The effect of diet on the intestinal epigenome

Epigenomics

Volumn 6, Issue 2, 2014, Pages 239-251

  Johnson, Ian T ^a   Belshaw, Nigel J ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

colon; DNA methylation; DNA methyltransferase; folic acid; mucosa; rectum

Indexed keywords

DNA METHYLTRANSFERASE INHIBITOR; FOLIC ACID; HISTONE DEACETYLASE; TRACE ELEMENT; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1;

AGING; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; COLON MUCOSA; COLORECTAL CANCER; CPG ISLAND; CROSS-SECTIONAL STUDY; DIET; DIETARY FIBER; DNA METHYLATION; EPIGENETICS; FOLATE METABOLISM; HUMAN; IN VITRO STUDY; INTESTINE; NONHUMAN; NUTRITIONAL STATUS; ONCOGENE; PRIORITY JOURNAL; RECTUM MUCOSA; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; COLORECTAL TUMOR; CYTOLOGY; ENZYMOLOGY; GENETIC EPIGENESIS; GENETICS; INTESTINE MUCOSA; METABOLISM; MOUSE; RAT;

ANIMALS; COLORECTAL NEOPLASMS; CPG ISLANDS; DIET; DIETARY FIBER; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; FOLIC ACID; HISTONE DEACETYLASES; HUMANS; INTESTINAL MUCOSA; INTESTINES; MICE; NUTRITIONAL STATUS; RATS;

EID: 84900474192     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.14.8     Document Type: Review

References (89)

