Folate and cancer: how DNA damage, repair and methylation impact on colon carcinogenesis
Corresponding Author
Susan J. Duthie
Nutrition and Epigenetics Group, Division of Vascular Health, Rowett Institute of Nutrition and Health, University of Aberdeen, Greenburn Road, Bucksburn, Aberdeen, AB21 9SB UK
Telephone: +44-1224-712751, Fax: +44-1224-716629, [email protected]
Search for more papers by this authorCorresponding Author
Susan J. Duthie
Nutrition and Epigenetics Group, Division of Vascular Health, Rowett Institute of Nutrition and Health, University of Aberdeen, Greenburn Road, Bucksburn, Aberdeen, AB21 9SB UK
Telephone: +44-1224-712751, Fax: +44-1224-716629, [email protected]
Search for more papers by this authorCommunicated by: Brian Fowler
Competing interest: None declared.
Presented at the International Fulda-Symposium on Homocysteine, Folate and Cobalamin Disorders, Fulda, Germany 11–13 November 2009
Abstract
Inappropriate diet may contribute to one third of cancer deaths. Folates, a group of water-soluble B vitamins present in high concentrations in green, leafy vegetables, maintain DNA stability through their ability to donate one-carbon units for cellular metabolism. Folate deficiency has been implicated in the development of several cancers, including cancer of the colorectum, breast, ovary, pancreas, brain, lung and cervix. Generally, data from the majority of human studies suggest that people who habitually consume the highest level of folate, or with the highest blood folate concentrations, have a significantly reduced risk of developing colon polyps or cancer. However, an entirely protective role for folate against carcinogenesis has been questioned, and recent data indicate that an excessive intake of synthetic folic acid (from high-dose supplements or fortified foods) may increase human cancers by accelerating growth of precancerous lesions. Nonetheless, on balance, evidence from the majority of human studies indicates that dietary folate is genoprotective against colon cancer. Suboptimal folate status in humans is widespread. Folate maintains genomic stability by regulating DNA biosynthesis, repair and methylation. Folate deficiency induces and accelerates carcinogenesis by perturbing each of these processes. This review presents recent evidence describing how these mechanisms act, and interact, to modify colon cancer risk.
References
- Arasaradam RP, Commane DM, Bradburn D, et al (2008) A review of dietary factors and its influence on DNA methylation in colorectal carcinogenesis. Epigenetics, 3: 193–198, .
- Bagley P, Selhub J (1998) A common mutation in the methylenetetrahydrofolate reductase gene is associated with an accumulation of formylated tetrahydrofolates in red blood cells. Proc Natl Acad Sci USA, 95: 13217–13220, .
- Balaghi M, Wagner C (1993) DNA methylation in folate deficiency: use of CpG methylase. Biochem Biophys Res Commun, 193: 1184–1190, .
- Basten GP, Duthie SJ, Pirie L, et al (2006) Sensitivity of markers of DNA stability and DNA repair activity to folate supplementation in healthy volunteers. Brit J Cancer, 94: 1942–1947, .
- Beetstra S, Thomas P, Salisbury C, et al (2005) Folic acid deficiency increases chromosomal instability, chromosome 21 aneuploidy and sensitivity to radiation-induced micronuclei. Mutat Res, 578: 317–326.
- Bigler J, Ulrich CM, Kawashima T, et al (2006) Polymorphisms in hOGG1, XRCC1 and XRCC3 as risk factors for colorectal polyps. Proc Am Assoc Cancer Res, 47: 2051.
- Billson HA, Harrison KL, Lees NP, et al (2009) Dietary variables associated with DNA N7-methylguanine and O6-alkylguanine DNA-alkyltransferase activity in human colorectal mucosa. Carcinogenesis, 30: 615–620, .
- Blount BC, Ames BN (1994) Analysis of uracil in DNA by gas chromatography-mass spectometry. Anal Biochem, 219: 195–200, .
- Blount BC, Mack MM, Wehr CM, et al (1997) Folate deficiency causes uracil misincorporation into human DNA and chromosomal breakage; implications for cancer and neuronal damage. Proc Natl Acad Sci USA, 94: 3290–3295, .
- Bonaa KH, Njolstad I, Ueland PM, et al (2006) NORVIT trial investigators. Homocysteine lowering and cardiovascular events after acute myocardial infarction. N Engl J Med, 354: 1578–1588, .
