Advertisement

DNA Methylation in Anti-cancer Effects of Dietary Catechols and Stilbenoids: An Overview of Underlying Mechanisms

  • Megan Beetch
  • Barbara Stefanska
Reference work entry

Abstract

Carcinogenesis involves an accumulation of genetic mutations and epigenetic alterations. DNA methylation, a dynamic epigenetic modification, may underlie genomic instability, silencing of genes with tumor suppressor functions, and activation of genes associated with cancer progression. Therefore, reversing DNA methylation patterns established during carcinogenesis constitutes a promising anti-cancer strategy. Interestingly, studies have indicated that certain dietary polyphenols, such as those from catechol and stilbenoid classes present in grapes, blueberries, and green tea, exert anti-cancer effects through epigenetic regulation of gene expression. A basis of evidence demonstrating the importance of DNA methylation in cancer formation and progression as well as the impact of catechol and stilbenoid compounds on these events are presented in this review. In vitro and in vivo evidence for the chemopreventive and therapeutic potential of polyphenols through their influence on DNA methylation is discussed. Current mechanistic insights on the changes in DNA methylation machinery upon exposure to polyphenols are further emphasized. Such studies are ongoing and crucially needed for transition into application of polyphenols as agents in cancer prevention and/or treatment in the clinical setting.

Keywords

DNA methylation Epigenetics Bioactive Polyphenols Catechols Stilbenoids Epigallocatechin gallate Resveratrol Pterostilbene Chemoprevention Cancer Carcinogenesis 

