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Oxidative Medicine and Cellular Longevity
Volume 2012 (2012), Article ID 313275, 14 pages
http://dx.doi.org/10.1155/2012/313275
Research Article

TPEN Induces Apoptosis Independently of Zinc Chelator Activity in a Model of Acute Lymphoblastic Leukemia and Ex Vivo Acute Leukemia Cells through Oxidative Stress and Mitochondria Caspase-3- and AIF-Dependent Pathways

Neuroscience Research Group, Medical Research Institute School of Medicine, University of Antioquia (UdeA), Calle 62 No. 52-59, Building 1, Laboratory 411/412, SIU, Medellin, Colombia

Received 25 September 2012; Accepted 4 November 2012

Academic Editor: Felipe Dal-Pizzol

Copyright © 2012 Miguel Mendivil-Perez 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. R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics 2012,” A Cancer Journal for Clinicians, vol. 62, pp. 10–29, 2012.
  2. G. Pasternak, A. Hochhaus, B. Schultheis, and R. Hehlmann, “Chronic myelogenous leukemia: molecular and cellular aspects,” Journal of Cancer Research and Clinical Oncology, vol. 124, no. 12, pp. 643–660, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. C. H. Pui, M. V. Relling, and J. R. Downing, “Mechanisms of disease: acute lymphoblastic leukemia,” The New England Journal of Medicine, vol. 350, no. 15, pp. 1535–1548, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell, vol. 100, no. 1, pp. 57–70, 2000. View at Scopus
  5. D. A. Tennant, R. V. Durán, H. Boulahbel, and E. Gottlieb, “Metabolic transformation in cancer,” Carcinogenesis, vol. 30, no. 8, pp. 1269–1280, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. J. F. R. Kerr, G. C. Gobé, C. M. Winterford, and B. V. Harmon, “Chapter 1 anatomical methods in cell death,” Methods in Cell Biology C, vol. 46, pp. 1–27, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Kroemer, L. Galluzzi, P. Vandenabeele et al., “Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009,” Cell Death and Differentiation, vol. 16, no. 1, pp. 3–11, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Galluzzi, I. Vitale, J. M. Abrams et al., “Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012,” Cell Death and Differentiation, vol. 19, pp. 107–120, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Nowak, D. Stewart, and H. P. Koeffler, “Differentiation therapy of leukemia: 3 decades of development,” Blood, vol. 113, no. 16, pp. 3655–3665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. G. L. Kelly and A. Strasser, “The essential role of evasion from cell death in cancer,” Advances in Cancer Research, vol. 111, pp. 39–96, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Chen, E. Wang, Y. Lu, K. K. Gaal, and Q. Huang, “Therapy-related acute lymphoblastic leukemia without 11q23 abnormality: report of six cases and a literature review,” American Journal of Clinical Pathology, vol. 133, no. 1, pp. 75–82, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Szotkowski, P. Rohon, L. Zapletalova, K. Sicova, J. Hubacek, and K. Indrak, “Secondary acute myeloid leukemia—a single center experience,” Neoplasma, vol. 57, no. 2, pp. 170–178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Kelaidi, L. Adès, and P. Fenaux, “Treatment of acute promyelocytic leukemia with high white cell blood counts,” Mediterranean Journal of Hematology and Infectious Diseases, vol. 3, Article ID e2011038, 2011.
  14. J. C. Reed, “Warner-Lambert/Parke Davis award lecture: mechanisms of apoptosis,” American Journal of Pathology, vol. 157, no. 5, pp. 1415–1430, 2000. View at Scopus
  15. The KEGG (Kyoto Encyclopedia of Genes and Genomes) PATHWAY Database, (Apoptosis), http://www.genome.jp/kegg/pathway/hsa/hsa04210.html.
  16. T. P. Dang, “Notch apoptosis and cancer,” Advances in Experimental Medicine and Biology, vol. 727, pp. 199–209, 2012.
