Disturbance of brain energy and redox homeostasis provoked by sulfite and thiosulfate: Potential pathomechanisms involved in the neuropathology of sulfite oxidase deficiency

Gene

Volumn 531, Issue 2, 2013, Pages 191-198

  Grings, Mateus ^a   Moura, Alana Pimentel ^a   Parmeggiani, Belisa ^a   Marcowich, Gustavo Flora ^a   Amaral, Alexandre Umpierrez ^a   de Souza Wyse, Angela Terezinha ^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

Bioenergetic dysfunction; Rat brain; Reactive species; Sulfite; Sulfite oxidase deficiency; Thiosulfate

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANTIOXIDANT; CREATINE KINASE; CYTOCHROME C OXIDASE; DICHLOROFLUORESCEIN; GLUTATHIONE; HYDROGEN PEROXIDE; MELATONIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SULFITE; SULFITE OXIDASE; THIOSULFATE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN CORTEX; CELL ENERGY; CELL TRANSFER; CONTROLLED STUDY; CYTOSOL; DRUG EFFICACY; DRUG INHIBITION; ENERGY; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME DEFICIENCY; HOMEOSTASIS; IN VITRO STUDY; MALE; METABOLITE; MITOCHONDRION; NEUROPATHOLOGY; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; SULFITE OXIDASE DEFICIENCY; SYNAPSE;

2′,7′-DICHLOROFLUORESCEIN DIACETATE; 2′,7′-DICHLOROFLUORESCIN; 2,6-DICHLOROINDOPHENOL; BIOENERGETIC DYSFUNCTION; CCK; CK; CREATINE KINASE; CYTOSOLIC CREATINE KINASE; DCF; DCF-DA; DCFH; DCIP; DICHLOROFLUORESCEIN; GSH; INORGANIC PHOSPHATE; L-NAME; MCK; MEL; MELATONIN; MITOCHONDRIAL CREATINE KINASE; N(Ω)-NITRO-L-ARGININE METHYL ESTER; PI; RAT BRAIN; REACTIVE OXYGEN SPECIES; REACTIVE SPECIES; REDUCED GLUTATHIONE; ROS; SO; SULFITE; SULFITE OXIDASE; SULFITE OXIDASE DEFICIENCY; TCK; THIOSULFATE; TOTAL CREATINE KINASE; TRO; TROLOX;

AMINO ACID METABOLISM, INBORN ERRORS; ANIMALS; BRAIN; BRAIN DISEASES, METABOLIC; ELECTRON TRANSPORT; ENERGY METABOLISM; HOMEOSTASIS; MALE; OXIDATION-REDUCTION; RATS; RATS, WISTAR; SULFITE OXIDASE; SULFITES; THIOSULFATES;

RATTUS;

EID: 84885421757     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2013.09.018     Document Type: Article

References (74)

