Abstract
Epigenetics oftenly described as the heritable changes in gene expression independent of changes in DNA sequence. Various environmental factors such as nutrition-dietary components, lifestyle, exercise, physical activity, toxins, and other contributing factors remodel the genome either in a constructive or detrimental way. Since epigenetic changes are reversible and nutrition is one of the many epigenetic regulators that modify gene expression without changing the DNA sequence, dietary nutrients and bioactive food components contribute to epigenetic phenomena either by directly suppressing DNA methylation or histone catalyzing enzymes or by changing the availability of substrates required for enzymatic reactions. Diets that contain catechol-dominant polyphenols are reported to suppress enzyme activity and activate epigenetically silenced genes. Furthermore, several dietary nutrients play a crucial role in one-carbon metabolism including folate, cobalamin, riboflavin, pyridoxine, and methionine by directly affecting S-adenosyl-l-methionine. Soy polyphenols block DNA methyltransferases and histone deacetylases to reverse aberrant CpG island methylation. Organosulfur rich compounds such as the sulforaphane found in broccoli appear to normalize DNA methylation and activate miR-140 expression, which represses SOX9 and ALDH1 and decreases tumor growth. The purpose of this short communication is to overview the epigenetic regulatory mechanisms of diet and other environmental factors. We discuss the epigenetic contributions of dietary components with a particular focus on nutritional polyphenols and flavonoids as epigenetic mediators that modify epigenetic tags and control gene expression. These mechanisms provide new insights to better understand the influence of dietary nutrients on epigenetic modifications and gene expression.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12272-017-0973-3/MediaObjects/12272_2017_973_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12272-017-0973-3/MediaObjects/12272_2017_973_Fig2_HTML.gif)
Similar content being viewed by others
References
Adlercreutz H, Mazur W (1997) Phyto-oestrogens and Western diseases. Ann Med 29:95–120
Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469
Arai Y, Ohgane J, Yagi S, Ito R, Iwasaki Y, Saito K, Akutsu K, Takatori S, Ishii R, Hayashi R, Izumi S, Sugino N, Kondo F, Horie M, Nakazawa H, Makino T, Shiota K (2011) Epigenetic assessment of environmental chemicals detected in maternal peripheral and cord blood samples. J Reprod Dev 57:507–517
Arents G, Moudrianakis EN (1995) The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc Natl Acad Sci USA 92:11170–11174
Asada K, Kotake Y, Asada R, Saunders D, Broyles RH, Towner RA, Fukui H, Floyd RA (2006) LINE-1 hypomethylation in a choline-deficiency-induced liver cancer in rats: dependence on feeding period. J Biomed Biotechnol 2006:1–6
Baccarelli A, Cassano PA, Litonjua A, Park SK, Suh H, Sparrow D, Vokonas P, Schwartz J (2008) Cardiac autonomic dysfunction: effects from particulate air pollution and protection by dietary methyl nutrients and metabolic polymorphisms. Circulation 117:1802–1809
Bao N, Lye KW, Barton MK (2004) MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7:653–662
Bassi D, Bueno Pde G, Nonaka KO, Selistre-Araujo HS, Leal AM (2015) Exercise alters myostatin protein expression in sedentary and exercised streptozotocin-diabetic rats. Arch Endocrinol Metab 59:148–153
Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412
Bestor TH (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9:2395–2402
Bestor T, Laudano A, Mattaliano R, Ingram V (1988) Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol 203:971–983
