Valproic acid-induced hepatotoxicity in alpers syndrome is associated with mitochondrial permeability transition pore opening-dependent apoptotic sensitivity in an induced pluripotent stem cell model

Hepatology

Volumn 61, Issue 5, 2015, Pages 1730-1739

  Li, Shengbiao ^a,b   Guo, Jingyi ^a,b   Ying, Zhongfu ^a   Chen, Shen ^a   Yang, Liang ^a   Chen, Keshi ^a   Long, Qi ^a   Qin, Dajiang ^a   Pei, Duanqing ^a   Liu, Xingguo ^a  

^a GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; CARNITINE; CASPASE 9; CYCLOSPORIN A; CYTOCHROME C; DNA DIRECTED DNA POLYMERASE GAMMA; MITOCHONDRIAL DNA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; SUPEROXIDE; VALPROIC ACID; ANTICONVULSIVE AGENT; CARRIER PROTEIN;

ALPERS DISEASE; APOPTOSIS; ARTICLE; CASE REPORT; CELL ULTRASTRUCTURE; CHILD; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; LIVER CELL; LIVER TOXICITY; MALE; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN SECRETION; SKIN FIBROBLAST; CELL CULTURE; COMPLICATION; DRUG-INDUCED LIVER INJURY; PHYSIOLOGY; SCHILDER DISEASE;

ANTICONVULSANTS; APOPTOSIS; CELLS, CULTURED; DIFFUSE CEREBRAL SCLEROSIS OF SCHILDER; DRUG-INDUCED LIVER INJURY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; VALPROIC ACID;

EID: 84928203511     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27712     Document Type: Article

References (50)

