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Diet, genetic susceptibility and carcinogenesis

Published online by Cambridge University Press:  27 September 2007

Paolo Vineis*
Affiliation:
Unit of Cancer Epidemiology, University of Torino and CPO-Piemonte, via Santena 7 10126 Torino, Italy
*
*Corresponding author: Email [email protected]
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Abstract

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At least six types of gene–environment interactions (GEI) have been proposed (Kouhry and Wagener, 1993) In the first type, neither the environmental exposure (EE) nor the genetic risk factor (GRF) have any effect by themselves, but interaction between them causes disease. This is the case of phenylalanine exposure and the phenylketonuria genotype. Type 2 is a situation in which the GRF has no effect on disease in the absence of exposure, but exacerbates the effects of the latter. This is the most important type of GEI in relation to metabolic susceptibility genes and human carcinogenesis. The third type is the converse of the second (EE is ineffective per se, but enhances the effect of GRF). Type 4 occurs when both EE and GRF increase the risk for disease, but the combination is interactive or synergistic: an example is the interaction between Xeroderma Pigmentosum and UV radiation. Types 5 and 6, according to the classification proposed by Kouhry, refer to cases in which the GRF is protective.

The model of GEI that is emerging as the most important in chemical carcinogenesis refers to metabolic susceptibility genes. The general population can be divided into subgroups depending on their susceptibility to the action of carcinogens, based on their ability to metabolize such compounds to electrophilic, reactive metabolites (which form adducts with DNA), or, respectively, electrophobic metabolites that are excreted. The present contribution is a short review of the relevant literature, with particular emphasis on some polymorphisms involved in dietary exposures. In addition, the practical implications of genetic testing in this field are discussed.

