Disturbance of redox homeostasis by ornithine and homocitrulline in rat cerebellum: A possible mechanism of cerebellar dysfunction in HHH syndrome

Life Sciences

Volumn 93, Issue 4, 2013, Pages 161-168

  Zanatta, Ângela ^a   Viegas, Carolina Maso ^a   Tonin, Anelise Miotti ^a   Busanello, Estela Natacha Brandt ^a   Grings, Mateus ^a   Moura, Alana Pimentel ^a   Leipnitz, Guilhian ^a   Wajner, Moacir ^a,b  

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

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

Cerebellum; Homocitrulline; Hyperornithinemia hyperammonemia homocitrullinuria syndrome; Ornithine; Oxidative stress

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM); CREATINE KINASE; CYTOCHROME C OXIDASE; GLUTATHIONE; HOMOCITRULLINE; HYDROGEN PEROXIDE; MELATONIN; NITRATE; NITRITE; ORNITHINE; OXOGLUTARATE DEHYDROGENASE; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATAXIA; BRAIN DYSFUNCTION; CEREBELLUM; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVITY; HOMEOSTASIS; HYPERORNITHINEMIA HYPERAMMONEMIA HOMOCITRULLINURIA SYNDROME; LIPID OXIDATION; LIPID PEROXIDATION; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN DETERMINATION; RAT; RESPIRATORY CHAIN; SYNAPTIC MEMBRANE;

CEREBELLUM; HOMOCITRULLINE; HYPERORNITHINEMIA-HYPERAMMONEMIA-HOMOCITRULLINURIA SYNDROME; ORNITHINE; OXIDATIVE STRESS;

ACONITATE HYDRATASE; ANIMALS; CEREBELLUM; CITRULLINE; CREATINE KINASE; ELECTRON TRANSPORT; GLUTATHIONE; HOMEOSTASIS; HYDROGEN PEROXIDE; HYPERAMMONEMIA; KETOGLUTARATE DEHYDROGENASE COMPLEX; NERVE TISSUE PROTEINS; NITRATES; NITRITES; ORNITHINE; OXIDATION-REDUCTION; RATS; RATS, WISTAR; SODIUM-POTASSIUM-EXCHANGING ATPASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; UREA CYCLE DISORDERS, INBORN;

RATTUS;

EID: 84880266905     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2013.06.013     Document Type: Article

References (53)

