N-acetylcysteine does not protect HepG2 cells against acetaminophen-induced apoptosis

Basic and Clinical Pharmacology and Toxicology

Volumn 94, Issue 5, 2004, Pages 213-225

  Manov, Irena ^a   Hirsh, Mark ^a   Iancu, Theodore C ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CALCIUM; GLUTATHIONE; LIPOCORTIN 5; PARACETAMOL; PHOSPHATIDYLSERINE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL NUCLEUS; CELL PROTECTION; CELL STRAIN HEPG2; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIPLOIDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INCUBATION TIME; LIVER TOXICITY; MITOCHONDRION; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

EID: 2442680168     PISSN: 17427835     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1742-7843.2004.pto940504.x     Document Type: Article

References (64)

1. Adamson, G. M. & A. W. Harman: Oxidative stress in cultured hepatocytes exposed to acetaminophen. Biochem. Pharmacol. 1993, 45, 2289-2294.
2. Boulares, A. H., A. J. Zoltoski, B. A. Stoica, O. Cuvillier & M. E. Smulson: Acetaminophen induces a caspase-dependent and Bcl-XL sensitive apoptosis in human hepatoma cells and lymphocytes. Pharmacology Toxicology 2002, 90, 38-50.
3. Bruno, M. K., E. A. Khairallah & S. D. Cohen: Inhibition of protein phosphatase activity and changes in protein phosphorylation following acetaminophen exposure in cultured mouse hepatocytes. Toxicol. Appl. Pharmacol. 1998, 153, 119-132.
4. Cohen, G.: Caspases: the executioners of apoptosis. Biochem J. 1997, 326, 1-16.
5. Coppola, S. & L. Ghibelli: GSH extrusion and the mitochondrial pathway of apoptotic signaling. Biochem. Soc. Trans. 2000, 28, 56-61.
6. Dai, Y. & A. I. Cederbaum: Cytotoxicity of acetaminophen in human cytochrome P4502E1-transfected HepG2 cells. J. Pharmacol. Exp. Therap. 1995, 273, 1497-1505.
7. Desmet, V. J. & R. D. Vos: Structural analysis of acute liver injury. In: Mechanisms of hepatocyte injury and death. Eds.: D. Kepler, H. Popper, L. Bianchi & W. Reutter. Lancaster MTP Press Ltd (38th Falk Symposium, Basel, 1983), 1984, pp. 11-30.
8. Dong, Z., P. Saikumar, J. M. Weinberg & M. A. Venkatachalam: Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Amer. J. Pathol. 1977, 151, 1205-1213.
9. + in cell physiology and pathophysiology. Cell Calcium 2000, 28, 339-348.
10. Dyugovskaya, L., P. Lavie & L. Lavie: Increased adhesion molecules expression and production of reactive oxygen species in leukocytes of sleep apnea patients. Am. J. Respir. Crit. Care. Med. 2002, 165, 934-939.
11. Ferret, P.-J., R. Hammoud, M. Tulliez, A. Tran, H. Trebeden, P. Jaffray, B. Malassagne, Y. Calmus, B. Weill & F. Batteux: Detoxification of reactive oxygen species by a nonpeptidyl mimic of superoxide dismutase cures acetaminophen-induced acute liver failure in the mouse. Hepatology 2001, 33, 1173-1180.
12. Fujimura, H., N. Kawasaki, T. Tanimoto, H. Sasaki & T. Suzuki: Effect of acetaminophen on the ultrastructure of isolated rat hepatocytes. Exp. Toxicol. Pathol. 1995, 47, 345-351.
13. Gallo, V., A. Kingsbury, R. Balazs & O. S. Jogensen: The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 1987, 7, 2203-2213.
14. Ghadially, F. N.: Ultrastructural pathology of the cell and matrix. Butterworth-Heinemann, Boston, 1997.
15. Gomez-Lechon, M. J., E. O'Connor, J. V. Castell & R. Jover: Sensitive markers used to identify compounds that trigger apoptosis in cultured hepatocytes. Toxicol. Sci. 2002, 65, 299-308.