List of Abbreviations

AP-1

Activator protein 1

APC

Adenotamous polyposis coli

ATM

Ataxia telangiectasia mutated

ATR

Ataxia telangiectasia and rad3-related protein

BRCA1

Breast cancer 1

CDK

Cyclin-dependent kinase

CHK1/2

Checkpoint kinase 1/2

COMT

Catechol-O-methyltransferase

DNA

Deoxyribonucleic acid

DNMT

DNA methyltransferase

EGCG

Epigallocatechin gallate

EMT

Epithelial-to-mesenchymal transtion

ER

Estrogen receptor

EXOSC4

Exosome component 4

GSTP1

Glutathione S-transferase pi 1

HCC

Hepatocellular carcinoma

HDAC

Histone deacetylase

IGF2

Insulin-like growth factor 2

MAML2

Mastermind-like transcriptional coactivator 2

MAPK

Mitogen-activated protein kinase

MBD2

Methyl-CpG-binding domain 2

MMP

Matrix metalloproteinase

MTHFR

Methylenetetrahydrofolate reductase

NENF

Neuron-derived neurotrophic factor

NF-κB

Nuclear factor kappa B

OCT1

Octamer-binding transcription factor 1

PCNA

Proliferating cell nuclear antigen

PI3K/Akt

Phosphatidylinositol-4,5-bisphosphate 3-kinase/protein kinase B

PTEN

Phosphatase and tensin homolog

RASAL2

Ras-GTPase-activating protein 2

RASSF-1α

Ras association domain family member 1

RNA

Ribonucleic acid

RXRα

Retinoid X receptor A

SAH

S-adenosyl-L-homocysteine

SAM

S-adenosyl-L-methionine

SENP6

SUMO1/sentrin-specific peptidase 6

STAT3

Signal transducer and activator 3

TNF

Tumor necrosis factor

TRAMP

Transgenic adenocarcinoma of the mouse prostate

TYMS

Thymidylate synthase

VEGF

Vascular endothelial growth factor

WBSCR22

Williams-Beuren syndrome chromosome region 22

References

  1. Aires V, Delmas D (2015) Common pathways in health benefit properties of RSV in cardiovascular diseases, cancers and degenerative pathologies. Curr Pharm Biotechnol 16(3):219–244CrossRefPubMedGoogle Scholar
  2. Allen E, Walters IB, Hanahan D (2011) Brivanib, a dual FGF/VEGF inhibitor, is active both first and second line against mouse pancreatic neuroendocrine tumors developing adaptive/evasive resistance to VEGF inhibition. Clin Cancer Res 17(16):5299–5310CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anderson OS, Sant KE, Dolinoy DC (2012) Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 23(8):853–859CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ardaens Y, Renan CA (1993) Modern imaging of ovarian cysts. Contracep Fertil Sex 21(4): 321–324Google Scholar
  5. Arts IC, Hollman PC (2005) Polyphenols and disease risk in epidemiologic studies. Am J Clin Nutr 81(1 Suppl):317S–325SCrossRefPubMedGoogle Scholar
  6. Baylin S (2001) DNA methylation and epigenetic mechanisms of carcinogenesis. Dev Biol 106:85–87. discussion 143–160Google Scholar
  7. Berkyurek AC, Suetake I, Arita K et al (2014) The DNA methyltransferase Dnmt1 directly interacts with the SET and RING finger-associated (SRA) domain of the multifunctional protein Uhrf1 to facilitate accession of the catalytic center to hemi-methylated DNA. J Biol Chem 289(1): 379–386CrossRefPubMedGoogle Scholar
  8. Bigey P, Ramchandani S, Theberge J, Araujo FD, Szyf M (2000) Transcriptional regulation of the human DNA Methyltransferase (dnmt1) gene. Gene 242(1–2):407–418CrossRefPubMedGoogle Scholar
  9. Burns J, Yokota T, Ashihara H, Lean ME, Crozier A (2002) Plant foods and herbal sources of resveratrol. J Agric Food Chem 50(11):3337–3340CrossRefGoogle Scholar
  10. Carter LG, D’Orazio JA, Pearson KJ (2014) Resveratrol and cancer: focus on in vivo evidence. Endocr Relat Cancer 21(3):R209–R225CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10(5):295–304CrossRefPubMedGoogle Scholar
  12. Chen T, Li E (2004) Structure and function of eukaryotic DNA methyltransferases. Curr Top Dev Biol 60:55–89CrossRefPubMedGoogle Scholar
