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Evidence-Based Complementary and Alternative Medicine
Volume 2015, Article ID 917435, 16 pages
http://dx.doi.org/10.1155/2015/917435
Research Article

Curcumin Attenuates Gentamicin-Induced Kidney Mitochondrial Alterations: Possible Role of a Mitochondrial Biogenesis Mechanism

1Departamento de Biología, Facultad de Química, UNAM, 04510 Ciudad de México, DF, Mexico
2Departamento de Biomedicina Cardiovascular, Instituto Nacional de Cardiología “Ignacio Chávez”, 14080 Ciudad de México, DF, Mexico
3Laboratorio de Fisiopatología Renal, Instituto Nacional de Cardiología “Ignacio Chávez”, 14080 Ciudad de México, DF, Mexico
4Unidad de Investigación en Enfermedades Oncológicas, Hospital Infantil de México “Federico Gómez”, 06720 Ciudad de México, DF, Mexico
5Departamento de Patología, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, 14000 Ciudad de México, DF, Mexico
6Departamento de Nefrología, Instituto Nacional de Cardiología “Ignacio Chávez”, 14080 Ciudad de México, DF, Mexico

Received 7 May 2015; Revised 3 July 2015; Accepted 15 July 2015

Academic Editor: Jian-Li Gao

Copyright © 2015 Mario Negrette-Guzmán 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. J. Trujillo, Y. I. Chirino, E. Molina-Jijón, A. C. Andérica-Romero, E. Tapia, and J. Pedraza-Chaverrí, “Renoprotective effect of the antioxidant curcumin: recent findings,” Redox Biology, vol. 1, no. 1, pp. 448–456, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Singh and N. Singh, “Molecular mechanism of curcumin induced cytotoxicity in human cervical carcinoma cells,” Molecular and Cellular Biochemistry, vol. 325, no. 1-2, pp. 107–119, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. J.-M. Kim, E.-M. Noh, K.-B. Kwon et al., “Curcumin suppresses the TPA-induced invasion through inhibition of PKCα-dependent MMP-expression in MCF-7 human breast cancer cells,” Phytomedicine, vol. 19, no. 12, pp. 1085–1092, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Nishikawa, J. Tsutsumi, and S. Kitani, “Anti-inflammatory and anti-oxidative effect of curcumin in connective tissue type mast cell,” Journal of Functional Foods, vol. 5, no. 2, pp. 763–772, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Z. Moghadamtousi, H. Abdul Kadir, P. Hassandarvish, H. Tajik, S. Abubakar, and K. Zandi, “A review on antibacterial, antiviral, and antifungal activity of curcumin,” BioMed Research International, vol. 2014, Article ID 186864, 12 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. S.-K. Shin, T.-Y. Ha, R. A. McGregor, and M.-S. Choi, “Long-term curcumin administration protects against atherosclerosis via hepatic regulation of lipoprotein cholesterol metabolism,” Molecular Nutrition and Food Research, vol. 55, no. 12, pp. 1829–1840, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. M. R. Smith, S. R. Gangireddy, V. R. Narala et al., “Curcumin inhibits fibrosis-related effects in IPF fibroblasts and in mice following bleomycin-induced lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 298, no. 5, pp. L616–L625, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. S. González-Reyes, S. Guzmán-Beltrán, O. N. Medina-Campos, and J. Pedraza-Chaverri, “Curcumin pretreatment induces Nrf2 and an antioxidant response and prevents hemin-induced toxicity in primary cultures of cerebellar granule neurons of rats,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 801418, 14 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. W. R. García-Niño and J. Pedraza-Chaverrí, “Protective effect of curcumin against heavy metals-induced liver damage,” Food and Chemical Toxicology, vol. 69, pp. 182–201, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Trujillo, L. F. Granados-Castro, C. Zazueta, A. C. Andérica-Romero, Y. I. Chirino, and J. Pedraza-Chaverrí, “Mitochondria as a target in the therapeutic properties of curcumin,” Archiv der Pharmazie, vol. 347, no. 12, pp. 873–884, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. 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
  12. F. Correa, M. Buelna-Chontal, S. Hernández-Reséndiz et al., “Curcumin maintains cardiac and mitochondrial function in chronic kidney disease,” Free Radical Biology and Medicine, vol. 61, pp. 119–129, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Izem-Meziane, B. Djerdjouri, S. Rimbaud et al., “Catecholamine-induced cardiac mitochondrial dysfunction and mPTP opening: protective effect of curcumin,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 302, no. 3, pp. H665–H674, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. P. H. Xu, Y. L. Yao, P. J. Guo, T. Wang, B. W. Yang, and Z. Zhang, “Curcumin protects rat heart mitochondria against anoxia-reoxygenation induced oxidative injury,” Canadian Journal of Physiology and Pharmacology, vol. 91, no. 9, pp. 715–723, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. 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
  16. W. R. García-Niño, E. Tapia, C. Zazueta et al., “Curcumin pretreatment prevents potassium dichromate-induced hepatotoxicity, oxidative stress, decreased respiratory Complex i activity, and membrane permeability transition pore opening,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 424692, 19 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. 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