- Branda RF, LaFayette AR, O'Neill JP, et al (1997) Effect of folate deficiency on mutations at the hprt locus in Chinese hamster ovary cells exposed to monofunctional alkylating agents. Cancer Res, 57: 2586–2588.
- Branda RF, O'Neill JP, Brooks EM, et al (2007) The effect of dietary folic acid deficiency on the cytotoxic and mutagenic responses to methyl methanesulfonate in wild type and in 30 methyladenine DNA glycosylase-deficient Aag null mice. Mutat Res, 615: 12–17.
- Chen J, Giovannucci E, Kelsey K, et al (1996) A methylenetetrahydrofolate reductase polymorphism and the risk of colorectal cancer. Cancer Res, 56: 4862–4864.
- Choi S-W, Kim Y-I, Weitzel JN, Mason JB (1998) Folate depletion impairs DNA excision repair in the colon of the rat. Gut, 43: 93–99, .
- Choi S-W, Stern LL, Dzialo HM, et al (1999) A common polymorphism in the methylenetetrahydrofolate reductase (MTHFR) gene decreases genomic DNA methylation, but does not reduce DNA strand breaks, p53 methylation or uracil misincorporation: implications for colorectal carcinogenesis. Gastroenterol, 116: G1707.
- Christmann M, Tomicic MT, Rood WP, Kaina B (2003) Mechanisms of human DNA repair: an update. Toxicology, 193: 3–34, .
- Cole BF, Baron JA, Sandler RS, et al (2007) Folic acid for the prevention of colorectal adenomas-a randomized clinical trial. JAMA, 297: 2351–2359, .
- Costello JF, Plass C (2001) Methylation matters. J Med Genet, 38: 285–303, .
- Cravo M, Fidalgo P, Pereira AD, et al (1994) DNA methylation as an intermediate biomarker in colorectal cancer: modulation by folic acid supplementation. Eur J Cancer Prev, 3: 473–479, .
- Cravo ML, Pinto AG, Chaves P, et al (1998) Effect of folate supplementation on DNA methylation of rectal mucosa in patients with colonic adenomas: correlation with nutrient intake. Clin Nutr, 17: 45–49, .
- Cravo ML, Albuquerque CM, deSousa S, et al (1998) Microsatellite instability in non-neoplastic mucosa of patients with ulcerative colitis: effect of folate supplementation. Am J Gastroenterol, 93: 2060–2064, .
- Crott JW, Mashiyama ST, Ames BN, Fenech MF (2001) Methylenetetrahydrofolate reductase C677T polymorphism does not alter folic acid deficiency-induced uracil incorporation into human lymphocyte DNA in vitro. Carcinogenesis, 22: 1019–1025, .
- Crott JW, Mashiyama ST, Ames BN, Fenech M (2001) The effect of folic acid deficiency and MTHFR C677T polymorphism on chromosome damage in human lymphocytes in vitro. Cancer Epidemiol Biomarker Prevent, 10: 1089–1096.
- Crott JW, Liu ZH, Choi SW, Mason JB (2007) Folate depletion in human lymphocytes upregulates p53 expression despite marked induction of strand breaks in exons 5–8 of the gene. Mutat Res, 626: 171–179.
- De Boer J, Hoeijmakers JHJ (2000) Nucleotide excision repair and human syndromes. Carcinogenesis, 21: 453–460, .
- De Bont R, vanLarebeke N (2004) Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis, 19: 169–185, .
- DeVos L, Chanson A, Liu Z, et al (2008) Associations between single nucleotide polymprphisms in folate uptake and metabolising genes with blood folate, homocysteine and DNA uracil concentrations. Am J Clin Nutr, 88: 1149–1158.
- Doll R, Peto R (1981) The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst, 66: 1191–11308.
- Duthie SJ, McMillan P (1997) Uracil misincorporation in human DNA detected using single cell gel electrophoresis. Carcinogenesis, 18: 1709–1714, .
- Duthie SJ, Hawdon A (1998) DNA stability (strand breakage, uracil misincorporation, and defective repair) is increased by folic acid depletion in human lymphocytes in vitro. FASEB J, 12: 1491–1497.