  13. Chiurillo MA (2015) Role of the Wnt/beta-catenin pathway in gastric cancer: an in-depth literature review. World J Exp Med 5(2):84–102CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF (1997) Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277(5334):1996–2000CrossRefPubMedGoogle Scholar
  15. Chung JH, 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):2553–2559CrossRefPubMedGoogle Scholar
  16. Collisson EA, Sadanandam A, Olson P et al (2011) Subtypes of pancreatic ductal adenocarcinoma and their differin5g responses to therapy. Nat Med 17(4):500–503CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dhar S, Kumar A, Zhang L et al (2016) Dietary pterostilbene is a novel MTA1-targeted chemopreventive and therapeutic agent in prostate cancer. Oncotarget 7(14):18469–18484CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dickinson D, Yu H, Ohno S et al (2014) Epigallocatechin-3-gallate prevents autoimmune-associated downregulation of p21 in salivary gland cells through a p53-independent pathway. Inflammation & allergy drug targets 13:15–24CrossRefGoogle Scholar
  19. Duan J, Yue W, JianYu E et al (2016) In vitro comparative studies of resveratrol and triacetylresveratrol on cell proliferation, apoptosis, and STAT3 and NFkappaB signaling in pancreatic cancer cells. Sci Rep 6:31672CrossRefPubMedPubMedCentralGoogle Scholar
  20. El-Mowafy AM, El-Mesery ME, Salem HA, Al-Gayyar MM, Darweish MM (2010) Prominent chemopreventive and chemoenhancing effects for resveratrol: unraveling molecular targets and the role of C-reactive protein. Chemotherapy 56(1):60–65CrossRefPubMedGoogle Scholar
  21. Esteller M, Fraga MF, Guo M et al (2001) DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum Mol Genet 10(26):3001–3007CrossRefPubMedGoogle Scholar
  22. Fini L, Piazzi G, Daoud Y et al (2011) Chemoprevention of intestinal polyps in ApcMin/+ mice fed with western or balanced diets by drinking annurca apple polyphenol extract. Cancer Prev Res 4(6):907–915CrossRefGoogle Scholar
  23. Galamb O, Kalmar A, Peterfia B et al (2016) Aberrant DNA methylation of WNT pathway genes in the development and progression of CIMP-negative colorectal cancer. Epigenetics 11(8): 588–602CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gallagher JC, Baylink DJ, Freeman R, McClung M (2001) Prevention of bone loss with tibolone in postmenopausal women: results of two randomized, double-blind, placebo-controlled, dose-finding studies. J Clin Endocrinol Metab 86(10):4717–4726CrossRefPubMedGoogle Scholar
  25. Giacosa A (2004) The Mediterranean diet and its protective role against cancer. Eur J Cancer Prev 13(3):155–157CrossRefPubMedGoogle Scholar
  26. Grosso G, Buscemi S, Galvano F et al (2013) Mediterranean diet and cancer: epidemiological evidence and mechanism of selected aspects. BMC Surg 13(Suppl 2):S14CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gruenbaum Y, Stein R, Cedar H, Razin A (1981) Methylation of CpG sequences in eukaryotic DNA. FEBS Lett 124(1):67–71CrossRefPubMedGoogle Scholar
  28. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674CrossRefGoogle Scholar
  29. Hata K, Okano M, Lei H, Li E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129(8):1983–1993PubMedGoogle Scholar
  30. Hatada I, Fukasawa M, Kimura M et al (2006) Genome-wide profiling of promoter methylation in human. Oncogene 25(21):3059–3064CrossRefPubMedGoogle Scholar
  31. Henning SM, Wang P, Carpenter CL, Heber D (2013) Epigenetic effects of green tea polyphenols in cancer. Epigenomics 5(6):729–741CrossRefPubMedPubMedCentralGoogle Scholar