Bhattacharya SK, Ramchandani S, Cervoni N, Szyf M (1999) A mammalian protein with specific demethylase activity for mCpG DNA. Nature 397:579–583
Birney E, Stamatoyannopoulos JA, Dutta A, Guigó R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS, Dekker J, Lieb JD, Tullius TD, Crawford GE, Sunyaev S, Noble WS, Dunham I, Denoeud F, Reymond A, Kapranov P, Rozowsky J, Zheng D, Castelo R, Frankish A, Harrow J, Ghosh S, Sandelin A, Hofacker IL, Baertsch R, Keefe D, Dike S, Cheng J, Hirsch HA, Sekinger EA, Lagarde J, Abril JF, Shahab A, Flamm C, Fried C, Hackermüller J, Hertel J, Lindemeyer M, Missal K, Tanzer A, Washietl S, Korbel J, Emanuelsson O, Pedersen JS, Holroyd N, Taylor R, Swarbreck D, Matthews N, Dickson MC, Thomas DJ, Weirauch MT, Gilbert J, Drenkow J, Bell I, Zhao X, Srinivasan KG, Sung WK, Ooi HS, Chiu KP, Foissac S, Alioto T, Brent M, Pachter L, Tress ML, Valencia A, Choo SW, Choo CY, Ucla C, Manzano C, Wyss C, Cheung E, Clark TG, Brown JB, Ganesh M, Patel S, Tammana H, Chrast J, Henrichsen CN, Kai C, Kawai J, Nagalakshmi U, Wu J, Lian Z, Lian J, Newburger P, Zhang X, Bickel P, Mattick JS, Carninci P, Hayashizaki Y, Weissman S, Hubbard T, Myers RM, Rogers J, Stadler PF, Lowe TM, Wei CL, Ruan Y, Struhl K, Gerstein M, Antonarakis SE, Fu Y, Green ED, Karaöz U, Siepel A, Taylor J, Liefer LA, Wetterstrand KA, Good PJ, Feingold EA, Guyer MS, Cooper GM, Asimenos G, Dewey CN, Hou M, Nikolaev S, Montoya-Burgos JI, Löytynoja A, Whelan S, Pardi F, Massingham T, Huang H, Zhang NR, Holmes I, Mullikin JC, Ureta-Vidal A, Paten B, Seringhaus M, Church D, Rosenbloom K, Kent WJ, Stone EA, NISC Comparative Sequencing Program, Baylor College of Medicine Human Genome Sequencing Center, Washington University Genome Sequencing Center, Broad Institute, Children’s Hospital Oakland Research Institute, Batzoglou S, Goldman N, Hardison RC, Haussler D, Miller W, Sidow A, Trinklein ND, Zhang ZD, Barrera L, Stuart R, King DC, Ameur A, Enroth S, Bieda MC, Kim J, Bhinge AA, Jiang N, Liu J, Yao F, Vega VB, Lee CW, Ng P, Shahab A, Yang A, Moqtaderi Z, Zhu Z, Xu X, Squazzo S, Oberley MJ, Inman D, Singer MA, Richmond TA, Munn KJ, Rada-Iglesias A, Wallerman O, Komorowski J, Fowler JC, Couttet P, Bruce AW, Dovey OM, Ellis PD, Langford CF, Nix DA, Euskirchen G, Hartman S, Urban AE, Kraus P, Van Calcar S, Heintzman N, Kim TH, Wang K, Qu C, Hon G, Luna R, Glass CK, Rosenfeld MG, Aldred SF, Cooper SJ, Halees A, Lin JM, Shulha HP, Zhang X, Xu M, Haidar JN, Yu Y, Ruan Y, Iyer VR, Green RD, Wadelius C, Farnham PJ, Ren B, Harte RA, Hinrichs AS, Trumbower H, Clawson H, Hillman-Jackson J, Zweig AS, Smith K, Thakkapallayil A, Barber G, Kuhn RM, Karolchik D, Armengol L, Bird CP, de Bakker PI, Kern AD, Lopez-Bigas N, Martin JD, Stranger BE, Woodroffe A, Davydov E, Dimas A, Eyras E, Hallgrímsdóttir IB, Huppert J, Zody MC, Abecasis GR, Estivill X, Bouffard GG, Guan X, Hansen NF, Idol JR, Maduro VV, Maskeri B, McDowell JC, Park M, Thomas PJ, Young AC, Blakesley RW, Muzny DM, Sodergren E, Wheeler DA, Worley KC, Jiang H, Weinstock GM, Gibbs RA, Graves T, Fulton R, Mardis ER, Wilson RK, Clamp M, Cuff J, Gnerre S, Jaffe DB, Chang JL, Lindblad-Toh K, Lander ES, Koriabine M, Nefedov M, Osoegawa K, Yoshinaga Y, Zhu B, de Jong PJ (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799–816
Bistulfi G, Vandette E, Matsui S, Smiraglia DJ (2010) Mild folate deficiency induces genetic and epigenetic instability and phenotype changes in prostate cancer cells. BMC Biol 21:1–12
Blackburn HL, McErlean S, Jellema GL, van Laar R, Vernalis MN, Ellsworth DL (2015) Gene expression profiling during intensive cardiovascular lifestyle modification: Relationships with vascular function and weight loss. Genom Data 4:50–53
