Disruption of redox homeostasis and brain damage caused in vivo by methylmalonic acid and ammonia in cerebral cortex and striatum of developing rats

Free Radical Research

Volumn 48, Issue 6, 2014, Pages 659-669

  Viegas, C M ^a   Zanatta, A ^a   Grings, M ^a   Hickmann, F H ^a   Monteiro, W O ^a   Soares, L E ^a   Sitta, A ^b   Leipnitz, G ^a   De Oliveira, F H ^b   Wajner, M ^a,b  

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

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

Hyperammonemia; Inherited metabolic disease; Methylmalonic acidemia; Propionic acidemia

Indexed keywords

AMMONIA; ANTIOXIDANT; CATALASE; DICHLOROFLUORESCEIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; METHYLMALONIC ACID; N(G) NITROARGININE METHYL ESTER; NITRATE; NITRITE; PROPIONIC ACID; SUPEROXIDE DISMUTASE; THIOL DERIVATIVE; UREASE; 2',7'-DICHLORODIHYDROFLUORESCEIN; FLUORESCEIN DERIVATIVE; NITRIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DAMAGE; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; HISTOPATHOLOGY; HYPERAMMONEMIA; MALE; METHYLMALONIC ACIDEMIA; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; PROPIONIC ACIDEMIA; RAT; WISTAR RAT; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; HOMEOSTASIS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; TOXICITY;

AMMONIA; ANIMALS; ANTIOXIDANTS; CATALASE; CEREBRAL CORTEX; CORPUS STRIATUM; FLUORESCEINS; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HOMEOSTASIS; HYPERAMMONEMIA; INFUSIONS, INTRAVENTRICULAR; MALE; METHYLMALONIC ACID; NG-NITROARGININE METHYL ESTER; NITRATES; NITRITES; OXIDATION-REDUCTION; RATS; RATS, WISTAR; SULFHYDRYL COMPOUNDS; SUPEROXIDE DISMUTASE; UREASE;

EID: 84899945977     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.898842     Document Type: Article

References (76)

