Diet, Epigenetics, and Cancer

Part of the Methods in Molecular Biology book series (MIMB, volume 863)

Abstract

Cancer encompasses a highly heterogeneous group of diseases. It has been thought that transition from promotion to progression in carcinogenesis may be driven primarily by epigenetic abnormalities. Diet is known to play crucial roles in cancer etiology and has an important role in epigenetics. Current knowledge in the interrelationship among cancer, nutrition and epigenetics is reviewed.

Key words

Nutrition Epigenetics Cancer 

References

  1. 1.
    Loeb, L.A. and Harris, C.C. (2008) Advances in chemical carcinogenesis: a historical review and prospective. Cancer Res 68, 6863–6872.PubMedCrossRefGoogle Scholar
  2. 2.
    Pogribny, I.P., Shpyleva, S.I., Muskhelishvili, L., Bagnyukova, T.V., James, S.J., and Beland, F.A. (2009) Role of DNA damage and alterations in cytosine DNA methylation in rat liver carcinogenesis induced by a methyl-deficient diet. Mutat Res 669, 56–62.PubMedCrossRefGoogle Scholar
  3. 3.
    Pitot, H.C. (2007) Adventures in hepatocarcinogenesis. Annu Rev Pathol 2, 1–29.PubMedCrossRefGoogle Scholar
  4. 4.
    Duthie, S.J. (2011) Epigenetic modifications and human pathologies: cancer and CVD. Proc Nutr Soc 70, 47–56.PubMedCrossRefGoogle Scholar
  5. 5.
    Jones, P.A. and Baylin, S.B. (2007) The epigenomics of cancer. Cell 128, 683–692.PubMedCrossRefGoogle Scholar
  6. 6.
    Doll, R. and Peto, R. (1981) The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 66, 1191–308.PubMedGoogle Scholar
  7. 7.
    Issa, J.P. (2003) Age-related epigenetic changes and the immune system. Clin Immunol109, 103–108.PubMedCrossRefGoogle Scholar
  8. 8.
    Issa, J.P., Ottaviano, Y.L., Celano, P., Hamilton, S.R., Davidson, N.E., and Baylin, S.B. (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7, 536–540.PubMedCrossRefGoogle Scholar
  9. 9.
    Wolff, G.L., Kodell, R.L., Moore, S.R., and Cooney, C.A. (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12, 949–957.PubMedGoogle Scholar
  10. 10.
    Yen, T.T., Gill, A.M., Frigeri, L.G., Barsh, G.S., and Wolff, G.L. (1994) Obesity, diabetes, and neoplasia in yellow A(vy)/- mice: ectopic expression of the agouti gene. FASEB J 8, 479–488.PubMedGoogle Scholar
  11. 11.
    Dolinoy, D.C. (2008) The agouti mouse model: an epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr Rev, 66 Suppl 1, S7–11.PubMedCrossRefGoogle Scholar
  12. 12.
    Duthie, S.J. Epigenetic modifications and human pathologies: cancer and CVD. Proc Nutr Soc 70, 47–56.Google Scholar
  13. 13.
    Kim, K.C., Friso, S., and Choi, S.W. (2009) DNA methylation, an epigenetic mechanism connecting folate to healthy embryonic development and aging. J Nutr Biochem 20, 917–926.PubMedCrossRefGoogle Scholar
  14. 14.
    Fraga, M.F., Ballestar, E., Paz, M.F., Ropero, S., Setien, F., Ballestar, M.L., Heine-Suner, D., Cigudosa, J.C., Urioste, M., Benitez, J., Boix-Chornet, M., Sanchez-Aguilera, A., Ling, C., Carlsson, E., Poulsen, P., Vaag, A., Stephan, Z., Spector, T.D., Wu, Y.Z., Plass, C., and Esteller, M. (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102, 10604–10609.PubMedCrossRefGoogle Scholar
  15. 15.
    Davis, C.D. and Uthus, E.O. (2004) DNA methylation, cancer susceptibility, and nutrient interactions. Exp Biol Med (Maywood) 229, 988–995.Google Scholar
  16. 16.
    Lee, W.J., Shim, J.Y., and Zhu, B.T. (2005) Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids. Mol Pharmacol 68, 1018–1030.PubMedCrossRefGoogle Scholar
  17. 17.