Bohn SK, Myhrstad MC, Thoresen M, Holden M, Karlsen A, Tunheim SH, Erlund I, Svendsen M, Seljeflot I, Moskaug JO, Duttaroy AK, Laake P, Arnesen H, Tonstad S, Collins A, Drevon CA, Blomhoff R (2010) Blood cell gene expression associated with cellular stress defense is modulated by antioxidant-rich food in a randomised controlled clinical trial of male smokers. BMC Med 16:1–15
Bollati V, Marinelli B, Apostoli P, Bonzini M, Nordio F, Hoxha M, Pegoraro V, Motta V, Tarantini L, Cantone L, Schwartz J, Bertazzi PA, Baccarelli A (2010) Exposure to metal-rich particulate matter modifies the expression of candidate microRNAs in peripheral blood leukocytes. Environ Health Perspect 118:763–768
Bora-Tatar G, Dayangac-Erden D, Demir AS, Dalkara S, Yelekci K, Erdem-Yurter H (2009) Molecular modifications on carboxylic acid derivatives as potent histone deacetylase inhibitors: activity and docking studies. Bioorg Med Chem 17:5219–5228
Borek C (2004) Dietary antioxidants and human cancer. Integr Cancer Ther 3:333–341
Bouchard-Mercier A, Paradis AM, Rudkowska I, Lemieux S, Couture P, Vohl MC (2013) Associations between dietary patterns and gene expression profiles of healthy men and women: a cross-sectional study. Nutr J 12(12):24
Boyanapalli SS, Paredes-Gonzalez X, Fuentes F, Zhang C, Guo Y, Pung D, Saw CL, Kong AN (2014) Nrf2 knockout attenuates the anti-inflammatory effects of phenethyl isothiocyanate and curcumin. Chem Res Toxicol 27:2036–2043
Branco MR, Ficz G, Reik W (2011) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13:7–13
Cai X, Hagedorn CH, Cullen BR (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10:1957–1966
Calvisi DF, Simile MM, Ladu S, Pellegrino R, De Murtas V, Pinna F, Tomasi ML, Frau M, Virdis P, De Miglio MR, Muroni MR, Pascale RM, Feo F (2007) Altered methionine metabolism and global DNA methylation in liver cancer: relationship with genomic instability and prognosis. Int J Cancer 121:2410–2420
Camporeale G, Giordano E, Rendina R, Zempleni J, Eissenberg JC (2006) Drosophila melanogaster holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan, and heat tolerance. J Nutr 136:2735–2742
Chen J, Xu X (2010) Diet, epigenetic, and cancer prevention. Adv Genet 71:237–255
Chen Y, Shu W, Chen W, Wu Q, Liu H, Cui G (2007) Curcumin, both histone deacetylase and p300/CBP-specific inhibitor, represses the activity of nuclear factor kappa B and Notch 1 in Raji cells. Basic Clin Pharmacol Toxicol 101:427–433
Cheng X, Blumenthal RM (2008) Mammalian DNA methyltransferases: a structural perspective. Structure 16:341–350
Choi SW, Friso S (2010) Epigenetics: a new bridge between nutrition and health. Adv Nutr 1:8–16
Crider KS, Yang TP, Berry RJ, Bailey LB (2012) Folate and DNA methylation: a review of molecular mechanisms and the evidence for folate’s role. Adv Nutr 3:21–38
Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319:1097–1113
Davis CD, Uthus EO (2004) DNA methylation, cancer susceptibility, and nutrient interactions. Exp Biol Med 229:988–995
Deng XH, Song HY, Zhou YF, Yuan GY, Zheng FJ (2013) Effects of quercetin on the proliferation of breast cancer cells and expression of survivin in vitro. Exp Ther Med 6:1155–1158
Detich N, Theberge J, Szyf M (2002) Promoter-specific activation and demethylation by MBD2/demethylase. J Biol Chem 277:35791–35794
Dhasarathy A, Wade PA (2008) The MBD protein family-reading an epigenetic mark? Mutat Res 647:39–43
Duraimani S, Schneider RH, Randall OS, Nidich SI, Xu S, Ketete M, Rainforth MA, Gaylord-King C, Salerno JW, Fagan J (2015) Effects of lifestyle modification on telomerase gene expression in hypertensive patients: a pilot trial of stress reduction and health education programs in African Americans. PLoS ONE 10:1–18
