Effects of Dietary Nutrients on Epigenetic Changes in Cancer

  • Nicoleta Andreescu
  • Maria Puiu
  • Mihai Niculescu
Part of the Methods in Molecular Biology book series (MIMB, volume 1856)


Gene–nutrient interactions are important contributors to health management and disease prevention. Nutrition can alter gene expression, as well as the susceptibility to disease, including cancer, through epigenetic changes. Nutrients can influence the epigenetic status through several mechanisms, such as DNA methylation, histone modifications, and miRNA-dependent gene silencing. These alterations were associated with either increased or decreased risk for cancer development. There is convincing evidence indicating that several foods have protective roles in cancer prevention, by inhibiting tumor progression directly or through modifying tumor’s microenvironment that leads to hostile conditions favorable to tumor initiation or growth. While nutritional intakes from foods cannot be adequately controlled for dosage, the role of nutrients in the epigenetics of cancer has led to more research aimed at developing nutriceuticals and drugs as cancer therapies. Clinical studies are needed to evaluate the optimum doses of dietary compounds, the safety profile of dosages, to establish the most efficient way of administration, and bioavailability, in order to maximize the beneficial effects already discovered, and to ensure replicability. Thus, nutrition represents a promising tool to be used not only in cancer prevention, but hopefully also in cancer treatment.

Key words

Epigenetics Nutrition Nutriepigenomics Cancer Epigenetic diet 



The work was funded, in part, by POSCCE Project ID: 1854, cod SMIS: 48749, contract 677/09.04.2015, and by POC Project Nutrigen, SMIS: 104852, contract 91/09.09.2016, ID P_37-684.


  1. 1.
    Kussmann M, Fay LB (2008) Nutrigenomics and personalized nutrition: science and concept. Pers Med 5(5):447–455Google Scholar
  2. 2.
    Meeran SM, Ahmed A, Tollefsbol TO (2010) Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin Epigenetics 1(3–4):101–116Google Scholar
  3. 3.
    Issa JP (2008) Cancer prevention: epigenetics steps up to the plate. Cancer Prev Res (Phila Pa) 1(4):219–222Google Scholar
  4. 4.
    Suter MA, Aagaard-Tillery KM (2009) Environmental influences on epigenetic profiles. Semin Reprod Med 27(5):380–390Google Scholar
  5. 5.
    Herceg Z (2009) Epigenetics and cancer: towards an evaluation of the impact of environmental and dietary factors. Mutagenesis 22(2):91–103Google Scholar
  6. 6.
    Junien C (2006) Impact of diets and nutrients/drugs on early epigenetic programming. J Inherit Metab Dis 29(2–3):359–365Google Scholar
  7. 7.
    Dolinoy DC, Weidman JR, Jirtle RL (2007) Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol 23(3):297–307Google Scholar
  8. 8.
    Landis-Piwowar KR, Milacic V, Dou QP (2008) Relationship between the methylation status of dietary flavonoids and their growth-inhibitory and apoptosis-inducing activities in human cancer cells. J Cell Biochem 105(2):514–523Google Scholar
  9. 9.
    Li Y, Tollefsbol TO (2010) Impact on DNA methylation in cancer prevention and therapy by bioactive dietary components. Curr Med Chem 17(20):2141–2151Google Scholar
  10. 10.
    Paluszczak J, Krajka-Kuźniak V, Baer-Dubowska W (2010) The effect of dietary polyphenols on the epigenetic regulation of gene expression in MCF7 breast cancer cells. Toxicol Lett 192(2):119–125Google Scholar
  11. 11.
    Majid S, Kikuno N, Nelles J, Noonan E, Tanaka Y, Kawamoto K, Hirata H, Li LC, Zhao H, Okino ST, Place RF, Pookot D, Dahiya R (2008) Genistein induces the p21WAF1/CIP1 and p16INK4a tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification. Cancer Res 68(8):2736–2734Google Scholar
  12. 12.
    Esteller M (2007) Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 8(4):286–298Google Scholar
  13. 13.
    Ducasse M, Brown MA (2006) Epigenetic aberrations and cancer. Mol Cancer 5:60Google Scholar
  14. 14.
    Doll R, Peto R (1981) The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 66(6):1191–1308Google Scholar
  15. 15.
