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BioMed Research International
Volume 2013, Article ID 825065, 8 pages
http://dx.doi.org/10.1155/2013/825065
Review Article

Oxidative Stress Induces Mitochondrial DNA Damage and Cytotoxicity through Independent Mechanisms in Human Cancer Cells

Division of Urology, Department of Surgery, Research Institute of McGill University Health Center, Room R1-107, 1650 Cedar Avenue, Montreal, QC, Canada H3G 1A4

Received 9 June 2012; Revised 22 August 2012; Accepted 23 August 2012

Academic Editor: Ryan Parr

Copyright © 2013 Yue Han and Junjian Z. Chen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. L. Jackson and L. A. Loeb, “The contribution of endogenous sources of DNA damage to the multiple mutations in cancer,” Mutation Research, vol. 477, no. 1-2, pp. 7–21, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Benhar, D. Engelberg, and A. Levitzki, “ROS, stress-activated kinases and stress signaling in cancer,” EMBO Reports, vol. 3, no. 5, pp. 420–425, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Behrend, G. Henderson, and R. M. Zwacka, “Reactive oxygen species in oncogenic transformation,” Biochemical Society Transactions, vol. 31, no. 6, pp. 1441–1444, 2003. View at Google Scholar · View at Scopus
  4. B. Kumar, S. Koul, L. Khandrika, R. B. Meacham, and H. K. Koul, “Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype,” Cancer Research, vol. 68, no. 6, pp. 1777–1785, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. K. J. A. Davies, “The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress,” IUBMB Life, vol. 48, no. 1, pp. 41–47, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. V. J. Thannickal and B. L. Fanburg, “Reactive oxygen species in cell signaling,” American Journal of Physiology, vol. 279, no. 6, pp. L1005–L1028, 2000. View at Google Scholar · View at Scopus
  7. M. Dizdaroglu, G. Rao, B. Halliwell, and E. Gajewski, “Damage to the DNA bases in mammalian chromatin by hydrogen peroxide in the presence of ferric and cupric ions,” Archives of Biochemistry and Biophysics, vol. 285, no. 2, pp. 317–324, 1991. View at Publisher · View at Google Scholar · View at Scopus
  8. J. A. Imlay, S. M. Chin, and S. Linn, “Toxic DNA damage by hydrogen peroxide through the fenton reaction in vivo and in vitro,” Science, vol. 240, no. 4852, pp. 640–642, 1988. View at Google Scholar · View at Scopus
  9. B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, Clarendon Press, Oxford, UK, 1999.
  10. J. F. Turrens and A. Boveris, “Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria,” Biochemical Journal, vol. 191, no. 2, pp. 421–427, 1980. View at Google Scholar · View at Scopus
  11. C. Richter, “Oxidative damage to mitochondrial DNA and its relationship to ageing,” International Journal of Biochemistry and Cell Biology, vol. 27, no. 7, pp. 647–653, 1995. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Toyokuni, “Persistent oxidative stress in cancer,” FEBS Letters, vol. 358, no. 1, pp. 1–3, 1995. View at Publisher · View at Google Scholar · View at Scopus
  13. P. C. Herrmann, J. W. Gillespie, L. Charboneau et al., “Mitochondrial proteome: altered cytochrome c oxidase subunit levels in prostate cancer,” Proteomics, vol. 3, no. 9, pp. 1801–1810, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. M. S. Fliss, H. Usadel, O. L. Caballero et al., “Facile detection of mitochondrial DNA mutations in tumors and bodily fluids,” Science, vol. 287, no. 5460, pp. 2017–2019, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Parrella, Y. Xiao, M. Fliss et al., “Detection of mitochondrial DNA mutations in primary breast cancer and fine-needle aspirates,” Cancer Research, vol. 61, no. 20, pp. 7623–7626, 2001. View at Google Scholar · View at Scopus
  16. J. Z. Chen, N. Gokden, G. F. Greene, P. Mukunyadzi, and F. F. Kadlubar, “Extensive somatic mitochondrial mutations in primary prostate cancer using laser capture microdissection,” Cancer Research, vol. 62, no. 22, pp. 6470–6474, 2002. View at Google Scholar · View at Scopus