    Delage, B. and Dashwood, R.H. (2008) Dietary manipulation of histone structure and function. Annu Rev Nutr 28, 347–366.PubMedCrossRefGoogle Scholar
  18. 18.
    Gilbert, E.R. and Liu, D. (2010) Flavonoids influence epigenetic-modifying enzyme activity: structure—function relationships and the therapeutic potential for cancer. Curr Med Chem 17, 1756–1768.PubMedCrossRefGoogle Scholar
  19. 19.
    Mas, S., Lafuente, M.J., Crescenti, A., Trias, M., Ballesta, A., Molina, R., Zheng, S., Wiencke, J.K., and Lafuente, A. (2007) Lower specific micronutrient intake in colorectal cancer patients with tumors presenting promoter hypermethylation in p16(INK4a), p4(ARF) and hMLH1. Anticancer Res 27, 1151–1156.PubMedGoogle Scholar
  20. 20.
    Ross, S.A., Dwyer, J., Umar, A., Kagan, J., Verma, M., Van Bemmel, D.M., and Dunn, B.K. (2008) Introduction: diet, epigenetic events and cancer prevention. Nutr Rev 66 Suppl 1, S1–6.PubMedCrossRefGoogle Scholar
  21. 21.
    Zhang, Y.W., Miao, Y.F., Yi, J., Geng, J., Wang, R., and Chen, L.B. (2010) Transcriptional inactivation of secreted frizzled-related protein 1 by promoter hypermethylation as a potential biomarker for non-small cell lung cancer. Neoplasma 57, 228–233.PubMedCrossRefGoogle Scholar
  22. 22.
    Rahman, I. (2008) Dietary polyphenols mediated regulation of oxidative stress and chromatin remodeling in inflammation. Nutr Rev, 66 Suppl 1, S42–45.PubMedCrossRefGoogle Scholar
  23. 23.
    Glynn, S.A. and Albanes, D. (1994) Folate and cancer: a review of the literature. Nutr Cancer 22, 101–119.PubMedCrossRefGoogle Scholar
  24. 24.
    Kim, Y.I. (2007) Folate and colorectal cancer: an evidence-based critical review. Mol Nutr Food Res 51, 267–292.PubMedCrossRefGoogle Scholar
  25. 25.
    Yang, Q., Bostick, R.M., Friedman, J.M., and Flanders, W.D. (2009) Serum folate and cancer mortality among U.S. adults: findings from the Third National Health and Nutritional Examination Survey linked mortality file. Cancer Epidemiol Biomarkers Prev 18, 1439–1447.PubMedCrossRefGoogle Scholar
  26. 26.
    Duthie, S.J. (2011) Folate and cancer: how DNA damage, repair and methylation impact on colon carcinogenesis. J Inherit Metab Dis 34, 101–109.PubMedCrossRefGoogle Scholar
  27. 27.
    Rampersaud, G.C., Kauwell, G.P., Hutson, A.D., Cerda, J.J., and Bailey, L.B. (2000) Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr 72, 998–1003.PubMedGoogle Scholar
  28. 28.
    Mason, J.B. and Choi, S.W. (2000) Folate and carcinogenesis: developing a unifying hypothesis. Adv Enzyme Regul 40, 127–141.PubMedCrossRefGoogle Scholar
  29. 29.
    Blount, B.C., Mack, M.M., Wehr, C.M., MacGregor, J.T., Hiatt, R.A., Wang, G., Wickramasinghe, S.N., Everson, R.B., and Ames, B.N. (1997) Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci U S A 94, 3290–3295.PubMedCrossRefGoogle Scholar
  30. 30.
    Choi, S.W., Friso, S., Dolnikowski, G.G., Bagley, P.J., Edmondson, A.N., Smith, D.E., and Mason, J.B. (2003) Biochemical and molecular aberrations in the rat colon due to folate depletion are age-specific. J Nutr 133, 1206–1212.PubMedGoogle Scholar
  31. 31.
    Shay, J.W. and Werbin, H. (1992) New evidence for the insertion of mitochondrial DNA into the human genome: significance for cancer and aging. Mutat Res 275, 227–235.PubMedCrossRefGoogle Scholar
  32. 32.
