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Oxidative Medicine and Cellular Longevity
Volume 2016 (2016), Article ID 9191407, 13 pages
http://dx.doi.org/10.1155/2016/9191407
Research Article

Preexposure to Olive Oil Polyphenols Extract Increases Oxidative Load and Improves Liver Mass Restoration after Hepatectomy in Mice via Stress-Sensitive Genes

Department of Chemistry and Biochemistry, Faculty of Medicine, University of Rijeka, Braće Branchetta 20, 51 000 Rijeka, Croatia

Received 9 September 2015; Revised 9 December 2015; Accepted 13 December 2015

Academic Editor: Ilaria Peluso

Copyright © 2016 Jelena Marinić 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. A. I. Su, L. G. Guidotti, J. P. Pezacki, F. V. Chisari, and P. G. Schultz, “Gene expression during the priming phase of liver regeneration after partial hepatectomy in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 17, pp. 11181–11186, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. F. Guerrieri, G. Vendemiale, I. Grattagliano, T. Cocco, G. Pellecchia, and E. Altomare, “Mitochondrial oxidative alterations following partial hepatectomy,” Free Radical Biology and Medicine, vol. 26, no. 1-2, pp. 34–41, 1999. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Tabrizian, S. Roayaie, and M. E. Schwartz, “Current management of hepatocellular carcinoma,” World Journal of Gastroenterology, vol. 20, no. 30, pp. 10223–10237, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. D. A. Rudnick and N. O. Davidson, “Functional relationships between lipid metabolism and liver regeneration,” International Journal of Hepatology, vol. 2012, Article ID 549241, 8 pages, 2012. View at Publisher · View at Google Scholar
  5. M. Holeček, “Nutritional modulation of liver regeneration by carbohydrates, lipids, and amino acids: a review,” Nutrition, vol. 15, no. 10, pp. 784–788, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Bouayed and T. Bohn, “Exogenous antioxidants—double-edged swords in cellular redox state: health beneficial effects at physiologic doses versus deleterious effects at high doses,” Oxidative Medicine and Cellular Longevity, vol. 3, no. 4, pp. 228–237, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. D. E. Hutter, B. G. Till, and J. J. Greene, “Redox state changes in density-dependent regulation of proliferation,” Experimental Cell Research, vol. 232, no. 2, pp. 435–438, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Ø. Moskaug, H. Carlsen, M. C. W. Myhrstad, and R. Blomhoff, “Polyphenols and glutathione synthesis regulation,” The American Journal of Clinical Nutrition, vol. 81, no. 1, supplement, pp. 277S–283S, 2005. View at Google Scholar · View at Scopus
  9. D. Seehofer, A. Schirmeier, S. Bengmark et al., “Curcumin attenuates oxidative stress and inflammatory response in the early phase after partial hepatectomy with simultaneous intraabdominal infection in rats,” Journal of Surgical Research, vol. 159, no. 1, pp. 497–502, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Trejo-Solís, V. Chagoya De Sánchez, A. Aranda-Fraustro, L. Sánchez-Sevilla, C. Gómez-Ruíz, and R. Hernández-Muñoz, “Inhibitory effect of vitamin e administration on the progression of liver regeneration induced by partial hepatectomy in rats,” Laboratory Investigation, vol. 83, no. 11, pp. 1669–1679, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. V. C. Gavino, C. J. Dillard, and A. L. Tappel, “Effect of dietary vitamin E and Santoquin on regenerating rat liver,” Life Sciences, vol. 36, no. 18, pp. 1771–1777, 1985. View at Publisher · View at Google Scholar · View at Scopus
  12. S. K. Katiyar and H. Mukhtar, “Green tea polyphenol (−)-epigallocatechin-3-gallate treatment to mouse skin prevents UVB-induced infiltration of leukocytes, depletion of antigen-presenting cells, and oxidative stress,” Journal of Leukocyte Biology, vol. 69, no. 5, pp. 719–726, 2001. View at Google Scholar · View at Scopus
  13. G. S. Manoj and K. Murugan, “Wound healing activity of methanolic and aqueous extracts of Plagiochila beddomei Steph. thallus in rat model,” Indian Journal of Experimental Biology, vol. 50, no. 8, pp. 551–558, 2012. View at Google Scholar
