Table of Contents Author Guidelines Submit a Manuscript
Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 801726, 11 pages
http://dx.doi.org/10.1155/2010/801726
Research Article

Diclofenac-Induced Apoptosis in the Neuroblastoma Cell Line SH-SY5Y: Possible Involvement of the Mitochondrial Superoxide Dismutase

1Dipartimento di Biochimica e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Via S. Pansini 5, 80131 Napoli, Italy
2Dipartimento di Studi delle Istituzioni e dei Sistemi Territoriali, Università degli Studi di Napoli “Parthenope”, Via Medina 40, 80133 Napoli, Italy

Received 8 January 2010; Revised 18 March 2010; Accepted 10 April 2010

Academic Editor: George Perry

Copyright © 2010 Francesca Cecere 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. M. Valko, D. Leibfritz, J. Moncol, M. T. D. Cronin, M. Mazur, and J. Telser, “Free radicals and antioxidants in normal physiological functions and human disease,” International Journal of Biochemistry & Cell Biology, vol. 39, no. 1, pp. 44–84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. M. J. Gomez-Lechon, E. O'Connor, J. V. Castel, and R. Jover, “Sensitive markers used to identify compounds that trigger apoptosis in cultured hepatocytes,” Toxicological Sciences, vol. 65, no. 2, pp. 299–308, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. M. J. Gomez-Lechon, X. Ponsoda, E. O'Connor, T. Donato, R. Jover, and J. V. Castell, “Diclofenac induces apoptosis in hepatocytes,” Toxicology in Vitro, vol. 17, no. 5-6, pp. 675–680, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Tsutsumi, T. Gotoh, W. Tomisato et al., “Endoplasmic reticulum stress response is involved in nonsteroidal anti-inflammatory drug-induced apoptosis,” Cell Death and Differentiation, vol. 11, no. 9, pp. 1009–1016, 2004. View at Google Scholar
  5. M. J. Thun, S. J. Henley, and C. Patrono, “Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues,” Journal of the National Cancer Institute, vol. 94, no. 4, pp. 252–266, 2002. View at Google Scholar · View at Scopus
  6. X. C. Xu, “COX-2 inhibitors in cancer treatment and prevention, a recent development,” Anti-Cancer Drugs, vol. 13, no. 2, pp. 127–137, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Lindskog, H. Gleissman, F. Ponthan, J. Castro, P. Kogner, and J. I. Johnsen, “Neuroblastoma cell death in response to docosahexaenoic acid: sensitization to chemotherapy and arsenic-induced oxidative stress,” International Journal of Cancer, vol. 118, no. 10, pp. 2584–2593, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Kudo, M. Kori, K. Matsuzaki et al., “Diclofenac inhibits proliferation and differentiation of neural stem cells,” Biochemical Pharmacology, vol. 66, no. 2, pp. 289–295, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. E. J. Hickey, R. R. Raje, V. E. Reid, S. M. Gross, and S. D. Ray, “Diclofenac induced in vivo nephrotoxicity may involve oxidative stress-mediated massive genomic DNA fragmentation and apoptotic cell death,” Free Radical Biology & Medicine, vol. 31, no. 2, pp. 139–152, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Kusuhara, H. Komatsu, H. Sumichika, and K. Sugahara, “Reactive oxygen species are involved in the apoptosis induced by nonsteroidal anti-inflammatory drugs in cultured gastric cells,” European Journal of Pharmacology, vol. 383, no. 3, pp. 331–337, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. M. J. Gomez-Lechon, X. Ponsoda, E. O'Connor, T. Donato, J. V. Castell, and R. Jover, “Diclofenac induces apoptosis in hepatocytes by alteration of mitochondrial function and generation of ROS,” Biochemical Pharmacology, vol. 66, no. 11, pp. 2155–2167, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Li, M. M. Wright, and R. M. Jackson, “Reactive species mediated injury of human lung epithelial cells after hypoxia-reoxygenation,” Experimental Lung Research, vol. 28, no. 5, pp. 373–389, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Pani, B. Bedogni, R. Anzevino et al., “Deregulated manganese superoxide dismutase expression and resistance to oxidative injury in p53-deficient cells,” Cancer Research, vol. 60, no. 16, pp. 4654–4660, 2000. View at Google Scholar · View at Scopus