  17. X. L. Zuo, J. M. Chen, X. Zhou, X. Z. Li, and G. Y. Mei, “Levels of selenium, zinc, copper, and antioxidant enzyme activity in patients with leukemia,” Biological Trace Element Research, vol. 114, no. 1–3, pp. 41–53, 2006. View at Scopus
  18. R. Ciarcia, D. D'Angelo, C. Pacilio et al., “Dysregulated calcium homeostasis and oxidative stress in chronic myeloid leukemia (CML) cells,” Journal of Cellular Physiology, vol. 224, no. 2, pp. 443–453, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. B. L. Vallee and K. H. Falchuk, “The biochemical basis of zinc physiology,” Physiological Reviews, vol. 73, no. 1, pp. 79–118, 1993. View at Scopus
  20. L. M. Plum, L. Rink, and H. Hajo, “The essential toxin: impact of zinc on human health,” International Journal of Environmental Research and Public Health, vol. 7, no. 4, pp. 1342–1365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Zhao, R. P. Planalp, R. Ma et al., “Role of zinc and iron chelation in apoptosis mediated by tachpyridine, an anti-cancer iron chelator,” Biochemical Pharmacology, vol. 67, no. 9, pp. 1677–1688, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Khan and S. Merajver, “Copper chelation in cancer therapy using tetrathiomolybdate: an evolving paradigm,” Expert Opinion on Investigational Drugs, vol. 18, no. 4, pp. 541–548, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Adler, H. Shafer, T. Hamilton, and J. P. Petrali, “Cytotoxic actions of the heavy metal chelator TPEN on NG108-15 neuroblastoma-glioma cells,” NeuroToxicology, vol. 20, no. 4, pp. 571–582, 1999. View at Scopus
  24. M. Donadelli, E. D. Pozza, C. Costanzo, M. T. Scupoli, A. Scarpa, and M. Palmieri, “Zinc depletion efficiently inhibits pancreatic cancer cell growth by increasing the ratio of antiproliferative/proliferative genes,” Journal of Cellular Biochemistry, vol. 104, no. 1, pp. 202–212, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Hashemi, S. Ghavami, M. Eshraghi, E. P. Booy, and M. Los, “Cytotoxic effects of intra and extracellular zinc chelation on human breast cancer cells,” European Journal of Pharmacology, vol. 557, no. 1, pp. 9–19, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Jiang, B. Zhivotovsky, D. H. Burgess, A. Gahm, S. C. Chow, and S. Orrenius, “The role of proteolysis in T cell apoptosis triggered by chelation of intracellular Zn2+,” Cell Death and Differentiation, vol. 4, no. 1, pp. 39–50, 1997. View at Scopus
  27. P. Makhov, K. Golovine, R. G. Uzzo et al., “Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis and sensitizes prostate cancer cells to TRAIL-mediated apoptosis,” Cell Death and Differentiation, vol. 15, no. 11, pp. 1745–1751, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. R. S. Corniola, N. M. Tassabehji, J. Hare, G. Sharma, and C. W. Levenson, “Zinc deficiency impairs neuronal precursor cell proliferation and induces apoptosis via p53-mediated mechanisms,” Brain Research C, vol. 1237, pp. 52–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. V. M. Kolenko, R. G. Uzzo, N. Dulin, E. Hauzman, R. Bukowski, and J. H. Finke, “Mechanism of apoptosis induced by zinc deficiency in peripheral blood T lymphocytes,” Apoptosis, vol. 6, no. 6, pp. 419–429, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Lee, Y. J. Kim, H. Ra et al., “The involvement of caspase-11 in TPEN-induced apoptosis,” FEBS Letters, vol. 582, no. 13, pp. 1871–1876, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. J. López, P. C. Redondo, G. M. Salido, J. A. Pariente, and J. A. Rosado, “N,N,N',N'-tetrakis(2-pyridylmethyl)ethylenediamine induces apoptosis through the activation of caspases-3 and -8 in human platelets. A role for endoplasmic reticulum stress,” Journal of Thrombosis and Haemostasis, vol. 7, no. 6, pp. 992–999, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Marini, F. Frabetti, S. Canaider, L. Dini, E. Falcieri, and G. G. Poirier, “Modulation of caspase-3 activity by zinc ions and by the cell redox state,” Experimental Cell Research, vol. 266, no. 2, pp. 323–332, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Ra, H. L. Kim, H. W. Lee, and Y. H. Kim, “Essential role of p53 in TPEN-induced neuronal apoptosis,” FEBS Letters, vol. 583, no. 9, pp. 1516–1520, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Jimenez-Del-Rio and C. Velez-Pardo, “The bad the good and the ugly about oxidative stress,” Oxidative Medicine and Cellular Longevity, vol. 2012, 13 pages, 2012.