1. Lee WS, Sokol RJ. Mitochondrial hepatopathies: advances in genetics, therapeutic approaches, and outcomes. J Pediatr 2013;163:942-948.
2. Lee WS, Sokol RJ. Mitochondrial hepatopathies: advances in genetics and pathogenesis. Hepatology 2007;45:1555-1565.
3. Stumpf JD, Copeland WC. Mitochondrial DNA replication and disease: insights from DNA polymerase gamma mutations. Cell Mol Life Sci 2011;68:219-233.
4. Hunter MF, Peters H, Salemi R, Thorburn D, Mackay MT. Alpers syndrome with mutations in POLG: clinical and investigative features. Pediatr Neurol 2011;45:311-318.
5. Nguyen KV, Sharief FS, Chan SS, Copeland WC, Naviaux RK. Molecular diagnosis of Alpers syndrome. J Hepatol 2006;45:108-116.
6. Chow CW, Thorburn DR. Morphological correlates of mitochondrial dysfunction in children. Hum Reprod 2000;15(Suppl 2):68-78.
7. Simonati A, Filosto M, Savio C, Tomelleri G, Tonin P, Dalla Bernardina B, Rizzuto N. Features of cell death in brain and liver, the target tissues of progressive neuronal degeneration of childhood with liver disease (Alpers-Huttenlocher disease). Acta Neuropathol 2003;106:57-65.
8. Sandbank U, Lerman P. Progressive cerebral poliodystrophy-Alpers' disease. Disorganized giant neuronal mitochondria on electron microscopy. J Neurol Neurosurg Psychiatry 1972;35:749-755.
9. Schaller A, Hahn D, Jackson CB, Kern I, Chardot C, Belli DC, et al. Molecular and biochemical characterisation of a novel mutation in POLG associated with Alpers syndrome. BMC Neurol 2011;11:4.
10. Nanau RM, Neuman MG. Adverse drug reactions induced by valproic acid. Clin Biochem 2013;46:1323-1338.
11. Schwabe MJ, Dobyns WB, Burke B, Armstrong DL. Valproate-induced liver failure in one of two siblings with Alpers disease. Pediatr Neurol 1997;16:337-343.
12. Pronicka E, Weglewska-Jurkiewicz A, Pronicki M, Sykut-Cegielska J, Kowalski P, Pajdowska M, et al. Drug-resistant epilepsia and fulminant valproate liver toxicity. Alpers-Huttenlocher syndrome in two children confirmed post mortem by identification of p.W748S mutation in POLG gene. Med Sci Monit 2011;17:CR203-CR209.
13. Saneto RP, Lee IC, Koenig MK, Bao X, Weng SW, Naviaux RK, Wong LJC. POLG DNA testing as an emerging standard of care before instituting valproic acid therapy for pediatric seizure disorders. Seizure 2010;19:140-146.
14. Chinnery PF, Zeviani M. 155th ENMC workshop: polymerase gamma and disorders of mitochondrial DNA synthesis, 21-23 September 2007, Naarden, The Netherlands. Neuromuscul Disord 2008;18:259-267.
15. Stewart JD, Horvath R, Baruffini E, Ferrero I, Bulst S, Watkins PB, et al. Polymerase gamma gene POLG determines the risk of sodium valproate-induced liver toxicity. Hepatology 2010;52:1791-1796.
16. Finsterer J, Zarrouk Mahjoub S. Mitochondrial toxicity of antiepileptic drugs and their tolerability in mitochondrial disorders. Exp Opin Drug Metab Toxicol 2012;8:71-79.
17. Hance N, Ekstrand MI, Trifunovic A. Mitochondrial DNA polymerase gamma is essential for mammalian embryogenesis. Hum Mol Genet 2005;14:1775-1783.
18. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005;309:481-484.
19. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004;429:417-423.
20. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
21. Carvajal-Vergara X, Sevilla A, D'Souza SL, Ang YS, Schaniel C, Lee DF, et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010;465:808-812.
22. Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, Fasano CA, et al. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 2009;461:402-406.
23. Cayo MA, Cai J, DeLaForest A, Noto FK, Nagaoka M, Clark BS, et al. JD induced pluripotent stem cell-derived hepatocytes faithfully recapitulate the pathophysiology of familial hypercholesterolemia. Hepatology 2012;56:2163-2171.
24. Choi SM, Kim Y, Shim JS, Park JT, Wang RH, Leach SD, et al. Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 2013;57:2458-2468.
25. Mousson de Camaret B, Chassagne M, Mayencon M, Padet S, Crehalet H, Clerc-Renaud P, et al. POLG exon 22 skipping induced by different mechanisms in two unrelated cases of Alpers syndrome. Mitochondrion 2011;11:223-227.
26. Song Z, Cai J, Liu Y, Zhao D, Yong J, Duo S, et al. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 2009;19:1233-1242.
27. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T, et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 2006;126:177-189.
28. Jacobs EE, Sanadi DR. The reversible removal of cytochrome c from mitochondria. J Biol Chem 1960;235:531-534.
29. Mangalat N, Tatevian N, Bhattacharjee M, Rhoads JM. Alpers syndrome: an unusual etiology of failure to thrive. Ultrastruct Pathol 2012;36:219-221.
30. Marchi S, Giorgi C, Suski JM, Agnoletto C, Bononi A, Bonora M, et al. Mitochondria-ros crosstalk in the control of cell death and aging. J Signal Transduct 2012;2012:329635.
31. Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J, et al. Superoxide flashes in single mitochondria. Cell 2008;134:279-290.
32. Ma Q, Fang H, Shang W, Liu L, Xu Z, Ye T, et al. Superoxide flashes: early mitochondrial signals for oxidative stress-induced apoptosis. J Biol Chem 2011;286:27573-27581.
33. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, et al. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci U S A 2013;110:5887-5892.
34. Siemes H, Nau H, Schultze K, Wittfoht W, Drews E, Penzien J, Seidel U. Valproate (VPA) metabolites in various clinical conditions of probable VPA-associated hepatotoxicity. Epilepsia 1993;34:332-346.
35. DeVivo DC. Effect of L-carnitine treatment for valproate-induced hepatotoxicity. Neurology 2002;58:507-508.
36. Konig SA, Siemes H, Blaker F, Boenigk E, Gross-Selbeck G, Hanefeld F, et al. Severe hepatotoxicity during valproate therapy: an update and report of eight new fatalities. Epilepsia 1994;35:1005-1015.
37. Romero-Falcon A, de la Santa-Belda E, Garcia-Contreras R, Varela JM. A case of valproate-associated hepatotoxicity treated with L-carnitine. Eur J Intern Med 2003;14:338-340.
38. Bohan TP, Helton E, McDonald I, Konig S, Gazitt S, Sugimoto T, et al. Effect of L-carnitine treatment for valproate-induced hepatotoxicity. Neurology 2001;56:1405-1409.
39. Farrell K, Abbott F. Role of N-acetylcysteine in the treatment of valproate hepatotoxicity. In: Levy RH, Penry JK, eds. Idiosyncratic Reactions to Valproate: Clinical Risk Patterns and Mechanisms of Toxicity. New York: Raven, 1991:149-153.
40. KAK S. Valproic acid induced hepatotoxicitv and protective role of carnitine. Pakistan J Pathol 1997:133-134.
41. Said SA, El-Agamy DS. Prevention of sodium valproate-induced hepatotoxicity by curcumin, rosiglitazone and N-acetylcysteine in rats. Arzneimittelforschung 2010;60:647-653.
42. Lheureux PE, Hantson P. Carnitine in the treatment of valproic acid-induced toxicity. Clin Toxicol (Phila) 2009;47:101-111.
43. Tong V, Teng XW, Chang TK, Abbott FS. Valproic acid I: time course of lipid peroxidation biomarkers, liver toxicity, and valproic acid metabolite levels in rats. Toxicol Sci 2005;86:427-435.
44. Mlejnek P, Dolezel P. N-acetylcysteine prevents the geldanamycin cytotoxicity by forming geldanamycin-N-acetylcysteine adduct. Chem Biol Interact 2014;220:248-254.
45. Cotgreave IA. N-acetylcysteine: pharmacological considerations and experimental and clinical applications. Adv Pharmacol 1997;38:205-227.
46. Hausenloy DJ, Duchen MR, Yellon DM. Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury. Cardiovasc Res 2003;60:617-625.
47. + channels. Biochim Biophys Acta 2006;1762:202-212.
48. Nishida H, Sato T, Ogura T, Nakaya H. New aspects for the treatment of cardiac diseases based on the diversity of functional controls on cardiac muscles: mitochondrial ion channels and cardioprotection. J Pharmacol Sci 2009;109:341-347.
49. Teshima Y, Akao M, Baumgartner WA, Marban E. Nicorandil prevents oxidative stress-induced apoptosis in neurons by activating mitochondrial ATP-sensitive potassium channels. Brain Res 2003;990:45-50.
50. + channel opening requires superoxide radical generation. Am J Physiol Heart Circ Physiol 2006;290:H434-H440.