First Report on a Series of Food-derived Mutagenic and Carcinogenic Heterocyclic Amines

Overview

Journal Proc Jpn Acad Ser B Phys Biol Sci

Specialties Biology
Science

Date 2024 Dec 11

PMID 39662942

Authors

Yukari Totsuka

Masako Ochiai

Keiji Wakabayashi

Affiliations

Soon will be listed here.

Abstract

Lifestyle, especially diet, significantly impacts cancer development. Sugimura, T. et al. discovered that grilled fish smoke and charred parts are highly mutagenic in Salmonella typhimurium. They identified two novel mutagenic heterocyclic amines (HCAs), 3-amino-1,4-dimethyl-5H-pyrido[4,3-b]indole (Trp-P-1) and its derivative, Trp-P-2, from tryptophan pyrolysate. Published in Proc. Jpn. Acad. (53, 58-61, 1977), their findings initiated the identification of over 10 mutagenic HCAs in cooked foods, most of them newly registered. These 10 HCAs were demonstrated to induce cancers in organs including the liver, colon, breast, and prostate in mice and rats. HCAs are metabolized primarily by CYP1A2 to hydroxyamino derivatives. Their ester forms then adduct at guanine bases, altering genes such as Apc and β-catenin. Quantification of HCAs in cooked foods and human samples, along with epidemiological observations, suggests HCAs likely contribute to human cancers.

References

Purchase I, Longstaff E, Ashby J, Styles J, Anderson D, Lefevre P . Evaluation of six short term tests for detecting organic chemical carcinogens and recommendations for their use. Nature. 1976; 264(5587):624-7. DOI: 10.1038/264624a0. View

Ochiai M, Ushigome M, Fujiwara K, Ubagai T, Kawamori T, Sugimura T . Characterization of dysplastic aberrant crypt foci in the rat colon induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Am J Pathol. 2003; 163(4):1607-14. PMC: 1868301. DOI: 10.1016/S0002-9440(10)63517-1. View

Watanabe J, Kawajiri K, Yonekawa H, Nagao M, Tagashira Y . Immunological analysis of the roles of two major types of cytochrome P-450 in mutagenesis of compounds isolated from pyrolysates. Biochem Biophys Res Commun. 1982; 104(1):193-9. DOI: 10.1016/0006-291x(82)91958-1. View

Zheng W, Gustafson D, Sinha R, Cerhan J, Moore D, Hong C . Well-done meat intake and the risk of breast cancer. J Natl Cancer Inst. 1998; 90(22):1724-9. DOI: 10.1093/jnci/90.22.1724. View

DeBruin L, Martos P, Josephy P . Detection of PhIP (2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine) in the milk of healthy women. Chem Res Toxicol. 2001; 14(11):1523-8. DOI: 10.1021/tx015556u. View

FELTON J, Knize M, Shen N, Lewis P, Andresen B, Happe J . The isolation and identification of a new mutagen from fried ground beef: 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis. 1986; 7(7):1081-6. DOI: 10.1093/carcin/7.7.1081. View

Minchin R, Reeves P, Teitel C, McManus M, Mojarrabi B, Ilett K . N-and O-acetylation of aromatic and heterocyclic amine carcinogens by human monomorphic and polymorphic acetyltransferases expressed in COS-1 cells. Biochem Biophys Res Commun. 1992; 185(3):839-44. DOI: 10.1016/0006-291x(92)91703-s. View

Ohgaki H, Matsukura N, Morino K, Kawachi T, Sugimura T, Takayama S . Carcinogenicity in mice of mutagenic compounds from glutamic acid and soybean globulin pyrolysates. Carcinogenesis. 1984; 5(6):815-9. DOI: 10.1093/carcin/5.6.815. View

Kato T, Ohgaki H, Hasegawa H, Sato S, Takayama S, Sugimura T . Carcinogenicity in rats of a mutagenic compound, 2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline. Carcinogenesis. 1988; 9(1):71-3. DOI: 10.1093/carcin/9.1.71. View

10.

TOHDA H, Oikawa A, Kawachi T, Sugimura T . Induction of sister-chromatid exchanges by mutagens from amino acid and protein pyrolysates. Mutat Res. 1980; 77(1):65-9. DOI: 10.1016/0165-1218(80)90121-4. View

11.

Cross A, Peters U, Kirsh V, Andriole G, Reding D, Hayes R . A prospective study of meat and meat mutagens and prostate cancer risk. Cancer Res. 2005; 65(24):11779-84. DOI: 10.1158/0008-5472.CAN-05-2191. View

12.

Ohgaki H, Hasegawa H, Suenaga M, Kato T, Sato S, Takayama S . Induction of hepatocellular carcinoma and highly metastatic squamous cell carcinomas in the forestomach of mice by feeding 2-amino-3,4-dimethylimidazo[4,5-f]quinoline. Carcinogenesis. 1986; 7(11):1889-93. DOI: 10.1093/carcin/7.11.1889. View

13.

Dingley K, Curtis K, Nowell S, FELTON J, Lang N, Turteltaub K . DNA and protein adduct formation in the colon and blood of humans after exposure to a dietary-relevant dose of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Cancer Epidemiol Biomarkers Prev. 1999; 8(6):507-12. View

14.

Ito N, Hasegawa R, Sano M, Tamano S, Esumi H, Takayama S . A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis. 1991; 12(8):1503-6. DOI: 10.1093/carcin/12.8.1503. View

15.

Shirai T, Sano M, Tamano S, Takahashi S, Hirose M, Futakuchi M . The prostate: a target for carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) derived from cooked foods. Cancer Res. 1997; 57(2):195-8. View

16.

Ishii K, Ando M, Kamataki T, Kato R, Nagao M . Metabolic activation of mutagenic tryptophan pyrolysis products (Trp-P-1 and Trp-P-2) by a purified cytochrome P-450-dependent monooxygenase system. Cancer Lett. 1980; 9(4):271-6. DOI: 10.1016/0304-3835(80)90017-8. View

17.

Le Marchand L, Hankin J, Pierce L, Sinha R, Nerurkar P, Franke A . Well-done red meat, metabolic phenotypes and colorectal cancer in Hawaii. Mutat Res. 2002; 506-507:205-14. DOI: 10.1016/s0027-5107(02)00167-7. View

18.

Nagao M, Honda M, Seino Y, Yahagi T, Sugimura T . Mutagenicities of smoke condensates and the charred surface of fish and meat. Cancer Lett. 1977; 2(4-5):221-6. DOI: 10.1016/s0304-3835(77)80025-6. View

19.

Totsuka Y, Fukutome K, Takahashi M, Takahashi S, Tada A, Sugimura T . Presence of N2-(deoxyguanosin-8-yl)-2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline (dG-C8-MeIQx) in human tissues. Carcinogenesis. 1996; 17(5):1029-34. DOI: 10.1093/carcin/17.5.1029. View

20.

Tamano S, Hasegawa R, Hagiwara A, Nagao M, Sugimura T, Ito N . Carcinogenicity of a mutagenic compound from food, 2-amino-3-methyl-9H-pyrido[2,3-b]indole (MeA alpha C), in male F344 rats. Carcinogenesis. 1994; 15(9):2009-15. DOI: 10.1093/carcin/15.9.2009. View