Kimchi protects against azoxymethane/dextran sulfate sodium-induced colorectal carcinogenesis in mice

Journal of Medicinal Food

Volumn 17, Issue 8, 2014, Pages 833-841

  Kim, Hee Young ^a   Song, Jia Le ^a   Chang, Hee Kyung ^b   Kang, Soon Ah ^c   Park, Kun Young ^a  

^a Pusan National University   (South Korea)

^b Kosin University   (South Korea)

^c Hoseo University   (South Korea)

Author keywords

colorectal carcinogenesis; COX 2; iNOS; kimchi; p21; p53; proinflammatory cytokines

Indexed keywords

AZOXYMETHANE; DEXTRAN SULFATE; GAMMA INTERFERON; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; BAGG ALBINO MOUSE; BRASSICA; CARCINOGENESIS; CHEMICALLY INDUCED; COLON; COLONIC NEOPLASMS; DIET THERAPY; DRUG EFFECTS; GENETICS; HUMAN; MALE; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY;

ANIMALS; AZOXYMETHANE; BRASSICA; CARCINOGENESIS; COLON; COLONIC NEOPLASMS; DEXTRAN SULFATE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-6; MALE; MICE; MICE, INBRED BALB C; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84905864112     PISSN: 1096620X     EISSN: 15577600     Source Type: Journal    
DOI: 10.1089/jmf.2013.2986     Document Type: Article

References (64)

