Ethylmalonic acid induces permeability transition in isolated brain mitochondria

Neurotoxicity Research

Volumn 26, Issue 2, 2014, Pages 168-178

  Cecatto, Cristiane ^a   Amaral, Alexandre Umpierrez ^a   Leipnitz, Guilhian ^a   Castilho, Roger Frigério ^c   Wajner, Moacir ^a,b  

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

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Calcium; Ethylmalonic encephalopathy; Mitochondrial integrity; Redox balance; Short chain acyl CoA dehydrogenase deficiency

Indexed keywords

CALCIUM; ETHYLMALONIC ACID; HYDROGEN PEROXIDE; MALONIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; CENTRAL NERVOUS SYSTEM AGENTS; MALONIC ACID DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUCCINIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN CELL; BRAIN MITOCHONDRION; BRAIN SLICE; CALCIUM TRANSPORT; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORPUS STRIATUM; ENERGY METABOLISM; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION SWELLING; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RAT; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PERMEABILITY; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE; WISTAR RAT;

RATTUS;

ANIMALS; BRAIN; CALCIUM; CENTRAL NERVOUS SYSTEM AGENTS; CORPUS STRIATUM; HYDROGEN PEROXIDE; MALE; MALONATES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL SWELLING; NADP; OXIDATION-REDUCTION; PERMEABILITY; RATS, WISTAR; SUCCINIC ACID; TISSUE CULTURE TECHNIQUES;

EID: 84903815990     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-014-9460-5     Document Type: Article

References (69)