  14. H. Tanaka, I. Matsumura, S. Ezoe et al., “E2F1 and c-Myc potentiate apoptosis through inhibition of NF-?B activity that facilitates MnSOD-mediated ROS elimination,” Molecular Cell, vol. 9, no. 5, pp. 1017–1029, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. J. E. Kokoszka, P. Coskun, L. A. Esposito, and D. C. Wallace, “Increased mitochondrial oxidative stress in the Sod2 (+/) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 5, pp. 2278–2283, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. S. K. Manna, H. J. Zhang, T. Yan, L. W. Oberley, and B. B. Aggarwal, “Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-κB and activated protein-1,” Journal of Biological Chemistry, vol. 273, no. 21, pp. 13245–13254, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. M. W. Epperly, C. A. Sikora, S. J. DeFilippi et al., “Manganese superoxide dismutase (SOD2) inhibits radiation-induced apoptosis by stabilization of the mitochondrial membrane,” Radiation Research, vol. 157, no. 5, pp. 568–577, 2002. View at Google Scholar · View at Scopus
  18. M. W. Epperly, M. Bernarding, J. Gretton, M. Jefferson, S. Nie, and J. S. Greenberger, “Overexpression of the transgene for manganese superoxide dismutase (MnSOD) in 32D cl 3 cells prevents apoptosis induction by TNF-α, IL-3 withdrawal, and ionizing radiation,” Experimental Hematology, vol. 31, no. 6, pp. 465–474, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Sato, T. Machida, S. Takahashi et al., “Fas-mediated apoptosome formation is dependent on reactive oxygen species derived from mitochondrial permeability transition in Jurkat cells,” Journal of Immunology, vol. 173, no. 1, pp. 285–296, 2004. View at Google Scholar · View at Scopus
  20. M. Pardo, J. A. Melendez, and O. Tirosh, “Manganese superoxide dismutase inactivation during Fas (CD95)-mediated apoptosis in Jurkat T cells,” Free Radical Biology & Medicine, vol. 41, no. 12, pp. 1795–1806, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Grimaldi, M. R. Ruocco, M. A. Lanzotti et al., “Characterisation of the components of the thioredoxin system in the archaeon Sulfolobus solfataricus,” Extremophiles, vol. 12, no. 4, pp. 553–562, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. X. Ponsoda, R. Jover, J. V. Castell, and M. J. Gomez-Lechon, “Measurement of intracellular LDH activity in 96-well cultures: a rapid and automated assay for cytotoxicity studies,” Journal of Tissue Culture Methods, vol. 13, no. 1, pp. 21–24, 1991. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Nicoletti, G. Migliorati, M. C. Pagliacci, F. Grignani, and C. Riccardi, “A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry,” Journal of Immunological Methods, vol. 139, no. 2, pp. 271–279, 1991. View at Publisher · View at Google Scholar · View at Scopus
  24. 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 Google Scholar · View at Scopus
  25. C. Beauchamp and I. Fridovich, “Superoxide dismutase: improved assays and an assay applicable to acrylamide gels,” Analytical Biochemistry, vol. 44, no. 1, pp. 276–287, 1971. View at Google Scholar · View at Scopus
  26. N. Wakasugi, Y. Tagaya, H. Wakasugi et al., “Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic virus type I- and Epstein-Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 21, pp. 8282–8286, 1990. View at Google Scholar · View at Scopus
