Table of Contents Author Guidelines Submit a Manuscript
Journal of Nutrition and Metabolism
Volume 2013 (2013), Article ID 821082, 10 pages
http://dx.doi.org/10.1155/2013/821082
Research Article

Plant Polyphenols and Oxidative Metabolites of the Herbal Alkenylbenzene Methyleugenol Suppress Histone Deacetylase Activity in Human Colon Carcinoma Cells

Division of Food Chemistry and Toxicology, Department of Chemistry, University of Kaiserslautern, Erwin-Schroedinger-Straße 52, 67663 Kaiserslautern, Germany

Received 25 May 2012; Revised 5 September 2012; Accepted 6 September 2012

Academic Editor: Christel Lamberg-Allardt

Copyright © 2013 Isabel Anna Maria Groh 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. Rafter, M. Govers, P. Martel et al., “PASSCLAIM-diet-related cancer,” European Journal of Nutrition, vol. 43, no. 2, pp. II47–II84, 2004. View at Google Scholar · View at Scopus
  2. A. Link, F. Balaguer, and A. Goel, “Cancer chemoprevention by dietary polyphenols: promising role for epigenetics,” Biochemical Pharmacology, vol. 80, no. 12, pp. 1771–1792, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Shilatifard, “Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression,” Annual Review of Biochemistry, vol. 75, pp. 243–269, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Sui, Y. Wang, L. H. Ju et al., “Epigenetic regulation of reelin and brain-derived neurotrophic factor genes in long-tern potentiation in rat medial prefrontal cortex,” Neurobiology of Learning Memory, vol. 97, no. 4, pp. 425–440, 2012. View at Google Scholar
  5. P. A. Marks, V. M. Richon, T. Miller, and W. K. Kelly, “Histone deacetylase inhibitors,” Advances in Cancer Research, vol. 91, pp. 137–168, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Dokmanovic and P. A. Marks, “Prospects: histone deacetylase inhibitors,” Journal of Cellular Biochemistry, vol. 96, no. 2, pp. 293–304, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Gao, M. A. Cueto, F. Asselbergs, and P. Atadja, “Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family,” Journal of Biological Chemistry, vol. 277, no. 28, pp. 25748–25755, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Rajendran, E. Ho, D. E. Williams et al., “Dietary phytochemicals, HDAC inhibition, and DNA damage/repair defects in cancer cells,” Clinical Epigenetics, vol. 3, no. 1, p. 4, 2011. View at Publisher · View at Google Scholar
  9. V. S. Thakur, K. Gupta, and S. Gupta, “Green tea polyphenols causes cell cycle arrest and apoptosis in prostate cancer cells by suppressing class I histone deacetylases,” Carcinogenesis, vol. 33, no. 2, pp. 377–384, 2012. View at Google Scholar
  10. W. Weichert, A. Röske, S. Niesporek et al., “Class I histone deacetylase expression has independent prognostic impact in human colorectal cancer: specific role of class I histone deacetylases in vitro and in vivo,” Clinical Cancer Research, vol. 14, no. 6, pp. 1669–1677, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Hahnen, J. Hauke, C. Tränkle et al., “Histone deacetlyase ihhibitors: possible implications for neurodegenerative disorders,” Expert Opinion on Investigational Drugs, vol. 17, pp. 169–184, 2008. View at Google Scholar