  32. Herman JG, Baylin SB (2001) Methylation-specific PCR. Curr Protoc Hum Genet. Chapter 10:Unit 10 16Google Scholar
  33. Howells LM, Berry DP, Elliott PJ et al (2011) Phase I randomized, double-blind pilot study of micronized resveratrol (SRT501) in patients with hepatic metastases – safety, pharmacokinetics, and pharmacodynamics. Cancer Prev Res 4(9):1419–1425CrossRefGoogle Scholar
  34. Huderson AC, Myers JN, Niaz MS, Washington MK, Ramesh A (2013) Chemoprevention of benzo(a)pyrene-induced colon polyps in ApcMin mice by resveratrol. J Nutr Biochem 24(4):713–724CrossRefPubMedGoogle Scholar
  35. Iida T, Suetake I, Tajima S et al (2002) PCNA clamp facilitates action of DNA cytosine methyltransferase 1 on hemimethylated DNA. Genes Cells 7(10):997–1007CrossRefPubMedGoogle Scholar
  36. Imai K, Suga K, Nakachi K (1997) Cancer-preventive effects of drinking green tea among a Japanese population. Prev Med 26(6):769–775CrossRefPubMedGoogle Scholar
  37. Jain S, Chang TT, Hamilton JP et al (2011) Methylation of the CpG sites only on the sense strand of the APC gene is specific for hepatocellular carcinoma. PLoS One 6(11):e26799CrossRefPubMedPubMedCentralGoogle Scholar
  38. James SJ, Pogribny IP, Pogribna M, Miller BJ, Jernigan S, Melnyk S (2003) Mechanisms of DNA damage, DNA hypomethylation, and tumor progression in the folate/methyl-deficient rat model of hepatocarcinogenesis. J Nutr 133(11 Suppl 1):3740S–3747SCrossRefPubMedGoogle Scholar
  39. Jang M, Cai L, Udeani GO et al (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275(5297):218–220CrossRefPubMedGoogle Scholar
  40. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13(7):484–492CrossRefPubMedGoogle Scholar
  41. Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293(5532):1068–1070CrossRefGoogle Scholar
  42. Kala R, Shah HN, Martin SL, Tollefsbol TO (2015) Epigenetic-based combinatorial resveratrol and pterostilbene alters DNA damage response by affecting SIRT1 and DNMT enzyme expression, including SIRT1-dependent gamma-H2AX and telomerase regulation in triple-negative breast cancer. BMC Cancer 15:672CrossRefPubMedPubMedCentralGoogle Scholar
  43. Khan N, Mukhtar H (2013) Modulation of signaling pathways in prostate cancer by green tea polyphenols. Biochem Pharmacol 85(5):667–672CrossRefPubMedGoogle Scholar
  44. Khan MA, Hussain A, Sundaram MK et al (2015) (−)-Epigallocatechin-3-gallate reverses the expression of various tumor-suppressor genes by inhibiting DNA methyltransferases and histone deacetylases in human cervical cancer cells. Oncol Rep 33(4):1976–1984CrossRefPubMedGoogle Scholar
  45. Lao VV, Grady WM (2011) Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol 8(12):686–700CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lee WJ, Zhu BT (2006) Inhibition of DNA methylation by caffeic acid and chlorogenic acid, two common catechol-containing coffee polyphenols. Carcinogenesis 27(2):269–277CrossRefPubMedGoogle Scholar
  47. Lee WJ, Shim JY, Zhu BT (2005) Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids. Mol Pharmacol 68(4):1018–1030CrossRefPubMedGoogle Scholar
  48. Lee HS, Ha AW, Kim WK (2012a) Effect of resveratrol on the metastasis of 4T1 mouse breast cancer cells in vitro and in vivo. Nutr Res Pract 6(4):294–300CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lee H, Zhang P, Herrmann A et al (2012b) Acetylated STAT3 is crucial for methylation of tumor-suppressor gene promoters and inhibition by resveratrol results in demethylation. Proc Natl Acad Sci U S A 109(20):7765–7769CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lee H, Kim Y, Jeong JH, Ryu JH, Kim WY (2016) ATM/CHK/p53 pathway dependent chemopreventive and therapeutic activity on lung cancer by Pterostilbene. PLoS One 11(9):e0162335CrossRefPubMedPubMedCentralGoogle Scholar
