Role of dietary mutagens in cancer and atherosclerosis

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 12, Issue 4, 2009, Pages 343-349

  Ferguson, Lynnette R ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Atherosclerosis; Cancer; Cardiovascular disease; DNA adducts; Mutation; Reactive species

Indexed keywords

AFLATOXIN B1; ARISTOLOCHIC ACID; BENZO[A]PYRENE; CLASTOGEN; MUTAGENIC AGENT;

ARTERY MUSCLE; ATHEROSCLEROSIS; CARCINOGENESIS; CHROMOSOME MUTATION; COOKING; DNA ADDUCT; DNA DAMAGE; FAMILIAL CANCER; FOOD CONTAMINATION; FOOD PROCESSING; GENE ACTIVATION; GENE IDENTIFICATION; GENE INACTIVATION; GENETIC ASSOCIATION; GENOME; HUMAN; MOLECULAR EPIDEMIOLOGY; MUTAGENIC ACTIVITY; NEOPLASM; NONHUMAN; ONCOGENE; OXIDATIVE STRESS; REVIEW; RISK FACTOR; SMOOTH MUSCLE FIBER; SOMATIC MUTATION; TUMOR SUPPRESSOR GENE;

ATHEROSCLEROSIS; CARCINOGENS; DIET; DNA ADDUCTS; DNA DAMAGE; GENES, TUMOR SUPPRESSOR; HUMANS; MUTAGENS; NEOPLASMS; ONCOGENES;

EID: 68049092059     PISSN: 13631950     EISSN: 14736519     Source Type: Journal    
DOI: 10.1097/MCO.0b013e32832c2237     Document Type: Review

References (80)

