Table of Contents Author Guidelines Submit a Manuscript
Evidence-Based Complementary and Alternative Medicine
Volume 2013 (2013), Article ID 974794, 13 pages
http://dx.doi.org/10.1155/2013/974794
Research Article

Curative Effects of Thiacremonone against Acetaminophen-Induced Acute Hepatic Failure via Inhibition of Proinflammatory Cytokines Production and Infiltration of Cytotoxic Immune Cells and Kupffer Cells

1College of Pharmacy and Medical Research Center, Chungbuk National University, 12 Gaeshin, Heungduk, Cheongju, Chungbuk 361-763, Republic of Korea
2Agriculture, Life and Environments Sciences, Chungbuk National University, 12 Gaeshin, Heungduk, Cheongju, Chungbuk 361-763, Republic of Korea
3Laboratory of Cytokine Immunology, Institute of Biomedical Science and Technology, College of Medicine, Konkuk University, Seoul 143-701, Republic of Korea
4College of Pharmacy, Chungbuk National University, 48 Gaesin-dong, Heungduk-gu, Cheongju, Chungbuk 361-763, Republic of Korea

Received 18 February 2013; Accepted 22 April 2013

Academic Editor: Vincenzo De Feo

Copyright © 2013 Yu Ri Kim et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Agarwal, L. Hennings, T. M. Rafferty et al., “Acetaminophen-induced hepatotoxicity and protein nitration in neuronal nitric-oxide synthase knockout mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 340, no. 1, pp. 134–142.
  2. A. M. Slitt, P. K. Dominick, J. C. Roberts, and S. D. Cohen, “Effect of ribose cysteine pretreatment on hepatic and renal acetaminophen metabolite formation and glutathione depletion,” Basic and Clinical Pharmacology and Toxicology, vol. 96, no. 6, pp. 487–494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Prescott, “Oral or intravenous N-acetylcysteine for acetaminophen poisoning?” Annals of Emergency Medicine, vol. 45, no. 4, pp. 409–413, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. J. Hu, J. S. H. Yoo, M. Lin, E. J. Wang, and C. S. Yang, “Protective effects of diallyl sulfide on acetaminophen-induced toxicities,” Food and Chemical Toxicology, vol. 34, no. 10, pp. 963–969, 1996. View at Publisher · View at Google Scholar · View at Scopus
  5. L. P. James, P. R. Mayeux, and J. A. Hinson, “Acetaminophen-induced hepatotoxicity,” Drug Metabolism and Disposition, vol. 31, no. 12, pp. 1499–1506, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. J. A. Hinson, D. W. Roberts, and L. P. James, “Mechanisms of acetaminophen-induced liver necrosis,” Handbook of Experimental Pharmacology, vol. 196, pp. 369–405, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Rubbo, R. Radi, M. Trujillo et al., “Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives,” Journal of Biological Chemistry, vol. 269, no. 42, pp. 26066–26075, 1994. View at Google Scholar · View at Scopus
  8. H. Sies, V. S. Sharov, L. O. Klotz, and K. Briviba, “Glutathione peroxidase protects against peroxynitrite-mediated oxidations: a new function for selenoproteins as peroxynitrite reductase,” Journal of Biological Chemistry, vol. 272, no. 44, pp. 27812–27817, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. S. L. Michael, P. R. Mayeux, T. J. Bucci et al., “Acetaminophen-induced hepatotoxicity in mice lacking inducible nitric oxide synthase activity,” Nitric Oxide, vol. 5, no. 5, pp. 432–441, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. B. V. Martin-Murphy, M. P. Holt, and C. Ju, “The role of damage associated molecular pattern molecules in acetaminophen-induced liver injury in mice,” Toxicology Letters, vol. 192, no. 3, pp. 387–394, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. Z. X. Liu, S. Govindarajan, and N. Kaplowitz, “Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity,” Gastroenterology, vol. 127, no. 6, pp. 1760–1774, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Ishida, T. Kondo, T. Ohshima, H. Fujiwara, Y. Iwakura, and N. Mukaida, “A pivotal involvement of IFN-γ in the pathogenesis of acetaminophen-induced acute liver injury,” FASEB Journal, vol. 16, no. 10, pp. 1227–1236, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. M. E. Blazka, J. L. Wilmer, S. D. Holladay, R. E. Wilson, and M. I. Luster, “Role of proinflammatory cytokines in acetaminophen hepatotoxicity,” Toxicology and Applied Pharmacology, vol. 133, no. 1, pp. 43–52, 1995. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Gandhi, T. Guo, and R. Ghose, “Role of c-Jun N-terminal kinase (JNK) in regulating tumor necrosis factor-alpha (TNF-α) mediated increase of acetaminophen (APAP) and chlorpromazine (CPZ) toxicity in murine hepatocytes,” Journal of Toxicological Sciences, vol. 35, no. 2, pp. 163–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Hu, D. Yan, J. Gao et al., “rhIL-1Ra reduces hepatocellular apoptosis in mice with acetaminophen-induced acute liver failure,” Laboratory Investigation, vol. 90, no. 12, pp. 1737–1746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Ju, T. P. Reilly, M. Bourdi et al., “Protective role of kupffer cells in acetaminophen-induced hepatic injury in mice,” Chemical Research in Toxicology, vol. 15, no. 12, pp. 1504–1513, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Ren, A. Kennedy, and L. M. Colletti, “CXC chemokine expression after stimulation with interferon-γ in primary rat hepatocytes in culture,” Shock, vol. 17, no. 6, pp. 513–520, 2002. View at Google Scholar · View at Scopus
  18. X. Li, D. Klintman, Q. Liu, T. Sato, B. Jeppsson, and H. Thorlacius, “Critical role of CXC chemokines in endotoxemic liver injury in mice,” Journal of Leukocyte Biology, vol. 75, no. 3, pp. 443–452, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Ramadori, F. Moriconi, I. Malik, and J. Dudas, “Physiology and pathophysiology of liver inflammation, damage and repair,” Journal of Physiology and Pharmacology, vol. 59, supplement 1, pp. 107–117, 2008. View at Google Scholar · View at Scopus
  20. A. C. Dragomir, R. Sun, V. Mishin, L. B. Hall, J. D. Laskin, and D. L. Laskin, “Role of galectin-3 in acetaminophen-induced hepatotoxicity and inflammatory mediator production,” Toxicological Sciences, vol. 127, no. 2, pp. 609–619, 2012. View at Google Scholar
  21. C. M. Hogaboam, C. L. Bone-Larson, M. L. Steinhauser et al., “Novel CXCR2-dependent liver regenerative qualities of ELR-containing CXC chemokines,” FASEB Journal, vol. 13, no. 12, pp. 1565–1574, 1999. View at Google Scholar · View at Scopus
  22. C. M. Hogaboam, C. L. Bone-Larson, M. L. Steinhauser et al., “Exaggerated hepatic injury due to acetaminophen challenge in mice lacking C-C chemokine receptor 2,” American Journal of Pathology, vol. 156, no. 4, pp. 1245–1252, 2000. View at Google Scholar · View at Scopus
  23. X. Ren, A. Carpenter, C. Hogaboam, and L. Colletti, “Mitogenic properties of endogenous and pharmacological doses of macrophage inflammatory protein-2 after 70% hepatectomy in the mouse,” American Journal of Pathology, vol. 163, no. 2, pp. 563–570, 2003. View at Google Scholar · View at Scopus
  24. C. L. Bone-Larson, C. M. Hogaboam, H. Evanhoff, R. M. Strieter, and S. L. Kunkel, “IFN-γ-inducible protein-10 (CXCL10) is hepatoprotective during acute liver injury through the induction of CXCR2 on hepatocytes,” Journal of Immunology, vol. 167, no. 12, pp. 7077–7083, 2001. View at Google Scholar · View at Scopus
  25. A. Richmond, “NF-κB, chemokine gene transcription and tumour growth,” Nature Reviews Immunology, vol. 2, no. 9, pp. 664–674, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Y. Wang, M. W. Mayo, R. G. Korneluk, D. V. Goeddel, and A. S. Baldwin Jr., “NF-B antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation,” Science, vol. 281, no. 5383, pp. 1680–1683, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. M. A. Meraz, J. M. White, K. C. F. Sheehan et al., “Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway,” Cell, vol. 84, no. 3, pp. 431–442, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Ghosh and P. C. Sil, “Protection