  51. Li X, Mohan S, Gu W, Wergedal J, Baylink DJ (2001) Quantitative assessment of forearm muscle size, forelimb grip strength, forearm bone mineral density, and forearm bone size in determining humerus breaking strength in 10 inbred strains of mice. Calcif Tissue Int 68(6):365–369CrossRefPubMedGoogle Scholar
  52. Li Y, Yuan YY, Meeran SM, Tollefsbol TO (2010) Synergistic epigenetic reactivation of estrogen receptor-alpha (ERalpha) by combined green tea polyphenol and histone deacetylase inhibitor in ERalpha-negative breast cancer cells. Mol Cancer 9:274CrossRefPubMedPubMedCentralGoogle Scholar
  53. Li K, Dias SJ, Rimando AM et al (2013) Pterostilbene acts through metastasis-associated protein 1 to inhibit tumor growth, progression and metastasis in prostate cancer. PLoS One 8(3):e57542CrossRefPubMedPubMedCentralGoogle Scholar
  54. Li S, Wu L, Feng J et al (2016) In vitro and in vivo study of epigallocatechin-3-gallate-induced apoptosis in aerobic glycolytic hepatocellular carcinoma cells involving inhibition of phosphofructokinase activity. Sci Rep 6:28479CrossRefPubMedPubMedCentralGoogle Scholar
  55. Liu HT, Gao P (2016) The roles of microRNAs related with progression and metastasis in human cancers. Tumour Biol 37:15383-15397Google Scholar
  56. Liu B, Song J, Luan J et al (2016) Promoter methylation status of tumor suppressor genes and inhibition of expression of DNA methyltransferase 1 in non-small cell lung cancer. Exp Biol Med (Maywood) 241(14):1531–1539CrossRefGoogle Scholar
  57. Lubecka K, Kurzava L, Flower K et al (2016) Stilbenoids remodel the DNA methylation patterns in breast cancer cells and inhibit oncogenic NOTCH signaling through epigenetic regulation of MAML2 transcriptional activity. Carcinogenesis 37(7):656–668CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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):28–32PubMedGoogle Scholar
  59. Manna SK, Mukhopadhyay A, Aggarwal BB (2000) Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. J Immunol 164(12):6509–6519CrossRefPubMedGoogle Scholar
  60. Martinez-Quetglas I, Pinyol R, Dauch D et al (2016) IGF2 is Upregulated by epigenetic mechanisms in hepatocellular carcinomas and is an actionable oncogene product in experimental models. Gastroenterology 151:1192CrossRefPubMedGoogle Scholar
  61. McCormack D, Schneider J, McDonald D, McFadden D (2011) The antiproliferative effects of pterostilbene on breast cancer in vitro are via inhibition of constitutive and leptin-induced Janus kinase/signal transducer and activator of transcription activation. Am J Surg 202(5):541–544CrossRefPubMedGoogle Scholar
  62. Medina-Aguilar R, Perez-Plasencia C, Marchat LA et al (2016) Methylation landscape of human breast cancer cells in response to dietary compound resveratrol. PLoS One 11(6):e0157866CrossRefPubMedPubMedCentralGoogle Scholar
  63. Mialon MM, Camous S, Renand G, Martal J, Menissier F (1993) Peripheral concentrations of a 60-kDa pregnancy serum protein during gestation and after calving and in relationship to embryonic mortality in cattle. Reprod Nutr Dev 33(3):269–282CrossRefPubMedGoogle Scholar
  64. Mittal A, Piyathilake C, Hara Y, Katiyar SK (2003) Exceptionally high protection of photocarcinogenesis by topical application of (−)-epigallocatechin-3-gallate in hydrophilic cream in SKH-1 hairless mouse model: relationship to inhibition of UVB-induced global DNA hypomethylation. Neoplasia 5(6):555–565CrossRefPubMedPubMedCentralGoogle Scholar
  65. Myung SK, Bae WK, Oh SM et al (2009) Green tea consumption and risk of stomach cancer: a meta-analysis of epidemiologic studies. Int J Cancer 124(3):670–677CrossRefPubMedGoogle Scholar
