Postweaning dietary folate deficiency provided through childhood to puberty permanently increases genomic DNA methylation in adult rat liver

Journal of Nutrition

Volumn 138, Issue 4, 2008, Pages 703-709

  Kotsopoulos, Joanne ^a   Sohn, Kyoung Jin ^b   Kim, Young In ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FOLIC ACID; GENOMIC DNA;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHILDHOOD; CONTROLLED STUDY; DIET SUPPLEMENTATION; DNA DETERMINATION; DNA METHYLATION; EPIGENETICS; FEMALE; FOLIC ACID DEFICIENCY; LIVER; NONHUMAN; PUBERTY; RAT; WEANING;

RATTUS;

EID: 41549104304     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/138.4.703     Document Type: Article

References (59)

1. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002;3:415-28.
2. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8:286-98.
3. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med. 2003;349:2042-54.
4. Li E, Jaenisch R. DNA methylation and methyltransferases. In: Ehrlich M, editor. DNA alterations in cancer: genetic and epigenetic changes. Natick (MA): Eaton Publishing; 2000. p. 351-65.
5. Shane B. Folate chemistry and metabolism. In: Bailey LB, editor. Folate in health and disease. New York: Marcel Dekker; 1995. p. 1-22.
6. Kim YI. Nutritional epigenetics: impact of folate deficiency on DNA methylation and colon cancer susceptibility. J Nutr. 2005;135:2703-9.
7. Christman JK, Sheikhnejad G, Dizik M, Abileah S, Wainfan E. Reversibility of changes in nucleic acid methylation and gene expression induced in rat liver by severe dietary methyl deficiency. Carcinogenesis. 1993;14:551-7.
8. Dizik M, Christman JK, Wainfan E. Alterations in expression and methylation of specific genes in livers of rats fed a cancer promoting methyl-deficient diet. Carcinogenesis. 1991;12:1307-12.
9. Pogribny IP, Basnakian AG, Miller BJ, Lopatina NG, Poirier LA, James SJ. Breaks in genomic DNA and within the p53 gene are associated with hypomethylation in livers of folate/methyl-deficient rats. Cancer Res. 1995;55:1894-901.
10. Pogribny IP, Miller BJ, James SJ. Alterations in hepatic p53 gene methylation patterns during tumor progression with folate/methyl deficiency in the rat. Cancer Lett. 1997;115:31-8.
11. Pogribny IP, Poirier LA, James SJ. Differential sensitivity to loss of cytosine methyl groups within the hepatic p53 gene of folate/methyl deficient rats. Carcinogenesis. 1995;16:2863-7.
12. Wainfan E, Dizik M, Stender M, Christman JK. Rapid appearance of hypomethylated DNA in livers of rats fed cancer-promoting, methyl-deficient diets. Cancer Res. 1989;49:4094-7.
13. Wainfan E, Kilkenny M, Dizik M. Comparison of methyltransferase activities of pair-fed rats given adequate or methyl-deficient diets. Carcinogenesis. 1988;9:861-3.
14. Wainfan E, Poirier LA. Methyl groups in carcinogenesis: effects on DNA methylation and gene expression. Cancer Res. 1992;52:s2071-7.
15. Zapisek WF, Cronin GM, Lyn-Cook BD, Poirier LA. The onset of oncogene hypomethylation in the livers of rats fed methyl-deficient, amino acid-defined diets. Carcinogenesis. 1992;13:1869-72.
16. Pogribny IP, James SJ, Jernigan S, Pogribna M. Genomic hypomethylation is specific for preneoplastic liver in folate/methyl deficient rats and does not occur in non-target tissues. Mutat Res. 2004;548:53-9.
17. Pogribny IP, Ross SA, Wise C, Pogribna M, Jones EA, Tryndyak VP, James SJ, Dragan YP, Poirier LA. Irreversible global DNA hypomethylation as a key step in hepatocarcinogenesis induced by dietary methyl deficiency. Mutat Res. 2006;593:80-7.
18. Kim YI. Folate and DNA methylation: a mechanistic link between folate deficiency and colorectal cancer? Cancer Epidemiol Biomarkers Prev. 2004;13:511-9.
19. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293:1089-93.
20. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33: Suppl:245-54.
21. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol. 2003;23:5293-300.
22. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998;12:949-57.
23. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG. Maternal methyl supplements increase offspring DNA methylation at Axin Fused. Genesis. 2006;44:401-6.
24. Walzem RL, Clifford AJ. Folate deficiency in rats fed diets containing free amino acids or intact proteins. J Nutr. 1988;118:1089-96.
25. Kim YI, Christman JK, Fleet JC, Cravo ML, Salomon RN, Smith D, Ordovas J, Selhub J, Mason JB. Moderate folate deficiency does not cause global hypomethylation of hepatic and colonic DNA or c-myc-specific hypomethylation of colonic DNA in rats. Am J Clin Nutr. 1995;61:1083-90.
26. Kim YI, Pogribny IP, Salomon RN, Choi SW, Smith DE, James SJ, Mason JB. Exon-specific DNA hypomethylation of the p53 gene of rat colon induced by dimethylhydrazine. Modulation by dietary folate. Am J Pathol. 1996;149:1129-37.
27. Kim YI, Salomon RN, Graeme-Cook F, Choi SW, Smith DE, Dallal GE, Mason JB. Dietary folate protects against the development of macroscopic colonic neoplasia in a dose responsive manner in rats. Gut. 1996;39:732-40.