of acetaminophen induced mitochondrial dysfunctions and hepatic necrosis via Akt-NF-κB pathway: role of a novel plant protein,” Chemico-Biological Interactions, vol. 177, no. 2, pp. 96–106, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. F. Hong, B. Jaruga, W. H. Kim et al., “Opposing roles of STAT1 and STAT3 in T cell-mediated hepatitis: regulation by SOCS,” Journal of Clinical Investigation, vol. 110, no. 10, pp. 1503–1513, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Gao, “Cytokines, STATs and liver disease,” Cellular & Molecular Immunology, vol. 2, no. 2, pp. 92–100, 2005. View at Google Scholar · View at Scopus
  31. F. Hong, S. Radaeva, H. N. Pan, Z. Tian, R. Veech, and B. Gao, “Interleukin 6 alleviates hepatic steatosis and ischemia/reperfusion injury in mice with fatty liver disease,” Hepatology, vol. 40, no. 4, pp. 933–941, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. N. Hecht, O. Pappo, D. Shouval, S. Rose-John, E. Galun, and J. H. Axelrod, “Hyper-IL-6 gene therapy reverses fulminant hepatic failure,” Molecular Therapy, vol. 3, no. 5, part 1, pp. 683–687, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Rahman, “Historical perspective on garlic and cardiovascular disease,” Journal of Nutrition, vol. 131, supplement 3, pp. 977S–979S, 2001. View at Google Scholar · View at Scopus
  34. S. Tanaka, K. Haruma, M. Yoshihara et al., “Aged garlic extract has potential suppressive effect on colorectal adenomas in humans,” Journal of Nutrition, vol. 136, supplement 3, pp. 821S–826S, 2006. View at Google Scholar · View at Scopus
  35. Y. Y. Yeh and L. Liu, “Cholesterol-lowering effect of garlic extracts and organosulfur compounds: human and animal studies,” Journal of Nutrition, vol. 131, supplement 3, pp. 989S–993S, 2001. View at Google Scholar · View at Scopus
  36. O. B. Jung, S. L. Hee, H. S. Jeong et al., “Thiacremonone augments chemotherapeutic agent-induced growth inhibition in human colon cancer cells through inactivation of nuclear factor-κB,” Molecular Cancer Research, vol. 7, no. 6, pp. 870–879, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. E. J. Kim, D. H. Lee, H. J. Kim et al., “Thiacremonone, a sulfur compound isolated from garlic, attenuates lipid accumulation partially mediated via AMPK activation in 3T3-L1 adipocytes,” The Journal of Nutritional Biochemistry, vol. 23, no. 12, pp. 1552–1558, 2012. View at Publisher · View at Google Scholar
  38. C. D. Fisher, L. M. Augustine, J. M. Maher et al., “Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2,” Drug Metabolism and Disposition, vol. 35, no. 6, pp. 995–1000, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Pari, P. Murugavel, S. L. Sitasawad, and K. S. Kumar, “Cytoprotective and antioxidant role of diallyl tetrasulfide on cadmium induced renal injury: an in vivo and in vitro study,” Life Sciences, vol. 80, no. 7, pp. 650–658, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. V. Narayanaswami and H. Sies, “Antioxidant activity of ebselen and related selenoorganic compounds in microsomal lipid peroxidation,” Free Radical Research Communications, vol. 10, no. 4-5, pp. 237–244, 1990. View at Google Scholar · View at Scopus
  41. B. Sabayan, F. Foroughinia, and A. Chohedry, “A postulated role of garlic organosulfur compounds in prevention of valproic acid hepatotoxicity,” Medical Hypotheses, vol. 68, no. 3, pp. 512–514, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. E. W. Son, S. J. Mo, D. K. Rhee, and S. Pyo, “Inhibition of ICAM-1 expression by garlic component, allicin, in gamma-irradiated human vascular endothelial cells via downregulation of the JNK signaling pathway,” International Immunopharmacology, vol. 6, no. 12, pp. 1788–1795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Qian, E. Hua, K. Bisht et al., “Inhibition of Polo-like kinase 1 prevents the growth of metastatic breast cancer cells in the brain,” Clinical and Experimental Metastasis, vol. 28, no. 8, pp. 899–908.