  27. A. Rosen, P. Lundman, M. Carlsson et al., “A CD4+ T cell line-secreted factor, growth promoting for normal and leukemic B cells, identified as thioredoxin,” International Immunology, vol. 7, no. 4, pp. 625–633, 1995. View at Google Scholar · View at Scopus
  28. K. Pekkari, J. Avila-Cariño, A. Bengtsson, R. Gurunath, A. Scheynius, and A. Holmgren, “Truncated thioredoxin. (Trx80) induces production of interleukin-12 and enhances CD14 expression in human monocytes,” Blood, vol. 97, no. 10, pp. 3184–3190, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Spector, G. Z. Yan, R. R. C. Huang, M. J. McDermott, P. R. C. Gascoyne, and V. Pigiet, “The effect of H2O2 upon thioredoxin-enriched lens epithelial cells,” Journal of Biological Chemistry, vol. 263, no. 10, pp. 4984–4990, 1988. View at Google Scholar · View at Scopus
  30. M. R. Fernando, H. Nanri, S. Yoshitake, K. Nagata-Kuno, and S. Minakami, “Thioredoxin regenerates proteins inactivated by oxidative stress in endothelial cells,” European Journal of Biochemistry, vol. 209, no. 3, pp. 917–922, 1992. View at Publisher · View at Google Scholar · View at Scopus
  31. K. C. Das, Y. Lewis-Molock, and C. W. White, “Elevation of manganese superoxide dismutase gene expression by thioredoxin,” American Journal of Respiratory Cell and Molecular Biology, vol. 17, no. 6, pp. 713–726, 1997. View at Google Scholar · View at Scopus
  32. T. Andoh, P. B. Chock, and C. C. Chiueh, “The roles of thioredoxin in protection against oxidative stress-induced apoptosis in SH-SY5Y cells,” Journal of Biological Chemistry, vol. 277, no. 12, pp. 9655–9660, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Kroemer and J. C. Reed, “Mitochondrial control of cell death,” Nature Medicine, vol. 6, no. 5, pp. 513–519, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. L. V. Johnson, M. L. Walsh, B. J. Bockus, and L. B. Chen, “Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy,” Journal of Cell Biology, vol. 88, no. 3, pp. 526–535, 1981. View at Google Scholar · View at Scopus
  35. J. H. Gill and C. Dive, “Apoptosis: basic mechanisms and relevance to toxicology,” in Apoptosis in Toxicology, R. Roberts, Ed., pp. 1–20, Taylor & Francis, New York, NY, USA, 2000. View at Google Scholar
  36. N. Zamzami, C. Brenner, I. Marzo, S. A. Susin, and G. Kroemer, “Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins,” Oncogene, vol. 16, no. 17, pp. 2265–2282, 1998. View at Google Scholar · View at Scopus
  37. S. Fulda, S. A. Susin, G. Kroemer, and K.-M. Debatin, “Molecular ordering of apoptosis induced by anticancer drugs in neuroblastoma cells,” Cancer Research, vol. 58, no. 19, pp. 4453–4460, 1998. View at Google Scholar · View at Scopus
  38. B. Mukherjee, S. Mahapatra, S. Das, G. Roy, and S. Dey, “HPLC detection of plasma concentrations of diclofenac in human volunteers administered with povidone-ethylcellulose-based experimental transdermal matrix-type patches,” Methods and Findings in Experimental and Clinical Pharmacology, vol. 28, no. 5, pp. 301–306, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. W. Tang, “The metabolism of diclofenac-enzymology and toxicology perspectives,” Current Drug Metabolism, vol. 4, no. 4, pp. 319–329, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. U. A. Boelsterli, “Diclofenac-induced liver injury: a paradigm of idiosyncratic drug toxicity,” Toxicology and Applied Pharmacology, vol. 192, no. 3, pp. 307–322, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. Yan, J. Li, N. Huebert, G. W. Caldwell, Y. Du, and H. Zhong, “Detection of a novel reactive metabolite of diclofenac: evidence for