  35. C. Le Goffe, G. Vallette, L. Charrier et al., “Metabolic control of resistance of human epithelial cells to H2O2 and NO stresses,” Biochemical Journal, vol. 364, no. 2, pp. 349–359, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. R. B. Hamanaka and N. S. Chandel, “Targeting glucose metabolism for cancer therapy,” The Journal of Experimental Medicine, vol. 209, pp. 211–215, 2012.
  37. A. R. Bonilla-Porras, M. Jimenez-Del-Rio, and C. Velez-Pardo, “Vitamin K3 and vitamin C alone or in combination induced apoptosis in leukemia cells by a similar oxidative stress signalling mechanism,” Cancer Cell International, vol. 11, article 19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Melinn and H. McLaughlin, “Nitroblue tetrazolium reduction in lymphocytes,” Journal of Leukocyte Biology, vol. 41, no. 4, pp. 325–329, 1987. View at Scopus
  39. A. Annibaldi and C. Widmann, “Glucose metabolism in cancer cells,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 13, no. 4, pp. 466–470, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Brigelius-Flohé and L. Flohé, “Basic principles and emerging concepts in the redox control of transcription factors,” Antioxidants and Redox Signaling, vol. 15, pp. 2335–2381, 2011.
  41. G. Gloire, E. Charlier, S. Rahmouni et al., “Restoration of SHIP-1 activity in human leukemic cells modifies NF-κB activation pathway and cellular survival upon oxidative stress,” Oncogene, vol. 25, no. 40, pp. 5485–5494, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Ichijo, E. Nishida, K. Irie et al., “Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways,” Science, vol. 275, no. 5296, pp. 90–94, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. F. S. Lee, J. Hagler, Z. J. Chen, and T. Maniatis, “Activation of the IκBα kinase complex by MEKK1, a kinase of the JNK pathway,” Cell, vol. 88, no. 2, pp. 213–222, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Schoonbroodt, V. Ferreira, M. Best-Belpomme et al., “Crucial role of the amino-terminal tyrosine residue 42 and the carboxylterminal PEST domain of IκBα in NF-κB activation by an oxidative stress,” Journal of Immunology, vol. 164, no. 8, pp. 4292–4300, 2000. View at Scopus
  45. Y. Takada, A. Mukhopadhyay, G. C. Kundu, G. H. Mahabeleshwar, S. Singh, and B. B. Aggarwal, “Hydrogen peroxide activates NF-κB through tyrosine phosphorylation of IκBα and serine phosphorylation of p65. Evidence for the involvement of IκBα kinase and Syk protein-tyrosine kinase,” Journal of Biological Chemistry, vol. 278, no. 26, pp. 24233–24241, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Fan, J. Dutta, N. Gupta, G. Fan, and C. Gélinas, “Regulation of programmed cell death by NF-κB and its role in tumorigenesis and therapy,” Advances in Experimental Medicine and Biology, vol. 615, pp. 223–250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. S. K. Radhakrishnan and S. Kamalakaran, “Pro-apoptotic role of NF-κB: implications for cancer therapy,” Biochimica et Biophysica Acta, vol. 1766, no. 1, pp. 53–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Wu and G. Lozano, “NF-κB activation of p53. A potential mechanism for suppressing cell growth in response to stress,” Journal of Biological Chemistry, vol. 269, no. 31, pp. 20067–20074, 1994. View at Scopus
  49. A. V. Vaseva and U. M. Moll, “The mitochondrial p53 pathway,” Biochimica et Biophysica Acta, vol. 1787, no. 5, pp. 414–420, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. I. A. Olovnikov, J. E. Kravchenko, and P. M. Chumakov, “Homeostatic functions of the p53 tumor suppressor: regulation of energy metabolism and antioxidant defense,” Seminars in Cancer Biology, vol. 19, no. 1, pp. 32–41, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. X. D. Zhang, Z. H. Qin, and J. Wang, “The role of p53 in cell metabolism,” Acta Pharmacologica Sinica, vol. 31, no. 9, pp. 1208–1212, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. E. McCormack, I. Haaland, G. Venas et al., “Synergistic induction of p53 mediated apoptosis by valproic acid and nutlin-3 in acute myeloid leukemia,” Leukemia, vol. 26, pp. 910–907, 2012.