  44. J. O. Ban, J. H. Oh, T. M. Kim et al., “Anti-inflammatory and arthritic effects of thiacremonone, a novel sulfurcompound isolated from garlic via inhibition of NF-κB,” Arthritis Research and Therapy, vol. 11, no. 5, article R145, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. M. C. Cho, S. L. Woo, J. T. Hong et al., “5-(3,5-Di-tert-butyl-4-hydroxybenzylidene) thiazolidine-2,4-dione modulates peroxisome proliferators-activated receptor γ in 3T3-L1 adipocytes: roles as a PPARγ ligand,” Molecular and Cellular Endocrinology, vol. 242, no. 1-2, pp. 96–102, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. M. C. Cho, H. E. Yoon, J. W. Kang et al., “A simple method to screen ligands of peroxisome proliferator-activated receptor δ,” European Journal of Pharmaceutical Sciences, vol. 29, no. 5, pp. 355–360, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. M. C. Cho, S. Lee, H. S. Choi et al., “Optimization of an enzyme-linked immunosorbent assay to screen ligand of Peroxisome proliferator-activated receptor alpha,” Immunopharmacology and Immunotoxicology, vol. 31, no. 3, pp. 459–467, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. D. Adams Jr., B. H. Lauterburg, and J. R. Mitchell, “Plasma glutathione and glutathione disulfide in the rat: regulation and response to oxidative stress,” Journal of Pharmacology and Experimental Therapeutics, vol. 227, no. 3, pp. 749–754, 1983. View at Google Scholar · View at Scopus
  49. H. Jaeschke, G. J. Gores, A. I. Cederbaum, J. A. Hinson, D. Pessayre, and J. J. Lemasters, “Mechanisms of hepatotoxicity,” Toxicological Sciences, vol. 65, no. 2, pp. 166–176, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. J. A. Hinson, S. L. Pike, N. R. Pumford, and P. R. Mayeux, “Nitrotyrosine-protein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice,” Chemical Research in Toxicology, vol. 11, no. 6, pp. 604–607, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. C. R. Gardner, D. E. Heck, C. S. Yang et al., “Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat,” Hepatology, vol. 27, no. 3, pp. 748–754, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. J. S. Beckman and W. H. Koppenol, “Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly,” American Journal of Physiology, vol. 271, no. 5, part 1, pp. C1424–C1437, 1996. View at Google Scholar · View at Scopus
  53. W. A. Pryor and G. L. Squadrito, “The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide,” American Journal of Physiology, vol. 268, no. 5, pp. L699–L722, 1995. View at Google Scholar · View at Scopus
  54. G. Ostapowicz, R. J. Fontana, F. V. Schioødt et al., “Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States,” Annals of Internal Medicine, vol. 137, no. 12, pp. 947–954, 2002. View at Google Scholar · View at Scopus
  55. M. E. Blazka, M. R. Elwell, S. D. Holladay, R. E. Wilson, and M. I. Luster, “Histopathology of acetaminophen-induced liver changes: role of interleukin 1α and tumor necrosis factor α,” Toxicologic Pathology, vol. 24, no. 2, pp. 181–189, 1996. View at Google Scholar · View at Scopus
  56. M. E. Blazka, D. R. Germolec, P. Simeonova, A. Bruccoleri, K. R. Pennypacker, and M. I. Luster, “Acetaminophen-induced hepatotoxicity is associated with early changes in NF-kB and NF-IL6 DNA binding activity,” Journal of Inflammation, vol. 47, no. 3, pp. 138–150, 1995. View at Google Scholar · View at Scopus
