Suppressed Helicobacter pylori-associated gastric tumorigenesis in Fat-1 transgenic mice producing endogenous ω-3 polyunsaturated fatty acids

Oncotarget

Volumn 7, Issue 41, 2016, Pages 66606-66622

  Han, Young Min ^a   Kim, Kyung Jo ^b   Jeong, Migyeung ^a   Park, Jong Min ^a   Go, Eun Jin ^a   Kang, Jing X ^c   Hong, Sung Pyo ^d   Hahm, Ki Baik ^a,d  

^a CHA University   (South Korea)

^b University of Ulsan   (South Korea)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d CHA Bundang Medical Center   (South Korea)

Author keywords

15 PGDH; Anti proliferation; COX 2; Fat 1 transgenic mice; 3 PUFAs

Indexed keywords

15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; CYCLOOXYGENASE 2; OMEGA 3 FATTY ACID; PANTOPRAZOLE; CADHERIN; FATH PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATROPHIC GASTRITIS; CANCER PREVENTION; CARCINOGENESIS; COMPARATIVE STUDY; CONTROLLED STUDY; COX 2 GENE; DIET SUPPLEMENTATION; GENE EXPRESSION; HELICOBACTER INFECTION; HIGH SODIUM INTAKE; MALE; MOUSE; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; STOMACH CANCER; ANIMAL; BIOSYNTHESIS; COMPLICATION; HELICOBACTER PYLORI; INFLAMMATION; METABOLISM; MICROBIOLOGY; PATHOLOGY; STOMACH TUMOR; TRANSGENIC MOUSE;

ANIMALS; CADHERINS; CARCINOGENESIS; FATTY ACIDS, OMEGA-3; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; INFLAMMATION; MICE; MICE, TRANSGENIC; STOMACH NEOPLASMS;

EID: 84994018384     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.11261     Document Type: Article

References (61)

1. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994 IARC Monogr Eval Carcinog Risks Hum. 1994; 61:1-241.
2. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001; 345:784-789.
3. Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, Terao S, Amagai K, Hayashi S, Asaka M, Japan Gast Study G. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008; 372:392-397.
4. Zhang W, Lu H, Graham DY. An Update on Helicobacter pylori as the Cause of Gastric Cancer. Gastrointestinal tumors. 2014; 1:155-165.
5. Kuipers EJ, Sipponen P. Helicobacter pylori eradication for the prevention of gastric cancer. Helicobacter. 2006; 11:52-57.
6. Lee HJ, Park JM, Han YM, Gil HK, Kim J, Chang JY, Jeong M, Go EJ, Hahm KB. The role of chronic inflammation in the development of gastrointestinal cancers: reviewing cancer prevention with natural anti-inflammatory intervention. Expert review of gastroenterology & hepatology. 2016; 10:129-139.
7. Park JM, Jeong M, Kim EH, Han YM, Kwon SH, Hahm KB. Omega-3 Polyunsaturated Fatty Acids Intake to Regulate Helicobacter pylori-Associated Gastric Diseases as Nonantimicrobial Dietary Approach. BioMed research international. 2015; 2015:712363.
8. Jeong M, Park JM, Han YM, Park KY, Lee DH, Yoo JH, Cho JY, Hahm KB. Dietary prevention of Helicobacter pylori-associated gastric cancer with kimchi. Oncotarget. 2015; 6:29513-29526. doi: 10.18632/oncotarget.4897.
9. Han YM, Park JM, Jeong M, Yoo JH, Kim WH, Shin SP, Ko WJ, Hahm KB. Dietary, non-microbial intervention to prevent Helicobacter pylori-associated gastric diseases. Annals of translational medicine. 2015; 3:122.
10. Hartgrink HH, Jansen EP, van Grieken NC, van de Velde CJ. Gastric cancer. Lancet. 2009; 374:477-490.
11. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002; 420:860-867.
12. Park SH, Kangwan N, Park JM, Kim EH, Hahm KB. Non-microbial approach for Helicobacter pylori as faster track to prevent gastric cancer than simple eradication. World journal of gastroenterology. 2013; 19:8986-8995.
13. Calder PC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. The American journal of clinical nutrition. 2006; 83:1505S-1519S.
14. Calder PC. Dietary modification of inflammation with lipids. The Proceedings of the Nutrition Society. 2002; 61:345-358.
15. Simopoulos AP. Omega-3 fatty acids in inflammation and autoimmune diseases. Journal of the American College of Nutrition. 2002; 21:495-505.
16. Yates CM, Calder PC, Ed Rainger G. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacology & therapeutics. 2014; 141:272-282.
17. Kremer JM. n-3 fatty acid supplements in rheumatoid arthritis. The American journal of clinical nutrition. 2000; 71:349S-351S.
18. Riediger ND, Othman RA, Suh M, Moghadasian MH. A systemic review of the roles of n-3 fatty acids in health and disease. Journal of the American Dietetic Association. 2009; 109:668-679.
19. Kang JX, Wang J. A simplified method for analysis of polyunsaturated fatty acids. BMC biochemistry. 2005; 6:5.
20. Kang JX. Fat-1 transgenic mice: a new model for omega-3 research. Prostaglandins, leukotrienes, and essential fatty acids. 2007; 77:263-267.
21. Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA. Chronic inflammation and cytokines in the tumor microenvironment. Journal of immunology research. 2014; 2014:149185.
22. Thompson L, Cockayne A, Spiller RC. Inhibitory effect of polyunsaturated fatty acids on the growth of Helicobacter pylori: a possible explanation of the effect of diet on peptic ulceration. Gut. 1994; 35:1557-1561.
23. Correia M, Michel V, Matos AA, Carvalho P, Oliveira MJ, Ferreira RM, Dillies MA, Huerre M, Seruca R, Figueiredo C, Machado JC, Touati E. Docosahexaenoic acid inhibits Helicobacter pylori growth in vitro and mice gastric mucosa colonization. PloS one. 2012; 7:e35072.