1. Cheigh HS, Park KY, Lee C: Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Crit Rev Food Sci 1994;34:175-203.
2. Park KY: Lactic acid bacterial in vegetable fermentation. In: Lactic Acid Bacteria: Microbiological and Functional Aspects. (Lahtinen S, Salminen S, Von Wright A, Ouwehand AC, eds.). CRC Press, New York, 2011, p. 187.
3. Park KY: The nutritional evaluation and anti-mutagenic and anticancer effects of kimchi. J Korean Soc Food Nutr 1995;24:169-182.
4. Cho EJ, Rhee SH, Lee SM, Park KY: In vitro antimutagenic and anticancer effects of kimchifractions. J Korean Assoc Cancer Prev 1997;2:113-131.
5. Kim EK, An SY, Lee MS, Kim TH, Lee HK, Hwang WS, Choe SJ, Kim TY, Han SJ, Kim HJ, Kim DJ, Lee KW: Fermented kimchi reduces body weight and improves metabolicparameters in overweight and obese patients. Nutr Res 2011;31:436-443.
6. Park JA, Tirupathi Pichiah PB, Yu JJ, Oh SH, Daily JW, 3rd, Cha YS: Anti-obesity effect of kimchi fermented with Weissella koreensis OK1-6 as starter in high-fat diet-induced obese C57BL/6J mice. J Appl Microbiol 2012;113:1507-1516.
7. Ryu BM, Ryu SH, Lee YS, Jeon YS, Moon GS: Effect of different kimchi diets on oxidation and photooxidation in liver and skin of hairless mice. J Korean Soc Food Nutr 2004;33:291-298.
8. Lee YM, Kwan MJ, Kim JK, Suh HS, Choi JS, Song YO: Isolation and identification of active principle in Chinese cabbage kimchi responsible for antioxidant activity. Korean J Food Sci Technol 2004;36:126-133.
9. Kim BK, Park KY, Kim HY, Ahn SC, Cho EJ: Anti-aging effects and mechanisms of kimchi during fermentation under stress-induced premature senescence cellular system. Food Sci Biotechnol 2011;20:643-649.
10. Kim HJ, Lee JS, Chung HY, Song SH, Suh H, Noh JS, Song YO: 3-(4′-Hydroxyl-3′, 5′-dimethoxyphenyl) propionic acid, an active principle of kimchi, inhibits development of atherosclerosis in rabbits. J Agric Food Chem 2007;55:10486-10492.
11. Noh JS, Kim HJ, Kwon MJ, Song YO: Active principle of kimchi, 3-(4′-hydroxyl-3′, 5′-dimethoxyphenyl) propionic acid, retards fatty streak formation at aortic sinus of apolipoprotein E knockout mice. J Med Food 2009;12:1206-1212.
12. Islam MS, Choi H: Antidiabetic effect of Korean traditional Baechu (Chinese cabbage) kimchi in a type 2 diabetes model of rats. J Med Food 2009;12:292-297.
13. Kong CS, Bahn YE, Kim BK, Lee KY, Park KY: Antiproliferative effect of chitosan-added kimchi in HT-29 human colon carcinoma cells. J Med Food 2010;13:6-12.
14. Park KY, Cho EJ, Rhee SH: Increased antimutagenic and anticancer activities of Chinese cabbage kimchi by changing kinds and levels of sub-ingredient. J Korean Soc Food Sci Nutr 1998;27:625-632.
15. Kim JY, Rhee SR, Park KY: Enhancement of anticancer activities of kimchi by manipulating ingredients. J Food Sci Nutr 2000;5:126-130.
16. Choi YS, Huwang JH, Kim JI, Jeon YS, Cheigh HS: Antioxidative antivity of mustard leaf kimchi with optional ingredients. J Korean Soc Food Sci Nutr 2000;29:1003-1008.
17. Itzkowitz SH, Yio X: Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2000;287:G7-G17.
18. Ekbom A, Helmick C, Zack M, Adami H-O: Ulcerative colitis and colorectal cancer: a population-based study. N Engl J Med 1990;323:1228-1233.
19. Popivanova BK, Kitamura K, Wu Y, Kondo T, Kagaya T, Kaneko S, Oshima M, Fujii C, Mukaida N: Blocking TNF-α in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008;118:560-570.
20. Wang S, Liu Z, Wang L, Zhang X: NF-kappaB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol 2009;6:327-334.
21. Koehne CH, Dubois RN: COX-2 inhibition and colorectal cancer. Semin Oncol 2004;31:12-21.
22. Rao CV: Nitric oxide signaling in colon cancer chemoprevention. Mutat Res 2004;555:107-119.
23. Potter JD: Colorectal cancer: molecules and populations. J Natl Cancer Inst 1999;91:916-932.
24. Xie J, Itzkowitz SH: Cancer in inflammatory bowel disease. World J Gastroenterol 2008;14:378-389.
25. Doyle VC: Nutrition and colorectal cancer risk: a literature review. Gastroenterol Nurs 2007;30:178-182.
26. Liu Y, Zhou W, Zhong D-W: Meta-analyses of the associations between four common TGF-β1 genetic polymorphisms and risk of colorectal tumor. Tumour Biol 2012;33:1191-1199.
27. Stewart BW, Kleihues P: World Cancer Report. IARC Press, Lyon, 2003.
28. Tanaka T, Kohno H, Suzuki R, Yamada Y, Sugie S, Mori H: A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci 2003;94:965-973.
29. Jung KO, Kil JH, Kim KH, Park KY: Effect of kimchi and its ingredients on the growth of Helicobacter pylori. Nutraceut Food 2003;8:149-153.
30. Mheen TI, Kwon TW: Effect of temperature and salt concentration on kimchi fermentation. Korean J Food Sci Technol 1984;16:443-450.
31. Lee EJ, Park KY, Kang SA, Han GJ, Park SE, Choi HS: Quality characteristics of kimchi fermented in permeability-controlled polyethylene containers. Korean J Food Preserv 2010;17:793-799.
32. Kim YT, Kim BK, Park KY: Antimutagenic and anticancer effects of leaf mustard and leaf mustard kimchi. J Food Sci Nutr 2007;12:84-88.
33. Jun DY, Kim JS, Park HS, Han CR, Fang Z, Woo MH, Rhee IK, Kim YH: Apoptogenic activity of auraptene of Zanthoxylum schinifolium toward human acute leukemia Jurkat T cells is associated with ER stress-mediated caspase-8 activation that stimulates mitochondria-dependent or -independent caspase cascade. Carcinogenesis 2007;28:1303-1313.
34. Choi SM, Kil JH, Jeon YS, Park KY: Fermentation characteristics, and antimutagenic and anticancer effects of mistletoe added kimchi. J Korean Asso Cancer Prev 2003;8:98-106.
