Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2013, Article ID 680414, 10 pages
http://dx.doi.org/10.1155/2013/680414
Research Article

Accelerated Aging during Chronic Oxidative Stress: A Role for PARP-1

Department of Toxicology, Maastricht University, P.O. Box 6200 MD, Maastricht, The Netherlands

Received 1 August 2013; Revised 20 September 2013; Accepted 23 September 2013

Academic Editor: David Vauzour

Copyright © 2013 Daniëlle M. P. H. J. Boesten 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. D. R. Whiting, L. Guariguata, C. Weil, and J. Shaw, “IDF Diabetes Atlas: global estimates of the prevalence of diabetes for 2011 and 2030,” Diabetes Research and Clinical Practice, vol. 94, no. 3, pp. 311–321, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. Shaw, R. A. Sicree, and P. Z. Zimmet, “Global estimates of the prevalence of diabetes for 2010 and 2030,” Diabetes Research and Clinical Practice, vol. 87, no. 1, pp. 4–14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. J. Houben, H. J. J. Moonen, F. J. van Schooten, and G. J. Hageman, “Telomere length assessment: biomarker of chronic oxidative stress?” Free Radical Biology and Medicine, vol. 44, no. 3, pp. 235–246, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Veryan, P. N. Christopher, A. Eva et al., “Identification of seven loci affecting mean telomere length and their association with disease,” Nature Genetics, vol. 45, pp. 422–427, 2013. View at Google Scholar
  5. C. B. Harley, A. B. Futcher, and C. W. Greider, “Telomeres shorten during ageing of human fibroblasts,” Nature, vol. 345, no. 6274, pp. 458–460, 1990. View at Publisher · View at Google Scholar · View at Scopus
  6. E. H. Blackburn, “Structure and function of telomeres,” Nature, vol. 350, no. 6319, pp. 569–573, 1991. View at Publisher · View at Google Scholar · View at Scopus
  7. D. B. Rhee, A. Ghosh, J. Lu, V. A. Bohr, and Y. Liu, “Factors that influence telomeric oxidative base damage and repair by DNA glycosylase OGG1,” DNA Repair, vol. 10, no. 1, pp. 34–44, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. T. von Zglinicki, “Oxidative stress shortens telomeres,” Trends in Biochemical Sciences, vol. 27, no. 7, pp. 339–344, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Hewitt, D. Jurk, F. D. M. Marques et al., “Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence,” Nature Communications, vol. 3, article 708, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Petersen, G. Saretzki, and T. von Zglinicki, “Preferential accumulation of single-stranded regions in telomeres of human fibroblasts,” Experimental Cell Research, vol. 239, no. 1, pp. 152–160, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. J. M. J. Houben, E. M. Mercken, H. B. Ketelslegers et al., “Telomere shortening in chronic obstructive pulmonary disease,” Respiratory Medicine, vol. 103, no. 2, pp. 230–236, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Savale, A. Chaouat, S. Bastuji-Garin et al., “Shortened telomeres in circulating leukocytes of patients with chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 7, pp. 566–571, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Adaikalakoteswari, M. Balasubramanyam, and V. Mohan, “Telomere shortening occurs in Asian Indian Type 2 diabetic patients,” Diabetic Medicine, vol. 22, no. 9, pp. 1151–1156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Aviv, “Chronology versus biology: telomeres, essential hypertension, and vascular aging,” Hypertension, vol. 40, no. 3, pp. 229–232, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Benetos, J. P. Gardner, M. Zureik et al., “Short telomeres are associated with increased carotid atherosclerosis in hypertensive subjects,” Hypertension, vol. 43, no. 2, pp. 182–185, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Kinouchi, N. Hiwatashi, M. Chida et al., “Telomere shortening in the colonic mucosa of patients with ulcerative colitis,” Journal of Gastroenterology, vol. 33, no. 3, pp. 343–348, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Rode, S. E. Bojesen, M. Weischer, J. Vestbo, and B. G. Nordestgaard, “Short telomere length, lung function and chronic obstructive pulmonary disease in 46 396 individuals,” Thorax, vol. 68, pp. 429–435, 2013. View at Google Scholar
