Curcumin exposure modulates multiple pro-apoptotic and anti-apoptotic signaling pathways to antagonize acetaminophen-induced toxicity

Current Neurovascular Research

Volumn 9, Issue 1, 2012, Pages 58-71

  Bulku, Elida ^a,c   Stohs, Sidney J ^b   Cicero, Lorraine ^c   Brooks, Tracy ^a   Halley, Herb ^a   Ray, Sidhartha D ^a,b,c  

^a MANCHESTER UNIVERSITY   (United States)

^b CREIGHTON UNIVERSITY SCHOOL OF PHARMACY AND HEALTH PROFESSIONS   (United States)

^c LONG ISLAND UNIVERSITY   (United States)

Author keywords

Acetaminophen; Antioxidants; Apoptosis; Bax; Bcl 2; Caspase 3; Curcumin; DNA fragmentation; Hepatotoxicity; Lipid peroxidation; Mdm2; Necrosis; Oxidative stress; p53

Indexed keywords

ALANINE AMINOTRANSFERASE; CASPASE 3; CURCUMIN; ENDONUCLEASE; GLUTATHIONE; LIVER PROTECTIVE AGENT; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NITRIC OXIDE; PARACETAMOL; PROTEIN BAX; PROTEIN BCL XL; PROTEIN P53; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA FRAGMENTATION; DOWN REGULATION; ENZYME ACTIVATION; IN VIVO STUDY; LIPID PEROXIDATION; LIVER INJURY; LIVER PROTECTION; LIVER TOXICITY; MALE; MORTALITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TREATMENT DURATION;

EID: 84858218929     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/156720212799297083     Document Type: Article

References (59)