    Zhu, W., Qin, W., and Sauter, E.R. (2004) Large-scale mitochondrial DNA deletion mutations and nuclear genome instability in human breast cancer. Cancer Detect Prev 28, 119–126.PubMedCrossRefGoogle Scholar
  33. 33.
    Crott, J.W., Choi, S.W., Branda, R.F., and Mason, J.B. (2005) Accumulation of mitochondrial DNA deletions is age, tissue and folate-dependent in rats. Mutat Res 570, 63–70.PubMedCrossRefGoogle Scholar
  34. 34.
    Choi, S.W. and Mason, J.B. (2000) Folate and carcinogenesis: an integrated scheme. J Nutr 130, 129–132.PubMedGoogle Scholar
  35. 35.
    Eden, A., Gaudet, F., Waghmare, A., and Jaenisch, R. (2003) Chromosomal instability and tumors promoted by DNA hypomethylation. Science 300, 455.PubMedCrossRefGoogle Scholar
  36. 36.
    Gaudet, F., Hodgson, J.G., Eden, A., Jackson-Grusby, L., Dausman, J., Gray, J.W., Leonhardt, H., and Jaenisch, R. (2003) Induction of tumors in mice by genomic hypomethylation. Science 300, 489–492.PubMedCrossRefGoogle Scholar
  37. 37.
    Holm, T.M., Jackson-Grusby, L., Brambrink, T., Yamada, Y., Rideout, W.M., 3 rd and Jaenisch, R. (2005) Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell 8, 275–285.PubMedCrossRefGoogle Scholar
  38. 38.
    Walsh, C.P., Chaillet, J.R., and Bestor, T.H. (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20, 116–117.PubMedCrossRefGoogle Scholar
  39. 39.
    James, S.J., Pogribny, I.P., Pogribna, M., Miller, B.J., Jernigan, S., and Melnyk, S. (2003) Mechanisms of DNA damage, DNA hypomethylation, and tumor progression in the folate/methyl-deficient rat model of hepatocarcinogenesis. J Nutr 133, 3740 S–3747 S.PubMedGoogle Scholar
  40. 40.
    Arasaradnam, R.P., Commane, D.M., Bradburn, D., and Mathers, J.C. (2008) A review of dietary factors and its influence on DNA methylation in colorectal carcinogenesis. Epigenetics 3, 193–198.PubMedCrossRefGoogle Scholar
  41. 41.
    Weingartner, J., Lotz, K., Fanghanel, J., Gedrange, T., Bienengraber, V., and Proff, P. (2007) Induction and prevention of cleft lip, alveolus and palate and neural tube defects with special consideration of B vitamins and the methylation cycle. J Orofac Orthop 68, 266–277.PubMedCrossRefGoogle Scholar
  42. 42.
    Dunlevy, L.P., Burren, K.A., Mills, K., Chitty, L.S., Copp, A.J., and Greene, N.D. (2006) Integrity of the methylation cycle is essential for mammalian neural tube closure. Birth Defects Res A Clin Mol Teratol 76, 544–552.PubMedCrossRefGoogle Scholar
  43. 43.
    Park, B.H., Kim, Y.J., Park, J.S., Lee, H.Y., Ha, E.H., Min, J.W., and Park, H.S. (2005) (Folate and homocysteine levels during pregnancy affect DNA methylation in human placenta). J Prev Med Public Health 38, 437–442.PubMedGoogle Scholar
  44. 44.
    Kim, J.M., Hong, K., Lee, J.H., Lee, S., and Chang, N. (2009) Effect of folate deficiency on placental DNA methylation in hyperhomocysteinemic rats. J Nutr Biochem 20, 172–6.PubMedCrossRefGoogle Scholar
  45. 45.
    Watkins, A.J., Wilkins, A., Cunningham, C., Perry, V.H., Seet, M.J., Osmond, C., Eckert, J.J., Torrens, C., Cagampang, F.R., Cleal, J., Gray, W.P., Hanson, M.A., and Fleming, T.P. (2008) Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol 586, 2231–2244.PubMedCrossRefGoogle Scholar
  46. 46.
    Lillycrop, K.A., Phillips, E.S., Jackson, A.A., Hanson, M.A., and Burdge, G.C. (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135, 1382–1386.PubMedGoogle Scholar
  47. 47.
