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Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 8325754, 12 pages
https://doi.org/10.1155/2017/8325754
Research Article

Modulation of Glutathione Hemostasis by Inhibition of 12/15-Lipoxygenase Prevents ROS-Mediated Cell Death after Hepatic Ischemia and Reperfusion

1Department of General, Visceral, Vascular and Transplant Surgery, University Hospital Munich, Ludwig-Maximilians University of Munich, Campus Großhadern, Munich, Germany
2Institute of Developmental Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, Munich, Germany
3Department of Internal Medicine II, University Hospital Munich, Ludwig-Maximilians University of Munich, Campus Großhadern, Munich, Germany
4Institute of Laboratory Medicine, University Hospital Munich, Ludwig-Maximilians University of Munich, Campus Großhadern, Munich, Germany

Correspondence should be addressed to Moritz Drefs

Received 29 March 2017; Accepted 18 June 2017; Published 24 July 2017

Academic Editor: Andrey A. Zamyatnin Jr.

Copyright © 2017 Moritz Drefs 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. C. Fondevila, R. W. Busuttil, and J. W. Kupiec-Weglinski, “Hepatic ischemia/reperfusion injury—a fresh look,” Experimental and Molecular Pathology, vol. 74, no. 2, pp. 86–93, 2003. View at Google Scholar
  2. O. Rougemont, K. Lehmann, and P. A. Clavien, “Preconditioning, organ preservation, and postconditioning to prevent ischemia-reperfusion injury to the liver,” Liver Transplantation, vol. 15, no. 10, pp. 1172–1182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. A. G. Tsiotou, G. H. Sakorafas, G. Anagnostopoulos, and J. Bramis, “Septic shock; current pathogenetic concepts from a clinical perspective,” Medical Science Monitor, vol. 11, no. 3, pp. RA76–RA85, 2005. View at Google Scholar
  4. H. Jaeschke, “Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 284, no. 1, pp. G15–G26, 2003. View at Publisher · View at Google Scholar
  5. E. E. Montalvo-Jave, T. Escalante-Tattersfield, J. A. Ortega-Salgado, E. Pina, and D. A. Geller, “Factors in the pathophysiology of the liver ischemia-reperfusion injury,” The Journal of Surgical Research, vol. 147, no. 1, pp. 153–159, 2008. View at Google Scholar
  6. J. S. Kim, L. He, T. Qian, and J. J. Lemasters, “Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes,” Current Molecular Medicine, vol. 3, no. 6, pp. 527–535, 2003. View at Google Scholar
  7. P. Vandenabeele, L. Galluzzi, T. Berghe, and G. Kroemer, “Molecular mechanisms of necroptosis: an ordered cellular explosion,” Nature Reviews Molecular Cell Biology, vol. 11, no. 10, pp. 700–714, 2010. View at Google Scholar
  8. S. Q. Rodriguez-Lara, E. G. Cardona-Munoz, E. J. Ramirez-Lizardo et al., “Alternative interventions to prevent oxidative damage following ischemia/reperfusion,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 7190943, 16 pages, 2016. View at Publisher · View at Google Scholar
  9. S. J. Dixon, K. M. Lemberg, M. R. Lamprecht et al., “Ferroptosis: an iron-dependent form of nonapoptotic cell death,” Cell, vol. 149, no. 5, pp. 1060–1072, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Galluzzi, I. Vitale, J. M. Abrams et al., “Molecular definitions of cell death subroutines: recommendations of the nomenclature committee on cell death 2012,” Cell Death and Differentiation, vol. 19, no. 1, pp. 107–120, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Conrad, J. P. Angeli, P. Vandenabeele, and B. R. Stockwell, “Regulated necrosis: disease relevance and therapeutic opportunities,” Nature Reviews Drug Discovery, vol. 15, no. 5, pp. 348–366, 2016. View at Google Scholar
