Intestinal carcinogenesis of two food processing contaminants, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine and 5-hydroxymethylfurfural, in transgenic FVB min mice expressing human sulfotransferases

Molecular Carcinogenesis

Volumn 51, Issue 12, 2012, Pages 984-992

  Svendsen, Camilla ^a   Meinl, Walter ^b   Glatt, Hansruedi ^b   Alexander, Jan ^a   Knutsen, Helle K ^a   Hjertholm, Hege ^a   Rasmussen, Tone ^a   Husøy, Trine ^a  

^a NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

2 amino 1 methyl 6 phenylimidazo 4,5 b pyridine; 5 hydroxymethylfurfural; Colorectal cancer; Min mice; Sulfotransferases

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 5 HYDROXYMETHYLFURFURAL; SULFOTRANSFERASE; SULFOTRANSFERASE 1A1; SULFOTRANSFERASE 1A2; UNCLASSIFIED DRUG;

ABERRANT CRYPT FOCUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CARCINOGENESIS; COLON TUMOR; CONTROLLED STUDY; FEMALE; FOOD CONTAMINATION; FOOD PROCESSING; INTESTINE TUMOR; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CARCINOGENS; FOOD HANDLING; FURALDEHYDE; HUMANS; IMIDAZOLES; INTESTINAL NEOPLASMS; MICE; MICE, TRANSGENIC; SULFOTRANSFERASES;

ANIMALIA; MUS; RODENTIA;

EID: 84863953497     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20869     Document Type: Article

References (40)

