Journal of Hepatology
Volume 42, Issue 1 , Pages 110-116 , January 2005

Involvement of mitochondrial permeability transition in acetaminophen-induced liver injury in mice

Received 27 April 2004 ,Revised 16 September 2004 ,Accepted 21 September 2004.

References 

  1. Mitchell JR, Jollow DJ, Potter WZ, Davis DC, Gillette JR, Brodie BB. Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism. J Pharmacol Exp Ther. 1973;187:185–194
  2. Dahlin DC, Miwa GT, Lu AY, Nelson SD. N-Acetyl-p-benzoquinone imine: a cytochrome P-450-mediated oxidation product of acetaminophen. Proc Natl Acad Sci USA. 1984;81:1327–1331
  3. Jollow DJ, Mitchell JR, Potter WZ, Davis DC, Gillette JR, Brodie BB. Acetaminophen-induced hepatic necrosis. II. Role of covalent binding in vivo. J Pharmacol Exp Ther. 1973;187:195–202
  4. Mitchell JR, Jollow DJ, Potter WZ, Gillette JR, Brodie BB. Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J Pharmacol Exp Ther. 1973;187:211–217
  5. Manautou JE, Emeigh Hart SG, Khairallah EA, Cohen SD. Protection against acetaminophen hepatotoxicity by a single dose of clofibrate: effects on selective protein arylation and glutathione depletion. Fundam Appl Toxicol. 1996;29:229–237
  6. Tarloff JB, Khairallah EA, Cohen SD, Goldstein RS. Sex- and age-dependent acetaminophen hepato- and nephrotoxicity in Sprague–Dawley rats: role of tissue accumulation, nonprotein sulfhydryl depletion, and covalent binding. Fundam Appl Toxicol. 1996;30:13–22
  7. Schnellmann JG, Pumford NR, Kusewitt DF, Bucci TJ, Hinson JA. Deferoxamine delays the development of the hepatotoxicity of acetaminophen in mice. Toxicol Lett. 1999;106:79–88
  8. Cohen SD, Pumford NR, Khairallah EA, Boekelheide K, Pohl LR, Amouzadeh HR, et al. Selective protein covalent binding and target organ toxicity. Toxicol Appl Pharmacol. 1997;143:1–12
  9. Qiu Y, Benet LZ, Burlingame AL. Identification of the hepatic protein targets of reactive metabolites of acetaminophen in vivo in mice using two-dimensional gel electrophoresis and mass spectrometry. J Biol Chem. 1998;273:17940–17953
  10. Moore M, Thor H, Moore G, Nelson S, Moldeus P, Orrenius S. The toxicity of acetaminophen and N-acetyl-p-benzoquinone imine in isolated hepatocytes is associated with thiol depletion and increased cytosolic Ca2+. J Biol Chem. 1985;260:13035–13040
  11. Burcham PC, Harman AW. Acetaminophen toxicity results in site-specific mitochondrial damage in isolated mouse hepatocytes. J Biol Chem. 1991;266:5049–5054
  12. Harman AW, Kyle ME, Serroni A, Farber JL. The killing of cultured hepatocytes by N-acetyl-p-benzoquinone imine (NAPQI) as a model of the cytotoxicity of acetaminophen. Biochem Pharmacol. 1991;41:1111–1117
  13. Nazareth WM, Sethi JK, McLean AE. Effect of paracetamol on mitochondrial membrane function in rat liver slices. Biochem Pharmacol. 1991;42:931–936
  14. Parmar DV, Ahmed G, Khandkar MA, Katyare SS. Mitochondrial ATPase: a target for paracetamol-induced hepatotoxicity. Eur J Pharmacol. 1995;293:225–229
  15. Gupta S, Rogers LK, Taylor SK, Smith CV. Inhibition of carbamyl phosphate synthetase-I and glutamine synthetase by hepatotoxic doses of acetaminophen in mice. Toxicol Appl Pharmacol. 1997;146:317–327
  16. Bernardi P. The permeability transition pore control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim Biophys Acta. 1996;1275:5–9
  17. Lemasters JJ, Nieminen AL, Qian T, Trost LC, Elmore SP, Nishimura Y, et al. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim Biophys Acta. 1998;1366:177–196
  18. Masubuchi Y, Nakayama S, Horie T. Role of mitochondrial permeability transition in diclofenac-induced hepatocyte injury in rats. Hepatology. 2002;35:544–551
  19. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta. 1995;1241:139–176
  20. Gujral JS, Knight TR, Farhood A, Bajt ML, Jaeschke H. Mode of cell death after acetaminophen overdose in mice: apoptosis or oncotic necrosis?. Toxicol Sci. 2002;67:322–328
  21. Jaeschke H, Knight TR, Bajt ML. The role of oxidant stress and reactive nitrogen species in acetaminophen hepatotoxicity. Toxicol Lett. 2003;144:279–288
  22. James LP, McCullough SS, Lamps LW, Hinson JA. Effect of N-acetylcysteine on acetaminophen toxicity in mice: relationship to reactive nitrogen and cytokine formation. Toxicol Sci. 2003;75:458–467
