In vitro evidence that sulfite impairs glutamatergic neurotransmission and inhibits glutathione metabolism-related enzymes in rat cerebral cortex

International Journal of Developmental Neuroscience

Volumn 42, Issue , 2015, Pages 68-75

  Parmeggiani, Belisa ^a   Moura, Alana Pimentel ^a   Grings, Mateus ^a   Bumbel, Anna Paula ^a   de Moura Alvorcem, Leonardo ^a   Tauana Pletsch, Julia ^a   Fernandes, Carolina Gonçalves ^a   Wyse, Angela T S ^a   Wajner, Moacir ^a,b   Leipnitz, Guilhian ^a  

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

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

Glutamatergic neurotransmission; Rat cerebral cortex; Redox homeostasis; Sulfite; Sulfite oxidase deficiency; Thiosulfate

Indexed keywords

GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; SULFITE; THIOSULFATE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; GLUTATHIONE; LACTATE DEHYDROGENASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRITIUM;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN SLICE; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME INHIBITION; GLUTAMATERGIC NEUROTRANSMISSION; GLUTATHIONE METABOLISM; IN VITRO STUDY; LONG TERM EXPOSURE; METABOLITE; NEUROTRANSMISSION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RAT; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; OXIDATIVE STRESS; PROTEIN CARBONYLATION; WISTAR RAT;

RATTUS;

ANIMALS; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUTAMIC ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; IN VITRO TECHNIQUES; L-LACTATE DEHYDROGENASE; NEUROTRANSMITTER AGENTS; OXIDATIVE STRESS; PROTEIN CARBONYLATION; RATS; RATS, WISTAR; SULFITES; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TRITIUM;

EID: 84925299634     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2015.03.005     Document Type: Article

References (44)

