Role of intracellular iron movement and oxidant stress in hepatocellular injury

The Liver: Biology and Pathobiology

Volumn , Issue , 2009, Pages 511-520

  Lemasters, John J ^a   Uchiyama, Akira ^b   Kim, Jae Sung ^c   Kon, Kazuyoshi ^b   Jaeschke, Hartmut ^d  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84888199621     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470747919.ch33     Document Type: Chapter

References (78)

1. Gunawan, B.K. and Kaplowitz, N. (2007) Mechanisms of drug-induced liver disease. Clin Liver Dis, 11 (3), 459-75, v.
2. Labbe, G., Pessayre, D. and Fromenty, B. (2008) Drug-induced liver injury through mitochondrial dysfunction: mechanisms and detection during preclinical safety studies. Fundam Clin Pharmacol, 22 (4), 335-53.
3. Jaeschke, H. and Hasegawa, T. (2006) Role of neutrophils in acute inflammatory liver injury. Liver Int, 26 (8), 912-19.
4. Malhi, H. and Gores, G.J. (2008) Cellular and molecular mechanisms of liver injury. Gastroenterology, 134 (6), 1641-54.
5. Jaeschke, H. and Lemasters, J.J. (2003) Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology, 125 (4), 1246-57.
6. Lemasters, J.J. (2005) Dying a thousand deaths: redundant pathways from different organelles to apoptosis and necrosis. Gastroenterology, 129 (1), 351-60.
7. Gutteridge, J.M. and Halliwell, B. (2000) Free radicals and antioxidants in the year 2000. A historical look to the future. Ann N Y Acad Sci, 899, 136-47.
8. Ma, Y., de Groot, H., Liu, Z., Hider, R.C. and Petrat, F. (2006) Chelation and determination of labile iron in primary hepatocytes by pyridinone fluorescent probes. Biochem J, 395 (1), 49-55.
9. Christ, W.J., Asano, O., Robidoux, A.L.C., Perez, M., Wang, Y., Dubuc, G.R. et al. (1995) E5531, a pure endotoxin antagonist of high potency. Science, 268, 80-83.
10. Kohgo, Y., Ohtake, T., Ikuta, K., Suzuki, Y., Hosoki, Y., Saito, H. et al. (2005) Iron accumulation in alcoholic liver diseases. Alcohol Clin Exp Res, 29 (11 Suppl), 189S-93S.
11. Swanson, C.A. (2003) Iron intake and regulation: implications for iron deficiency and iron overload. Alcohol, 30 (2), 99-102.
12. Petersen, D.R. (2005) Alcohol, iron-associated oxidative stress, and cancer. Alcohol, 35 (3), 243-49.
13. Brewer, G.J. (2007) Iron and copper toxicity in diseases of aging, particularly atherosclerosis and Alzheimer’s disease. Exp Biol Med (Maywood), 232 (2), 323-35.
14. Imeryuz, N., Tahan, V., Sonsuz, A., Eren, F., Uraz, S., Yuksel, M. et al. (2007) Iron preloading aggravates nutritional steatohepatitis in rats by increasing apoptotic cell death. J Hepatol, 47 (6), 851-59.
15. Ramm, G.A. and Ruddell, R.G. (2005) Hepatotoxicity of iron overload: mechanisms of iron-induced hepatic fibrogenesis. Semin Liver Dis, 25 (4), 433-49.
16. Starke, P.E. and Farber, J.L. (1985) Ferric iron and superoxide ions are required for the killing of cultured hepatocytes by hydrogen peroxide. Evidence for the participation of hydroxyl radicals formed by an iron-catalyzed Haber-Weiss reaction. J Biol Chem, 260 (18), 10 099-104.
17. Kyle, M.E., Miccadei, S., Nakae, D. and Farber, J.L. (1987) Superoxide dismutase and catalase protect cultured hepatocytes from the cytotoxicity of acetaminophen. Biochem Biophys Res Commun, 149 (3), 889-96.
18. Dawson, T.L., Gores, G.J., Nieminen, A.L., Herman, B. and Lemasters, J.J. (1993) Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am J Physiol, 264 (4Pt 1), C961-67.