1. USFDA, 2011: Available from: http: //www.iconplc.com/newsevents/events/ webinars/fda-expectations-on-drug-/index.xml
2. Ammon HP, Wahl MA. Pharmacology of Curcuma Longa. Planta Med 1991; 57: 1-7.
3. Aggarwal BB, Banerjee S, Bharadwaj U, Sung B, Shishodia S, Sethi G. Curcumin induces the degradation of cyclin E expression through ubiquitin-dependent pathway and up-regulates cyclindependent kinase inhibitors p21 and p27 in multiple human tumor cell lines. Biochem Pharmacol 2007; 73(7): 1024-32. (Pubitemid 46283583)
4. Ha HL, Shin HJ, Feitelson MA, Yu DY. Oxidative stress and antioxidants in hepatic pathogenesis. World J Gastroenterol 2010; 16(48): 6035-43.
5. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB Bioavailability of Curcumin: Problems and Promises. Mol Pharm 2007; 4(6): 807-18.
6. Anand P, Nair H. B, Sung B, et al. Design of curcumin-loaded PLGA nanoparticles formulation with enhanced cellular uptake, and increased bioactivity in vitro and superior bioavailability in vivo. Biochem. Pharmacol 2010; 79(3): 330-8.
7. Dikshit M, Rastogi L, Shukla R, Srimal RC. Prevention of ischaemia-induced biochemical changes by curcumin and quinidine in the cat heart. Ind J Med Res 1995; 101: 31-5.
8. Mortellini R, Foresti R, Bassi R, Green CJ. Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase- 1 and protects endothelial cells against oxidative stress. Free Radic Biol Med 2000; 28: 1303-12. (Pubitemid 30417475)
9. Brouet I, Ohshima H. Curcumin, an anti-tumour promoter and antiinflammatory agent, inhibits induction of nitric oxide synthetase in activated macrophages. Biochem Biophys Res Commun 1995; 206: 533-40.
10. Singh R, Sharma P. Hepatoprotective Effect of Curcumin on Lindane-induced Oxidative Stress in Male Wistar Rats. Toxicol Int 2011; 18(2): 124-9.
11. Pae HO, Jeong SO, Kim HS, et al. Dimethoxycurcumin, a synthetic curcumin analogue with higher metabolic stability, inhibits NO production, inducible NO synthase expression and NF-κB activation in RAW264.7 macrophages activated with LPS. Mol Nutr Food Res 2008; 52(9): 1082-91.
12. Lee, WM. Acetaminophen and the U.S. Acute Liver Failure Study Group: Lowering the risks of hepatic failure. Hepatology 2004; 40: 6-9. (Pubitemid 38868915)
13. Nelson, SD. Molecular mechanisms of the hepatotoxicity caused by acetaminophen. Semin. Liver Dis 1990; 10: 267-78.
14. Esterline RL, Ray SD, Ji S. Reversible and irreversible inhibition of hepatic mitochondrial respiration by acetaminophen and its toxic metabolite, N-acetyl-p-benzoquinoneimine (NAPQI). Biochem Pharmacol 1989; 38(14): 2387-90. (Pubitemid 19173883)
15. Ray SD, Corcoran GB. In: General and Applied Toxicology, Ballantyne B, Marrs T, Syversen T, Eds. Apoptosis and Cell Death, in McMillan Publishing 2009; Vol. I, Chapter-11, pp. 247-312.
16. Ghosh J, Das J, Manna P, Sil P. C. Arjunolic acid, a triterpenoid saponin, prevents acetaminophen (APAP)-induced liver and hepatocyte injury via the inhibition of APAP bioactivation and JNK-mediated mitochondrial protection. Free Radic Biol Med 2010; 48(4): 535-53.
17. Chao DT, Korsmeyer, SJ. BCL-2 family: Regulators of cell death. Annu Rev Immunol 1998; 16: 395-419. (Pubitemid 28183370)
18. Martin LJ, Adams NA, Pan Y, Price A, Wong M. The mitochondrial permeability transition pore regulates nitric oxidemediated apoptosis of neurons induced by target deprivation. J Neurosci 2011; 31(1): 359-70.
19. 2+-Calmodulin Antagonist Chlorpromazine and Poly (ADP-Ribose) Polymerase Modulators 4-Aminobenzamide and Nicotinamide Influence Hepatic Expression of Bcl-XL and P53 and Protect against acetaminophen-induced programmed and unprogrammed cell death in mice. Free Radic Biol Med 2001; 31: 277-91.