  14. R. T. Narendhirakannan and T. P. Limmy, “Anti-inflammatory and anti-oxidant properties of Sida rhombifolia stems and roots in adjuvant induced arthritic rats,” Immunopharmacology and Immunotoxicology, vol. 34, no. 2, pp. 326–336, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Qin, X. W. Guo, L. Li, H. W. Wang, and W. Kim, “The antioxidant property of chitosan green tea polyphenols complex induces transglutaminase activation in wound healing,” Journal of Medicinal Food, vol. 16, no. 6, pp. 487–498, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Shen, K. Thai, J. H. Stewart et al., “Peritoneal surface disease from colorectal cancer: comparison with the hepatic metastases surgical paradigm in optimally resected patients,” Annals of Surgical Oncology, vol. 15, no. 12, pp. 3422–3432, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Yonemura, A. Elnemr, Y. Endou et al., “Effects of neoadjuvant intraperitoneal/systemic chemotherapy (bidirectional chemotherapy) for the treatment of patients with peritoneal metastasis from gastric cancer,” International Journal of Surgical Oncology, vol. 2012, Article ID 148420, 8 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Hao, F. Lang, Y. Chen et al., “Resveratrol alleviates endotoxin-induced myocardial toxicity via the Nrf2 transcription factor,” PLoS ONE, vol. 8, no. 7, Article ID e69452, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Oršolić, D. Sirovina, G. Gajski, V. Garaj-Vrhovac, M. Jazvinšćak Jembrek, and I. Kosalec, “Assessment of DNA damage and lipid peroxidation in diabetic mice: effects of propolis and epigallocatechin gallate (EGCG),” Mutation Research, vol. 757, no. 1, pp. 36–44, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. S.-T. Chan, Y.-C. Lin, C.-H. Chuang, R.-J. Shiau, J.-W. Liao, and S.-L. Yeh, “Oral and intraperitoneal administration of quercetin decreased lymphocyte DNA damage and plasma lipid peroxidation induced by TSA in vivo,” BioMed Research International, vol. 2014, Article ID 580626, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Domitrović, Č. Milin, and B. Radošević-Stašić, “Liver fatty acid and element changes after partial hepatectomy in mice fed olive oil- and corn oil-enriched diets,” Biological Trace Element Research, vol. 109, no. 1, pp. 61–74, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. V. Kirimlioglu, H. Kirimlioglu, S. Yilmaz et al., “Effect of fish oil, olive oil, and vitamin E on liver pathology, cell proliferation, and antioxidant defense system in rats subjected to partial hepatectomy,” Transplantation Proceedings, vol. 38, no. 2, pp. 564–567, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. J. D. Lambert, S. M. Sang, and C. S. Yang, “Possible controversy over dietary polyphenols: benefits vs risks,” Chemical Research in Toxicology, vol. 20, no. 4, pp. 583–585, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. J. W. Fahey and P. Talalay, “Antioxidant functions of sulforaphane: a potent inducer of phase II detoxication enzymes,” Food and Chemical Toxicology, vol. 37, no. 9-10, pp. 973–979, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. J. L. Quiles, A. J. Farquharson, D. K. Simpson, I. Grant, and K. W. J. Wahle, “Olive oil phenolics: effects on DNA oxidation and redox enzyme mRNA in prostate cells,” British Journal of Nutrition, vol. 88, no. 3, pp. 225–234, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. M. C. W. Myhrstad, H. Carlsen, O. Nordström, R. Blomhoff, and J. Ø. Moskaug, “Flavonoids increase the intracellular glutathione level by transactivation of the γ-glutamylcysteine synthetase catalytical subunit promoter,” Free Radical Biology and Medicine, vol. 32, no. 5, pp. 386–393, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Patel and G. Maru, “Polymeric black tea polyphenols induce phase II enzymes via Nrf2 in mouse liver and lungs,” Free Radical Biology and Medicine, vol. 44, no. 11, pp. 1897–1911, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Erlank, A. Elmann, R. Kohen, and J. Kanner, “Polyphenols activate Nrf2 in astrocytes via H2O2, semiquinones, and quinones,” Free Radical Biology and Medicine, vol. 51, no. 12, pp. 2319–2327, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. I. Carmona-Ramírez, A. Santamaría, J. C. Tobón-Velasco et al., “Curcumin restores Nrf2 levels and prevents quinolinic acid-induced neurotoxicity,” Journal of Nutritional Biochemistry, vol. 24, no. 1, pp. 14–24, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Lau, N. F. Villeneuve, Z. Sun, P. K. Wong, and D. D. Zhang, “Dual roles of Nrf2 in cancer,” Pharmacological Research, vol. 58, no. 5-6, pp. 262–270, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. E. Purdom-Dickinson, E. V. Sheveleva, H. Sun, and Q. M. Chen, “Translational control of Nrf2 protein in activation of antioxidant response by oxidants,” Molecular Pharmacology, vol. 72, no. 4, pp. 1074–1081, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. H.-K. Na and Y.