24. Nam KT, Oh SY, Ahn B, Kim YB, Jang DD, Yang KH, Hahm KB, Kim DY. Decreased Helicobacter pylori associated gastric carcinogenesis in mice lacking inducible nitric oxide synthase. Gut. 2004; 53: 1250-1255.
25. Yeo M, Kim DK, Han SU, Lee JE, Kim YB, Cho YK, Kim JH, Cho SW, Hahm KB. Novel action of gastric proton pump inhibitor on suppression of Helicobacter pylori induced angiogenesis. Gut. 2006; 55:26-33.
26. Mantovani A, Allavena P, Sica A, Balkwill F. Cancerrelated inflammation. Nature. 2008; 454:436-444.
27. Kovaleva IE, Grivennikov SI, Luzikov VN. On the effect of cholesterol on the fate of CYP11A1 imported into yeast mitochondria in vivo. Biochemistry Biokhimiia. 2000; 65:1206-1211.
28. Wang D, Dubois RN. Eicosanoids and cancer. Nature reviews Cancer. 2010; 10:181-193.
29. Wall R, Ross RP, Fitzgerald GF, Stanton C. Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutrition reviews. 2010; 68:280-289.
30. Abete P, Testa G, Galizia G, Della-Morte D, Cacciatore F, Rengo F. PUFA for human health: diet or supplementation? Current pharmaceutical design. 2009; 15:4186-4190.
31. Chapkin RS, McMurray DN, Lupton JR. Colon cancer, fatty acids and anti-inflammatory compounds. Current opinion in gastroenterology. 2007; 23:48-54.
32. Groeger AL, Cipollina C, Cole MP, Woodcock SR, Bonacci G, Rudolph TK, Rudolph V, Freeman BA, Schopfer FJ. Cyclooxygenase-2 generates antiinflammatory mediators from omega-3 fatty acids. Nature chemical biology. 2010; 6:433-441.
33. Masoodi M, Kuda O, Rossmeisl M, Flachs P, Kopecky J. Lipid signaling in adipose tissue: Connecting inflammation & metabolism. Biochimica et biophysica acta. 2015; 1851:503-518.
34. Ulrich CM, Bigler J, Potter JD. Non-steroidal antiinflammatory drugs for cancer prevention: promise, perils and pharmacogenetics. Nature reviews Cancer. 2006; 6:130-140.
35. Tan VP, Wong BC. Gastric cancer chemoprevention: the current evidence. Gastroenterology clinics of North America. 2013; 42:299-316.
36. Na HK, Park JM, Lee HG, Lee HN, Myung SJ, Surh YJ. 15-Hydroxyprostaglandin dehydrogenase as a novel molecular target for cancer chemoprevention and therapy. Biochemical pharmacology. 2011; 82:1352-1360.
37. Tai HH. Prostaglandin catabolic enzymes as tumor suppressors. Cancer metastasis reviews. 2011; 30:409-417.
38. Han YM, Park JM, Cha JY, Jeong M, Go EJ, Hahm KB. Endogenous conversion of omega-6 to omega-3 polyunsaturated fatty acids in fat-1 mice attenuated intestinal polyposis by either inhibiting COX-2/beta-catenin signaling or activating 15-PGDH/IL-18. International journal of cancer. 2016; 138: 2247-2256.
39. Park JM, Park SH, Hong KS, Han YM, Jang SH, Kim EH, Hahm KB. Special licorice extracts containing lowered glycyrrhizin and enhanced licochalcone A prevented Helicobacter pyloriinitiated, salt diet-promoted gastric tumorigenesis. Helicobacter. 2014; 19:221-236.
40. Thiel A, Ganesan A, Mrena J, Junnila S, Nykanen A, Hemmes A, Tai HH, Monni O, Kokkola A, Haglund C, Petrova TV, Ristimaki A. 15-hydroxyprostaglandin dehydrogenase is down-regulated in gastric cancer. Clinical cancer research. 2009; 15:4572-4580.
41. Nishizawa T, Suzuki H. Gastric Carcinogenesis and Underlying Molecular Mechanisms: Helicobacter pylori and Novel Targeted Therapy. BioMed research international. 2015; 2015:794378.
42. Ding SZ, Goldberg JB, Hatakeyama M. Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. Future oncology. 2010; 6:851-862.
43. Yu H, Zeng J, Liang X, Wang W, Zhou Y, Sun Y, Liu S, Li W, Chen C, Jia J. Helicobacter pylori promotes epithelial-mesenchymal transition in gastric cancer by downregulating programmed cell death protein 4 (PDCD4). PloS one. 2014; 9:e105306.
44. Sasaki T, Yamashita Y, Kuniyasu H. AKT plays a crucial role in gastric cancer. Oncology letters. 2015; 10:607-611.