CYP2C9-mediated bioactivation via arene oxides,” Drug Metabolism and Disposition, vol. 33, no. 6, pp. 706–713, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Lauer, G. Tuschl, M. Kling, and S. O. Mueller, “Species-specific toxicity of diclofenac and troglitazone in primary human and rat hepatocytes,” Chemico-Biological Interactions, vol. 179, no. 1, pp. 17–24, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Fukuda, K. Kitaichi, F. Abe et al., “Altered brain penetration of diclofenac and mefenamic acid, but not acetaminophen, in Shiga-like toxin II-treated mice,” Journal of Pharmacological Sciences, vol. 97, no. 4, pp. 525–532, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Q. Yin, Y. H. Kim, C. K. Moon, and B. H. Lee, “Reactive oxygen species-mediated induction of apoptosis by a plant alkaloid 6-methoxydihydrosanguinarine in HepG2 cells,” Biochemical Pharmacology, vol. 70, no. 2, pp. 242–248, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Sidoti-de Fraisse, V. Rincheval, Y. Risler, B. Mignotte, and J. L. Vayssière, “TNF-α activates at least two apoptotic signaling cascades,” Oncogene, vol. 17, no. 13, pp. 1639–1651, 1998. View at Google Scholar · View at Scopus
  46. L. A. Macmillan-Crow and D. L. Cruthirds, “Invited review: manganese superoxide dismutase in disease,” Free Radical Research, vol. 34, no. 4, pp. 325–336, 2001. View at Google Scholar · View at Scopus
  47. G. H. W. Wong, “Protective roles of cytokines against radiation: induction of mitochondrial MnSOD,” Biochimica et Biophysica Acta, vol. 1271, no. 1, pp. 205–209, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Ahlemeyer, E. Bauerbach, M. Plath et al., “Retinoic acid reduces apoptosis and oxidative stress by preservation of SOD protein level,” Free Radical Biology & Medicine, vol. 30, no. 10, pp. 1067–1077, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. C. S. Niu, C. K. Chang, L. S. Lin et al., “Modification of superoxide dismutase (SOD) mRNA and activity by a transient hypoxic stress in cultured glial cells,” Neuroscience Letters, vol. 251, no. 3, pp. 145–148, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. G. A. Visner, W. C. Dougall, J. M. Wilson, I. A. Burr, and H. S. Nick, “Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor. Role in the acute inflammatory response,” Journal of Biological Chemistry, vol. 265, no. 5, pp. 2856–2864, 1990. View at Google Scholar · View at Scopus
  51. K. Mokuno, K. Ohtani, A. Suzumura et al., “Induction of manganese superoxide dismutase by cytokines and lipopolysaccharide in cultured mouse astrocytes,” Journal of Neurochemistry, vol. 63, no. 2, pp. 612–616, 1994. View at Google Scholar · View at Scopus
  52. G. H. W. Wong and D. V. Goeddel, “Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism,” Science, vol. 242, no. 4880, pp. 941–944, 1988. View at Google Scholar · View at Scopus
  53. P. X. Petit, S. A. Susin, N. Zamzami, B. Mignotte, and G. Kroemer, “Mitochondria and programmed cell death: back to the future,” FEBS Letters, vol. 396, no. 1, pp. 7–13, 1996. View at Publisher · View at Google Scholar · View at Scopus
  54. D. R. Green and G. Kroemer, “Pharmacological manipulation of cell death: clinical applications in sight?” Journal of Clinical Investigation, vol. 115, no. 10, pp. 2610–2617, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. N. Morioka, K. Kumagai, K. Morita, S. Kitayama, and T. Dohi, “Nonsteroidal anti-inflammatory drugs potentiate 1-methyl-4-phenylpyridinium (MPP+)-induced cell death by promoting the intracellular accumulation of MPP+ in PC12 cells,” Journal of Pharmacology and Experimental Therapeutics, vol. 310, no. 2, pp. 800–807, 2004. View at Publisher · View at Google Scholar · View at Scopus