-J. Surh, “Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG,” Food and Chemical Toxicology, vol. 46, no. 4, pp. 1271–1278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. T. A. Beyer, W. Xu, D. Teupser et al., “Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance,” The EMBO Journal, vol. 27, no. 1, pp. 212–223, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Homma, Y. Ishii, Y. Morishima et al., “Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer,” Clinical Cancer Research, vol. 15, no. 10, pp. 3423–3432, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. N. M. Reddy, S. R. Kleeberger, J. H. Bream et al., “Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling,” Oncogene, vol. 27, no. 44, pp. 5821–5832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Itoh, N. Wakabayashi, Y. Katoh et al., “Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain,” Genes & Development, vol. 13, no. 1, pp. 76–86, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. Z. Jian, K. Li, P. Song et al., “Impaired activation of the Nrf2-ARE signaling pathway undermines H2O2-induced oxidative stress response: a possible mechanism for melanocyte degeneration in vitiligo,” Journal of Investigative Dermatology, vol. 134, no. 8, pp. 2221–2230, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Kobayashi and M. Yamamoto, “Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species,” Advances in Enzyme Regulation, vol. 46, no. 1, pp. 113–140, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Swain and W. E. Hillis, “The phenolic constituents of Prunus domestica. I.—the quantitative analysis of phenolic constituents,” Journal of the Science of Food and Agriculture, vol. 10, no. 1, pp. 63–68, 1959. View at Publisher · View at Google Scholar
  40. T. Gutfinger, “Polyphenols in olive oils,” Journal of the American Oil Chemists Society, vol. 58, no. 11, pp. 966–968, 1981. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Mateos, J. L. Espartero, M. Trujillo et al., “Determination of phenols, flavones, and lignans in virgin olive oils by solid-phase extraction and high-performance liquid chromatography with diode array ultraviolet detection,” Journal of Agricultural and Food Chemistry, vol. 49, no. 5, pp. 2185–2192, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Broznić, J. Marinić, M. Tota, G. Č. Jurešić, and Č. Milin, “Kinetic evaluation of imidacloprid degradation in mice organs treated with olive oil polyphenols extract,” Croatica Chemica Acta, vol. 81, no. 1, pp. 203–209, 2008. View at Google Scholar · View at Scopus
  43. V. Ruíz-Gutiérrez, F. J. G. Muriana, R. Maestro, and E. Graciani, “Oleuropein on lipid and fatty acid composition of rat heart,” Nutrition Research, vol. 15, no. 1, pp. 37–51, 1995. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Cao, J. Xu, X. Zou et al., “Hydroxytyrosol prevents diet-induced metabolic syndrome and attenuates mitochondrial abnormalities in obese mice,” Free Radical Biology and Medicine, vol. 67, pp. 396–407, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Zheng, H. Li, K. Cao et al., “Maternal hydroxytyrosol administration improves neurogenesis and cognitive function in prenatally stressed offspring,” Journal of Nutritional Biochemistry, vol. 26, no. 2, pp. 190–199, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. R. W. Owen, W. Mier, A. Giacosa, W. E. Hull, B. Spiegelhalder, and H. Bartsch, “Phenolic compounds and squalene in olive oils: the concentration and antioxidant potential of total phenols, simple phenols, secoiridoids, lignansand squalene,” Food and Chemical Toxicology, vol. 38, no. 8, pp. 647–659, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Beer, A. Zetterberg, R. A. Ihrie et al., “Developmental context determines latency of MYC-induced tumorigenesis,” PLoS Biology, vol. 2, no. 11, pp. 1785–1798, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal-tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Publisher · View at Google Scholar · View at Scopus
  49. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  50. Z. Z. Huang, C. J. Chen, Z. H. Zeng et al., “Mechanism and significance of increased glutathione level in human hepatocellular carcinoma and liver regeneration,” The FASEB journal : official publication of the Federation of American Societies for Experimental Biology, vol. 15, no. 1, pp. 19–21, 2001. View at Google Scholar · View at Scopus
  51. K. Kuramitsu, D. Gallo, M. Yoon et al., “Carbon monoxide enhances early liver regeneration in mice after hepatectomy,” Hepatology, vol. 53, no. 6, pp. 2016–2026, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. H. R. Moinova and R. T. Mulcahy, “Up-regulation of the human gamma-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element,” Biochemical and Biophysical Research Communications, vol. 261, no. 3, pp. 661–668, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Prestera, P. Talalay, J. Alam, Y. I. Ahn, P. J. Lee, and A. M. Choi, “Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: regulation by upstream antioxidant-responsive elements (ARE),” Molecular Medicine, vol. 1, no. 7, pp. 827–837, 1995. View at Google Scholar · View at Scopus
  54. H. J. Prochaska and C. L. Fernandes, “Elevation of serum phase II enzymes by anticarcinogenic enzyme inducers: markers for a chemoprotected state?” Carcinogenesis, vol. 14, no. 12, pp. 2441–2445, 1993. View at Google Scholar · View at Scopus