1. Waxman A. WHO global strategy on diet, physical activity and health. Food Nutr Bull 2004; 25:292-302.
2. Ross JS, Stagliano NE, Donovan MJ, et al. Atherosclerosis and cancer: common molecular pathways of disease development and progression. An N Y Acad Sci 2001; 947:271-292; discussion 292-273.
3. Andreassi MG. Coronary atherosclerosis and somatic mutations: an overview of the contributive factors for oxidative DNA damage. Mutat Res 2003; 543:67-86.
4. Ramos KS, Partridge CR. Atherosclerosis and cancer: flip sides of the neoplastic response in mammalian cells? Cardiovasc Toxicol 2005; 5:245-255.
5. Gudmundsson J, Sulem P, Rafnar T, et al. Common sequence variants on 2p15 and Xp11.22 confer susceptibility to prostate cancer. Nat Genet 2008; 40:281-283.
6. Eeles RA, Kote-Jarai Z, Giles GG, et al. Multiple newly identified loci associated with prostate cancer susceptibility. Nat Genet 2008; 40:316-321.
7. Thomas G, Jacobs KB, Yeager M, et al. Multiple loci identified in a genomewide association study of prostate cancer. Nat Genet 2008; 40:310-315.
8. Burton PR, Clayton DG, Cardon LR, et al. Genome-wide association study of 14 000 cases of seven common diseases and 3000 shared controls. Nature 2007; 447:661-678.
9. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61:759-767.
10. De Flora S, Ferguson LR. Overview of mechanisms of cancer chemopreventive agents. Mutat Res 2005; 591:8-15.
11. Andreassi MG, Botto N, Colombo MG, et al. Genetic instability and atherosclerosis: can somatic mutations account for the development of cardiovascular diseases? Environ Mol Mutagene 2000; 35:265-269.
12. Andreassi MG. DNA damage, vascular senescence and atherosclerosis. J Mol Med 2008; 86:1033-1043. This useful review collates recent evidence on the role played by oxidative-stressinduced DNA damage and dysfunctional telomeres in the pathogenesis of atherosclerosis. It suggests that, though there is an association between various mutational events and atherosclerosis, this may not necessarily show a causal relationship but instead may reveal a role for an activated DNA response pathway in cellular vascular senescence.
13. van Schooten FJ, Knaapen AM, Izzotti A, et al. DNA damage, mutagenesis and cardiovascular disease. Mutat Res 2007; 621:1-4.
14. De Flora S, Izzotti A. Mutagenesis and cardiovascular diseases: molecular mechanisms, risk factors, and protective factors.Mutat Res 2007; 621:5-17.
15. Velculescu VE. Defining the blueprint of the cancer genome. Carcinogenesis 2008; 29:1087-1091. This review summarizes recent work using some of the newer and more sensitive methods for sequencing and bioinformatic approaches to consider the number and type of alterations responsible for the development of common tumor types. Such systematic studies originally revealed the importance of signal transduction gene in several tumor types and have now been extended to include the majority of protein-coding genes in breast and colorectal cancers. Such analyses have identified new genes and pathways not hitherto linked to human cancer, thereby suggesting new targets for personalized diagnostic and therapeutic intervention and indicating directions for future large-scale genomic analyses in human tumors.
16. Zaridze DG. Molecular epidemiology of cancer. Biochemistry (Russia) 2008; 73:532-542. This review considers the role of molecular markers for the assessment of individual exposure to carcinogenic agents and provides specific examples of the studies relating mutation patterns to specific carcinogenic exposures. These methods provide an essential link in proving the relationship between specific dietary mutagen exposures and cancer development. It considers the implications of genetic polymorphisms and their role in the interaction between diet, environmental factors, lifestyles and cancer risk.
17. Shelling AN, Ferguson LR. Genetic variation in human disease and a new role for copy number variants. Mutat Res 2007; 622:33-41.
18. Sonnenschein C, Soto AM. Theories of carcinogenesis: an emerging perspective. Semin Cancer Biol 2008; 18:372-377.
19. Laconi E, Doratiotto S, Vineis P. The microenvironments of multistage carcinogenesis. Semin Cancer Biol 2008; 18:322-329.
20. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington DC: American Institute for Cancer Research; 2007.
21. Ferguson LR, Philpott M. Nutrition and mutagenesis. Ann Rev Nutr 2008; 28:313-329. A recent review on the nature of dietary mutagens, their role in mutagenesis and methods of human study.
22. Bonassi S, Znaor A, Ceppi M, et al. An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis 2007; 28:625-631.
23. Bonassi S, Norppa H, Ceppi M, et al. Chromosomal aberration frequency in lymphocytes predicts the risk of cancer: results from a pooled cohort study of 22 358 subjects in 11 countries. Carcinogenesis 2008; 29:1178-1183.
24. Iarmarcovai G, Ceppi M, Botta A, et al. Micronuclei frequency in peripheral blood lymphocytes of cancer patients: a meta-analysis. Mutat Res 2008; 659:274-283. This meta-analysis assesses the frequency of micronuclei, as a biomarker of chromosomal damage, genome instability and cancer risk, in cancer patients. It substantiates the existing evidence concerning the role of chromosomal mutation in various steps of carcinogenesis.
25. Ross R. The pathogenesis of atherosclerosis: an update. N Engl J Med 1986; 314:488-500.
26. Ross R. Atherosclerosis: an inflammatory disease [see comment]. N Engl J Med 1999; 340:115-126.
27. Izzotti A, De Flora S, Petrilli GL, et al. Cancer biomarkers in human atherosclerotic lesions: detection of DNA adducts, cancer epidemiology. Biomarkers Prev 1995; 4:105-110.
28. Nair J, De Flora S, Izzotti A, et al. Lipid peroxidation-derived etheno-DNA adducts in human atherosclerotic lesions. Mutat Res 2007; 621:95-105.
29. Binková B, Smerhovský Z, Strejc P, et al. DNA-adducts and atherosclerosis: a study of accidental and sudden death males in the Czech Republic. Mutat Res 2002; 501:115-128.
30. Martinet W, Knaapen MW, De Meyer GR, et al. Elevated levels of oxidative DNA damage and DNA repair enzymes in human atherosclerotic plaques. Circulation 2002; 106:927-932.
31. Collins AR, Gedik CM, Olmedilla B, et al. Oxidative DNA damage measured in human lymphocytes: large differences between sexes and between countries, and correlations with heart disease mortality rates. FASEB J 1998; 12:1397-1400.
32. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci U S A 1973; 70:1753-1756.
33. Trosko JE, Chang CC. An integrative hypothesis linking cancer, diabetes and atherosclerosis: the role of mutations and epigenetic changes. Med Hypotheses 1980; 6:455-468.
34. Majesky MW, Reidy MA, Benditt EP, et al. Focal smooth muscle proliferation in the aortic intima produced by an initiation-promotion sequence. Proc Natl Acad Sci U S A 1985; 82:3450-3454.
35. Bridges BA, Bowyer DE, Hansen ES, et al. International commission for protection against environmental mutagens and carcinogens: the possible involvement of somatic mutations in the development of atherosclerotic plaques - Report of ICPEMC Subcommittee 7/1: Conclusions and recommendations. Mutat Res 1990; 239:143-148.
36. De Flora S, Izzotti A, Randerath K, et al. DNA adducts and chronic degenerative disease. Pathogenetic relevance and implications in preventive medicine. Mutat Res 1996; 366:197-238.
37. Federici C, Botto N, Manfredi S, et al. Relation of increased chromosomal damage to future adverse cardiac events in patients with known coronary artery disease. Am J Cardiol 2008; 102:1296-1300. A prospective study that establishes high levels of chromosome damage as predictors of subsequent adverse cardiac events in high-risk patients. Although dietary (or other) mutagens cannot be established as causal, such an approach, combined with nutritional epidemiology, could help confirm the role of these in atherosclerosis.
38. Casalone R, Granata P, Minelli E, et al. Cytogenetic analysis reveals clonal proliferation of smooth muscle cells in atherosclerotic plaques. Hum Genet 1991; 87:139-143.
39. Vanni R, Licheri S. Clonal cytogenetic changes in atheroslcerotic plaques including trisomy 20. Dis Markers 1991; 9:81-85.
40. Matturri L, Cazzullo A, Turconi P, et al. Cytogenetic aspects of cell proliferation in atherosclerotic plaques. Cardiologia (Rome, Italy) 1997; 42:833-836.