  12. B. E. Morrison, N. Majdzadeh, and S. R. D'Mello, “Histone deacetylases: focus on the nervous system,” Cellular and Molecular Life Sciences, vol. 64, no. 17, pp. 2258–2269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. D. M. Chuang, Y. Leng, Z. Marinova, H. J. Kim, and C. T. Chiu, “Multiple roles of HDAC inhibition in neurodegenerative conditions,” Trends in Neurosciences, vol. 32, no. 11, pp. 591–601, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Abel and R. S. Zukin, “Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders,” Current Opinion in Pharmacology, vol. 8, no. 1, pp. 57–64, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. O. Moradei, C. R. Maroun, I. Paquin, and A. Vaisburg, “Histone deacetylase inhibitors: latest developments, trends and prospects,” Current Medicinal Chemistry, vol. 5, no. 5, pp. 529–560, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. W. S. Xu, R. B. Parmigiani, and P. A. Marks, “Histone deacetylase inhibitors: molecular mechanisms of action,” Oncogene, vol. 26, no. 37, pp. 5541–5552, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Jung, “Inhibitors of histone deacetylase as new anticancer agents,” Current Medicinal Chemistry, vol. 8, no. 12, pp. 1505–1511, 2001. View at Google Scholar · View at Scopus
  18. G. G. Duthie, S. J. Duthie, and J. A. M. Kyle, “Plant polyphenols in cancer and heart disease: implications as nutritional antioxidants,” Nutrition Research Reviews, vol. 13, no. 1, pp. 79–106, 2000. View at Google Scholar · View at Scopus
  19. C. S. Yang, J. M. Landau, M. T. Huang, and H. L. Newmark, “Inhibition of carcinogenesis by dietary polyphenolic compounds,” Annual Review of Nutrition, vol. 21, pp. 381–406, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Pandey, S. Shukla, and S. Gupta, “Promoter demethylation and chromatin remodeling by green tea polyphenols leads to re-expression of GSTP1 in human prostate cancer cells,” International Journal of Cancer, vol. 126, no. 11, pp. 2520–2533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. V. S. Thakur, K. Gupta, and S. Gupta, “Green tea polyphenols increased p53 transcriptional activity and acetylation by suppressing class I histone deacetylase,” International Journal of Oncology, vol. 41, no. 1, pp. 353–361, 2012. View at Publisher · View at Google Scholar
  22. M. Waldecker, T. Kautenburger, H. Daumann, C. Busch, and D. Schrenk, “Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon,” Journal of Nutritional Biochemistry, vol. 19, no. 9, pp. 587–593, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. H. L. Liu, Y. Chen, G. H. Cui, and J. F. Zhou, “Curcumin, a potent anti-tumor reagent, is a novel histone deacetylase inhibitor regulating B-NHL cell line Raji proliferation,” Acta Pharmacologica Sinica, vol. 26, no. 5, pp. 603–609, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Kikuno, H. Shiina, S. Urakami et al., “Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells,” International Journal of Cancer, vol. 123, no. 3, pp. 552–560, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Gardner, H. Wakazono, P. Bergin et al., “Cytochrome P450 mediated bioactivation of methyleugenol to 1'-hydroxymethyleugenol in Fischer 344 rat and human liver microsomes,” Carcinogenesis, vol. 18, no. 9, pp. 1775–1783, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. S. M. F. Jeurissen, J. J. P. Bogaards, M. G. Boersma et al., “Human cytochrome P450 enzymes of importance for the bioactivation of methyleugenol to the proximate carcinogen 1-hydroxymethyleugenol,” Chemical Research in Toxicology, vol. 19, no. 1, pp. 111–116, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. National Toxicology Program (NTP), “Toxicology and cancinogenesis studies of methyleugenol in F344/N rats and B6C3F1 mice (gavage studies),” DRAFT NTP-TR-491 98-3950, NIH, 2000. View at Google Scholar
  28. R. L. Smith, T. B. Adams, J. Doull et al., “Safety assessment of allylalkoxybenzene derivatives used as flavouring substances—methyl eugenol and estragole,” Food and Chemical Toxicology, vol. 40, no. 7, pp. 851–870, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. Scientific Committee of Food (SCF), “Opinion of the Scientific Committee of Food on Methyleugenol (4-Allyl-1, 2- dimethoxybenzene),” 2001.
