Table of Contents Author Guidelines Submit a Manuscript
Evidence-Based Complementary and Alternative Medicine
Volume 2013, Article ID 424692, 19 pages
http://dx.doi.org/10.1155/2013/424692
Research Article

Curcumin Pretreatment Prevents Potassium Dichromate-Induced Hepatotoxicity, Oxidative Stress, Decreased Respiratory Complex I Activity, and Membrane Permeability Transition Pore Opening

1Department of Biology, Faculty of Chemistry, National Autonomous University of Mexico (UNAM), University City, 04510 Mexico City, DF, Mexico
2Renal Pathophysiology Laboratory, Department of Nephrology, National Institute of Cardiology “Ignacio Chávez”, 14080 Mexico City, DF, Mexico
3Department of Cardiovascular Biomedicine, National Institute of Cardiology “Ignacio Chávez”, 14080 Mexico City, DF, Mexico
4Experimental Pathology Section, National Institute of Medical Sciences and Nutrition “Salvador Zubirán”, 14000 Mexico City, DF, Mexico
5Department of Preclinical Toxicology, National Polytechnic Institute, 14740 Mexico City, DF, Mexico

Received 18 March 2013; Revised 7 June 2013; Accepted 16 June 2013

Academic Editor: Shrikant Anant

Copyright © 2013 Wylly Ramsés García-Niño 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. P. Anand, C. Sundaram, S. Jhurani, A. B. Kunnumakkara, and B. B. Aggarwal, “Curcumin and cancer: an “old-age” disease with an “age-old” solution,” Cancer Letters, vol. 267, no. 1, pp. 133–164, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. I. Chattopadhyay, K. Biswas, U. Bandyopadhyay, and R. K. Banerjee, “Turmeric and curcumin: biological actions and medicinal applications,” Current Science, vol. 87, no. 1, pp. 44–53, 2004. View at Google Scholar · View at Scopus
  3. B. Aggarwal, I. Bhatt, H. Ichikawa et al., “Curcumin—biological and medicinal properties,” in Turmeric: the Genus Curcuma, Medicinal and Aromatic Plants-Industrial Profiles, pp. 297–368, CRC Press, New York, NY, USA, 2007. View at Google Scholar
  4. Y. Rivera-Espinoza and P. Muriel, “Pharmacological actions of curcumin in liver diseases or damage,” Liver International, vol. 29, no. 10, pp. 1457–1466, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Iqbal, S. D. Sharma, Y. Okazaki, M. Fujisawa, and S. Okada, “Dietary supplementation of curcumin enhances antioxidant and phase II metabolizing enzymes in ddY male mice: possible role in protection against chemical carcinogenesis and toxicity,” Pharmacology and Toxicology, vol. 92, no. 1, pp. 33–38, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Tajbakhsh, K. Mohammadi, I. Deilami et al., “Antibacterial activity of indium curcumin and indium diacetylcurcumin,” African Journal of Biotechnology, vol. 7, no. 21, pp. 3832–3835, 2008. View at Google Scholar · View at Scopus
  7. J. S. Jurenka, “Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research,” Alternative Medicine Review, vol. 14, no. 2, pp. 141–153, 2009. View at Google Scholar · View at Scopus
  8. B. B. Aggarwal, A. Kumar, and A. C. Bharti, “Anticancer potential of curcumin: preclinical and clinical studies,” Anticancer Research, vol. 23, no. 1, pp. 363–398, 2003. View at Google Scholar · View at Scopus
  9. E. O. Farombi, S. Shrotriya, H.-K. Na, S.-H. Kim, and Y.-J. Surh, “Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1,” Food and Chemical Toxicology, vol. 46, no. 4, pp. 1279–1287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. A. A. Nanji, K. Jokelainen, G. L. Tipoe, A. Rahemtulla, P. Thomas, and A. J. Dannenberg, “Curcumin prevents alcohol-induced liver disease in rats by inhibiting the expression of NF-κB-dependent genes,” American Journal of Physiology, vol. 284, no. 2, pp. G321–G327, 2003. View at Google Scholar · View at Scopus
  11. N. Mathuria and R. J. Verma, “Curcumin ameliorates aflatoxin-induced lipid peroxidation in liver, kidney and testis of mice—an in vitro study,” Acta Poloniae Pharmaceutica, vol. 64, no. 5, pp. 413–416, 2007. View at Google Scholar · View at Scopus
  12. M. I. Yousef, S. A. M. Omar, M. I. El-Guendi, and L. A. Abdelmegid, “Potential protective effects of quercetin and curcumin on paracetamol-induced histological changes, oxidative stress, impaired liver and kidney functions and haematotoxicity in rat,” Food and Chemical Toxicology, vol. 48, no. 11, pp. 3246–3261, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. R. A. M. Hemeida and O. M. Mohafez, “Curcumin attenuates methotraxate-induced hepatic oxidative damage in rats,” Journal of the Egyptian National Cancer Institute, vol. 20, no. 2, pp. 141–148, 2008. View at Google Scholar · View at Scopus
  14. H. S. Farghaly and M. A. Hussein, “Protective effect of curcumin against paracetamol-induced liver damage,” Australian Journal of Basic and Applied Sciences, vol. 4, no. 9, pp. 4266–4274, 2010. View at Google Scholar · View at Scopus