    Lundstrom K (2014) Nutritional influence on epigenetics and disease. Austin Publ Group, New Jersey 1(3):1014Google Scholar
  16. 16.
    Li Y, Tollefsbol TO (2011) p16(INK4a) suppression by glucose restriction contributes to human cellular lifespan extension through SIRT1-mediated epigenetic and genetic mechanisms. PLoS One 6(2):e17421Google Scholar
  17. 17.
    Meeran SM, Patel SN, Tollefsbol TO (2010) Sulforaphane causes epigenetic repression of hTERT expression in human breast cancer cell lines. PLoS One 5(7):e11457Google Scholar
  18. 18.
    Ross SA, Davis CD (2011) MicroRNA, nutrition, and cancer prevention. Adv Nutr 2(6):472–485Google Scholar
  19. 19.
    Ong TP, Moreno FS, Ross SA (2011) Targeting the epigenome with bioactive food components for cancer prevention. J Nutrigenet Nutrigenomics 4(5):275–292Google Scholar
  20. 20.
    World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. RR Donnelley, IllinoisGoogle Scholar
  21. 21.
    Donaldson MS (2004) Nutrition and cancer: a review of the evidence for an anti-cancer diet. Nutr J 3(1):19 Available from: Scholar
  22. 22.
    Zhang N (2015) Epigenetic modulation of DNA methylation by nutrition and its mechanisms in animals. Anim Nutr 1(3):144–151Google Scholar
  23. 23.
    Altmann S, Murani E, Schwerin M, Metges CC, Wimmers K, Ponsuksili S (2012) Somatic cytochrome c (CYCS) gene expression and promoter-specific DNA methylation in a porcine model of prenatal exposure to maternal dietary protein excess and restriction. Br J Nutr 107(6):791–799Google Scholar
  24. 24.
    Dudley KJ, Sloboda DM, Connor KL, Beltrand J, Vickers MH (2011) Offspring of mothers fed a high fat diet display hepatic cell cycle inhibition and associated changes in gene expression and DNA methylation. PLoS One 6(7):e21662Google Scholar
  25. 25.
    Jousse C, Parry L, Lambert-Langlais S, Maurin A-C, Averous J, Bruhat A, Carraro V, Tost J, Letteron P, Chen P, Jockers R, Launay JM, Mallet J, Fafournoux P (2011) Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome. FASEB J 25(9):3271–3278Google Scholar
  26. 26.
    Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13(2):97–109Google Scholar
  27. 27.
    Zeisel SH (2009) Epigenetic mechanisms for nutrition determinants of later health outcomes. Am J Clin Nutr 89(5):1488S–1493SGoogle Scholar
  28. 28.
    Cheng X, Blumenthal RM (2008) Mammalian DNA methyltransferases: a structural perspective. Structure 16(3):341–350Google Scholar
  29. 29.
    Niculescu MD, Lupu DS (2011) Nutritional influence on epigenetics and effects on longevity. Curr Opin Clin Nutr Metab Care 14(1):35–40Google Scholar
  30. 30.
    Wajed SA, Laird PW, DeMeester TR (2001) DNA methylation: an alternative pathway to cancer. Ann Surg 234:1):10–1):20Google Scholar
  31. 31.
    Liao Y-P, Chen L-Y, Huang R-L, Su P-H, Chan MWY, Chang C-C, Yu MH, Wang PH, Yen MS, Nephew KP, Lai HC (2014) Hypomethylation signature of tumor-initiating cells predicts poor prognosis of ovarian cancer patients. Hum Mol Genet 23(7):1894–1906Google Scholar
  32. 32.
    Yang X, Yan L, Davidson NE (2001) DNA methylation in breast cancer. Endocr Relat Cancer 8(2):115–127Google Scholar
  33. 33.
    Daniel M, Tollefsbol TO (2015) Epigenetic linkage of aging, cancer and nutrition. J Exp Biol 218(1):59–70Google Scholar
  34. 34.
    Bishop KS, Ferguson LR (2015) The interaction between epigenetics, nutrition and the development of cancer. Nutrients 7(2):922–947Google Scholar
  35. 35.
    Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349(21):2042–2054Google Scholar
  36. 36.
    Singhal RP, Mays-Hoopes LL, Eichhorn GL (1987) DNA methylation in aging of mice. Mech Ageing Dev 41(3):199–210Google Scholar
  37. 37.