  12. C. Nastos, K. Kalimeris, N. Papoutsidakis et al., “Global consequences of liver ischemia/reperfusion injury,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 906965, 13 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Garcea, A. Gescher, W. Steward, A. Dennison, and D. Berry, “Oxidative stress in humans following the Pringle manoeuvre,” Hepatobiliary & Pancreatic Diseases International, vol. 5, no. 2, pp. 210–214, 2006. View at Google Scholar
  14. C. D. Collard and S. Gelman, “Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury,” Anesthesiology, vol. 94, no. 6, pp. 1133–1138, 2001. View at Google Scholar
  15. C. Vela, M. Thomsen, S. Delbosc, D. Calise, J. P. Cristol, and G. Mourad, “Lipid and oxidative stress disorders in a rat model of chronic rejection,” Transplantation Proceedings, vol. 39, no. 8, pp. 2617–2619, 2007. View at Google Scholar
  16. S. Shi and F. Xue, “Current antioxidant treatments in organ transplantation,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 8678510, 9 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Birben, U. M. Sahiner, C. Sackesen, S. Erzurum, and O. Kalayci, “Oxidative stress and antioxidant defense,” The World Allergy Organization Journal, vol. 5, no. 1, pp. 9–19, 2012. View at Google Scholar
  18. A. W. Girotti, “Mechanisms of lipid peroxidation,” Journal of Free Radicals in Biology & Medicine, vol. 1, no. 2, pp. 87–95, 1985. View at Google Scholar
  19. B. J. Zimmerman and D. N. Granger, “Reperfusion injury,” The Surgical Clinics of North America, vol. 72, no. 1, pp. 65–83, 1992. View at Google Scholar
  20. H. Jaeschke and J. J. Lemasters, “Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury,” Gastroenterology, vol. 125, no. 4, pp. 1246–1257, 2003. View at Google Scholar
  21. S. Pallast, K. Arai, X. Wang, E. H. Lo, and K. Leyen, “12/15-Lipoxygenase targets neuronal mitochondria under oxidative stress,” Journal of Neurochemistry, vol. 111, no. 3, pp. 882–889, 2009. View at Google Scholar
  22. D. J. Conrad, “The arachidonate 12/15 lipoxygenases. A review of tissue expression and biologic function,” Clinical Reviews in Allergy & Immunology, vol. 17, no. 1-2, pp. 71–89, 1999. View at Google Scholar
  23. J. Loscalzo, “Membrane redox state and apoptosis: death by peroxide,” Cell Metabolism, vol. 8, no. 3, pp. 182-183, 2008. View at Google Scholar
  24. J. P. Thomas, M. Maiorino, F. Ursini, and A. W. Girotti, “Protective action of phospholipid hydroperoxide glutathione peroxidase against membrane-damaging lipid peroxidation. In situ reduction of phospholipid and cholesterol hydroperoxides,” The Journal of Biological Chemistry, vol. 265, no. 1, pp. 454–461, 1990. View at Google Scholar
  25. J. P. Friedmann Angeli, M. Schneider, B. Proneth et al., “Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice,” Nature Cell Biology, vol. 16, no. 12, pp. 1180–1191, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Seiler, M. Schneider, H. Forster et al., “Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death,” Cell Metabolism, vol. 8, no. 3, pp. 237–248, 2008. View at Google Scholar
  27. K. Leyen, H. Y. Kim, S. R. Lee, G. Jin, K. Arai, and E. H. Lo, “Baicalein and 12/15-lipoxygenase in the ischemic brain,” Stroke, vol. 37, no. 12, pp. 3014–3018, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Yigitkanli, A. Pekcec, H. Karatas et al., “Inhibition of 12/15-lipoxygenase as therapeutic strategy to treat stroke,” Annals of Neurology, vol. 73, no. 1, pp. 129–135, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Yigitkanli, Y. Zheng, A. Pekcec, E. H. Lo, and K. Leyen, “Increased 12/15-lipoxygenase leads to widespread brain injury following global cerebral ischemia,” Translational Stroke Research, vol. 8, no. 2, pp. 194–202, 2017. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Song, H. Yang, H. X. Wang et al., “Inhibition of 12/15 lipoxygenase by baicalein reduces myocardial ischemia/reperfusion injury via modulation of multiple signaling pathways,” Apoptosis: An International Journal on Programmed Cell Death, vol. 19, no. 4, pp. 567–580, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Liang, H. Remmen, V. Frohlich, J. Lechleiter, A. Richardson, and Q. Ran, “Gpx4 protects mitochondrial ATP generation against oxidative damage,” Biochemical and Biophysical Research Communications, vol. 356, no. 4, pp. 893–898, 2007. View at Google Scholar