16. Gujral, J. S., T. R. Knight, A. Farhood, M. L. Bajt & H. Jaeschke: Mode of cell death after acetaminophen overdose in mice: apoptosis or oncotic necrosis? Toxicol. Sci. 2002, 67, 322-328.
17. Hammond, C. L., T. K. Lee & N. Ballatori: Novel roles for glutathione in gene expression, cell death, and membrane transport of organic solutes. J. Hepatol. 2001, 34, 946-954.
18. Hentze, H., M. Latta, G. Künstle, R. Lucas & A. Wendel: Redox control of hepatic cell death. Toxicol. Lett. 2003, 139, 111-118.
19. Holownia, A., J. Mapoles, J. F. Menez & J. J. Braszko: Acetaminophen metabolism and cytotoxicity in PC12 cells transfected with cytochrome P4502E1. J. Mol. Med. 1997, 75, 522-527.
20. Jones, A. L.: Mechanism of action and value of N-acetylcysteine in the treatment of early and late acetaminophen poisoning: a critical review. J. Toxicol. Clin. Toxicol. 1998, 36, 277-285.
21. Krishna, R. & L. D. Mayer: Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur. J. Pharm. Sci. 2000, 11, 265-283.
22. Kroemer, G. & J. C. Reed: Mitochondrial control of cell death. Nat. Med. 2000, 6, 513-519.
23. Lawson, J. A., M. A. Fisher, C. A. Simmons, A. Farhood & H. Jaeschke: Inhibition of FAS receptor (CD95)-induced hepatic caspase activation and apoptosis by acetaminophen in mice. Toxicol. Appl. Pharmacol. 1999, 156, 179-186.
24. LeBlanc, G. A.: Hepatic vectoral transport of xenobiotics. Chem. Biol. Interact. 1994, 90, 101-120.
25. Lepri, E., C. Gambelunghe, A. Fioravanti, M. Pedini, A. Micheletti & S. Rufini: N-acetylcysteine increases apoptosis induced by H(2)O(2) and mo-antiFas triggering in a 3DO hybridoma cell line. Cell Biochem. Funct. 2000, 18, 201-208.
26. Levin, S., T. J. Bucci, S. M. Cohen, A.S. Fix, J. E. Hardisty, E. K. LeGrand, R. R. Maronpot & B. F. Trump: The nomenclature of cell death: Recommendations of an ad hoc Committee of the Society of Toxicologic Pathologists. Toxicol. Pathol. 1999, 27, 484-490.
27. Lowry, O. H., N. J. Rosenbough, A. L. Farr & R. J. Randall: Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265-275.
28. Mandel, H., C. Hartman, D. Berkowitz, O. N. Elpeleg, I. Manov & T. C. Iancu: The hepatic mitochondrial DNA depletion syndrome: ultrastructural changes in liver biopsies. Hepatology 2001, 34, 776-784.
29. Manov, I., M. Hirsh & T. C. Iancu: Acetaminophen hepatotoxicity and mechanisms of its protection by N-acetylcysteine: a study of Hep3B cells. Exp. Toxicol. Pathol. 2002, 53, 489-500.
30. Manyike, P. T., E. D. Kharasch, T. F. Kalhorn & J. T. Slattery: Contribution of CYP2E1 and CYP3A to acetaminophen reactive metabolite formation. Clin. Pharmacol. Ther. 2000, 67, 275-282.
31. McCloskey, P., R. J. Edwards, R. Tootle, C. Selden, E. Roberts & H. J. F. Hodgson: Resistance of the three immortalized human hepatocytes cell lines to acetaminophen and N-acetyl-p-benzoquinoneimine toxicity. J. Hepatol. 1999, 31, 841-851.
32. Minta, A., J. P. Kao & R. Y. Tsien: Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 1989, 264, 8171-8178.
33. Nakayama, G. R., M. C. Caton, M. P. Nova & Z. Parandoosh: Assessment of the Alamar Blue assay for cellular growth and viability in vitro. J. Immunol. Meth. 1997, 204, 205-208.