20. Ray SD, Patel N, Nagori A, Naqvi A, Stohs S. Four week exposure to a novel nutritional mixture containing a series of polyphenolic phytochemicals antagonizes acetaminophen-induced programmed and unprogrammed cell death in the liver in vivo. Mol Cellu Biochem 2006; 293(1-2): 119-36. (Pubitemid 44843007)
21. Donatus IA, Sardjoko-Vermeulen NP. Cytotoxic and cytoprotective activities of curcumin. Effects on paracetamol-induced cytotoxicity, lipid peroxidation and glutathione depletion in rat hepatocytes. Biochem. Pharmacol 1990; 39: 1869-75. (Pubitemid 20187320)
22. Soni KB, Rajan A, Kuttan R. Reversal of aflatoxin induced liver damage by turmeric and curcumin. Cancer Lett 1992; 66: 115-21.
23. Zhang F, Altorki NK, Mestre JR, Subbaramaiah K, Dannenberg AJ. Curcumin inhibits cyclooxygenase-2 transcription in bile acidand phorbol ester-treated human gastrointestinal epithelial cells. Carcinogenesis 1999; 20(3): 445-51. (Pubitemid 29112633)
24. Kaur G, Tirkey N, Bharrhan S, Chanana V, Rishi P, Chopra K. Inhibition of oxidative stress and cytokine activity by curcumin in amelioration of endotoxin-induced experimental hepatoxicity in rodents 2006 British Society for Immunology, Clin Exptl Immunol 2006; 145: 313-21. (Pubitemid 44060123)
25. Shapiro H, Ashkenazi M, Weizman N, et al. Curcumin ameliorates acute thioacetamide-induced hepatotoxicity J Gastroenterol Hepatol 2006; 21 (2): 358-366(9).
26. Reyes-Gordillo K, Segovia J, Shibayama M, Tsutsumi V, Vergara P, et al. Curcumin prevents and reverses cirrhosis induced by bile duct obstruction or CCl4 in rats: role of TGF-beta modulation and oxidative stress. Fundam Clin Pharmacol 2008; 22(4): 417-27.
27. Messner DJ, Sivam G, Kowdley KV. Curcumin reduces the toxic effects of iron loading in rat liver epithelial cells. Liver Int 2009; 29(1): 63-72.
28. Wroblewski F, Ladue JS. Serum glutamic oxalacetic aminopherase (transaminase) in hepatitis. J Am Med Assoc 1956; 160(13): 1130-134.
29. Talke H, Schubert GE: Enzymatische Hanstoff-bestimmung in Blut and Serum in optischen Test nach Warberg. Klin Wochschr 1965; 43: 174-5.
30. Ray SD, Mumaw VR, Raje RR, Fariss MW. Protection of acetaminophen-induced hepatocellular apoptosis and necrosis by cholesteryl hemisuccinate pretreatments. J Pharm Exp Therapeu 1996; 279: 1470-83. (Pubitemid 27166797)
31. 2+ antagonists inhibit DNA fragmentation and toxic cell death induced by acetaminophen. FASEB J 1993; 7: 453-63.
32. Ray SD, Jena N. hepatotoxic dose of acetaminophen modulates expression of bcl-2, bcl-XL, and bcl-Xs during apoptotic and necrotic death of mouse liver cells in vivo. Arch Toxicol 2000; 73: 594-606. (Pubitemid 30062492)
33. Aggarwal BB, Sundaram C, Malani N, and Ichikawa H. Curcumin: the Indian solid gold. Adv Exp Med Biol 2007; 595: 1-75.
34. Zhu YG, Chen X-C, Chen ZZ, Zeng YQ, Shi G-B, et al. Curcumin protects mitochondria from oxidative damage and attenuates apoptosis in cortical neurons. Acta Pharmacol Sin 2004; 25 (12): 1606-12. (Pubitemid 39628027)
35. Bulku E, Zinkovsky D, Patel N, Ray SD. Curcumin pre-exposure in vivo prevents acetaminophen-induced apoptotic and necrotic cell deaths in the liver. Proceedings of Experimental Biology meetings, San Francisco, CA, 2006; FASEB JOURNAL 20 (5): A1144- A1144, Part 2, 2006.
36. Cheung C, Yu AM, Ward JM, et al. The CYP2E1-humanized transgenic mouse: role of CYP2E1 in acetaminophen hepatotoxicity. Drug Metab. Dispos 2005; 33: 449-57. (Pubitemid 40279947)
37. Ray SD, Kumar A, Bagchi D. A novel proanthocyanidin IH636 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. (Pubitemid 29434537)
38. Pari L, Amali DR. Protective role of tetrahydrocurcumin (THC) an active principle of turmeric on chloroquine induced hepatotoxicity in rats. J Pharm Pharm Sci 2005; 8(1): 115-23. (Pubitemid 41528877)