  18. J.-J. Kuo, H.-H. Chang, T.-H. Tsai, and T.-Y. Lee, “Positive effect of curcumin on inflammation and mitochondrial dysfunction in obese mice with liver steatosis,” International Journal of Molecular Medicine, vol. 30, no. 3, pp. 673–679, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Liu, W. Zhang, L. Wang et al., “Curcumin prevents cerebral ischemia reperfusion injury via increase of mitochondrial biogenesis,” Neurochemical Research, vol. 39, no. 7, pp. 1322–1331, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. B. H. Ali, N. Al-Wabel, O. Mahmoud, H. M. Mousa, and M. Hashad, “Curcumin has a palliative action on gentamicin-induced nephrotoxicity in rats,” Fundamental and Clinical Pharmacology, vol. 19, no. 4, pp. 473–477, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. E. O. Farombi and M. Ekor, “Curcumin attenuates gentamicin-induced renal oxidative damage in rats,” Food and Chemical Toxicology, vol. 44, no. 9, pp. 1443–1448, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Quiros, L. Vicente-Vicente, A. I. Morales, J. M. López-Novoa, and F. J. López-Hernández, “An integrative overview on the mechanisms underlying the renal tubular cytotoxicity of gentamicin,” Toxicological Sciences, vol. 119, no. 2, pp. 245–256, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Negrette-Guzmán, S. Huerta-Yepez, O. N. Medina-Campos et al., “Sulforaphane attenuates gentamicin-induced nephrotoxicity: role of mitochondrial protection,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 135314, 17 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Servais, P. Van Der Smissen, G. Thirion et al., “Gentamicin-induced apoptosis in LLC-PK1 cells: involvement of lysosomes and mitochondria,” Toxicology and Applied Pharmacology, vol. 206, no. 3, pp. 321–333, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. A. I. Morales, D. Detaille, M. Prieto et al., “Metformin prevents experimental gentamicin-induced nephropathy by a mitochondria-dependent pathway,” Kidney International, vol. 77, no. 10, pp. 861–869, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Chen, H. S. Wong, H. Y. Leung et al., “An ursolic acid-enriched extract of Cynomorium songaricum protects against carbon tetrachloride hepatotoxicity and gentamicin nephrotoxicity in rats possibly through a mitochondrial pathway: a comparison with ursolic acid,” Journal of Functional Foods, vol. 7, no. 1, pp. 330–341, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Manikandan, M. Beulaja, R. Thiagarajan, A. Priyadarsini, R. Saravanan, and M. Arumugam, “Ameliorative effects of curcumin against renal injuries mediated by inducible nitric oxide synthase and nuclear factor kappa B during gentamicin-induced toxicity in Wistar rats,” European Journal of Pharmacology, vol. 670, no. 2-3, pp. 578–585, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Negrette-Guzmán, S. Huerta-Yepez, E. Tapia, and J. Pedraza-Chaverri, “Modulation of mitochondrial functions by the indirect antioxidant sulforaphane: a seemingly contradictory dual role and an integrative hypothesis,” Free Radical Biology and Medicine, vol. 65, pp. 1078–1089, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. R. C. Scarpulla, “Transcriptional paradigms in mammalian mitochondrial biogenesis and function,” Physiological Reviews, vol. 88, no. 2, pp. 611–638, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Servais, Y. Jossin, F. Van Bambeke, P. M. Tulkens, and M.-P. Mingeot-Leclercq, “Gentamicin causes apoptosis at low concentrations in renal LLC-PK 1 cells subjected to electroporation,” Antimicrobial Agents and Chemotherapy, vol. 50, no. 4, pp. 1213–1221, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. 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
  32. E. Martínez-Abundis, N. García, F. Correa, S. Hernández-Reséndiz, J. Pedraza-Chaverri, and C. Zazueta, “Effects of α-mangostin on mitochondrial energetic metabolism,” Mitochondrion, vol. 10, no. 2, pp. 151–157, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Balogun, M. Hoque, P. Gong et al., “Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element,” Biochemical Journal, vol. 371, no. 3, pp. 887–895, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Piantadosi, M. S. Carraway, A. Babiker, and H. B. Suliman, “Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via nrf2-mediated transcriptional control of nuclear respiratory factor-1,” Circulation Research, vol. 103, no. 11, pp. 1232–1240, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. N. C. MacGarvey, H. B. Suliman, R. R. Bartz et al., “Activation of mitochondrial biogenesis by heme oxygenase-1-mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis,” The American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 8, pp. 851–861, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Palomino and J. Pachón, “Aminoglucósidos,” Enfermedades Infecciosas y Microbiología Clínica, vol. 21, no. 2, pp. 105–115, 2003. View at Publisher · View at Google Scholar