Duthie SJ (2011) Folate and cancer: how DNA damage, repair and methylation impact on colon carcinogenesis. J Inherit Metab Dis 34:101–109
Duthie SJ, Narayanan S, Sharp L, Little J, Basten G, Powers H (2004) Folate, DNA stability and colo-rectal neoplasia. Proc Nutr Soc 63:571–578
Edmunds JW, Mahadevan LC, Clayton AL (2008) Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27:406–420
Esquela-Kerscher A, Slack FJ (2006) Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6:259–269
Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, Volinia S, Guler G, Morrison CD, Chan KK, Marcucci G, Calin GA, Huebner K, Croce CM (2007) MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA 104:15805–15810
Feinberg AP, Tycko B (2004) The history of cancer epigenetics. Nat Rev Cancer 4:143–153
Feng Q, Zhang Y (2001) The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 15:827–832
Frombaum M, Le Clanche S, Bonnefont-Rousselot D, Borderie D (2012) Antioxidant effects of resveratrol and other stilbene derivatives on oxidative stress and *NO bioavailability: potential benefits to cardiovascular diseases. Biochimie 94:269–276
Geng Y, Zhang B, Lotz M (1993) Protein tyrosine kinase activation is required for lipopolysaccharide induction of cytokines in human blood monocytes. J Immunol 151:6692–6700
Ghoshal K, Li X, Datta J, Bai S, Pogribny I, Pogribny M, Huang Y, Young D, Jacob ST (2006) A folate- and methyl-deficient diet alters the expression of DNA methyltransferases and methyl CpG binding proteins involved in epigenetic gene silencing in livers of F344 rats. J Nutr 136:1522–1527
Giuliani C, Noguchi Y, Harii N, Napolitano G, Tatone D, Bucci I, Piantelli M, Monaco F, Kohn LD (2008) The flavonoid quercetin regulates growth and gene expression in rat FRTL-5 thyroid cells. Endocrinology 149:84–92
Giuliani C, Bucci I, Di Santo S, Rossi C, Grassadonia A, Mariotti M, Piantelli M, Monaco F, Napolitano G (2014) Resveratrol inhibits sodium/iodide symporter gene expression and function in rat thyroid cells. PLoS ONE 9:1–6
Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311:395–398
Groth A, Rocha W, Verreault A, Almouzni G (2007) Chromatin challenges during DNA replication and repair. Cell 128:721–733
Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88
Hassan YI, Zempleni J (2008) A novel, enigmatic histone modification: biotinylation of histones by holocarboxylase synthetase. Nutr Rev 66:721–725
Healy S, Perez-Cadahia B, Jia D, McDonald MK, Davie JR, Gravel RA (2009) Biotin is not a natural histone modification. Biochim Biophys Acta 1789:719–733
Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39:311–318
Hong JT, Yen JH, Wang L, Lo YH, Chen ZT, Wu MJ (2009) Regulation of heme oxygenase-1 expression and MAPK pathways in response to kaempferol and rhamnocitrin in PC12 cells. Toxicol Appl Pharmacol 237:59–68
Ichimura A, Ruike Y, Terasawa K, Tsujimoto G (2011) miRNAs and regulation of cell signaling. FEBS J 278:1610–1618
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 133:3740s–3747s
Jardim MJ, Fry RC, Jaspers I, Dailey L, Diaz-Sanchez D (2009) Disruption of microRNA expression in human airway cells by diesel exhaust particles is linked to tumorigenesis-associated pathways. Environ Health Perspect 117:1745–1751
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080
Ji Z, Zhang L, Peng V, Ren X, McHale CM, Smith MT (2010) A comparison of the cytogenetic alterations and global DNA hypomethylation induced by the benzene metabolite, hydroquinone, with those induced by melphalan and etoposide. Leukemia 24:986–991