  18. K. D. Salpea, P. J. Talmud, J. A. Cooper et al., “Association of telomere length with type 2 diabetes, oxidative stress and UCP2 gene variation,” Atherosclerosis, vol. 209, no. 1, pp. 42–50, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Steinert, J. W. Shay, and W. E. Wright, “Modification of subtelomeric DNA,” Molecular and Cellular Biology, vol. 24, no. 10, pp. 4571–4580, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Gonzalo, I. Jaco, M. F. Fraga et al., “DNA methyltransferases control telomere length and telomere recombination in mammalian cells,” Nature Cell Biology, vol. 8, no. 4, pp. 416–424, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Benetti, M. García-Cao, and M. A. Blasco, “Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres,” Nature Genetics, vol. 39, no. 2, pp. 243–250, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Ohki and F. Ishikawa, “Telomere-bound TRF1 and TRF2 stall the replication fork at telomeric repeats,” Nucleic Acids Research, vol. 32, no. 5, pp. 1627–1637, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Pacher and C. Szabo, “Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease,” American Journal of Pathology, vol. 173, no. 1, pp. 2–13, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. W. L. Kraus and M. O. Hottiger, “PARP-1 and gene regulation: progress and puzzles,” Molecular Aspects of Medicine, 2013. View at Publisher · View at Google Scholar
  25. P. O. Hassa and M. O. Hottiger, “A role of poly (ADP-Ribose) polymerase in NF-κB transcriptional activation,” Biological Chemistry, vol. 380, no. 7-8, pp. 953–959, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. T. L. Andreone, M. O'Connor, A. Denenberg, P. W. Hake, and B. Zingarelli, “Poly(ADP-ribose) polymerase-1 regulates activation of activator protein-1 in murine fibroblasts,” Journal of Immunology, vol. 170, no. 4, pp. 2113–2120, 2003. View at Google Scholar · View at Scopus
  27. R. M. Cawthon, “Telomere measurement by quantitative PCR,” Nucleic Acids Research, vol. 30, no. 10, article e47, 2002. View at Google Scholar · View at Scopus
  28. N. W. Kim, M. A. Piatyszek, K. R. Prowse et al., “Specific association of human telomerase activity with immortal cells and cancer,” Science, vol. 266, no. 5193, pp. 2011–2015, 1994. View at Google Scholar · View at Scopus
  29. M. E. Lee, S. Y. Rha, H.-C. Jeung, H. C. Chung, and B.-K. Oh, “Subtelomeric DNA methylation and telomere length in human cancer cells,” Cancer Letters, vol. 281, no. 1, pp. 82–91, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Bladier, E. J. Wolvetang, P. Hutchinson, J. B. De Haan, and I. Kola, “Response of a primary human fibroblast cell line to H2O2: senescence- like growth arrest or apoptosis?” Cell Growth and Differentiation, vol. 8, no. 5, pp. 589–598, 1997. View at Google Scholar · View at Scopus
  31. S. Hix, M. B. Kadiiska, R. P. Mason, and O. Augusto, “In vivo metabolism of tert-Butyl hydroperoxide to methyl radicals. EPR spin-trapping and DNA methylation studies,” Chemical Research in Toxicology, vol. 13, no. 10, pp. 1056–1064, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. Q. Yang, “Cellular senescence, telomere recombination and maintenance,” Cytogenetic and Genome Research, vol. 122, no. 3-4, pp. 211–218, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Akimcheva, B. Zellinger, and K. Riha, “Genome stability in Arabidopsis cells exhibiting alternative lengthening of telomeres,” Cytogenetic and Genome Research, vol. 122, no. 3-4, pp. 388–395, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. M. A. Dunham, A. A. Neumann, C. L. Fasching, and R. R. Reddel, “Telomere maintenance by recombination in human cells,” Nature Genetics, vol. 26, no. 4, pp. 447–450, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. M. P. Hande, A. S. Balajee, A. Tchirkov, A. Wynshaw-Boris, and P. M. Lansdorp, “Extra-chromosomal telomeric DNA in cells from Atm-/- mice and patients with ataxia-telangiectasia,” Human Molecular Genetics, vol. 10, no. 5, pp. 519–528, 2001. View at Google Scholar · View at Scopus
