Quercetin tests negative for genotoxicity in transcriptome analyses of liver and small intestine of mice

Food and Chemical Toxicology

Volumn 81, Issue , 2015, Pages 34-39

  Hoek van den Hil, Elise F ^a   van Schothorst, Evert M ^a   van der Stelt, Inge ^a   Hollman, Peter C H ^a   Keijer, Jaap ^a   Rietjens, Ivonne M C M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Flavonoid; Genotoxicity; Quercetin; Transcriptomics

Indexed keywords

AFLATOXIN B1; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; N (2 FLUORENYL)ACETAMIDE; QUERCETIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CLASSIFIER; CONTROLLED STUDY; DNA DAMAGE; DRUG SAFETY; GENOTOXICITY; LIPID DIET; LIVER; LIVER TOXICITY; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; SMALL INTESTINE; TRANSCRIPTOMICS; ANIMAL; BLOOD; C57BL MOUSE; DIETARY SUPPLEMENT; DRUG EFFECTS; GENE EXPRESSION PROFILING; METABOLISM; UPREGULATION;

MUS;

2-ACETYLAMINOFLUORENE; AFLATOXIN B1; ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; DIET, HIGH-FAT; DIETARY SUPPLEMENTS; DNA DAMAGE; GENE EXPRESSION PROFILING; INTESTINE, SMALL; LIVER; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; QUERCETIN; UP-REGULATION;

EID: 84927915487     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2015.04.005     Document Type: Article

References (44)