Johnson JL, de Mejia EG (2013) Flavonoid apigenin modified gene expression associated with inflammation and cancer and induced apoptosis in human pancreatic cancer cells through inhibition of GSK-3beta/NF-kappaB signaling cascade. Mol Nutr Food Res 57:2112–2127
Jones SB, DePrimo SE, Whitfield ML, Brooks JD (2005) Resveratrol-induced gene expression profiles in human prostate cancer cells. Cancer Epidemiol Biomarkers Prev 14:596–604
Jones PA, Archer TK, Baylin SB, Beck S, Berger S, Bernstein BE, Carpten JD, Clark SJ, Costello JF, Doerge RW, Esteller M, Feinberg AP, Gingeras TR, Greally JM, Henikoff S, Herman JG, Jackson-Grusby L, Jenuwein T, Jirtle RL, Kim YJ, Laird PW, Lim B, Martienssen R, Polyak K, Stunnenberg H, Tlsty TD, Tycko B, Ushijima T, Zhu J, Pirrotta V, Allis CD, Elgin SC, Jones PA, Martienssen R, Rine J, Wu C (2008) Moving ahead with an international human epigenome project. Nature 454:711–715
Jump DB (2002) Dietary polyunsaturated fatty acids and regulation of gene transcription. Curr Opin Lipidol 13:155–164
Kanduc D, Ghoshal A, Quagliariello E, Farber E (1988) DNA hypomethylation in ethionine-induced rat preneoplastic hepatocyte nodules. Biochem Biophys Res Commun 150:739–744
Kanzleiter T, Jahnert M, Schulze G, Selbig J, Hallahan N, Schwenk RW, Schurmann A (2015) Exercise training alters DNA methylation patterns in genes related to muscle growth and differentiation in mice. Am J Physiol Endocrinol Metab 308:912–920
Kareta MS, Botello ZM, Ennis JJ, Chou C, Chedin F (2006) Reconstitution and mechanism of the stimulation of de novo methylation by human DNMT3L. J Biol Chem 281:25893–25902
Khan SI, Aumsuwan P, Khan IA, Walker LA, Dasmahapatra AK (2012) Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome. Chem Res Toxicol 25:61–73
Kiec-Wilk B, Razny U, Mathers JC, Dembinska-Kiec A (2009) DNA methylation, induced by beta-carotene and arachidonic acid, plays a regulatory role in the pro-angiogenic VEGF-receptor (KDR) gene expression in endothelial cells. J Physiol Pharmacol 60:49–53
Kim YI (2004) Folate and DNA methylation: a mechanistic link between folate deficiency and colorectal cancer? Cancer Epidemiol Biomarkers Prev 13:511–519
Kim KC, Choi S-W (2015) Nutritional epigenetics and aging. In: Nutrition, exercise and epigenetics: ageing interventions. Springer International Publishing, Cham, pp 1–28
Kim VN, Nam JW (2006) Genomics of microRNA. Trends Genet 22:165–173
Kioka N, Hosokawa N, Komano T, Hirayoshi K, Nagata K, Ueda K (1992) Quercetin, a bioflavonoid, inhibits the increase of human multidrug resistance gene (MDR1) expression caused by arsenite. FEBS Lett 301:307–309
Koch CM, Andrews RM, Flicek P, Dillon SC, Karaöz U, Clelland GK, Wilcox S, Beare DM, Fowler JC, Couttet P, James KD, Lefebvre GC, Bruce AW, Dovey OM, Ellis PD, Dhami P, Langford CF, Weng Z, Birney E, Carter NP, Vetrie D, Dunham I (2007) The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res 17:691–707
Kondo K, Takahashi Y, Hirose Y, Nagao T, Tsuyuguchi M, Hashimoto M, Ochiai A, Monden Y, Tangoku A (2006) The reduced expression and aberrant methylation of p16(INK4a) in chromate workers with lung cancer. Lung Cancer 53:295–302
Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705
Krivtsov AV, Feng Z, Lemieux ME, Faber J, Vempati S, Sinha AU, Xia X, Jesneck J, Bracken AP, Silverman LB, Kutok JL, Kung AL, Armstrong SA (2008) H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell 14:355–368
Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858
Lee YW, Klein CB, Kargacin B, Salnikow K, Kitahara J, Dowjat K, Zhitkovich A, Christie NT, Costa M (1995) Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens. Mol Cell Biol 15:2547–2557
Lee Y, Jeon K, Lee JT, Kim S, Kim VN (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670
Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060