  32. M. Bilzer, A. Baron, R. Schauer, C. Steib, S. Ebensberger, and A. L. Gerbes, “Glutathione treatment protects the rat liver against injury after warm ischemia and Kupffer cell activation,” Digestion, vol. 66, no. 1, pp. 49–57, 2002. View at Google Scholar
  33. R. J. Schauer, A. L. Gerbes, D. Vonier et al., “Glutathione protects the rat liver against reperfusion injury after prolonged warm ischemia,” Annals of Surgery, vol. 239, no. 2, pp. 220–231, 2004. View at Google Scholar
  34. Y. Shang, Y. L. Siow, C. K. Isaak, and O. Karmin, “Downregulation of glutathione biosynthesis contributes to oxidative stress and liver dysfunction in acute kidney injury,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 9707292, 13 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Rossi, C. Pergola, S. Cuzzocrea, and L. Sautebin, “The role of 5-lipoxygenase and leukotrienes in shock and ischemia-reperfusion injury,” TheScientificWorldJOURNAL, vol. 7, pp. 56–74, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Hughes, A. Farhood, and H. Jaeschke, “Role of leukotriene B4 in the pathogenesis of hepatic ischemia-reperfusion injury in the rat,” Prostaglandins, Leukotrienes, and Essential Fatty Acids, vol. 45, no. 2, pp. 113–119, 1992. View at Google Scholar
  37. N. Matsui, N. Fukuishi, Y. Fukuyama, Y. Yasui, and M. Akagi, “Protective effect of the 5-lipoxygenase inhibitor ardisiaquinone A on hepatic ischemia-reperfusion injury in rats,” Planta Medica, vol. 71, no. 8, pp. 717–720, 2005. View at Google Scholar
  38. G. Daglar, T. Karaca, Y. N. Yuksek et al., “Effect of montelukast and MK-886 on hepatic ischemia-reperfusion injury in rats,” The Journal of Surgical Research, vol. 153, no. 1, pp. 31–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Bochorakova, H. Paulova, J. Slanina, P. Musil, and E. Taborska, “Main flavonoids in the root of Scutellaria baicalensis cultivated in Europe and their comparative antiradical properties,” Phytotherapy Research, vol. 17, no. 6, pp. 640–644, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. J. D. Deschamps, V. A. Kenyon, and T. R. Holman, “Baicalein is a potent in vitro inhibitor against both reticulocyte 15-human and platelet 12-human lipoxygenases,” Bioorganic & Medicinal Chemistry, vol. 14, no. 12, pp. 4295–4301, 2006. View at Google Scholar
  41. B. Dinda, S. Dinda, S. DasSharma, R. Banik, A. Chakraborty, and M. Dinda, “Therapeutic potentials of baicalin and its aglycone, baicalein against inflammatory disorders,” European Journal of Medicinal Chemistry, vol. 131, pp. 68–80, 2017. View at Google Scholar
  42. T. Hori, N. Ohashi, F. Chen et al., “Simple and sure methodology for massive hepatectomy in the mouse,” Annals of Gastroenterology, vol. 24, no. 4, pp. 307–318, 2011. View at Google Scholar
  43. G. Lukas, S. D. Brindle, and P. Greengard, “The route of absorption of intraperitoneally administered compounds,” The Journal of Pharmacology and Experimental Therapeutics, vol. 178, no. 3, pp. 562–564, 1971. View at Google Scholar
  44. S. Mehendale, H. Aung, C. Z. Wang et al., “Scutellaria baicalensis and a constituent flavonoid, baicalein, attenuate ritonavir-induced gastrointestinal side-effects,” The Journal of Pharmacy and Pharmacology, vol. 59, no. 11, pp. 1567–1572, 2007. View at Google Scholar
  45. P. V. Turner, T. Brabb, C. Pekow, and M. A. Vasbinder, “Administration of substances to laboratory animals: routes of administration and factors to consider,” Journal of the American Association for Laboratory Animal Science, vol. 50, no. 5, pp. 600–613, 2011. View at Google Scholar