1. M.Y. Aksenov, and W.R. Markesbery Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer's disease Neurosci Lett 302 2001 141 145
2. A.U. Amaral, G. Leipnitz, C.G. Fernandes, B. Seminotti, A. Zanatta, and C.M. Viegas Evidence that the major metabolites accumulating in hyperornithinemia-hyperammonemia-homocitrullinuria syndrome induce oxidative stress in brain of young rats Int J Dev Neurosci 7 2009 635 641
3. O. Braissant Current concepts in the pathogenesis of urea cycle disorders Mol Genet Metab 100 Suppl. 1 2010 S3 S12
4. R.W. Browne, and D. Armstrong Reduced glutathione and glutathione disulfide Methods Mol. Biol. 108 1998 347 352
5. J.A. Camacho, C. Obie, B. Biery, B.K. Goodman, C.A. Hu, and S. Almashanu Hyperornithinaemia-hyperammonaemia-homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter Nat Genet 2 1999 151 158
6. 2 +-stimulated ATPase activity Anal Biochem 157 1986 375 380
7. C.G. da Silva, C.A. Ribeiro, G. Leipnitz, C.S. Dutra-Filho, A.T.A.T. Wyse, and C.M. Wannmacher Inhibition of cytochrome c oxidase activity in rat cerebral cortex and human skeletal muscle by D-2-hydroxyglutaric acid in vitro Biochim Biophys Acta 1586 2002 81 91
8. H. Esterbauer, and K.H. Cheeseman Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal Methods Enzymol 186 1990 407 421
9. P. Evelson, M. Travacio, M. Repetto, J. Escobar, S. Llesuy, and E.A. Lissi Evaluation of total reactive antioxidant potential (TRAP) of tissue homogenates and their cytosol Arch Biochem Biophys 388 2001 261 266
10. G. Fiermonte, V. Dolce, L. David, F.M. Santorelli, C. Dionisi-Vici, and F. Palmieri The mitochondrial ornithine transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms J Biol Chem 278 2003 32778 32783
11. M. Filosto, A. Alberici, A. Tessa, A. Padovani, and F.M. Santorelli Hyperornithinemia-hyperammonemia-homocitrullinuria (HHH) syndrome in adulthood: a rare recognizable condition Neurol Sci 2012 [Epub ahead of print]
12. J.C. Fischer, W. Ruitenbeek, J.A. Berden, J.M. Trijbels, J.H. Veerkamp, and M. Stadhouders Differential investigation of the capacity of succinate oxidation in human skeletal muscle Clin Chim Acta 153 1985 23 36
13. P.R. Gardner, G. Costantino, C. Szabó, and A.L. Salzman Nitric oxide sensitivity of the aconitases J Biol Chem 272 1997 25071 25076
14. A. Gropman Brain imaging in urea cycle disorders Mol Genet Metab 100 2010 S20 S30
15. A.L. Gropman, and M.L. Batshaw Cognitive outcome in urea cycle disorders Mol Genet Metab 81 2004 S58 S62
16. B. Halliwell, and J.M.C. Gutteridge Cellular responses to oxidative stress: adaptation, damage, repair, senescence and death B. Halliwell, J.M.C. Gutteridge, Free radicals in biology and medicine 2007 Oxford University Press Oxford 187 267
17. R.E. Hansen, and J.R. Winther An introduction to methods for analyzing thiols and disulfides: reactions, reagents, and practical considerations Anal Biochem 394 2009 147 158
18. B.P. Hughes A method for the estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathological sera Clin Chim Acta 7 1962 597 603
19. D.H. Jones, and A.I. Matus Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation Biochim Biophys Acta 356 1974 276 287
20. S.Z. Kim, W.J. Song, W.L. Nyhan, C. Ficicioglu, and R. Mandell Shih VE Long-term follow-up of four patients affected by HHH syndrome Clin Chim Acta 413 2012 1151 1155
21. S.H. Korman, N. Kanazawa, B. Abu-Libdeh, A. Gutman, and S. Tsujino Hyperornithinemia, hyperammonemia, and homocitrullinuria syndrome with evidence of mitochondrial dysfunction due to a novel SLC25A15 (ORNT1) gene mutation in a Palestinian family J Neurol Sci 218 2004 53 58
22. J.C. Lai, and A.J. Cooper Brain alpha-ketoglutarate dehydrogenase complex: kinetic properties, regional distribution, and effects of inhibitors J Neurochem 47 1986 1376 1386
23. G. Leipnitz, B. Seminotti, A.U. Amaral, G. de Bortoli, A. Solano, and P.F. Schuck Induction of oxidative stress by the metabolites accumulating in 3-methylglutaconic aciduria in cerebral cortex of young rats Life Sci 82 2008 652 662
24. L.P. Liang, Y.S. Ho, and M. Patel Mitochondrial superoxide production in kainate-induced hippocampal damage Neuroscience 101 2000 563 570
25. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
26. K.M. Miranda, M.G. Espey, and D.A. Wink A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite Nitric Oxide 5 2001 62 71
27. T. Miyamoto, N. Kanazawa, C. Hayakawa, and S. Tsujino A novel mutation, P126R, in a Japanese patient with HHH syndrome Pediatr Neurol 26 2002 65 67
28. J.G. Mohanty, J.S. Jaffe, E.S. Schulman, and D.G. Raible A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative J Immunol Methods 202 1997 133 141