1. Fenton WA, Gravel RA, Ronenblatt DS. Disorders of propion-Ate and methylmalonate metabolism. In: Scriver C, Beuadet A, Valle A, Sky W (eds.). The metabolic and molecular bases of inherited disease. New York: McGraw-Hill Inc; 2001.
2. Pena L, Burton BK. Survey of health status and complications among propionic acidemia patients. Am J Med Genet A 2012;158A:1641-1646.
3. Roodhooft AM, Baumgartner ER, Martin JJ, Blom W, Van Acker KJ. Symmetrical necrosis of the basal ganglia in methylmalonic acidaemia. Eur J Pediatr. 1990;149:582-584.
4. O'Shea CJ, Sloan JL, Wiggs EA, Pao M, Gropman A, Baker EH, et al. Neurocognitive phenotype of isolated meth-ylmalonic acidemia. Pediatrics 2012;129:e1541-1551.
5. Brismar J, Ozand PT. CT and MR of the brain in disorders of the propionate and methylmalonate metabolism. AJNR Am J Neuroradiol 1994;15:1459-1473.
6. Baumgarter ER, Viardot C. Long-term follow-up of 77patients with isolated methylmalonic acidaemia. J Inherit Metab Dis 1995;18:138-142.
7. Leonard JV. The management and outcome of propionic and methylmalonic acidaemia. J Inherit Metab Dis 1995;18: 430-434.
8. Hörster F, Hoffmann GF. Pathophysiology, diagnosis, and treatment of methylmalonic aciduria-recent advances and new challenges. Pediatr Nephrol 2004;19:1071-1074.
9. Haas RH, Marsden DL, Capistrano-Estrada S, Hamilton R, Grafe MR, Wong W, Nyhan WL. Acute basal ganglia infarction in propionic acidemia. J Child Neurol 1995;10:18-22.
10. Deodato F, Boenzi S, Santorelli FM, Dionisi-Vici C. Methylmalonic and propionic aciduria. Am J Med Genet C Semin Med Genet 2006;142C: 104-112.
11. Haberlandt E, Canestrini C, Brunner-Krainz M, Möslinger D, Mussner K, Plecko B, et al. Epilepsy in patients with propionic acidemia. Neuropediatrics 2009;40:120-125.
12. Broomfield A, Gunny R, Prabhakar P, Grunewald S. Spontaneous rapid resolution of acute basal ganglia changes in an untreated infant with propionic acidemia: a clue to pathogenesis? Neuropediatrics 2010;41:256-260.
13. Schreiber J, Chapman KA, Summar ML, Ah Mew N, Sutton VR, MacLeod E, et al. Neurologic considerations in propionic acidemia. Mol Genet Metab 2012;105:10-15.
14. de Mello CF, Begnini J, Jiménez-Bernal RE, Rubin MA, de Bastiani J, da Costa E, Wajner M. Intrastriatal methylmalonic acid administration induces rotational behavior and convulsions through glutamatergic mechanisms. Brain Res 1996;721:120-125.
15. Fighera MR, Bonini JS, de Oliveira TG, Frussa-Filho R, Rocha JB, Dutra-Filho CS, et al. GM1 ganglioside attenuates convulsions and thiobarbituric acid reactive substances production induced by the intrastriatal injection of methylmalonic acid. Int J Biochem Cell Biol 2003;35:465-473.
16. Malfatti CR, Royes LF, Francescato L, Sanabria ER, Rubin MA, Cavalheiro EA, Mello CF. Intrastriatal methylmalonic acid administration induces convulsions and TBARS production, and alters Na +, K+-ATPase activity in the rat striatum and cerebral cortex. Epilepsia 2003;44:761-767.
17. Ribeiro MC, de Avila DS, Schneider CY, Hermes FS, Furian AF, Oliveira MS, et al. alpha-Tocopherol protects against pentylenetetrazol-And methylmalonate-induced convulsions. Epilepsy Res 2005;66:185-194.
18. Royes LF, Fighera MR, Furian AF, Oliveira MS, da Silva LG, Malfatti CR, et al. Creatine protects against the convulsive behavior and lactate production elicited by the intrastriatal injection of methylmalonate. Neuroscience 2003;118:1079-1090.
19. Royes LF, Fighera MR, Furian AF, Oliveira MS, Fiorenza NG, de Carvalho Myskiw J, et al. Involvement of NO in the convulsive behavior and oxidative damage induced by the intrastriatal injection of methylmalonate. Neurosci Lett 2005;376:116-120.
20. Royes LF, Fighera MR, Furian AF, Oliveira MS, Myskiw JEC, Fiorenza NG, et al. Eff ectiveness of creatine monohydrate on seizures and oxidative damage induced by methylmalonate. Pharmacol Biochem Behav 2006;83:136-144.
21. Furian AF, Fighera MR, Oliveira MS, Ferreira AP, Fiorenza NG, de Carvalho Myskiw J, et al. Methylene blue prevents methylmalonate-induced seizures and oxidative damage in rat striatum. Neurochem Int 2007;50:164-171.
22. Fernandes CG, Borges CG, Seminotti B, Amaral AU, Knebel LA, Eichler P, et al. Experimental evidence that methylmalonic acid provokes oxidative damage and compromises antioxidant defenses in nerve terminal and striatum of young rats. Cell Mol Neurobiol 2011;31:775-785.
23. Rigo FK, Pasquetti L, Malfatti CR, Fighera MR, Coelho RC, Petri CZ, Mello CF. Propionic acid induces convulsions and protein carbonylation in rats. Neurosci Lett 2006;408:151-154.
24. Wajner M, Goodman SI. Disruption of mitochondrial homeostasis in organic acidurias: insights from human and animal studies. J Bioenerg Biomembr 2011;43:31-38.