1. Bird A. Perceptions of epigenetics. Nature 447, 396-398 (2007). (Pubitemid 46816744)
2. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 14, R115 (2013).
3. Kaelin WG Jr, McKnight SL. Influence of metabolism on epigenetics and disease. Cell 153, 56-69 (2013).
4. Gut P, Verdin E. Thenexus of chromatin regulation and intermediary metabolism. Nature 502, 489-498 (2013).
5. Kirchner H, Osler ME, Krook A, Zierath JR. Epigenetic flexibility in metabolic regulation: disease cause and prevention? Trends Cell Biol. 23, 203-209 (2013).
6. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat. Rev. Gastroenterol. Hepatol. 8, 686-700 (2011).
7. Waterland RA. Epigenetic mechanisms and gastrointestinal development. J. Pediatr. 149, S137-S142 (2006). (Pubitemid 44278867)
8. Sato T, van Es JH, Snippert HJ et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418 (2011).
9. McDuffie LA, Bucher BT, Erwin CR et al. Intestinal adaptation after small bowel resection in human infants. J. Pediatr. Surg. 46, 1045-1051 (2011).
10. Drozdowski L, Thomson AB. Intestinal mucosal adaptation. World J. Gastroenterol. 12, 4614-4627 (2006). (Pubitemid 44269717)
11. Inoue S, Mochizuki K, Goda T. Jejunal induction of SI and SGLT1 genes in rats by high-starch/low-fat diet is associated with histone acetylation and binding of GCN5 on the genes. J. Nutr. Sci. Vitaminol. (Tokyo) 57, 162-169 (2011).
12. Suzuki T, Douard V, Mochizuki K, Goda T, Ferraris RP. Diet-induced epigenetic regulation in vivo of the intestinal fructose transporter Glut5 during development of rat small intestine. Biochem J. 435, 43-53 (2011).
13. Honma K, Mochizuki K, Goda T. Induction by fructose force-feeding of histone H3 and H4 acetylation at their lysine residues around the Slc2a5 gene and its expression in mice. Biosci. Biotechnol. Biochem. 77, 2188-2191 (2013).
14. Brenner H, Kloor M, Pox CP.Colorectal cancer. Lancet doi:10.1016/S0140- 6736(13)61649-9 ( 2013) (Epub ahead of print).
15. Lynch JP, Hoops TC. The genetic pathogenesis of colorectal cancer. Hematol. Oncol. Clin. North Am. 16, 775-810 (2002). (Pubitemid 35215825)
16. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301, 89-92 (1983). (Pubitemid 13154475)
17. Kane MF, Loda M, Gaida GM et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res. 57, 808-811. (1997). (Pubitemid 27097998)
18. Gonzalez-Zulueta M, Bender CM, Yang AS et al. Methylation of the 5' CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res. 55, 4531-4535. (1995).
19. Hinoue T, Weisenberger DJ, Lange CP et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 22, 271-282 (2012).
20. Irizarry RA, Ladd-Acosta C, Wen B et al. The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 41, 178-186 (2009).
21. Rawson JB, Manno M, Mrkonjic M et al. Promoter methylation of Wnt antagonists DKK1 and SFRP1 is associated with opposing tumor subtypes in two large populations of colorectal cancer patients. Carcinogenesis 32, 741-747 (2011).
22. Bardhan K, Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers (Basel) 5, 676-713 (2013).
23. Eckhardt F, Lewin J, Cortese R et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet. 38, 1378-1385 (2006). (Pubitemid 44837559)
24. Maegawa S, Hinkal G, Kim HS et al. Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res. 20, 332-340 (2010).
25. Kondo Y, Issa JP. Epigenetic changes in colorectal cancer. Cancer Metastasis Rev. 23, 29-39 (2004). (Pubitemid 38221595)
26. Issa JP, Ottaviano YL, Celano P et al. Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat. Genet. 7, 536-540 (1994). (Pubitemid 24308343)
27. Campbell-Thompson M, Lynch IJ, Bhardwaj B. Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res. 61, 632-640 (2001). (Pubitemid 32128626)
28. Shen L, Kondo Y, Rosner GL et al. MGMT promoter methylation and field defect in sporadic colorectal cancer. J. Natl Cancer Inst. 97, 1330-1338 (2005). (Pubitemid 41487800)
29. Belshaw NJ, Elliott GO, Foxall RJ et al. Profiling CpG island field methylation in both morphologically normal and neoplastic human colonic mucosa. Br. J. Cancer 99, 136-142 (2008). (Pubitemid 351920230)
30. Silviera ML, Smith BP, Powell J, Sapienza C. Epigenetic differences in normal colon mucosa of cancer patients suggest altered dietary metabolic pathways. Cancer Prev. Res. 5, 374-384 (2012).
31. Kaz AM, Wong CJ, Dzieciatkowski S et al. Patterns of DNA methylation in the normal colon vary by anatomical location, gender, and age. Epigenetics doi:10.4161/epi.27650 (2014) (Epub ahead of print).
32. Belshaw NJ, Pal N, Tapp HS et al. Patterns of DNA methylation in individual colonic crypts reveal aging and cancer-related field defects in the morphologically normal mucosa. Carcinogenesis 31, 1158-1163 (2010).
33. Silva AJ, Ward K, White R. Mosaic methylation in clonal tissue. Dev. Biol. 156, 391-398 (1993). (Pubitemid 23122304)
34. Laird CD, Pleasant ND, Clark AD et al. Hairpin-bisulfite PCR: Assessing epigenetic methylation patterns on complementary strands of individual DNA molecules. Proc. Natl Acad. Sci. USA 101, 204-209 (2004). (Pubitemid 38084228)