Lee S, Kim YJ, Kwon S, Lee Y, Choi SY, Park J, Kwon HJ (2009) Inhibitory effects of flavonoids on TNF-alpha-induced IL-8 gene expression in HEK 293 cells. BMB Rep 42:265–270
Levenson JM, Sweatt JD (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6:108–118
Li Y, Liu L, Andrews LG, Tollefsbol TO (2009) Genistein depletes telomerase activity through cross-talk between genetic and epigenetic mechanisms. Int J Cancer 125:286–296
Li Q, Yao Y, Eades G, Liu Z, Zhang Y, Zhou Q (2014) Downregulation of miR-140 promotes cancer stem cell formation in basal-like early stage breast cancer. Oncogene 33:2589–2600
Link A, Balaguer F, Goel A (2010) Cancer chemoprevention by dietary polyphenols: promising role for epigenetics. Biochem Pharmacol 80:1771–1792
Liu HL, Chen Y, Cui GH, Zhou JF (2005) Curcumin, a potent anti-tumor reagent, is a novel histone deacetylase inhibitor regulating B-NHL cell line Raji proliferation. Acta Pharmacol Sin 26:603–609
Liu J, Ballaney M, Al-alem U, Quan C, Jin X, Perera F, Chen LC, Miller RL (2008) Combined inhaled diesel exhaust particles and allergen exposure alter methylation of T helper genes and IgE production in vivo. Toxicol Sci 102:76–81
Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR (2005) MicroRNA expression profiles classify human cancers. Nature 435:834–838
Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260
Majumdar S, Chanda S, Ganguli B, Mazumder DN, Lahiri S, Dasgupta UB (2010) Arsenic exposure induces genomic hypermethylation. Environ Toxicol 25:315–318
Mariño-Ramírez L, Kann MG, Shoemaker BA, Landsman D (2005) Histone structure and nucleosome stability. Expert Rev Proteomics 2:719–729
Meltzer PS (2005) Cancer genomics: small RNAs with big impacts. Nature 435:745–746
Miao F, Natarajan R (2005) Mapping global histone methylation patterns in the coding regions of human genes. Mol Cell Biol 25:4650–4661
Miranda TB, Jones PA (2007) DNA methylation: the nuts and bolts of repression. J Cell Physiol 213:384–390
Moore LD, Le T, Fan G (2013) DNA methylation and its basic function. Neuropsychopharmacology 38:23–38
Mutlu Altundag E, Kasaci T, Yilmaz AM, Karademir B, Kocturk S, Taga Y, Yalcin AS (2016) Quercetin-induced cell death in human papillary thyroid cancer (B-CPAP) cells. J Thyroid Res 2016:1–10
Myzak MC, Tong P, Dashwood WM, Dashwood RH, Ho E (2007) Sulforaphane retards the growth of human PC-3 xenografts and inhibits HDAC activity in human subjects. Exp Biol Med 232:227–234
Nakahara K, Carthew RW (2004) Expanding roles for miRNAs and siRNAs in cell regulation. Curr Opin Cell Biol 16:127–133
Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389
Newberne PM, Rogers AE (1986) Labile methyl groups and the promotion of cancer. Annu Rev Nutr 6:407–432
Nicholson SK, Tucker GA, Brameld JM (2008) Effects of dietary polyphenols on gene expression in human vascular endothelial cells. Proc Nutr Soc 67:42–47
Nicholson SK, Tucker GA, Brameld JM (2010) Physiological concentrations of dietary polyphenols regulate vascular endothelial cell expression of genes important in cardiovascular health. Br J Nutr 103:1398–1403
Okano M, Xie S, Li E (1998) Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19:219–220
Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257
Okoji RS, Yu RC, Maronpot RR, Froines JR (2002) Sodium arsenite administration via drinking water increases genome-wide and Ha-ras DNA hypomethylation in methyl-deficient C57BL/6J mice. Carcinogenesis 23:777–785
Ono K, Kuwabara Y, Han J (2011) MicroRNAs and cardiovascular diseases. FEBS J 278:1619–1633
Ornish D, Magbanua MJ, Weidner G, Weinberg V, Kemp C, Green C, Mattie MD, Marlin R, Simko J, Shinohara K, Haqq CM, Carroll PR (2008) Changes in prostate gene expression in men undergoing an intensive nutrition and lifestyle intervention. Proc Natl Acad Sci USA 105:8369–8374