28. Kotsopoulos J, Medline A, Renlund R, Sohn KJ, Martin R, Hwang SW, Lu S, Archer MC, Kim YI. Effects of dietary folate on the development and progression of mammary tumors in rats. Carcinogenesis. 2005;26:1603-12.
29. Kotsopoulos J, Sohn KJ, Martin R, Choi M, Renlund R, McKerlie C, Hwang SW, Medline A, Kim YI. Dietary folate deficiency suppresses N-methyl-N- nitrosourea-induced mammary tumorigenesis in rats. Carcinogenesis. 2003;24:937-44.
30. Song J, Sohn KJ, Medline A, Ash C, Gallinger S, Kim YI. Chemopreventive effects of dietary folate on intestinal polyps in Apc+/-Msh2-/-mice. Cancer Res. 2000;60:3191-9.
31. Cravo ML, Mason JB, Dayal Y, Hutchinson M, Smith D, Selhub J, Rosenberg IH. Folate deficiency enhances the development of colonic neoplasia in dimethylhydrazine-treated rats. Cancer Res. 1992;52:5002-6.
32. Rong N, Selhub J, Goldin BR, Rosenberg IH. Bacterially synthesized folate in rat large intestine is incorporated into host tissue folyl polyglutamates. J Nutr. 1991;121:1955-9.
33. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123:1939-51.
34. Choumenkovitch SF, Selhub J, Wilson PW, Rader JI, Rosenberg IH, Jacques PF. Folic acid intake from fortification in United States exceeds predictions. J Nutr. 2002;132:2792-8.
35. Lewis CJ, Crane NT, Wilson DB, Yetley EA. Estimated folate intakes: data updated to reflect food fortification, increased bioavailability, and dietary supplement use. Am J Clin Nutr. 1999;70:198-207.
36. Pfeiffer CM, Caudill SP, Gunter EW, Osterloh J, Sampson EJ. Biochemical indicators of B vitamin status in the US population after folic acid fortification: results from the National Health and Nutrition Examination Survey 1999-2000. Am J Clin Nutr. 2005;82:442-50.
37. Quinlivan EP, Gregory JF III. Effect of food fortification on folic acid intake in the United States. Am J Clin Nutr. 2003;77:221-5.
38. Tamura T. Microbiological assay of folate. In: Piccairo MF, Stokstad R, Gregory JF, editors. Folic acid metabolism in health and disease. New York: Wiley-Liss; 1990. p. 121-37.
39. Varela-Moreiras G, Selhub J. Long-term folate deficiency alters folate content and distribution differentially in rat tissues. J Nutr. 1992;122:986-91.
40. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 1991;19:4293.
41. Kim YI, Pogribny IP, Basnakian AG, Miller JW, Selhub J, James SJ, Mason JB. Folate deficiency in rats induces DNA strand breaks and hypomethylation within the p53 tumor suppressor gene. Am J Clin Nutr. 1997;65:46-52.
42. Sohn KJ, Stempak JM, Reid S, Shirwadkar S, Mason JB, Kim YI. The effect of dietary folate on genomic and p53-specific DNA methylation in rat colon. Carcinogenesis. 2003;24:81-90.
43. Clifford AJ, Wilson DS, Bills ND. Repletion of folate-depleted rats with an amino acid-based diet supplemented with folic acid. J Nutr. 1989;119:1956-61.
44. Min mouse. Cancer Res. 2000;60:5434-40.
45. Henning SM, McKee RW, Swendseid ME. Hepatic content of S-adenosylmethionine, S-adenosylhomocysteine and glutathione in rats receiving treatments modulating methyl donor availability. J Nutr. 1989;119:1478-82.
46. Shivapurkar N, Poirier LA. Tissue levels of S-adenosylmethionine and S-adenosylhomocysteine in rats fed methyl-deficient, amino acid-defined diets for one to five weeks. Carcinogenesis. 1983;4:1051-7.
47. Ghoshal K, Li X, Datta J, Bai S, Pogribny I, Pogribny M, Huang Y, Young D, Jacob ST. 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. 2006;136:1522-7.
48. Selhub J. Homocysteine metabolism. Annu Rev Nutr. 1999;19:217-46.
49. Horne DW, Cook RJ, Wagner C. Effect of dietary methyl group deficiency on folate metabolism in rats. J Nutr. 1989;119:618-21.
50. Selhub J, Seyoum E, Pomfret EA, Zeisel SH. Effects of choline deficiency and methotrexate treatment upon liver folate content and distribution. Cancer Res. 1991;51:16-21.
51. Kim YI, Miller JW, da Costa KA, Nadeau M, Smith D, Selhub J, Zeisel SH, Mason JB. Severe folate deficiency causes secondary depletion of choline and phosphocholine in rat liver. J Nutr. 1994;124:2197-203.
52. Balaghi M, Wagner C. DNA methylation in folate deficiency: use of CpG methylase. Biochem Biophys Res Commun. 1993;193:1184-90.
53. Miller JW, Nadeau MR, Smith J, Smith D, Selhub J. Folate-deficiency- induced homocysteinaemia in rats: disruption of S-adenosylmethionine's co-ordinate regulation of homocysteine metabolism. Biochem J. 1994;298:415-9.
54. Achon M, Alonso-Aperte E, Ubeda N, Varela-Moreiras G. Supranormal dietary folic acid supplementation: effects on methionine metabolism in weanling rats. Br J Nutr. 2007;98:490-6.
55. Choi SW, Friso S, Keyes MK, Mason JB. Folate supplementation increases genomic DNA methylation in the liver of elder rats. Br J Nutr. 2005;93:31-5.
56. Waterland RA, Lin JR, Smith CA, Jirtle RL. Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum Mol Genet. 2006;15:705-16.
57. Cropley JE, Suter CM, Beckman KB, Martin DIK. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proc Natl Acad Sci USA. 2006;103:17308-12.
58. 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. 2005;26:981-90.
59. Jhaveri MS, Wagner C, Trepel JB. Impact of extracellular folate levels on global gene expression. Mol Pharmacol. 2001;60:1288-95.