  53. M. N. Saha, J. Micallef, L. Qiu, and H. Chang, “Pharmacological activation of the p53 pathway in haematological malignancies,” Journal of Clinical Pathology, vol. 63, no. 3, pp. 204–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. J. W. Tyner, A. M. Jemal, M. Thayer, B. J. Druker, and B. H. Chang, “Targeting surviving and p53 in pediatric acute lymphoblastic leukemia,” Leukemia, vol. 26, pp. 623–632, 2012.
  55. P. Ak and A. J. Levine, “p53 and NF-κB: different strategies for responding to stress lead to a functional antagonism,” The FASEB Journal, vol. 24, no. 10, pp. 3643–3652, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. M. C. Willingham, “Cytochemical methods for the detection of apoptosis,” Journal of Histochemistry and Cytochemistry, vol. 47, no. 9, pp. 1101–1110, 1999. View at Scopus
  57. H. Boujrad, O. Gubkina, N. Robert, S. Krantic, and S. A. Susin, “AIF-mediated programmed necrosis: a highly regulated way to die,” Cell Cycle, vol. 6, no. 21, pp. 2612–2619, 2007. View at Scopus
  58. P. Stambolsky, L. Weisz, I. Shats et al., “Regulation of AIF expression by p53,” Cell Death and Differentiation, vol. 13, no. 12, pp. 2140–2149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Perez-Alvarez, V. Iglesias-Guimarais, M. E. Solesio et al., “Methadone induces CAD degradation and AIF-mediated necrotic-like cell death in neuroblastoma cells,” Pharmacological Research, vol. 63, no. 4, pp. 352–360, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. B. Guo, M. Yang, D. Liang, L. Yang, J. Cao, and L. Zhang, “Cell apoptosis induced by zinc deficiency in osteoblastic MC3T3-E1 cells via a mitochondrial-mediated pathway,” Molecular and Cellular Biochemistry, vol. 361, pp. 209–216, 2012.
  61. D. K. Perry, M. J. Smyth, H. R. Stennicke et al., “Zinc is a potent inhibitor of the apoptotic protease, caspase-3: a novel target for zinc in the inhibition of apoptosis,” Journal of Biological Chemistry, vol. 272, no. 30, pp. 18530–18533, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. O. Son, Y. S. Jang, X. Shi, and J. C. Lee, “Activation of JNK and c-Jun is involved in glucose oxidase-mediated cell death of human lymphoma cells,” Molecules and Cells, vol. 28, no. 6, pp. 545–551, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. T. Buschmann, O. Potapova, A. Bar-Shira et al., “Jun NH2-terminal kinase phosphorylation of p53 on Thr-81 is important for p53 stabilization and transcriptional activities in response to stress,” Molecular and Cellular Biology, vol. 21, no. 8, pp. 2743–2754, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Yin, W. Chen, C. Tang et al., “NF-κB JNK and p53 pathways are involved in tubeimoside-1-induced apoptosis in HepG2 cells with oxidative stress and G2/M cell cycle arrest,” Food and Chemical Toxicology, vol. 49, pp. 3046–3054, 2011.
  65. C. Palmi, E. Vendramini, D. Silvestri et al., “Poor prognosis for P2RY8-CRLF2 fusion but not for CRLF2 over-expression in children with intermediate risk B-cell precursor acute lymphoblastic leukemia,” Leukemia, vol. 26, no. 10, pp. 2245–2253.
  66. M. Schrappe, S. P. Hunger, C. H. Pui et al., “Outcomes after induction failure in childhood acute lymphoblastic leukemia,” The New England Journal of Medicine, vol. 366, pp. 1371–1381, 2012.