  36. N. Š. Vidaček, A. Ćukušić, M. Ivanković et al., “Abrupt telomere shortening in normal human fibroblasts,” Experimental Gerontology, vol. 45, no. 3, pp. 235–242, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. N. Khan, D. N. Syed, N. Ahmad, and H. Mukhtar, “Fisetin: a dietary antioxidant for health promotion,” Antioxidants & Redox Signaling, vol. 19, no. 2, pp. 151–162, 2013. View at Publisher · View at Google Scholar
  38. P. Maher, T. Akaishi, and K. Abe, “Flavonoid fisetin promotes ERK-dependent long-term potentiation and enhances memory,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 44, pp. 16568–16573, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. R. R. R. de Sousa, K. C. S. Queiroz, A. C. S. Souza et al., “Phosphoprotein levels, MAPK activities and NFκkB expression are affected by fisetin,” Journal of Enzyme Inhibition and Medicinal Chemistry, vol. 22, no. 4, pp. 439–444, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Geraets, H. J. J. Moonen, K. Brauers, E. F. M. Wouters, A. Bast, and G. J. Hageman, “Dietary flavones and flavonoles are inhibitors of poly(ADP-ribose) polymerase-1 in pulmonary epithelial cells,” Journal of Nutrition, vol. 137, no. 10, pp. 2190–2195, 2007. View at Google Scholar · View at Scopus
  41. B. Sengupta, B. Pahari, L. Blackmon, and P. K. Sengupta, “Prospect of bioflavonoid fisetin as a quadruplex DNA ligand: a biophysical approach,” PLoS ONE, vol. 8, Article ID e65383, 2013. View at Google Scholar
  42. Q. Wang, J.-Q. Liu, Z. Chen et al., “G-quadruplex formation at the 3′ end of telomere DNA inhibits its extension by telomerase, polymerase and unwinding by helicase,” Nucleic Acids Research, vol. 39, no. 14, pp. 6229–6237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Gomez, J.-L. Mergny, and J.-F. Riou, “Detection of telomerase inhibitors based on G-quadruplex ligands by a modified telomeric repeat amplification protocol assay,” Cancer Research, vol. 62, no. 12, pp. 3365–3368, 2002. View at Google Scholar · View at Scopus
  44. L. Oganesian and T. M. Bryan, “Physiological relevance of telomeric G-quadruplex formation: a potential drug target,” BioEssays, vol. 29, no. 2, pp. 155–165, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. J. K. Krady, A. Basu, C. M. Allen et al., “Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy,” Diabetes, vol. 54, no. 5, pp. 1559–1565, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. C. C. Alano, T. M. Kauppinen, A. V. Valls, and R. A. Swanson, “Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 25, pp. 9685–9690, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Du, Z. Ma, S. Lin et al., “Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 25, pp. 14669–14674, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. D. C. Wu, V. Jackson-Lewis, M. Vila et al., “Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease,” Journal of Neuroscience, vol. 22, no. 5, pp. 1763–1771, 2002. View at Google Scholar · View at Scopus
  49. S. Zhu, I. G. Stavrovskaya, M. Drozda et al., “Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice,” Nature, vol. 417, no. 6884, pp. 74–78, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Van Den Bosch, P. Tilkin, G. Lemmens, and W. Robberecht, “Minocycline delays disease onset and mortality in a transgenic model of ALS,” NeuroReport, vol. 13, no. 8, pp. 1067–1070, 2002. View at Google Scholar · View at Scopus
