Naringin accelerates the regression of pre-neoplastic lesions and the colorectal structural reorganization in a murine model of chemical carcinogenesis

Food and Chemical Toxicology

Volumn 64, Issue , 2014, Pages 200-209

  Sequetto, Priscila L ^a   Oliveira, Tânia T ^a   Maldonado, Izabel R S C ^a   Augusto, Luís Eugênio F ^a   Mello, Vanessa J ^b   Pizziolo, Virginia R ^a   Almeida, Márcia R ^a   Silva, Marcelo E ^c   Novaes, RÔmulo D ^c,d  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^c FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

^d FEDERAL UNIVERSITY OF ALFENAS   (Brazil)

Author keywords

1,2 Dimethylhydrazine; Flavonoide; Large intestine; Pathology; Toxicology

Indexed keywords

1,2 DIMETHYLHYDRAZINE; AURANTIIN; COPPER; IRON; MAGNESIUM; MUCIN; SELENIUM; SODIUM CHLORIDE; ZINC;

ABERRANT CRYPT FOCUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARGYROPHILIC NUCLEOLAR ORGANIZING REGION; ARTICLE; CANCER REGRESSION; CELL COUNT; CELL NUCLEUS; CELL PROLIFERATION; CHEMICAL CARCINOGENESIS; CHROMOSOME NOR; COLORECTAL CANCER; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; ERYTHROCYTE; FEMALE; MITOSIS; NONHUMAN; PRECANCER; PRENEOPLASTIC COLORECTAL LESION; RAT; TISSUE LEVEL;

ANIMALIA; MURINAE; RATTUS; RATTUS NORVEGICUS;

1,2-DIMETHYLHYDRAZINE; 8-HYDROXY-2′-DEOXYGUANOSINE; 8-OHDG; AB; ABERRANT CRYPT FOCI; ACF; AGNORS; ALCIAN BLUE; ARGYROPHILIC NUCLEOLAR ORGANIZING REGIONS; DMH; EDS; FLAVONOIDE; LARGE INTESTINE; PAS; PATHOLOGY; PERIODIC ACID-SCHIFF; TOXICOLOGY; VOLUME DENSITY; VV; X-RAY ENERGY DISPERSIVE SPECTROSCOPY;

1,2-DIMETHYLHYDRAZINE; ANIMALS; CARCINOGENS; COLORECTAL NEOPLASMS; FEMALE; FLAVANONES; MICE; MICROSCOPY, ELECTRON, SCANNING; PRECANCEROUS CONDITIONS; RATS; RATS, WISTAR;

EID: 84890708093     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.11.032     Document Type: Article

References (54)

