Neurochemical evidence that 3-methylglutaric acid inhibits synaptic Na+,K+-ATPase activity probably through oxidative damage in brain cortex of young rats

International Journal of Developmental Neuroscience

Volumn 29, Issue 1, 2011, Pages 1-7

  Ribeiro, César Augusto João ^a   Hickmann, Fernanda Hermes ^a   Wajner, Moacir ^a,b  

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

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

3 Methylglutaconic aciduria; 3 Methylglutaric acid; Energy metabolism; Oxidative stress; Synaptosomes

Indexed keywords

3 HYDROXYISOVALERIC ACID; 3 METHYLGLUTACONIC ACID; 3 METHYLGLUTARIC ACID; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CREATINE; DICHLORODIHYDROFLUORESCEIN; ISOVALERIC ACID; MELATONIN; RESAZURIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; BRAIN SYNAPTOSOME; CONTROLLED STUDY; MITOCHONDRIAL RESPIRATION; NEUROTRANSMISSION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; CEREBRAL CORTEX; GLUTARATES; HUMANS; MALE; MEGLUTOL; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, WISTAR; SODIUM-POTASSIUM-EXCHANGING ATPASE; SYNAPTIC MEMBRANES; VALERATES;

RATTUS;

EID: 78650171622     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2010.10.007     Document Type: Article

References (70)