19. Nieminen, A.L., Byrne, A.M., Herman, B. and Lemasters, J.J. (1997) Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. Am J Physiol, 272 (4Pt 1), C1286-94.
20. Lemasters, J.J. (2004) Rusty notions of cell injury. J Hepatol, 40 (4), 696-98.
21. Kerkweg, U., Li, T., de Groot, H. and Rauen, U. (2002) Cold-induced apoptosis of rat liver cells in University of Wisconsin solution: the central role of chelatable iron. Hepatology, 35 (3), 560-67.
22. Rauen, U., Petrat, F., Sustmann, R. and de Groot, H. (2004) Iron-induced mitochondrial permeability transition in cultured hepatocytes. J Hepatol, 40 (4), 607-15.
23. Hochhauser, E., Ben Ari, Z., Pappo, O., Chepurko, Y. and Vidne, B.A. (2005) TPEN attenuates hepatic apoptotic ischemia/reperfusion injury and remote early cardiac dysfunction. Apoptosis, 10 (1), 53-62.
24. Rauen, U., Li, T., Sustmann, R. and de Groot, H. (2004) Protection against iron- and hydrogen peroxide-dependent cell injuries by a novel synthetic iron catalase mimic and its precursor, the iron-free ligand. Free Radic Biol Med, 37 (9), 1369-83.
25. Day, B.J., Fridovich, I. and Crapo, J.D. (1997) Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxide-mediated injury. Arch Biochem Biophys, 347 (2), 256-62.
26. Chen, Y.Y., Ho, K.P., Xia, Q. and Qian, Z.M. (2002) Hydrogen peroxide enhances iron-induced injury in isolated heart and ventricular cardiomyocyte in rats. Mol Cell Biochem, 231 (1-2), 61-68.
27. Ponka, P. and Lok, C.N. (1999) The transferrin receptor: role in health and disease. Int J Biochem Cell Biol, 31 (10), 1111-37.
28. Mackenzie, B. and Garrick, M.D. (2005) Iron imports. II. Iron uptake at the apical membrane in the intestine. Am J Physiol Gastrointest Liver Physiol, 289 (6), G981-86.
29. Tabuchi, M., Yoshimori, T., Yamaguchi, K., Yoshida, T. and Kishi, F. (2000) Human NRAMP2/DMT1, which mediates iron transport across endosomal membranes, is localized to late endosomes and lysosomes in HEp-2 cells. J Biol Chem, 275 (29), 22 220-28.
30. Dong, X.P., Cheng, X., Mills, E., Delling, M., Wang, F., Kurz, T. et al. (2008) The type IV mucolipidosisassociated protein TRPML1 is an endolysosomal iron release channel. Nature, 455 (7215), 992-96.
31. West, A.R. and Oates, P.S. (2008) Subcellular location of heme oxygenase 1 and 2 and divalent metal transporter 1 in relation to endocytotic markers during heme iron absorption. J Gastroenterol Hepatol, 23 (1), 150-58.
32. World Heath Organization (2006) World Health Organization Diabetes Program. http://www.who. int/diabetes/en/.
33. Hunter, D.R., Haworth, R.A. and Southard, J.H. (1976) Relationship between configuration, function, and permeability in calcium-treated mitochondria. J Biol Chem, 251, 5069-77.
34. Bernardi, P. and Forte, M. (2007) The mitochondrial permeability transition pore. Novartis Found Symp, 287, 157-64; discussion 164-69.
35. Kim, J.S., He, L. and Lemasters, J.J. (2003) Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun, 304 (3), 463-70.
36. Zoratti, M. and Szabo, I. (1995) The mitochondrial permeability transition. Biochim Biophys Acta, 1241 (2), 139-76.
37. Halestrap, A.P., Clarke, S.J. and Javadov, S.A. (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res, 61 (3), 372-85.
38. Halestrap, A.P. and Brennerb, C. (2003) The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem, 10 (16), 1507-25.
39. Crompton, M., Virji, S., Doyle, V., Johnson, N. and Ward, J.M. (1999) The mitochondrial permeability transition pore. Biochem Soc Symp, 66, 167-79.