41. Penn A, Snyder C. Arteriosclerotic plaque development is 'promoted' by polynuclear aromatic hydrocarbons. Carcinogenesis 1988; 9:2185-2189.
42. Sorensen M, Autrup H, Moller P, et al. Linking exposure to environmental pollutants with biological effects. Mutat Res 2003; 544:255-271.
43. Knaapen AM, Curfs DM, Pachen DM, et al. The environmental carcinogen benzo[a]pyrene induces expression of monocyte-chemoattractant protein-1 in vascular tissue: a possible role in atherogenesis. Mutat Res 2007; 621:31-41.
44. Godschalk R, Curfs D, Bartsch H, et al. Benzo[a]pyrene enhances lipid peroxidation induced DNA damage in aorta of apolipoprotein E knockout mice. Free Radic Res 2003; 37:1299-1305.
45. Ferguson LR, Philpott M, Karunasinghe N. Dietary cancer and prevention using antimutagens. Toxicology 2004; 198:147-159.
46. Shahin M, Smith BL, Prakash AS. Bracken carcinogens in the human diet. Mutat Res 1999; 443:69-79.
47. Fu PP, Xia Q, Lin G, et al. Pyrrolizidine alkaloids: genotoxicity, metabolism enzymes, metabolic activation, and mechanisms. Drug Metab Rev 2004; 36:1-55.
48. Prakash AS, Pereira TN, Reilly PE, et al. Pyrrolizidine alkaloids in human diet. Mutat Res 1999; 443:53-67.
49. Mei N, Guo L, Fu PP, et al. Mutagenicity of comfrey (Symphytum Officinale) in rat liver. Br J Cancer 2005; 92:873-875.
50. Sayre RM, Dowdy JC. The increase in melanoma: are dietary furocoumarins responsible? Med Hypotheses 2008; 70:855-859.
51. Eastmond DA, Macgregor JT, Slesinski RS, et al. Trivalent chromium: assessing the genotoxic risk of an essential trace element and widely used human and animal nutritional supplement. Crit Rev Toxicol 2008; 38:173-190. Trivalent chromium [Cr(III)] is an essential nutrient that is widely used as a nutritional supplement for humans and animals. This review summarizes literature since 1990 on genotoxic effects of Cr(III) compounds to conclude that Cr(III) can react with DNA and cause DNA damage in cell culture systems but is unlikely to be mutagenic in humans at current exposure levels.
52. Gatz SA, Wiesmuller L. Take a break: resveratrol in action on DNA. Carcinogenesis 2008; 29:321-332. This review considers the potential genotoxic effects of resveratrol (RV), a material commonly extracted from grape seeds, that has been suggested to have antiaging and anticancer effects. It raises the possibility that resveratrol could have undesirable effects on genomic integrity and requires more targeted in-vivo study.
53. Smela ME, Currier SS, Bailey EA, et al. The chemistry and biology of aflatoxin B(1): from mutational spectrometry to carcinogenesis. Carcinogenesis 2001; 22:535-545.
54. Pfohl-Leszkowicz A, Manderville RA. Ochratoxin A: an overview on toxicity and carcinogenicity in animals and humans. Mol Nutr Food Res 2007; 51:61-99; Erratum in appears in Mol Nutr Food Res 2007; 51:1192..
55. Nedelko T, Arlt VM, Phillips DH, et al. TP53 mutation signature supports involvement of aristolochic acid in the aetiology of endemic nephropathy-associated tumours. Int J Cancer 2009; 124:987-990. A good summary of the evidence leading to the conclusion that mutagen that is found in the diet in the Balkans is likely to be involved in the etiology of a common cancer.
56. Grollman AP, Shibutani S, MoriyaM, et al. Aristolochic acid and the etiology of endemic (Balkan) nephropathy. Proc Natl Acad Sci U S A 2007; 104: 12129-12134.
57. Turesky RJ. Formation and biochemistry of carcinogenic heterocyclic aromatic amines in cooked meats. Toxicol Lett 2007; 168:219-227.
58. Phillips DH. Polycyclic aromatic hydrocarbons in the diet. Mutat Res 1999; 443:139-147.
59. Lijinsky W. N-Nitroso compounds in the diet. Mutat Res 1999; 443:129-138.
60. Bingham SA, Pignatelli B, Pollock JR, et al. Does increased endogenous formation of N-nitroso compounds in the human colon explain the association between red meat and colon cancer? Carcinogenesis 1996; 17:515-523.
61. Besaratinia A, Pfeifer GP. Investigating human cancer etiology by DNA lesion footprinting and mutagenicity analysis. Carcinogenesis 2006; 27:1526-1537.
62. Exon JH. A review of the toxicology of acrylamide. J Toxicol Environ Health B Critl Rev 2006; 9:397-412.
63. Sevanian A, Peterson AR. The cytotoxic and mutagenic properties of cholesterol oxidation products. Food Chem Toxicol 1986; 24:1103-1110.