1. Anikster Y., Kleta R., Shaag A., Gahl W.A., Elpeleg O. Type III 3-methylglutaconic aciduria (optic atrophy plus syndrome, or Costeff optic atrophy syndrome): identification of the OPA3 gene and its founder mutation in Iraqi Jews. American Journal of Human Genetics 2001, 69:1218-1224.
2. Arn P., Funanage V.L. 3-Methylglutaconic aciduria disorders: the clinical spectrum increases. Journal of Pediatric Hematology/Oncology 2006, 28:62-63.
3. Barschak A.G., Sitta A., Deon M., de Oliveira M.H., Haeser A., Dutra-Filho C.S., Wajner M., Vargas C.R. Evidence that oxidative stress is increased in plasma from patients with maple syrup urine disease. Metabolic Brain Disease 2006, 21:279-286.
4. Barth P.G., Valianpour F., Bowen V.M., Lam J., Duran M., Vaz F.M., Wanders R.J. X-linked cardioskeletal myopathy and neutropenia (Barth syndrome): an update. American Journal of Medical Genetics A 2004, 126A:349-354.
5. Behl C., Moosmann B. Oxidative nerve cell death in Alzheimer's disease and stroke: antioxidants as neuroprotective compounds. Biological Chemistry 2002, 383:521-536.
6. Benari Y. Limbic seizure and brain damage produced by kainic acid - mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
7. Berg D., Youdim M.B. Role of iron in neurodegenerative disorders. Topics in Magnetic Resonance Imaging 2006, 17:5-17.
8. Bergmeyer H.U., Brent E. UV-assay with pyruvate and NADH. Methods of Enzymatic Analysis 1974, 574-579. Academic Press, New York. H.U. Bergmeyer (Ed.).
9. Besley G.T., Lendon M., Broadhead D.M., Till J., Heptinstall L.E., Phillips B. Mitochondrial complex deficiencies in a male with cardiomyopathy and 3-methylglutaconic aciduria. Journal of Inherited Metabolic Diseases 1995, 18:221-223.
10. Bogdanov M.B., Andreassen O.A., Dedeoglu A., Ferrante R.J., Beal M.F. Increased oxidative damage to DNA in a transgenic mouse model of Huntington's disease. Journal of Neurochemistry 2001, 79:1246-1249.
11. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
12. Cardoso S.M., Pereira C., Oliveira R. Mitochondrial function is differentially affected upon oxidative stress. Free Radical Biology and Medicine 1999, 26:3-13.
13. Chan K.M., Delfert D., Junger K.D. A direct colorimetric assay for Ca2+-stimulated atpase activity. Analytical Biochemistry 1986, 157:375-380.
14. Chen X., Zhong Z., Xu Z., Chen L., Wang Y. 2′,7′-Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy. Free Radical Research 2010, 44:587-604.
15. Choi D.W., Rothman S.M. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annual Review of Neuroscience 1990, 13:171-182.
16. Cousin M.A., Nicholls D.G., Pocock J.M. Modulation of ion gradients and glutamate release in cultured cerebellar granule cells by ouabain. Journal of Neurochemistry 1995, 64:2097-2104.
17. da Silva C.G., Ribeiro C.A.J., Leipnitz G., Dutra C.S., Wyse A.T.S., Wannmacher C.M.D., Sarkis J.J.F., Jakobs C., Wajner M. Inhibition of cytochrome c oxidase activity in rat cerebral cortex and human skeletal muscle by D-2-hydroxyglutaric acid in vitro. Biochimica et Biophysica Acta 2002, 1586:81-91.
18. +-ATPase activities and glutathione-reduced levels in rat hippocampus after pilocarpine-induced seizures. Cellular and Molecular Neurobiology 2010, 30:381-387.
19. de Oliveira Marques F., Hagen M.E., Pederzolli C.D., Sgaravatti A.M., Durigon K., Testa C.G., Wannmacher C.M., de Souza Wyse A.T., Wajner M., Dutra-Filho C.S. Glutaric acid induces oxidative stress in brain of young rats. Brain Research 2003, 964:153-158.
20. Di Rosa G., Deodato F., Loupatty F.J., Rizzo C., Carrozzo R., Santorelli F.M., Boenzi S., D'Amico A., Tozzi G., Bertini E., Maiorana A., Wanders R.J., Dionisi-Vici C. Hypertrophic cardiomyopathy, cataract, developmental delay, lactic acidosis: a novel subtype of 3-methylglutaconic aciduria. Journal of Inherited Metabolic Disease 2006, 29:546-550.
21. + adenosine triphosphate in rat striatal synaptosomes. Neuroscience Letters 1999, 277:91-94.
22. Fontella F.U., Gassen E., Pulrolnik V., Wannmacher C.M., Klein A.B., Wajner M., Dutra-Filho C.S. Stimulation of lipid peroxidation in vitro in rat brain by the metabolites accumulating in maple syrup urine disease. Metabolic Brain Disease 2002, 17:47-54.
23. Gibson K.M., Elpeleg O.N., Jakobs C., Costeff H., Kelley R.I. Multiple syndromes of 3-methylglutaconic aciduria. Pediatric Neurology 1993, 9:120-123.
24. Gonzalez R.J., Tarloff J.B. Evaluation of hepatic subcellular fractions for Alamar blue and MTT reductase activity. Toxicology In vitro 2001, 15:257-259.
25. + pump in epilepsy. Annals of Neurology 1984, 16:S128-S134.
26. Gunay-Aygun M. 3-Methylglutaconic aciduria: a common biochemical marker in various syndromes with diverse clinical features. Molecular Genetics and Metabolism 2005, 84:1-3.
27. Hoffmann G.F., Meier-Augenstein W., Stockler S., Surtees R., Rating D., Nyhan W.L. Physiology and pathophysiology of organic acids in cerebrospinal fluid. Journal of Inherited Metabolic Disease 1993, 16:648-669.