  37. J. Feng, T. Tao, W. Yan, C. S. Chen, and X. Qin, “Curcumin inhibits mitochondrial injury and apoptosis from the early stage in EAE mice,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 728751, 10 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. A. M. Sanli, E. Turkoglu, G. Serbes et al., “Effect of curcumin on lipid peroxidation, early ultrastructural findings and neurological recovery after experimental spinal cord contusion injury in rats,” Turkish Neurosurgery, vol. 22, no. 2, pp. 189–195, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Srivastava, R. S. Yadav, L. P. Chandravanshi et al., “Unraveling the mechanism of neuroprotection of curcumin in arsenic induced cholinergic dysfunctions in rats,” Toxicology and Applied Pharmacology, vol. 279, no. 3, pp. 428–440, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Pan, H. Li, J.-F. Ma et al., “Curcumin inhibition of JNKs prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease through suppressing mitochondria dysfunction,” Translational Neurodegeneration, vol. 1, article 16, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Abdul-Hamid and N. Moustafa, “Protective effect of curcumin on histopathology and ultrastructure of pancreas in the alloxan treated rats for induction of diabetes,” The Journal of Basic & Applied Zoology, vol. 66, no. 4, pp. 169–179, 2013. View at Publisher · View at Google Scholar
  42. J.-J. Kuo, H.-H. Chang, T.-H. Tsai, and T.-Y. Lee, “Curcumin ameliorates mitochondrial dysfunction associated with inhibition of gluconeogenesis in free fatty acid-mediated hepatic lipoapoptosis,” International Journal of Molecular Medicine, vol. 30, no. 3, pp. 643–649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Gibellini, E. Bianchini, S. De Biasi, M. Nasi, A. Cossarizza, and M. Pinti, “527209,” Evidence-Based Complementary and Alternative Medicine, vol. 2015, Article ID 527209, 13 pages, 2015. View at Publisher · View at Google Scholar
  44. M. D. Brand and D. G. Nicholls, “Assessing mitochondrial dysfunction in cells,” Biochemical Journal, vol. 435, no. 2, pp. 297–312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. C. F. Simmons Jr., R. T. Bogusky, and H. D. Humes, “Inhibitory effects of gentamicin on renal mitochondrial oxidative phosphorylation,” The Journal of Pharmacology and Experimental Therapeutics, vol. 214, no. 3, pp. 709–715, 1980. View at Google Scholar · View at Scopus
  46. J. M. Weinberg and H. D. Humes, “Mechanisms of gentamicin induced dysfunction of renal cortical mitochondria. I. Effects of mitochondrial respiration,” Archives of Biochemistry and Biophysics, vol. 205, no. 1, pp. 222–231, 1980. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. Weinberg, P. G. Harding, and H. D. Humes, “Mechanisms of gentamicin-induced dysfunction of renal cortical mitochondria. II. Effects on mitochondrial monovalent cation transport,” Archives of Biochemistry and Biophysics, vol. 205, no. 1, pp. 232–239, 1980. View at Publisher · View at Google Scholar · View at Scopus
  48. 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
  49. B. D. Sahu, S. Tatireddy, M. Koneru et al., “Naringin ameliorates gentamicin-induced nephrotoxicity and associated mitochondrial dysfunction, apoptosis and inflammation in rats: possible mechanism of nephroprotection,” Toxicology and Applied Pharmacology, vol. 277, no. 1, pp. 8–20, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. L. M. Mela-Riker, L. L. Widener, D. C. Houghton, and W. M. Bennett, “Renal mitochondrial integrity during continuous gentamicin treatment,” Biochemical Pharmacology, vol. 35, no. 6, pp. 979–984, 1986. View at Publisher · View at Google Scholar · View at Scopus
  51. C.-L. Yang, X.-H. Du, and Y.-X. Han, “Renal cortical mitochondria are the source of oxygen free radicals enhanced by gentamicin,” Renal Failure, vol. 17, no. 1, pp. 21–26, 1995. View at Publisher · View at Google Scholar · View at Scopus
  52. C. E. Guerrero-Beltrán, M. Calderón-Oliver, E. Martínez-Abundis et al., “Protective effect of sulforaphane against cisplatin-induced mitochondrial alterations and impairment in the activity of NAD(P)H: quinone oxidoreductase 1 and γ glutamyl cysteine ligase: studies in mitochondria isolated from rat kidney and in LLC-PK1 cells,” Toxicology Letters, vol. 199, no. 1, pp. 80–92, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. 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
  54. M. Crompton, “The mitochondrial permeability transition pore and its role in cell death,” The Biochemical Journal, vol. 341, part 2, pp. 233–249, 1999. View at Google Scholar · View at Scopus
  55. S. Orrenius, “Reactive oxygen species in mitochondria-mediated cell death,” Drug Metabolism Reviews, vol. 39, no. 2-3, pp. 443–455, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Rasola and P. Bernardi, “Mitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis,” Cell Calcium, vol. 50, no. 3, pp. 222–233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. N. Dehne, U. Rauen, H. De Groot, and J. Lautermann, “Involvement of the mitochondrial permeability transition in gentamicin ototoxicity,” Hearing Research, vol. 169, no. 1-2, pp. 47–55, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Muthuraman, S. K. Singla, A. Rana, A. Singh, and S. Sood, “Reno-protective role of flunarizine (mitochondrial permeability transition pore inactivator) against gentamicin induced nephrotoxicity in rats,” Journal of the Pharmaceutical Society of Japan, vol. 131, no. 3, pp. 437–443, 2011. View at Google Scholar · View at Scopus