  30. A. T. Cartus, K.-H. Merz, and D. Schrenk, “Metabolism of methylisoeugenol in liver microsomes of human, rat, and bovine origin,” Drug Metabolism and Disposition, vol. 39, no. 9, pp. 1727–1733, 2011. View at Publisher · View at Google Scholar
  31. P. Skehan, R. Storeng, D. Scudiero et al., “New colorimetric cytotoxicity assay for anticancer-drug screening,” Journal of the National Cancer Institute, vol. 82, no. 13, pp. 1107–1112, 1990. View at Google Scholar · View at Scopus
  32. M. Kern, Z. Tjaden, Y. Ngiewih et al., “Inhibitors of the epidermal growth factor receptor in apple juice extract,” Molecular Nutrition & Food Research, vol. 49, no. 4, pp. 317–328, 2005. View at Publisher · View at Google Scholar
  33. Z. Yu, W. Li, and F. Liu, “Inhibition of proliferation and induction of apoptosis by genistein in colon cancer HT-29 cells,” Cancer Letters, vol. 215, no. 2, pp. 159–166, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Chen and Q. Ping Dou, “Tea polyphenols and their roles in cancer prevention and chemotherapy,” International Journal of Molecular Sciences, vol. 9, no. 7, pp. 1196–1206, 2008. View at Publisher · View at Google Scholar
  35. V. Nandakumar, M. Vaid, and S. K. Katiyar, “(−)-Epigallocatechin-3-gallate reactivates silenced tumor suppressor genes, Cip1/p21 and p16INK4a, by reducing DNA methylation and increasing histones acetylation in human skin cancer cells,” Carcinogenesis, vol. 32, no. 4, pp. 537–544, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. I. Khan, P. Aumsuwan, I. A. Khan, L. A. Walker, and A. K. Dasmahapatra, “Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome,” Chemical Research in Toxicology, vol. 25, no. 1, pp. 61–73, 2012. View at Publisher · View at Google Scholar
  37. M. Z. Fang, D. Chen, Y. Sun, Z. Jin, J. K. Christman, and C. S. Yang, “Reversal of hypermethylation and reactivation of p16INK4a, RARbeta, and MGMT genes by genistein and other isoflavones from soy,” Clinical Cancer Research, vol. 11, no. 19, pp. 7033–7041, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Li, L. Liu, L. G. Andrews, and T. O. Tollefsbol, “Genistein depletes telomerase activity through cross-talk between genetic and epigenetic mechanisms,” International Journal of Cancer, vol. 125, no. 2, pp. 286–296, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Majid, A. A. Dar, A. E. Ahmad et al., “BTG3 tumor suppressor gene promoter demethylation, histone modification and cell cycle arrest by genistein in renal cancer,” Carcinogenesis, vol. 30, no. 4, pp. 662–670, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Hong, T. Nakagawa, W. Pan et al., “Isoflavones stimulate estrogen receptor-mediated core histone acetylation,” Biochemical and Biophysical Research Communications, vol. 317, no. 1, pp. 259–264, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. M. N. Clifford, “Chlorogenic acids and other cinnamates—nature, occurrence and dietary burden,” Journal of the Science of Food and Agriculture, vol. 79, no. 3, pp. 362–372, 1999. View at Publisher · View at Google Scholar
  42. M. R. Olthof, P. C. Hollman, and M. B. Katan, “Chlorogenic acid and caffeic acid are absorbed in humans,” Journal of Nutrition, vol. 131, no. 1, pp. 66–71, 2001. View at Google Scholar
  43. G. H. Degen, P. Janning, P. Diel, and H. M. Bolt, “Estrogenic isoflavones in rodent diets,” Toxicology Letters, vol. 128, no. 1–3, pp. 145–157, 2002. View at Publisher · View at Google Scholar
  44. C. S. Yang and Z. Y. Wang, “Tea and cancer,” Journal of the National Cancer Institute, vol. 85, no. 13, pp. 1038–1049, 1993. View at Publisher · View at Google Scholar
  45. A. Farah, M. Monteiro, C. M. Donangelo, and S. Lafay, “Chlorogenic acids from green coffee extract are highly bioavailable in humans,” Journal of Nutrition, vol. 138, no. 12, pp. 2309–2315, 2008. View at Publisher · View at Google Scholar
  46. C. D. Gardner, L. M. Chatterjee, and A. A. Franke, “Effects of isoflavone supplements vs. soy foods on blood concentrations of genistein and daidzein in adults,” Journal of Nutritional Biochemistry, vol. 20, no. 3, pp. 227–234, 2009. View at Publisher · View at Google Scholar