1. Aeschbacher H.U., Meier H., Ruch E. Nonmutagenicity in vivo of the food flavonol quercetin. Nutr. Cancer 1982, 4:90-98.
2. An X., Ng S.S., Xie D., Zeng Y.X., Sze J., Wang J., et al. Functional characterisation of cell cycle-related kinase (CCRK) in colorectal cancer carcinogenesis. Eur. J. Cancer 2010, 46:1752-1761.
3. Barjesteh van Waalwijk van Doorn-Khosrovani S., Janssen J., Maas L.M., Godschalk R.W., Nijhuis J.G., van Schooten F.J. Dietary flavonoids induce MLL translocations in primary human CD34 + cells. Carcinogenesis 2007, 28:1703-1709.
4. Beekmann K., Actis-Goretta L., van Bladeren P.J., Dionisi F., Destaillats F., Rietjens I.M. A state-of-the-art overview of the effect of metabolic conjugation on the biological activity of flavonoids. Food Funct 2012, 3:1008-1018.
5. Boehm O., Zur B., Koch A., Tran N., Freyenhagen R., Hartmann M., et al. Clinical chemistry reference database for Wistar rats and C57/BL6 mice. Biol. Chem 2007, 388:547-554.
6. Cardus A., Uryga A.K., Walters G., Erusalimsky J.D. SIRT6 protects human endothelial cells from DNA damage, telomere dysfunction, and senescence. Cardiovasc. Res 2013, 97:571-579.
7. Caria H., Chaveca T., Laires A., Rueff J. Genotoxicity of quercetin in the micronucleus assay in mouse bone marrow erythrocytes, human lymphocytes, V79 cell line and identification of kinetochore-containing (CREST staining) micronuclei in human lymphocytes. Mutat. Res 1995, 343:85-94.
8. Carver J.H., Carrano A.V., MacGregor J.T. Genetic effects of the flavonols quercetin, kaempferol, and galangin on Chinese hamster ovary cells in vitro. Mutat. Res 1983, 113:45-60.
9. Cierniak A., Papiez M., Kapiszewska M. Modulatory effect of quercetin on DNA damage, induced by etoposide in bone marrow cells and on changes in the activity of antioxidant enzymes in rats. Rocz. Akad. Med. Bialymst 2004, 49(Suppl. 1):167-169.
10. Di Fiore R., D'Anneo A., Tesoriere G., Vento R. RB1 in cancer: different mechanisms of RB1 inactivation and alterations of pRb pathway in tumorigenesis. J. Cell. Physiol 2013, 228:1676-1687.
11. Halliwell B. Oxidative stress in cell culture: an under-appreciated problem?. FEBS Lett 2003, 540:3-6.
12. Hard G.C., Seely J.C., Betz L.J., Hayashi S.M. Re-evaluation of the kidney tumors and renal histopathology occurring in a 2-year rat carcinogenicity bioassay of quercetin. Food Chem. Toxicol 2007, 45:600-608.
13. Hirono I., Ueno I., Hosaka S., Takanashi H., Matsushima T., Sugimura T., et al. Carcinogenicity examination of quercetin and rutin in ACI rats. Cancer Lett 1981, 13:15-21.
14. Hochberg Y., Benjamini Y. More powerful procedures for multiple significance testing. Stat. Med 1990, 9:811-818.
15. Hoek-van den Hil E.F., van Schothorst E.M., van der Stelt I., Swarts H.J.M., Venema D., Sailer M., et al. Quercetin decreases high-fat diet induced body weight gain and accumulation of hepatic and circulating lipids in mice. Genes Nutr 2014, 9:418.
16. Hoevenaars F.P., van Schothorst E.M., Horakova O., Voigt A., Rossmeisl M., Pico C., et al. BIOCLAIMS standard diet (BIOsd): a reference diet for nutritional physiology. Genes Nutr 2012, 7:399-404.
17. Hollman P.C., Cassidy A., Comte B., Heinonen M., Richelle M., Richling E., et al. The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J. Nutr 2011, 141:989S-1009S.
18. Ito N. Is quercetin carcinogenic?. Jpn J. Cancer Res 1992, 83:312-313.
19. Ito N., Hagiwara A., Tamano S., Kagawa M., Shibata M., Kurata Y., et al. Lack of carcinogenicity of quercetin in F344/DuCrj rats. Jpn J. Cancer Res 1989, 80:317-325.
20. Kroon P.A., Clifford M.N., Crozier A., Day A.J., Donovan J.L., Manach C., et al. How should we assess the effects of exposure to dietary polyphenols in vitro?. Am. J. Clin. Nutr 2004, 80:15-21.
21. Lamson D.W., Brignall M.S. Antioxidants and cancer, part 3: quercetin. Altern. Med. Rev 2000, 5:196-208.
22. MacGregor J.T., Jurd L. Mutagenicity of plant flavonoids: structural requirements for mutagenic activity in Salmonella typhimurium. Mutat. Res 1978, 54:297-309.
23. Melis J.P., Derks K.W., Pronk T.E., Wackers P., Schaap M.M., Zwart E., et al. In vivo murine hepatic microRNA and mRNA expression signatures predicting the (non-)genotoxic carcinogenic potential of chemicals. Arch. Toxicol 2014, 88:1023-1034.
