Deoxycholic acid at neutral and acid pH, is genotoxic to oesophageal cells through the induction of ROS: The potential role of anti-oxidants in Barrett's oesophagus

Carcinogenesis

Volumn 28, Issue 1, 2007, Pages 136-142

  Jenkins, Gareth J S ^a   D'Souza, Francis R ^a   Suzen, Sinan H ^b   Eltahir, Zak S ^a   James, Sally A ^a   Parry, James M ^a   Griffiths, Paul A ^a   Baxter, John N ^a  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b ANKARA UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; DEOXYCHOLIC ACID; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

ACIDITY; ARTICLE; BARRETT ESOPHAGUS; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CELL DEATH; CELL SURVIVAL; CHROMOSOME DAMAGE; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; ESOPHAGEAL ADENOCARCINOMA; GENE MUTATION; GENETIC CODE; GENOTOXICITY; HUMAN; HUMAN CELL; MICRONUCLEUS; PH MEASUREMENT; PRIORITY JOURNAL; SURVIVAL RATE;

ADENOCARCINOMA; ANTIOXIDANTS; ASCORBIC ACID; BARRETT ESOPHAGUS; CARCINOMA, SQUAMOUS CELL; CELL SURVIVAL; DEOXYCHOLIC ACID; DETERGENTS; DNA DAMAGE; ESOPHAGEAL NEOPLASMS; HUMANS; HYDROGEN-ION CONCENTRATION; MICRONUCLEUS TESTS; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33845622957     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl147     Document Type: Article

References (48)