  47. M. J. : Lee, P. Maliakal, L. Chen et al., “Pharmacokinetics of tea catechins after ingestion of green tea and (−)-epigallocatechin-3-gallate by humans: formation of different metabolites and individual variability,” Cancer Epidemiology, Biomarkers & Prevention, vol. 11, no. 10, pp. 1025–1032, 2002. View at Google Scholar
  48. E. J. Kim, H. K. Shin, and J. H. Y. Park, “Genistein inhibits insulin-like growth factor-I receptor signaling in HT-29 human colon cancer cells: a possible mechanism of the growth inhibitory effect of genistein,” Journal of Medicinal Food, vol. 8, no. 4, pp. 431–438, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. W. Qi, C. R. Weber, K. Wasland, and S. D. Savkovic, “Genistein inhibits proliferation of colon cancer cells by attenuating a negative effect of epidermal growth factor on tumor suppressor FOXO3 activity,” BMC Cancer, vol. 11, p. 219, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Kern, D. Fridrich, J. Reichert et al., “Limited stability in cell culture medium and hydrogen peroxide formation affect the growth inhibitory properties of delphinidin and its degradation product gallic acid,” Molecular Nutrition and Food Research, vol. 51, no. 9, pp. 1163–1172, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Bellion, M. Olk, F. Will et al., “Formation of hydrogen peroxide in cell culture media by apple polyphenols and its effect on antioxidant biomarkers in the colon cell line HT29,” Molecular Nutrition & Food Research, vol. 53, no. 10, pp. 1226–1236, 2009. View at Publisher · View at Google Scholar
  52. L. H. Long, M. V. Clement, and B. Halliwell, “Artifacts in cell culture: rapid generation of hydrogen peroxide on addition of (−)-epigallocatechin, (−)-epigallocatechin gallate, (+)-catechin, and quercetin to commonly used cell culture media,” Biochemical and Biophysical Research Communications, vol. 273, no. 1, pp. 50–53, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. K. S. Suh, S. Chon, S. Oh et al., “Prooxidative effects of green tea polyphenol (−)-epigallocatethin-3-gallate on the HIT-T15 pancreatic beta cell line,” Cell Biology and Toxicology, vol. 26, no. 3, pp. 189–199, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. L. H. Long, D. Kirkland, J. Whitwell, and B. Halliwell, “Different cytotoxic and clastogenic effects of epigallocatechin gallate in various cell-culture media due to variable rates of its oxidation in the culture medium,” Mutation Research, vol. 634, no. 1-2, pp. 177–183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. M. López-Lázaro, J. M. Calderón-Montaño, E. Burgos-Morón, and C. A. Austin, “Green tea constituents (−)-epigallocatechin-3-gallate (EGCG) and gallic acid induce topoisomerase I- and topoisomerase II-DNA complexes in cells mediated by pyrogallol-induced hydrogen peroxide,” Mutagenesis, vol. 26, no. 4, pp. 489–498, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. I. A. Groh, A. T. Cartus, S. Vallicotti et al., “Genotoxic potential of methyleugenol and selected methyleugenol metabolites in cultured Chinese hamster V79 cells,” Food and Function, vol. 3, no. 4, pp. 428–436, 2012. View at Google Scholar
  57. A. T. Cartus, K. Hermann, L. W. Weishaupt, W. Engst, H. Glatt, and D. Schrenk, “Metabolism of methyleugenol in liver microsomes and primary hepatocytes: pattern of metabolites, cytotoxicity, and DNA-adduct formation,” Journal of Toxicological Sciences, vol. 129, no. 1, pp. 21–34, 2012. View at Publisher · View at Google Scholar
  58. J. L. Burkey, J. M. Sauer, C. A. McQueen, and I. Glenn Sipes, “Cytotoxicity and genotoxicity of methyleugenol and related congeners-a mechanism of activation for methyleugenol,” Mutation Research, vol. 453, no. 1, pp. 25–33, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Eot-Houllier, G. Fulcrand, L. Magnaghi-Jaulin, and C. Jaulin, “Histone deacetylase inhibitors and genomic instability,” Cancer Letters, vol. 274, no. 2, pp. 169–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. P. Rajendran, B. Delage, W. M. Dashwood et al., “Histone deacetylase turnover and recovery in sulforaphane-treated colon cancer cells: competing actions of 14-3-3 and Pin1 in HDAC3/SMRT corepressor complex dissociation/reassembly,” Molecular Cancer, vol. 10, p. 68, 2011. View at Publisher · View at Google Scholar · View at Scopus