Induction of the mitochondrial permeability transition (MPT) by micromolar iron: Liberation of calcium is more important than NAD(P)H oxidation

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 9, 2012, Pages 1537-1549

  Gáll, Juraj ^a   Škrha Jr , Jan ^a   Buchal, Richard ^a   Sedláčková, Eva ^a   Verébová, Karina ^a,b   Pláteník, Jan ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (Czech Republic)

Author keywords

Calcium signaling; Chelators; Iron toxicity; Mitochondrial permeability transition; Oxidative stress

Indexed keywords

BOVINE SERUM ALBUMIN; CALCIUM; EDETIC ACID; IRON; MALIC ACID; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUCCINIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOOXIDATION; CALCIUM SIGNALING; CONTROLLED STUDY; LIVER MITOCHONDRION; MALE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION SWELLING; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; IRON; MALE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NAD; OXIDATION-REDUCTION; RATS; RATS, WISTAR;

BOVINAE; RATTUS;

EID: 84862233135     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.05.008     Document Type: Article

References (71)

1. D.R. Hunter, R.A. Haworth, and J.H. Southard Relationship between configuration, function, and permeability in calcium-treated mitochondria J. Biol. Chem. 251 1976 5069 5077
2. 2+-induced membrane transition in mitochondria, I. the protective mechanisms Arch. Biochem. Biophys. 195 1979 453 459 (Pubitemid 9235077)
3. 2+ trigger site Arch. Biochem. Biophys. 195 1979 460 467 (Pubitemid 9235078)
4. 2+ release Arch. Biochem. Biophys. 195 1979 468 477 (Pubitemid 9235079)
5. T.E. Gunter, and D.R. Pfeiffer Mechanisms by which mitochondria transport calcium Am. J. Physiol. 258 1990 C755 C786
6. M. Zoratti, and I. Szabo The mitochondrial permeability transition Biochim. Biophys. Acta 1241 1995 139 176
7. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem. J. 341 1999 233 249 (Pubitemid 29373645)
8. A.P. Halestrap, G.P. McStay, and S.J. Clarke The permeability transition pore complex: another view Biochimie 84 2002 153 166
9. P. Bernardi, A. Krauskopf, E. Basso, V. Petronilli, E. Blachy-Dyson, F. Di Lisa, and M.A. Forte The mitochondrial permeability transition from in vitro artifact to disease target FEBS J. 273 2006 2077 2099
10. A.P. Halestrap What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol. 46 2009 821 831
11. F. Ichas, L.S. Jouaville, and J.P. Mazat Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals Cell 89 1997 1145 1153 (Pubitemid 127678747)
12. R.J. Miller Mitochondria - the Kraken wakes! Trends Neurosci. 21 1998 95 97 (Pubitemid 28080668)
13. J.S. Armstrong The role of the mitochondrial permeability transition in the cell death Mitochondrion 6 2006 225 234 (Pubitemid 44567384)
14. G. Kroemer, L. Galluzzi, and C. Brenner Mitochondrial membrane permeabilization in cell death Physiol. Rev. 87 2007 99 163 (Pubitemid 46209992)
15. H. Malhi, G.J. Gores, and J.J. Lemasters Apoptosis and necrosis in the liver: a tale of two deaths? Hepatology 43 2006 S31 S44
16. P. Bernardi Modulation of the mitochondrial cyclosporine A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization J. Biol. Chem. 267 1992 8834 8839
17. 2+ release from mitochondria by the oxidation/reduction state of pyridine nucleotides Proc. Natl. Acad. Sci. U. S. A. 75 1978 1690 1694 (Pubitemid 8344377)
18. A.J. Kowaltowski, R.F. Castilho, and A.E. Vercesi Mitochondrial permeability transition and oxidative stress FEBS Lett. 495 2001 12 15 (Pubitemid 32367965)
19. P. Costantini, B.V. Chernyak, V. Petronilli, and P. Bernardi Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites J. Biol. Chem. 271 1996 6746 6751 (Pubitemid 26104106)
20. G.P. McStay, S.J. Clarke, and A.P. Halestrap Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore Biochem. J. 367 2002 541 548 (Pubitemid 35216831)
21. P. Ponka Cellular iron metabolism Kidney Int. 55 Suppl. 69 1999 S-2 S-11
22. P. Ponka, M. Tenenbein, and J. Eaton Iron G. Nordberg, B. Fowler, M. Nordberg, L. Fridberg, Handbook of Toxicology of Metals third ed. 2007 Elsevier B.V. Amsterdam 577 598