    Kappen, C. (2005) Folate supplementation in three genetic models: implications for understanding folate-dependent developmental pathways. Am J Med Genet C Semin Med Genet 135 C, 24–30.PubMedCrossRefGoogle Scholar
  48. 48.
    Lillycrop, K.A., Slater-Jefferies, J.L., Hanson, M.A., Godfrey, K.M., Jackson, A.A., and Burdge, G.C. (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97, 1064–1073.PubMedCrossRefGoogle Scholar
  49. 49.
    Sinclair, K.D., Allegrucci, C., Singh, R., Gardner, D.S., Sebastian, S., Bispham, J., Thurston, A., Huntley, J.F., Rees, W.D., Maloney, C.A., Lea, R.G., Craigon, J., McEvoy, T.G., and Young, L.E. (2007) DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A 104, 19351–19356.PubMedCrossRefGoogle Scholar
  50. 50.
    Waterland, R.A. and Michels, K.B. (2007) Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr 27, 363–388.PubMedCrossRefGoogle Scholar
  51. 51.
    McKay, J.A., Williams, E.A., and Mathers, J.C. (2004) Folate and DNA methylation during in utero development and aging. Biochem Soc Trans 32, 1006–7.PubMedCrossRefGoogle Scholar
  52. 52.
    Giovannucci, E., Stampfer, M.J., Colditz, G.A., Rimm, E.B., Trichopoulos, D., Rosner, B.A., Speizer, F.E., and Willett, W.C. (1993) Folate, methionine, and alcohol intake and risk of colorectal adenoma. J Natl Cancer Inst 85, 875–884.PubMedCrossRefGoogle Scholar
  53. 53.
    Sohn, K.J., Jang, H., Campan, M., Weisenberger, D.J., Dickhout, J., Wang, Y.C., Cho, R.C., Yates, Z., Lucock, M., Chiang, E.P., Austin, R.C., Choi, S.W., Laird, P.W., and Kim, Y.I. (2009) The methylenetetrahydrofolate reductase C677T mutation induces cell-specific changes in genomic DNA methylation and uracil misincorporation: a possible molecular basis for the site-specific cancer risk modification. Int J Cancer 124, 1999–2005.PubMedCrossRefGoogle Scholar
  54. 54.
    van den Donk, M., Pellis, L., Crott, J.W., van Engeland, M., Friederich, P., Nagengast, F.M., van Bergeijk, J.D., de Boer, S.Y., Mason, J.B., Kok, F.J., Keijer, J., and Kampman, E. (2007) Folic acid and vitamin B-12 supplementation does not favorably influence uracil incorporation and promoter methylation in rectal mucosa DNA of subjects with previous colorectal adenomas. J Nutr 137, 2114–2120.PubMedGoogle Scholar
  55. 55.
    Choi, S.W., Friso, S., Keyes, M.K., and Mason, J.B. (2005) Folate supplementation increases genomic DNA methylation in the liver of elder rats. Br J Nutr 93, 31–35.PubMedCrossRefGoogle Scholar
  56. 56.
    Keyes, M.K., Jang, H., Mason, J.B., Liu, Z., Crott, J.W., Smith, D.E., Friso, S., and Choi, S.W. (2007) Older age and dietary folate are determinants of genomic and p16-specific DNA methylation in mouse colon. J Nutr 137, 1713–1717.PubMedGoogle Scholar
  57. 57.
    Herrmann, W., Schorr, H., Obeid, R., and Geisel, J. (2003) Vitamin B-12 status, particularly holotranscobalamin II and methylmalonic acid concentrations, and hyperhomocysteinemia in vegetarians. Am J Clin Nutr 78, 131–136.PubMedGoogle Scholar
  58. 58.
    Bissoli, L., Di Francesco, V., Ballarin, A., Mandragona, R., Trespidi, R., Brocco, G., Caruso, B., Bosello, O., and Zamboni, M. (2002) Effect of vegetarian diet on homocysteine levels. Ann Nutr Metab 46, 73–79.PubMedCrossRefGoogle Scholar
  59. 59.
    Yi, P., Melnyk, S., Pogribna, M., Pogribny, I.P., Hine, R.J., and James, S.J. (2000) Increase in plasma homocysteine associated with parallel increases in plasma S-adenosylhomocysteine and lymphocyte DNA hypomethylation. J Biol Chem 275, 29318–29323.PubMedCrossRefGoogle Scholar
  60. 60.