24. Nagao M., Morita N., Yahagi T., Shimizu M., Kuroyanagi M., Fukuoka M., et al. Mutagenicities of 61 flavonoids and 11 related compounds. Environ. Mutagen 1981, 3:401-419.
25. National Toxicology P. Toxicology and carcinogenesis studies of quercetin (CAS No. 117-39-5) in F344 rats (feed studies). Natl Toxicol. Program Tech. Rep. Ser 1992, 409:1-171.
26. Ngomuo A.J., Jones R.S. Genotoxicity studies of quercetin and shikimate in vivo in the bone marrow of mice and gastric mucosal cells of rats. Vet. Hum. Toxicol 1996, 38:176-180.
27. Paini A., Scholz G., Marin-Kuan M., Schilter B., O'Brien J., van Bladeren P.J., et al. Quantitative comparison between in vivo DNA adduct formation from exposure to selected DNA-reactive carcinogens, natural background levels of DNA adduct formation and tumour incidence in rodent bioassays. Mutagenesis 2011, 26:605-618.
28. Pamukcu A.M., Yalciner S., Hatcher J.F., Bryan G.T. Quercetin, a rat intestinal and bladder carcinogen present in bracken fern (Pteridium aquilinum). Cancer Res 1980, 40:3468-3472.
29. Pellis L., Franssen-van Hal N.L., Burema J., Keijer J. The intraclass correlation coefficient applied for evaluation of data correction, labeling methods, and rectal biopsy sampling in DNA microarray experiments. Physiol. Genomics 2003, 16:99-106.
30. Peterson J.J., Dwyer J.T., Jacques P.F., McCullough M.L. Associations between flavonoids and cardiovascular disease incidence or mortality in European and US populations. Nutr. Rev 2012, 70:491-508.
31. Resende F.A., Vilegas W., Dos Santos L.C., Varanda E.A. Mutagenicity of flavonoids assayed by bacterial reverse mutation (Ames) test. Molecules 2012, 17:5255-5268.
32. Rueff J., Laires A., Borba H., Chaveca T., Gomes M.I., Halpern M. Genetic toxicology of flavonoids: the role of metabolic conditions in the induction of reverse mutation, SOS functions and sister-chromatid exchanges. Mutagenesis 1986, 1:179-183.
33. Saito D., Shirai A., Matsushima T., Sugimura T., Hirono I. Test of carcinogenicity of quercetin, a widely distributed mutagen in food. Teratog. Carcinog. Mutagen 1980, 1:213-221.
34. Silva I.D., Gaspar J., da Costa G.G., Rodrigues A.S., Laires A., Rueff J. Chemical features of flavonols affecting their genotoxicity. Potential implications in their use as therapeutical agents. Chem. Biol. Interact 2000, 124:29-51.
35. Srivastava A.K., Bhatnagar P., Singh M., Mishra S., Kumar P., Shukla Y., et al. Synthesis of PLGA nanoparticles of tea polyphenols and their strong in vivo protective effect against chemically induced DNA damage. Int. J. Nanomed 2013, 8:1451-1462.
36. Stoewsand G.S., Anderson J.L., Boyd J.N., Hrazdina G., Babish J.G., Walsh K.M., et al. Quercetin: a mutagen, not a carcinogen, in Fischer rats. J. Toxicol. Environ. Health 1984, 14:105-114.
37. Taj S., Nagarajan B. Inhibition by quercetin and luteolin of chromosomal alterations induced by salted, deep-fried fish and mutton in rats. Mutat. Res 1996, 369:97-106.
38. Thomas R.S., O'Connell T.M., Pluta L., Wolfinger R.D., Yang L., Page T.J. A comparison of transcriptomic and metabonomic technologies for identifying biomarkers predictive of two-year rodent cancer bioassays. Toxicol. Sci 2007, 96:40-46.
39. Utesch D., Feige K., Dasenbrock J., Broschard T.H., Harwood M., Danielewska-Nikiel B., et al. Evaluation of the potential in vivo genotoxicity of quercetin. Mutat. Res 2008, 654:38-44.
40. van der Woude H., Alink G.M., van Rossum B.E., Walle K., van Steeg H., Walle T., et al. Formation of transient covalent protein and DNA adducts by quercetin in cells with and without oxidative enzyme activity. Chem. Res. Toxicol 2005, 18:1907-1916.
41. van Schothorst E.M., Pagmantidis V., de Boer V.C., Hesketh J., Keijer J. Assessment of reducing RNA input for Agilent oligo microarrays. Anal. Biochem 2007, 363:315-317.
42. Vanhees K., de Bock L., Godschalk R.W., van Schooten F.J., van Waalwijk van Doorn-Khosrovani S.B. Prenatal exposure to flavonoids: implication for cancer risk. Toxicol. Sci 2011, 120:59-67.
43. Vanhees K., Godschalk R.W., Sanders A., van Waalwijk van Doorn-Khosrovani S.B., van Schooten F.J. Maternal quercetin intake during pregnancy results in an adapted iron homeostasis at adulthood. Toxicology 2011, 290:350-358.
44. Vrijsen R., Michotte Y., Boeye A. Metabolic activation of quercetin mutagenicity. Mutat. Res 1990, 232:243-248.