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BioMed Research International
Volume 2013 (2013), Article ID 627046, 13 pages
http://dx.doi.org/10.1155/2013/627046
Research Article

5-Lipoxygenase Deficiency Reduces Acetaminophen-Induced Hepatotoxicity and Lethality

1Department of Pathology, Biological Science Centre, State University of Londrina, Rodovia Celso Garcia Cid Pr 445, Km 380. Cx. Postal 6001, 86051-990 Londrina PR, Brazil
2Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Avenida Bandeirantes 3900, 14049-900 Ribeirão Preto, SP, Brazil
3Department of Pharmaceutical Sciences, Health Sciences Centre, State University of Londrina, Rodovia Celso Garcia Cid Pr 445, Km 380, Cx. Postal 10011, 86051-990 Londrina, PR, Brazil

Received 30 April 2013; Revised 4 September 2013; Accepted 6 September 2013

Academic Editor: Chun-Ming Wong

Copyright © 2013 Miriam S. N. Hohmann 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. B. Samuelsson, S.-E. Dahlen, and J. A. Lindgren, “Leukotrienes and lipoxins: structures, biosynthesis, and biological effects,” Science, vol. 237, no. 4819, pp. 1171–1176, 1987. View at Scopus
  2. C. D. Funk, “Prostaglandins and leukotrienes: advances in eicosanoid biology,” Science, vol. 294, no. 5548, pp. 1871–1875, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. A. W. Ford-Hutchinson, M. A. Bray, and M. V. Doig, “Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes,” Nature, vol. 286, no. 5770, pp. 264–265, 1980. View at Scopus
  4. M. Chen, B. K. Lam, A. D. Luster et al., “Joint tissues amplify inflammation and alter their invasive behavior via leukotriene B4 in experimental inflammatory arthritis,” Journal of Immunology, vol. 185, no. 9, pp. 5503–5511, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. F. G. Al-Amran, N. R. Hadi, and A. M. Hashim, “Leukotriene biosynthesis inhibition ameliorates acute lung injury following hemorrhagic shock in rats,” Journal of Cardiothoracic Surgery, vol. 6, no. 1, article no. 81, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Alric, C. Orfila, N. Carrere et al., “Reactive oxygen intermediates and eicosanoid production by Kupffer cells and infiltrated macrophages in acute and chronic liver injury induced in rats by CCl4,” Inflammation Research, vol. 49, no. 12, pp. 700–707, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Titos, J. Clària, A. Planagumà et al., “Inhibition of 5-lipoxygenase induces cell growth arrest and apoptosis in rat Kupffer cells: implications for liver fibrosis,” The FASEB Journal, vol. 17, no. 12, pp. 1745–1747, 2003. View at Scopus
  8. Y. Takamatsu, K. Shimada, K. Chijiiwa, S. Kuroki, K. Yamaguchi, and M. Tanaka, “Role of leukotrienes on hepatic ischemia/reperfusion injury in rats,” Journal of Surgical Research, vol. 119, no. 1, pp. 14–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Titos, J. Clària, A. Planagumà et al., “Inhibition of 5-lipoxygenase-activating protein abrogates experimental liver injury: role of Kupffer cells,” Journal of Leukocyte Biology, vol. 78, no. 4, pp. 871–878, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Horrillo, A. Planagumà, A. González-Périz et al., “Comparative protection against liver inflammation and fibrosis by a selective cyclooxygenase-2 inhibitor and a nonredox-type 5-lipoxygenase inhibitor,” Journal of Pharmacology and Experimental Therapeutics, vol. 323, no. 3, pp. 778–786, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. L. F. Prescott, “Hepatotoxicity of mild analgesics,” British Journal of Clinical Pharmacology, vol. 10, supplement 2, pp. 375S–377S, 1980. View at Scopus
  12. A. M. Larson, J. Polson, R. J. Fontana et al., “Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study,” Hepatology, vol. 42, no. 6, pp. 1364–1372, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. D. G. N. Craig, C. M. Bates, J. S. Davidson, K. G. Martin, P. C. Hayes, and K. J. Simpson, “Overdose pattern and outcome in paracetamol-induced acute severe hepatotoxicity,” British Journal of Clinical Pharmacology, vol. 71, no. 2, pp. 273–282, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. J. R. Mitchell, D. J. Jollow, and W. Z. Potter, “Acetaminophen induced hepatic necrosis. I. Role of drug metabolism,” Journal of Pharmacology and Experimental Therapeutics, vol. 187, no. 1, pp. 185–194, 1973. View at Scopus
  15. C. J. Patten, P. E. Thomas, R. L. Guy et al., “Cytochrome P450 enzymes involved in acetaminophen activation by rat and human liver microsomes and their kinetics,” Chemical Research in Toxicology, vol. 6, no. 4, pp. 511–518, 1993. View at Scopus
