Chemoprevention of colonic tumorigenesis by dietary hydroxylated polymethoxyflavones in azoxymethane-treated mice

Molecular Nutrition and Food Research

Volumn 55, Issue 2, 2011, Pages 278-290

  Lai, Ching Shu ^a,b   Tsai, Mei Ling ^a   Cheng, An Chin ^c   Li, Shiming ^d   Lo, Chih Yu ^e   Wang, Yu ^d   Xiao, Hang ^f   Ho, Chi Tang ^d   Wang, Ying Jan ^b   Pan, Min Hsiung ^a  

^a NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c CHANG JUNG CHRISTIAN UNIVERSITY   (Taiwan)

^d RUTGERS UNIVERSITY   (United States)

^e NATIONAL CHIAYI UNIVERSITY   (Taiwan)

^f UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

5 Hydroxy polymethoxyflavones; Aberrant crypt foci; Apoptosis; Colonic tumorigenesis; Inflammation

Indexed keywords

AZOXYMETHANE; CARCINOGEN; CYCLOOXYGENASE 2; FLAVONE DERIVATIVE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NOS2 PROTEIN, MOUSE; PTGS2 PROTEIN, MOUSE;

ABERRANT CRYPT FOCUS; ADENOMA; ANIMAL; APOPTOSIS; ARTICLE; CHEMISTRY; COLON; COLON TUMOR; DIET; DRUG EFFECT; FRUIT; GENE EXPRESSION REGULATION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; ISOLATION AND PURIFICATION; MALE; METABOLISM; MOUSE; PATHOLOGY; RANDOMIZATION; SIGNAL TRANSDUCTION; SWEET ORANGE; TIME;

ABERRANT CRYPT FOCI; ADENOMA; ANIMALS; APOPTOSIS; AZOXYMETHANE; CARCINOGENS; CITRUS SINENSIS; COLON; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; DIET; FLAVONES; FRUIT; GENE EXPRESSION REGULATION, NEOPLASTIC; MALE; MICE; MICE, INBRED ICR; NITRIC OXIDE SYNTHASE TYPE II; RANDOM ALLOCATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS;

CITRUS; MUS;

EID: 78650893286     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201000224     Document Type: Article

References (54)