23. B. Halliwell, and J.M.C. Gutteridge Role of free radicals and catalytic metal ions in human disease: an overview Methods Enzymol. 186 1990 1 85 (Pubitemid 20279941)
24. B. Halliwell, and J.M.C. Gutteridge Free Radicals in Biology and Medicine 4th edition 2007 Oxford University Press New York
25. S. Goldstein, D. Meyerstein, and G. Czapski The Fenton reagents Free Radic. Biol. Med. 15 1993 435 445 (Pubitemid 23283560)
26. C.C. Winterbourn Toxicity of iron and hydrogen peroxide: the Fenton reaction Toxicol. Lett. 82/83 1995 969 974 (Pubitemid 26054777)
27. L.A. Reinke, J.M. Rau, and P.B. McCay Characteristics of an oxidant formed during iron (II) autoxidation Free Radic. Biol. Med. 16 1994 485 492 (Pubitemid 24105996)
28. B. Halliwell Drug antioxidant effects. A basis for drug selection? Drugs 42 1991 569 605 (Pubitemid 21920775)
29. A. Jacobs Low molecular weight intracellular iron transport compounds Blood 50 1977 433 439 (Pubitemid 8180426)
30. W. Breuer, M. Shvartsman, and Z.I. Cabantchik Intracellular labile iron Int. J. Biochem. Cell Biol. 40 2008 350 354 (Pubitemid 351241220)
31. O. Kakhlon, and Z.I. Cabantchik The labile iron pool: characterization, measurement, and participation in cellular processes Free Radic. Biol. Med. 33 2002 1037 1046
32. F. Petrat, H. de Groot, R. Sustmann, and U. Rauen The chelatable iron pool in living cells: a methodically defined quantity Biol. Chem. 383 2002 489 502 (Pubitemid 34506286)
33. I. Napier, P. Ponka, and D.R. Richardson Iron trafficking in the mitochondrion: novel pathways revealed by disease Blood 105 2005 1867 1874 (Pubitemid 40731766)
34. A.D. Sheftel, and R. Lill The power plant of the cell is also a smithy: the emerging role of mitochondria in cellular iron homeostasis Ann. Med. 41 2009 82 99
35. I. Romslo, and T. Flatmark Energy-dependent accumulation of iron by isolated rat liver mitochondria. I. General features Biochim. Biophys. Acta 305 1973 29 40
36. 2+ Biochim. Biophys. Acta 325 1973 38 46
37. A.-S. Zhang, A.D. Sheftel, and P. Ponka Intracellular kinetics of iron in reticulocytes: evidence for endosome involvement in iron targeting to mitochondria Blood 105 2005 368 375 (Pubitemid 40053106)
38. M. Shvartsman, R. Kikkeri, A. Shanzer, and Z.I. Cabantchik Non-transferrin-bound iron reaches mitochondria by a chelator-inaccessible mechanism: biological and clinical implications Am. J. Physiol. Cell Physiol. 293 2007 C1383 C1394
39. G.C. Shaw, J.J. Cope, L. Li, K. Corson, C. Hersey, G.E. Ackermann, B. Gwynn, A.J. Lambert, R.A. Wingert, D. Traver, N.S. Trede, B.A. Barut, Y. Zhou, E. Minet, A. Donovan, A. Brownlie, R. Balzan, M.J. Weiss, L.L. Peters, J. Kaplan, L.I. Zon, and B.H. Paw Mitoferrin is essential for erythroid iron assimilation Nature 440 2006 96 100 (Pubitemid 43336274)
40. U. Rauen, U. Kerkweg, D. Weisheit, F. Petrat, R. Sustmann, and H. de Groot Cold-induced apoptosis of hepatocytes: mitochondrial permeability transition triggered by nonmitochondrial chelatable iron Free Radic. Biol. Med. 35 2003 1664 1678 (Pubitemid 37547920)
41. U. Rauen, F. Petrat, R. Sustmann, and H. de Groot Iron-induced mitochondrial permeability transition in cultured hepatocytes J. Hepatol. 40 2004 607 615 (Pubitemid 38367782)
42. A. Uchiyama, J.S. Kim, K. Kon, H. Jaeschke, K. Ikejima, S. Watanabe, and J.J. Lemasters Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury Hepatology 48 2008 1644 1654
43. A. Masini, T. Trenti, D. Ceccarelli-Stanzani, and E. Ventura The effect of ferric iron complex on isolated rat liver mitochondria. I. Respiratory and electrochemical responses Biochim. Biophys. Acta 810 1985 20 26 (Pubitemid 16242080)
44. A. Masini, T. Trenti, D. Ceccarelli-Stanzani, and E. Ventura The effect of ferric iron complex on isolated rat liver mitochondria. II. Ion movements Biochim. Biophys. Acta 810 1985 27 32 (Pubitemid 16242081)
45. A. Masini, T. Trenti, D. Ceccarelli, and U. Muscatello The effect of a ferric iron complex on isolated rat liver mitochondria. III. Mechanistic aspects of iron-induced calcium efflux Biochim. Biophys. Acta 891 1987 150 156 (Pubitemid 17042973)