  46. K. H. Diehl, R. Hull, D. Morton et al., “A good practice guide to the administration of substances and removal of blood, including routes and volumes,” Journal of Applied Toxicology, vol. 21, no. 1, pp. 15–23, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Tietze, “Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues,” Analytical Biochemistry, vol. 27, no. 3, pp. 502–522, 1969. View at Google Scholar
  48. B. H. Lauterburg, J. D. Adams, and J. R. Mitchell, “Hepatic glutathione homeostasis in the rat: efflux accounts for glutathione turnover,” Hepatology, vol. 4, no. 4, pp. 586–590, 1984. View at Google Scholar
  49. Y. Zhai, H. Petrowsky, J. C. Hong, R. W. Busuttil, and J. W. Kupiec-Weglinski, “Ischaemia-reperfusion injury in liver transplantation—from bench to bedside,” Nature Reviews Gastroenterology & Hepatology, vol. 10, no. 2, pp. 79–89, 2013. View at Google Scholar
  50. X. H. Zhu, J. P. Pan, Y. F. Wu, and Y. T. Ding, “Effects of warm ischemia time on biliary injury in rat liver transplantation,” World Journal of Gastroenterology, vol. 18, no. 43, pp. 6308–6314, 2012. View at Google Scholar
  51. Z. Du, S. Dong, P. Lin et al., “Warm ischemia may damage peribiliary vascular plexus during DCD liver transplantation,” International Journal of Clinical and Experimental Medicine, vol. 8, no. 1, pp. 758–763, 2015. View at Google Scholar
  52. T. Ikeda, K. Yanaga, K. Kishikawa, S. Kakizoe, M. Shimada, and K. Sugimachi, “Ischemic injury in liver transplantation: difference in injury sites between warm and cold ischemia in rats,” Hepatology, vol. 16, no. 2, pp. 454–461, 1992. View at Google Scholar
  53. G. Datta, B. J. Fuller, and B. R. Davidson, “Molecular mechanisms of liver ischemia reperfusion injury: insights from transgenic knockout models,” World Journal of Gastroenterology, vol. 19, no. 11, pp. 1683–1698, 2013. View at Google Scholar
  54. R. S. Hotchkiss, A. Strasser, J. E. McDunn, and P. E. Swanson, “Cell death,” The New England Journal of Medicine, vol. 361, no. 16, pp. 1570–1583, 2009. View at Google Scholar
  55. J. Pirenne, B. Gunson, H. Khaleef et al., “Influence of ischemia-reperfusion injury on rejection after liver transplantation,” Transplantation Proceedings, vol. 29, no. 1-2, pp. 366-367, 1997. View at Google Scholar
  56. Y. Xie, X. Song, X. Sun et al., “Identification of baicalein as a ferroptosis inhibitor by natural product library screening,” Biochemical and Biophysical Research Communications, vol. 473, no. 4, pp. 775–780, 2016. View at Publisher · View at Google Scholar · View at Scopus
  57. B. A. Carlson, R. Tobe, E. Yefremova et al., “Glutathione peroxidase 4 and vitamin E cooperatively prevent hepatocellular degeneration,” Redox Biology, vol. 9, pp. 22–31, 2016. View at Publisher · View at Google Scholar · View at Scopus
  58. W. S. Yang, R. SriRamaratnam, M. E. Welsch et al., “Regulation of ferroptotic cancer cell death by GPX4,” Cell, vol. 156, no. 1-2, pp. 317–331, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Doll, B. Proneth, Y. Y. Tyurina et al., “ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition,” Nature Chemical Biology, vol. 13, no. 1, pp. 91–98, 2017. View at Publisher · View at Google Scholar
  60. M. Rentsch, A. Beham, I. Iesalnieks, T. Mirwald, M. Anthuber, and K. W. Jauch, “Impact of prolonged cold ischemia and reperfusion on apoptosis, activation of caspase 3, and expression of bax after liver transplantation in the rat,” Transplantation Proceedings, vol. 33, no. 1-2, pp. 850-851, 2001. View at Google Scholar
  61. T. H. Mueller, K. Kienle, A. Beham, E. K. Geissler, K. W. Jauch, and M. Rentsch, “Caspase 3 inhibition improves survival and reduces early graft injury after ischemia and reperfusion in rat liver transplantation,” Transplantation, vol. 78, no. 9, pp. 1267–1273, 2004. View at Google Scholar