  51. M. Chen, V. O. Ona, M. Li et al., “Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease,” Nature Medicine, vol. 6, no. 7, pp. 797–801, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Lampl, M. Boaz, R. Gilad et al., “Minocycline treatment in acute stroke: an open-label, evaluator-blinded study,” Neurology, vol. 69, no. 14, pp. 1404–1410, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Emerit, M. Edeas, and F. Bricaire, “Neurodegenerative diseases and oxidative stress,” Biomedicine and Pharmacotherapy, vol. 58, no. 1, pp. 39–46, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Li, C. Szabó, P. Pacher et al., “Evaluation of orally active poly(ADP-ribose) polymerase inhibitor in streptozotocin-diabetic rat model of early peripheral neuropathy,” Diabetologia, vol. 47, no. 4, pp. 710–717, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Szabó, A. Biser, R. Benko, E. Böttinger, and K. Suszták, “Poly(ADP-ribose) polymerase inhibitors ameliorate nephropathy of type 2 diabetic Leprdb/db mice,” Diabetes, vol. 55, no. 11, pp. 3004–3012, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Brownlee, “The pathobiology of diabetic complications: a unifying mechanism,” Diabetes, vol. 54, no. 6, pp. 1615–1625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. I. Sinha-Hikim, R. Shen, I. Nzenwa, R. Gelfand, S. K. Mahata, and A. P. Sinha-Hikim, “Minocycline suppresses oxidative stress and attenuates fetal cardiac myocyte apoptosis triggered by in utero cocaine exposure,” Apoptosis, vol. 16, no. 6, pp. 563–573, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Beneke, O. Cohausz, M. Malanga, P. Boukamp, F. Althaus, and A. Bürkle, “Rapid regulation of telomere length is mediated by poly(ADP-ribose) polymerase-1,” Nucleic Acids Research, vol. 36, no. 19, pp. 6309–6317, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. K. T. Howitz, K. J. Bitterman, H. Y. Cohen et al., “Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan,” Nature, vol. 425, no. 6954, pp. 191–196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Suh, F. Afaq, J. J. Johnson, and H. Mukhtar, “A plant flavonoid fisetin induces apoptosis in colon cancer cells by inhibition of COX2 and Wnt/EGFR/NF-κB-signaling pathways,” Carcinogenesis, vol. 30, no. 2, pp. 300–307, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. S. R. Kim, J. H. Park, M. E. Lee, J. S. Park, S. C. Park, and J. A. Han, “Selective COX-2 inhibitors modulate cellular senescence in human dermal fibroblasts in a catalytic activity-independent manner,” Mechanisms of Ageing and Development, vol. 129, no. 12, pp. 706–713, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. M. A. Blasco, “The epigenetic regulation of mammalian telomeres,” Nature Reviews Genetics, vol. 8, no. 4, pp. 299–309, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Z. Guan, W. P. Guan, T. Maeda, and N. Makino, “The subtelomere of short telomeres is hypermethylated in Alzheimer's disease,” Aging and Disease, vol. 3, pp. 164–170, 2012. View at Google Scholar
  64. T. Maeda, J. Z. Guan, J.-I. Oyama, Y. Higuchi, and N. Makino, “Aging-associated alteration of subtelomeric methylation in Parkinson's disease,” Journals of Gerontology A, vol. 64, no. 9, pp. 949–955, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Caiafa, T. Guastafierro, and M. Zampieri, “Epigenetics: Poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns,” FASEB Journal, vol. 23, no. 3, pp. 672–678, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Caiafa and J. Zlatanova, “CCCTC-binding factor meets poly(ADP-ribose) polymerase-1,” Journal of Cellular Physiology, vol. 219, no. 2, pp. 265–270, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Reale, G. De Matteis, G. Galleazzi, M. Zampieri, and P. Caiafa, “Modulation of DNMT1 activity by ADP-ribose polymers,” Oncogene, vol. 24, no. 1, pp. 13–19, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. J. L. Won, J.-Y. Shim, and B. T. Zhu, “Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids,” Molecular Pharmacology, vol. 68, no. 4, pp. 1018–1030, 2005. View at Publisher · View at Google Scholar · View at Scopus