Deregulation of mitochondrial functions provoked by long-chain fatty acid accumulating in long-chain 3-hydroxyacyl-CoA dehydrogenase and mitochondrial permeability transition deficiencies in rat heart - Mitochondrial permeability transition pore opening as a potential contributing pathomechanism of cardiac alterations in these disorders

FEBS Journal

Volumn 282, Issue 24, 2015, Pages 4714-4726

  Cecatto, Cristiane ^a   Hickmann, Fernanda H ^a   Rodrigues, Marília D N ^a   Amaral, Alexandre U ^a   Wajner, Moacir ^a,b  

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

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

calcium homeostasis; heart; long chain 3 hydroxy fatty acid; mitochondrial bioenergetics; mitochondrial permeability transition

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; 3 HYDROXYPALMITIC ACID; 3 HYDROXYTETRADECANOIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BEHENIC ACID; CALCIUM ION; CYCLOSPORIN A; FATTY ACID DERIVATIVE; LONG CHAIN 3 HYDROXY FATTY ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RUTHENIUM RED; UNCLASSIFIED DRUG; 3-HYDROXYPALMITIC ACID; BETA-HYDROXYMYRISTIC ACID; CALCIUM CHANNEL BLOCKING AGENT; CARRIER PROTEIN; ENZYME INHIBITOR; LONG CHAIN 3 HYDROXYACYL COENZYME A DEHYDROGENASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL TRIFUNCTIONAL PROTEIN; MYRISTIC ACID DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PALMITIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CALCIUM HOMEOSTASIS; CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HEART MITOCHONDRION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION SWELLING; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; ANTIBODY SPECIFICITY; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; DEFICIENCY; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; DRUG EFFECTS; ENZYMOLOGY; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MYOPATHY; NEUROLOGIC DISEASE; OXIDATIVE PHOSPHORYLATION; RHABDOMYOLYSIS; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; CARDIOMYOPATHIES; CELL MEMBRANE PERMEABILITY; ENZYME INHIBITORS; HUMANS; LIPID METABOLISM, INBORN ERRORS; LONG-CHAIN-3-HYDROXYACYL-COA DEHYDROGENASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL MYOPATHIES; MITOCHONDRIAL SWELLING; MITOCHONDRIAL TRIFUNCTIONAL PROTEIN; MYRISTIC ACIDS; NADP; NERVOUS SYSTEM DISEASES; ORGAN SPECIFICITY; OXIDATIVE PHOSPHORYLATION; PALMITIC ACIDS; RATS, WISTAR; RHABDOMYOLYSIS;

EID: 84969429403     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13526     Document Type: Article

References (71)