Type
Research Article
Copyright
Copyright © CABI Publishing 2001

References

1Vogelstein, B, Kinzler, KW. The genetic basis of human cancer. McGraw-Hill, New York, 1998.Google Scholar
2Shen, MR, Jones, IM, Mohrenweiser, H.Nonconservative amino acid substitution variants exist at polymorphic frequncy in DNA repair genes in healthy humans. Cancer Res. 1998; 58: 604608.Google Scholar
3Bailey, LB, Gregory, JF 3rd. Polymorphisms of methylenetetrahydrofolate reductase and other enzymes: metabolic significance, risks and impact on folate requirement. J. Nutr. 1999; 129(5): 919922.CrossRefGoogle ScholarPubMed
4Zhang, S, Hunter, DJ, Forman, MR, Rosner, BA, Speizer, FE, Colditz, GA, Manson, JE, Hankinson, SE, Willett, WC. Dietary carotenoids and vitamins A, C, and E and risk of breast cancer. J. Natl. Cancer Inst. 1999 Mar 17; 91(6): 547–56.CrossRefGoogle Scholar
5Chen, J, Giovannucci, EL, Hunter, DJ. MTHFR polymorphism, menthyl-replete dites and the risk of colorctal carcinoma and adenoma among U.S. men and women: an example of gene-environment interactions in colorectal tumorgenesis. J. Nutr. 1999; 129(2S Suppl): 560S564S.CrossRefGoogle Scholar
6Chen, J, Giovannucci, E, Hankinson, SE, Ma, J, Willett, WC, Spiegelman, D, Kelsey, KT, Hunter, DJ. A prospective study of methylenetetrahydrofolate reductase and methionine synthase gene polymorphisms, and risk of colorectal adenoma. Carcinogenesis 1998; 19(12): 21292132.CrossRefGoogle ScholarPubMed
7Morita, H, Kurihara, H, Tsubaki, S, Sugiyama, T, Hamada, C, Kurihara, Y, Shindo, T, Oh-hashi, Y, Kitamura, K, Yazaki, Y.Methylenetetrahydrofolate reductase gene polymorphism and ischemic stroke in Japanese. Arterioscler Thromb. Vase. Biol. 1998; 18(9): 14651469.CrossRefGoogle ScholarPubMed
8Girelli, D, Friso, S, Trabetti, E, Olivieri, O, Russo, C, Pessotto, R, Faccini, G, Pignatti, PF, Mazzucco, A, Corrocher, R: Methylenetetrahydrofolate reductase C677T mutation, plasma homocysteine, and folate in subjects from northern Italy with or without angiographically documented severe coronary atherosclerotic disease: evidence for an important genetic–environmental interaction. Blood 1998; 91(11): 41584163.CrossRefGoogle ScholarPubMed
9Ma, J, Stampfer, MJ, Hennekens, CH, Frosst, P, Selhub, J, Horsford, J, Malinow, MR, Willett, WC, Rozen, R: Methylenetetrahydrofolate reductase polymorphism, plasma folate, homocysteine, and risk of myocardial infarction in US physicians. Circulation 1996; 94(10): 24102416.CrossRefGoogle ScholarPubMed
10Roberts-Thomson, IC, Ryan, P, Khoo, KK, Hart, WJ, McMichael, AJ, Butler, RN. Diet, acetylator phenotype and risk of colorectal neoplasia. The Lancet 1996; 347(9012): 13721374.CrossRefGoogle ScholarPubMed
11Vineis, P, McMichael, AJ. Interplay between heterocyclic amines in cooked meat and metabolic phenotype in the etiology of colon cancer. Cancer Causes Control 1996; 7: 479486.CrossRefGoogle ScholarPubMed
12Pero, RW, Miller, DG, Lipkin, M, Malkowitz, M, Gupta, S, Winawer, SJ, Enker, W, Good, R.Reduced capacity for DNA repair synthesis in patients with or genetically predisposed to colorectal cancer. JNCI 1993; 70: 867875.Google Scholar
13Pero, RW, Ritchie, M, Winawer, SJ, Markowitz, MM, Miller, DGF. Unscheduled DNA synthesis in mononuclear leukocytes from patients with colorectal polyps. Cancer Res. 1995; 45: 33883391.Google Scholar
14Kiecolt-Glaser, JK, Stephens, RE, Lipetz, PD, Speciher, CE, Glaser, R.Distress and DNA repair in human lymphocytes. J. Behavioral Medicine 1985; 8: 311320.CrossRefGoogle ScholarPubMed
15Kovacs, E, Stucki, D, Weber, W, Muller, H.Impaired DNA-repair synthesis in lymphocytes of breast cancer patients. Eur. J. Cancer Clin. Oncol. 1986; 22: 863869.CrossRefGoogle ScholarPubMed
16Roth, M, Muller, H, Boyle, JM. Immunochemical determination of an intial step in thymine dimer excision repair in xeroderma pigmentosum variant fibroblasts and biobsy material from the normal population and patients with basal cell carcinoma and melanoma. Carcinogenesis 1987; 8: 13011307.CrossRefGoogle Scholar