  15. S. Zheng, F. Yumei, and A. Chen, “De novo synthesis of glutathione is a prerequisite for curcumin to inhibit hepatic stellate cell (HSC) activation,” Free Radical Biology and Medicine, vol. 43, no. 3, pp. 444–453, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Priya and P. R. Sudhakaran, “Curcumin-induced recovery from hepatic injury involves induction of apoptosis of activated hepatic stellate cells,” Indian Journal of Biochemistry and Biophysics, vol. 45, no. 5, pp. 317–325, 2008. View at Google Scholar · View at Scopus
  17. Y. Fu, S. Zheng, J. Lin, J. Ryerse, and A. Chen, “Curcumin protects the rat liver from CCl4-caused injury and fibrogenesis by attenuating oxidative stress and suppressing inflammation,” Molecular Pharmacology, vol. 73, no. 2, pp. 399–409, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. U. Subudhi, K. Das, B. Paital, S. Bhanja, and G. B. N. Chainy, “Alleviation of enhanced oxidative stress and oxygen consumption of l-thyroxine induced hyperthyroid rat liver mitochondria by vitamin E and curcumin,” Chemico-Biological Interactions, vol. 173, no. 2, pp. 105–114, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Pechova and L. Pavlata, “Chromium as an essential nutrient: a review,” Veterinarni Medicina, vol. 52, no. 1, pp. 1–18, 2007. View at Google Scholar · View at Scopus
  20. D. Bagchi, S. J. Stohs, B. W. Downs, M. Bagchi, and H. G. Preuss, “Cytotoxicity and oxidative mechanisms of different forms of chromium,” Toxicology, vol. 180, no. 1, pp. 5–22, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. X. He, G. X. Lin, M. G. Chen, J. X. Zhang, and Q. Ma, “Protection against chromium (VI)-Induced oxidative stress and apoptosis by Nrf2. Recruiting Nrf2 into the nucleus and disrupting the nuclear Nrf2/Keap1 Association,” Toxicological Sciences, vol. 98, no. 1, pp. 298–309, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. A. Armienta, O. Morton, R. Rodríguez, O. Cruz, A. Aguayo, and N. Ceniceros, “Chromium in a tannery wastewater irrigated area, León Valley, Mexico,” Bulletin of Environmental Contamination and Toxicology, vol. 66, no. 2, pp. 189–195, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Pawlikowski, E. Szalińska, M. Wardas, and J. Dominik, “Chromium originating from tanneries in river sediments: a preliminary investigation from the upper Dunajec River (Poland),” Polish Journal of Environmental Studies, vol. 15, no. 6, pp. 885–894, 2006. View at Google Scholar · View at Scopus
  24. O. Morton-Bermea, E. Hernández-Álvarez, R. Lozano, J. Guzmán-Morales, and G. Martínez, “Spatial distribution of heavy metals in top soils around the industrial facilities of Cromatos de México, Tultitlan Mexico,” Bulletin of Environmental Contamination and Toxicology, vol. 85, no. 5, pp. 520–524, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Pedraza-Chaverrí, D. Barrera, O. N. Medina-Campos et al., “Time course study of oxidative and nitrosative stress and antioxidant enzymes in K2Cr2O7-induced nephrotoxicity,” BMC Nephrology, vol. 6, article 4, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Linos, A. Petralias, C. A. Christophi et al., “Oral ingestion of hexavalent chromium through drinking water and cancer mortality in an industrial area of Greece—an ecological study,” Environmental Health, vol. 10, no. 1, article 50, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Stift, J. Friedl, F. Längle, G. Berlakovich, R. Steininger, and F. Mühlbacher, “Successful treatment of a patient suffering from severe acute potassium dichromate poisoning with liver transplantation,” Transplantation, vol. 69, no. 11, pp. 2454–2455, 2000. View at Google Scholar · View at Scopus
  28. A. I. Rafael, A. Almeida, P. Santos et al., “A role for transforming growth factor-β apoptotic signaling pathway in liver injury induced by ingestion of water contaminated with high levels of Cr(VI),” Toxicology and Applied Pharmacology, vol. 224, no. 2, pp. 163–173, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Witmer, E. Faria, H. S. Park et al., “In vivo effects of chromium,” Environmental Health Perspectives, vol. 102, no. 3, pp. 169–176, 1994. View at Google Scholar · View at Scopus
  30. T.-C. Aw, “Clinical and epidemiological data on lung cancer at a chromate plant,” Regulatory Toxicology and Pharmacology, vol. 26, no. 1, pp. S8–S12, 1997. View at Google Scholar · View at Scopus