1. Tyni T, &, Pihko H, (1999) Long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency. Acta Paediatr 88, 237-245.
2. Roe CR, &, Ding J, (2001) Mitochondrial fatty acid oxidation disorders. In The Online Metabolic and Molecular Bases of Inherited Disease (, Valle D, Beaudet AL, Vogelstein B, Kinzler KW, Antonarakis SE, &, Ballabio A, eds), pp. 1-65. McGraw-Hill, New York.
3. Rinaldo P, Matern D, &, Bennett MJ, (2002) Fatty acid oxidation disorders. Annu Rev Physiol 64, 477-502.
4. Sander J, Sander S, Steuerwald U, Janzen N, Peter M, Wanders RJ, Marquardt I, Korenke GC, &, Das AM, (2005) Neonatal screening for defects of the mitochondrial trifunctional protein. Mol Genet Metab 85, 108-114.
5. Das AM, Illsinger S, Lucke T, Hartmann H, Ruiter JP, Steuerwald U, Waterham HR, Duran M, &, Wanders RJ, (2006) Isolated mitochondrial long-chain ketoacyl-CoA thiolase deficiency resulting from mutations in the HADHB gene. Clin Chem 52, 530-534.
6. Hintz SR, Matern D, Strauss A, Bennett MJ, Hoyme HE, Schelley S, Kobori J, Colby C, Lehman NL, &, Enns GM, (2002) Early neonatal diagnosis of long-chain 3-hydroxyacyl coenzyme a dehydrogenase and mitochondrial trifunctional protein deficiencies. Mol Genet Metab 75, 120-127.
7. Jones PM, Moffitt M, Joseph D, Harthcock PA, Boriack RL, Ibdah JA, Strauss AW, &, Bennett MJ, (2001) Accumulation of free 3-hydroxy fatty acids in the culture media of fibroblasts from patients deficient in long-chain l-3-hydroxyacyl-CoA dehydrogenase: a useful diagnostic aid. Clin Chem 47, 1190-1194.
8. Spiekerkoetter U, Bennett MJ, Ben-Zeev B, Strauss AW, &, Tein I, (2004) Peripheral neuropathy, episodic myoglobinuria, and respiratory failure in deficiency of the mitochondrial trifunctional protein. Muscle Nerve 29, 66-72.
9. Spiekerkoetter U, Mueller M, Cloppenburg E, Motz R, Mayatepek E, Bueltmann B, &, Korenke C, (2008) Intrauterine cardiomyopathy and cardiac mitochondrial proliferation in mitochondrial trifunctional protein (TFP) deficiency. Mol Genet Metab 94, 428-430.
10. Moczulski D, Majak I, &, Mamczur D, (2009) An overview of beta-oxidation disorders. Postepy Hig Med Dosw (Online) 63, 266-277.
11. den Boer ME, Dionisi-Vici C, Chakrapani A, van Thuijl AO, Wanders RJ, &, Wijburg FA, (2003) Mitochondrial trifunctional protein deficiency: a severe fatty acid oxidation disorder with cardiac and neurologic involvement. J Pediatr 142, 684-689.
12. Tyni T, Rapola J, Paetau A, Palotie A, &, Pihko H, (1997) Pathology of long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency caused by the G1528C mutation. Pediatr Pathol Lab Med 17, 427-447.
13. Rocchiccioli F, Wanders RJ, Aubourg P, Vianey-Liaud C, Ijlst L, Fabre M, Cartier N, &, Bougneres PF, (1990) Deficiency of long-chain 3-hydroxyacyl-CoA dehydrogenase: a cause of lethal myopathy and cardiomyopathy in early childhood. Pediatr Res 28, 657-662.
14. Schaefer J, Jackson S, Dick DJ, &, Turnbull DM, (1996) Trifunctional enzyme deficiency: adult presentation of a usually fatal beta-oxidation defect. Ann Neurol 40, 597-602.
15. Spiekerkoetter U, (2010) Mitochondrial fatty acid oxidation disorders: clinical presentation of long-chain fatty acid oxidation defects before and after newborn screening. J Inherit Metab Dis 33, 527-532.
16. Olsen RK, Cornelius N, &, Gregersen N, (2013) Genetic and cellular modifiers of oxidative stress: what can we learn from fatty acid oxidation defects? Mol Genet Metab 110 (Suppl), S31-S39.
17. Wakabayashi M, Kamijo Y, Nakajima T, Tanaka N, Sugiyama E, Yangyang T, Kimura T, &, Aoyama T, (2012) Fatty acid accumulation and resulting PPARalpha activation in fibroblasts due to trifunctional protein deficiency. PPAR Res 2012, 371691.
18. Tonin AM, Grings M, Busanello EN, Moura AP, Ferreira GC, Viegas CM, Fernandes CG, Schuck PF, &, Wajner M, (2010) Long-chain 3-hydroxy fatty acids accumulating in LCHAD and MTP deficiencies induce oxidative stress in rat brain. Neurochem Int 56, 930-936.
19. Tonin AM, Amaral AU, Busanello EN, Grings M, Castilho RF, &, Wajner M, (2013) Long-chain 3-hydroxy fatty acids accumulating in long-chain 3-hydroxyacyl-CoA dehydrogenase and mitochondrial trifunctional protein deficiencies uncouple oxidative phosphorylation in heart mitochondria. J Bioenerg Biomembr 45, 47-57.
20. Tonin AM, Ferreira GC, Grings M, Viegas CM, Busanello EN, Amaral AU, Zanatta A, Schuck PF, &, Wajner M, (2010) Disturbance of mitochondrial energy homeostasis caused by the metabolites accumulating in LCHAD and MTP deficiencies in rat brain. Life Sci 86, 825-831.