17Kovacs, E, Almendral, A.Reduced DNA repair synthesis in healthy women having first degree relatives with breast cancer. Eur. J. Cancer. Clin. Oncol. 1987; 23: 10511057.CrossRefGoogle ScholarPubMed
18Kovacs, E, Langemann, H.Defective DNA repair in a large family having a large family having a high occurrence of cancer. Oncology 1988; 45: 444447.CrossRefGoogle Scholar
19Markowitz, MM, Johnson, DB, Pero, RW, Winawer, SJ, Miller, DG. Effects of cumene hydroperoxide on adenosine diphosphate ribosyl transferase in mononuclear leukocytes of patients with adenomatous polyps in the colon. Carcinogenesis 1998; 9: 349355.CrossRefGoogle Scholar
20Pero, RW, Johnson, DB, Miller, DG, Zang, E, Markowitz, M, Doyle, GA, Lund-Pero, M, Salford, L, Sordillo, P, Raskin, N, Beattie, EJ. Adenosine diphosphate ribosyl transferase responses to a standardized dose of hydrogen peroxide in the mononuclear leukocytes of patients with a diagnosis of cancer. Carcinogenesis 1989; 10: 16571664.CrossRefGoogle ScholarPubMed
21Spitz, MR, Fueger, JJ, Beddingfield, NA, Annegers, JF, Hsu, TC, Newell, GR, Schantz, SS. Chromosome sensitivity to Bleomycin-induced mutagenesis, an independent factor for upper aerodigestive tract cancers. Cancer Res. 1989; 49: 46264628.Google ScholarPubMed
22Pero, RW, Johnson, DB, Markowitz, MM, Doyle, G, Lund-Pero, M, Seidegard, J, Halper, M, Miller, DG. DNA repair synthesis in individuals with and without a family history of cancer. carcinogensis 1989; 10: 693697.CrossRefGoogle ScholarPubMed
23Schantz, SP, Spitz, MR, Hsu, TC. Mutagen sensitivity in patients with head and neck cancers: a biologic marker for risk of multiple primary malignancies. JNCI 1990; 82: 17731775.CrossRefGoogle ScholarPubMed
24Alcalay, J, Freeman, SE, Goldberg, LH, Wolf, JE. Excision repair of pyrimidine dimers induced by simulated solar radiation in the skin of patients with basal cell carcinoma. J. Invest. Dermatol. 1990; 95: 506509.CrossRefGoogle ScholarPubMed
25Athas, WF, Hedayati, MA, Matanoski, GM, Farmer, ER, Grossman, L.Development and field-test validation of an assay for DNA repair in circulating human lymphocytes. Cancer Res. 1991; 51: 57865793.Google ScholarPubMed
26Kovacs, E, Langemann, H.Differences in the kinetics of DNA repair in cancer patients and healthy controls. Oncology 1991; 48: 312316.CrossRefGoogle ScholarPubMed
27Spitz, MR, Fueger, JJ, Halabi, S, Schantz, SP, Sample, D, Hsu, TC. Mutagen sensitivity in upper digestive tract cancer: a casecontrol analysis. Cancer epidemiol. Biomarkers Prev. 1993; 2: 329333.Google Scholar
28Parshad, R, Price, FM, Pirollo, KF, Chang, EH, Sanford, KK. Cytogenetic response to G2-Phase X irradiation in relation to DNA repair and radiosensitivity in a cancer prone family with Li-Fraumeni syndrome. Radiation Res. 1993; 136: 236240.CrossRefGoogle Scholar
29Wei, Q, Matanoski, GM, Farmer, ER, Hedayati, MA, Grossman, L.DNA repair and aging in basal cell carcinoma: a molecular epidemiology study. PNAS 1993; 90: 16141618.CrossRefGoogle ScholarPubMed
30Spitz, MR, Hoque, A, Trizna, Z, Schantz, P, Amos, CI, King, TM, Bondy, ML, Hong, WK, Hsu, TC. Mutagen sensitivity as a risk factor for second malignant tumors following malignancies of the upper aerodigestive tract. JNCI 1994; 86: 16811684.CrossRefGoogle ScholarPubMed
31Scott, D, Spreadborough, A, Levine, E, Roberts, SA. Genetic predisposition in breast cancer. Lancet 1994; 344: 1444.CrossRefGoogle ScholarPubMed
32Hall, J, English, DR, Artuso, M, Armstrong, BK, Winter, M.DNA repair capacity as a risk factor for non-melanocytic skin cancer – a molecular epidemiological study. Int. J. Cancer 1994; 58: 179184.CrossRefGoogle ScholarPubMed
33Spits, AR, Hsu, TC, Wu, X, Fueger, JJ, Amos, CI, Roth, JA. Mutagen sensitivity as a biological marker of lung cancer risk in African Americans. Cancer Epidemiol. Biomarkers Prev. 1995; 4: 99103.Google Scholar
34Wei, G, Cheng, L, Hong, WK, Spitz, MR. Reduced DNA repair in lung cancer patients. Cancer Res. 1996; 56: 41034107.Google ScholarPubMed