    Cheng JC, Matsen CB, Gonzales FA, Ye W, Greer S, Marquez VE, Jones PA, Selker EU (2003) Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J Natl Cancer Inst 95(5):399–409Google Scholar
  38. 38.
    Hughes LA, van den Brandt PA, de Bruïne AP, Wouters KAD, Hulsmans S, Spiertz A, Goldbohm RA, de Goeij AF, Herman JG, Weijenberg MP, van Engeland M (2009) Early life exposure to famine and colorectal cancer risk: a role for epigenetic mechanisms. PLoS One 4(11):e7951Google Scholar
  39. 39.
    Issa J-P (2004) CpG island methylator phenotype in cancer. Nat Rev Cancer 4(12):988–993Google Scholar
  40. 40.
    Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105(44):17046–17049Google Scholar
  41. 41.
    Pembrey M, Saffery R, Bygren LO (2014) Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research. J Med Genet 51:563–572Google Scholar
  42. 42.
    Kyle UG, Pichard C (2006) The Dutch famine of 1944-1945: a pathophysiological model of long-term consequences of wasting disease. Curr Opin Clin Nutr Metab Care 9(4):388–394Google Scholar
  43. 43.
    Lillycrop KA, Burdge GC (2012) Epigenetic mechanisms linking early nutrition to long term health. Best Pract Res Clin Endocrinol Metab 26(5):667–676Google Scholar
  44. 44.
    Teegarden D, Romieu I, Lelièvre SA (2012) Redefining the impact of nutrition on breast cancer incidence: is epigenetics involved? Nutr Res Rev 25(1):68–95Google Scholar
  45. 45.
    Yamaji T, Inoue M, Sasazuki S, Iwasaki M, Kurahashi N, Shimazu T, Tsugane S, Japan Public Health Center-based Prospective Study Group (2008) Fruit and vegetable consumption and squamous cell carcinoma of the esophagus in Japan: the JPHC study. Int J Cancer 123(8):1935–1940Google Scholar
  46. 46.
    Whitehead N, Reyner F, Lindenbaum J (1989) The journal of the American Medical Association: Megaloblastic changes in cervical epithelium. Association with oral contraceptive therapy and reversal with folic acid. Nutr Rev 47(10):318–321Google Scholar
  47. 47.
    Shrubsole MJ, Shu XO, Li HL, Cai H, Yang G, Gao YT, Gao J, Zheng W (2011) Dietary B vitamin and methionine intakes and breast cancer risk among Chinese women. Am J Epidemiol 173(10):1171–1182Google Scholar
  48. 48.
    Maruti SS, Ulrich CM, White E (2009) Folate and one-carbon metabolism nutrients from supplements and diet in relation to breast cancer risk. Am J Clin Nutr 89(2):624–633Google Scholar
  49. 49.
    Singh SM, Murphy B, O’Reilly RL (2003) Involvement of gene-diet/drug interaction in DNA methylation and its contribution to complex diseases: from cancer to schizophrenia. Clin Genet 64(6):451–460Google Scholar
  50. 50.
    Stefanska B, Karlic H, Varga F, Fabianowska-Majewska K, Haslberger A (2012) Epigenetic mechanisms in anti-cancer actions of bioactive food components—the implications in cancer prevention. Br J Pharmacol 167:279–297Google Scholar
  51. 51.
    van den Donk M, Pellis L, Crott JW, van Engeland M, Friederich P, Nagengast FM, van Bergeijk JD, de Boer SY, Mason JB, Kok FJ, Keijer J, 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(9):2114–2120Google Scholar
  52. 52.
    Supic G, Jagodic M, Magic Z (2013) Epigenetics: a new link between nutrition and cancer. Nutr Cancer 65(6):781–792Google Scholar
  53. 53.
    Selhub J (2002) Folate, vitamin B12 and vitamin B6 and one carbon metabolism. J Nutr Health Aging 6(1):39–42Google Scholar
  54. 54.
    Wei EK, Giovannucci E, Selhub J, Fuchs CS, Hankinson SE, Ma J (2005) Plasma vitamin B6 and the risk of colorectal cancer and adenoma in women. J Natl Cancer Inst 97(9):684–692Google Scholar
  55. 55.
    Mandal S, Davie JR (2010) Estrogen regulated expression of the p21 Waf1/Cip1 gene in estrogen receptor positive human breast cancer cells. J Cell Physiol 224(1):28–32Google Scholar
  56. 56.