35. Kim HY: Fermentation properties and inhibitory effects of anticancer functional baechu kimchi on AOM/DSS induced colitisassociated colon cancer in Balb/c mice. Master Thesis, Pusan National University, Busan, Korea, 2013.
36. Ullman TA, Itzkowitz SH: Intestinal inflammation and cancer. Gastroenterology 2011;140:1807-1816.
37. Tsujii M, Du Bois RN: Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 1995;83:493-501.
38. Salvemini D: Regulation of cyclooxygenase enzymes by nitric oxide. Cell Mol Life Sci 1997;53:576-582.
39. Sun Y, Tang XM, Half E, Kuo MT, Sinicrope FA: Cyclooxygenase- 2 overexpression reduces apoptotic susceptibility by inhibiting the cytochrome c-dependent apoptotic pathway in human colon cancer cells. Cancer Res 2002;62:6323-6328.
40. Sinicrope FA, Gill S: Role of cyclooxygenase-2 in colorectal cancer. Cancer Metastasis Rev 2004;23:63-75.
41. Rao CV, Kawamori T, Hamid R, Reddy BS: Chemoprevention of colonic aberrant crypt foci by an inducible nitric oxide synthase-selective inhibitor. Carcinogenesis 1999;20:641-644.
42. Rao CV, Indranie C, Simi B, Manning PT, Connor JR, Reddy BS: Chemopreventive properties of a selective inducible nitric oxide synthase inhibitor in colon carcinogenesis, administered alone or in combination with celecoxib, a selective cyclooxygenase- 2 inhibitor. Cancer Res 2002;62:165-170.
43. Eberhart CE, Coffey R, Radhika A, Giardiello F, Ferrenbach S, Du Bois R: Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 1994;107:1183-1188.
44. Greenhough A, Smartt HJ, Moore AE, Roberts HR, Williams AC, Paraskeva C, Kaidi A: The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 2009;30:377-386.
45. Kawamori T, Rao CV, Seibert K, Reddy BS: Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res 1998;58:409-412.
46. Triantafillidis JK, Nasioulas G, Kosmidis PA: Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res 2009;29:2727-2737.
47. Chang WC, Coudry RA, Clapper ML, Zhang X, Williams KL, Spittle CS, Li T, Cooper HS: Loss of p53 enhances the induction of colitis-associated neoplasia by dextran sulfatesodium. Carcinogenesis 2007;28:2375-2381.
48. Fujii S, Fujimori T, Kawamata H, Takeda J, Kitajima K, Omotehara F, Kaihara T, Kusaka T, Ichikawa K, Ohkura Y, Ono Y, Imura J, Yamaoka S, Sakamoto C, Ueda Y, Chiba T: Development of colonic neoplasia in p53 deficient mice with experimental colitis induced by dextran sulphate sodium. Gut 2004;53:710-716.
49. Hu Y, Le Leu RK, Young GP: Absence of acute apoptotic response to genotoxic carcinogens in p53-deficient mice is associated with increased susceptibility to azoxymethane-induced colon tumours. Int J Cancer 2005;115:561-567.
50. Qiu W, Carson-Walter EB, Kuan SF, Zhang L, Yu J: PUMA suppresses intestinal tumorigenesis in mice. Cancer Res 2009; 69:4999-5006.
51. Brugarolas J, Chandrasekaranl C, Gordoni JI, Beachil D, Jacks T: Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995;377:552-557.
52. Deng C, Zhang P, Wade Harper J, Elledge SJ, Leder P: Mice lacking p21CIP1/WAF1 undergonormal development, but are defective in G1 checkpoint control. Cell 1995;82:675-684.
53. Yang WC, Mathew J, Velcich A, Edelmann W, Kucherlapati R, Lipkin M, Yang K, Augenlicht LH: Targeted inactivation of the p21WAF1/cip1 gene enhances Apc-initiated tumor formation and the tumor-promoting activity of a Western-style high-risk diet by altering cell maturation in the intestinal mucosa. Cancer Res 2001;61:565-569.
54. Poole AJ, Heap D, Carroll RE, Tyner AL: Tumor suppressor functions for the Cdk inhibitor p21 in the mouse colon. Oncogene 2004;23:8128-8134.
55. Cheung KL, Khor TO, Huang MT, Kong AN: Differential in vivo mechanism of chemoprevention of tumor formation in azoxymethane/dextran sodium sulfate mice by PEITC and DBM. Carcinogenesis 2010;31:880-885.
56. Kim HY: Antioxidative effects of mustard leaves in vitro and in vivo. Doctoral Thesis, Pusan National University, Busan, Korea, 2002.
57. Yan X, Murphy BT, Hammond GB, Vinson JA, Neto CC: Antioxidant activities and antitumor screening of extracts from cranberry fruit (Vaccinium macrocarpon). J Agric Food Chem 2002;50:5844-5849.
58. Kim JE, Lee DE, Lee KW, Son JE, Seo SK, Li J, Jung SK, Heo YS, Mottamal M, Bode AM, Dong Z, Lee HJ: Isorhamnetin suppresses skin cancer through direct inhibition of MEK1 and PI3-K. Cancer Prev Res (Phila) 2011;4:582-591.
59. Boesch-Saadatmandi C, Loboda A, Wagner AE, Stachurska A, Jozkowicz A, Dulak J, Döring F, Wolffram S, Rimbach G: Effect of quercetin and its metabolites isorhamnetin and quercetin-3-glucuronide on inflammatory gene expression: role of miR-155. J Nutr Biochem 2011;22:293-299.
60. Saud SM, Young MR, Jones-Hall YL, Ileva L, Evbuomwan MO, Wise J, Colburn NH, Kim YS, Bobe G: Chemopreventive activity of plant flavonoid isorhamnetin in colorectal cancer is mediated by oncogenic Src and β-catenin. Cancer Res 2013;73: 5473-5484.
61. Hiroyuki N, Hideomi A, Koichi A, Kazutosi N: Antitumor activity of marine algae. Hydrobiologia 1990;204:577-584.
62. Chihara G, Maeda Y, Hamuro J, Sasaki T, Fukuoka F. Inhibition of mouse sarcoma 180 by polysaccharides from Lentinus edodes (Berk.) Sing. Nature 1969;222:687-688.
63. Yoon TJ, Yoo YC, Kang TB, Baeck YJ, Huh CS, Song SK, Lee KH, Azuma I, Kim JB: Prophylactic effect of Korean mistletoe (Viscum album coloratum) extract on tumor metastasis is mediated by enhancement of NK cell activity. Int J Immunopharmacol 1998;20:163-172.
64. Kim BK: Antiaging effects and anticancer mechanisms of kimchi during fermentation. Doctoral Thesis, Pusan National University, Busan, Korea, 2009.