Chemoprevention of esophageal adenocarcinoma in a rat model by ursodeoxycholic acid

Clinical and Experimental Medicine

Volumn 15, Issue 3, 2015, Pages 343-350

  Ojima, Eisuke ^a   Fujimura, Takashi ^a   Oyama, Katsunobu ^a   Tsukada, Tomoya ^a   Kinoshita, Jun ^a   Miyashita, Tomoharu ^a   Tajima, Hidehiro ^a   Fushida, Sachio ^a   Harada, Shin ichi ^a   Mukaisho, Ken ichi ^b   Hattori, Takanori ^b   Ohta, Tetsuo ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Barrett s esophagus; Caudal type homeobox 2; Chemoprevention; Esophageal adenocarcinoma; Gastroesophageal reflux disease; Ursodeoxycholic acid

Indexed keywords

BILE ACID; CHOLIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR CDX2; URSODEOXYCHOLIC ACID; ANTINEOPLASTIC AGENT; CDX2 PROTEIN, RAT; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BARRETT ESOPHAGUS; BILE; CANCER PREVENTION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGITIS; ESOPHAGUS; GASTROESOPHAGEAL REFLUX; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEQUENCE ANALYSIS; ADENOCARCINOMA; ANIMAL; CYTOCHEMISTRY; DISEASE MODEL; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION PROFILING; MICROSCOPY; PATHOLOGY; PROCEDURES; TREATMENT OUTCOME; WISTAR RAT;

ANIMALIA; RATTUS;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; CHEMOPREVENTION; DISEASE MODELS, ANIMAL; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; GENE EXPRESSION PROFILING; HISTOCYTOCHEMISTRY; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY; NF-KAPPA B; RATS, WISTAR; TRANSCRIPTION FACTORS; TREATMENT OUTCOME; URSODEOXYCHOLIC ACID;

EID: 84938419786     PISSN: 15918890     EISSN: 15919528     Source Type: Journal    
DOI: 10.1007/s10238-014-0301-x     Document Type: Article

References (34)