    Fang MZ, Chen D, Sun Y, Jin Z, Christman JK, Yang CS (2005) Reversal of hypermethylation and reactivation of p16INK4a, RARbeta, and MGMT genes by genistein and other isoflavones from soy. Clin cancer res off J am Assoc. Cancer Res 11(19 Pt 1):7033–7041Google Scholar
  57. 57.
    Chung J-H, Ostrowski MC, Romigh T, Minaguchi T, Waite KA, Eng C (2006) The ERK1/2 pathway modulates nuclear PTEN-mediated cell cycle arrest by cyclin D1 transcriptional regulation. Hum Mol Genet 15(17):2553–2559Google Scholar
  58. 58.
    Olthof MR, Hollman PC, Zock PL, Katan MB (2001) Consumption of high doses of chlorogenic acid, present in coffee, or of black tea increases plasma total homocysteine concentrations in humans. Am J Clin Nutr 73(3):532–538Google Scholar
  59. 59.
    Goel A, Aggarwal BB (2010) Curcumin, the golden spice from Indian saffron, is a chemosensitizer and radiosensitizer for tumors and chemoprotector and radioprotector for normal organs. Nutr Cancer 62(7):919–930Google Scholar
  60. 60.
    Maheshwari RK, Singh AK, Gaddipati J, Srimal RC (2006) Multiple biological activities of curcumin: a short review. Life Sci 78(18):2081–2087Google Scholar
  61. 61.
    Liu Z, Xie Z, Jones W, Pavlovicz RE, Liu S, Yu J, Li PK, Lin J, Fuchs JR, Marcucci G, Li C, Chan KK (2009) Curcumin is a potent DNA hypomethylation agent. Bioorg Med Chem Lett 19(3):706–709Google Scholar
  62. 62.
  63. 63.
    Kouzarides TBS (2007) Chromatin modifications and their mechanism of action. In: Allis CD, Jenuwein T, Reinberg D (eds) Epigenetics. Cold Spring Harbor Press, New York, pp 191–209Google Scholar
  64. 64.
    Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395Google Scholar
  65. 65.
    Su LJ, Mahabir S, Ellison GL, McGuinn LA, Reid BC (2012) Epigenetic contributions to the relationship between cancer and dietary intake of nutrients, bioactive food components, and Environmental Toxicants. Front Genet 2:91 Available from: Scholar
  66. 66.
    Cohen I, Poreba E, Kamieniarz K, Schneider R (2011) Histone modifiers in cancer: friends or foes? Genes Cancer 2(6):631–647Google Scholar
  67. 67.
    Kuroishi T, Rios-Avila L, Pestinger V, Wijeratne SSK, Zempleni J (2011) Biotinylation is a natural, albeit rare, modification of human histones. Mol Genet Metab 104(4):537–545Google Scholar
  68. 68.
    Morimoto T, Sunagawa Y, Kawamura T, Takaya T, Wada H, Nagasawa A, Komeda M, Fujita M, Shimatsu A, Kita T, Hasegawa K (2008) The dietary compound curcumin inhibits p300 histone acetyltransferase activity and prevents heart failure in rats. J Clin Invest 118(3):868–878Google Scholar
  69. 69.
    Boily G, Seifert EL, Bevilacqua L, He XH, Sabourin G, Estey C, Moffat C, Crawford S, Saliba S, Jardine K, Xuan J, Evans M, Harper ME, McBurney MW (2008) SirT1 regulates energy metabolism and response to caloric restriction in mice. PLoS One 3(3):e1759Google Scholar
  70. 70.
    Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, Su H, Sun W, Chang H, Xu G, Gaudet F, Li E, Chen T (2009) The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 41(1):125–129Google Scholar
  71. 71.
    Mariadason JM (2009) HDACs and HDAC inhibitors in colon cancer. Epigenetics 3(1):28–37Google Scholar
  72. 72.
    Nian H, Delage B, Ho E, Dashwood RH (2009) Modulation of histone deacetylase activity by dietary isothiocyanates and allyl sulfides: studies with sulforaphane and garlic organosulfur compounds. Environ Mol Mutagen 50(3):213–221Google Scholar
  73. 73.
    Druesne-Pecollo N, Latino-Martel P (2011) Modulation of histone acetylation by garlic sulfur compounds. Anti Cancer Agents Med Chem 11(3):254–259Google Scholar
  74. 74.