  62. S. Ahmed, K. G. Grant, L. E. Edwards et al., “Data-driven modeling reconciles kinetics of ERK phosphorylation, localization, and activity states,” Molecular Systems Biology, vol. 10, p. 718, 2014. View at Google Scholar
  63. F. J. Oliver, G. Rubia, V. Rolli, M. C. Ruiz-Ruiz, G. Murcia, and J. M. Murcia, “Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant,” The Journal of Biological Chemistry, vol. 273, no. 50, pp. 33533–33539, 1998. View at Publisher · View at Google Scholar · View at Scopus
  64. R. J. Davis, “Signal transduction by the c-Jun N-terminal kinase,” Biochemical Society Symposium, vol. 64, pp. 1–12, 1999. View at Google Scholar
  65. P. P. Roux and J. Blenis, “ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions,” Microbiology and Molecular Biology Reviews, vol. 68, no. 2, pp. 320–344, 2004. View at Google Scholar
  66. N. Akyurek, E. M. Kafali, and S. Muhtaroglu, “The effects of dimethylsulfoxide on experimental hepatic ischemia,” Swiss Surgery, vol. 6, no. 1, pp. 23–27, 2000. View at Publisher · View at Google Scholar
  67. M. Sahin, F. M. Avsar, H. Ozel et al., “The effects of dimethyl sulfoxide on liver damage caused by ischemia-reperfusion,” Transplantation Proceedings, vol. 36, no. 9, pp. 2590–2592, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Ito, R. C. Lind, C. K. Begay, A. J. Gandolfi, M. K. McCuskey, and R. S. McCuskey, “Late administration of dimethyl sulfoxide minimizes the hepatic microvascular inflammatory response to chloroform in rats,” Hepatology Research, vol. 18, no. 3, pp. 203–217, 2000. View at Google Scholar
  69. C. Iida, K. Fujii, E. Koga, Y. Washino, I. Ichi, and S. Kojo, “Inhibitory effect of dimethyl sulfoxide (DMSO) on necrosis and oxidative stress caused by D-galactosamine in the rat liver,” Journal of Nutritional Science and Vitaminology, vol. 53, no. 2, pp. 160–165, 2007. View at Google Scholar
  70. M. Rentsch, K. Puellmann, S. Sirek et al., “Benefit of Kupffer cell modulation with glycine versus Kupffer cell depletion after liver transplantation in the rat: effects on postischemic reperfusion injury, apoptotic cell death graft regeneration and survival,” Transplant International, vol. 18, no. 9, pp. 1079–1089, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Maemura, Q. Zheng, T. Wada et al., “Reactive oxygen species are essential mediators in antigen presentation by Kupffer cells,” Immunology and Cell Biology, vol. 83, no. 4, pp. 336–343, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. S. W. Jacob and E. E. Rosenbaum, “The toxicology of dimethyl sulfoxide (DMSO),” Headache, vol. 6, no. 3, pp. 127–136, 1966. View at Google Scholar
  73. X. Huang, Y. He, Y. Chen et al., “Baicalin attenuates bleomycin-induced pulmonary fibrosis via adenosine A2a receptor related TGF-beta1-induced ERK1/2 signaling pathway,” BMC Pulmonary Medicine, vol. 16, no. 1, p. 132, 2016. View at Google Scholar
  74. L. Zhang, Z. Pu, J. Wang, Z. Zhang, and D. Hu, “Baicalin inhibits hypoxia-induced pulmonary artery smooth muscle cell proliferation via the AKT/HIF-1alpha/p27-associated pathway,” International Journal of Molecular Sciences, vol. 15, no. 5, pp. 8153–8168, 2014. View at Google Scholar
  75. M. Pazin, T. B. Andreo, L. C. Pereira, M. F. F. Bernardes, R. S. Ferrari, and D. J. Dorta, “Baicalein can be a great antioxidant, but it can impair mitochondrial bioenergetics and cause cytotoxicity at high concentrations,” Applied Research in Toxicology, vol. 1, no. 1, pp. 9–18, 2015. View at Google Scholar
  76. Y. Wang, Q. Wang, S. Zhang, Y. Zhang, and L. Tao, “Baicalein increases the cytotoxicity of cisplatin by enhancing gap junction intercellular communication,” Molecular Medicine Reports, vol. 10, no. 1, pp. 515–521, 2014. View at Publisher · View at Google Scholar · View at Scopus