1. Glatt H. Sulfotransferases in the bioactivation of xenobiotics. Chem Biol Interact 2000; 129: 141-170.
2. Glatt H, Engelke CE, Pabel U, et al. Sulfotransferases: Genetics and role in toxicology. Toxicol Lett 2000; 112-113: 341-348.
3. Gamage N, Barnett A, Hempel N, et al. Human sulfotransferases and their role in chemical metabolism. Toxicol Sci 2006; 90: 5-22.
4. Casarett LJ, Doull J, Klaassen CD. Casarett and Doull's toxicology: The basic science of poisons. New York: McGraw-Hill; 2008.
5. Teubner W, Meinl W, Florian S, Kretzschmar M, Glatt H. Identification and localization of soluble sulfotransferases in the human gastrointestinal tract. Biochem J 2007; 404: 207-215.
6. Meinl W, Sczesny S, Brigelius-Flohe R, Blaut M, Glatt H. Impact of gut microbiota on intestinal and hepatic levels of phase 2 xenobiotic-metabolizing enzymes in the rat. Drug Metab Dispos 2009; 37: 1179-1186.
7. Glatt H. Activation and inactivation of carcinogens by human sulfotransferases. Human cytosolic sulfotransferases. London: Taylor & Francis; 2005. pp. 281-306.
8. Monien BH, Frank H, Seidel A, Glatt H. Conversion of the common food constituent 5-hydroxymethylfurfural into a mutagenic and carcinogenic sulfuric acid ester in the mouse in vivo. Chem Res Toxicol 2009; 22: 1123-1128.
9. Surh YJ, Liem A, Miller JA, Tannenbaum SR. 5-Sulfooxymethylfurfural as a possible ultimate mutagenic and carcinogenic metabolite of the Maillard reaction product, 5-hydroxymethylfurfural. Carcinogenesis 1994; 15: 2375-2377.
10. Glatt H, Schneider H, Murkovic M, Monien BH, Meinl W. Hydroxymethyl-substituted furans: Mutagenictiy in Salmonella typhimurium strains engineered for expression of various human and rodent sulfotransferases. Mutagenesis 2011 (in press).
11. Glatt H. Metabolic factors affecting the mutagenicity of heterocyclic amines. Acrylamide and other hazardous compounds in heat-treated foods. Cambridge: Woodhead Publishing; 2006. pp. 358-404.
12. Shirai T, Sano M, Tamano S, et al. 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: 195-198.
13. Ito N, Hasegawa R, Sano M, et al. A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP). Carcinogenesis 1991; 12: 1503-1506.
14. Steffensen IL, Paulsen JE, Eide TJ, Alexander J. 2-Amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine increases the numbers of tumors, cystic crypts and aberrant crypt foci in multiple intestinal neoplasia mice. Carcinogenesis 1997; 18: 1049-1054.
15. Paulsen JE, Steffensen IL, Andreassen A, Vikse R, Alexander J. Neonatal exposure to the food mutagen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine via breast milk or directly induces intestinal tumors in multiple intestinal neoplasia mice. Carcinogenesis 1999; 20: 1277-1282.
16. Steffensen IL, Schut HA, Paulsen JE, Andreassen A, Alexander J. Intestinal tumorigenesis in multiple intestinal neoplasia mice induced by the food mutagen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine: Perinatal susceptibility, regional variation, and correlation with DNA adducts. Cancer Res 2001; 61: 8689-8696.
17. IARC. Monographs on the Evaluation of Carcinogenic Risks to Humans, Volume 56, Some Naturally Occurring Substances: Food Items and Constitutents, Heterocyclic Aromatic Amines and Mycotoxins. 1993.
18. National Toxicology Program, Department of Health and Human Services. Toxicology and Carcinogenesis Studies of 5-(Hydroxymethyl)-2-furfural (CAS No. 67-47-0) in F344/N Rats and B6C3F1 Mice (Gavage Studies). 2008.
19. Zhang XM, Chan CC, Stamp D, Minkin S, Archer MC, Bruce WR. Initiation and promotion of colonic aberrant crypt foci in rats by 5-hydroxymethyl-2-furaldehyde in thermolyzed sucrose. Carcinogenesis 1993; 14: 773-775.
20. Svendsen C, Husoy T, Glatt H, Paulsen JE, Alexander J. 5-Hydroxymethylfurfural and 5-sulfooxymethylfurfural increase adenoma and flat ACF number in the intestine of Min/+ mice. Anticancer Res 2009; 29: 1921-1926.
21. Svendsen C, Alexander J, Knutsen HK, Husoy T. The Min mouse on FVB background: Susceptibility to spontaneous and carcinogen-induced intestinal tumourigenesis. Anticancer Res 2011; 31: 785-788.
22. Dobbernack G, Meinl W, Schade N, et al. Altered tissue distribution of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine-DNA adducts in mice transgenic for human sulfotransferases 1A1 and 1A2. Caecinogenesis 2011 (in press).
23. Shoemaker AR, Gould KA, Luongo C, Moser AR, Dove WF. Studies of neoplasia in the Min mouse. Biochim Biophys Acta 1997; 1332: F25-F48.
24. Olstorn HB, Paulsen JE, Alexander J. Effects of perinatal exposure to acrylamide and glycidamide on intestinal tumorigenesis in Min/+ mice and their wild-type litter mates. Anticancer Res 2007; 27: 3855-3864.
25. Paulsen JE, Steffensen IL, Loberg EM, Husoy T, Namork E, Alexander J. Qualitative and quantitative relationship between dysplastic aberrant crypt foci and tumorigenesis in the Min/+ mouse colon. Cancer Res 2001; 61: 5010-5015.
26. Richard K, Hume R, Kaptein E, Stanley EL, Visser TJ, Coughtrie MW. Sulfation of thyroid hormone and dopamine during human development: Ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain. J Clin Endocrinol Metab 2001; 86: 2734-2742.
27. Muckel E, Frandsen H, Glatt HR. Heterologous expression of human N-acetyltransferases 1 and 2 and sulfotransferase 1A1 in Salmonella typhimurium for mutagenicity testing of heterocyclic amines. Food Chem Toxicol 2002; 40: 1063-1068.
28. Frandsen H. Biomonitoring of urinary metabolites of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP) following human consumption of cooked chicken. Food Chem Toxicol 2008; 46: 3200-3205.
29. Turteltaub KW, Dingley KH, Curtis KD, et al. Macromolecular adduct formation and metabolism of heterocyclic amines in humans and rodents at low doses. Cancer Lett 1999; 143: 149-155.
30. Alnouti Y, Klaassen CD. Tissue distribution and ontogeny of sulfotransferase enzymes (Sults) in mice. Toxicol Sci 2006; 93: 242-255.
31. Glatt H, Meinl W. Pharmacogenetics of soluble sulfotransferases (SULTs). Naunyn Schmiedebergs Arch Pharmacol 2004; 369: 55-68.
32. Bakhiya N, Monien B, Frank H, Seidel A, Glatt H. Renal organic anion transporters OAT1 and OAT3 mediate the cellular accumulation of 5-sulfooxymethylfurfural, a reactive, nephrotoxic metabolite of the Maillard product 5-hydroxymethylfurfural. Biochem Pharmacol 2009; 78: 414-419.
33. Janzowski C, Glaab V, Samimi E, Schlatter J, Eisenbrand G. 5-Hydroxymethylfurfural: Assessment of mutagenicity. DNA-damaging potential and reactivity towards cellular glutathione. Food Chem Toxicol 2000; 38: 801-809.
34. Lee YC, Shlyankevich M, Jeong HK, Douglas JS, Surh YJ. Bioactivation of 5-hydroxymethyl-2-furaldehyde to an electrophilic and mutagenic allylic sulfuric acid ester. Biochem Biophys Res Commun 1995; 209: 996-1002.
35. Severin I, Dumont C, Jondeau-Cabaton A, Graillot V, Chagnon MC. Genotoxic activities of the food contaminant 5-hydroxymethylfurfural using different in vitro bioassays. Toxicol Lett 2010; 192: 189-194.
36. Sommer Y, Hollnagel H, Schneider H, Glatt H. Metabolism of 5-hydroxymethyl-2-furfural (HMF) to the mutagen, 5-sulfoxymethyl-2-furfural (SMF) by individual human sulfotransferases. Naunyn Schmiedebergs Arch Pharmacol 2003; 367: 166.
37. Glatt H, Schneider H, Liu Y. V79-hCYP2E1-hSULT1A1, a cell line for the sensitive detection of genotoxic effects induced by carbohydrate pyrolysis products and other food-borne chemicals. Mutat Res 2005; 580: 41-52.
38. Nishi Y, Miyakawa Y, Kato K. Chromosome aberrations induced by pyrolysates of carbohydrates in Chinese hamster V79cells. Mutat Res 1989; 227: 117-123.
39. Glatt H, Meinl W. Sulfotransferases and acetyltransferases in mutagenicity testing: Technical aspects. Methods Enzymol 2005; 400: 230-249.
40. Durling LJ, Busk L, Hellman BE. Evaluation of the DNA damaging effect of the heat-induced food toxicant 5-hydroxymethylfurfural (HMF) in various cell lines with different activities of sulfotransferases. Food Chem Toxicol 2009; 47: 880-884.