- Duthie SJ, Narayanan S, Blum S, Pirie L, Brand GM (2000) Folate deficiency in vitro induces uracil misincorporation, DNA hypomethylation and inhibits DNA excision repair in immortalised normal human colon epithelial cells. Nutr Cancer, 37: 127–133, .
10.1207/S15327914NC372_18 Google Scholar
- Duthie SJ, Grant G, Narayanan S (2000) Increased uracil misincorporation in lymphocytes from folate-deficient rats. Brit J Cancer, 83: 1532–1537, .
- Duthie SJ, Narayanan S, Brand GM, Grant G (2000) DNA stability and genomic methylation status in colonocytes isolated from methyl-donor-deficient rats. Eur J Nutr, 39: 106–111, .
- Duthie SJ, Mavrommatis Y, Rucklidge G, et al (2008) The response of human colonocytes to folate deficiency in vitro: functional and proteomic analysis. J Proteome Res, 7: 3254–3266, .
- Duthie SJ, Pirie LP, Grant G, Watson AJ, Margison GP (2010) Long term folate deficiency differentially alters hepatic and colon MGMT and OGG-1 DNA repair protein expression in rats but has no impact on genome-wide DNA methylation. Cancer Prev Res, 3: 92–100, .
- Ebbing M, Bleie O, Ueland PM, et al (2008) Mortality and cardiovascular events in patients treated with homocysteine-lowering B vitamins after coronary artery angiography: a randomised controlled trial. JAMA, 300: 795–804, .
- Ebbing M, Bonaa KH, Nygard O, et al (2009) Cancer incidence and mortality after treatment with folic acid and vitamin B12. JAMA, 302: 2119–2126, .
- Fenech M, Aitken C, Rinaldi J (1998) Folate, vitamin B12, homocysteine status and DNA damage in young Australian adults. Carcinogenesis, 19: 1163–1171, .
- Figueiredo JC, Grau MV, Wallace K, et al (2009) Globle DNA hypomethylation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol Biomark Prev, 18: 1041–1049, .
- Figueiredo JC, Grau MV, Haile RW, et al (2009) Folic acid and risk of prostate cancer: results from a randomised clinical trial. J Natl Cancer Inst, 101: 432–435, .
- Fortini P, Pascucci B, Parlanti E, et al (2003) 8-oxoguanine DNA damage: at the crossroads of alternative repair pathways. Mutat Res, 531: 127–139.
- Friso S, Choi S-Y, Girelli D, et al (2002) A common mutation in the 5, 10-methylenetetrahydrofolate reductase gene affects genomic DNA methylation status through an interaction with folate status. Proc Natl Acad Sci USA, 99: 5606–5611, .
- Frosst P, Blom HJ, Milos R, et al (1995) Candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet, 10: 111–113, .
- Giovannucci E (2002) Epidemiologic studies of folate and colorectal neoplasia: a review. J Nutr, 132: 2350S–2355S.
- Glynn SA, Albanes D (1994) Folate and cancer-a review of the literature. Nutr Cancer, 22: 101–119, .
- Hirsch S, Sanchez H, Alba C, et al (2009) Colon cancer in Chile before and after the start of the flour fortification program with folic acid. Eur J Gastroenterol Hepatol, 21: 463–469, .
- Ingrosso D, Cimmino A, Perna AF, Masella L (2003) Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinemia in patients with uremia. Blood, 361: 1693–1699.
- Jacob RA, Gretz DM, Taylor PC, et al (1998) Moderate folate depletion increases plasma homocysteine and decreases lymphocyte DNA methylation in postmenopausal women. J Nutr, 128: 1204–1212.
- Jacques PF, Bostom AG, Williams RR, et al (1996) Relation between folate status, a common mutation in methylenetetrahydrofolate reductase, and plasma homocysteine concentrations. Circulation, 93: 7–9.
- James SJ, Yin L (1989) Diet-induced DNA damage and altered nucleotide metabolism in lymphocytes from methyl-donor-deficient rats. Carcinogenesis, 10: 1209–1214, .
- James SJ, Cross DR, Miller BJ (1992) Alterations in nucleotide pools in rats fed diets deficient in choline, methionine and/or folic acid. Carcinogenesis, 13: 2471–2474, .