  17. J. Z. Chen, N. Gokden, G. F. Greene, B. Green, and F. F. Kadlubar, “Simultaneous generation of multiple mitochondrial DNA mutations in human prostate tumors suggests mitochondrial hyper-mutagenesis,” Carcinogenesis, vol. 24, no. 9, pp. 1481–1487, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Radloff, W. Bauer, and J. Vinograd, “A dye-buoyant-density method for the detection and isolation of closed circular duplex DNA: the closed circular DNA in HeLa cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 57, no. 5, pp. 1514–1521, 1967. View at Google Scholar · View at Scopus
  19. D. L. Robberson and D. A. Clayton, “Replication of mitochondrial DNA in mouse L cells and their thymidine kinase—derivatives: displacement replication on a covalently-closed circular template,” Proceedings of the National Academy of Sciences of the United States of America, vol. 69, no. 12, pp. 3810–3814, 1972. View at Google Scholar · View at Scopus
  20. D. Bogenhagen and D. A. Clayton, “Mechanism of mitochondrial DNA replication in mouse L-cells. Introduction of superhelical turns into newly replicated molecules,” Journal of Molecular Biology, vol. 119, no. 1, pp. 69–81, 1978. View at Google Scholar · View at Scopus
  21. D. A. Clayton, “Replication of animal mitochondrial DNA,” Cell, vol. 28, no. 4, pp. 693–705, 1982. View at Google Scholar · View at Scopus
  22. C. Nicco, A. Laurent, C. Chereau, B. Weill, and F. Batteux, “Differential modulation of normal and tumor cell proliferation by reactive oxygen species,” Biomedicine and Pharmacotherapy, vol. 59, no. 4, pp. 169–174, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. Q. Kong, J. A. Beel, and K. O. Lillehei, “A threshold concept for cancer therapy,” Medical Hypotheses, vol. 55, no. 1, pp. 29–35, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. R. H. Burdon, “Superoxide and hydrogen peroxide in relation to mammalian cell proliferation,” Free Radical Biology and Medicine, vol. 18, no. 4, pp. 775–794, 1995. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Laurent, C. Nicco, C. Chéreau et al., “Controlling tumor growth by modulating endogenous production of reactive oxygen species,” Cancer Research, vol. 65, no. 3, pp. 948–956, 2005. View at Google Scholar · View at Scopus
  26. N. Aykin-Burns, I. M. Ahmad, Y. Zhu, L. W. Oberley, and D. R. Spitz, “Increased levels of superoxide and H2O2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation,” Biochemical Journal, vol. 418, no. 1, pp. 29–37, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Ranzato, S. Biffo, and B. Burlando, “Selective ascorbate toxicity in malignant mesothelioma a redox trojan mechanism,” American Journal of Respiratory Cell and Molecular Biology, vol. 44, no. 1, pp. 108–117, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. S. D. Lim, C. Sun, J. D. Lambeth et al., “Increased Nox1 and hydrogen peroxide in prostate cancer,” Prostate, vol. 62, no. 2, pp. 200–207, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. O. Warburg, “On the origin of cancer cells,” Science, vol. 123, no. 3191, pp. 309–314, 1956. View at Google Scholar · View at Scopus
  30. J. S. Penta, F. M. Johnson, J. T. Wachsman, and W. C. Copeland, “Mitochondrial DNA in human malignancy,” Mutation Research, vol. 488, no. 2, pp. 117–133, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Dorward, S. Sweet, R. Moorehead, and G. Singh, “Mitochondrial contributions to cancer cell physiology: redox balance, cell cycle, and drug resistance,” Journal of Bioenergetics and Biomembranes, vol. 29, no. 4, pp. 385–392, 1997. View at Publisher · View at Google Scholar · View at Scopus
  32. B. N. Ames, M. K. Shigenaga, and T. M. Hagen, “Oxidants antioxidants, and the degenerative diseases of aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, pp. 6465–6467, 1988. View at Google Scholar