35. De Cabo SF, Santos J, Fernandez-Piqueras J. Molecular and cytological evidence of S-adenosyl-L-homocysteine as an innocuous undermethylating agent in vivo. Cytogenet. Cell Genet. 71, 187-192 (1995).
36. Hoffman DR, Cornatzer WE, Duerre JA. Relationship between tissue levels of S-adenosylmethionine, S-adenylhomocysteine, and transmethylation reactions. Can. J. Biochem. 57, 56-65 (1979). (Pubitemid 9140347)
37. Williams KT, Schalinske KL. New insights into the regulation of methyl group and homocysteine metabolism. J. Nutr. 137, 311-314 (2007). (Pubitemid 46213441)
38. Duthie SJ, Narayanan S, Brand GM, Grant G. DNA stability and genomic methylation status in colonocytes isolated from methyl-donor-deficient rats. Eur. J. Nutr. 39, 106-111 (2000). (Pubitemid 30439027)
39. Stempak JM, Sohn KJ, Chiang EP, Shane B, Kim YI. Cell and stage of transformation-specific effects of folate deficiency on methionine cycle intermediates and DNA methylation in an in vitro model. Carcinogenesis 26, 981-990 (2005). (Pubitemid 41214328)
40. Charles MA, Johnson IT, Belshaw NJ. Supra-physiological folic acid concentrations induce aberrant DNA methylation in normal human cells in vitro. Epigenetics 7, 689-694 (2012).
41. Sie KKY, Li J, Ly A et al. Effect of maternal and postweaning folic acid supplementation on global and gene-specific DNA methylation in the liver of the rat offspring. Mol. Nutr. Food Res. 57, 677-685 (2013).
42. Michaud EJ, van Vugt MJ, Bultman SJ et al. Differential expression of a new dominant agouti allele (Aiapy) is correlated with methylation state and is influenced by parental lineage. Genes Dev. 8, 1463-1472 (1994).
43. Yen TT, Gill AM, Frigeri LG, Barsh GS, Wolff GL. Obesity, diabetes, and neoplasia in yellow A(vy)/-mice: ectopic expression of the agouti gene. FASEB J. 8, 479-488 (1994).
44. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 12, 949-957 (1998). (Pubitemid 28359576)
45. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J. Nutr. 132, 2393S-2400S (2002). (Pubitemid 34848114)
46. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell Biol. 23, 5293-5300 (2003). (Pubitemid 36950884)
47. Sie KKY, Medline A, van Weel J et al. Effect of maternal and postweaning folic acid supplementation on colorectal cancer risk in the offspring. Gut 60, 1687-1694 (2011).
48. Bailey SW, Ayling JE. The extremely slow and variable activity of dihydrofolate reductase in human liver and its implications for high folic acid intake. Proc. Natl Acad. Sci. USA 106, 15424-15429 (2009).
49. Troen AM, Mitchell B, Sorensen B et al. Unmetabolized folic acid in plasma is associated with reduced natural killer cell cytotoxicity among postmenopausal women. J. Nutr. 136, 189-194 (2006). (Pubitemid 43156507)
50. Cravo ML, Pinto AG, Chaves P et al. Effect of folate supplementation on DNA methylation of rectal mucosa in patients with colonic adenomas: correlation with nutrient intake. Clin. Nutr. 17, 45-49 (1998). (Pubitemid 28230839)
51. Kim YI, Baik HW, Fawaz K et al. Effects of folate supplementation on two provisional molecular markers of colon cancer: a prospective, randomized trial. Am. J. Gastroenterol. 96, 184-195 (2001). (Pubitemid 32104827)
52. Pufulete M, Al-Ghnaniem R, Khushal A et al. Effect of folic acid supplementation on genomic DNA methylation in patients with colorectal adenoma. Gut 54, 648-653 (2005). (Pubitemid 40559249)
53. Figueiredo JC, Grau MV, Wallace K et al. Global DNA Hypomethyation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol. Biomarkers Prev. 18, 1041-1049 (2009).
54. van den Donk M, Pellis L, Crott JW et al. 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), 2114-2120 (2007). (Pubitemid 47367274)
55. Wallace K, Grau MV, Levine AJ et al. Association between folate levels and CpG Island hypermethylation in normal colorectal mucosa. Cancer Prev. Res. (Phila.) 3, 1552-1564 (2010).
56. Abbadi RA, Emery P, Pufulete M. Short-term folate supplementation in physiological doses has no effect on ESR1 and MLH1 methylation in colonic mucosa of individuals with adenoma. J. Nutrigenet. Nutrigenomics 5, 327-338 (2012).
57. Al-Ghnaniem R, Peters J, Foresti R, Heaton N, Pufulete M. Methylation of estrogen receptor alpha and mutL homolog 1 in normal colonic mucosa: association with folate and vitamin B-12 status in subjects with and without colorectal neoplasia. Am. J. Clin. Nutr. 86, 1064-1072 (2007). (Pubitemid 47538310)
58. Hanks J, Ayed I, Kukreja N et al. The association between MTHFR 677C T genotype and folate status and genomic and gene-specific DNA methylation in the colon of individuals without colorectal neoplasia. Am. J. Clin. Nutr. 98, 1564-1574 (2013).
59. Tapp HS, Commane DM, Bradburn DM et al. Nutritional factors and gender influence age-related DNA methylation in the human rectal mucosa. Aging Cell 12, 148-155 (2013).
60. Perng W, Mora-Plazas M, Marin C et al. A prospective study of LINE-1DNA methylation and development of adiposity in school-age children. PLoS ONE 8(4), e62587 (2013).