Paluszczak J, Krajka-Kuzniak V, Baer-Dubowska W (2010) The effect of dietary polyphenols on the epigenetic regulation of gene expression in MCF7 breast cancer cells. Toxicol Lett 192:119–125
Papoutsis AJ, Lamore SD, Wondrak GT, Selmin OI, Romagnolo DF (2010) Resveratrol prevents epigenetic silencing of BRCA-1 by the aromatic hydrocarbon receptor in human breast cancer cells. J Nutr 140:1607–1614
Pogue AI, Li YY, Cui JG, Zhao Y, Kruck TP, Percy ME, Tarr MA, Lukiw WJ (2009) Characterization of an NF-kappaB-regulated, miRNA-146a-mediated down-regulation of complement factor H (CFH) in metal-sulfate-stressed human brain cells. J Inorg Biochem 103:1591–1595
Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, Jacobsen SE, Reik W (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463:1101–1105
Probst AV, Dunleavy E, Almouzni G (2009) Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 10:192–206
Qin W, Zhu W, Shi H, Hewett JE, Ruhlen RL, MacDonald RS, Rottinghaus GE, Chen YC, Sauter ER (2009) Soy isoflavones have an antiestrogenic effect and alter mammary promoter hypermethylation in healthy premenopausal women. Nutr Cancer 61:238–244
Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR (2008) DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135:1201–1212
Rajewsky N (2006) microRNA target predictions in animals. Nat Genet 38(Suppl):S8–S13
Ramchandani S, Bhattacharya SK, Cervoni N, Szyf M (1999) DNA methylation is a reversible biological signal. Proc Natl Acad Sci USA 96:6107–6112
Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci USA 97:5237–5242
Reichard JF, Schnekenburger M, Puga A (2007) Long term low-dose arsenic exposure induces loss of DNA methylation. Biochem Biophys Res Commun 352:188–192
Rönn T, Volkov P, Davegårdh C, Dayeh T, Hall E, Olsson AH, Nilsson E, Tornberg A, Dekker Nitert M, Eriksson KF, Jones HA, Groop L, Ling C (2013) A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet 9:1–16
Routh A, Sandin S, Rhodes D (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci USA 105:8872–8877
Ruthenburg AJ, Li H, Patel DJ, Allis CD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8:983–994
Sato F, Tsuchiya S, Meltzer SJ, Shimizu K (2011) MicroRNAs and epigenetics. FEBS J 278:1598–1609
Schneider Y, Vincent F, Duranton B, Badolo L, Gosse F, Bergmann C, Seiler N, Raul F (2000) Anti-proliferative effect of resveratrol, a natural component of grapes and wine, on human colonic cancer cells. Cancer Lett 158:85–91
Scott JM, Weir DG (1998) Folic acid, homocysteine and one-carbon metabolism: a review of the essential biochemistry. J Cardiovasc Risk 5:223–227
Selhub J (2002) Folate, vitamin B12 and vitamin B6 and one carbon metabolism. J Nutr Health Aging 6:39–42
Shapiro AB, Ling V (1997) Effect of quercetin on Hoechst 33342 transport by purified and reconstituted P-glycoprotein. Biochem Pharmacol 53:587–596
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 64:451–460
Slattery ML, Potter JD, Samowitz W, Schaffer D, Leppert M (1999) Methylenetetrahydrofolate reductase, diet, and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 8:513–518
Song C, Kanthasamy A, Anantharam V, Sun F, Kanthasamy AG (2010) Environmental neurotoxic pesticide increases histone acetylation to promote apoptosis in dopaminergic neuronal cells:relevance to epigenetic mechanisms of neurodegeneration. Mol Pharmacol 77:621–632
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 167:279–297
Steger DJ, Lefterova MI, Ying L, Stonestrom AJ, Schupp M, Zhuo D, Vakoc AL, Kim JE, Chen J, Lazar MA, Blobel GA, Vakoc CR (2008) DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol Cell Biol 28:2825–2839