  33. S. W. Chan, P. N. Nguyen, D. Ayele, S. Chevalier, A. Aprikian, and J. Z. Chen, “Mitochondrial DNA damage is sensitive to exogenous H2O2 but independent of cellular ROS production in prostate cancer cells,” Mutation Research, vol. 716, pp. 40–50, 2011. View at Google Scholar
  34. J. Chen, F. F. Kadlubar, and J. Z. Chen, “DNA supercoiling suppresses real-time PCR: a new approach to the quantification of mitochondrial DNA damage and repair,” Nucleic Acids Research, vol. 35, no. 4, pp. 1377–1388, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Higuchi, C. Fockler, G. Dollinger, and R. Watson, “Kinetic PCR analysis: real-time monitoring of DNA amplification reactions,” Bio/Technology, vol. 11, no. 9, pp. 1026–1030, 1993. View at Publisher · View at Google Scholar · View at Scopus
  36. C. A. Heid, J. Stevens, K. J. Livak, and P. M. Williams, “Real time quantitative PCR,” Genome Research, vol. 6, no. 10, pp. 986–994, 1996. View at Google Scholar · View at Scopus
  37. S. W. Chan and J. Z. Chen, “Measuring mtDNA damage using a supercoiling-sensitive qPCR approach,” Methods in Molecular Biology, vol. 554, pp. 183–197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Yaffee, P. Walter, C. Richter, and M. Müller, “Direct observation of iron-induced conformational changes of mitochondrial DNA by high-resolution field-emission in-lens scanning electron microscopy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 11, pp. 5341–5346, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. W. G. Li, F. J. Miller, H. J. Zhang, D. R. Spitz, L. W. Oberley, and N. L. Weintraub, “H2O2-induced O2.- production by a non-phagocytic NAD(P)H oxidase causes oxidant injury,” Journal of Biological Chemistry, vol. 276, no. 31, pp. 29251–29256, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. C. H. Coyle, L. J. Martinez, M. C. Coleman, D. R. Spitz, N. L. Weintraub, and K. N. Kader, “Mechanisms of H2O2-induced oxidative stress in endothelial cells,” Free Radical Biology and Medicine, vol. 40, no. 12, pp. 2206–2213, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. B. M. Boulden, J. D. Widder, J. C. Allen et al., “Early determinants of H2O2-induced endothelial dysfunction,” Free Radical Biology and Medicine, vol. 41, no. 5, pp. 810–817, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. A. R. Cross and O. T. G. Jones, “The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase,” Biochemical Journal, vol. 237, no. 1, pp. 111–116, 1986. View at Google Scholar · View at Scopus
  43. N. Li, K. Ragheb, G. Lawler et al., “DPI induces mitochondrial superoxide-mediated apoptosis,” Free Radical Biology and Medicine, vol. 34, no. 4, pp. 465–477, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Riganti, E. Gazzano, M. Polimeni, C. Costamagna, A. Bosia, and D. Ghigo, “Diphenyleneiodonium inhibits the cell redox metabolism and induces oxidative stress,” Journal of Biological Chemistry, vol. 279, no. 46, pp. 47726–47731, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. A. J. Lambert, J. A. Buckingham, H. M. Boysen, and M. D. Brand, “Diphenyleneiodonium acutely inhibits reactive oxygen species production by mitochondrial complex I during reverse, but not forward electron transport,” Biochimica et Biophysica Acta, vol. 1777, no. 5, pp. 397–403, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. P. B. Walter, M. D. Knutson, A. Paler-Martinez et al., “Iron deficiency and iron excess damage mitochondria and mitochondrial DNA in rats,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 2264–2269, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. S. W. Chan, Mitochondrial DNA as a sensitive surrogate to oxidative stress in prostate cancer cells and circulating lymphocytes [M.S. thesis], McGill University, 2009.
  48. M. S. Gabriel, S. W. Chan, A. Alhathal, J. Z. Chen, and A. Zini, “Influence of microsurgical varicocelectomy on human sperm mitochondrial DNA copy number: a pilot study,” Journal of Assisted Reproduction and Genetics, vol. 29, no. 8, pp. 759–764, 2012. View at Publisher · View at Google Scholar