40. Kokoszka, J.E., Waymire, K.G., Levy, S.E., Sligh, J.E., Cai, J., Jones, D.P. et al. (2004) The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature, 427 (6973), 461-65.
41. Krauskopf, A., Eriksson, O., Craigen, W.J., Forte, M.A. and Bernardi, P. (2006) Properties of the permeability transition in VDAC1(-/-) mitochondria. Biochim Biophys Acta, 1757 (5-6), 590-95.
42. Juhaszova, M., Wang, S., Zorov, D.B., Nuss, H.B., Gleichmann, M., Mattson, M.P. et al. (2008) The identity and regulation of the mitochondrial permeability transition pore: where the known meets the unknown. Ann N Y Acad Sci, 1123, 197-212.
43. Forte, M. and Bernardi, P. (2005) Genetic dissection of the permeability transition pore. J Bioenerg Biomembr, 37 (3), 121-28.
44. He, L. and Lemasters, J.J. (2002) Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett, 512 (1-3), 1-7.
45. Petrat, F., de Groot, H. and Rauen, U. (2001) Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem J, 356 (Pt 1), 61-69.
46. Petrat, F., de Groot, H., Sustmann, R. and Rauen, U. (2002) The chelatable iron pool in living cells: a methodically defined quantity. Biol Chem, 383 (3-4), 489-502.
47. Breuer, W., Epsztejn, S., Millgram, P. and Cabantchik, I.Z. (1995) Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am J Physiol, 268 (6Pt 1), C1354-61.
48. Zahrebelski, G., Nieminen, A.L., al Ghoul, K., Qian, T., Herman, B. and Lemasters, J.J. (1995) Progression of subcellular changes during chemical hypoxia to cultured rat hepatocytes: a laser scanning confocal microscopic study. Hepatology, 21 (5), 1361-72.
49. Nieminen, A.L., Saylor, A.K., Tesfai, S.A., Herman, B. and Lemasters, J.J. (1995) Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide. Biochem J, 307 (Pt 1), 99-106.
50. Kon, K., Kim, J.S., Jaeschke, H. and Lemasters, J.J. (2004) Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology, 40 (5), 1170-79.
51. Kon, K., Kim, J.-S., Jaeschke, H. and Lemasters, J.J. (2004) Increase of cytosolic ferrous iron induces the mitochondrial permeability transition in acetaminophen-induced toxicity to mouse hepatocytes [Abstract]. Hepatology, 40 (Suppl 1), 647A.
52. Kim, J.S., Jin, Y. and Lemasters, J.J. (2006) Reactive oxygen species, but not Ca2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol, 290 (5), H2024-34.
53. Sakaida, I., Kayano, K., Wasaki, S., Nagatomi, A., Matsumura, Y. and Okita, K. (1995) Protection against acetaminophen-induced liver injury in vivo by an iron chelator, deferoxamine. Scand J Gastroenterol, 30 (1), 61-67.
54. Schnellmann, J.G., Pumford, N.R., Kusewitt, D.F., Bucci, T.J. and Hinson, J.A. (1999) Deferoxamine delays the development of the hepatotoxicity of acetaminophen in mice. Toxicol Lett, 106 (1), 79-88.
55. Wildenthal, K., Decker, R.S. (1980) The role of lysosomes in the heart. Adv Myocardiol, 2, 349-58.
56. Ollinger, K. and Brunk, U.T. (1995) Cellular injury induced by oxidative stress is mediated through lysosomal damage. Free Radic Biol Med, 19 (5), 565-74.
57. Brunk, U.T., Neuzil, J. and Eaton, J.W. (2001) Lysosomal involvement in apoptosis. Redox Rep, 6 (2), 91-97.
58. Persson, H.L., Yu, Z., Tirosh, O., Eaton, J.W. and Brunk, U.T. (2003) Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Radic Biol Med, 34 (10), 1295-305.
59. Yu, Z., Persson, H.L., Eaton, J.W. and Brunk, U.T. (2003) Intralysosomal iron: a major determinant of oxidant-induced cell death. Free Radic Biol Med, 34 (10), 1243-52.
60. Kurz, T., Gustafsson, B. and Brunk, U.T. (2006) Intralysosomal iron chelation protects against oxidative stress-induced cellular damage. FEBS J, 273 (13), 3106-17.