    Comin-Anduix, B., Boren, J., Martinez, S., Moro, C., Centelles, J.J., Trebukhina, R., Petushok, N., Lee, W.N., Boros, L.G., and Cascante, M. (2001) The effect of thiamine supplementation on tumour proliferation. A metabolic control analysis study. Eur J Biochem 268, 4177–4182.PubMedCrossRefGoogle Scholar
  61. 61.
    Duthie, G.G., Duthie, S.J., and Kyle, J.A. (2000) Plant polyphenols in cancer and heart disease: implications as nutritional antioxidants. Nutr Res Rev 13, 79–106.PubMedCrossRefGoogle Scholar
  62. 62.
    Ferguson, L.R. (2001) Role of plant polyphenols in genomic stability. Mutat Res 475, 89–111.PubMedCrossRefGoogle Scholar
  63. 63.
    Duthie, S.J. (2007) Berry phytochemicals, genomic stability and cancer: evidence for chemoprotection at several stages in the carcinogenic process. Mol Nutr Food Res 51, 665–674.PubMedCrossRefGoogle Scholar
  64. 64.
    Fang, M., Chen, D., and Yang, C.S. (2007) Dietary polyphenols may affect DNA methylation. J Nutr 137, 223 S–228 S.PubMedGoogle Scholar
  65. 65.
    Fang, M.Z., Wang, Y., Ai, N., Hou, Z., Sun, Y., Lu, H., Welsh, W., and Yang, C.S. (2003) Tea polyphenol (−)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res 63, 7563–7570.PubMedGoogle Scholar
  66. 66.
    Fang, M.Z., Chen, D., Sun, Y., Jin, Z., Christman, J.K., and Yang, C.S. (2005) Reversal of hypermethylation and reactivation of p16INK4a, RARbeta, and MGMT genes by genistein and other isoflavones from soy. Clin Cancer Res 11, 7033–7041.PubMedCrossRefGoogle Scholar
  67. 67.
    Kato, K., Long, N.K., Makita, H., Toida, M., Yamashita, T., Hatakeyama, D., Hara, A., Mori, H., and Shibata, T. (2008) Effects of green tea polyphenol on methylation status of RECK gene and cancer cell invasion in oral squamous cell carcinoma cells. Br J Cancer 99, 647–654.PubMedCrossRefGoogle Scholar
  68. 68.
    Chuang, J.C., Yoo, C.B., Kwan, J.M., Li, T.W., Liang, G., Yang, A.S., and Jones, P.A. (2005) Comparison of biological effects of non-nucleoside DNA methylation inhibitors versus 5-aza-2′-deoxycytidine. Mol Cancer Ther 4, 1515–1520.PubMedCrossRefGoogle Scholar
  69. 69.
    Stresemann, C., Brueckner, B., Musch, T., Stopper, H., and Lyko, F. (2006) Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines. Cancer Res 66, 2794–2800.PubMedCrossRefGoogle Scholar
  70. 70.
    Lu, H., Meng, X., Li, C., Sang, S., Patten, C., Sheng, S., Hong, J., Bai, N., Winnik, B., Ho, C.T., and Yang, C.S. (2003) Glucuronides of tea catechins: enzymology of biosynthesis and biological activities. Drug Metab Dispos 31, 452–461.PubMedCrossRefGoogle Scholar
  71. 71.
    Christman, J.K. (2002) 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21, 5483–5495.PubMedCrossRefGoogle Scholar
  72. 72.
    Adlercreutz, H., Mousavi, Y., and Hockerstedt, K. (1992) Diet and breast cancer. Acta Oncol 31, 175–181.PubMedCrossRefGoogle Scholar
  73. 73.
    Dijsselbloem, N., Vanden Berghe, W., De Naeyer, A., and Haegeman, G. (2004) Soy isoflavone phyto-pharmaceuticals in interleukin-6 affections. Multi-purpose nutraceuticals at the crossroad of hormone replacement, anti-cancer and anti-inflammatory therapy. Biochem Pharmacol 68, 1171–1185.PubMedCrossRefGoogle Scholar
  74. 74.