1. Aksenov M.Y., Markesbery W.R. Change in thiol content and expression of glutathione redox system gene in the hippocampus and cerebellum in Alzheimer's disease. Neurosci. Lett. 2001, 302:141-145.
2. Almeida R.F., Thomazi A.P., Godinho G.F., Saute J.A., Wofchuk S.T., Souza D.O., Ganzella M. Effects of depressive-like behavior of rats on brain glutamate uptake. Neurochem. Res. 2010, 35(8):1164-1171.
3. Arenas A., López-Alarcón C., Kogan M., Lissi E., Davies M.J., Silva E. Chemical modification of lysozyme, glucose 6-phosphate dehydrogenase, and bovine eye lens proteins induced by peroxyl radicals: role of oxidizable amino acid residues. Chem. Res. Toxicol. 2013, 26(1):67-77.
4. Banerjee R., Vitvitsky V., Garg S.K. The undertow of sulfur metabolism on glutamatergic neurotransmission. Trends Biochem. Sci. 2008, 33(9):413-419.
5. Basheer S.N., Waters P.J., Lam C.W., Acquaviva-Bourdain C., Hendson G., Poskitt K., Hukin J. Isolated sulfite oxidase deficiency in the newborn: lactic acidaemia and leukoencephalopathy. Neuropediatrics 2007, 38(1):38-41.
6. Beste C., Stock A.K., Ness V., Hoffmann R., Saft C. Evidence for divergent effects of neurodegeneration in Huntington's disease on attentional selection and neural plasticity: implications for excitotoxicity. Brain Struct. Funct. 2014, article in press.
7. Bindu P.S., Christopher R., Mahadevan A., Bharath R.D. Clinical and imaging observations in isolated sulfite oxidase deficiency. J. Child Neurol. 2011, 26(8):1036-1040.
8. Browne R.W., Armstrong D. Reduced glutathione and glutathione disulfide. Methods Mol. Biol. 1998, 108:347-352.
9. Carlberg I., Mannervik B. Glutathione reductase. Methods Enzymol. 1985, 113:484-490.
10. Chiarani F., Bavaresco C.S., Dutra-Filho C.S., Netto C.A., Wyse A.T. Sulfite increases lipoperoxidation and decreases the activity of catalase in brain of rats. Metab. Brain Dis. 2008, 23(1):123-132.
11. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65(1):1-105.
12. Dublin A.B., Hald J.K., Wootton-Gorges S.L. Isolated sulfite oxidase deficiency: MR imaging features. AJNR Am. J. Neuroradiol. 2002, 23(3):484-485.
13. Evelson P., Travacio M., Repetto M., Escobar J., Llesuy S., Lissi E.A. Evaluation of total reactive antioxidant potential (TRAP) of tissue homogenates and their cytosols. Arch. Biochem. Biophys. 2001, 388:261-266.
14. Frizzo M.E., Lara D.R., Prokopiuk A.S., Vargas C.R., Salbego C.G., Wajner M., Souza D.O. Guanosine enhances glutamate uptake in brain cortical slices at normal and excitotoxic conditions. Cell Mol. Neurobiol. 2002, 22(3):353-363.
15. Grings M., Moura A.P., Parmeggiani B., Marcowich G.F., Amaral A.U., de Souza Wyse A.T., Wajner M., Leipnitz G. Disturbance of brain energy and redox homeostasis provoked by sulfite and thiosulfate: potential pathomechanisms involved in the neuropathology of sulfite oxidase deficiency. Gene 2013, 531(2):191-198.
16. Gu F., Chauhan V., Chauhan A. Glutathione redox imbalance in brain disorders. Curr. Opin. Clin. Nutr. Metab. Care 2015, 18(1):89-95.
17. - radicals. J. Am. Chem. Soc. 1972, 94:47-57.
18. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine 2007, Oxford University Press, New York. fourth ed.
19. Johnson J.L., Duran M. Molybdenum cofactor deficiency and isolated sulfite oxidase deficiency. The Metabolicand Molecular Bases of Inherited Disease 2001, 3181-3217. McGraw-Hill, New York. C.R. Scriver, A.L. Beaudet, D. Valle, W.S. Sly (Eds.).
20. Kocamaz E., Adiguzel E., Er B., Gundogdu G., Kucukatay V. Sulfite leads to neuron loss in the hippocampus of both normal and SOX-deficient rats. Neurochem. Int. 2012, 61(3):341-346.
21. Kostic M., Zivkovic N., Stojanovic I. Multiple sclerosis and glutamate excitotoxicity. Rev. Neurosci. 2012, 24(1):71-88.
22. Küçükatay V., Savcioğlu F., Hacioğlu G., Yargiçoğlu P., Ağar A. Effect of sulfite on cognitive function in normal and sulfite oxidase deficient rats. Neurotoxicol. Teratol. 2005, 27(1):47-54.
23. Leong S.F., Clark J.B. Regional development of glutamate dehydrogenase in the rat brain. J. Neurochem. 1984, 43:106-111.
24. Mannervik B., Guthenberg C. Glutathione transferase (human placenta). Methods Enzymol. 1981, 77:231-235.
25. Matés J.M., Pérez-Gómez C., Núñez de Castro I., Asenjo M., Márquez J. Glutamine and its relationship with intracellular redox status, oxidative stress and cell proliferation/death. Int. J. Biochem. Cell Biol. 2002, 34(5):439-458.
26. Mehta A., Prabhakar M., Kumar P., Deshmukh R., Sharma P.L. Excitotoxicity: bridge to various triggers in neurodegenerative disorders?. Eur. J. Pharmacol. 2013, 698(1-3):6-18.
27. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
28. Mysona B., Dun Y., Duplantier J., Ganapathy V., Smith S.B. Effects of hyperglycemia and oxidative stress on the glutamate transporters GLAST and system xc- in mouse retinal Müller glial cells. Cell Tissue Res. 2009, 335(3):477-488.
29. Niknahad H., O'Brien P.J. Mechanism of sulfite cytotoxicity in isolated rat hepatocytes. Chem. Biol. Interact. 2008, 174(3):147-154.
30. Olney J.W. Glutamate-induced retinal degeneration in neonatal mice: electron microscopy of the acutely evolving lesion. J. Neuropathol. Exp. Neurol. 1969, 28(3):455-474.
31. Ozsoy O., Aras S., Ozkan A., Parlak H., Aslan M., Yargicoglu P., Agar A. 2014. The effect of ingested sulfite on visual evoked potentials, lipid peroxidation, and antioxidant status of brain in normal and sulfite oxidase-deficient aged rats. Toxicol. Ind. Health 2014, article in press.
32. Oztürk O.H., Küçükatay V., Yönden Z., Ağar A., Bağci H., Delibaş N. Expressions of N-methyl-d-aspartate receptors NR2A and NR2B subunit proteins in normal and sulfite-oxidase deficient rat's hippocampus: effect of exogenous sulfite ingestion. Arch. Toxicol. 2006, 80(10):671-679.
33. Reznick A.Z., Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 1994, 233:357-363.
34. Robinson H.C., Pasternak C.A. The isolation of S-sulphoglutathione from the small intestine of the rat. Biochem. J. 1964, 93(3):487-492.
35. Rosa R.B., Dalcin K.B., Schmidt A.L., Gerhardt D., Ribeiro C.A., Ferreira G.C., Schuck P.F., Wyse A.T., Porciúncula L.O., Wofchuk S., Salbego C.G., Souza D.O., Wajner M. Evidence that glutaric acid reduces glutamate uptake by cerebral cortex of infant rats?. Life Sci. 2007, 81(25-26):1668-1676.
36. Salman M.S., Ackerley C., Senger C., Becker L. New insights into the neuropathogenesis of molybdenum cofactor deficiency. Can. J. Neurol. Sci. 2002, 29:91-96.
37. Schwarz G., Mendel R.R., Ribbe M.W. Molybdenum cofactors, enzymes and pathways. Nature 2009, 460(7257):839-847.
38. Tan W.H., Eichler F.S., Hoda S., Lee M.S., Baris H., Hanley C.A., Grant P.E., Krishnamoorthy K.S., Shih V.E. Isolated sulfite oxidase deficiency: a case report with a novel mutation and review of the literature. Pediatrics 2005, 116(3):757-766.
39. Taylor S.L., Higley N.A., Bush R.K. Sulfites in foods: uses analytical methods, residues, fate, exposure assessment, metabolism, toxicity, and hypersensitivity. Adv. Food Res. 1986, 30:1-76.
40. Trotti D., Danbolt N.C., Volterra A. Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration?. Trends Pharmacol. Sci. 1998, 19(8):328-334.
41. Wendel A. Glutathione peroxidase. Methods Enzymol. 1981, 77:325-332.
42. Woo W.H., Yang H., Wong K.P., Halliwell B. Sulphite oxidase gene expression in human brain and in other human and rat tissues. Biochem. Biophys. Res. Commun. 2003, 305(3):619-623.
43. Yagi K. Simple procedure for specific assay of lipid hydroperoxides in serum or plasma. Methods Mol. Biol. 1998, 108:107-110.
44. Zhang X., Vincent A.S., Halliwell B., Wong K.P. A mechanism of sulfite neurotoxicity: direct inhibition of glutamate dehydrogenase. J. Biol. Chem. 2004, 279(41):43035-43045.