1. Appignani B.A., Kaye E.M., Wolpert S.M. CT and MR appearance of the brain in two children with molybdenum cofactor deficiency. AJNR Am. J. Neuroradiol. 1996, 17:317-320.
2. Arnold S. The power of life-cytochrome c oxidase takes center stage in metabolic control, cell signalling and survival. Mitochondrion 2012, 12:46-56.
3. Arstall M.A., Bailey C., Gross W.L., Bak M., Balligand J.L., Kelly R.A. Reversible S-nitrosation of creatine kinase by nitric oxide in adult rat ventricular myocytes. J. Mol. Cell. Cardiol. 1998, 30:979-988.
4. Baker M.T., Dehring D.J., Gregerson M.S. Sulfite supported lipid peroxidation in propofol emulsions. Anesthesiology 2002, 97:1162-1167.
5. Basheer S.N., et al. Isolated sulfite oxidase deficiency in the newborn: lactic acidaemia and leukoencephalopathy. Neuropediatrics 2007, 38:38-41.
6. Bindu P.S., Christopher R., Mahadevan A., Bharath R.D. Clinical and imaging observations in isolated sulfite oxidase deficiency. J. Child. Neurol. 2011, 26:1036-1040.
7. Bulteau A.L., Ikeda-Saito M., Szweda L.I. Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 2003, 42:14846-14855.
8. Burmistrov S.O., Mashek O.P., Kotin A.M. The action of acute alcoholic intoxication on the antioxidant system and creatine kinase activity in the brain of rat embryos. Eksp. Klin. Farmakol. 1992, 55:54-56.
9. Cantu D., Fulton R.E., Drechsel D.A., Patel M. Mitochondrial aconitase knockdown attenuates paraquat-induced dopaminergic cell death via decreased cellular metabolism and release of iron and H(2)O(2). J. Neurochem. 2011, 118:79-92.
10. Chan K.M., Delfert D., Junger K.D. A direct colorimetric assay for Ca2+-stimulated ATPase activity. Anal. Biochem. 1986, 157:375-380.
11. Chan K.Y., Li C.K., Lai C.K., Ng S.F., Chan A.Y. Infantile isolated sulphite oxidase deficiency in a Chinese family: a rare neurodegenerative disorder. Hong Kong Med. J. 2002, 8:279-282.
12. Chapman K. Sulfite-containing pharmaceuticals. Can. Med. Assoc. J. 1993, 148:714.
13. 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, 23:123-132.
14. da Silva C.G., et al. Inhibition of cytochrome c oxidase activity in rat cerebral cortex and human skeletal muscle by d-2-hydroxyglutaric acid in vitro. Biochim. Biophys. Acta 2002, 1586:81-91.
15. da Silva C.G., et al. Inhibition of creatine kinase activity from rat cerebral cortex by d-2-hydroxyglutaric acid in vitro. Neurochem. Int. 2004, 44:45-52.
16. Derin N., Yargiçoǧlu P., Aslan M., Elmas O., Agar A., Aicigüzel Y. The effect of sulfite and chronic restraint stress on brain lipid peroxidation and anti-oxidant enzyme activities. Toxicol. Ind. Health 2006, 22:233-240.
17. Derin N., Akpinar D., Yargicoglu P., Agar A., Aslan M. Effect of alpha-lipoic acid on visual evoked potentials in rats exposed to sulfite. Neurotoxicol. Teratol. 2009, 31:34-39.
18. Du F., Cooper A., Lukas S.E., Cohen B.M., Ongur D. Creatine kinase and ATP synthase reaction rates in human frontal lobe measured by (31)P magnetization transfer spectroscopy at 4T. Magn. Reson. Imaging 2013, 31:102-108.
19. Edwards M.C., et al. Isolated sulfite oxidase deficiency: review of two cases in one family. Ophthalmology 1999, 106:1957-1961.
20. Eichler F., Tan W.H., Shih V.E., Grant P.E., Krishnamoorthy K. Proton magnetic resonance spectroscopy and diffusion-weighted imaging in isolated sulfite oxidase deficiency. J. Child Neurol. 2006, 21:801-805.
21. Fischer J.C., et al. Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin. Chim. Acta 1985, 153:23-36.
22. Galano A. On the direct scavenging activity of melatonin towards hydroxyl and a series of peroxyl radicals. Phys. Chem. Chem. Phys. 2011, 13:7178-7188.
23. Gardner P.R., Nguyen D.D., White C.W. Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:12248-12252.