  31. C.-C. Lin, M.-L. Wu, C.-C. Yang, J. Ger, W.-J. Tsai, and J.-F. Deng, “Acute severe chromium poisoning after dermal exposure to hexavalent chromium,” Journal of the Chinese Medical Association, vol. 72, no. 4, pp. 219–221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Shrivastava, R. K. Upreti, P. K. Seth, and U. C. Chaturvedi, “Effects of chromium on the immune system,” FEMS Immunology and Medical Microbiology, vol. 34, no. 1, pp. 1–7, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. S. I. Nudler, F. A. Quinteros, E. A. Miler, J. P. Cabilla, S. A. Ronchetti, and B. H. Duvilanski, “Chromium VI administration induces oxidative stress in hypothalamus and anterior pituitary gland from male rats,” Toxicology Letters, vol. 185, no. 3, pp. 187–192, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. N. M. Gatto, M. A. Kelsh, D. H. Mai, M. Suh, and D. M. Proctor, “Occupational exposure to hexavalent chromium and cancers of the gastrointestinal tract: a meta-analysis,” Cancer Epidemiology, vol. 34, no. 4, pp. 388–399, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Henkler, J. Brinkmann, and A. Luch, “The role of oxidative stress in carcinogenesis induced by metals and xenobiotics,” Cancers, vol. 2, no. 2, pp. 376–396, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Ueno, T. Kashimoto, N. Susa et al., “Detection of dichromate (VI)-induced DNA strand breaks and formation of paramagnetic chromium in multiple mouse organs,” Toxicology and Applied Pharmacology, vol. 170, no. 1, pp. 56–62, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Bagchi, M. Bagchi, and S. J. Stohs, “Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene,” Molecular and Cellular Biochemistry, vol. 222, no. 1-2, pp. 149–158, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. A. K. Patlolla, C. Barnes, C. Yedjou, V. R. Velma, and P. B. Tchounwou, “Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in sprague-dawley rats,” Environmental Toxicology, vol. 24, no. 1, pp. 66–73, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Bagchi, E. A. Hassoun, M. Bagchi, D. F. Muldoon, and S. J. Stohs, “Oxidative stress induced by chronic administration of sodium dichromate [Cr(VI)] to rats,” Comparative Biochemistry and Physiology C, vol. 110, no. 3, pp. 281–287, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. K. J. Liu and X. Shi, “In vivo reduction of chromium (VI) and its related free radical generation,” Molecular and Cellular Biochemistry, vol. 222, no. 1-2, pp. 41–47, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Ueno, N. Susa, Y. Furukawa, K. Aikawa, and I. Itagaki, “Cellular injury and lipid peroxidation induced by hexavalent chromium in isolated rat hepatocytes,” Nippon Juigaku Zasshi, vol. 51, no. 1, pp. 137–145, 1989. View at Google Scholar · View at Scopus
  42. N. Soudani, I. Ben Amara, M. Sefi, T. Boudawara, and N. Zeghal, “Effects of selenium on chromium (VI)-induced hepatotoxicity in adult rats,” Experimental and Toxicologic Pathology, vol. 63, no. 6, pp. 541–548, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Woźniak, Z. Borzecki, and Z. Swies, “Histopathologic and histochemical examination of rat liver after prolonged experimental application of potassium bichromate,” Annales Universitatis Mariae Curie-Sklodowska. Sectio D, vol. 46, pp. 65–68, 1991. View at Google Scholar · View at Scopus
  44. S. Acharya, K. Mehta, S. Krishnan, and C. V. Rao, “A subtoxic interactive toxicity study of ethanol and chromium in male Wistar rats,” Alcohol, vol. 23, no. 2, pp. 99–108, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Pourahmad, A. Mihajlovic, and P. J. O'Brien, “Hepatocyte lysis induced by environmental metal toxins may involve apoptotic death signals initiated by mitochondrial injury,” Advances in Experimental Medicine and Biology, vol. 500, pp. 249–252, 2001. View at Google Scholar · View at Scopus
  46. D. Ryberg and J. Alexander, “Inhibitory action of hexavalent chromium (Cr(VI)) on the mitochondrial respiration and a possible coupling to the reduction of Cr(VI),” Biochemical Pharmacology, vol. 33, no. 15, pp. 2461–2466, 1984. View at Publisher · View at Google Scholar · View at Scopus
  47. M. A. S. Fernandes, M. S. Santos, M. C. Alpoim, V. M. C. Madeira, and J. A. F. Vicente, “Chromium(VI) interaction with plant and animal mitochondrial bioenergetics: a comparative study,” Journal of Biochemical and Molecular Toxicology, vol. 16, no. 2, pp. 53–63, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. D. Chorvatovicova, Z. Kovacikova, J. Sandula, and J. Navarova, “Protective effect of sulfoethylglucan against hexavalent chromium,” Mutation Research, vol. 302, no. 4, pp. 207–211, 1993. View at Publisher · View at Google Scholar · View at Scopus