  16. D. J. Jollow, J. R. Mitchell, and W. Z. Potter, “Acetaminophen induced hepatic necrosis. II. Role of covalent binding in vivo,” Journal of Pharmacology and Experimental Therapeutics, vol. 187, no. 1, pp. 195–202, 1973. View at Scopus
  17. J. R. Mitchell, D. J. Jollow, and W. Z. Potter, “Acetaminophen induced hepatic necrosis. IV. Protective role of glutathione,” Journal of Pharmacology and Experimental Therapeutics, vol. 187, no. 1, pp. 211–217, 1973. View at Scopus
  18. 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
  19. R. F. Schwabe, E. Seki, and D. A. Brenner, “Toll-Like Receptor Signaling in the Liver,” Gastroenterology, vol. 130, no. 6, pp. 1886–1900, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Jeannin, S. Jaillon, and Y. Delneste, “Pattern recognition receptors in the immune response against dying cells,” Current Opinion in Immunology, vol. 20, no. 5, pp. 530–537, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. D. L. Laskin and K. J. Pendino, “Macrophages and inflammatory mediators in tissue injury,” Annual Review of Pharmacology and Toxicology, vol. 35, pp. 655–677, 1995. View at Scopus
  22. S. L. Michael, N. R. Pumford, P. R. Mayeux, M. R. Niesman, and J. A. Hinson, “Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species,” Hepatology, vol. 30, no. 1, pp. 186–195, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. R. A. Roberts, P. E. Ganey, C. Ju, L. M. Kamendulis, I. Rusyn, and J. E. Klaunig, “Role of the Kupffer cell in mediating hepatic toxicity and carcinogenesis,” Toxicological Sciences, vol. 96, no. 1, pp. 2–15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. D. A. Valério, S. R. Georgetti, D. A. Magro et al., “Quercetin reduces inflammatory pain: inhibition of oxidative stress and cytokine production,” Journal of Natural Products, vol. 72, no. 11, pp. 1975–1979, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. Z.-X. Liu, D. Han, B. Gunawan, and N. Kaplowitz, “Neutrophil depletion protects against murine acetaminophen hepatotoxicity,” Hepatology, vol. 43, no. 6, pp. 1220–1230, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. A.-C. Dragomir, J. D. Laskin, and D. L. Laskin, “Macrophage activation by factors released from acetaminophen-injured hepatocytes: potential role of HMGB1,” Toxicology and Applied Pharmacology, vol. 253, no. 3, pp. 170–177, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Zhai, R. W. Busuttil, and J. W. Kupiec-Weglinski, “Liver ischemia and reperfusion injury: new insights into mechanisms of innate-adaptive immune-mediated tissue inflammation,” American Journal of Transplantation, vol. 11, no. 8, pp. 1563–1569, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Jaeschke, A. Farhood, and C. W. Smith, “Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo,” FASEB Journal, vol. 4, no. 15, pp. 3355–3359, 1990. View at Scopus
  29. H. Jaeschke, A. Farhood, and C. W. Smith, “Neutrophil-induced liver cell injury in endotoxin shock is a CD11b/CD18-dependent mechanism,” American Journal of Physiology, vol. 261, no. 6, pp. G1051–G1056, 1991. View at Scopus
  30. H. Yaman, E. Cakir, E. O. Akgul et al., “Pentraxin 3 as a potential biomarker of acetaminophen-induced liver injury,” Experimental and Toxicologic Pathology, vol. 65, no. 1-2, pp. 147–151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. P. P. Bradley, D. A. Priebat, R. D. Christensen, and G. Rothstein, “Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker,” Journal of Investigative Dermatology, vol. 78, no. 3, pp. 206–209, 1982. View at Scopus
  32. C. D. Horinouchi, D. A. Mendes, S. Soley Bda, et al., “Combretum leprosum Mart. (Combretaceae): potential as an antiproliferative and anti-inflammatory agent,” Journal of EthNopharmacology, vol. 145, no. 1, pp. 311–319, 2013. View at Publisher · View at Google Scholar
  33. J. Sedlak and R. H. Lindsay, “Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent,” Analytical Biochemistry, vol. 25, pp. 192–205, 1968. View at Scopus
  34. V. Katalinic, D. Modun, I. Music, and M. Boban, “Gender differences in antioxidant capacity of rat tissues determined by 2,2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays,” Comparative Biochemistry and Physiology Part C, vol. 140, no. 1, pp. 47–52, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Watanuki, K. Ota, A. C. M. A. R. Tassakka, T. Kato, and M. Sakai, “Immunostimulant effects of dietary Spirulina platensis on carp, Cyprinus carpio,” Aquaculture, vol. 258, no. 1–4, pp. 157–163, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. R. P. Guedes, L. Dal Bosco, C. M. Teixeira et al., “Neuropathic pain modifies antioxidant activity in rat spinal cord,” Neurochemical Research, vol. 31, no. 5, pp. 603–609, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. W. A. Verri Jr., A. T. G. Guerrero, S. Y. Fukada et al., “IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 7, pp. 2723–2728, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. V. Darias, S. Abdala, D. Martin-Herrera, M. Luisa Tello, and S. Vega, “CNS effects of a series of 1,2,4-triazolyl heterocarboxylic derivatives,” Pharmazie, vol. 53, no. 7, pp. 477–481, 1998. View at Scopus