25. Brusque AM, Mello CF, Buchanan DN, Terracciano ST, Rocha MP, Vargas CR, et al. Eff ect of chemically induced propionic acidemia on neurobehavioral development of rats. Pharmacol Biochem Behav 1999;64:529-534.
26. de Mello CF, Rubin MA, Coelho J, Wajner M, Souza DO. Eff ects of methylmalonate and propionate on [3H] glutamate binding, adenylate cyclase activity and lipid synthesis in rat cerebral cortex. Biochem Mol Biol Int 1997; 42:1143-1150.
27. Treacy E, Arbour L, Chessex P, Graham G, Kasprzak L, Casey K, et al. Glutathione defi ciency as a complication of methylmalonic acidemia: response to high doses of ascorbate. J Pediatr 1996;129:445-448.
28. Treacy E, Clow C, Mamer OA, Scriver CR. Methylmalonic acidemia with a severe chemical but benign clinical pheno-type. J Pediatr 1993;122:428-429.
29. Richard E, Monteoliva L, Juarez S, Pérez B, Desviat LR, Ugarte M, Albar JP. Quantitative analysis of mitochondrial protein expression in methylmalonic acidemia by two-dimensional diff erence gel electrophoresis. J Proteome Res 2006;5:1602-1610.
30. Richard E, Jorge-Finnigan A, Garcia-Villoria J, Merinero B, Desviat LR, Gort L, et al. Genetic and cellular studies of oxi-dative stress in methylmalonic aciduria (MMA) cobalamin defi ciency type C (cblC) with homocystinuria (MMACHC). Hum Mutat 2009;30:1558-1566.
31. Ribas GS, Manfredini V, de Mari JF, Wayhs CY, Vanzin CS, Biancini GB, et al. Reduction of lipid and protein damage in patients with disorders of propionate metabolism under treatment: a possible protective role of L-carnitine supplementation. Int J Dev Neurosci 2010;28:127-132.
32. Ribas GS, Biancini GB, Mescka C, Wayhs CY, Sitta A, Wajner M, Vargas CR. Oxidative stress parameters in urine from patients with disorders of propionate metabolism: a benefi cial eff ect of L:-carnitine supplementation. Cell Mol Neurobiol 2012;32:77-82.
33. Pinar-Sueiro S, Martínez-Fernández R, Lage-Medina S, Aldamiz-Echevarria L, Vecino E. Optic neuropathy in meth-ylmalonic acidemia: the role of neuroprotection. J Inherit Metab Dis 2010;33 Suppl 3:S199-203.
34. Batshaw ML, Thomas GH, Cohen SR, Matalon R, Mahoney MJ. Treatment of the cbl B form of methylmalonic acidaemia with adenosylcobalamin. J Inherit Metab Dis 1984; 7:65-68.
35. Chandler RJ, Zerfas PM, Shanske S, Sloan J, Hoffmann V, DiMauro S, Venditti CP. Mitochondrial dysfunction in mut methylmalonic acidemia. FASEB J 2009;23:1252-1261.
36. Fontella FU, Pulrolnik V, Gassen E, Wannmacher CM, Klein AB, Wajner M, Dutra-Filho CS. Propionic and L-methylmalonic acids induce oxidative stress in brain of young rats. Neuroreport 2000;11:541-544.
37. Fragaki K, Cano A, Benoist JF, Rigal O, Chaussenot A, Rouzier C, et al. Fatal heart failure associated with CoQ10 and multiple OXPHOS defi ciency in a child with propionic acidemia. Mitochondrion 2011;11:533-536.
38. Gallego-Villar L, Pérez-Cerdá C, Pérez B, Abia D, Ugarte M, Richard E, Desviat LR. Functional characterization of novel genotypes and cellular oxidative stress studies in propionic acidemia. J Inherit Metab Dis 2013;36:731-740.
39. Nakao S, Moriya Y, Furuyama S, Niederman R, Sugiya H. Propionic acid stimulates superoxide generation in human neutrophils. Cell Biol Int 1998;22:331-337.
40. Filipowicz HR, Ernst SL, Ashurst CL, Pasquali M, Longo N. Metabolic changes associated with hyperammonemia in patients with propionic acidemia. Mol Genet Metab 2006; 88: 123-130.
41. Chapman KA, Gropman A, MacLeod E, Stagni K, Summar ML, Ueda K, et al. Acute management of propionic acidemia. Mol Genet Metab 2012;105:16-25.
42. Leonard JV, Walter JH, McKiernan PJ. The management of organic acidaemias: the role of transplantation. J Inherit Metab Dis 2001;24:309-311.
43. Zwickler T, Haege G, Riderer A, Hörster F, Hoffmann GF, Burgard P, Kölker S. Metabolic decompensation in methylmalonic aciduria: which biochemical parameters are discriminative? J Inherit Metab Dis 2012;35:797-806.
44. Diemer NH, Laursen H. Glial cell reactions in rats with hyper-Ammoniemia induced by urease or porto-caval anastomosis. Acta Neurol Scand 1977;55:425-442.
45. Viegas CM, Tonin AM, Zanatta A, Seminotti B, Busanello EN, Fernandes CG, et al. Impairment of brain redox homeostasis caused by the major metabolites accumulating in hyperornithinemia-hyperammonemia-homocitrullinuria syndrome in vivo. Metab Brain Dis 2012;27:521-530.
46. Viegas CM, Busanello EN, Tonin AM, de Moura AP, Grings M, Ritter L, et al. Dual mechanism of brain damage induced in vivo by the major metabolites accumulating in hyperornithinemia-hyperammonemia-homocitrullinuria syndrome. Brain Res 2011;1369:235-244.
47. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. San Diego: Academic Press; 1986.