21. Das AM, Fingerhut R, Wanders RJ, &, Ullrich K, (2000) Secondary respiratory chain defect in a boy with long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency: possible diagnostic pitfalls. Eur J Pediatr 159, 243-246.
22. Tyni T, Majander A, Kalimo H, Rapola J, &, Pihko H, (1996) Pathology of skeletal muscle and impaired respiratory chain function in long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency with the G1528C mutation. Neuromuscul Disord 6, 327-337.
23. Tonin AM, Amaral AU, Busanello EN, Gasparotto J, Gelain DP, Gregersen N, &, Wajner M, (2014) Mitochondrial bioenergetics deregulation caused by long-chain 3-hydroxy fatty acids accumulating in LCHAD and MTP deficiencies in rat brain: a possible role of mPTP opening as a pathomechanism in these disorders? Biochim Biophys Acta 1842, 1658-1667.
24. Wanders RJ, Vreken P, den Boer ME, Wijburg FA, van Gennip AH, &, IJlst L, (1999) Disorders of mitochondrial fatty acyl-CoA beta-oxidation. J Inherit Metab Dis 22, 442-487.
25. Spierkerkoetter U, Khuchua Z, Yue Z, &, Strauss AW, (2004) The early-onset phenotype of mitochondrial trifunctional protein deficiency: a lethal disorder with multiple tissue involvement. J Inherit Metab Dis 27, 294-296.
26. Spiekerkoetter U, Sun B, Khuchua Z, Bennett MJ, &, Strauss AW, (2003) Molecular and phenotypic heterogeneity in mitochondrial trifunctional protein deficiency due to beta-subunit mutations. Hum Mutat 21, 598-607.
27. Ventura FV, Tavares de Almeida I, &, Wanders RJ, (2007) Inhibition of adenine nucleotide transport in rat liver mitochondria by long-chain acyl-coenzyme A beta-oxidation intermediates. Biochem Biophys Res Commun 352, 873-878.
28. Oey NA, den Boer ME, Wijburg FA, Vekemans M, Auge J, Steiner C, Wanders RJ, Waterham HR, Ruiter JP, &, Attie-Bitach T, (2005) Long-chain fatty acid oxidation during early human development. Pediatr Res 57, 755-759.
29. Ventura FV, Ruiter JP, IJlst L, de Almeida IT, &, Wanders RJ, (1998) Lactic acidosis in long-chain fatty acid beta-oxidation disorders. J Inherit Metab Dis 21, 645-654.
30. Moore LE, (1971) Effect of temperature and calcium ions on rate constants of myelinated nerve. Am J Physiol 221, 131-137.
31. Yarana C, Sripetchwandee J, Sanit J, Chattipakorn S, &, Chattipakorn N, (2012) Calcium-induced cardiac mitochondrial dysfunction is predominantly mediated by cyclosporine A-dependent mitochondrial permeability transition pore. Arch Med Res 43, 333-338.
32. Pottecher J, Guillot M, Belaidi E, Charles AL, Lejay A, Gharib A, Diemunsch P, &, Geny B, (2013) Cyclosporine A normalizes mitochondrial coupling, reactive oxygen species production, and inflammation and partially restores skeletal muscle maximal oxidative capacity in experimental aortic cross-clamping. J Vasc Surg 57, 1100-1108 e2.
33. 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, 18558-18561.
34. Tanveer A, Virji S, Andreeva L, Totty NF, Hsuan JJ, Ward JM, &, Crompton M, (1996) Involvement of cyclophilin D in the activation of a mitochondrial pore by Ca2+ and oxidant stress. Eur J Biochem 238, 166-172.
35. Rottenberg H, &, Marbach M, (1989) Adenine nucleotides regulate Ca2+ transport in brain mitochondria. FEBS Lett 247, 483-486.
36. Saito A, &, Castilho RF, (2010) Inhibitory effects of adenine nucleotides on brain mitochondrial permeability transition. Neurochem Res 35, 1667-1674.
37. Zoratti M, &, Szabo I, (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241, 139-176.
38. Starkov AA, (2010) The molecular identity of the mitochondrial Ca2+ sequestration system. FEBS J 277, 3652-3663.
39. Rasola A, &, Bernardi P, (2011) Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis. Cell Calcium 50, 222-233.
40. Hickmann FH, Cecatto C, Kleemann D, Monteiro WO, Castilho RF, Amaral AU, &, Wajner M, (2015) Uncoupling, metabolic inhibition and induction of mitochondrial permeability transition in rat liver mitochondria caused by the major long-chain hydroxyl monocarboxylic fatty acids accumulating in LCHAD deficiency. Biochim Biophys Acta 1847, 620-628.
41. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, et al,. (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345.
42. De Stefani D, Raffaello A, Teardo E, Szabo I, &, Rizzuto R, (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340.
43. Marchi S, &, Pinton P, (2014) The mitochondrial calcium uniporter complex: molecular components, structure and physiopathological implications. J Physiol 592, 829-839.
44. Crompton M, Virji S, Doyle V, Johnson N, &, Ward JM, (1999) The mitochondrial permeability transition pore. Biochem Soc Symp 66, 167-179.
45. 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, 22-27.