1. Pera M. Epidemiology of esophageal cancer, especially adenocarcinoma of the esophagus and esophagogastric junction. Recent Results Cancer Res. 2000;155:1–14.
2. Pohl H, Welch HG. The role of overdiagnosis and reclassification in the marked increase of esophageal adenocarcinoma incidence. J Natl Cancer Inst. 2005;97:142–6.
3. Fujimura T, Oyama K, Sasaki S, Nishijima K, Miyashita T, Ohta T, Miwa K, Hattori T. Inflammation-related carcinogenesis and prevention in esophageal adenocarcinoma using rat duodenoesophageal reflux models. Cancers. 2011;3:3206–24.
4. Jankowski JA, Harrison RF, Perry I, Balkwill F, Tselepis C. Barrett’s metaplasia. Lancet. 2000;356:2079–85.
5. Stein HJ, Feussner H, Kauer W, DeMeester TR, Siewert R. Alkaline gastroesophageal reflux: assessment by ambulatory esophageal aspiration and pH monitoring. Am J Surg. 1994;167:163–8.
6. Gillen P, Keeling P, Byrne PJ, Healy M, O’Moore RR, Hennessy TPJ. Implication of duodenogastric reflux in the pathogenesis of Barrett’s oesophagus. Br J Surg. 1998;75:540–3.
7. Iftikhar SY, Ledingham S, Steele RJC, Evans DF, Lendrum K, Atkinson M, Hardcastle JD. Bile reflux in columnar-lined Barrett’s oesophagus. Ann R Coll Surg Engl. 1993;75:411–6.
8. Lagergren J, Bergström R, Lindgren A, Nyrén O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340:825–31.
9. Nehra D, Howell P, Williams CP, Pye JK, Beynon J. Toxic bile acids in gastro-oesophageal reflux disease: influence of gastric acidity. Gut. 1999;44:598–602.
10. Bozikas A, Marsman WA, Rosmolen WD, van Baal JWPM, Kulik W, ten Kate FJW, Krishnadath KK, Bergman JJGHM. The effect of oral administration of ursodeoxycholic acid and high-dose proton pump inhibitors on the histology of Barrett’s esophagus. Dis Esophagus. 2008;21:346–54.
11. Champion G, Richter JE, Vaezi MF, Singh S, Alexander R. Duodenogastroesophageal reflux: relationship to pH and importance in Barrett’s esophagus. Gastroenterology. 1994;107:747–54.
12. Kazumori H, Ishihara S, Rumi MAK, Kadowaki Y, Kinoshita Y. Bile acids directly augment caudal related homeobox gene Cdx2 expression in oesophageal keratinocytes in Barrett’s epithelium. Gut. 2006;55:16–25.
13. Phillips RW, Frierson HF Jr, Moskaluk CA. Cdx2 as a marker of epithelial intestinal differentiation in the esophagus. Am J Surg Pathol. 2003;27:1442–7.
14. Tamagawa Y, Ishimura N, Uno G, Yuki T, Kazumori H, Ishihara S, Amano Y, Kinoshita Y. Notch signaling pathway and Cdx2 expression in the development of Barrett’s esophagus. Lab Invest. 2012;92:896–909.
15. Moons LMG, Bax DA, Kuipers EJ, van Dekken H, Haringsma J, van Vliet AHM, Siersema PD, Kusters JG. The homeodomain protein CDX2 is an early marker of Barrett’s oesophagus. J Clin Pathol. 2004;57:1063–8.
16. Debruyne PR, Witek M, Gong L, Birbe R, Chervoneva I, Jin T, Domon-cell C, Palazzo JP, Freund J, Li P, Pitari GM, Schulz S, Waldman SA. Bile acids induce ectopic expression of intestinal guanylyl cyclase C through nuclear factor-κB and Cdx2 in human esophageal cells. Gastroenterology. 2006;130:1191–206.
17. Liu T, Zhang X, So C, Wang S, Wang P, Yan L, Myers R, Chen Z, Patterson AP, Yang CS, Chen X. Regulation of Cdx2 expression by promoter methylation, and effects of Cdx2 transfection on morphology and gene expression of human esophageal epithelial cells. Carcinogenesis. 2007;28:488–96.
18. Paumgartner G, Beuers U. Ursodeoxycholic acid in cholestatic liver disease: mechanisms of action and therapeutic use revisited. Hepatology. 2002;36:525–31.
19. Goldman A, Condon A, Adler E, Minnella M, Bernstein C, Bernstein H, Dvorak K. Protective effects of glycoursodeoxycholic acid in Barrett’s esophagus cells. Dis Esophagus. 2010;23:83–93.
20. Thomas C, Pellicciari R, Pruzanski M, Auwerx J, Schoonjans K. Targeting bile-acid signaling for metabolic diseases. Nat Rev Drug Discov. 2008;7:678–93.
21. Earnest DL, Holubec H, Wali RK, Jolley CS, Bissonette M, Bhattacharyya AK, Roy H, Khare S, Brasitus TA. Chemoprevention of azoxymethane-induced colonic carcinogenesis by supplemental dietary ursodeoxycholic acid. Cancer Res. 1994;54:5071–4.
22. Loddenkemper C, Keller S, Hanski M, Cao M, Jahreis G, Stein H, Zeitz M, Hanski C. Prevention of colitis-associated carcinogenesis in a mouse model by diet supplementation with ursodeoxycholic acid. Int J Cancer. 2006;118:2750–7.
23. Alberts DS, Martínez ME, Hess LM, Einspahr JG, Green SB, Bhattacharyya AK, Guillen J, Krutzsch M, Batta AK, Salen G, Fales L, Koonce K, Parish D, Clouser M, Roe D, Lance P. Phase III trial of ursodeoxycholic acid to prevent colorectal adenoma recurrence. J Natl Cancer Inst. 2005;97:846–53.
24. Miwa K, Sahara H, Segawa M, Kinami S, Sato T, Miyazaki I, Hattori T. Reflux of duodenal or gastro-duodenal contents induces esophageal carcinoma in rats. Int J Cancer. 1996;67:269–74.
25. Chen K, Mukaisho K, Sugihara H, Araki Y, Yamamoto G, Hattori T. High animal-fat intake changes the bile-acid composition of bile juice and enhances the development of Barrett’s esophagus and esophageal adenocarcinoma in a rat duodenal-contents reflux model. Cancer Sci. 2007;98:1683–8.
26. Jenkins GJS, Harries K, Doak SH, Wilmes A, Griffiths AP, Baxter JN, Parry JM. The bile acid deoxycholic acid (DCA) at neutral pH, activates NF-κB and induces IL-8 expression in oesophageal cells in vitro. Carcinogenesis. 2004;25:317–23.
27. Oyama K, Fujimura T, Ninomiya I, Miyashita T, Kinami S, Fushida S, Ohta T, Miwa K. A COX-2 inhibitor prevents the esophageal inflammation–metaplasia–adenocarcinoma sequence in rats. Carcinogenesis. 2005;26:565–70.
28. Rost D, Rudolph G, Kloeters-Plachky P, Stiehl A. Effect of high-dose ursodeoxycholic acid on its biliary enrichment in primary sclerosing cholangitis. Hepatology. 2004;40:693–8.
29. Eda A, Osawa H, Satoh K, Yanaka I, Kihira K, Ishino Y, Mutoh H, Sugano K. Aberrant expression of CDX2 in Barrett’s epithelium and inflammatory esophageal mucosa. J Gastroenterol. 2003;38:14–22.
30. Burnat G, Majka J, Konturek PC. Bile acids are multifunctional modulators of the Barrett’s carcinogenesis. J Physiol Pharmacol. 2010;61:185–92.
31. Rayet B, Gélinas C. Aberrant rel/nfκb genes and activity in human cancer. Oncogene. 1999;18:6938–47.
32. O’Riordan JM, Abdel-Latif MM, Ravi N, McNamara D, Byrne PJ, McDonald GS, Keeling PW, Kelleher D, Reynolds JV. Proinflammatory cytokine and nuclear factor kappa-B expression along the inflammation–metaplasia–dysplasia–adenocarcinoma sequence in the esophagus. Am J Gastroenterol. 2005;100:1257–64.
33. Cronin J, Williams L, McAdam E, Eltahir Z, Griffiths P, Baxter J, Jenkins G. The role of secondary bile acids in neoplastic development in the esophagus. Biochem Soc Trans. 2010;38:337–42.
34. Miura T, Ouchida R, Yoshikawa N, Okamoto K, Makino Y, Nakamura T, Morimoto C, Makino I, Tanaka H. Functional modulation of the glucocorticoid receptor and suppression of NF-κB-dependent transcription by ursodeoxycholic acid. J Biol Chem. 2001;276:47371–8.