1. Janakiram, N. B., Rao, C. V., Molecular markers and targets for colorectal cancer prevention. Acta Pharmacol. Sin. 2008, 29, 1-20.
2. Benson, A. B., III Epidemiology, disease progression, and economic burden of colorectal cancer. J. Manag. Care Pharm. 2007, 13, S5-S18.
3. Fearon, E. R., Vogelstein, B., A genetic model for colorectal tumorigenesis. Cell 1990, 61, 759-767.
4. Takayama, T., Katsuki, S., Takahashi, Y., Ohi, M. et al., Aberrant crypt foci of the colon as precursors of adenoma and cancer. N. Engl. J. Med. 1998, 339, 1277-1284.
5. Takayama, T., Miyanishi, K., Hayashi, T., Kukitsu, T. et al., Aberrant crypt foci: detection, gene abnormalities, and clinical usefulness. Clin. Gastroenterol. Hepatol. 2005, 3, S42-S45.
6. Segditsas, S., Tomlinson, I., Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 2006, 25, 7531-7537.
7. Li, J., Mizukami, Y., Zhang, X., Jo, W. S. et al., Oncogenic K-ras stimulates Wnt signaling in colon cancer through inhibition of GSK-3beta. Gastroenterology 2005, 128, 1907-1918.
8. Giehl, K., Oncogenic Ras in tumour progression and metastasis. Biol. Chem. 2005, 386, 193-205.
9. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. et al., Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378, 785-789.
10. Cohen, G., Mustafi, R., Chumsangsri, A., Little, N. et al., Epidermal growth factor receptor signaling is up-regulated in human colonic aberrant crypt foci. Cancer Res. 2006, 66, 5656-5664.
11. Fichera, A., Little, N., Jagadeeswaran, S., Dougherty, U. et al., Epidermal growth factor receptor signaling is required for microadenoma formation in the mouse azoxymethane model of colonic carcinogenesis. Cancer Res. 2007, 67, 827-835.
12. Itzkowitz, S. H., Yio, X., Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am. J. Physiol Gastrointest. Liver Physiol. 2004, 287, G7-G17.
13. Kundu, J. K., Surh, Y. J., Inflammation: gearing the journey to cancer. Mutat. Res. 2008, 659, 15-30.
14. Takahashi, M., Wakabayashi, K., Gene mutations and altered gene expression in azoxymethane-induced colon carcinogenesis in rodents. Cancer Sci. 2004, 95, 475-480.
15. Mathew, A., Peters, U., Chatterjee, N., Kulldorff, M. et al., Fat, fiber, fruits, vegetables, and risk of colorectal adenomas. Int. J. Cancer 2004, 108, 287-292.
16. Michels, K. B., Giovannucci, E., Chan, A. T., Singhania, R. et al., Fruit and vegetable consumption and colorectal adenomas in the Nurses' Health Study. Cancer Res. 2006, 66, 3942-3953.
17. Kune, G., Watson, L., Colorectal cancer protective effects and the dietary micronutrients folate, methionine, vitamins B6, B12, C, E, selenium, and lycopene. Nutr. Cancer 2006, 56, 11-21.
18. Silalahi, J., Anticancer and health protective properties of citrus fruit components. Asia Pac. J. Clin. Nutr. 2002, 11, 79-84.
19. Li, S., Lo, C. Y., Ho, C. T., Hydroxylated polymethoxyflavones and methylated flavonoids in sweet orange (Citrus sinensis) peel. J. Agric. Food Chem. 2006, 54, 4176-4185.
20. Li, S., Pan, M. H., Lo, C. Y., Tan, D. et al., Chemistry and health effects of polymethoxyflavones and hydroxylated polymethoxyflavones. J. Functional Foods 2009, 1, 2-12.
21. Lai, C. S., Li, S., Chai, C. Y., Lo, C. Y. et al., Inhibitory effect of citrus 5-hydroxy-3, 6, 7, 8, 3', 4'-hexamethoxyflavone on 12-O-tetradecanoylphorbol 13-acetate-induced skin inflammation and tumor promotion in mice. Carcinogenesis 2007, 28, 2581-2588.
22. Kohno, H., Yoshitani, S., Tsukio, Y., Murakami, A. et al., Dietary administration of citrus nobiletin inhibits azoxymethane-induced colonic aberrant crypt foci in rats. Life Sci. 2001, 69, 901-913.
23. Suzuki, R., Kohno, H., Murakami, A., Koshimizu, K. et al., Citrus nobiletin inhibits azoxymethane-induced large bowel carcinogenesis in rats. Biofactors 2004, 22, 111-114.
24. Li, S., Pan, M. H., Lai, C. S., Lo, C. Y. et al., Isolation and syntheses of polymethoxyflavones and hydroxylated polymethoxyflavones as inhibitors of HL-60 cell lines. Bioorg. Med. Chem. 2007, 15, 3381-3389.
25. Qiu, P., Dong, P., Guan, H., Li, S. et al., Inhibitory effects of 5-hydroxy polymethoxyflavones on colon cancer cells. Mol. Nutr. Food Res. 2010, 54, S244-S252.
26. Li, S., Wang, Y., Wang, Z., Xiao, H. et al., Quantitative analysis of hydroxylated polymethoxyflavones by high-performance liquid chromatography. Biomed. Chromatogr. 2010. DOI: 10.1002/bmc.1372.
27. AIN 76. Report of the American Institute of Nutrition Ad Hoc Committee on standards for nutritional studies. J. Nutr. 1977, 107, 1340-1348.