28. Ibel H., Endres W., Hadorn H.B., Deufel T., Paetzke I., Duran M., Kennaway N.G., Gibson K.M. Multiple respiratory chain abnormalities associated with hypertrophic cardiomyopathy and 3-methylglutaconic aciduria. European Journal of Pediatrics 1993, 152:665-670.
29. IJlst L., Loupatty F.J., Ruiter J.P., Duran M., Lehnert W., Wanders R.J. 3-Methylglutaconic aciduria type I is caused by mutations in AUH. American Journal of Human Genetics 2002, 71:1463-1466.
30. Jamme I., Petit E., Divoux D., Gerbi A., Maixent J.M., Nouvelot A. Modulation of mouse cerebral Na+K(+)-ATPase activity by oxygen free radicals. Neuroreport 1995, 7:333-337.
31. Kaplan J.H. Biochemistry of Na K-ATPase. Annual Review of Biochemistry 2002, 71:511-535.
32. Keston A.S., Brandt R. The fluorometric analysis of ultramicro quantities of hydrogen peroxide. Analytical Biochemistry 1965, 11:1-5.
33. Kurella E., Kukley M., Tyulina O., Dobrota D., Matejovicova M., Mezesova V., Boldyrev A. Kinetic parameters of Na/K-ATPase modified by free radicals in vitro and in vivo. Annals of New York Academy of Sciences 1997, 834:661-665.
34. Latini A., Borba Rosa R., Scussiato K., Llesuy S., Bello-Klein A., Wajner M. 3-Hydroxyglutaric acid induces oxidative stress and decreases the antioxidant defenses in cerebral cortex of young rats. Brain Research 2002, 956:367-373.
35. Latini A., da Silva C.G., Ferreira G.C., Schuck P.F., Scussiato K., Sarkis J.J., Dutra Filho C.S., Wyse A.T., Wannmacher C.M., Wajner M. Mitochondrial energy metabolism is markedly impaired by D-2-hydroxyglutaric acid in rat tissues. Molecular. Genetics and Metabolism 2005, 86:188-199.
36. Latini A., Scussiato K., Leipnitz G., Dutra-Filho C.S., Wajner M. Promotion of oxidative stress by 3-hydroxyglutaric acid in rat striatum. Journal of Inherited Metabolic Diseases 2005, 28:57-67.
37. Lees G.J. Inhibition of sodium-potassium ATPase-A potentially ubiquitous mechanism contributing to central nervous system neuropathology. Brain Research Reviews 1991, 16:283-300.
38. Lees G.J. Contributory mechanisms in the causation of neurodegenerative disorders. Neuroscience 1993, 54:287-322.
39. Lees G.J., Leong W. The sodium-potassium ATPase inhibitor ouabain is neurotoxici in the rat substantia nigra and striatum. Neuroscience Letters 1995, 188:113-116.
40. Lehotsky J., Kaplan P., Racay P., Matejovicova M., Drgova A., Mezesova V. Membrane ion transport systems during oxidative stress in rodent brain: protective effect of stobadine and other antioxidants. Life Sciences 1999, 65:1951-1958.
41. Leipnitz G., Seminotti B., Amaral A.U., de Bortoli G., Solano A., Schuck P.F., Wyse A.T., Wannmacher C.M., Latini A., Wajner M. Induction of oxidative stress by the metabolites accumulating in 3-methylglutaconic aciduria in cerebral cortex of young rats. Life Sciences 2008, 82:652-662.
42. Mancuso M., Coppede F., Migliore L., Siciliano G., Murri L. Mitochondrial dysfunction, oxidative stress and neurodegeneration. Journal of Alzheimer's Disease 2006, 10:59-73.
43. Nakai M., Mori A., Watanabe A., Mitsumoto Y. 1-Methyl-4-phenylpyridinium (MPP+) decreases mitochondrial oxidation-reduction (REDOX) activity and membrane potential (Deltapsi(m)) in rat striatum. Experimental Neurology 2003, 179:103-110.
44. Nicholls D.G. Bioenergetics and transmitter release in the isolated nerve terminal. Neurochemical Research 2003, 28:1433-1441.
45. Parker W.D., Boyson S.J., Luder A.S., Parks J.K. Evidence for a defect in NADH: ubiquinone oxidoreductase (complex I) in Huntington's disease. Neurology 1990, 40:1231-1234.
46. Parker W.D., Parks J., Filley C.M., Kleinschmidt-DeMasters B.K. Electron transport chain defects in Alzheimer's disease brain. Neurology 1994, 44:1090-1096.
47. Peral M.J., Vazquez-Carretero M.D., Ilundain A.A. Na(+)/Cl(-)/creatine transporter activity and expression in rat brain synaptosomes. Neuroscience 2010, 165:53-60.
48. Rauchova H., Drahota Z., Koudelova J. The role of membrane fluidity changes and thiobarbituric acid-reactive substances production in the inhibition of cerebral cortex Na+/K+-ATPase activity. Physiological Research 1999, 48:73-78.
49. Ribeiro C.A.J., Balestro F., Grando V., Wajner M. Isovaleric acid reduces Na+K+-ATPase activity in synaptic membranes from cerebral cortex of young rats. Cellular and Molecular Neurobiology 2007, 27:529-540.
50. Ruesch S., Krahenbuhl S., Kleinle S., Liechti-Gallati S., Schaffner T., Wermuth B., Weber J., Wiesmann U.N. Combined 3-methylglutaconic and 3-hydroxy-3-methylglutaric aciduria with endocardial fibroelastosis and dilatative cardiomyopathy in male and female siblings with partial deficiency of complex II/III in fibroblasts. Enzyme and Protein 1996, 49:321-329.
51. +-ATPase activity in rat brain. Pharmacology. Biochemistry and Behavior 2010, 95:88-91.