24. Gardner P.R., Costantino G., Szabo C., Salzman A.L. Nitric oxide sensitivity of the aconitases. J. Biol. Chem. 1997, 272:25071-25076.
25. Halliwell B., Gutteridge J.M.C. Measurement of Reactive Species 2007, Oxford University Press, Oxford. 4th ed.
26. Hayatsu H. Bisulfite modification of nucleic acids and their constituents. Prog. Nucleic Acid Res. Mol. Biol. 1976, 16:75-124.
27. Hayatsu H., Miller R.C. The cleavage of DNA by the oxygen-dependent reaction of bisulfite. Biochem. Biophys. Res. Commun. 1972, 46:120-124.
28. - radicals. J. Am. Chem. Soc. 1972, 94:47-57.
29. Hegg D.A., Hobbs P.V. Oxidation of sulfur dioxide in aqueous systems with particular reference to the atmosphere. Atmos. Environ. 1978, 12:241-253.
30. Herken E.N., Kocamaz E., Erel O., Celik H., Kucukatay V. Effect of sulfite treatment on total antioxidant capacity, total oxidant status, lipid hydroperoxide, and total free sulfydryl groups contents in normal and sulfite oxidase-deficient rat plasma. Cell Biol. Toxicol. 2009, 25:355-362.
31. Hughes B.P. A method for estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathological sera. Clin. Chim. Acta 1962, 7:597-603.
32. Johnson J.L. Prenatal diagnosis of molybdenum cofactor deficiency and isolated sulfite oxidase deficiency. Prenat. Diagn. 2003, 23:6-8.
33. Johnson J.L., Duran M. Molybdenum Cofactor Deficiency and Isolated Sulfite Oxidase Deficiency. The Metabolic and Molecular Bases of Inherited Disease 2001, 3181-3217. McGraw-Hill, New York. C.R. Scriver, A.L. Beaudet, D. Valle, W.S. Sly (Eds.).
34. Jones D.H., Matus A.I. Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation. Biochim. Biophys. Acta 1974, 356:276-287.
35. Kencebay C., et al. Merit of quinacrine in the decrease of ingested sulfite-induced toxic action in rat brain. Food Chem. Toxicol. 2013, 52:129-136.
36. 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, 61:341-346.
37. Konorev E.A., Hogg N., Kalyanaraman B. Rapid and irreversible inhibition of creatine kinase by peroxynitrite. FEBS Lett. 1998, 427:171-174.
38. Küçükatay V., Savcioǧlu F., Hacioǧlu G., Yargiçoǧlu P., Aǧar A. Effect of sulfite on cognitive function in normal and sulfite oxidase deficient rats. Neurotoxicol. Teratol. 2005, 27:47-54.
39. LeBel C.P., Ischiropoulos H., Bondy S.C. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 1992, 5:227-231.
40. Li C., et al. Hydrogen peroxide targets the cysteine at the active site and irreversibly inactivates creatine kinase. Int. J. Biol. Macromol. 2011, 49:910-916.
41. Liang L.P., Waldbaum S., Rowley S., Huang T.T., Day B.J., Patel M. Mitochondrial oxidative stress and epilepsy in SOD2 deficient mice: attenuation by a lipophilic metalloporphyrin. Neurobiol. Dis. 2012, 45:1068-1076.
42. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
43. Morrison J.F. The activation of aconitase by ferrous ions and reducing agents. Biochem. J. 1954, 58:685-692.
44. Mottley C., Mason R.P. Sulfate anion free radical formation by the peroxidation of (Bi)sulfite and its reaction with hydroxyl radical scavengers. Arch. Biochem. Biophys. 1988, 267:681-689.
45. Myers C.R., Antholine W.E., Myers J.M. The pro-oxidant chromium(VI) inhibits mitochondrial complex I, complex II, and aconitase in the bronchial epithelium: EPR markers for Fe-S proteins. Free Radic. Biol. Med. 2010, 49:1903-1915.
46. Ngu L.H., Afroze B., Chen B.C., Affandi O., Zabedah M.Y. Molybdenum cofactor deficiency in a Malaysian child. Singapore Med. J. 2009, 50:e365-e367.
47. Ozturk O.H., Oktar S., Aydin M., Kucukatay V. Effect of sulfite on antioxidant enzymes and lipid peroxidation in normal and sulfite oxidase-deficient rat erythrocytes. J. Physiol. Biochem. 2010, 66:205-212.
48. Patel M. Mitochondrial dysfunction and oxidative stress: cause and consequence of epileptic seizures. Free Radic. Biol. Med. 2004, 37:1951-1962.