28. McLellan, E. A., Medline, A., Bird, R.P., Sequential analyses of the growth and morphological characteristics of aberrant crypt foci: putative preneoplastic lesions. Cancer Res. 1991, 51, 5270-5274.
29. Morin, P. J., Sparks, A. B., Korinek, V., Barker, N. et al., Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275, 1787-1790.
30. Korinek, V., Barker, N., Morin, P. J., van, W. D. et al., Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 1997, 275, 1784-1787.
31. Tetsu, O., McCormick, F., Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999, 398, 422-426.
32. Easwaran, V., Lee, S. H., Inge, L., Guo, L. et al., beta-Catenin regulates vascular endothelial growth factor expression in colon cancer. Cancer Res. 2003, 63, 3145-3153.
33. Lee, C. H., Jeon, Y. T., Kim, S. H., Song, Y. S., NF-kappaB as a potential molecular target for cancer therapy. Biofactors 2007, 29, 19-35.
34. Ma, X. T., Wang, S., Ye, Y. J., Du, R. Y. et al., Constitutive activation of Stat3 signaling pathway in human colorectal carcinoma. World J. Gastroenterol. 2004, 10, 1569-1573.
35. Levy, D. E., Lee, C. K., What does Stat3 do? J. Clin. Invest 2002, 109, 1143-1148.
36. Wakeling, A. E., Guy, S. P., Woodburn, J. R., Ashton, S. E. et al., ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res. 2002, 62, 5749-5754.
37. Brabletz, T., Jung, A., Dag, S., Hlubek, F. et al., beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am. J. Pathol. 1999, 155, 1033-1038.
38. Wali, R. K., Khare, S., Tretiakova, M., Cohen, G. et al., Ursodeoxycholic acid and F(6)-D(3) inhibit aberrant crypt proliferation in the rat azoxymethane model of colon cancer: roles of cyclin D1 and E-cadherin. Cancer Epidemiol. Biomarkers Prev. 2002, 11, 1653-1662.
39. Tsanou, E., Peschos, D., Batistatou, A., Charalabopoulos, A. et al., The E-cadherin adhesion molecule and colorectal cancer. A global literature approach. Anticancer Res. 2008, 28, 3815-3826.
40. Wijnhoven, B. P., Dinjens, W. N., Pignatelli, M., E-cadherin-catenin cell-cell adhesion complex and human cancer. Br. J. Surg. 2000, 87, 992-1005.
41. Jawhari, A., Farthing, M., Pignatelli, M., The importance of the E-cadherin-catenin complex in the maintenance of intestinal epithelial homoeostasis: more than intercellular glue? Gut 1997, 41, 581-584.
42. Bing, R. J., Miyataka, M., Rich, K. A., Hanson, N. et al., Nitric oxide, prostanoids, cyclooxygenase, and angiogenesis in colon and breast cancer. Clin. Cancer Res. 2001, 7, 3385-3392.
43. Normanno, N., De, L. A., Bianco, C., Strizzi, L. et al., Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 2006, 366, 2-16.
44. Biscardi, J. S., Maa, M. C., Tice, D. A., Cox, M. E. et al., c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J. Biol. Chem. 1999, 274, 8335-8343.
45. Emlet, D. R., Moscatello, D. K., Ludlow, L. B., Wong, A. J., Subsets of epidermal growth factor receptors during activation and endocytosis. J. Biol. Chem. 1997, 272, 4079-4086.
46. Rojas, M., Yao, S., Lin, Y. Z., Controlling epidermal growth factor (EGF)-stimulated Ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J. Biol. Chem. 1996, 271, 27456-27461.
47. Coffey, R. J., Hawkey, C. J., Damstrup, L., Graves-Deal, R. et al., Epidermal growth factor receptor activation induces nuclear targeting of cyclooxygenase-2, basolateral release of prostaglandins, and mitogenesis in polarizing colon cancer cells. Proc. Natl. Acad. Sci. USA 1997, 94, 657-662.
48. Lin, S. Y., Makino, K., Xia, W., Matin, A. et al., Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat. Cell Biol. 2001, 3, 802-808.
49. Khosravi, S. P., Fernandez, P., I Tumoral angiogenesis: review of the literature. Cancer Invest. 2008, 26, 104-108.
50. Toomey, D. P., Murphy, J. F., Conlon, K. C., COX-2, VEGF and tumour angiogenesis. Surgeon 2009, 7, 174-180.
51. Hanahan, D., Weinberg, R. A., The hallmarks of cancer. Cell 2000, 100, 57-70.
52. Sergeev, I. N., Ho, C. T., Li, S., Colby, J., Dushenkov, S., Apoptosis-inducing activity of hydroxylated polymethoxyflavones and polymethoxyflavones from orange peel in human breast cancer cells. Mol. Nutr. Food Res. 2009, 51, 1478-1484.
53. Sergeev, I. N., Li, S., Colby, J., Ho, C. T., Dushenkov, S., Polymethoxylated flavones induce Ca2+-mediated apoptosis in breast cancer cells. Life Sci. 2006, 80, 245-253.
54. Sergeev, I. N., Li, S., Ho, C. T., Rawson, N. E., Dushenkov, S., Polymethoxyflavones activate Ca2+-dependent apoptotic targets in adipocytes. J. Agric. Food Chem. 2009, 57, 5771-5776.