Nobiletin and its colonic metabolites suppress colitis-associated colon carcinogenesis by down-regulating iNOS, inducing antioxidative enzymes and arresting cell cycle progression

Journal of Nutritional Biochemistry

Volumn 42, Issue , 2017, Pages 17-25

  Wu, Xian ^a   Song, Mingyue ^a   Gao, Zili ^a   Sun, Yue ^a,b   Wang, Minqi ^a   Li, Fang ^a   Zheng, Jinkai ^a,c   Xiao, Hang ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b ANHUI AGRICULTURAL UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Cell cycle; Chemoprevention; Colon carcinogenesis; iNOS; Metabolites; Nobiletin; Nrf2

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTINEOPLASTIC AGENT; DRUG METABOLITE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE QUINONE OXIDOREDUCTASE 1; NOBILETIN; OXIDOREDUCTASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIOXIDANT; ENZYME; FLAVONE DERIVATIVE; NOS2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; COLITIS; COLON CARCINOGENESIS; COLON TISSUE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; HCT 116 CELL LINE; HUMAN; HUMAN CELL; MACROPHAGE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAW 264.7 CELL LINE; SIGNAL TRANSDUCTION; UPREGULATION; VALIDATION STUDY; ANIMAL; CELL CYCLE; CELL LINE; COLON TUMOR; COMPLICATION; DRUG EFFECTS; INBRED MOUSE STRAIN; METABOLISM; ORAL DRUG ADMINISTRATION;

ADMINISTRATION, ORAL; ANIMALS; ANTICARCINOGENIC AGENTS; ANTIOXIDANTS; CELL CYCLE; CELL LINE; COLITIS; COLONIC NEOPLASMS; DOWN-REGULATION; ENZYMES; FLAVONES; HCT116 CELLS; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE, INBRED STRAINS; NITRIC OXIDE SYNTHASE TYPE II;

EID: 85009429485     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2016.12.020     Document Type: Article

References (37)