    Dashwood RH, Ho E (2007) Dietary histone deacetylase inhibitors: from cells to mice to man. Semin Cancer Biol 17(5):363–369Google Scholar
  75. 75.
    Attoub S, Hassan AH, Vanhoecke B, Iratni R, Takahashi T, Gaben A-M, Bracke M, Awad S, John A, Kamalboor HA, Al Sultan MA, Arafat K, Gespach C, Petroianu G (2011) Inhibition of cell survival, invasion, tumor growth and histone deacetylase activity by the dietary flavonoid luteolin in human epithelioid cancer cells. Eur J Pharmacol 651(1–3):18–25Google Scholar
  76. 76.
    Cheng X, Blumenthal RM (2010) Coordinated chromatin control: structural and functional linkage of DNA and histone methylation. Biochemistry (Mosc) 49(14):2999–3008Google Scholar
  77. 77.
    Kang J, Chen J, Shi Y, Jia J, Zhang Y (2005) Curcumin-induced histone hypoacetylation: the role of reactive oxygen species. Biochem Pharmacol 69(8):1205–1213Google Scholar
  78. 78.
    Chung S, Yao H, Caito S, Hwang J-W, Arunachalam G, Rahman I (2010) Regulation of SIRT1 in cellular functions: role of polyphenols. Arch Biochem Biophys 501(1):79–90Google Scholar
  79. 79.
    Tili E, Michaille J-J, Alder H, Volinia S, Delmas D, Latruffe N (2010) Resveratrol modulates the levels of microRNAs targeting genes encoding tumor-suppressors and effectors of TGFβ signaling pathway in SW480 cells. Biochem Pharmacol 80(12):2057–2065Google Scholar
  80. 80.
    Khanim FL, Gommersall LM, Wood VHJ, Smith KL, Montalvo L, O’Neill LP, Xu Y, Peehl DM, Stewart PM, Turner BM, Campbell MJ (2010) Altered SMRT levels disrupt vitamin D3 receptor signalling in prostate cancer cells. Oncogene 23(40):6712–6725Google Scholar
  81. 81.
    Gao Y, Tollefsbol T (2015) Impact of epigenetic dietary components on cancer through histone modifications. Curr Med Chem 22(17):2051–2064Google Scholar
  82. 82.
    Li Y, Yuan Y-Y, Meeran SM, Tollefsbol TO (2010) Synergistic epigenetic reactivation of estrogen receptor-α (ERα) by combined green tea polyphenol and histone deacetylase inhibitor in ERα-negative breast cancer cells. Mol Cancer 9:274Google Scholar
  83. 83.
    Lopez-Serra P, Esteller M (2012) DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 31(13):1609–1622Google Scholar
  84. 84.
    Liloglou T, Bediaga NG, Brown BRB, Field JK, Davies MPA (2014) Epigenetic biomarkers in lung cancer. Cancer Lett 342(2):200–212Google Scholar
  85. 85.
    Toraño EG, Fernandez AF, Urdinguio RG, Fraga MF (2014) Role of epigenetics in neural differentiation: implications for health and disease. In: Maulik N, Karagiannis T (eds) Molecular mechanisms and physiology of disease. Springer, New York, pp 63–79 Available from: Scholar
  86. 86.
    Ferdin J, Kunej T, Calin GA (2010) Non-coding RNAs: identification of cancer-associated microRNAs by gene profiling. Technol Cancer Res Treat 9(2):123–138Google Scholar
  87. 87.
    Gavrilas L, Ionescu C, Tudoran O, Lisencu C, Balacescu O, Miere D (2016) The role of bioactive dietary components in modulating miRNA expression in colorectal cancer. Nutrients 8:590Google Scholar
  88. 88.
    Slattery M, Herrick J, Mullany L, Stevens J, Wolff R (2016) Diet and lifestyle factors associated with miRNA expression in colorectal tissue. Pharmacogenomics Pers Med 10:1–16Google Scholar
  89. 89.
    Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, Jacob ST, Ghoshal K (2006) Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem 99(3):671–678Google Scholar
  90. 90.
    Wang L-L, Zhang Z, Li Q, Yang R, Pei X, Xu Y, Wang J, Zhou SF, Li Y (2009) Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum Reprod 24(3):562–579Google Scholar
  91. 91.
