Mitochondrial permeability transition in rat hepatocytes after anoxia/reoxygenation: Role of Ca 2+-dependent mitochondrial formation of reactive oxygen species

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 302, Issue 7, 2012, Pages

  Kim, Jae Sung ^a   Wang, Jin Hee ^a   Lemasters, John J ^b  

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

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cell death; Ischemia; Reperfusion

Indexed keywords

AMINOQUINOLINE DERIVATIVE; ANTIOXIDANT; APOCYNIN; CALCEIN; CALCIUM ION; CYCLOSPORIN A; DEFEROXAMINE MESYLATE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; N,N' DIPHENYLPHENYLENEDIAMINE; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; TETRAMETHYLRHODAMINE METHYL ESTER;

ANIMAL CELL; ANOXIA; APOPTOSIS; ARTICLE; CELL DEATH; FLUOROMETRY; IMMUNOBLOTTING; LIVER CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; REOXYGENATION;

ANIMALS; APOPTOSIS; CALCIUM; CALCIUM SIGNALING; HEPATOCYTES; INTRACELLULAR MEMBRANES; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NECROSIS; OXYGEN; PERMEABILITY; RATS; REACTIVE OXYGEN SPECIES;

EID: 84859477469     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00082.2011     Document Type: Article

References (50)

1. 2+-dependent induction of permeability transition in rat brain mitochondria. Amino Acids 38: 431-437, 2010.
2. Berger NA, Petzold SJ. Identification of minimal size requirements of DNA for activation of poly(ADP-ribose) polymerase. Biochemistry 24: 4352-4355, 1985.
3. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155, 1999.
4. Bhogal RH, Curbishley SM, Weston CJ, Adams DH, Afford SC. Reactive oxygen species mediate human hepatocyte injury during hypoxia/ reoxygenation. Liver Transpl 16: 1303-1313, 2010.
5. Black D, Bird MA, Samson CM, Lyman S, Lange PA, Schrum LW, Qian T, Lemasters JJ, Brenner DA, Rippe RA, Behrns KE. Primary cirrhotic hepatocytes resist TGFbeta-induced apoptosis through a ROSdependent mechanism. J Hepatol 40: 942-951, 2004.
6. Bond JM, Herman B, Lemasters JJ. Protection by acidotic pH against anoxia/reoxygenation injury to rat neonatal cardiac myocytes. Biochem Biophys Res Commun 179: 798-803, 1991.
7. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287: C817-C833, 2004.
8. 2+to the mitochondrial permeability transition induced by tert-butylhydroperoxide in rat hepatocytes. Hepatology 29: 1523-1531, 1999.
9. Cathcart R, Schwiers E, Ames BN. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal Biochem 134: 111-116, 1983.
10. Chen X, Ding WX, Ni HM, Gao W, Shi YH, Gambotto AA, Fan J, Beg AA, Yin XM. Bid-independent mitochondrial activation in tumor necrosis factor alpha-induced apoptosis and liver injury. Mol Cell Biol 27: 541-553, 2007.
11. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255: 357-360, 1988.
12. Currin RT, Gores GJ, Thurman RG, Lemasters JJ. Protection by acidotic pH against anoxic cell killing in perfused rat liver: evidence for a pH paradox. FASEB J 5: 207-210, 1991.
13. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42, 2000.
14. Garcia-Rivas GJ, Carvajal K, Correa F, Zazueta C. Ru360, a specific mitochondrial calcium uptake inhibitor, improves cardiac post-ischaemic functional recovery in rats in vivo. Br J Pharmacol 149: 829-837, 2006.
15. Gunter TE, Pfeiffer DR. Mechanisms by which mitochondria transport calcium. Am J Physiol Cell Physiol 258: C755-C786, 1990.
16. Hatano E, Bradham CA, Stark A, Iimuro Y, Lemasters JJ, Brenner DA. The mitochondrial permeability transition augments Fas-induced apoptosis in mouse hepatocytes. J Biol Chem 275: 11814-11823, 2000.
17. He L, Lemasters JJ. Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett 512: 1-7, 2002.
18. Kim JS, Ohshima S, Pediaditakis P, Lemasters JJ. Nitric oxide protects rat hepatocytes against reperfusion injury mediated by the mitochondrial permeability transition. Hepatology 39: 1533-1543, 2004.
19. Kim JS, Qian T, Lemasters JJ. Mitochondrial permeability transition in the switch from necrotic to apoptotic cell death in ischemic rat hepatocytes. Gastroenterology 124: 494-503, 2003.
20. Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304: 463-470, 2003.
21. 2+overloading, trigger pH-and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 290: H2024-H2034, 2006.
22. Kon K, Kim JS, Jaeschke H, Lemasters JJ. Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 40: 1170-1179, 2004.
23. Lemasters JJ. The mitochondrial permeability transition and the calcium, oxygen and pH paradoxes: one paradox after another. Cardiovasc Res 44: 470-473, 1999.
24. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 1787: 1395-1401, 2009.
25. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157, 1996.
26. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312: 159-163, 1985.
27. Murillo MM, Carmona-Cuenca I, Del CG, Ortiz C, Roncero C, Sanchez A, Fernandez M, Fabregat I. Activation of NADPH oxidase by transforming growth factor-beta in hepatocytes mediates up-regulation of epidermal growth factor receptor ligands through a nuclear factor-kappaBdependent mechanism. Biochem J 405: 251-259, 2007.
28. Nayler WG, Poole-Wilson PA, Williams A. Hypoxia and calcium. J Mol Cell Cardiol 11: 683-706, 1979.
29. Nicoud IB, Knox CD, Jones CM, Anderson CD, Pierce JM, Belous AE, Earl TM, Chari RS. 2-APB protects against liver ischemia-reperfusion injury by reducing cellular and mitochondrial calcium uptake. Am J Physiol Gastrointest Liver Physiol 293: G623-G630, 2007.
30. Nieminen AL, Byrne AM, Herman B, Lemasters JJ. Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. Am J Physiol Cell Physiol 272: C1286-C1294, 1997.
31. Nieminen AL, Gores GJ, Bond JM, Imberti R, Herman B, Lemasters JJ. A novel cytotoxicity screening assay using a multiwell fluorescence scanner. Toxicol Appl Pharmacol 115: 147-155, 1992.
32. Panov A, Dikalov S, Shalbuyeva N, Hemendinger R, Greenamyre JT, Rosenfeld J. Species-and tissue-specific relationships between mitochondrial permeability transition and generation of ROS in brain and liver mitochondria of rats and mice. Am J Physiol Cell Physiol 292: C708-C718, 2007.
33. Piper HM. Energy deficiency, calcium overload or oxidative stress: possible causes of irreversible ischemic myocardial injury. Klin Wochenschr 67: 465-476, 1989.
34. Pronobesh C, Dagagi AV, Pallab C, Kumar WA. Protective role of the calcium channel blocker amlodipine against mitochondrial injury in ischemia and reperfusion injury of rat liver. Acta Pharm 58: 421-428, 2008.
35. Qian T, Herman B, Lemasters JJ. The mitochondrial permeability transition mediates both necrotic and apoptotic death of hepatocytes exposed to Br-A23187. Toxicol Appl Pharmacol 154: 117-125, 1999.
36. Qian T, Nieminen AL, Herman B, Lemasters JJ. Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes. Am J Physiol Cell Physiol 273: C1783-C1792, 1997.
37. Regueira T, Lepper PM, Brandt S, Ochs M, Vuda M, Takala J, Jakob SM, Djafarzadeh S. Hypoxia inducible factor-1 alpha induction by tumour necrosis factor-alpha, but not by toll-like receptor agonists, modulates cellular respiration in cultured human hepatocytes. Liver Int 29: 1582-1592, 2009.
38. Reinehr R, Becker S, Eberle A, Grether-Beck S, Haussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J Biol Chem 280: 27179-27194, 2005.
39. Suleiman MS, Halestrap AP, Griffiths EJ. Mitochondria: a target for myocardial protection. Pharmacol Ther 89: 29-46, 2001.
40. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441-446, 1999.
41. Theruvath TP, Zhong Z, Pediaditakis P, Ramshesh VK, Currin RT, Tikunov A, Holmuhamedov E, Lemasters JJ. Minocycline and N-methyl-4-isoleucine cyclosporin (NIM811) mitigate storage/reperfusion injury after rat liver transplantation through suppression of the mitochondrial permeability transition. Hepatology 47: 236-246, 2008.
42. 2+transients during the contractile cycle in adult rabbit cardiac myocytes. Biochem Biophys Res Commun 236: 738-742, 1997.
43. Turrens JF, Alexandre A, Lehninger AL. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237: 408-414, 1985.
44. Uchiyama A, Kim JS, Kon K, Jaeschke H, Ikejima K, Watanabe S, Lemasters JJ. Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury. Hepatology 48: 1644-1654, 2008.
45. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730, 2001.
46. Weinberg JM. The cell biology of ischemic renal injury. Kidney Int 39: 476-500, 1991.
47. Zager RA, Schimpf BA, Gmur DJ. Physiological pH effects on posthypoxic proximal tubular injury. Circ Res 72: 837-846, 1993.
48. Zhao Y, Ding WX, Qian T, Watkins S, Lemasters JJ, Yin XM. Bid activates multiple mitochondrial apoptotic mechanisms in primary hepatocytes after death receptor engagement. Gastroenterology 125: 854-867, 2003.
49. Zhou W, Zhang Y, Hosch MS, Lang A, Zwacka RM, Engelhardt JF. Subcellular site of superoxide dismutase expression differentially controls AP-1 activity and injury in mouse liver following ischemia-reperfusion. Hepatology 33: 902-914, 2001.
50. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 1757: 509-517, 2006.