52. Satoh E., Nakazato Y. On the mechanism of ouabain-induced release of acetylcholine from synaptosomes. Journal of Neurochemistry 1992, 58:1038-1044.
53. Sauer S.W., Okun J.G., Fricker G., Mahringer A., Muller I., Crnic L.R., Muhlhausen C., Hoffmann G.F., Horster F., Goodman S.I., Harding C.O., Koeller D.M., Kolker S. Intracerebral accumulation of glutaric and 3-hydroxyglutaric acids secondary to limited flux across the blood-brain barrier constitute a biochemical risk factor for neurodegeneration in glutaryl-CoA dehydrogenase deficiency. Journal of Neurochemistry 2006, 97:899-910.
54. Sestili P., Martinelli C., Bravi G., Piccoli G., Curci R., Battistelli M., Falcieri E., Agostini D., Gioacchini A.M., Stocchi V. Creatine supplementation affords cytoprotection in oxidatively injured cultured mammalian cells via direct antioxidant activity. Free Radicals in Biology and Medicine 2006, 40:837-849.
55. Shoji Y., Takahashi T., Sawaishi Y., Ishida A., Matsumori M., Enoki M., Watanabe H., Takada G. 3-Methylglutaconic aciduria type I: clinical heterogeneity as a neurometabolic disease. Journal of Inherited Metabolic Diseases 1999, 22:1-8.
56. Silva-Adaya D., Perez-De La Cruz V., Herrera-Mundo M.N., Mendoza-Macedo K., Villeda-Hernandez J., Binienda Z., Ali S.F., Santamaria A. Excitotoxic damage, disrupted energy metabolism, and oxidative stress in the rat brain: antioxidant and neuroprotective effects of L-carnitine. Journal of Neurochemistry 2008, 105:677-689.
57. Springer J.E., Azbill R.D., Carlson S.L. A rapid and sensitive assay for measuring mitochondrial metabolic activity in isolated neural tissue. Brain Research Protocols 1998, 2:259-263.
58. Stellmer F., Keyser B., Burckhardt B.C., Koepsell H., Streichert T., Glatzel M., Jabs S., Thiem J., Herdering W., Koeller D.M., Goodman S.I., Lukacs Z., Ullrich K., Burckhardt G., Braulke T., Muhlhausen C. 3-Hydroxyglutaric acid is transported via the sodium-dependent dicarboxylate transporter NaDC3. Journal of Molecular Medicine 2007, 85:763-770.
59. Stoy N., Mackay G.M., Forrest C.M., Christofides J., Egerton M., Stone T.W., Darlington L.G. Tryptophan metabolism and oxidative stress in patients with Huntington's disease. Journal of Neurochemistry 2005, 93:611-623.
60. Sweadner K.J. Two molecular forms of Na+-stimulated+K+-stimulated ATPase in brain - separation and difference in affinity for Strophanthidin. Journal of Biological Chemistry 1979, 254:6060-6067.
61. Sweetman L., Williams J.C. Disorders of branched-chain amino acid and organic acid metabolism. The Metabolic and Molecular Basis of Inherited Disease 2001, vol. II:2125-2159. McGraw-Hill Professional.
62. Swerdlow R.H., Parks J.K., Cassarino D.S., Maguire D.J., Maguire R.S., Bennett J.P., Davis R.E., Parker W.D. Cybrids in Alzheimer's disease: a cellular model of the disease. Neurology 1997, 49:918-925.
63. Swerdlow R.H., Parks J.K., Miller S.W., Tuttle J.B., Trimmer P.A., Sheehan J.P., Bennett J.P., Davis R.E., Parker W.D. Origin and functional consequences of the complex I defect in Parkinson's disease. Annals of Neurology 1996, 40:663-671.
64. Tsakiris S., Deliconstantinos G. Influence of phosphatidylserine on (Na+K+)-stimulated ATPase and acetylcholinesterase activities of dog brain synaptosomal plasma membranes. Biochemical Journal 1984, 220:301-307.
65. Wortmann S., Rodenburg R.J., Huizing M., Loupatty F.J., de Koning T., Kluijtmans L.A., Engelke U., Wevers R., Smeitink J.A., Morava E. Association of 3-methylglutaconic aciduria with sensori-neural deafness, encephalopathy, and Leigh-like syndrome (MEGDEL association) in four patients with a disorder of the oxidative phosphorylation. Molecular Genetics and Metabolism 2006, 88:47-52.
66. Wyse A.T., Sarkis J.J., Cunha-Filho J.S., Teixeira M.V., Schetinger M.R., Wajner M., Wannmacher C.M. ATP diphosphohydrolase activity in synaptosomes from cerebral cortex of rats subjected to chemically induced phenylketonuria. Brazilian Journal of Medical and Biological Research 1995, 28:643-649.
67. Wyse A.T., Bavaresco C.S., Bandinelli C., Streck E.L., Franzon R., Dutra-Filho C.S., Wajner M. Nitric oxide synthase inhibition by L-NAME prevents the decrease of Na+K+-ATPase activity in midbrain of rats subjected to arginine administration. Neurochemical Research 2001, 26:515-520.
68. Yagi K Simple procedure for specific assay of lipid hydroperoxides in serum or plasma. Methods in Molecular Biology 1998, 108:107-110.
69. Yousef M.I., El-Hendy H.A., El-Demerdash F.M., Elagamy E.I. Dietary zinc deficiency induced-changes in the activity of enzymes and the levels of free radicals, lipids and protein electrophoretic behavior in growing rats. Toxicology 2002, 175:223-234.
70. Yufu K., Itoh T., Edamatsu R., Mori A., Hirakawa M. Effect of hyperbaric oxygenation on the Na+K(+)-ATPase and membrane fluidity of cerebrocortical membranes after experimental subarachnoid hemorrhage. Neurochemical Research 1993, 18:1033-1039.