  23. Schneider WC, Hogeboom GH. Intracellular distribution of enzymes. V. Further studies on the distribution of cytochrome c in liver homogenate. J Biol Chem. 1950;183:123–128
  24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem. 1951;193:265–275
  25. Keller DA, Menzel DB. Picomole analysis of glutathione, glutathione disulfide, glutathione S-sulfonate, and cysteine S-sulfonate by high-performance liquid chromatography. Anal Biochem. 1985;151:418–423
  26. Emaus RK, Grunwald R, Lemasters JJ. Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: spectral and metabolic properties. Biochim Biophys Acta. 1986;850:436–448
  27. Berg-Candolfi M, Candolfi E, Benet LZ. Suppression of intestinal and hepatic cytochrome P4503A in murine toxoplasma infection Effects of N-acetylcysteine and N(G)-monomethyl-l-arginine on the hepatic suppression. Xenobiotica. 1996;26:381–394
  28. Lee SS, Buters JT, Pineau T, Fernandez-Salguero P, Gonzalez FJ. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J Biol Chem. 1996;271:12063–12067
  29. Sinclair JF, Szakacs JG, Wood SG, Walton HS, Bement JL, Gonzalez FJ, et al. Short-term treatment with alcohols causes hepatic steatosis and enhances acetaminophen hepatotoxicity in Cyp2e1(−/−) mice. Toxicol Appl Pharmacol. 2000;168:114–122
  30. Zhang J, Huang W, Chua SS, Wei P, Moore DD. Modulation of acetaminophen-induced hepatotoxicity by the xenobiotic receptor CAR. Science. 2002;298:422–424
  31. Wolf A, Trendelenburg CF, Diez-Fernandez C, Prieto P, Houy S, Trommer WE, et al. Cyclosporine A-induced oxidative stress in rat hepatocytes. J Pharmacol Exp Ther. 1997;280:1328–1334
  32. Knight TR, Kurtz A, Bajt ML, Hinson JA, Jaeschke H. Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: role of mitochondrial oxidant stress. Toxicol Sci. 2001;62:212–220
  33. Jaeschke H. Glutathione disulfide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: the protective effect of allopurinol. J Pharmacol Exp Ther. 1990;255:935–941
  34. Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun. 2003;304:463–470
  35. Beales D, McLean AE. Protection in the late stages of paracetamol-induced liver cell injury with fructose, cyslosporin A and trifluoperazine. Toxicology. 1996;107:201–208
  36. Haouzi D, Cohen I, Vieira HL, Poncet D, Boya P, Castedo M, et al. Mitochondrial permeability transition as a novel principle of hepatorenal toxicity in vivo. Apoptosis. 2002;7:395–405
  37. Powis G, Svingen BA, Dahlin DC, Nelson SD. Enzymatic and non-enzymatic reduction of N-acetyl-p-benzoquinone imine and some properties of the N-acetyl-p-benzosemiquinone imine radical. Biochem Pharmacol. 1984;33:2367–2370
  38. Weis M, Moore GA, Cotgreave IA, Nelson SD, Moldeus P. Quinone imine-induced Ca2+ release from isolated rat liver mitochondria. Chem Biol Interact. 1990;76:227–240
  39. Brustovetsky N, Klingenberg M. Mitochondrial ADP/ATP carrier can be reversibly converted into a large channel by Ca2+. Biochemistry. 1996;35:8483–8488
  40. Grewal KK, Racz WJ. Intracellular calcium disruption as a secondary event in acetaminophen-induced hepatotoxicity. Can J Physiol Pharmacol. 1993;71:26–33
  41. Petronilli V, Costantini P, Scorrano L, Colonna R, Passamonti S, Bernardi P. The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J Biol Chem. 1994;269:16638–16642
  42. Bourdi M, Masubuchi Y, Reilly TP, Amouzadeh HR, Martin JL, George JW, et al. Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase. Hepatology. 2002;35:289–298
  43. Gardner CR, Laskin JD, Dambach DM, Sacco M, Durham SK, Bruno MK, et al. Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: potential role of tumor necrosis factor-alpha and interleukin-10. Toxicol Appl Pharmacol. 2002;184:27–36
  44. Radi R, Cassina A, Hodara R, Quijano C, Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med. 2002;33:1451–1464
  45. Cai J, Yang J, Jones DP. Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta. 1998;1366:139–149
  46. Eguchi Y, Shimizu S, Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 1997;57:1835–1840
  47. El-Hassan H, Anwar K, Macanas-Pirard P, Crabtree M, Chow SC, Johnson VL, et al. Involvement of mitochondria in acetaminophen-induced apoptosis and hepatic injury: roles of cytochrome c, Bax, Bid, and caspases. Toxicol Appl Pharmacol. 2003;191:118–129

PII: S0168-8278(04)00429-5

doi: 10.1016/j.jhep.2004.09.015

Journal of Hepatology
Volume 42, Issue 1 , Pages 110-116 , January 2005

Article Tools

* Image Usage & Resolution