  49. N. Susa, S. Ueno, Y. Furukawa, J. Ueda, and M. Sugiyama, “Potent protective effect of melatonin on chromium(VI)-induced DNA single-strand breaks, cytotoxicity, and lipid peroxidation in primary cultures of rat hepatocytes,” Toxicology and Applied Pharmacology, vol. 144, no. 2, pp. 377–384, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Molina-Jijón, E. Tapia, C. Zazueta et al., “Curcumin prevents Cr(VI)-induced renal oxidant damage by a mitochondrial pathway,” Free Radical Biology and Medicine, vol. 51, no. 8, pp. 1543–1557, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. A. K. Chandra, A. Chatterjee, R. Ghosh, and M. Sarkar, “Effect of curcumin on chromium-induced oxidative damage in male reproductive system,” Environmental Toxicology and Pharmacology, vol. 24, no. 2, pp. 160–166, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Kim and K. J. Na, “Nephrotoxicity of sodium dichromate depending on the route of administration,” Archives of Toxicology, vol. 65, no. 7, pp. 537–541, 1991. View at Google Scholar · View at Scopus
  53. E. Coballase-Urrutia, J. Pedraza-Chaverri, N. Cárdenas-Rodríguez et al., “Hepatoprotective effect of acetonic and methanolic extracts of Heterotheca inuloides against CCl4-induced toxicity in rats,” Experimental and Toxicologic Pathology, vol. 63, no. 4, pp. 363–370, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. O. H. Lowry, N. J. Rosebrough, A. L. Farr, and R. J. Randall, “Protein measurement with the Folin phenol reagent,” The Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951. View at Google Scholar · View at Scopus
  55. Y. I. Chirino, D. J. Sánchez-González, C. M. Martínez-Martínez, C. Cruz, and J. Pedraza-Chaverri, “Protective effects of apocynin against cisplatin-induced oxidative stress and nephrotoxicity,” Toxicology, vol. 245, no. 1-2, pp. 18–23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. P. D. Maldonado, D. Barrera, I. Rivero et al., “Antioxidant S-allylcysteine prevents gentamicin-induced oxidative stress and renal damage,” Free Radical Biology and Medicine, vol. 35, no. 3, pp. 317–324, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Chirino, Y. Sánchez-Pérez, A. Osornio-Vargas et al. et al., “PM(10) impairs the antioxidant defense system and exacerbates oxidative stress driven cell death,” Toxicology Letters, vol. 193, pp. 209–216, 2010. View at Google Scholar
  58. D. Barrera, P. D. Maldonado, O. N. Medina-Campos, R. Hernández-Pando, M. E. Ibarra-Rubio, and J. Pedraza-Chaverrí, “Protective effect of SnCl2 on K2Cr2O7-induced nephrotoxicity in rats: the indispensability of HO-1 preinduction and lack of association with some antioxidant enzymes,” Life Sciences, vol. 73, no. 23, pp. 3027–3041, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Pedraza-Chaverrí, P. D. Maldonado, O. N. Medina-Campos et al., “Garlic ameliorates gentamicin nephrotoxicity: relation to antioxidant enzymes,” Free Radical Biology and Medicine, vol. 29, no. 7, pp. 602–611, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Orozco-Ibarra, O. Medina-Campos, D. Sánchez-González et al. et al., “Evaluation of oxidative stress in D-serine induced nephrotoxicity,” Toxicology, vol. 229, pp. 123–135, 2007. View at Google Scholar
  61. J. Pedraza-Chaverrí, A. E. González-Orozco, P. D. Maldonado, D. Barrera, O. N. Medina-Campos, and R. Hernández-Pando, “Diallyl disulfide ameliorates gentamicin-induced oxidative stress and nephropathy in rats,” European Journal of Pharmacology, vol. 473, no. 1, pp. 71–78, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Pedraza-Chaverri, P. Yam-Canul, Y. I. Chirino et al., “Protective effects of garlic powder against potassium dichromate-induced oxidative stress and nephrotoxicity,” Food and Chemical Toxicology, vol. 46, no. 2, pp. 619–627, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. E. Tapia, V. Soto, K. M. Ortiz-Vega et al., “Curcumin induces Nrf2 nuclear translocation and prevents glomerular hypertension, hyperfiltration, oxidant stress, and the decrease in antioxidant enzymes in 5/6 nephrectomized rats,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 269039, 14 pages, 2012. View at Publisher · View at Google Scholar
  64. F. Correa, N. García, C. Robles, E. Martínez-Abundis, and C. Zazueta, “Relationship between oxidative stress and mitochondrial function in the post-conditioned heart,” Journal of Bioenergetics and Biomembranes, vol. 40, no. 6, pp. 599–606, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Zúñiga-Toalá, E. Tapia, C. Zazueta et al. et al., “Nordihydroguaiaretic acid pretreatment prevents ischemia and reperfusion induced renal injury, oxidant stress and mitochondrial alterations,” Journal of Medicinal Plants Research, vol. 6, pp. 2938–2947, 2012. View at Google Scholar
  66. F. Correa, V. Soto, and C. Zazueta, “Mitochondrial permeability transition relevance for apoptotic triggering in the post-ischemic heart,” International Journal of Biochemistry and Cell Biology, vol. 39, no. 4, pp. 787–798, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. N. García, C. Zazueta, R. Carrillo, F. Correa, and E. Chávez, “Copper sensitizes the mitochondrial permeability transition to carboxytractyloside and oleate,” Molecular and Cellular Biochemistry, vol. 209, no. 1-2, pp. 119–123, 2000. View at Google Scholar · View at Scopus