1. Adam-Vizi V, Starkov AA (2010) Calcium and mitochondrial reactive oxygen species generation: how to read the facts. J Alzheimers Dis 20(Suppl 2):S413-426. doi:10.3233/JAD-2010-100465
2. Akerman KE, Wikstrom MK (1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Lett 68(2):191-197
3. Amaral AU, Cecatto C, Busanello EN, Ribeiro CA, Melo DR, Leipnitz G, Castilho RF, Wajner M (2012) Ethylmalonic acid impairs brain mitochondrial succinate and malate transport. Mol Genet Metab 105(1):84-90. doi:10.1016/j.ymgme.2011.10.006
4. Amendt BA, Greene C, Sweetman L, Cloherty J, Shih V, Moon A, Teel L, Rhead WJ (1987) Short-chain acyl-coenzyme a dehydrogenase deficiency. Clinical and biochemical studies in two patients. J Clin Invest 79(5):1303-1309. doi:10.1172/JCI112953 (Pubitemid 17099630)
5. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434(7033):658-662. doi:10.1038/nature03434 (Pubitemid 40488559)
6. 2+ exchanger in excitotoxicity. Cell 120(2):275-285. doi:10.1016/j.cell.2004.11.049
7. Barschak AG, Ferreira Gda C, Andre KR, Schuck PF, Viegas CM, Tonin A, Dutra Filho CS, Wyse AT, Wannmacher CM, Vargas CR, Wajner M (2006) Inhibition of the electron transport chain and creatine kinase activity by ethylmalonic acid in human skeletal muscle. Metab Brain Dis 21(1):11-19. doi:10.1007/s11011-006- 9000-y (Pubitemid 43886889)
8. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, Bernardi P (2005) Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. J Biol Chem 280(19): 18558-18561. doi:10.1074/jbc.C500089200 (Pubitemid 41379552)
9. Belliere J, Devun F, Cottet-Rousselle C, Batandier C, Leverve X, Fontaine E (2012) Prerequisites for ubiquinone analogs to prevent mitochondrial permeability transition-induced cell death. J Bioenerg Biomembr 44(1):207-212. doi:10.1007/s10863-012-9406-7
10. Bernardi P (1992) Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 267(13):8834-8839
11. Bernardi P (2013) The mitochondrial permeability transition pore: a mystery solved? Front Physiol 4:95. doi:10.3389/fphys.2013.00095
12. Bernardi P, von Stockum S (2012) The permeability transition pore as a Ca(2+) release channel: new answers to an old question. Cell Calcium 52(1):22-27. doi:10.1016/j.ceca.2012.03.004
13. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
14. Brismar J, Ozand PT (1994) CT and MR of the brain in the diagnosis of organic acidemias. Experiences from 107 patients. Brain Dev 16(Suppl):104-124 (Pubitemid 124009023)
15. Brustovetsky N, Dubinsky JM (2000) Limitations of cyclosporin A inhibition of the permeability transition in CNS mitochondria. J Neurosci 20(22):8229-8237
16. Corydon MJ, Vockley J, Rinaldo P, Rhead WJ, Kjeldsen M, Winter V, Riggs C, Babovic-Vuksanovic D, Smeitink J, De Jong J, Levy H, Sewell AC, Roe C, Matern D, Dasouki M, Gregersen N (2001) Role of common gene variations in the molecular pathogenesis of shortchain acyl-CoA dehydrogenase deficiency. Pediatr Res 49(1): 18-23. doi:10.1203/00006450-200101000-00008 (Pubitemid 32014994)
17. Crompton M, Virji S, Doyle V, Johnson N, Ward JM (1999) The mitochondrial permeability transition pore. Biochem Soc Symp 66:167-179 (Pubitemid 129639031)
18. 2+-ATPase function. Neurochem Res 33(9):1749-1758. doi:10.1007/s11064-008-9619-7
19. Ferreira GC, Andre KR, Schuck PF, Viegas CM, Tonin A, Coelho Dde M, Wyse AT, Wannmacher CM, Vargas CR, Wajner M (2006) Effect of in vivo administration of ethylmalonic acid on energy metabolism in rat tissues. Metab Brain Dis 21(1):29-39. doi:10.1007/s11011-006-9004-7 (Pubitemid 43886891)
20. Figueira TR, Melo DR, Vercesi AE, Castilho RF (2012) Safranine as a fluorescent probe for the evaluation of mitochondrial membrane potential in isolated organelles and permeabilized cells. Methods Mol Biol 810:103-117. doi:10.1007/978-1-61779-382-0-7
21. Figueira TR, Barros MH, Camargo AA, Castilho RF, Ferreira JC, Kowaltowski AJ, Sluse FE, Souza-Pinto NC, Vercesi AE (2013) Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid Redox Signal 18(16):2029-2074. doi:10.1089/ars.2012.4729
22. Fiskum G, Murphy AN, Beal MF (1999) Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J Cereb Blood Flow Metab 19(4):351-369. doi:10.1097/00004647-199904000-00001 (Pubitemid 30161223)
23. Friberg H, Wieloch T (2002) Mitochondrial permeability transition in acute neurodegeneration. Biochimie 84(2-3):241-250
24. Garavaglia B, Colamaria V, Carrara F, Tonin P, Rimoldi M, Uziel G (1994) Muscle cytochrome c oxidase deficiency in two Italian patients with ethylmalonic aciduria and peculiar clinical phenotype. J Inherit Metab Dis 17(3):301-303 (Pubitemid 24239572)