1. Anetor J.L., Wanibuchi H., Fukushima S. Arsenic exposure and its health effects and risk of in developing countries: micronutrients as host defense. Asian Pacific J. Cancer 2007, 8:13-23.
2. Araújo J.R., Gonçalves P., Martel F. Chemopreventive effect of dietary polyphenols in colorectal cancer cell lines. Nutr. Res. 2011, 31:77-87.
3. Bird R.P. Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett. 1987, 37:147-151.
4. Bird R.P. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett. 1995, 93:55-71.
5. Chen M.C., Ye Y.Y., Ji G., Liu J.W. Hesperidin upregulates heme oxyenase-1 to attenuate hydrogen peroxide-induced cell damage in hepatic L02 cells. J. Agric. Food Chem. 2010, 58:3330-3335.
6. Choudhary G., Hansen H. Human health perspective on environmental exposure to hydrazines: a review. Chemosphere 1998, 37:801-843.
7. Coombs N.J., Gough A.C., Primrose J.N. Optimization of DNA and RNA extraction from archival formalin-fixed tissue. Nucleic Acids Res. 1999, 27:e12.
8. Dani V., Goel A., Vaiphei K., Dhawan D.K. Chemopreventive potential of zinc in experimentally induced colon carcinogenesis. Toxicol. Lett. 2007, 171:10-18.
9. Duffield-Lillico A.J., Reid M.E., Turnbull B.W., Combs G.F., Slate E.H., Fischbach L.A., Marshall J.R., Clark L.C. Baseline characteristics and the effect of selenium supplementation on cancer incidence in a randomized clinical trial: a summary report of the nutritional prevention of cancer trial. Cancer Epidemiol. Biomark. Prev. 2002, 11:630-639.
10. Fukai T., Marumo A., Kaitou K., Kanda T., Terada S., Nomura T. Anti-Helicobacter pylori flavonoids from licorice extract. Life Sci. 2002, 71:1449-1463.
11. Grigolo B., Lisignoli G., Toneguzzi S., Mazzetti I., Facchini A. Copper/zinc superoxide dismutase expression by different human osteosarcoma cell lines. Anticancer Res. 1998, 18:1175-1180.
12. Howell W.M., Black D.A. Controlled silver-staining of nucleolus organizer with a protective colloidal developer: a 1-step method. Experimentia 1982, 62:361-367.
13. Jain M., Parmar H.S. Evaluation of antioxidative and anti-inflammatory potential of hesperidin and naringin on the rat air pouch model of inflammation. Inflam. Res. 2011, 60:483-491.
14. Jaiswal A.S., Narayan S. Zinc stabilizes adenomatous polyposis coli (APC) protein levels and induces cell cycle arrest in colon cancer. J. Cell Biochem. 2004, 93:345-357.
15. Jung U.J., Kim H.J., Lee J.S., Lee M.K., Kim H.O., Park E.J., Kim H.K., Jeong T.S., Choi M.S. Naringin supplementation lowers plasma lipids and enhances erythrocyte antioxidant enzyme activities in hypercholesterolemic subjects. Clin. Nutr. 2003, 22:561-568.
16. Kajimoto S., Takanashi N., Kajimoto T., Xu M., Cao J., Masuda Y., Aiuchi T., Nakajo S., Ida Y., Nakaya K. Sophoranone, extracted from a traditional Chinese medicine Shan Dou Gen, induces apoptosis in human leukemia U937 cells via formation of reactive oxygen species and opening of mitochondrial permeability transition pores. Int. J. Cancer 2002, 99:879-890.
17. Kakimoto M., Inoguchi T., Sonta T., Yu H.Y., Imamura M., Etoh T., Hashimoto T., Nawata H. Accumulation of 8-hydroxy-2'-deoxyguanosine and mitochondrial DNA deletion in kidney of diabetic rats. Diabetes 2002, 51:1588-1595.
18. Kanno S., Shouji A., Tomizawam A., Hiura T., Osanai Y., Ujibe M., Obara Y., Nakahata N., Ishikawa M. Inhibitory effect of naringin on lipopolysaccharide (LPS)-induced endotoxin shock in mice and nitric oxide production in RAW 264.7 macrophages. Life Sci. 2006, 78:673-681.
19. Kanno S., Tomizawa A., Hiura T., Osanai Y., Shouji A., Ujibe M., Ohtake T., Kimura K., Ishikawa M. Inhibitory effects of naringenin on tumor growth in human cancer cell lines and sarcoma S-180-implanted mice. Biol. Pharm. Bull. 2005, 28:527-530.
20. Klein C., Creach K., Irintcheva V., Hughes K.J., Blackwell P.L., Corbett J.A., Baldassare J.J. Zinc induces ERK-dependent cell death through a specific Ras isoform. Apoptosis 2006, 11:1933-1944.
21. Lee J.H., Park C.H., Jung K.C., Rhee H.S., Yang C.H. Negative regulation of β-catenin/Tcf signaling by naringenin in AGS gastric cancer cell. Biochem. Biophys. Res. Commun. 2005, 335:771-776.
22. Liu M., Zou W., Yang C., Peng W., Su W. Metabolism and excretion studies of oral administered naringin, a putative antitussive, in rats and dogs. Biopharm. Drug Dispos. 2012, 33:123-134.
23. Magnuson B., Carr I., Bird R. Ability of aberrant crypt foci characteristics to predict colonic tumor incidence in rats fed cholic acid. Cancer Res. 1993, 53:4499-4504.
24. Mandarim-de-Lacerda C.A. Stereological tools in biomedical research. Ann. Acad. Braz. Sci. 2003, 75:469-486.
25. Master Z., Chaudhary A., Sutter T.R., Kristine L. Willett effects of flavonoids on CYP1 expression in RL95-2 endometrial carcinoma cells. Food Chem. 2012, 133:912-922.
26. Meira L.B., Bugni J.M., Green S.L., Lee C.W., Pang B., Borenshtein D., Rickman B.H., Rogers A.B., Moroski-Erkul C.A., McFaline J.L., Schauer D.B., Dedon P.C., Fox J.G., Samson L.D. DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J. Clin. Invest. 2008, 118:2516-2525.
27. Méplan C., Hesketh J. The influence of selenium and selenoprotein gene variants on colorectal cancer risk. Mutagenesis 2012, 279:177-186.