1. [1] Li, S., Pan, M.-H., Lo, C.-Y., Tan, D., Wang, Y., Shahidi, F., et al. Chemistry and health effects of polymethoxyflavones and hydroxylated polymethoxyflavones. J Funct Foods 1 (2009), 2–12.
2. [2] Wu, X., Song, M., Wang, M., Zheng, J., Gao, Z., Xu, F., et al. Chemopreventive effects of nobiletin and its colonic metabolites on colon carcinogenesis. Mol Nutr Food Res 59 (2015), 2383–2394.
3. [3] Song, M., Charoensinphon, N., Wu, X., Zheng, J., Gao, Z., Xu, F., et al. Inhibitory effects of metabolites of 5-demethylnobiletin on human Nonsmall cell lung cancer cells. J Agric Food Chem 64 (2016), 4943–4949.
4. [4] Tang, M.X., Ogawa, K., Asamoto, M., Chewonarin, T., Suzuki, S., Tanaka, T., et al. Effects of nobiletin on PhIP-induced prostate and colon carcinogenesis in F344 rats. Nutr Cancer 63 (2011), 227–233.
5. [5] Suzuki, R., Kohno, H., Murakami, A., Koshimizu, K., Ohigashi, H., Yano, M., et al. Citrus nobiletin inhibits azoxymethane-induced large bowel carcinogenesis in rats. Biofactors 22 (2004), 111–114.
6. [6] Wu, X., Song, M., Rakariyatham, K., Zheng, J., Guo, S., Tang, Z., et al. Anti-inflammatory effects of 4'-demethylnobiletin, a major metabolite of nobiletin. J Funct Foods 19 (2015), 278–287.
7. [7] Wu, X., Song, M., Rakariyatham, K., Zheng, J., Wang, M., Xu, F., et al. Inhibitory effects of 4'-demethylnobiletin, a metabolite of nobiletin, on 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced inflammation in mouse ears. J Agric Food Chem 63 (2015), 10921–10927.
8. [8] Yasuda, N., Ishii, T., Oyama, D., Fukuta, T., Agato, Y., Sato, A., et al. Neuroprotective effect of nobiletin on cerebral ischemia–reperfusion injury in transient middle cerebral artery-occluded rats. Brain Res 1559 (2014), 46–54.
9. [9] Lee, Y.S., Cha, B.Y., Choi, S.S., Choi, B.K., Yonezawa, T., Teruya, T., et al. Nobiletin improves obesity and insulin resistance in high-fat diet-induced obese mice. J Nutr Biochem 24 (2013), 156–162.
10. [10] Lai, C.S., Wu, J.C., Ho, C.T., Pan, M.H., Disease chemopreventive effects and molecular mechanisms of hydroxylated polymethoxyflavones. Biofactors 41 (2015), 301–313.
11. [11] Zheng, J., Song, M., Dong, P., Qiu, P., Guo, S., Zhong, Z., et al. Identification of novel bioactive metabolites of 5-demethylnobiletin in mice. Mol Nutr Food Res 57 (2013), 1999–2007.
12. [12] Li, S., Wang, Z., Sang, S., Huang, M.T., Ho, C.T., Identification of nobiletin metabolites in mouse urine. Mol Nutr Food Res 50 (2006), 291–299.
13. [13] Li, S., Sang, S., Pan, M.H., Lai, C.S., Lo, C.Y., Yang, C.S., et al. Anti-inflammatory property of the urinary metabolites of nobiletin in mouse. Bioorg Med Chem Lett 17 (2007), 5177–5181.
14. [14] Funaro, A., Wu, X., Song, M., Zheng, J., Guo, S., Rakariyatham, K., et al. Enhanced anti-inflammatory activities by the combination of Luteolin and Tangeretin. J Food Sci 81 (2016), H1320–H1327.
15. [15] DiMarco-Crook, C., Xiao, H., Diet-based strategies for cancer chemoprevention: the role of combination regimens using dietary bioactive components. Doyle, M.P., Klaenhammer, T.R., (eds.) Annual review of food science and technology Annual reviews: Palo alto, 6, 2015, 505–526.
16. [16] Zheng, J., Bi, J., Johnson, D., Sun, Y., Song, M., Qiu, P., et al. Analysis of 10 metabolites of polymethoxyflavones with high sensitivity by electrochemical detection in high-performance liquid chromatography. J Agric Food Chem 63 (2015), 509–516.
17. [17] Reeves, P.G., Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 127 (1997), 838S–841S.
18. [18] Guo, S., Qiu, P., Xu, G., Wu, X., Dong, P., Yang, G., et al. Synergistic anti-inflammatory effects of nobiletin and sulforaphane in lipopolysaccharide-stimulated RAW 264.7 cells. J Agric Food Chem 60 (2012), 2157–2164.
19. [19] Qiu, P., Dong, P., Guan, H., Li, S., Ho, C.T., Pan, M.H., et al. Inhibitory effects of 5-hydroxy polymethoxyflavones on colon cancer cells. Mol Nutr Food Res 54:Suppl. 2 (2010), S244–S252.
20. [20] Xiao, H., Hao, X., Simi, B., Ju, J., Jiang, H., Reddy, B.S., et al. Green tea polyphenols inhibit colorectal aberrant crypt foci (ACF) formation and prevent oncogenic changes in dysplastic ACF in azoxymethane-treated F344 rats. Carcinogenesis 29 (2008), 113–119.
21. [21] Surh, Y.J., Chun, K.S., Cha, H.H., Han, S.S., Keum, Y.S., Park, K.K., et al. Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-kappa B activation. Mutat Res 480-481 (2001), 243–268.
22. [22] Rao, C.V., Nitric oxide signaling in colon cancer chemoprevention. Mutat Res 555 (2004), 107–119.
23. [23] Lai, C.S., Li, S., Chai, C.Y., Lo, C.Y., Dushenkov, S., Ho, C.T., et al. Anti-inflammatory and antitumor promotional effects of a novel urinary metabolite, 3',4'-didemethylnobiletin, derived from nobiletin. Carcinogenesis 29 (2008), 2415–2424.
24. [24] Xiong, Y., Chen, D., Yu, C., Lv, B., Peng, J., Wang, J., et al. Citrus nobiletin ameliorates experimental colitis by reducing inflammation and restoring impaired intestinal barrier function. Mol Nutr Food Res 59 (2015), 829–842.
25. [25] Wang, W.W., Smith, D.L., Zucker, S.D., Bilirubin inhibits iNOS expression and NO production in response to endotoxin in rats. Hepatology 40 (2004), 424–433.
26. [26] Rushworth, S.A., MacEwan, D.J., O'Connell, M.A., Lipopolysaccharide-induced expression of NAD(P)H:quinone oxidoreductase 1 and heme oxygenase-1 protects against excessive inflammatory responses in human monocytes. J Immunol 181 (2008), 6730–6737.
27. [27] Khor, T.O., Huang, M.T., Kwon, K.H., Chan, J.Y., Reddy, B.S., Kong, A.N., Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res 66 (2006), 11580–11584.
28. [28] Owa, T., Yoshino, H., Yoshimatsu, K., Nagasu, T., Cell cycle regulation in the G1 phase: a promising target for the development of new chemotherapeutic anticancer agents. Curr Med Chem 8 (2001), 1487–1503.
29. [29] Malumbres, M., Barbacid, M., Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 9 (2009), 153–166.
30. [30] McKay, J.A., Douglas, J.J., Ross, V.G., Curran, S., Loane, J.F., Ahmed, F.Y., et al. Analysis of key cell-cycle checkpoint proteins in colorectal tumours. J Pathol 196 (2002), 386–393.
31. [31] Takahashi, M., Fukuda, K., Ohata, T., Sugimura, T., Wakabayashi, K., Increased expression of inducible and endothelial constitutive nitric oxide synthases in rat colon tumors induced by azoxymethane. Cancer Res 57 (1997), 1233–1237.
32. [32] Klaunig, J.E., Kamendulis, L.M., Hocevar, B.A., Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 38 (2010), 96–109.
33. [33] Kwak, M.K., Kensler, T.W., Targeting NRF2 signaling for cancer chemoprevention. Toxicol Appl Pharmacol 244 (2010), 66–76.
34. [34] Khor, T.O., Huang, M.T., Prawan, A., Liu, Y., Hao, X., Yu, S., et al. Increased susceptibility of Nrf2 knockout mice to colitis-associated colorectal cancer. Cancer Prev Res 1 (2008), 187–191.
35. [35] Thangapazham, R.L., Sharma, A., Maheshwari, R.K., Multiple molecular targets in cancer chemoprevention by curcumin. AAPS J 8 (2006), E443–E449.
36. [36] Kundu, J.K., Surh, Y.J., Cancer chemopreventive and therapeutic potential of resveratrol: mechanistic perspectives. Cancer Lett 269 (2008), 243–261.
37. [37] Clarke, J.D., Dashwood, R.H., Ho, E., Multi-targeted prevention of cancer by sulforaphane. Cancer Lett 269 (2008), 291–304.