34. Nelson, S. D.: Mechanisms of the formation and disposition of reactive metabolites that can cause acute liver injure. Drug Metab. Rev. 1995, 27, 147-177.
35. Nicod, L., C. Viollon, A. Rigner, A. Jacqueson & L. Richert: Rifampicin and isoniazid increase acetaminophen and isoniazid cytotoxicity in human HepG2 hepatoma cells. Hum. Exp. Toxicol. 1997, 16, 28-34.
36. Nicoletti, I., G. Migliorati, M. C. Pagliacci, F. Grignani & C. Riccardi: A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Meth. 1991, 139, 271-279.
37. Payen, L., A. Courtois, J.-P. Campion, A. Guillouzo & O. Fardel: Characterization and inhibition by wide range of xenobiotics of organic anion excretion by primary human hepatocytes. Biochem. Pharmacol. 2000, 60, 1967-1975.
38. Prescott, L. F.: Paracetamol: past, present, and future. Amer. J. Ther. 2000, 7, 143-147.
39. Pumford, N. R., N. C. Halmes & J. A. Hinson: Covalent binding of xenobiotics to specific proteins in the liver. Drug Metab. Rev. 1997, 29, 39-57.
40. Ray, S. D., L. Kamendulis, M. W. Gurule, R. D. Yorkin & G. B. Corcoran: Ca2+ antagonists inhibit DNA fragmentation and toxic cell death induced by acetaminophen. FASEB J. 1993, 7, 453-463.
41. Ray, S. D., V. R. Mumaw, R. R. Raje & M. W. Fariss: Protection of acetaminophen-induced hepatocellular apoptosis and necrosis by cholesteryl hemisuccinate pretreatment. J. Pharmacol. Exp.-Therap. 1996, 279, 1470-1483.
42. Ray, S. D., M. A. Kumar & D. Bagchi: A novel proanthocyanidin IH636 grape seed extract increases in vivo Bcl-XL expression and prevents acetaminophen-induced programmed and unprogrammed cell death in mouse liver. Arch. Biochem. Biophys. 1999, 369, 42-58.
43. Ray, S. D. & N. Jena: A hepatotoxic dose of acetaminophen modulates expression of BCL-2, BCL-X(L) and BCL-X(S) during apoptotic and necrotic death of mouse liver cells in vivo. Arch. Toxicol. 2000, 73, 594-606.
44. Roelofsen, H., T. A. Vos, I. J., Schippers, F. Kuipers, H. Koning, H. Moshage, P. L. Jansen & M. Muller: Increasing level of the multidrug resistance protein in lateral membranes of proliferating hepatocyte-derived cells. Gastroenterology 1997, 112, 511-521.
45. Rumack, B. H., R. C. Peterson, G. G. Koch & I. A. Amara: Acetaminophen overdose. Arch. Intern. Med. 1981, 141, 380-389.
46. Saetersdal, T. S., R. Myklebust, N. P. Berg Justesen, H. Engedal, W & W. C. Olsen: Calcium containing particles in mitochondria of heart muscle cells as shown by cryo-ultramicrotomy and X-ray microanalysis. Cell. Tissue Res. 1977, 182, 17-31.
47. Schippers, I. J., H. Moshage, H. Roelofsen, M. Muller, H. S. Heymans, M. Ruiters & F. Kuipers: Immortalized human hepatocytes as a tool for the study of hepatocytic (de-) differentiation. Cell. Biol. Toxicol. 1997, 13, 375-386.
48. Schmidt, L. E., K. Dalhoff & H. E. Poulsen: Acute versus chronic alcohol consumption in acetaminophen-induced hepatotoxicity. Hepatology 2002, 35, 876-882.
49. Shear, N. H., I. M. Malkiewicz, D. Klein, G. Koren, S. Randor & M. G. Neuman: Acetaminophen-induced toxicity in human epidermoid cell line A431 and hepatoblastoma cell line HepG2, in vitro, is diminished by silymarin. Skin Pharmacol. 1995, 8, 279-291.