39. Abdel-Zaher AO, Abdel-Hady RH, Mahmoud MM, Farrag MMY. The potential protective role of alpha-lipoic acid against acetaminophen-induced hepatic and renal damage. Toxicology 2008; 243: 261-70. (Pubitemid 50011452)
40. Michael SL, Mayeux PR, Bucci, TJ, et al. Acetaminophen-induced hepatotoxicity in mice lacking inducible nitric oxide synthase activity 2001; Nitric Oxide 5, 432-41.
41. Hinson JA, Pike SL, Pumford NR, Mayeux PR. Nitrotyrosineprotein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice. Chem Res Toxicol 1998; 11, 604-7. (Pubitemid 28285584)
42. Hinson JA, Bucci TJ, Irwin LK, Michael SL, Mayeux PR. Effect of inhibitors of nitric oxide synthase on acetaminophen-induced hepatotoxicity in mice. Nitric Oxide 2002; 6(2): 160-7. (Pubitemid 34848438)
43. Aggarwal BB, Kumar A, Bharti AC. Anticancer Potential of Curcumin: Preclinical and Clinical Studies. Anticancer Res 2003; 23: 363-98. (Pubitemid 36361976)
44. 2+ in the nucleus during acetaminophen-induced liver injury. Toxicol Appl Pharmacol 1990; 106, 346-51.
45. Hsu YT, Youle RJ. Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 1997; 272: 13829-34. (Pubitemid 27224822)
46. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. Movement of Bax from the Cytosol to Mitochondria during Apoptosis, J Cell Biol 1997; 139, 1281-292. (Pubitemid 27523214)
47. Hsu YT, Wolter KG, Youle RJ. Cytosol-to-membrane redistribution of Bax and Bcl-XL during apoptosis. Proc. Natl Acad. Sci. USA 1997; 94, 3668-72.
48. Desagher S, Osen-Sand A, Nichols A, et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999; 144(5): 891-901. (Pubitemid 29238966)
49. Nechushtan A, Smith C. L, Lamensdorf I, Yoon S. H, Youle R. J. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 2001; 153(6): 1265-76. (Pubitemid 34289264)
50. Yin XM, Oltvai ZN, Korsmeyer SJ. BH1 and BH2 domains of Bcl- 2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 1994; 369(6478): 321-3. (Pubitemid 24159542)
51. Zha H, Fisk H. A, Yaffe M. P, Mahajan N, Herman B, Reed J. C. Structure-function comparisons of the proapoptotic protein Bax in yeast and mammalian cells. Mol Cell Biol 1996; 16(11): 6494-508. (Pubitemid 26361008)
52. Narita M, Shimizu S, Ito T, et al. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 1998; 95(25): 14681-6. (Pubitemid 29003690)
53. Marzo I, Brenner C, Zamzami N, et al. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998; 281(5385): 2027-31. (Pubitemid 28475490)
54. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74(4): 609-19. (Pubitemid 23259742)
55. González de Aguilar JL, Gordon JW, René F, de Tapia M, Lutz- Bucher B, et al. Alteration of the Bcl-x/Bax ratio in a transgenic mouse model of amyotrophic lateral sclerosis: evidence for the implication of the p53 signaling pathway. Neurobiol Dis 2000; 7: 406-15.
56. Choudhuri T, Pal S, Agwarwal ML, Das T, Sa G. Curcumin induces apoptosis in human breast cancer cells through p53- dependent Bax induction. FEBS Lett 2002; 512: 334-40. (Pubitemid 34164505)
57. Ray SD, Patel D, Wong V, et al. Unique organoprotective properties of a novel a novel IH636 grape seed proanthocyanidin extract on cadmium chloride-induced nephrotoxicity, dimethylnitrosamine-induced spleenotoxicity, and mocap-induced neurotoxicity in mice. Res Commu Mol Pathol Pharmacol 2000; 107: 105-128. (Pubitemid 32240570)
58. Ray SD, Lam TS, Rotollo JA, et al. Oxidative Stress is the Master Operator of Drug & Chemically-Induced Programmed & Unprogrammed Cell Death: Implications of Natural Antioxidants In vivo. Biofactors 2004; 21(1-4): 223-232. (Pubitemid 40921858)
59. Ray SD, Parikh H, Bagchi D. Long-Term grape seed proanthocyanidin extract exposure to B6C3F1 mice significantly attenuates dimethylnitrosamine-induced liver tumor induction and mortality by differentially modulating programmed and unprogrammed cell deaths. Mutation Res 2005; 579 (1-2): 81-106. (Pubitemid 41540134)