46. Gandhi S, Wood-Kaczmar A, Yao Z, Plun-Favreau H, Deas E, Klupsch K, Downward J, Latchman DS, Tabrizi SJ, Wood NW, et al,. (2009) PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell 33, 627-638.
47. Jaiswal MK, Zech WD, Goos M, Leutbecher C, Ferri A, Zippelius A, Carri MT, Nau R, &, Keller BU, (2009) Impairment of mitochondrial calcium handling in a mtSOD1 cell culture model of motoneuron disease. BMC Neurosci 10, 64.
48. Martin LJ, Gertz B, Pan Y, Price AC, Molkentin JD, &, Chang Q, (2009) The mitochondrial permeability transition pore in motor neurons: involvement in the pathobiology of ALS mice. Exp Neurol 218, 333-346.
49. Quintanilla RA, &, Johnson GV, (2009) Role of mitochondrial dysfunction in the pathogenesis of Huntington's disease. Brain Res Bull 80, 242-247.
50. Rosenstock TR, Carvalho AC, Jurkiewicz A, Frussa-Filho R, &, Smaili SS, (2004) Mitochondrial calcium, oxidative stress and apoptosis in a neurodegenerative disease model induced by 3-nitropropionic acid. J Neurochem 88, 1220-1228.
51. Drago I, De Stefani D, Rizzuto R, &, Pozzan T, (2012) Mitochondrial Ca2+ uptake contributes to buffering cytoplasmic Ca2+ peaks in cardiomyocytes. Proc Natl Acad Sci USA 109, 12986-12991.
52. Castilho RF, Vicente JA, Kowaltowski AJ, &, Vercesi AE, (1997) 4,6-Dinitro-o-cresol uncouples oxidative phosphorylation and induces membrane permeability transition in rat liver mitochondria. Int J Biochem Cell Biol 29, 1005-1011.
53. Kowaltowski AJ, Castilho RF, &, Vercesi AE, (1996) Opening of the mitochondrial permeability transition pore by uncoupling or inorganic phosphate in the presence of Ca2+ is dependent on mitochondrial-generated reactive oxygen species. FEBS Lett 378, 150-152.
54. Kowaltowski AJ, Castilho RF, &, Vercesi AE, (2001) Mitochondrial permeability transition and oxidative stress. FEBS Lett 495, 12-15.
55. Lehninger AL, Vercesi A, &, Bababunmi EA, (1978) Regulation of Ca2+ release from mitochondria by the oxidation-reduction state of pyridine nucleotides. Proc Natl Acad Sci USA 75, 1690-1694.
56. Hoek JB, &, Rydstrom J, (1988) Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem J 254, 1-10.
57. Zago EB, Castilho RF, &, Vercesi AE, (2000) The redox state of endogenous pyridine nucleotides can determine both the degree of mitochondrial oxidative stress and the solute selectivity of the permeability transition pore. FEBS Lett 478, 29-33.
58. Wojtczak L, Wieckowski MR, &, Schonfeld P, (1998) Protonophoric activity of fatty acid analogs and derivatives in the inner mitochondrial membrane: a further argument for the fatty acid cycling model. Arch Biochem Biophys 357, 76-84.
59. Skulachev VP, (1991) Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett 294, 158-162.
60. Olpin SE, (2013) Pathophysiology of fatty acid oxidation disorders and resultant phenotypic variability. J Inherit Metab Dis 36, 645-658.
61. Hagenfeldt L, von Dobeln U, Holme E, Alm J, Brandberg G, Enocksson E, &, Lindeberg L, (1990) 3-Hydroxydicarboxylic aciduria-a fatty acid oxidation defect with severe prognosis. J Pediatr 116, 387-392.
62. Costa CG, Dorland L, de Almeida IT, Jakobs C, Duran M, &, Poll-The BT, (1998) The effect of fasting, long-chain triglyceride load and carnitine load on plasma long-chain acylcarnitine levels in mitochondrial very long-chain acyl-CoA dehydrogenase deficiency. J Inherit Metab Dis 21, 391-399.
63. Mathur A, Sims HF, Gopalakrishnan D, Gibson B, Rinaldo P, Vockley J, Hug G, &, Strauss AW, (1999) Molecular heterogeneity in very-long-chain acyl-CoA dehydrogenase deficiency causing pediatric cardiomyopathy and sudden death. Circulation 99, 1337-1343.
64. Ferranti R, da Silva MM, &, Kowaltowski AJ, (2003) Mitochondrial ATP-sensitive K+ channel opening decreases reactive oxygen species generation. FEBS Lett 536, 51-55.
65. 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, 752-758.
66. 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, 44-54.
67. 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.
68. Akerman KE, &, Wikstrom MK, (1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Lett 68, 191-197.
69. 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.
70. Lemasters JJ, &, Hackenbrock CR, (1976) Continuous measurement and rapid kinetics of ATP synthesis in rat liver mitochondria, mitoplasts and inner membrane vesicles determined by firefly-luciferase luminescence. Eur J Biochem 67, 1-10.
71. Maioli MA, Lemos DE, Guelfi M, Medeiros HC, Riet-Correa F, Medeiros RM, Barbosa-Filho JM, &, Mingatto FE, (2012) Mechanism for the uncoupling of oxidative phosphorylation by juliprosopine on rat brain mitochondria. Toxicon 60, 1355-1362.