28. Miyamoto S., Kohno H., Suzuki R., Sugie S., Murakami A., Ohigashi H., Tanaka T. Preventive effects of chrysin on the development of azoxymethane-induced colonic aberrant crypt foci in rats. Oncol. Rep. 2006, 15:1169-1173.
29. Moon J.Y., Wang X., Morris M.E. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicol. in Vitro 2006, 20:187-210.
30. Naczk M., Shahidi F. Extraction and analysis of phenolics in food. J. Chromatogr. A 2004, 1054:95-111.
31. Newell L.E., Heddle J.A. The potent colon carcinogen, 1,2-dimethylhydrazine induces mutations primarily in the colon. Mutat. Res. 2004, 564:1-7.
32. Okada S. Iron-induced tissue damage and cancer: the role of reactive oxygen species-free radicals. Pathol. Int. 1996, 46:311-332.
33. Park K.S., Ahn Y., Kim J.A., Yun M.S., Seong B.L., Choi K.Y. Extracellular zinc stimulates ERK dependent activation of p21 Cip/WAF1 and inhibits proliferation of colorectal cancer cells. Br. J. Pharmacol. 2002, 137:597-607.
34. Park S., Murphy S.P., Wilkens L.R., Henderson B.E., Kolonel L.N. Multivitamin use and the risk of mortality and cancer incidence: the multiethnic cohort study. Am. J. Epidemiol. 2011, 173:906-914.
35. Pierini R., Gee J.M., Belshaw N.J., Johnson I.T. Flavonoids and intestinal cancers. Br. J. Nutr. 2008, 99:53-59.
36. Pories S.E., Ramchurren N., Summerhayes I., Steele G. Animal models for colon carcinogenesis. Arch. Surg. 1993, 128:647-653.
37. Ramos S., Rodríguez-Ramiro I., Martín M.A., Goya L., Bravo L. Dietary flavanols exert different effects on antioxidant defenses and apoptosis/proliferation in Caco-2 and SW480 colon cancer cells. Toxicol. in Vitro 2011, 25:1771-1781.
38. Roberts R.B., Min L., Washington M.K., Olsen S.J., Settle S.H., Coffey R.J., Threadgill D.W. Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis. Proc. Natl. Acad. Sci. USA 2002, 99:1521-1526.
39. Rossi M., Negri E., Talamini R., Bosetti C., Parpinel M., Gnagnarella P., Franceschi S., Dal Maso L., Montella M., Giacosa A., La Vecchia C. Flavonoids and colorectal cancer in Italy. Cancer Epidemiol. Biomark. Prev. 2006, 15:1555-1558.
40. Scalbert A., Williamson G. Dietary intake and bioavailability of polyphenols. J. Nutr. 2000, 130:2073S-2085S.
41. Sengottuvelan M., Viswanathan P., Nalini N. Chemopreventive effect of trans-resveratrol-α phytoalexin against colonic aberrant crypt foci and cell proliferation in 1,2-dimethylhydrazine induced colon carcinogenesis. Carcinogenesis 2006, 27:1038-1046.
42. Seo H.J., Jeong K.S., Lee M.K., Park Y.B., Jung U.J., Kim H.J., Choi M.S. Role of naringin supplement in regulation of lipid and ethanol metabolism in rats. Life Sci. 2003, 73:933-946.
43. Sequetto P.L., Oliveira T.T., Soares I.A., Maldonado I.R., Mello V.J., Pizziolo V.R., Almeida M.R., Novaes R.D. The flavonoid chrysin attenuates colorectal pathological remodeling reducing the number and severity of pre-neoplastic lesions in rats exposed to the carcinogen 1,2-dimethylhydrazine. Cell Tissue Res. 2013, 352:327-339.
44. Singh D., Chopra K. The effect of naringin, a bioflavonoid on ischemia-reperfusion induced renal injury in rats. Pharmacol. Res. 2004, 50:187-193.
45. Spilsbury A., Vauzour D., Spencer J.P.E., Rattray M. Regulation of NF-κB activity in astrocytes: effects of flavonoids at dietary-relevant concentrations. Biochem. Biophys. Res. Commun. 2012, 418:578-583.
46. Talalay P., De Long M.J., Prochaska H.J. Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc. Natl. Acad. Sci. 1988, 85:8261-8265.
47. Tanaka T., Makita H., Kawabata K., Mori H., Kakumoto M., Satoh K., Hara A., Sumida T., Tanaka T., Ogawa H. Chemoprevention of azoxymethane-induced rat colon carcinogenesis by the naturally occurring flavonoids, diosmin and hesperidin. Carcinogenesis 1997, 18:957-965.
48. Theodoratou E., Kyle J., Cetnarskyj R., Farrington S.M., Tenesa A., Barnetson R., Porteous M., Dunlop M., Campbell H. Dietary flavonoids and the risk of colorectal cancer. Cancer Epidemiol. Biomark. Prev. 2007, 16:684-693.
49. Ullman T.A., Itzkowitz S.H. Intestinal inflammation and cancer. Gastroenterology 2011, 140:1807-1816.
50. Vanamala J., Leonardi T., Patil B.S., Taddeo S.S., Murphy M.E., Pike L.M., Chapkin R.S., Lupton J.R., Turner N.D. Suppression of colon carcinogenesis by bioactive compounds in grapefruit. Carcinogenesis 2006, 27:1257-1265.
51. Wargovich M.J., Jimenez A., McKee K., Steele V.E., Velasco M., Woods J., Price R., Gray K., Kelloff G.J. Efficacy of potential chemopreventive agents on rat colon aberrant crypt formation and progression. Carcinogenesis 2000, 21:1149-1155.
52. Weinberg W. The role of iron in cancer. Eur. J. Cancer Prev. 1996, 5:19-36.
53. Wolffram S., Blöck M., Ader P. Quercetin-3-glucoside is transported by the glucose carrier SGLT1 across the brush border membrane of rat small intestine. J. Nutr. 2002, 132:630-635.
54. Yoshimi N., Morioka T., Kinjo T., Inamine M., Kaneshiro T., Shimizu T., Suzui M., Yamada Y., Mori H. Histological and immunohistochemical observations of mucin-depleted foci (MDF) stained with Alcian blue, in rat colon carcinogenesis induced with 1,2-dimethylhydrazine dihydrochloride. Cancer Sci. 2004, 95:792-797.