61. Lee JE, Li HJ, Chan AT et al. Circulating levels of Vitamin D and colon and rectal cancer: The Physicians' Health Study and a meta-analysis of prospective studies. Cancer Prev. Res. (Phila.) 4, 735-743 (2011).
62. Ashktorab H, Nguza B, Fatemi M et al. Case-Control study of vitamin D, dickkopf homolog 1 (DKK1) gene methylation, VDR gene polymorphism and the risk of colon adenoma in african americans. PLoS ONE 6(10), e25314 (2011).
63. Rawson JB, Sun ZY, Dicks E et al. Vitamin D intake is negatively associated with promoter methylation of the Wnt antagonist gene DKK1 in a large group of colorectal cancer patients. Nutr. Cancer 64, 919-928 (2012).
64. Stefanska B, Karlic H, Varga F, Fabianowska-Majewska K, Haslberger AG. Epigenetic mechanisms in anti-cancer actions of bioactive food components-the implications in cancer prevention. Br. J. Pharmacol. 167, 279-297 (2012).
65. Davis CD, Uthus EO, Finley JW. 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 (2000). (Pubitemid 32005315)
66. Davis CD, Uthus EO. Dietary folate and selenium affect dimethylhydrazine-induced aberrant crypt formation, global DNA methylation and one-carbon metabolism in rats. J. Nutr. 133, 2907-2914 (2003). (Pubitemid 37099780)
67. Uthus EO, Ross SA, Davis CD. Differential effects of dietary selenium (Se) and folate on methyl metabolism in liver and colon of rats. Biol. Trace Elem. Res. 109, 201-214 (2006). (Pubitemid 43780419)
68. Zeng HW, Yan L, Cheng WH, Uthus EO. Dietary selenomethionine increases exon-specific DNA methylation of the p53 gene in rat liver and colon mucosa. J. Nutr. 141, 1464-1468 (2011).
69. Fairweather-Tait SJ, Bao YP, Broadley MR et al. Selenium in human health and disease. Antioxid. Redox Signal. 14, 1337-1383 (2011).
70. Fiala ES, Staretz ME, Pandya GA, El-Bayoumy K, Hamilton SR. 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 (1998). (Pubitemid 28376802)
71. Cummings JH, Mann JI, Nishida C, Vorster HH. Dietary fibre: an agreed definition. Lancet 373, 365-366 (2009).
72. Hamer HM, Jonkers D, Venema K et al. Review article: the role of butyrate on colonic function. Aliment. Pharmacol. Ther. 27, 104-119 (2008). (Pubitemid 350256609)
73. Benjamin D, Jost JP. Reversal of methylation-mediated repression with short-chain fatty acids: evidence for an additional mechanism to histone deacetylation. Nucleic Acids Res. 29, 3603-3610 (2001). (Pubitemid 32898774)
74. Mariadason JM. HDACs and HDAC inhibitors in colon cancer. Epigenetics 3, 28-37 (2008). (Pubitemid 351540961)
75. Worthley DL, Le Leu RK, Whitehall VL et al. A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. Am. J. Clin. Nutr. 90, 578-586 (2009).
76. Johnson IT. Phytochemicals and cancer. Proc. Nutr. Soc. 66, 207-215 (2007). (Pubitemid 46684974)
77. Dashwood RH, Ho E. Dietary histone deacetylase inhibitors: from cells to mice to man. Semin. Cancer Biol. 17, 363-369 (2007). (Pubitemid 47369168)
78. Johnson IT, Belshaw NJ. Environment, diet and CpG island methylation: Epigenetic signals in gastrointestinal neoplasia. Food Chem. Toxicol. 46, 1346-1359 (2008). (Pubitemid 351258207)
79. Fini L, Piazzi G, Daoud Y et al. Chemoprevention of intestinal polyps in Apc(Min/+) mice fed with western or balanced diets by drinking annurca apple polyphenol extract. Cancer Prev. Res. 4, 907-915 (2011).
80. Issa JP. DNA methylation as a therapeutic target in cancer. Clin. Cancer Res. 13, 1634-1637 (2007).
81. Karahoca M, Momparler RL. Pharmacokinetic and pharmacodynamic analysis of 5-aza-2'-deoxycytidine (decitabine) in the design of its dose-schedule for cancer therapy. Clin. Epigenetics 5, 3 (2013).
82. Fang MZ, Wang Y, Ai N et al. Tea polyphenol (-)-epigallocatechin-3- gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res. 63, 7563-7570 (2003). (Pubitemid 37466673)
83. Wang LS, Arnold M, Huang YW et al. Modulation of genetic and epigenetic biomarkers of colorectal cancer in humans by black raspberries: a Phase I pilot study. Clin. Cancer Res. 17, 598-610 (2011).
84. Wang LS, Kuo CT, Huang TH et al. Black raspberries protectively regulate methylation of wnt pathway genes in precancerous colon tissue. Cancer Prev. Res. (Phila.) 6(12), 1317-1327 (2013).
85. Wang LS, Kuo CT, Stoner K et al. Dietary black raspberries modulate DNA methylation in dextran sodium sulfate (DSS)-induced ulcerative colitis. Carcinogenesis 34(12), 2842-2850 (2013).
86. Wang LS, Kuo CT, Cho SJ et al. Black raspberry-derived anthocyanins demethylate tumor suppressor genes through the inhibition of DNMT1 and DNMT3B in colon cancer cells. Nutr. Cancerl 65, 118-125 (2013).
87. de Vogel S, Schneede J, Ueland PM et al. Biomarkers related to one-carbon metabolism as potential risk factors for distal colorectal adenomas. Cancer Epidemiol. Biomarkers Prev. 20, 1726-1735 (2011).
88. Zhou ZY, Wan XY, Cao JW. Dietary methionine intake and risk of incident colorectal cancer: a meta-analysis of 8 prospective studies involving 431, 029 participants. PLoS ONE 8, e83588 (2013).
89. Lee JE, Giovannucci E, Fuchs CS et al. Choline and betaine intake and the risk of colorectal cancer in men. Cancer Epidemiol. Biomarkers. Prev. 19, 884-887 (2010).