  68. C. Zazueta, N. García, E. Martínez-Abundis, N. Pavón, L. Hernández-Esquivel, and E. Chávez, “Reduced capacity of Ca2+ retention in liver as compared to kidney mitochondria. ADP requirement,” Journal of Bioenergetics and Biomembranes, vol. 42, no. 5, pp. 381–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. C. Zazueta, M. Franco, F. Correa et al., “Hypothyroidism provides resistance to kidney mitochondria against the injury induced by renal ischemia-reperfusion,” Life Sciences, vol. 80, no. 14, pp. 1252–1258, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Kumar and S. Roy, “Effect of chromium on certain aspects of cellular toxicity,” Iranian Journal of Toxicology, vol. 2, pp. 260–267, 2009. View at Google Scholar
  71. D. E. Amacher, “Serum transaminase elevations as indicators of hepatic injury following the administration of drugs,” Regulatory Toxicology and Pharmacology, vol. 27, no. 2, pp. 119–130, 1998. View at Publisher · View at Google Scholar · View at Scopus
  72. Z. Hassan, M. Elobeid, P. Virk et al., “Bisphenol A induces hepatotoxicity through oxidative stress in rat model,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 194829, 6 pages, 2012. View at Publisher · View at Google Scholar
  73. S. Kalayarasan, N. Sriram, A. Sureshkumar, and G. Sudhandiran, “Chromium (VI)-induced oxidative stress and apoptosis is reduced by garlic and its derivative S-allylcysteine through the activation of Nrf2 in the hepatocytes of Wistar rats,” Journal of Applied Toxicology, vol. 28, no. 7, pp. 908–919, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. A. C. P. Reddy and B. R. Lokesh, “Effect of curcumin and eugenol on iron-induced hepatic toxicity in rats,” Toxicology, vol. 107, no. 1, pp. 39–45, 1996. View at Publisher · View at Google Scholar · View at Scopus
  75. M.-E. Wang, Y.-C. Chen, I.-S. Chen, S.-C. Hsieh, S.-S. Chen, and C.-H. Chiu, “Curcumin protects against thioacetamide-induced hepatic fibrosis by attenuating the inflammatory response and inducing apoptosis of damaged hepatocytes,” Journal of Nutritional Biochemistry, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Han, N. Hanawa, B. Saberi, and N. Kaplowitz, “Mechanisms of liver injury. III. Role of glutathione redox status in liver injury,” American Journal of Physiology, vol. 291, no. 1, pp. G1–G7, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. E. Kheradpezhouh, M.-R. Panjehshahin, R. Miri et al., “Curcumin protects rats against acetaminophen-induced hepatorenal damages and shows synergistic activity with N-acetyl cysteine,” European Journal of Pharmacology, vol. 628, no. 1–3, pp. 274–281, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. P. Sankar, A. G. Telang, and A. Manimaran, “Protective effect of curcumin on cypermethrin-induced oxidative stress in Wistar rats,” Experimental and Toxicologic Pathology, vol. 64, no. 5, pp. 487–493, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Von Burg and D. Liu, “Chromium and hexavalent chromium,” Journal of Applied Toxicology, vol. 13, no. 3, pp. 225–230, 1993. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Costa, “Toxicity and carcinogenicity of Cr(VI) in animal models and humans,” Critical Reviews in Toxicology, vol. 27, no. 5, pp. 431–442, 1997. View at Google Scholar · View at Scopus
  81. S. S. Anand, “Protective effect of vitamin B6 in chromium-induced oxidative stress in liver,” Journal of Applied Toxicology, vol. 25, no. 5, pp. 440–443, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. M. V. Rao, S. S. Parekh, and S. L. Chawla, “Vitamin-E supplementation ameliorates chromium-and/or nickel induced oxidative stress in vivo,” Journal of Health Science, vol. 52, no. 2, pp. 142–147, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. D. Chorvatovicova, E. Ginter, A. Kosinova, and Z. Zloch, “Effect of vitamins C and E on toxicity and mutagenicity of hexavalent chromium in rat and guinea pig,” Mutation Research, vol. 262, no. 1, pp. 41–46, 1991. View at Google Scholar · View at Scopus
  84. N. Susa, S. Ueno, and Y. Furukawa, “Protective effects of thiol compounds on chromate-induced toxicity in vitro and in vivo,” Environmental Health Perspectives, vol. 102, no. 3, pp. 247–250, 1994. View at Google Scholar · View at Scopus
  85. I. I. Boşgelmez, T. Söylemezoǧlu, and G. Güvendik, “The protective and antidotal effects of taurine on hexavalent chromium-induced oxidative stress in mice liver tissue,” Biological Trace Element Research, vol. 125, no. 1, pp. 46–58, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. Q.-Y. Wei, W.-F. Chen, B. Zhou, L. Yang, and Z.-L. Liu, “Inhibition of lipid peroxidation and protein oxidation in rat liver mitochondria by curcumin and its analogues,” Biochimica et Biophysica Acta, vol. 1760, no. 1, pp. 70–77, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Alp, I. Aytekin, N. Hatipoglu, A. Alp, and M. Ogun, “Effects of sulforophane and curcumin on oxidative stress created by acute malathion toxicity in rats,” European Review For Medical and Pharmacological Sciences, vol. 16, pp. 144–148, 2012. View at Google Scholar