  66. Nguyen AV, Martinez M, Stamos MJ et al (2009) Results of a phase I pilot clinical trial examining the effect of plant-derived resveratrol and grape powder on Wnt pathway target gene expression in colonic mucosa and colon cancer. Cancer Manag Res 1:25–37CrossRefPubMedPubMedCentralGoogle Scholar
  67. Niles RM, Cook CP, Meadows GG, Fu YM, McLaughlin JL, Rankin GO (2006) Resveratrol is rapidly metabolized in athymic (nu/nu) mice and does not inhibit human melanoma xenograft tumor growth. J Nutr 136(10):2542–2546CrossRefPubMedPubMedCentralGoogle Scholar
  68. Nishikawa T, Nakajima T, Moriguchi M et al (2006) A green tea polyphenol, epigalocatechin-3-gallate, induces apoptosis of human hepatocellular carcinoma, possibly through inhibition of Bcl-2 family proteins. J Hepatol 44(6):1074–1082CrossRefPubMedGoogle Scholar
  69. 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 73:532–538CrossRefPubMedGoogle Scholar
  70. Pandey M, Shukla S, Gupta S (2010) Promoter demethylation and chromatin remodeling by green tea polyphenols leads to re-expression of GSTP1 in human prostate cancer cells. Int J Cancer 126(11):2520–2533PubMedPubMedCentralGoogle Scholar
  71. Pere H, Montier Y, Bayry J et al (2011) A CCR4 antagonist combined with vaccines induces antigen-specific CD8+ T cells and tumor immunity against self antigens. Blood 118(18): 4853–4862CrossRefPubMedGoogle Scholar
  72. Pethe V, Shekhar PV (1999) Estrogen inducibility of c-Ha-ras transcription in breast cancer cells. Identification of functional estrogen-responsive transcriptional regulatory elements in exon 1/intron 1 of the c-Ha-ras gene. J Biol Chem 274(43):30969–30978CrossRefPubMedGoogle Scholar
  73. Qin W, Zhang K, Clarke K, Weiland T, Sauter ER (2014) Methylation and miRNA effects of resveratrol on mammary tumors vs. normal tissue. Nutr Cancer 66(2):270–277CrossRefPubMedGoogle Scholar
  74. Razin A (1998) CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 17(17):4905–4908CrossRefPubMedPubMedCentralGoogle Scholar
  75. Renan MJ (1993) How many mutations are required for tumorigenesis? Implications from human cancer data. Mol Carcinog 7(3):139–146CrossRefPubMedGoogle Scholar
  76. Renan R, Freire VN, Auto MM, Farias GA (1993) Transmission coefficient of electrons through a single graded barrier. Phy Rev B Condens Matter 48(11):8446–8449CrossRefGoogle Scholar
  77. Romagnolo DF, Papoutsis AJ, Laukaitis C, Selmin OI (2015) Constitutive expression of AhR and BRCA-1 promoter CpG hypermethylation as biomarkers of ERalpha-negative breast tumorigenesis. BMC Cancer 15:1026CrossRefPubMedPubMedCentralGoogle Scholar
  78. Salvesen HB, MacDonald N, Ryan A et al (2001) PTEN methylation is associated with advanced stage and microsatellite instability in endometrial carcinoma. Int J Cancer 91(1):22–26CrossRefPubMedGoogle Scholar
  79. Shariati-Kohbanani M, Zare-Bidaki M, Taghavi MM et al (2016) DNA methylation and microRNA patterns are in association with the expression of BRCA1 in ovarian cancer. Cell Mol Biol (Noisy-le-Grand, France) 62(1):16–23Google Scholar
  80. Sharma S, Kelly TK, Jones PA (2010) Epigenetics in cancer. Carcinogenesis 31(1):27–36CrossRefPubMedGoogle Scholar
  81. Shin YS, Kang SU, Park JK et al (2016) Anti-cancer effect of (−)-epigallocatechin-3-gallate (EGCG) in head and neck cancer through repression of transactivation and enhanced degradation of beta-catenin. Phytomedicine 23(12):1344–1355CrossRefPubMedGoogle Scholar
  82. Shirakami Y, Shimizu M, Adachi S et al (2009) (−)-Epigallocatechin gallate suppresses the growth of human hepatocellular carcinoma cells by inhibiting activation of the vascular endothelial growth factor-vascular endothelial growth factor receptor axis. Cancer Sci 100(10):1957–1962CrossRefPubMedGoogle Scholar
