Toldi J., Vecsei L. Mitochondrial disturbances, excitotoxicity, neuroinflammation and kynurenines: novel therapeutic strategies for neurodegenerative disorders. J. Neurol. Sci. 2012, 322:187-191.