- James SJ, Pogribny IP, Pogribna M, et al (2003) Mechanisms of DNA damage, DNA hypomethylation and tumour progression in the folate/methyl deficient rat model. J Nutr, 133: 3740S–3747S.
- Kim YI (2007) Folate and colorectal cancer: an evidence-based critical review. Mol Nutr Food Res, 51: 267–292, .
- Kim YI, Salomon RN, Graeme-Cook F, Choi SW (1996) Dietary folate protects against the development of macroscopic colonic neoplasia in a dose-dependent manner in rats. Gut, 39: 732–740, .
- Kim Y-I, Pogribny IP, Salomon RN, et al (1996) Exon-specific DNA hypomethylation of the p53 gene of rat colon induced by dimethylhydrazine: modulation by dietary folate. Am J Clin Pathol, 149: 1129–1137.
- Kim Y-I, Shirwadkar S, Choi S-W, et al (2000) Effects of dietary folate on DNA strand breaks within mutation-prone exons of the p53 gene in rat colon. Gastroenterol, 119: 151–161, .
- Kono S, Chen K (2005) Genetic polymorphisms of methylenetetrahydrofolate reductase and colorectal cancer and adenoma. Cancer Sci, 96: 535–542, .
- Krugman II, Kumaravel TS, Lohani A, et al (2002) Folic acid deficiency and homocysteine impair DNA repair in hippocampal neurons and sensitise them to amyloid toxicity in experimental models of Alzheimer's disease. J Neurosci, 22: 1752–1762.
10.1523/JNEUROSCI.22-05-01752.2002 Google Scholar
- Ma J, Stampfer MJ, Giovannucci E, et al (1997) Methylenetetrahydrofolate reductase polymorphism: dietary interactions and risk of colorectal cancer. Cancer Res, 57: 1098–1102.
- Mason JB, Dickstein A, Jacques PF, et al (2007) A temporal association between folic acid fortification and an increase in colorectal cancer rates may be illuminating important biological principles: a hypothesis. Cancer Epidemiol Biomark Prev, 16: 1325–1329, .
- Melnyk S, Pogribny M, Miller BJ, et al (1999) Uracil misincorporation, DNA strand breaks and gene amplification are associated with tumorigenic cell transformation in folate deficient/repleted Chinese hamster ovary cells. Cancer Letts, 146: 35–44, .
- Narayanan S, McConnell J, Little J, et al (2004) Methylenetetrahydrofolate reductase gene: association with folate metabolism and DNA stability (strand breaks, misincorporated uracil and DNA methylation status). Cancer Epidemiol Biomark Prev, 13: 1–8.
- Paz MF, Avila S, Fraga MF, et al (2002) Germ-line variants in methyl-group metabolism genes and susceptibility to DNA methylation in normal tissues and human primary tumours. Cancer Res, 62: 4519–4524.
- Pogribny IP, Muskheloshvili L, Miller BJ, James SJ (1997) Presence and consequence of uracil in preneoplastic DNA from folate/methyl-deficient rats. Carcinogenesis, 18: 2071–2076, .
- Pogribny IP, James SJ, Jernigan S, Pogribna M (2004) Genomic hypomethylation is specific for preneoplastic liver in folate/methyl deficient rats and does not occur in non-target tissues. Mutat Res, 548: 53–59.
- Povey AC, Lees NP, Harrison KL, Hall CN, Margison GP (2002) Altered O-6-alkylguanine DNA alkyltransferase (MGMT) activity in normal colorectal tissue and adenomas is associated with K-ras GC-AT gene mutations. Proc Am Assoc Cancer Res, 5049: 1020.
- Pufulete M, Al-Ghnaniem R, Khushal A, et al (2005) Effect of folic acid supplementation on genomic DNA methylation in patients with colorectal adenoma. Gut, 54: 648–653, .
- Quinlivan EP, Davis SR, Shelnutt KP, et al (2005) Methylenetetrahydrofolate reductase 677C-T polymorphism anf folate status affect one-carbon incorporation into human DNA deoxynucleosides. J Nutr, 135: 389–396.
- Rampersaud GC, Kauwell GPA, Cerda HAD, JJ BLB (2000) Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr, 72: 998–1003.