48. Sweetman L. Organic acid analyses. In: Hommes FA (ed.). Techniques in Diagnostic Human Biochemical Genetics: A Laboratory Manual, 1st ed. New York: Wiley-Liss; 1991. p. 143.
49. Wajner M, Coelho DEM, Ingrassia R, de Oliveira AB, Busanello EN, Raymond K, et al. Selective screening for organic acidemias by urine organic acid GC-MS analysis in Brazil: fi fteen-year exper ience. Clin Chim Acta 2009; 400: 77-81.
50. Evelson P, Travacio M, Repetto M, Escobar J, Llesuy S, Lissi EA. Evaluation of total reactive antioxidant potential (TRAP) of tissue homogenates and their cytosols. Arch Bio-chem Biophys 2001;388:261-266.
51. Browne RW, Armstrong D. Reduced glutathione and glutath-ione disulfide. Methods Mol Biol 1998;108:347-352.
52. Aksenov MY, Markesber y WR. Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer's disease. Neurosci Lett 2001;302:141-145.
53. Navarro-Gonzálvez JA, García-Benayas C, Arenas J. Semiau-tomated measurement of nitrate in biological fluids. Clin Chem 1998;44:679-681.
54. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2 ́, 7́-dichlorofl uorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992;5:227-231.
55. Aebi H. Catalase in vitro. Methods Enzymol 1984;105: 121-126.
56. Marklund S. Pyrogallol autoxidation. In: Greenwald R (ed.). Handbook for Oxygen Radical Research, 1st ed. Boca Raton, FL: CRC Press; 1985. pp. 243-247.
57. Wendel A. Glutathione peroxidase. Methods Enzymol 1981;77:325-333.
58. Carlberg I, Mannervik B. Glutathione reductase. Methods Enzymol 1985;113:484-490.
59. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
60. Butterworth RF, Norenberg MD, Felipo V, Ferenci P, Albrecht J, Blei AT, et al. Experimental models of hepatic encephalopathy: ISHEN guidelines. Liver Int 2009;29: 783-788.
61. Chen CY, Tsai TC, Lee WJ, Chen HC. Continuous hemodia-fi ltration in the treatment of hyperammonemia due to methyl-malonic acidemia. Ren Fail 2007;29:751-754.
62. Halliwell B, Gutteridge J. Measurement of reactive species. In: Halliwell B, Gutteridge J, (eds). Free Radicals in Biology and Medicine. Oxford: Oxford University Press; 2007. pp. 268-340.
63. Hansen RE, Roth D, Winther JR. Quantifying the global cellular thiol-disulfi de status. Proc Natl Acad Sci U S A 2009;106:422-427.
64. Thomas JA, Poland B, Honzatko R. Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch Biochem Biophys 1995;319:1-9.
65. Requejo R, Hurd TR, Costa NJ, Murphy MP. Cysteine residues exposed on protein surfaces are the dominant intramito-chondrial thiol and may protect against oxidative damage. FEBS J 2010;277:1465-1480.
66. Brusque AM, Rotta LN, Tavares RG, Emanuelli T, Schwarzbold CV, Dutra-Filho CS, et al. Eff ects of methylmalonic and propi-onic acids on glutamate uptake by synaptosomes and synaptic vesicles and on glutamate release by synaptosomes from cerebral cortex of rats. Brain Res 2001;920:194-201.
67. Kölker S, Ahlemeyer B, Krieglstein J, Hoffmann GF. Methyl-malonic acid induces excitotoxic neuronal damage in vitro. J Inherit Metab Dis 2000;23:355-358.
68. Okun JG, Hörster F, Farkas LM, Feyh P, Hinz A, Sauer S, et al. Neurodegeneration in methylmalonic aciduria involves inhibition of complex II and the tricarboxylic acid cycle, and synergistically acting excitotoxicity. J Biol Chem 2002;277: 14674-14680.
69. Braissant O, McLin VA, Cudalbu C. Ammonia toxicity to the brain. J Inherit Metab Dis 2013;36:595-612.
70. Ribeiro LR, Fighera MR, Oliveira MS, Furian AF, Rambo LM, Ferreira AP, et al. Methylmalonate-induced seizures are attenuated in inducible nitric oxide synthase knockout mice. Int J Dev Neurosci 2009;27:157-163.
71. Royes LF, Fighera MR, Furian AF, Oliveira MS, Fiorenza NG, Petry JC, et al. The role of nitric oxide on the convulsive behavior and oxidative stress induced by methylmalonate: an electroencephalographic and neurochemical study. Epilepsy Res 2007;73:228-237.
72. Halliwell B, Gutteridge JM. The defi nition and measurement of antioxidants in biological systems. Free Radic Biol Med 1995;18:125-126.
73. Felipo V, Butterworth RF. Neurobiology of ammonia. Prog Neurobiol 2002;67:259-279.
74. Lai JC, Cooper AJ. Brain alpha-ketoglutarate dehydrogenase complex: kinetic properties, regional distribution, and eff ects of inhibitors. J Neurochem 1986;47:1376-1386.
75. Kosenko E, Kaminsky Y, Stavroskaya IG, Felipo V. Alteration of mitochondrial calcium homeostasis by ammonia-induced activation of NMDA receptors in rat brain in vivo. Brain Res 2000;880:139-146.
76. Ribas GS, Manfredini V, de Marco MG, Vieira RB, Wayhs CY, Vanzin CS, et al. Prevention by L-carnitine of DNA damage induced by propionic and L-methylmalonic acids in human peripheral leukocytes in vitro. Mutat Res 2010;702:123-128.