  88. M. Tokaç, G. Taner, S. Aydın et al. et al., “Protective effects of curcumin against oxidative stress parameters and DNA damage in the livers and kidneys of rats with biliary obstruction,” Food and Chemical Toxicology, vol. 6915, pp. 53–57, 2013. View at Google Scholar
  89. A. A. M. Adly, “Oxidative stress and disease: an updated review,” Research Journal of Immunology, vol. 3, no. 2, pp. 129–145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. I. Dalle-Donne, R. Rossi, D. Giustarini, A. Milzani, and R. Colombo, “Protein carbonyl groups as biomarkers of oxidative stress,” Clinica Chimica Acta, vol. 329, no. 1-2, pp. 23–38, 2003. View at Publisher · View at Google Scholar · View at Scopus
  91. T. Ak and I. Gülçin, “Antioxidant and radical scavenging properties of curcumin,” Chemico-Biological Interactions, vol. 174, no. 1, pp. 27–37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. A. T. Dinkova-Kostova and P. Talalay, “Direct and indirect antioxidant properties of inducers of cytoprotective proteins,” Molecular Nutrition and Food Research, vol. 52, no. 1, pp. S128–S138, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. V. I. Lushchak, “Glutathione homeostasis and functions: potential targets for medical interventions,” Journal of Amino Acids, vol. 2012, Article ID 736837, 26 pages, 2012. View at Publisher · View at Google Scholar
  94. L. L. P. Gutierrez, N. C. Mazzotti, A. S. R. Araújo et al., “Peripheral markers of oxidative stress in chronic mercuric chloride intoxication,” Brazilian Journal of Medical and Biological Research, vol. 39, no. 6, pp. 767–772, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Whillier, P. Kuchel, and J. Raftos, “Oxidative stress in type II diabetes mellitus and the role of the endogenous antioxidant glutathione,” in Role of the Adipocyte in Development of Type 2 Diabetes, C. Croniger, Ed., pp. 129–252, InTech Europe, Croatia, 2011. View at Google Scholar
  96. D. S. El-Agamy, “Comparative effects of curcumin and resveratrol on aflatoxin B 1-induced liver injury in rats,” Archives of Toxicology, vol. 84, no. 5, pp. 389–396, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Matés, C. Pérez-Gómez, and I. N. de Castro, “Antioxidant enzymes and human diseases,” Clinical Biochemistry, vol. 32, pp. 595–603, 1999. View at Google Scholar
  98. A. C. Elia, A. J. M. Dörr, C. Mastrangelo, M. Prearo, and M. C. Abete, “Glutathione and antioxidant enzymes in the hepatopancreas of crayfish Procambarus clarkii (Girard, 1852) of Lake Trasimeno (Italy),” Bulletin Francais de la Peche et de la Protection des Milieux Aquatiques, no. 380-381, pp. 1351–1361, 2006. View at Google Scholar · View at Scopus
  99. F. M. El-Demerdash, M. I. Yousef, and F. M. E. Radwan, “Ameliorating effect of curcumin on sodium arsenite-induced oxidative damage and lipid peroxidation in different rat organs,” Food and Chemical Toxicology, vol. 47, no. 1, pp. 249–254, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. X. Guangwei, L. Rongzhu, X. Wenrong et al., “Curcumin pretreatment protects against acute acrylonitrile-induced oxidative damage in rats,” Toxicology, vol. 267, no. 1–3, pp. 140–146, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. S. Al-Jassabi, M. Azirun, and A. Saad, “Biochemical studies on the role of curcumin in the potection of liver and kidney damage by anti-malaria drug, chloroquine,” American-Eurasian Journal of Toxicological Sciences, vol. 3, pp. 17–22, 2011. View at Google Scholar
  102. V. Mathews, P. Binu, M. Sauganth-Paul, M. Abhilash, A. Manju, and R. Nair, “Hepatoprotective efficacy of curcumin against arsenic trioxide toxicity,” Asian Pacific Journal of Tropical Biomedicine, vol. 2, pp. S706–S711, 2012. View at Google Scholar
  103. Y. Wei, R. S. Rector, J. P. Thyfault, and J. A. Ibdah, “Nonalcoholic fatty liver disease and mitochondrial dysfunction,” World Journal of Gastroenterology, vol. 14, no. 2, pp. 193–199, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Königsberg, N. E. López-Díazguerrero, L. Bucio, and M. C. Gutiérrez-Ruiz, “Uncoupling effect of mercuric chloride on mitochondria isolated from an hepatic cell line,” Journal of Applied Toxicology, vol. 21, no. 4, pp. 323–329, 2001. View at Publisher · View at Google Scholar · View at Scopus