25. Garcia-Silva MT, Ribes A, Campos Y, Garavaglia B, Arenas J (1997) Syndrome of encephalopathy, petechiae, and ethylmalonic aciduria. Pediatr Neurol 17(2):165-170 (Pubitemid 27465187)
26. Giordano C, Viscomi C, Orlandi M, Papoff P, Spalice A, Burlina A, Di Meo I, Tiranti V, Leuzzi V, d'Amati G, Zeviani M (2012) Morphologic evidence of diffuse vascular damage in human and in the experimental model of ethylmalonic encephalopathy. J Inherit Metab Dis 35(3):451-458. doi:10.1007/s10545-011-9408-3
27. Gregersen N, Winter VS, Corydon MJ, Corydon TJ, Rinaldo P, Ribes A, Martinez G, Bennett MJ, Vianey-Saban C, Bhala A, Hale DE, Lehnert W, Kmoch S, Roig M, Riudor E, Eiberg H, Andresen BS, Bross P, Bolund LA, Kolvraa S (1998) Identification of four new mutations in the short-chain acyl-CoA dehydrogenase (SCAD) gene in two patients: one of the variant alleles, 511C->T, is present at an unexpectedly high frequency in the general population, as was the case for 625G->A, together conferring susceptibility to ethylmalonic aciduria. Hum Mol Genet 7(4):619-627 (Pubitemid 28152260)
28. Kehrer JP, Lund LG (1994) Cellular reducing equivalents and oxidative stress. Free Radic Biol Med 17(1):65-75 (Pubitemid 24212712)
29. Kowaltowski AJ, Castilho RF, Vercesi AE (2001) Mitochondrial permeability transition and oxidative stress. FEBS Lett 495(1-2):12-15 (Pubitemid 32367965)
30. Kristal BS, Dubinsky JM (1997) Mitochondrial permeability transition in the central nervous system: induction by calcium cycling-dependent and -independent pathways. J Neurochem 69(2):524-538 (Pubitemid 27327953)
31. Leipnitz G, Schuck PF, Ribeiro CA, Dalcin KB, Assis DR, Barschak AG, Pulrolnik V, Wannmacher CM, Wyse AT, Wajner M (2003)
32. Ethylmalonic acid inhibits mitochondrial creatine kinase activity from cerebral cortex of young rats in vitro. Neurochem Res 28(5):771-777
33. Le-Quoc D, Le-Quoc K (1989) Relationships between the NAD(P) redox state, fatty acid oxidation, and inner membrane permeability in rat liver mitochondria. Arch Biochem Biophys 273(2):466-478 (Pubitemid 19222000)
34. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80(5):780-787 (Pubitemid 34809230)
35. 2+ and respiratory chain complex II inhibition. J Neurochem 90(5):1025-1035. doi:10.1111/j.1471-4159.2004.02565.x
36. Marshall D, Soliakov L, Redfern P, Wonnacott S (1996) Tetrodotoxin-sensitivity of nicotine-evoked dopamine release from rat striatum. Neuropharmacology 35(11):1531-1536 (Pubitemid 27026482)
37. Mirandola SR, Melo DR, Schuck PF, Ferreira GC, Wajner M, Castilho RF (2008) Methylmalonate inhibits succinate-supported oxygen consumption by interfering with mitochondrial succinate uptake. J Inherit Metab Dis 31(1):44-54. doi:10.1007/s10545-007-0798-1
38. 2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J Immunol Methods 202(2):133-141
39. ++ transport by ruthenium red. Biochem Biophys Res Commun 42(2):298-305
40. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1-2):55-63
41. Murphy AN, Fiskum G, Beal MF (1999) Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J Cereb Blood Flow Metab 19(3):231-245. doi:10.1097/00004647-199903000-00001 (Pubitemid 30026913)
42. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80(1):315-360 (Pubitemid 30060567)
43. Nowaczyk MJ, Blaser SI, Clarke JT (1998) Central nervous system malformations in ethylmalonic encephalopathy. Am J Med Genet 75(3):292-296. doi:10.1002/(SICI)1096-8628(19980123)75 (Pubitemid 28076857)
44. Ozand PT, Rashed M, Millington DS, Sakati N, Hazzaa S, Rahbeeni Z, al Odaib A, Youssef N, Mazrou A, Gascon GG et al (1994) Ethylmalonic aciduria: an organic acidemia with CNS involvement and vasculopathy. Brain Dev 16(Suppl):12-22 (Pubitemid 124009012)
45. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego
46. Pedersen CB, Kolvraa S, Kolvraa A, Stenbroen V, Kjeldsen M, Ensenauer R, Tein I, Matern D, Rinaldo P, Vianey-Saban C, Ribes A, Lehnert W, Christensen E, Corydon TJ, Andresen BS, Vang S, Bolund L, Vockley J, Bross P, Gregersen N (2008) The ACADS gene variation spectrum in 114 patients with short-chain acyl-CoA dehydrogenase (SCAD) deficiency is dominated by missense variations leading to protein misfolding at the cellular level. Hum Genet 124(1):43-56. doi:10.1007/s00439-008-0521-9
47. Pedersen CB, Zolkipli Z, Vang S, Palmfeldt J, Kjeldsen M, Stenbroen V, Schmidt SP, Wanders RJ, Ruiter JP, Wibrand F, Tein I, Gregersen N (2010) Antioxidant dysfunction: potential risk for neurotoxicity in ethylmalonic aciduria. J Inherit Metab Dis 33(3):211-222. doi:10.1007/s10545-010-9086-6