    Woodson, K., Weisenberger, D.J., Campan, M., Laird, P.W., Tangrea, J., Johnson, L.L., Schatzkin, A., and Lanza, E. (2005) Gene-specific methylation and subsequent risk of colorectal adenomas among participants of the polyp prevention trial. Cancer Epidemiol Biomarkers Prev 14, 1219–1223.PubMedCrossRefGoogle Scholar
  75. 75.
    Ottaviano, Y.L., Issa, J.P., Parl, F.F., Smith, H.S., Baylin, S.B., and Davidson, N.E. (1994) Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54, 2552–2555.PubMedGoogle Scholar
  76. 76.
    Juge, N., Mithen, R.F., and Traka, M. (2007) Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci 64, 1105–1127.PubMedCrossRefGoogle Scholar
  77. 77.
    Myzak, M.C. and Dashwood, R.H. (2006) Chemoprotection by sulforaphane: keep one eye beyond Keap1. Cancer Lett 233, 208–218.PubMedCrossRefGoogle Scholar
  78. 78.
    Dashwood, R.H., and Ho, E. (2008) Dietary agents as histone deacetylase inhibitors: sulforaphane and structurally related isothiocyanates. Nutr Rev 66 Suppl 1, S36–38.PubMedCrossRefGoogle Scholar
  79. 79.
    Myzak, M.C., Karplus, P.A., Chung, F.L., and Dashwood, R.H. (2004) A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 64, 5767–5774.PubMedCrossRefGoogle Scholar
  80. 80.
    Myzak, M.C., Hardin, K., Wang, R., Dashwood, R.H., and Ho, E. (2006) Sulforaphane inhibits histone deacetylase activity in BPH-1, LnCaP and PC-3 prostate epithelial cells. Carcinogenesis 27, 811–819.PubMedCrossRefGoogle Scholar
  81. 81.
    Pledgie-Tracy, A., Sobolewski, M.D., and Davidson, N.E. (2007) Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol Cancer Ther 6, 1013–1021.PubMedCrossRefGoogle Scholar
  82. 82.
    Myzak, M.C., Tong, P., Dashwood, W.M., Dashwood, R.H., and Ho, E. (2007) Sulforaphane retards the growth of human PC-3 xenografts and inhibits HDAC activity in human subjects. Exp Biol Med (Maywood) 232, 227–234.Google Scholar
  83. 83.
    Myzak, M.C., Dashwood, W.M., Orner, G.A., Ho, E., and Dashwood, R.H. (2006) Sulforaphane inhibits histone deacetylase in vivo and suppresses tumorigenesis in Apc-minus mice. FASEB J 20, 506–508.PubMedGoogle Scholar
  84. 84.
    Ho, E., Clarke, J.D., and Dashwood, R.H. (2009) Dietary sulforaphane, a histone deacetylase inhibitor for cancer prevention. J Nutr 139, 2393–2396.PubMedCrossRefGoogle Scholar
  85. 85.
    Rowling, M.J., McMullen, M.H., and Schalinske, K.L. (2002) Vitamin A and its derivatives induce hepatic glycine N-methyltransferase and hypomethylation of DNA in rats. J Nutr 132, 365–369.PubMedGoogle Scholar
  86. 86.
    de Assis, S., Wang, M., Goel, S., Foxworth, A., Helferich, W., and Hilakivi-Clarke, L. (2006) Excessive weight gain during pregnancy increases carcinogen-induced mammary tumorigenesis in Sprague-Dawley and lean and obese Zucker rats. J Nutr 136, 998–1004.PubMedGoogle Scholar
  87. 87.
    Fernandez-Twinn, D.S., Ekizoglou, S., Gusterson, B.A., Luan, J., and Ozanne, S.E. (2007) Compensatory mammary growth following protein restriction during pregnancy and lactation increases early-onset mammary tumor incidence in rats. Carcinogenesis 28, 545–552.PubMedCrossRefGoogle Scholar
  88. 88.
    Esquela-Kerscher, A., and Slack, F.J. (2006) Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer 6, 259–269.PubMedCrossRefGoogle Scholar
  89. 89.
    Sood, P., Krek, A., Zavolan, M., Macino, G., and Rajewsky, N. (2006) Cell-type-specific signatures of microRNAs on target mRNA expression. Proc Natl Acad Sci U S A 103, 2746–2751.PubMedCrossRefGoogle Scholar
  90. 90.