46. 2+ ions is stimulated by t-butyl hydroperoxide and mediated by reactive oxygen species generated by mitochondria Free Radic. Biol. Med. 18 1995 479 486
47. 2+ release from rat liver mitochondria Arch. Biochem. Biophys. 398 2002 198 202 (Pubitemid 34848586)
48. 2+-induced lipid peroxidation in the initiation of the mitochondrial permeability transition Arch. Biochem. Biophys. 414 2003 255 260 (Pubitemid 36627358)
49. J. Gáll, J. Škrha Jr., R. Buchal, E. Sedláč ková, K. Verébová, and J. Pláteník Induction of mitochondrial permeability transition (MPT) by iron in isolated rat liver mitochondria requires both NAD(P)H oxidation and iron import FEBS J. 276 Suppl. 1 2009 197
50. B. Tadolini, and G. Hakim The mechanism of iron(III) stimulation of lipid peroxidation Free. Radic. Res. 25 1996 221 227 (Pubitemid 26356525)
51. J.C.K. Lai, and J.B. Clark Preparation of synaptic and nonsynaptic mitochondria from mammalian brain Methods Enzymol. 55 1979 51 60
52. J. Nedergaard, and B. Cannon Overview-preparation and properties of mitochondria from different sources Methods Enzymol. 55 1979 3 28
53. S.D. Aust, D.M. Miller, and V.M. Samokyszyn Iron redox reactions and lipid peroxidation Methods Enzymol. 186 1990 457 463 (Pubitemid 20279988)
54. A. Scarpa, and J.G. Lindsay Maintenance of energy-linked functions in rat-liver mitochondria aged in the presence of nupercaine Eur. J. Biochem. 27 1972 401 407
55. M. Di Paola, and M. Lorusso Interaction of free fatty acids with mitochondria: coupling, uncoupling and permeability transition Biochim. Biophys. Acta 1757 2006 1330 1337 (Pubitemid 44442109)
56. E.B. Zago, R.F. Castilho, and A.E. Vercesi 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 2000 29 33 (Pubitemid 30462253)
57. V.V. Lemeshko Biphasic oxidation of mitochondrial NAD(P)H Biochem. Biophys. Res. Commun. 291 2002 170 175 (Pubitemid 34681155)
58. V. Adam-Vizi, and C. Chinopoulos Bioenergetics and the formation of mitochondrial reactive oxygen species Trends Pharmacol. Sci. 27 2006 639 645 (Pubitemid 44767940)
59. J.B. Hoek, and J. Rydstrom Physiological roles of nicotinamide nucleotide transhydrogenase Biochem. J. 254 1988 1 10
60. E. Graf, J.R. Mahoney, R.G. Bryant, and J.W. Eaton Iron-catalyzed hydroxyl radical formation. Stringent requirement for free iron coordination site J. Biol. Chem. 259 1984 3620 3624 (Pubitemid 14173396)
61. D.O. Lambeth, G.R. Ericsson, M.A. Yorek, and P.D. Ray Implications for in vitro studies of the autoxidation of ferrous ion and the iron-catalyzed autoxidation of dithiothreitol Biochim. Biophys. Acta 719 1982 501 508 (Pubitemid 13191712)
62. D.R. Richardson, and P. Ponka Pyridoxal isonicotinoyl hydrazone and its analogs: potential orally effective iron-chelating agents for the treatment of iron overload disease J. Lab. Clin. Med. 131 1998 306 315
63. J.L. Buss, M. Hermes-Lima, and Ponka P. Pyridoxal isonicotinoyl hydrazone and its analogues Adv. Exp. Med. Biol. 509 2002 205 229
64. http://www.stanford.edu/~cpatton/constants.htm Last accessed January 4th 2012
65. 2+ and includes lipid peroxidation and alterations in membrane proteins Arch. Biochem. Biophys. 308 1994 158 163
66. M. Hermes-Lima, R.F. Castilho, A.R. Meinicke, and A.E. Vercesi Characteristics of Fe(II)ATP complex-induced damage to the rat liver mitochondrial membrane Mol. Cell. Biochem. 145 1995 53 60
67. B.S. Kristal, B.K. Park, and B.P. Yu 4-hydroxyhexenal is a potent inducer of the mitochondrial permeability transition J. Biol. Chem. 271 1996 6033 6038 (Pubitemid 26095405)
68. F. Petrat, H. de Groot, and U. Rauen Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells Biochem. J. 356 2001 61 69 (Pubitemid 34275706)
69. A.L. Nieminen, A.M. Byrne, B. Herman, and J.J. Lemasters Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species Am. J. Physiol. 272 1997 C1286 C1294
70. M.J. Berridge, M.D. Bootman, and P. Lipp Calcium - a life and death signal Nature 395 1998 645 648 (Pubitemid 28475949)
71. D.E. Clapham Calcium signaling Cell 131 2007 1047 1058 (Pubitemid 350258556)