  105. G. T. Vatassery, E. G. DeMaster, J. C. K. Lai, W. E. Smith, and H. T. Quach, “Iron uncouples oxidative phosphorylation in brain mitochondria isolated from vitamin E-deficient rats,” Biochimica et Biophysica Acta, vol. 1688, no. 3, pp. 265–273, 2004. View at Publisher · View at Google Scholar · View at Scopus
  106. G. L. P. Andreu, N. M. Inada, A. E. Vercesi, and C. Curti, “Uncoupling and oxidative stress in liver mitochondria isolated from rats with acute iron overload,” Archives of Toxicology, vol. 83, no. 1, pp. 47–53, 2009. View at Publisher · View at Google Scholar · View at Scopus
  107. D. N. Roy, S. Mandal, G. Sen, and T. Biswas, “Superoxide anion mediated mitochondrial dysfunction leads to hepatocyte apoptosis preferentially in the periportal region during copper toxicity in rats,” Chemico-Biological Interactions, vol. 182, no. 2-3, pp. 136–147, 2009. View at Publisher · View at Google Scholar · View at Scopus
  108. A. Navarro and A. Boveris, “Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging,” American Journal of Physiology, vol. 287, no. 5, pp. R1244–R1249, 2004. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Jurczuk, J. Moniuszko-Jakoniuk, and J. Rogalska, “Evaluation of oxidative stress in hepatic mitochondria of rats exposed to cadmium and ethanol,” Polish Journal of Environmental Studies, vol. 15, no. 6, pp. 853–860, 2006. View at Google Scholar · View at Scopus
  110. R. Jasso-Chávez, A. Pacheco-Rosales, E. Lira-Silva, J. C. Gallardo-Pérez, N. García, and R. Moreno-Sánchez, “Toxic effects of Cr(VI) and Cr(III) on energy metabolism of heterotrophic Euglena gracilis,” Aquatic Toxicology, vol. 100, no. 4, pp. 329–338, 2010. View at Google Scholar · View at Scopus
  111. K. Rembacz, E. Sawicka, and A. Długosz, “Role of estradiol in chromium-induced oxidative stress,” Acta Poloniae Pharmaceutica, vol. 69, pp. 1372–1379, 2012. View at Google Scholar
  112. K. I. Priyadarsini, D. K. Maity, G. H. Naik et al., “Role of phenolic O–H and methylene hydrogen on the free radical reactions and antioxidant activity of curcumin,” Free Radical Biology and Medicine, vol. 35, no. 5, pp. 475–484, 2003. View at Publisher · View at Google Scholar · View at Scopus
  113. Y.-G. Zhu, X.-C. Chen, Z.-Z. Chen et al., “Curcumin protects mitochondria from oxidative damage and attenuates apoptosis in cortical neurons,” Acta Pharmacologica Sinica, vol. 25, no. 12, pp. 1606–1612, 2004. View at Google Scholar · View at Scopus
  114. A. González-Salazar, E. Molina-Jijón, F. Correa et al., “Curcumin protects from cardiac reperfusion damage by attenuation of oxidant stress and mitochondrial dysfunction,” Cardiovascular Toxicology, vol. 11, no. 4, pp. 357–364, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. H. He, G. Wang, Y. Gao, W. Ling, Z. Yu, and T. Jin, “Curcumin attenuates Nrf2 signaling defect, oxidative stress in muscle and glucose intolerance in high fat diet-fed mice,” World Journal of Diabetes, vol. 3, pp. 94–104, 2012. View at Google Scholar
  116. M. Waseem, P. Kaushik, and S. Parvez, “Mitochondria-mediated mitigatory role of curcumin in cisplatin-induced nephrotoxicity,” Cell Biochemistry and Function, 2013. View at Publisher · View at Google Scholar
  117. V. Calabrese, R. Lodi, C. Tonon et al., “Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia,” Journal of the Neurological Sciences, vol. 233, no. 1-2, pp. 145–162, 2005. View at Publisher · View at Google Scholar · View at Scopus
  118. M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature, vol. 443, no. 7113, pp. 787–795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. C. P. M. S. Oliveira, A. M. M. Coelho, H. V. Barbeiro et al., “Liver mitochondrial dysfunction and oxidative stess in the pathogenesis of experimental nonalcoholic fatty liver disease,” Brazilian Journal of Medical and Biological Research, vol. 39, no. 2, pp. 189–194, 2006. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Raza, A. John, E. M. Brown, S. Benedict, and A. Kambal, “Alterations in mitochondrial respiratory functions, redox metabolism and apoptosis by oxidant 4-hydroxynonenal and antioxidants curcumin and melatonin in PC12 cells,” Toxicology and Applied Pharmacology, vol. 226, no. 2, pp. 161–168, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. N. Sivalingam, J. Basivireddy, K. A. Balasubramanian, and M. Jacob, “Curcumin attenuates indomethacin-induced oxidative stress and mitochondrial dysfunction,” Archives of Toxicology, vol. 82, no. 7, pp. 471–481, 2008. View at Publisher · View at Google Scholar · View at Scopus