    Michael, M.Z., SM, O.C., van Holst Pellekaan, N.G., Young, G.P., and James, R.J. (2003) Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 1, 882–891.Google Scholar
  91. 91.
    Akao, Y., Nakagawa, Y., and Naoe, T. (2006) let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharm Bull 29, 903–906.PubMedCrossRefGoogle Scholar
  92. 92.
    Bandres, E., Cubedo, E., Agirre, X., Malumbres, R., Zarate, R., Ramirez, N., Abajo, A., Navarro, A., Moreno, I., Monzo, M., and Garcia-Foncillas, J. (2006) Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer 5, 29.PubMedCrossRefGoogle Scholar
  93. 93.
    Monzo, M., Navarro, A., Bandres, E., Artells, R., Moreno, I., Gel, B., Ibeas, R., Moreno, J., Martinez, F., Diaz, T., Martinez, A., Balague, O., and Garcia-Foncillas, J. (2008) Overlapping expression of microRNAs in human embryonic colon and colorectal ­cancer. Cell Res 18, 823–833.PubMedCrossRefGoogle Scholar
  94. 94.
    Schepeler, T., Reinert, J.T., Ostenfeld, M.S., Christensen, L.L., Silahtaroglu, A.N., Dyrskjot, L., Wiuf, C., Sorensen, F.J., Kruhoffer, M., Laurberg, S., Kauppinen, S., Orntoft, T.F., and Andersen, C.L. (2008) Diagnostic and prognostic microRNAs in stage II colon cancer. Cancer Res 68, 6416–6424.PubMedCrossRefGoogle Scholar
  95. 95.
    Cheng, A.M., Byrom, M.W., Shelton, J., and Ford, L.P. (2005) Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33, 1290–1297.PubMedCrossRefGoogle Scholar
  96. 96.
    Carthew, R.W. (2006) Gene regulation by microRNAs. Curr Opin Genet Dev 16, 203–208.PubMedCrossRefGoogle Scholar
  97. 97.
    Grady, W.M., Parkin, R.K., Mitchell, P.S., Lee, J.H., Kim, Y.H., Tsuchiya, K.D., Washington, M.K., Paraskeva, C., Willson, J.K., Kaz, A.M., Kroh, E.M., Allen, A., Fritz, B.R., Markowitz, S.D., and Tewari, M. (2008) Epigenetic silencing of the intronic microRNA hsa-miR-342 and its host gene EVL in colorectal cancer. Oncogene 27, 3880–3888.PubMedCrossRefGoogle Scholar
  98. 98.
    Davidson, L.A., Wang, N., Shah, M.S., Lupton, J.R., Ivanov, I., and Chapkin, R.S. (2009) n-3 Polyunsaturated fatty acids modulate carcinogen-directed non-coding microRNA signatures in rat colon. Carcinogenesis 30, 2077–2084.PubMedCrossRefGoogle Scholar
  99. 99.
    Cooney, C.A. (2001) Dietary selenium and arsenic affect DNA methylation. J Nutr 131, 1871–1872.PubMedGoogle Scholar
  100. 100.
    Clark, L.C., Cantor, K.P., and Allaway, W.H. (1991) Selenium in forage crops and cancer mortality in U.S. counties. Arch Environ Health 46, 37–42.PubMedCrossRefGoogle Scholar
  101. 101.
    Davis, C.D., Uthus, E.O., and Finley, J.W. (2000) Dietary selenium and arsenic affect DNA methylation in vitro in Caco-2 cells and in vivo in rat liver and colon. J Nutr,130, 2903–2909.PubMedGoogle Scholar
  102. 102.
    Fiala, E.S., Staretz, M.E., Pandya, G.A., El-Bayoumy, K., and Hamilton, S.R. (1998) Inhibition of DNA cytosine methyltransferase by chemopreventive selenium compounds, determined by an improved assay for DNA cytosine methyltransferase and DNA cytosine methylation. Carcinogenesis 19, 597–604.PubMedCrossRefGoogle Scholar
  103. 103.
    Dashwood, R.H., Myzak, M.C., and Ho, E. (2006) Dietary HDAC inhibitors: time to rethink weak ligands in cancer chemoprevention? Carcinogenesis 27, 344–349.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Division of Cancer Controls and Population SciencesNational Cancer InstituteRockvilleUSA

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