  39. 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
  40. T. Ezzat, D. K. Dhar, M. Malago, and S. W. M. Olde Damink, “Dynamic tracking of stem cells in an acute liver failure model,” World Journal of Gastroenterology, vol. 18, no. 6, pp. 507–516, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. L.-Q. Qin, Y. Wang, J.-Y. Xu, T. Kaneko, A. Sato, and P.-Y. Wang, “One-day dietary restriction changes hepatic metabolism and potentiates the hepatotoxicity of carbon tetrachloride and chloroform in rats,” Tohoku Journal of Experimental Medicine, vol. 212, no. 4, pp. 379–387, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. D. J. Antoine, D. P. Williams, A. Kipar, H. Laverty, and B. Kevin Park, “Diet restriction inhibits apoptosis and HMGB1 oxidation and promotes inflammatory cell recruitment during acetaminophen hepatotoxicity,” Molecular Medicine, vol. 16, no. 11-12, pp. 479–490, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Scholmerich, “Interleukin in acute pancreatitis,” Scandinavian Journal of Gastroenterology, Supplement, vol. 31, no. 219, pp. 37–42, 1996. View at Scopus
  44. M. Faurschou and N. Borregaard, “Neutrophil granules and secretory vesicles in inflammation,” Microbes and Infection, vol. 5, no. 14, pp. 1317–1327, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. 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
  46. C. Cover, J. Liu, A. Farhood et al., “Pathophysiological role of the acute inflammatory response during acetaminophen hepatotoxicity,” Toxicology and Applied Pharmacology, vol. 216, no. 1, pp. 98–107, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. W. A. Verri Jr., T. M. Cunha, S. H. Ferreira et al., “IL-15 mediates antigen-induced neutrophil migration by triggering IL-18 production,” European Journal of Immunology, vol. 37, no. 12, pp. 3373–3380, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. 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
  49. C. R. Gardner, J. D. Laskin, D. M. Dambach et al., “Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: potential role of tumor necrosis factor-α and interleukin-10,” Toxicology and Applied Pharmacology, vol. 184, no. 1, pp. 27–36, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. H.-M. Kang and M. E. Saltveit, “Antioxidant capacity of lettuce leaf tissue increases after wounding,” Journal of Agricultural and Food Chemistry, vol. 50, no. 26, pp. 7536–7541, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Chan, X.-D. Han, and Y. W. Kan, “An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 8, pp. 4611–4616, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Takahashi, “Oxidative stress and redox regulation on in vitro development of mammalian embryos,” Journal of Reproduction and Development, vol. 58, no. 1, pp. 1–9, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. R. A. Gubitosi-Klug, R. Talahalli, Y. Du, J. L. Nadler, and T. S. Kern, “5-Lipoxygenase, but not 12/15-lipoxygenase, contributes to degeneration of retinal capillaries in a mouse model of diabetic retinopathy,” Diabetes, vol. 57, no. 5, pp. 1387–1393, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. C. H. C. Serezani, D. M. Aronoff, S. Jancar, and M. Peters-Golden, “Leukotriene B4 mediates p47phox phosphorylation and membrane translocation in polyunsaturated fatty acid-stimulated neutrophils,” Journal of Leukocyte Biology, vol. 78, no. 4, pp. 976–984, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. N. Chiang, C. N. Serhan, S.-E. Dahlén et al., “The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo,” Pharmacological Reviews, vol. 58, no. 3, pp. 463–487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. C. N. Serhan, “Controlling the resolution of acute inflammation: a new genus of dual anti-inflammatory and proresolving mediators,” Journal of Periodontology, vol. 79, no. 8, pp. 1520–1526, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. W. P. Beierschmitt, J. D. McNeish, R. J. Griffiths, A. Nagahisa, M. Nakane, and D. E. Amacher, “Induction of hepatic microsomal drug-metabolizing enzymes by inhibitors of 5-lipoxygenase (5-LO): studies in rats and 5-LO knockout mice,” Toxicological Sciences, vol. 63, no. 1, pp. 15–21, 2001. View at Publisher · View at Google Scholar · View at Scopus