29. J.F. Morrison The activation of aconitase by ferrous ions and reducing agents Biochem J 58 1954 685 692
30. A.P. Moura, C.A. Ribeiro, A. Zanatta, E.N. Busanello, A.M. Tonin, and M. Wajner 3-methylcrotonylglycine disrupts mitochondrial energy homeostasis and inhibits synaptic Na(+), K(+)-ATPase activity in brain of young rats Cell Mol Neurobiol 32 2012 297 307
31. C.R. Myers, W.E. Antholine, and J.M. Myers The pro-oxidant chromium(VI) inhibits mitochondrial complex I, complex II, and aconitase in the bronchialepithelium: EPR markers for Fe-S proteins Free Radic Biol Med 49 2010 1903 1915
32. F. Palmieri Diseases caused by defects of mitochondrial carriers: a review Biochim Biophys Acta 1777 2008 564 578
33. M. Patel, B.J. Day, J.D. Crapo, I. Fridovich, and J.O. McNamara Requirement for superoxide in excitotoxic cell death Neuron 16 1996 345 355
34. R. Requejo, E.T. Chouchani, T.R. Hurd, K.E. Menger, M.B. Hampton, and M.P. Murphy Measuring mitochondrial protein thiol redox state Methods Enzymol 474 2010 123 147
35. A.Z. Reznick, and L. Packer Oxidative damage to proteins: spectrophotometric method for carbonyl assay Methods Enzymol. 233 1994 357 363
36. C.A. Ribeiro, F.H. Hickmann, and M. Wajner Neurochemical evidence that 3-methylglutaric acid inhibits synaptic Na +, K +-ATPase activity probably through oxidative damage in brain cortex of young rats Int J Dev Neurosci 29 2011 1 7
37. R.E. Rosenthal, F. Hamud, G. Fiskum, P.J. Varghese, and S. Sharpe Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine J Cereb Blood Flow Metab 7 1987 752 758
38. P. Rustin, D. Chretien, T. Bourgeron, B. Gerard, A. Rotig, and J.M. Saudubray Biochemical and molecular investigations in respiratory chain deficiencies Clin Chim Acta 228 1994 35 51
39. A.H. Schapira, V.M. Mann, J.M. Cooper, D. Dexter, S.E. Daniel, and P. Jenner Anatomic and disease specificity of NADH CoQ1 reductase (complex I) deficiency in Parkinson's disease J Neurochem 55 1990 2142 2145
40. P.F. Schuck, G. Leipnitz, C.A. Ribeiro, K.B. Dalcin, D.R. Assis, and A.G. Barschak Inhibition of creatine kinase activity in vitro by ethylmalonic acid in cerebral cortex of young rats Neurochem Res 27 2002 1633 1639
41. M.V. Sofroniew, and H.V. Vinters Astrocytes: biology and pathology Acta Neuropathol 119 2010 7 35
42. S.R. Thomas, J. Neuzil, D. Mohr, and R. Stocker Coantioxidants make alpha-tocopherol an efficient antioxidant for low-density lipoprotein Am J Clin Nutr 62 1995 1357S 1364S
43. A.M. Tonin, M. Grings, L.A. Knebel, A. Zanatta, A.P. Moura, and C.A. Ribeiro Disruption of redox homeostasis in cerebral cortex of developing rats by acylcarnitines accumulating in medium-chain acyl-CoA dehydrogenase deficiency Int J Dev Neurosci 30 2012 383 390
44. L. Tretter, and V. Adam-Vizi Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of a-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress J Neurosci 20 2000 8972 8979
45. L. Tretter, and V. Adam-Vizi Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase J Neurosci 24 2004 7771 7778
46. L. Tretter, B. Liktor, and V. Adam-Vizi Dual effect of pyruvate in isolated nerve terminals: generation of reactive oxygen species and protection of aconitase Neurochem Res 10 2005 1331 1338
47. +)-stimulated ATPase and acetylcholinesterase activities of dog brain synaptosomal plasma membranes Biochem J 220 1984 301 307
48. S. Tsujino, N. Kanazawa, T. Ohashi, Y. Eto, T. Saito, and J. Kira Three novel mutations (G27E, insAAC, R179X) in the ORNT1 gene of Japanese patients with hyperornithinemia, hyperammonemia, and homocitrullinuria syndrome Ann Neurol 47 2000 625 631
49. M. Tuchman, B. Lee, U. Lichter-Konecki, M.L. Summar, M. Yudkoff, and S.D. Cederbaum Cross-sectional multicenter study of patients with urea cycle disorders in the United States Mol Genet Metab 94 2008 397 402
50. D. Valle, and O. Simell The hyperornithinemias C. Scriver, A. Beaudet, W. Sly, D. Valle, The metabolic and molecular bases of inherited disease 2001 McGraw New York 1147 1185
51. J. Vasquez-Vivar, B. Kalyanaraman, and M.C. Kennedy Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation J Biol Chem 275 2000 14064 14069
52. C.M. Viegas, A. Zanatta, L.A. Knebel, P.F. Schuck, A.M. Tonin, and C. Ferreira Gda Experimental evidence that ornithine and homocitrulline disrupt energy metabolism in brain of young rats Brain Res 1291 2009 102 112
53. C.M. Viegas, E.N. Busanello, A.M. Tonin, A.P. de Moura, M. Grings, and L. Ritter Dual mechanism of brain damage induced in vivo by the major metabolites accumulating in hyperornithinemia-hyperammonemia-homocitrullinuria syndrome Brain Res 1369 2011 235 244 Tecnológico Rio Grande do Sul Rio Grande do Sul Excitotoxicidade e Neuroproteção