35Li, D, Wang, M, Cheng, L, Spitz, MR, Hittelman, WN, Wei, Q.In vitro induction of benzo(a)pyrene diol epoxide-DNA adducts in peripheral lymphocytes as a susceptibility marker for human lung cancer. Cancer Res. 1996; 56: 36383641.Google ScholarPubMed
36Scott, D, Spreadborough, AR, Jones, LA, Roberts, SA, Moore, CJ. Chromosomal radiosensitivity in G2-Phase lymphocytes as an indicator of cancer predisposition. Radiation Res. 1996; 145: 316.CrossRefGoogle ScholarPubMed
37Parshad, R, Price, FM, Bohr, VA, Cowans, KH, Zujewski, JA, Sanford, KK. Deficient DNA repair capacity, a predisposing factor in breast cancer. Br. J. Cancer 1994; 74: 15.CrossRefGoogle Scholar
38Schantz, SP, Zhang, ZF, Spitz, MS, Sun, M, Hsu, TC. Genetic susceptibility to head and neck cancer: interaction between nutrition and mutagen sensitivity. The laryngoscope 1997; 107: 765781.CrossRefGoogle ScholarPubMed
39Hu, JJ, Roush, GC, Dubin, N, Berwick, M, Roses, DF, Harris, MN. Poly (ADP-ribose) polymerase in human breast cancer: a case-control study. Pharmacogenetics 1997; 7: 309316.CrossRefGoogle Scholar
40Jaloszynski, P, Kujawski, M, Czub-Swierczek, M, Markowska, J, Szyfter, K.Bleomycin-induced DNA damage and its removal in lympocytes of breast cancer patients studied by comet assay. Mut. Res. 1997; 385: 223233.CrossRefGoogle Scholar
41Patel, RK, Trivedi, AH, Arora, DC, Bhatavdekar, JM, Patel, DD. DNA repair proficiency in breast cancer patients and their first-degree relatives. Int. J. Cancer 1997; 73: 2024.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
42Spitz, MR, Lippman, SM, Jiang, H, Lee, JJ, Khuri, F, Hsu, TC, Trizna, Z, Schantz, SP, Benner, S, Hong, WK. Mutagen sensitivity as a predictor of tumor recurrence in patients with cancer of the upper aerodigestive tract. JNCI 1998; 90: 243245.CrossRefGoogle ScholarPubMed
43Moller, P, Knodsen, LE, Frentz, G, Dybdahl, M, Wallin, H, Nexo, BA. Seasonal variation of DNA damage and repair in patients with non-melanoma skin cancer and referents with and without psoriasis. Mutation. Res. 1998; 407: 2534.CrossRefGoogle ScholarPubMed
44Rao, NM, Pai, SA, Shinde, SR. Gosh SN Reduced DNA repair capacity in breast cancer patients and unaffected individuals from breast cancer families. Cancer Genet. Cyotogenet. 1998; 102: 6573.CrossRefGoogle Scholar
45Peluso, M, Airoldi, L, Armelle, M, Martone, T, Coda, R, Malaveille, C, Giacomelli, G, Terrone, C, Casetta, G, Vineis, P.White blood cell DNA adducts, smoking, and NAT2 and GSTM1 genotypes in bladder cancer: a case-control study. Cancer Epidemiol. Biomarkers prev. 1998; 7: 341346.Google ScholarPubMed
46Perera, FP. Molecular epidemiology: insights into cancer susceptibility, risk assessment, and prevention. JNCI 1996; 88: 496509.CrossRefGoogle ScholarPubMed
47Palli, D, Vineis, P, Russo, A, Berrino, F, Krogh, V, Masala, G, Munnia, A, Panico, S, Taioli, E, Tumino, R, Garte, S, Peluso, M.Diet, metabolic polymorphisms and dna adducts: The epic-Italy cross-sectional study. Int. J. Cancer 2000; 87(3): 444451.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
48Peluso, M, Airoldi, L, Magagnotti, C, Fiorini, L, Munnia, A, Hautefeuille, A, Malaveille, C, Vineis, P.White blood cell DNA adducts and fruit and vegetable consumption in bladder cancer. Carcinogenesis 2000; 21(2): 183187.CrossRefGoogle ScholarPubMed
49Doll, R, Peto, R.Cigarette smoking and bronchial carcinoma: dose and time relationships among regular smokers and lifelong non-smokers. J. Epidemiol. Comm. Health 1978; 32: 303313.CrossRefGoogle ScholarPubMed
50Lee, PN, O'Neill, JA. The effect of both time and dose on tumor incidence rate in benzopyrene skin painting experiments. Br. J. Cancer 1971; 25: 759770.CrossRefGoogle ScholarPubMed
51Lee, PN, Rothwell, K, Whitehead, JK. Fractionation of mouse skin carcinogens in cigarette smoke condensate. Br. J. Cancer 1977; 35: 730742.CrossRefGoogle Scholar
52Iversen, OH. The skin tumorigenic and carcinogenic effects of different doses, numbers of dose fractions and concentrations of 7,12-dimethylbenz[a]anthracene in acetone applied on hairless mouse epidermis. Possible implications for human carcinogenesis. Carcinogenesis 1991 Mar; 12(3): 493502.CrossRefGoogle Scholar