  83. Singh B, Shoulson R, Chatterjee A et al (2014) Resveratrol inhibits estrogen-induced breast carcinogenesis through induction of NRF2-mediated protective pathways. Carcinogenesis 35(8):1872–1880CrossRefPubMedPubMedCentralGoogle Scholar
  84. Sinha D, Sarkar N, Biswas J, Bishayee A (2016) Resveratrol for breast cancer prevention and therapy: preclinical evidence and molecular mechanisms. Semin Cancer Biol 40-41:209–232CrossRefPubMedGoogle Scholar
  85. Sodir NM, Swigart LB, Karnezis AN, Hanahan D, Evan GI, Soucek L (2011) Endogenous Myc maintains the tumor microenvironment. Genes Dev 25(9):907–916CrossRefPubMedPubMedCentralGoogle Scholar
  86. Srivastava AK, MacFarlane G, Srivastava VP, Mohan S, Baylink DJ (2001a) A new monoclonal antibody ELISA for detection and characterization of C-telopeptide fragments of type I collagen in urine. Calcif Tissue Int 69(6):327–336CrossRefPubMedGoogle Scholar
  87. Srivastava AK, Bhattacharyya S, Li X, Mohan S, Baylink DJ (2001b) Circadian and longitudinal variation of serum C-telopeptide, osteocalcin, and skeletal alkaline phosphatase in C3H/HeJ mice. Bone 29(4):361–367CrossRefPubMedGoogle Scholar
  88. Stefanska B, Rudnicka K, Bednarek A, Fabianowska-Majewska K (2010) Hypomethylation and induction of retinoic acid receptor beta 2 by concurrent action of adenosine analogues and natural compounds in breast cancer cells. Eur J Pharmacol 638(1–3):47–53CrossRefPubMedGoogle Scholar
  89. Stefanska B, Huang J, Bhattacharyya B et al (2011) Definition of the landscape of promoter DNA hypomethylation in liver cancer. Cancer Res 71(17):5891–5903CrossRefPubMedGoogle Scholar
  90. 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(2):279–297CrossRefPubMedPubMedCentralGoogle Scholar
  91. Stefanska B, Suderman M, Machnes Z, Bhattacharyya B, Hallett M, Szyf M (2013) Transcription onset of genes critical in liver carcinogenesis is epigenetically regulated by methylated DNA-binding protein MBD2. Carcinogenesis 34(12):2738–2749CrossRefPubMedGoogle Scholar
  92. Stefanska B, Cheishvili D, Suderman M et al (2014) Genome-wide study of hypomethylated and induced genes in patients with liver cancer unravels novel anticancer targets. Clin Cancer Res 20(12):3118–3132CrossRefPubMedGoogle Scholar
  93. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403(6765): 41–45CrossRefGoogle Scholar
  94. Sun CL, Yuan JM, Koh WP, Yu MC (2006) Green tea, black tea and colorectal cancer risk: a meta-analysis of epidemiologic studies. Carcinogenesis 27(7):1301–1309CrossRefPubMedGoogle Scholar
  95. Szyf M, Pakneshan P, Rabbani SA (2004) DNA methylation and breast cancer. Biochem Pharmacol 68(6):1187–1197CrossRefPubMedGoogle Scholar
  96. Tsai CL, Li HP, Lu YJ et al (2006) Activation of DNA methyltransferase 1 by EBV LMP1 involves c-Jun NH(2)-terminal kinase signaling. Cancer Res 66(24):11668–11676CrossRefPubMedGoogle Scholar
  97. Tsuchida N, Murugan AK, Grieco M (2016) Kirsten Ras* oncogene: significance of its discovery in human cancer research. Oncotarget 7:46717CrossRefPubMedPubMedCentralGoogle Scholar
  98. Tuveson D, Hanahan D (2011) Translational medicine: cancer lessons from mice to humans. Nature 471(7338):316–317CrossRefPubMedGoogle Scholar
  99. Umemura T, Kai S, Hasegawa R et al (2003) Prevention of dual promoting effects of pentachlorophenol, an environmental pollutant, on diethylnitrosamine-induced hepato- and cholangiocarcinogenesis in mice by green tea infusion. Carcinogenesis 24(6):1105–1109CrossRefPubMedGoogle Scholar