    Parasramka MA, Ho E, Williams DE, Dashwood RH (2012) MicroRNAs, diet, and cancer: new mechanistic insights on the epigenetic actions of phytochemicals. Mol Carcinog 51(3):213–230Google Scholar
  92. 92.
    Saini S, Majid S, Dahiya R (2010) Diet, microRNAs and prostate cancer. Pharm Res 27(6):1014–1026Google Scholar
  93. 93.
    Sun M, Estrov Z, Ji Y, Coombes KR, Harris DH, Kurzrock R (2008) Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol Cancer Ther 7:464–473Google Scholar
  94. 94.
    Yang J, Cao Y, Sun J, Zhang Y (2010) Curcumin reduces the expression of Bcl-2 by upregulating miR-15a and miR-16 in MCF-7 cells. Med Oncol 27(4):1114–1118Google Scholar
  95. 95.
    Sun Q, Cong R, Yan H, Gu H, Zeng Y, Liu N (2009) Genistein inhibits growth of human uveal melanoma cells and affects microRNA-27a and target gene expression. Oncol Rep 22:563–567Google Scholar
  96. 96.
    Panagiotakos D, Sitara M, Pitsavos C, Stefanadis C (2007) Estimating the 10-year risk of cardiovascular disease and its economic consequences, by the level of adherence to the Mediterranean diet: the ATTICA study. J Med Food 10(2):239–243Google Scholar
  97. 97.
    Komduur RH, Korthals M, te Molder H (2009) The good life: living for health and a life without risks? On a prominent script of nutrigenomics. Br J Nutr 101(3):307–316Google Scholar
  98. 98.
    Elsamanoudy AZ, Neamat-Allah MAM, Mohammad FAH, Hassanien M, Nada HA (2016) The role of nutrition related genes and nutrigenetics in understanding the pathogenesis of cancer. J Microsc Ultrastruct 4(3):115–122Google Scholar
  99. 99.
    Béliveau R, Gingras D (2007) Role of nutrition in preventing cancer. Can Fam Physician 53(11):1905–1911Google Scholar
  100. 100.
    Ames BN, Gold LS, Willett WC (1995) The causes and prevention of cancer. Proc Natl Acad Sci U S A 92(12):5258–5265Google Scholar
  101. 101.
    Ioannides C, Lewis DFV (2004) Cytochromes P450 in the bioactivation of chemicals. Curr Top Med Chem 4(16):1767–1788Google Scholar
  102. 102.
    Conney AH (2003) Enzyme induction and dietary chemicals as approaches to cancer chemoprevention: the seventh DeWitt S. Goodman Lecture. Cancer Res 63(21):7005–7031Google Scholar
  103. 103.
    Lamy S, Gingras D, Béliveau R (2002) Green tea catechins inhibit vascular endothelial growth factor receptor phosphorylation. Cancer Res 62(2):381–385Google Scholar
  104. 104.
    Béliveau R, Gingras D (2004) Green tea: prevention and treatment of cancer by nutraceuticals. Lancet 364(9439):1021–1022Google Scholar
  105. 105.
    Shanafelt TD, Lee YK, Call TG, Nowakowski GS, Dingli D, Zent CS, Kay NE (2006) Clinical effects of oral green tea extracts in four patients with low grade B-cell malignancies. Leuk Res 30(6):707–712Google Scholar
  106. 106.
    Labrecque L, Lamy S, Chapus A, Mihoubi S, Durocher Y, Cass B, Bojanowski MW, Gingras D, Béliveau R (2005) Combined inhibition of PDGF and VEGF receptors by ellagic acid, a dietary-derived phenolic compound. Carcinogenesis 26(4):821–826Google Scholar
  107. 107.
    Lamy S, Blanchette M, Michaud-Levesque J, Lafleur R, Durocher Y, Moghrabi A, Barrette S, Gingras D, Béliveau R (2006) Delphinidin, a dietary anthocyanidin, inhibits vascular endothelial growth factor receptor-2 phosphorylation. Carcinogenesis 27(5):989–996Google Scholar
  108. 108.
    Hardy TM, Tollefsbol TO (2006) Epigenetic diet: impact on the epigenome and cancer. Epigenomics 3(4):503–518Google Scholar
  109. 109.
    Aykan NF (2015) Red meat and colorectal cancer. Oncol Rev 9(1):288 Available from: Scholar
  110. 110.