45. Song X, Xin N, Wang W, Zhao C. Wnt/beta-catenin, an oncogenic pathway targeted by H. pylori in gastric carcinogenesis. Oncotarget. 2015; 6:35579-35588. doi: 10.18632/oncotarget.5758.
46. Donnelly JM, Chawla A, Houghton J, Zavros Y. Sonic hedgehog mediates the proliferation and recruitment of transformed mesenchymal stem cells to the stomach. PloS one. 2013; 8:e75225.
47. Xia HH, Talley NJ. Apoptosis in gastric epithelium induced by Helicobacter pylori infection: implications in gastric carcinogenesis. The American journal of gastroenterology. 2001; 96:16-26.
48. Beckenkamp A, Davies S, Willig JB, Buffon A. DPPIV/CD26: a tumor suppressor or a marker of malignancy? Tumour biology. 2016; 37:7059-7073.
49. Takaishi S, Wang TC. Gene expression profiling in a mouse model of Helicobacter-induced gastric cancer. Cancer science. 2007; 98:284-293.
50. Busiello I, Acquaviva R, Di Popolo A, Blanchard TG, Ricci V, Romano M, Zarrilli R. Helicobacter pylori gamma-glutamyltranspeptidase upregulates COX-2 and EGF-related peptide expression in human gastric cells. Cellular microbiology. 2004; 6: 255-267.
51. Tuccillo C, Manzo BA, Nardone G, D'Argenio G, Rocco A, Di Popolo A, Della VN, Staibano S, De Rosa G, Ricci V, Del Vecchio BC, Zarrilli R, Romano M. Up-regulation of heparin binding epidermal growth factor-like growth factor and amphiregulin expression in Helicobacter pylori-infected human gastric mucosa. Digestive and liver disease. 2002; 34:498-505.
52. Pham TM, Fujino Y, Kikuchi S, Tamakoshi A, Yatsuya H, Matsuda S, Yoshimura T, Group JS. A nested case-control study of stomach cancer and serum insulin-like growth factor (IGF)-1, IGF-2 and IGF-binding protein (IGFBP)-3. European journal of cancer. 2007; 43:1611-1616.
53. Ramljak D, Jones AB, Diwan BA, Perantoni AO, Hochadel JF, Anderson LM. Epidermal growth factor and transforming growth factor-alpha-associated overexpression of cyclin D1, Cdk4, and c-Myc during hepatocarcinogenesis in Helicobacter hepaticusinfected A/JCr mice. Cancer research. 1998; 58: 3590-3597.
54. MacLean CH, Newberry SJ, Mojica WA, Khanna P, Issa AM, Suttorp MJ, Lim YW, Traina SB, Hilton L, Garland R, Morton SC. Effects of omega-3 fatty acids on cancer risk: a systematic review. Jama. 2006; 295:403-415.
55. Higurashi T, Takahashi H, Endo H, Hosono K, Yamada E, Ohkubo H, Sakai E, Uchiyama T, Hata Y, Fujisawa N, Uchiyama S, Ezuka A, Nagase H, et al. Metformin efficacy and safety for colorectal polyps: a double-blind randomized controlled trial. BMC cancer. 2012; 12:118.
56. Hull MA, Sandell AC, Montgomery AA, Logan RF, Clifford GM, Rees CJ, Loadman PM, Whitham D. A randomized controlled trial of eicosapentaenoic acid and/or aspirin for colorectal adenoma prevention during colonoscopic surveillance in the NHS Bowel Cancer Screening Programme (The seAFOod Polyp Prevention Trial): study protocol for a randomized controlled trial. Trials. 2013; 14:237.
57. Gaddy JA, Radin JN, Loh JT, Zhang F, Washington MK, Peek RM, Jr., Algood HM, Cover TL. High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infection and immunity. 2013; 81:2258-2267.
58. Nam SY, Kim N, Lee CS, Choi KD, Lee HS, Jung HC, Song IS. Gastric mucosal protection via enhancement of MUC5AC, MUC6 by geranylgeranylacetone. Digestive diseases and sciences. 2005; 50:2110-2120.
59. Goo MJ, Ki MR, Lee HR, Yang HJ, Yuan DW, Hong IH, Park JK, Hong KS, Han JY, Hwang OK, Kim DH, Do SH, Cohn RD, et al. Helicobacter pylori promotes hepatic fibrosis in the animal model. Laboratory investigation. 2009; 89:1291-1303.
60. Lacy ER, Ito S. Microscopic analysis of ethanol damage to rat gastric mucosa after treatment with a prostaglandin. Gastroenterology. 1982; 83:619-625.
61. Nowak J, Weylandt KH, Habbel P, Wang J, Dignass A, Glickman JN, Kang JX. Colitis-associated colon tumorigenesis is suppressed in transgenic mice rich in endogenous n-3 fatty acids. Carcinogenesis. 2007; 28:1991-1995.