  100. Van Emburgh BO, Robertson KD (2011) Modulation of Dnmt3b function in vitro by interactions with Dnmt3L, Dnmt3a and Dnmt3b splice variants. Nucleic Acids Res 39(12):4984–5002CrossRefPubMedPubMedCentralGoogle Scholar
  101. Volate SR, Muga SJ, Issa AY, Nitcheva D, Smith T, Wargovich MJ (2009) Epigenetic modulation of the retinoid X receptor alpha by green tea in the azoxymethane-Apc Min/+ mouse model of intestinal cancer. Mol Carcinog 48(10):920–933CrossRefPubMedPubMedCentralGoogle Scholar
  102. Williams GH, Stoeber K (2012) The cell cycle and cancer. J Pathol 226(2):352–364CrossRefPubMedGoogle Scholar
  103. Williamson G, Manach C (2005) Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am J Clin Nutr 81(1 Suppl):243S–255SCrossRefPubMedGoogle Scholar
  104. Wilson AS, Power BE, Molloy PL (2007) DNA hypomethylation and human diseases. Biochim Biophys Acta 1775(1):138–162PubMedGoogle Scholar
  105. Xiang LP, Wang A, Ye JH et al (2016) Suppressive effects of tea catechins on breast cancer. Forum Nutr 8(8):458Google Scholar
  106. Yan T, Wergedal J, Zhou Y, Mohan S, Baylink DJ, Strong DD (2001) Inhibition of human osteoblast marker gene expression by retinoids is mediated in part by insulin-like growth factor binding protein-6. Growth Horm IGF Res 11(6):368–377CrossRefPubMedGoogle Scholar
  107. Yang CS, Wang H, Li GX, Yang Z, Guan F, Jin H (2011) Cancer prevention by tea: evidence from laboratory studies. Pharmacol Res 64(2):113–122CrossRefPubMedGoogle Scholar
  108. Yang C, Du W, Yang D (2016) Inhibition of green tea polyphenol EGCG((−)-epigallocatechin-3-gallate) on the proliferation of gastric cancer cells by suppressing canonical wnt/beta-catenin signalling pathway. Int J Food Sci Nutr 67(7):818–827CrossRefPubMedGoogle Scholar
  109. Yong WS, Hsu FM, Chen PY (2016) Profiling genome-wide DNA methylation. Epigenetics Chromatin 9:26CrossRefPubMedPubMedCentralGoogle Scholar
  110. Yuan JM (2013) Cancer prevention by green tea: evidence from epidemiologic studies. Am J Clin Nutr 98(6 Suppl):1676S–1681SCrossRefPubMedPubMedCentralGoogle Scholar
  111. Yuan JM, Sun C, Butler LM (2011) Tea and cancer prevention: epidemiological studies. Pharmacol Res 64(2):123–135CrossRefPubMedPubMedCentralGoogle Scholar
  112. Zamora-Ros R, Touillaud M, Rothwell JA, Romieu I, Scalbert A (2014) Measuring exposure to the polyphenol metabolome in observational epidemiologic studies: current tools and applications and their limits. Am J Clin Nutr 100(1):11–26CrossRefPubMedPubMedCentralGoogle Scholar
  113. Zhang J, Lei Z, Huang Z et al (2016) Epigallocatechin-3-gallate(EGCG) suppresses melanoma cell growth and metastasis by targeting TRAF6 activity. Oncotarget 7:79557PubMedPubMedCentralGoogle Scholar
  114. Zhong L, Goldberg MS, Gao YT, Hanley JA, Parent ME, Jin F (2001) A population-based case-control study of lung cancer and green tea consumption among women living in shanghai. China Epidemiol 12(6):695–700CrossRefGoogle Scholar
  115. Zhong LX, Li H, Wu ML et al (2015) Inhibition of STAT3 signaling as critical molecular event in resveratrol-suppressed ovarian cancer cells. J Ovarian Res 8:25CrossRefPubMedPubMedCentralGoogle Scholar
  116. Zhu W, Qin W, Zhang K et al (2012) Trans-resveratrol alters mammary promoter hypermethylation in women at increased risk for breast cancer. Nutr Cancer 64(3):393–400CrossRefPubMedPubMedCentralGoogle Scholar
  117. Ziegler CC, Rainwater L, Whelan J, McEntee MF (2004) Dietary resveratrol does not affect intestinal tumorigenesis in Apc(Min/+) mice. J Nutr 134(1):5–10CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Land and Food Systems, Food, Nutrition and HealthUniversity of British ColumbiaVancouverCanada

Personalised recommendations