61. Werneburg, N.W., Guicciardi, M.E., Bronk, S.F. and Gores, G.J. (2002) Tumor necrosis factoralpha-associated lysosomal permeabilization is cathepsin B dependent. Am J Physiol Gastrointest Liver Physiol, 283 (4), G947-56.
62. Werneburg, N.W., Guicciardi, M.E., Bronk, S.F., Kaufmann, S.H. and Gores, G.J. (2007) Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J Biol Chem, 282 (39), 28960-70.
63. Uchiyama, A., Kim, J.S., Kon, K., Jaeschke, H., Ikejima, K., Watanabe, S. et al. (2008) Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury. Hepatology, 48 (5), 1644-54.
64. Liu, Z.D. and Hider, R.C. (2002) Design of clinically useful iron(III)-selective chelators. Med Res Rev, 22 (1), 26-64.
65. Lemasters, J.J., Trollinger, D.R., Qian, T., Cascio, W.E. and Ohata, H. (1999) Confocal imaging of Ca2+, pH, electrical potential, and membrane permeability in single living cells. Methods Enzymol, 302, 341-58.
66. Ying, W.L., Emerson, J., Clarke, M.J. and Sanadi, D.R. (1991) Inhibition of mitochondrial calcium ion transport by an oxo-bridged dinuclear ruthenium ammine complex. Biochemistry, 30 (20), 4949-52.
67. Kehrer, J.P. (2000) The Haber-Weiss reaction and mechanisms of toxicity. Toxicology, 149 (1), 43-50.
68. Cederbaum, A.I. (1989) Oxygen radical generation by microsomes: role of iron and implications for alcohol metabolism and toxicity. Free Radic Biol Med, 7 (5), 559-67.
69. Flatmark, T. and Romslo, I. (1975) Energy-dependent accumulation of iron by isolated rat liver mitochondria. Requirement of reducing equivalents and evidence for a unidirectional flux of Fe(II) across the inner membrane. J Biol Chem, 250 (16), 6433-38.
70. Castilho, R.F., Meinicke, A.R., Almeida, A.M., Hermes-Lima, M. and Vercesi, A.E. (1994) Oxidative damage of mitochondria induced by Fe(II)citrate is potentiated by Ca2+ and includes lipid peroxidation and alterations in membrane proteins. Arch Biochem Biophys, 308 (1), 158-63.
71. Britton, R.S., Leicester, K.L. and Bacon, B.R. (2002) Iron toxicity and chelation therapy. Int J Hematol, 76 (3), 219-28.
72. Feldstein, A.E., Werneburg, N.W., Li, Z., Bronk, S.F. and Gores, G.J. (2006) Bax inhibition protects against free fatty acid-induced lysosomal permeabilization. Am J Physiol Gastrointest Liver Physiol, 290 (6), G1339-46.
73. Rossi, L., Lombardo, M.F., Ciriolo, M.R. and Rotilio, G. (2004) Mitochondrial dysfunction in neurodegenerative diseases associated with copper imbalance. Neurochem Res, 29 (3), 493-504.
74. She, H., Xiong, S., Lin, M., Zandi, E., Giulivi, C. and Tsukamoto, H. (2002) Iron activates NF-kappaB in Kupffer cells. Am J Physiol Gastrointest Liver Physiol, 283 (3), G719-26.
75. Chen, L., Xiong, S., She, H., Lin, S.W., Wang, J. and Tsukamoto, H. (2007) Iron causes interactions of TAK1, p21ras, and phosphatidylinositol 3-kinase in caveolae to activate IkappaB kinase in hepatic macrophages. J Biol Chem, 282 (8), 5582-88.
76. Xiong, S., She, H., Takeuchi, H., Han, B., Engelhardt, J.F., Barton, C.H. et al. (2003) Signaling role of intracellular iron in NF-kappaB activation. J Biol Chem, 278 (20), 17646-54.
77. Wang, G.L. and Semenza, G.L. (1993) Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood, 82 (12), 3610-15.
78. Wenger, R.H. (2002) Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J, 16 (10), 1151-62.