Svajger U, Jeras M (2012) Anti-inflammatory effects of resveratrol and its potential use in therapy of immune-mediated diseases. Intl Rev Immunol 31:202–222
Takiguchi M, Achanzar WE, Qu W, Li G, Waalkes MP (2003) Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp Cell Res 286:355–365
Tao L, Yang S, Xie M, Kramer PM, Pereira MA (2000) Effect of trichloroethylene and its metabolites, dichloroacetic acid and trichloroacetic acid, on the methylation and expression of c-Jun and c-Myc protooncogenes in mouse liver: prevention by methionine. Toxicol Sci 54:399–407
Tate PH, Bird AP (1993) Effects of DNA methylation on DNA-binding proteins and gene expression. Curr Opin Genet Dev 3:226–231
Thune I, Brenn T, Lund E, Gaard M (1997) Physical activity and the risk of breast cancer. N Engl J Med 336:1269–1275
Vanden Berghe W (2012) Epigenetic impact of dietary polyphenols in cancer chemoprevention: lifelong remodeling of our epigenomes. Pharmacol Res 65:565–576
Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151:4756–4764
Waterland RA (2006) Assessing the effects of high methionine intake on DNA methylation. J Nutr 136:1706s–1710s
Wen L, Li X, Yan L, Tan Y, Li R, Zhao Y, Wang Y, Xie J, Zhang Y, Song C, Yu M, Liu X, Zhu P, Li X, Hou Y, Guo H, Wu X, He C, Li R, Tang F, Qiao J (2014) Whole-genome analysis of 5-hydroxymethylcytosine and 5-methylcytosine at base resolution in the human brain. Genome Biol 15:1–17
Wright RO, Schwartz J, Wright RJ, Bollati V, Tarantini L, Park SK, Hu H, Sparrow D, Vokonas P, Baccarelli A (2010) Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ Health Perspect 118:790–795
Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329:444–448
Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, Van Schooten FJ, Berndt ML, Pogribny IP, Koturbash I, Williams A, Douglas GR, Kovalchuk O (2008) Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Procd Natl Acad Sci USA 105:605–610
Yoder JA, Bestor TH (1998) A candidate mammalian DNA methyltransferase related to pmt1p of fission yeast. Hum Mol Genet 7:279–284
Zapisek WF, Cronin GM, Lyn-Cook BD, Poirier LA (1992) The onset of oncogene hypomethylation in the livers of rats fed methyl-deficient, amino acid-defined diets. Carcinogenesis 13:1869–1872
Zempleni J, Chew YC, Bao B, Pestinger V, Wijeratne SS (2009) Repression of transposable elements by histone biotinylation. J Nutr 139:2389–2392
Zhang G, Wang K, Schultz E, Khoo SK, Zhang X, Annamalay A, Laing IA, Hales BJ, Goldblatt J, Le Souef PN (2016a) Western environment/lifestyle is associated with increased genome methylation and decreased gene expression in Chinese immigrants living in Australia. Environ Mol Mutagen 57:65–73
Zhang L, Miao XJ, Wang X, Pan HH, Li P, Ren H, Jia YR, Lu C, Wang HB, Yuan L, Zhang GL (2016b) Antiproliferation of berberine is mediated by epigenetic modification of constitutive androstane receptor (CAR) metabolic pathway in hepatoma cells. Sci Rep 17:1–10
Zhao CQ, Young MR, Diwan BA, Coogan TP, Waalkes MP (1997) Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc Natl Acad Sci USA 4:10907–10912
Acknowledgements
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (2012R1A6A1028677). We thank Aging Tissue Bank for providing research information.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare no conflicts of interest.
Rights and permissions
About this article
Cite this article
Abdul, Q.A., Yu, B.P., Chung, H.Y. et al. Epigenetic modifications of gene expression by lifestyle and environment. Arch. Pharm. Res. 40, 1219–1237 (2017). https://doi.org/10.1007/s12272-017-0973-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12272-017-0973-3