  55. H. Fiander and H. Schneider, “Dietary ortho phenols that induce glutathione S-transferase and increase the resistance of cells to hydrogen peroxide are potential cancer chemopreventives that act by two mechanisms: the alleviation of oxidative stress and the detoxification of mutagenic xenobiotics,” Cancer Letters, vol. 156, no. 2, pp. 117–124, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. I. H. Alexandris, S. F. Assimakopoulos, C. E. Vagianos et al., “Oxidative state in intestine and liver after partial hepatectomy in rats. Effect of bombesin and neurotensin,” Clinical Biochemistry, vol. 37, no. 5, pp. 350–356, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. C. S. Lai, L. E. Hopwood, J. S. Hyde, and S. Lukiewicz, “ESR studies of O2 uptake by Chinese hamster ovary cells during the cell cycle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 4, pp. 1166–1170, 1982. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Hortelano, B. Dewez, A. M. Genaro, M. J. M. Diaz-Guerra, and L. Bosca, “Nitric-oxide is released in regenerating liver after partial-hepatectomy,” Hepatology, vol. 21, no. 3, pp. 776–786, 1995. View at Publisher · View at Google Scholar · View at Scopus
  59. T. A. Beyer and S. Werner, “The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver,” Cell Cycle, vol. 7, no. 7, pp. 874–878, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. G. Scapagnini, R. Foresti, V. Calabrese, A. M. G. Stella, C. J. Green, and R. Motterlini, “Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers (vol 61, pg 554, 2002),” Molecular Pharmacology, vol. 61, no. 5, p. 1264, 2002. View at Google Scholar
  61. S. A. Reisman, I. I. Csanaky, R. I. Yeager, and C. D. Klaassen, “Nrf2 activation enhances biliary excretion of sulfobromophthalein by inducing glutathione-S-transferase activity,” Toxicological Sciences, vol. 109, no. 1, pp. 24–30, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. F. Q. Schafer and G. R. Buettner, “Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple,” Free Radical Biology and Medicine, vol. 30, no. 11, pp. 1191–1212, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. C. A. Redaelli, Y.-H. Tian, T. Schaffner, M. Ledermann, H. U. Baer, and J.-F. Dufour, “Extended preservation of rat liver graft by induction of heme oxygenase-1,” Hepatology, vol. 35, no. 5, pp. 1082–1092, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. H. J. Forman, K. J. A. Davies, and F. Ursini, “How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo,” Free Radical Biology and Medicine, vol. 66, pp. 24–35, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Fabiani, P. Rosignoli, A. De Bartolomeo, R. Fuccelli, M. Servili, and G. Morozzi, “The production of hydrogen peroxide is not a common mechanism by which olive oil phenols induce apoptosis on HL60 cells,” Food Chemistry, vol. 125, no. 4, pp. 1249–1255, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Columbano and H. Shinozuka, “Liver regeneration versus direct hyperplasia,” The FASEB Journal, vol. 10, no. 10, pp. 1118–1128, 1996. View at Google Scholar
  67. A. T. Dinkova-Kostova and X. J. Wang, “Induction of the Keap1/Nrf2/ARE pathway by oxidizable diphenols,” Chemico-Biological Interactions, vol. 192, no. 1-2, pp. 101–106, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. G. Galati, O. Sabzevari, J. X. Wilson, and P. J. O'Brien, “Prooxidant activity and cellular effects of the phenoxyl radicals of dietary flavonoids and other polyphenolics,” Toxicology, vol. 177, no. 1, pp. 91–104, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. X. J. Wang, J. D. Hayes, L. G. Higgins, C. R. Wolf, and A. T. Dinkova-Kostova, “Activation of the NRF2 signaling pathway by copper-mediated redox cycling of para- and ortho-hydroquinones,” Chemistry and Biology, vol. 17, no. 1, pp. 75–85, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Briante, F. Febbraio, and R. Nucci, “Antioxidant/prooxidant effects of dietary non-flavonoid phenols on the Cu2+-induced oxidation of human low-density lipoprotein (LDL),” Chemistry & Biodiversity, vol. 1, no. 11, pp. 1716–1729, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Jakovac, D. Grebić, I. Mrakovcic-Sutic et al., “Metallothionein expression and tissue metal kinetics after partial hepatectomy in mice,” Biological Trace Element Research, vol. 114, no. 1–3, pp. 249–268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Zrelli, M. Matsuoka, S. Kitazaki et al., “Hydroxytyrosol induces proliferation and cytoprotection against oxidative injury in vascular endothelial cells: role of Nrf2 activation and HO-1 induction,” Journal of Agricultural and Food Chemistry, vol. 59, no. 9, pp. 4473–4482, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. L. A. Furchtgott, C. C. Chow, and V. Periwal, “A model of liver regeneration,” Biophysical Journal, vol. 96, no. 10, pp. 3926–3935, 2009. View at Publisher · View at Google Scholar · View at Scopus