  122. K. Sas, H. Robotka, J. Toldi, and L. Vécsei, “Mitochondria, metabolic disturbances, oxidative stress and the kynurenine system, with focus on neurodegenerative disorders,” Journal of the Neurological Sciences, vol. 257, no. 1-2, pp. 221–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. R. G. Efremov, R. Baradaran, and L. A. Sazanov, “The architecture of respiratory complex I,” Nature, vol. 465, no. 7297, pp. 441–445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. D. Gonzalez-Halphen, A. Ghelli, L. Iommarini, V. Carelli, and M. D. Esposti, “Mitochondrial complex I and cell death: a semi-automatic shotgun model,” Cell Death and Disease, vol. 2, no. 10, article e222, 2011. View at Publisher · View at Google Scholar · View at Scopus
  125. R. B. Mythri, G. Harish, S. K. Dubey, K. Misra, and M. M. Srinivas Bharath, “Glutamoyl diester of the dietary polyphenol curcumin offers improved protection against peroxynitrite-mediated nitrosative stress and damage of brain mitochondria in vitro: implications for Parkinson's disease,” Molecular and Cellular Biochemistry, vol. 347, no. 1-2, pp. 135–143, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. M. Izem-Meziane, B. Djerdjouri, S. Rimbaud et al., “Catecholamine-induced cardiac mitochondrial dysfunction and mPTP opening: protective effect of curcumin,” American Journal of Physiology, vol. 302, no. 3, pp. H665–H674, 2012. View at Publisher · View at Google Scholar · View at Scopus
  127. G. Feldmann, D. Haouzi, A. Moreau et al., “Opening of the mitochondrial permeability transition pore causes matrix expansion and outer membrane rupture in Fas-mediated hepatic apoptosis in mice,” Hepatology, vol. 31, no. 3, pp. 674–683, 2000. View at Google Scholar · View at Scopus
  128. S. Javadov and M. Karmazyn, “Mitochondrial permeability transition pore opening as an endpoint to initiate cell death and as a putative target for cardioprotection,” Cellular Physiology and Biochemistry, vol. 20, no. 1–4, pp. 1–22, 2007. View at Publisher · View at Google Scholar · View at Scopus
  129. A. P. Halestrap, G. P. McStay, and S. J. Clarke, “The permeability transition pore complex: another view,” Biochimie, vol. 84, no. 2-3, pp. 153–166, 2002. View at Publisher · View at Google Scholar · View at Scopus
  130. J.-W. Xiao, C.-G. Zhong, and B. Li, “Study of L-02 hepatocyte apoptosis induced by hexavalent chromium associated with mitochondria function damage,” Wei Sheng Yan Jiu, vol. 35, no. 4, pp. 416–418, 2006. View at Google Scholar · View at Scopus
  131. D. E. Pritchard, J. Singh, D. L. Carlisle, and S. R. Patierno, “Cyclosporin A inhibits chromium(VI)-induced apoptosis and mitochondrial cytochrome c release and restores clonogenic survival in CHO cells,” Carcinogenesis, vol. 21, no. 11, pp. 2027–2033, 2000. View at Google Scholar · View at Scopus
  132. A. I. Ghoneim, “Effects of curcumin on ethanol-induced hepatocyte necrosis and apoptosis: implication of lipid peroxidation and cytochrome c,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 379, no. 1, pp. 47–60, 2009. View at Publisher · View at Google Scholar · View at Scopus
  133. G. Eckert, C. Schiborr, S. Hagl et al., “Curcumin prevents mitochondrial dysfunction in the brain of the senescence-accelerated mouse-prone 8,” Neurochemistry International, vol. 62, pp. 595–602, 2013. View at Google Scholar
  134. H. Ligeret, S. Barthelemy, R. Zini, J.-P. Tillement, S. Labidalle, and D. Morin, “Effects of curcumin and curcumin derivatives on mitochondrial permeability transition pore,” Free Radical Biology and Medicine, vol. 36, no. 7, pp. 919–929, 2004. View at Publisher · View at Google Scholar · View at Scopus
  135. C.-Y. Cheng, Y.-H. Lin, and C.-C. Su, “Curcumin inhibits the proliferation of human hepatocellular carcinoma J5 cells by inducing endoplasmic reticulum stress and mitochondrial dysfunction,” International Journal of Molecular Medicine, vol. 26, no. 5, pp. 673–678, 2010. View at Publisher · View at Google Scholar · View at Scopus
  136. W. Wang, I. Chiang, K. Ding et al., “Curcumin-induced apoptosis in human hepatocellular carcinoma J5 cells: critical role of Ca+2-dependent pathway,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 512907, 7 pages, 2012. View at Publisher · View at Google Scholar
  137. J. Cao, Y. Liu, L. Jia et al., “Curcumin induces apoptosis through mitochondrial hyperpolarization and mtDNA damage in human hepatoma G2 cells,” Free Radical Biology and Medicine, vol. 43, no. 6, pp. 968–975, 2007. View at Publisher · View at Google Scholar · View at Scopus
  138. M. Wang, Y. Ruan, Q. Chen, S. Li, Q. Wang, and J. Cai, “Curcumin induced HepG2 cell apoptosis-associated mitochondrial membrane potential and intracellular free Ca2+ concentration,” European Journal of Pharmacology, vol. 650, no. 1, pp. 41–47, 2011. View at Publisher · View at Google Scholar · View at Scopus
  139. A. S. Darvesha, B. B. Aggarwal, and A. Bishayee, “Curcumin and liver cancer: a review,” Current Pharmaceutical Biotechnology, vol. 13, no. 1, pp. 218–228, 2012. View at Publisher · View at Google Scholar · View at Scopus