48. Pull I, McIlwain H (1972) Metabolism of (14 C)adenine and derivatives by cerebral tissues, superfused and electrically stimulated. Biochem J 126(4):965-973
49. Rasola A, Bernardi P (2011) Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis. Cell Calcium 50(3):222-233. doi:10.1016/j.ceca.2011.04.007
50. Ribes A, Riudor E, Garavaglia B, Martinez G, Arranz A, Invernizzi F, Briones P, Lamantea E, Sentis M, Barcelo A, Roig M (1998)
51. Mild or absent clinical signs in twin sisters with short-chain acyl-CoA dehydrogenase deficiency. Eur J Pediatr 157(4):317-320
52. Rizzuto R, De Stefani D, Raffaello A, Mammucari C (2012) Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13(9):566-578. doi:10.1038/nrm3412
53. Rosenthal RE, Hamud F, Fiskum G, Varghese PJ, Sharpe S (1987) Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine. J Cereb Blood Flow Metab 7(6):752-758. doi:10.1038/jcbfm.1987.130 (Pubitemid 18029817)
54. 2+ transport in brain mitochondria. FEBS Lett 247(2):483-486
55. Saito A, Castilho RF (2010) Inhibitory effects of adenine nucleotides on brain mitochondrial permeability transition. Neurochem Res 35(11):1667-1674. doi:10.1007/s11064-010-0228-x
56. Schuck PF, Leipnitz G, Ribeiro CA, Dalcin KB, Assis DR, Barschak AG, Pulrolnik V, Wannmacher CM, Wyse AT, Wajner M (2002) Inhibition of creatine kinase activity in vitro by ethylmalonic acid in cerebral cortex of young rats. Neurochem Res 27(12):1633-1639 (Pubitemid 36020116)
57. Schuck PF, Ferreira Gda C, Viegas CM, Tonin AM, Busanello EN, Pettenuzzo LF, Netto CA, Wajner M (2009) Chronic early postnatal administration of ethylmalonic acid to rats causes behavioral deficit. Behav Brain Res 197(2):364-370. doi:10.1016/j.bbr.2008.09.031
58. Schuck PF, Busanello EN, Moura AP, Tonin AM, Grings M, Ritter L, Vargas CR, da Costa Ferreira G, Wajner M (2010) Promotion of lipid and protein oxidative damage in rat brain by ethylmalonic acid. Neurochem Res 35(2):298-305. doi:10.1007/s11064-009-0055-0
59. +, K(+)-ATPase activity and mRNA levels in rat cerebral cortex. Synapse 67(3):111-117. doi:10.1002/syn.21618
60. 2+ sequestration system. FEBS J 277(18):3652-3663. doi:10.1111/j.1742-4658.2010.07756.x
61. Tahara EB, Navarete FD, Kowaltowski AJ (2009) Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med 46(9):1283-1297. doi:10.1016/j.freeradbiomed. 2009.02.008
62. 2+ and oxidant stress. Eur J Biochem 238(1):166-172
63. Tein I, Elpeleg O, Ben-Zeev B, Korman SH, Lossos A, Lev D, Lerman-Sagie T, Leshinsky-Silver E, Vockley J, Berry GT, Lamhonwah AM, Matern D, Roe CR, Gregersen N (2008) Short-chain acyl-CoA dehydrogenase gene mutation (c.319C > T) presents with clinical heterogeneity and is candidate founder mutation in individuals of Ashkenazi Jewish origin. Mol Genet Metab 93(2):179-189. doi:10.1016/j.ymgme.2007.09.021
64. Tiranti V, D'Adamo P, Briem E, Ferrari G, Mineri R, Lamantea E, Mandel H, Balestri P, Garcia-Silva MT, Vollmer B, Rinaldo P, Hahn SH, Leonard J, Rahman S, Dionisi-Vici C, Garavaglia B, Gasparini P, Zeviani M (2004) Ethylmalonic encephalopathy is caused by mutations in ETHE1, a gene encoding a mitochondrial matrix protein. Am J Hum Genet 74(2):239-252. doi:10.1086/381653 (Pubitemid 38168612)
65. Tiranti V, Briem E, Lamantea E, Mineri R, Papaleo E, De Gioia L, Forlani F, Rinaldo P, Dickson P, Abu-Libdeh B, Cindro-Heberle L, Owaidha M, Jack RM, Christensen E, Burlina A, Zeviani M (2006) ETHE1 mutations are specific to ethylmalonic encephalopathy. J Med Genet 43(4):340-346. doi:10.1136/jmg.2005. 036210
66. Tiranti V, Viscomi C, Hildebrandt T, Di Meo I, Mineri R, Tiveron C, Levitt MD, Prelle A, Fagiolari G, Rimoldi M, Zeviani M (2009) Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat Med 15(2):200-205. doi:10.1038/nm.1907
67. Zafeiriou DI, Augoustides-Savvopoulou P, Haas D, Smet J, Triantafyllou P, Vargiami E, Tamiolaki M, Gombakis N, van Coster R, Sewell AC, Vianey-Saban C, Gregersen N (2007) Ethylmalonic encephalopathy: clinical and biochemical observations. Neuropediatrics 38(2):78-82. doi:10.1055/s-2007-984447 (Pubitemid 47434500)
68. Zolkipli Z, Pedersen CB, Lamhonwah AM, Gregersen N, Tein I (2011) Vulnerability to oxidative stress in vitro in pathophysiology of mitochondrial short-chain acyl-CoA dehydrogenase deficiency: response to antioxidants. PLoS One 6(4):e17534. doi:10.1371/journal.pone.0017534
69. Zoratti M, Szabo I (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241(2):139-176