50. Shen, J. C., T. T. Wang, S. Chang & S. D. Hursting: Mechanistic studies of the effects of the retinoid N-(4-hydroxyphenyl) retinamide on prostate cancer cell growth and apoptosis. Mol. Carcinog. 1999, 24, 160-168.
51. Shen, H.-M., C.-F. Yang, J. Liu & C.-N. Ong: Dual role of glutathione in selenite-induced oxidative stress and apoptosis in human hepatoma cells. Free Radic. Biol. Med. 2000, 28, 1115-1124.
52. Smilkstein, M. J., G. L. Knapp, K. W. Kulig & B. H. Rumack: Efficacy of oral N-acetylcysteine in the treatment of acetaminophen overdose. Analysis of the national multicenter study (1976 to 1985). New Engl. J. Med 1988, 319, 1557-1562.
53. Sumida, A., S. Fukuen, I. Yamamoto, H. Matsuda, M. Naohara & J. Azuma: Quantitative analysis of constitutive and inducible SYPs mRNA expression in the HepG2 cell line using reverse transcription-competitive PCR. Biochem. Biophys. Res. Commun. 2000, 267, 756-760.
54. Testai, E.: The drug-metabolizing enzymatic system and the experimental tools used for in vitro toxicology for metabolic studies. Cell. Biol. Toxicol. 2001, 17, 272-285.
55. Tietze, F.: Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: application to mammalian blood and other tissues. Anal. Biochem. 1969, 27, 502-522.
56. Tonge, R. P., E. J. Kelly, S. A. Bruschi, T. Kalhorn, D. L. Eaton, D. Nebert & S. D. Nelson: Role of CYP1A2 in the hepatotoxicity of acetaminophen: investigation using Cyp1a2 null mice. Toxicol. Appl. Pharmacol. 1998, 153, 102-108.
57. Vandenberghe, P. A. & J. L. Ceuppens: Flow cytometric measurement of cytoplasmic free calcium in human peripheral blood T lymphocytes with fluo-3, a new fluorescent calcium indicator. J. Immunol. Meth. 1990, 127, 197-205.
58. Vandeputte, C., I. Guizon, I. Genestie-Denis, B. Vannier & G. Lorenzon: A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell. Biol. Toxicol. 1994, 10, 415-421.
59. Villagrasa, V., J. Cortijo, M. Marti-Cabrera, J. L. Ortiz, L. Berto, A. Esteras, L. Bruseghini & E. J. Morcillo: Inhibitory effects of N-acetylcysteine on superoxide anion generation in human polymorphonuclear leukocytes. J. Pharm. Pharmacol. 1997, 49, 525-529.
60. Wiger, R., H. S. Finstad, J. K. Hongslo, K. Haug & J. A. Holme: Paracetamol inhibits cell cycling and induces apoptosis in HL-60 cells. Pharmacology & Toxicology 1997, 81, 285-293.
61. Wroblewski, J., R. Wroblewski, C. Mory & C. Colliex: Elemental analysis and fine structure of mitochondrial granules in growth plate chondrocytes studied by electron energy loss spectroscopy and energy dispersive X-ray microanalysis. Scanning. Microsc. 1991, 5, 885-892.
62. Yu, S. P., L. M. Canzoniero & D. W. Choi: Ion homeostasis and apoptosis. Curr. Opin. Cell. Biol. 2001, 13, 405-411.
63. Xie, Z., P. Kometiani, J. Liu, J. Li, J. I. Shapiro & A. Askari: Intracellular reactive oxygen species mediate the linkage of Na+/K+-ATPase to hypertrophy and its marker genes in cardiac myocytes. J. Biol. Chem. 1999, 247, 19323-19328.
64. Zimmerman, H. J. & W. C. Maddrey: Acetaminophen (paracetamol) hepatotoxicity with regular intake of alcohol: analysis of instances of therapeutic misadventure. Hepatology 1995, 22, 767-773.