- Reidy JA (1988) Role of deoxyuridine incorporation and DNA repair in the expression of human chromosomal fragile sites. Mutat Res, 211: 215–220.
- Sanjoaquin MA, Allen N, Couto E, Roddam AW, Key TJ (2005) Folate intake and colorectal cancer risk: a meta-analytical approach. Int J Cancer, 113: 825–828, .
- Schernhammer ES, Giovannucci E, Kawasaki T, et al (2009) Dietary folate, alcohol and B vitamins in relation to LINE-1 hypomethylation in colon cancer. Gut (e-pub ahead of print).
- Sharp L, Little J (2004) Polymorphisms in genes involved in folate metabolism and colorectal neoplasia: a HuGE review. Am J Epidemiol, 159: 423–443, .
- Sohn Y-J, Stempack JM, Reid S, et al (2003) The effect of dietary folate on genomic and p53-specific DNA methylation in rat colon. Carcinogenesis, 24: 81–90, .
- Sohn KJ, Jang H, Campan M, et al (2009) The methylenetetrahydrofolate reductase C677T mutation induces cell-specific changes in genomic DNA methylation and uracil misincorporation: a possible molecular basis for the site-specific cancer modification. Int J Cancer, 124: 1999–2005, .
- Song J, Medline A, Mason JB, Gallinger S, Kim Y-I (2000) Effects of dietary folate on intestinal tumorigenesis in the ApcMin Msh mouse. Cancer Res, 60: 3191–3199.
- Song J, Sohn K-J, Medline A, Ash C, Gallinger S, Kim Y-I (2000) Chemopreventive effects of dietary folate on intestinal polyps in Apc+/-Msh-/-mice. Cancer Res, 6: 3191–3199.
- Stempak JM, Sohn K-Y, Chiang E-P, Shane B, Kim Y-I (2005) 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, .
- Stern LL, Mason JB, Selhub J, Choi SW (2000) Genomic DNA hypomethylation, a characteristic of most cancers, is present in peripheral leukocytes of individuals who are homozygous for the C677T polymorphism in the methylenetetrahydrofolate reductase gene. Cancer Epidemiol Biomark Prev, 9: 849–853.
- Stolzenberg-Solomon RZ, Chang SC, Leitzmann MF, et al (2006) Folate intake, alcohol use and postmenopausal breast cancer risk in the Prostate Lung Colorectal and Ovarian Cancer Screening Trial. Am J Clin Nutr, 83: 895–904.
- van denDonk M, Pellis L, Crott JW, et al (2007) Folic acid and vitamin B12 supplementation does not favorably influence uracil misincorporation and promoter methylation in rectal mucosa DNA of subjects with previous colorectal adenomas. J Nutr, 137: 2114–2120.
10.1093/jn/137.9.2114 Google Scholar
- Wainfan E, Poirier LA (1992) Methyl groups in carcinogenesis: effects on DNA methylation and gene expression. Cancer Res, 52: 2071s–2077s.
- Wasson GR, McGlynn AP, McNulty H, et al (2006) Global DNA and p53 region-specific hypomethylation in human colonic cells is induced by folate depletion and reversed by folate supplementation. J Nutr, 136: 2748–2753.
- Wei Q, Shen H, Wang LE, et al (2003) Association between low dietary folate intake and suboptimal cellular DNA repair capacity. Cancer Epidemiol Biomark Prev, 12: 963–969.
- Whitehouse A, Meredith DM, Markham AF (1998) DNA mismatch repair genes and their association with colorectal cancer. Int J Mol Med, 1: 469–474.
- Wickramasinghe SN, Fida S (1994) Bone marrow cells from vitamin B12-and folate-deficient patients misincorporate uracil into DNA. Blood, 83: 1656–1661.
- (2007) Food, nutrition, physical activity and the prevention of cancer: a global perspective, Washington: American Institute of Cancer Research.
- Yang Q, Bostick RM, Friedman JM, Flanders WD (2009) Serum folate and cancer mortality among US adults: findings from the third national health and nutritional examination survey linked mortality file. Cancer Epidemiol Biomark Prev, 18: 1439–1447, .
- Zijno A, Andreoli C, Leopardi P, et al (2003) Folate status, metabolic genotype and biomarkers of genotoxicity in healthy subjects. Carcinogenesis, 24: 1097–1103, .