  57. M. Bourdi, Y. Masubuchi, T. P. Reilly et al., “Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase,” Hepatology, vol. 35, no. 2, pp. 289–298, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Iwakura, H. Ishigame, S. Saijo, and S. Nakae, “Functional Specialization of Interleukin-17 Family Members,” Immunity, vol. 34, no. 2, pp. 149–162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Bourdi, D. P. Eiras, M. P. Holt et al., “Role of IL-6 in an IL-10 and IL-4 double knockout mouse model uniquely susceptible to acetaminophen-induced liver injury,” Chemical Research in Toxicology, vol. 20, no. 2, pp. 208–216, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. J. A. Lawson, A. Farhood, R. D. Hopper, M. L. Bajt, and H. Jaeschke, “The hepatic inflammatory response after acetaminophen overdose: role of neutrophils,” Toxicological Sciences, vol. 54, no. 2, pp. 509–516, 2000. View at Google Scholar · View at Scopus
  61. C. R. Gardner, P. Hankey, V. Mishin et al., “Regulation of alternative macrophage activation in the liver following acetaminophen intoxication by stem cell-derived tyrosine kinase,” Toxicology and Applied Pharmacology, vol. 262, no. 2, pp. 139–148, 2012. View at Google Scholar
  62. C. M. Hogaboam, C. Bone-Larson, A. Matsukawa et al., “Therapeutic use of chemokines,” Current Pharmaceutical Design, vol. 6, no. 6, pp. 651–663, 2000. View at Google Scholar · View at Scopus
  63. T. Ishibe, A. Kimura, Y. Ishida et al., “Reduced acetaminophen-induced liver injury in mice by genetic disruption of IL-1 receptor antagonist,” Laboratory Investigation, vol. 89, no. 1, pp. 68–79, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Arsura, M. Wu, and G. E. Sonenshein, “TGFβ1 inhibits NF-κB/Rel activity inducing apoptosis of B cells: transcriptional activation of IκB,” Immunity, vol. 5, no. 1, pp. 31–40, 1996. View at Publisher · View at Google Scholar · View at Scopus
  65. O. 'Dea E and A. Hoffmann, “NF-kappaB signaling,” Wiley Interdisciplinary Reviews: Systems Biology and Medicine, vol. 1, no. 1, pp. 107–115, 2009. View at Google Scholar
  66. D. M. Dambach, S. K. Durham, J. D. Laskin, and D. L. Laskin, “Distinct roles of NF-κB p50 in the regulation of acetaminophen-induced inflammatory mediator production and hepatotoxicity,” Toxicology and Applied Pharmacology, vol. 211, no. 2, pp. 157–165, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. C. K. Sen, K. E. Traber, and L. Packer, “Inhibition of NF-κB activation in human T-cell lines by anetholdithiolthione,” Biochemical and Biophysical Research Communications, vol. 218, no. 1, pp. 148–153, 1996. View at Publisher · View at Google Scholar · View at Scopus
  68. S. K. Manna, A. Mukhopadhyay, N. T. Van, and B. B. Aggarwal, “Silymarin suppresses TNF-induced activation of NF-κB, c-Jun N-terminal kinase, and apoptosis,” Journal of Immunology, vol. 163, no. 12, pp. 6800–6809, 1999. View at Google Scholar · View at Scopus
  69. K. Reyes-Gordillo, J. Segovia, M. Shibayama, P. Vergara, M. G. Moreno, and P. Muriel, “Curcumin protects against acute liver damage in the rat by inhibiting NF-κB, proinflammatory cytokines production and oxidative stress,” Biochimica et Biophysica Acta, vol. 1770, no. 6, pp. 989–996, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. M. D. Wheeler, S. Yamashina, M. Froh, I. Rusyn, and R. G. Thurman, “Adenoviral gene delivery can inactivate Kupffer cells: role of oxidants in NF-κB activation and cytokine production,” Journal of Leukocyte Biology, vol. 69, no. 4, pp. 622–630, 2001. View at Google Scholar · View at Scopus
  71. B. Jaruga, F. Hong, W. H. Kim, and B. Gao, “IFN-γ/STAT1 acts as a proinflammatory signal in T cell-mediated hepatitis via induction of multiple chemokines and adhesion molecules: a critical role of IRF-1,” American Journal of Physiology, vol. 287, no. 5, pp. G1044–G1052, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Numata, M. Kubo, H. Watanabe et al., “Overexpression of suppressor of cytokine signaling-3 in T cells exacerbates acetaminophen-induced hepatotoxicity,” Journal of Immunology, vol. 178, no. 6, pp. 3777–3785, 2007. View at Google Scholar · View at Scopus