64. Kendall CW, Koo M, Sokoloff E, et al. Effect of dietary oxidized cholesterol on azoxymethane-induced colonic preneoplasia in mice. Cancer Lett 1992; 66:241-248.
65. Imai H, Werthessen NT, Subramanyam V, et al. Angiotoxicity of oxygenated sterols and possible precursors. Science 1980; 207:651-653.
66. Morin RJ, Peng SK. The role of cholesterol oxidation products in the pathogenesis of atherosclerosis. Ann Clin Lab Sci 1989; 19:225-237.
67. Abstracts of the 14th Annual Meeting of the Society for Free Radical Biology and Medicine (SFRBM), 14-18 November2007; Washington, DC, USA; Free Radic Biol Med 43 (Suppl 1); 2007.
68. Norrish AE, Ferguson LR, Knize MG, et al. Heterocyclic amine content of cooked meat and risk of prostate cancer. J Natl Cancer Inst 1999; 91:2038-2044.
69. Koutros S, Cross AJ, Sandler DP, et al. Meat and meat mutagens and risk of prostate cancer in the agricultural health study. Cancer Epidemiol Biomarkers Preven 2008; 17:80-87. A large prospective study that associates meat types, meat cooking methods, meat doneness and meat mutagens and the risk for prostate cancer in the Agricultural Health Study. It reports no association between meat type or specific cooking method and prostate cancer risk. However, intake of well or very well done total meat and that of the two heterocyclic amines 2-amino-3,4,8-trimethylimidazo-[4,5-f]-quinoxaline and 2-amino-3,8-dimethylimidazo-[4,5-b]quinoxaline were associated with increased risk.
70. Stolzenberg-Solomon RZ, Cross AJ, Silverman DT, et al. Meat and meatmutagen intake and pancreatic cancer risk in the NIH-AARP cohort, Cancer Epidemiology. Biomarkers Preven 2007; 16:2664-2675.
71. Lea IA, Jackson MA, Li X, et al. Genetic pathways and mutation profiles of human cancers: site- and exposure-specific patterns. Carcinogenesis 2007; 28:1851-1858.
72. Pfeifer GP, Hainaut P. On the origin of G ? T transversions in lung cancer. Mutat Res 2003; 526:39-43.
73. Pineau P, Marchio A, Battiston C, et al. Chromosome instability in human hepatocellular carcinoma depends on p53 status and aflatoxin exposure. Mutat Res 2008; 653:6-13. This study provides a detailed molecular characterization of mutations in 15 different genomic targets, including allelic loss at 13 chromosome arms and mutations of beta-catenin and p53 genes in 223 HCC, and relates this to intake of the dietary mutagen, AFB1. European samples were provided by 90 cases from Italy, 81 samples from France, in comparison with 52 specimens from Shanghai. Italian and French cases did not significantly differ for 14 of the 15 targets tested, whereas tumors from Shanghai were significantly different, with half of the changes in TP53 showing the Arg249Ser mutation, hallmark of exposure to AFB1.
74. Ferguson LR. Biomarkers as endpoints in intervention studies. In Vineis P, Garte S, Wild C, editors. Molecular epidemiology of chronic diseases: new techniques and approaches. Ealing Broadway, London: John Wiley and Sons Ltd; 2008. pp. 255-266. A recent review on the use of biomarkers in relating mutagen exposure, or reduction of mutagen exposure, to disease endpoints.
75. Albert RE, Vanderlaan M, Burns FJ, et al. Effect of carcinogens on chicken atherosclerosis. Cancer Res 1977; 37:2232-2235.
76. Curfs DM, Lutgens E, Gijbels MJ, et al. Chronic exposure to the carcinogenic compound benzo[a]pyrene induces larger and phenotypically different atherosclerotic plaques in ApoE-knockout mice. Am J Pathol 2004; 164:101-108.
77. Van Schooten FJ, Hirvonen A, Maas LM, et al. Putative susceptibility markers of coronary artery disease: association between VDR genotype, smoking, and aromatic DNA adduct levels in human right atrial tissue. FASEB J 1998; 12:1409-1417.
78. de Nigris F, Sica V, Herrmann J, et al. c-Myc oncoprotein: cell cycle-related events and new therapeutic challenges in cancer and cardiovascular diseases. Cell Cycle 2003; 2:325-328.
79. Mercer J, Mahmoudi M, Bennett M. DNA damage, p53, apoptosis and vascular disease. Mutat Res 2007; 621:75-86.
80. Johnson CD, Balagurunathan Y, Lu KP, et al. Genomic profiles and predictive biological networks in oxidant-induced atherogenesis. Physiol Genomics 2003; 13:263-275.