    Oostindjer M, Alexander J, Amdam GV, Andersen G, Bryan NS, Chen D, Corpet DE, De Smet S, Dragsted LO, Haug A, Karlsson AH, Kleter G, de Kok TM, Kulseng B, Milkowski AL, Martin RJ, Pajari AM, Paulsen JE, Pickova J, Rudi K, Sødring M, Weed DL, Egelandsdal B (2015) The role of red and processed meat in colorectal cancer development: a perspective. Meat Sci 97(4):583–596Google Scholar
  111. 111.
    Joosen AMCP, Kuhnle GGC, Aspinall SM, Barrow TM, Lecommandeur E, Azqueta A, Collins AR, Bingham SA (2009) Effect of processed and red meat on endogenous nitrosation and DNA damage. Carcinogenesis 30(8):1402–1407Google Scholar
  112. 112.
    Ijssennagger N, Rijnierse A, de Wit NJW, Boekschoten MV, Dekker J, Schonewille A, Müller M, van der Meer R (2013) Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon. Carcinogenesis 34(7):1628–1635Google Scholar
  113. 113.
    Bastide NM, Pierre FHF, Corpet DE (2011) Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res (Phila Pa) 4(2):177–184Google Scholar
  114. 114.
    Sugimura T (2000) Nutrition and dietary carcinogens. Carcinogenesis 21(3):387–395Google Scholar
  115. 115.
    Frentzel-Beyme R, Helmert U (2000) Association between malignant tumors of the thyroid gland and exposure to environmental protective and risk factors. Rev Environ Health 5(3):337–358Google Scholar
  116. 116.
    Kohlmeier M (2013) Nutrigenetics: applying the science of personal nutrition [Internet]. Academic, Oxford. Available from: Scholar
  117. 117.
    Camp KM, Trujillo E (2014) Position of the academy of nutrition and dietetics: nutritional genomics. J Acad Nutr Diet 114(2):299–312Google Scholar
  118. 118.
    Yong W-S, Hsu F-M, Chen P-Y (2016) Profiling genome-wide DNA methylation. Epigenetics Chromatin [Internet]; 9. Available from:
  119. 119.
    Busch C, Burkard M, Leischner C, Lauer UM, Frank J, Venturelli S (2015) Epigenetic activities of flavonoids in the prevention and treatment of cancer. Clin Epigenetics 7:64 Available from: Scholar
  120. 120.
    Chakravarty S, Bhat UA, Reddy RG, Gupta P, Kumar A (2014) Histone Deacetylase inhibitors and psychiatric disorders. In: Epigenetics in psychiatry. Elsevier, New York, pp 515–544 Available from: Scholar
  121. 121.
    Peedicayil J (2014) Epigenetic drugs for multiple sclerosis. Curr Neuropharmacol 4(1):3–9Google Scholar
  122. 122.
    Gilbert ER, Liu D (2010) Flavonoids influence epigenetic-modifying enzyme activity: structure—function relationships and the therapeutic potential for cancer. Curr Med Chem 17(17):1756–1768Google Scholar
  123. 123.
    Rajendran P, Williams DE, Ho E, Dashwood RH (2011) Metabolism as a key to histone deacetylase inhibition. Crit Rev Biochem Mol Biol 46(3):181–199Google Scholar
  124. 124.
    Haberland M, Montgomery RL, Olson EN (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10(1):32–42Google Scholar
  125. 125.
    Poole RM (2014) Belinostat: first global approval. Drugs 74(13):1543–1554Google Scholar
  126. 126.
    Garnock-Jones KP (2015) Panobinostat: first global approval. Drugs 75(6):695–704Google Scholar
  127. 127.
    Rodríguez-Paredes M, Esteller M (2011) Cancer epigenetics reaches mainstream oncology. Nat Med 17(3):330–339Google Scholar
  128. 128.
    Chang LC, Yu YL (2016) Dietary components as epigenetic-regulating agents against cancer. BioMedicine 6(1):2 Available from: Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Nicoleta Andreescu
    • 1
  • Maria Puiu
    • 1
  • Mihai Niculescu
    • 1
    • 2
  1. 1.Medical Genetics Discipline, Center of Genomic MedicineUniversity of Medicine and Pharmacy “Victor Babes”TimisoaraRomania
  2. 2.Advanced NutrigenomicsHillsboroughUSA

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