49. Peiser G.D., Yang S.F. Sulfite-mediated destruction of β-carotene. J. Agric. Food Chem. 1979, 27:446-449.
50. Ramirez O., Jimenez E. Opposite transitions of chick brain catalytically active cytosolic creatine kinase isoenzymes during development. Int. J. Dev. Neurosci. 2000, 18:815-823.
51. Reiter R.J., Tan D.X., Manchester L.C., Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem. Biophys. 2001, 34:237-256.
52. Rosenthal R.E., Hamud F., Fiskum G., Varghese P.J., Sharpe S. Cerebral ischemia and reperfusion - prevention of brain mitochondrial injury by lidoflazine. J. Cereb. Blood Flow Metab. 1987, 7:752-758.
53. Rustin P., et al. Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta 1994, 228:35-51.
54. Sass J.O., et al. Functional deficiencies of sulfite oxidase: differential diagnoses in neonates presenting with intractable seizures and cystic encephalomalacia. Brain Dev. 2010, 32:544-549.
55. Schapira A.H.V., et al. Anatomic and disease specificity of NADH CoQ1 reductase (Complex I) deficiency in Parkinson's disease. J. Neurochem. 1990, 55:2142-2145.
56. Schuierer G., Kurlemann G., Bick U., Stephani U. Molybdenum-cofactor deficiency: CT and MR findings. Neuropediatrics 1995, 26:51-54.
57. Shi X., Mao Y. 8-Hydroxy-2'-deoxyguanosine formation and DNA damage induced by sulfur trioxide anion radicals. Biochem. Biophys. Res. Commun. 1994, 205:141-147.
58. Slot H.M., et al. Molybdenum-cofactor deficiency: an easily missed cause of neonatal convulsions. Neuropediatrics 1993, 24:139-142.
59. Southerland W.M., Akogyeram C.O., Toghrol F., Sloan L., Scherrer R. Interaction of bisulfite with unsaturated fatty acids. J. Toxicol. Environ. Health 1982, 10:479-491.
60. Stachowiak O., Dolder M., Wallimann T., Richter C. Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J. Biol. Chem. 1998, 273:16694-16699.
61. Tamura H., et al. Melatonin as a free radical scavenger in the ovarian follicle. Endocr. J. 2013, 60:1-13.
62. Tan W.H., et al. Isolated sulfite oxidase deficiency: a case report with a novel mutation and review of the literature. Pediatrics 2005, 116:757-766.
63. 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.
64. Vasquez-Vivar J., Kalyanaraman B., Kennedy M.C. Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J. Biol. Chem. 2000, 275:14064-14069.
65. Vijayakumar K., et al. Clinical neuroimaging features and outcome in molybdenum cofactor deficiency. Pediatr. Neurol. 2011, 45:246-252.
66. Vincent A.S., et al. Sulfite-mediated oxidative stress in kidney cells. Kidney Int. 2004, 65:393-402.
67. Wallimann T., et al. Creatine kinase: an enzyme with a central role in cellular energy metabolism. MAGMA 1998, 6:116-119.
68. Wang P.F., McLeish M.J., Kneen M.M., Lee G., Kenyon G.L. An unusually low pK(a) for Cys282 in the active site of human muscle creatine kinase. Biochemistry 2001, 40:11698-11705.
69. Wendt S., Schlattner U., Wallimann T. Differential effects of peroxynitrite on human mitochondrial creatine kinase isoenzymes. Inactivation, octamer destabilization, and identification of involved residues. J. Biol. Chem. 2003, 278:1125-1130.
70. Wolosker H., Panizzutti R., Engelender S. Inhibition of creatine kinase by S-nitrosoglutathione. FEBS Lett. 1996, 392:274-276.
71. 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, 305:619-623.
72. Wyse A.T., Brusque A.M., Silva C.G., Streck E.L., Wajner M., Wannmacher C.M. Inhibition of Na+, K+-ATPase from rat brain cortex by propionic acid. Neuroreport 1998, 9:1719-1721.
73. Yang S.F. Destruction of tryptophan during the aerobic oxidation of sulfite ions. Environ. Res. 1973, 6:395-402.
74. Zhang X., Vincent A.S., Halliwell B., Wong K.P. A mechanism of sulfite neurotoxicity: direct inhibition of glutamate dehydrogenase. J. Biol. Chem. 2004, 279:43035-43045.