1. Cook,J.W., Kennaway,E.L. and Kennaway,N.M. (1940) Production of tumours in mice by deoxycholic acid. Nature, 145, 627.
2. Aries,V., Crowther,J.S., Drasar,B.S., Hill,M.J. and Williams,R.E.O. (1969) Bacteria and the aetiology of the large bowel. Gut, 10, 334-335.
3. Stein,H.J., Kauer,W.K.D., Feussner,H. and Siewert,J.R. (1998) Bile reflux in benign and malignant Barrett's esophagus: Effect of medical acid suppression and Nissen fundoplication. J Gastrointestinal Surg., 2, 333-341.
4. Jankowski,J.A., Wright,N.A., Meltzer,S.J., Triadafilopoulos,G., Geboes,K., Casson,A.G., Kerr,D. and Young,L.S. (1999) Molecular evolution of the metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am J Pathology, 154, 965-973.
5. Jankowski,J.A., Harrison,R.F., Perry,I., Balkwill,F. and Tselepis,C. (2000) Barrett's metaplasia. Lancet, 356, 2079-2085.
6. Triadafilopoulos,G. (2000) Proton pump inhibitors for Barrett's oesophagus. Gut, 46, 144-146.
7. Nehra,D., Howell,P., Williams,C.P., Pye,J.K. and Beynon,J. (1999) Toxic bile acids in gastro-oesophageal reflux disease: Influence of gastric acidity. Gut, 44, 598-602.
8. Billington,D., Evans,C.E., Godfrey,P.P. and Coleman,R. (1980) Effects of bile salts on the plasma membranes of isolated rat hepatocytes. Biochem. J., 188, 321-327.
9. Gores,G.J., Miyoshi,H., Botla,R., Aguilar,H.I. and Bronk,S.F. (1998) Induction of the mitochondrial permeability transition as a mechanism of liver injury during cholestasis: A role for mitochondrial proteases. Biochem. Biophys. Acta, 1366, 167-175.
10. Palmeira,C.M. and Rolo,A.P. (2004) Mitochondrially-mediated toxicity of bile acids. Toxicology, 203, 1-15.
11. Vaezi,M.F. and Richter,J.E. (2000) Duodenogastro-oesophageal reflux. Best Prac. Res. Clin. Gastroenterol., 14, 719-729.
12. Nagengast,F.M., Grubben,M.J.A.L. and Vanmunster,I.P. (1995) Role of bile-acids in colorectal carcinogenesis. Eur. J. Cancer, 31A, 1067-1070.
13. LaRue,J.M., Stratagoules,E.D. and Martinez,J.D. (2000) Deoxycholic acid-induced apoptosis is switched to necrosis by bcl-2 and calphostin C. Cancer Lett., 152, 107-113.
14. Tselepis,C., Morris,C.D., Wakelin,D., Hardy,R., Perry,I., Luong,Q.T., Harper,E., Harrison,R., Attwood,S.E.A. and Jankowski,J.A.Z. (2003) Upregulation of the oncogene c-myc in Barretts adenocarcinoma: Induction of c-myc by acidified bile in vitro. Gut, 52, 174-180.
15. Zhang,F., Subbaramaiah,K., Altorki,N. and Dannenberg,A.J. (1998) Dihydroxy bile acids activate the transcription of cyclooxygenase-2. J. Biol. Chem., 273, 2424-2428.
16. Jenkins,G.J.S., Harries,K., Doak,S.H., Wilmes,A., Griffiths,A.P., Baxter,J.N. and Parry,J.M. (2004) The bile acid deoxycholic acid at neutral pH activates NFKB and causes upregulation of IL-8. Carcinogenesis, 25, 317-323.
17. Theisen,J., Peters,J.H. and Stein,H.J. (2003) Experimental evidence for mutagenic potential of duodenogastric juice on Barrett's oesophagus. World J. Surg., 27, 1018-1020.
18. Scates,D.K., Venitt,S., Phillips,R.K.S. and Spigelman,A.D. (1995) High pH reduces DNA damage caused by bile from patients with familial adenomatous polyposis-antacids may attenuate duodenal polyposis. Gut, 36, 918-921.
19. Scates,D.K., Spigelman,A.D., Phillips,R.K.S. and Venitt,S. (1996) Differences in the levels and pattern of DNA adduct labelling in human cell lines MCL5 and CCRF, proficient in carcinogen metabolism, treated in vitro with bile from familial adenomatous polyposis patients and from unaffected controls. Carcinogenesis, 17, 707-713.
20. Fimognari,C., Nusse,M., Cesari,R., Cantelli-Forti,G. and Hrelia,P. (2001) Micronuclei induction, cell cycle delay and apoptosis as markers of cellular stress caused by ursodeoxycholic acid in human lymphocytes. Mutat. Res., 495, 1-9.
21. Kandell,R.L. and Bernstein,C. (1991) Bile salt/acid induction of DNA damage in bacterial and mammalian cells: Implications for colorectal cancer. Nutr. Cancer, 16, 227-238.
22. Booth,L.A., Gilmore,I.T. and Bilton,R.F. (1997) Secondary bile acid induced DNA damage in HT29 cells: Are free radicals involved? Free Radic. Res., 26, 135-144.
23. Jolly,A.J., Wild,C.P. and Hardie,L.J. (2004) Acid and bile salts induce DNA damage in human oesophageal cell lines. Mutagenesis, 19, 319-324.
24. Silverman,S.J. and Andrews,A.W. (1977) Bile acids: Co-mutagenic activity in the Salmonella-mammalian-microsome mutagenicity test. J. Natl. Cancer Inst., 59, 1557-1559.
25. Venitt,S., Bosworth,D. and Easton,D.F. (1987) Lack of mutagenic activity of bile acids in bacterial fluctuation test. Mutat. Res., 190, 191-196.
26. Mori,Y., Nii,H., Masuda,A., Mizumoto,K., Konishi,Y., Une,M. and Hoshita,T. (1991) Absence of mutagenic action of 5-beta-cholan-24-oic acid derivatives in the bacterial fluctuation and standard ames tests. Mutat. Res., 262, 267-274.
27. Fein,M., Fuchs,K.H., Stopper,H., Diem,S. and Herderich,M. (2000) Duodenogastric reflux and foregut carcinogenesis: Analysis of duodenal juice in a rodent model of cancer. Carcinogenesis, 21, 2079-2083.
28. Venturi,M., Hambly,R.J., Glinghammar,B., Rafter,J.J. and Rowland,I.R. (1997) Genotoxic activity in human faecal water and the role of bile acids; a study using the alkaline comet assay. Carcinogenesis, 18, 2353-2359.
29. Debruyne,P.R., Bruyneel,E.A., Li,X.D., Zimber,A., Gespach,C. and Mareel,M.M. (2001) The role of bile acids in carcinogenesis. Mutat. Res., 480, 359-369.
30. Patel,T. and Gores,G.J. (1997) Inhibition of bile salt induced hepatocyte apoptosis by the antioxidant lazaroid U83836E. Toxicol. Appl. Pharmacol., 142, 116-122.
31. Fang,Y.W., Han,S.I., Mitchell,C., Gupta,S., Studer,E., Grant,S., Hylemon,P.B. and Dent,P. (2004) Bile acids induce mitochondrial ROS, which promote activation of receptor tyrosine kinases and signaling pathways in rat hepatocytes. Hepatology, 40, 961-971.
32. Scates,D.K., Spigelman,A.D. and Venitt,S. (1994) Bile acids do not form adducts when incubated with DNA in vitro. Carcinogenesis, 15, 2945-2948.
33. Glinghammar,B., Inoue,H. and Rafter,J.J. (2002) Deoxycholic acid causes DNA damage in colonic cells with subsequent induction of caspases, COX-2 promoter activity and the transcription factors NF-kB and AP-1. Carcinogenesis, 23, 839-845.
34. Wetscher,G.J., Ronald,R.A., Bagchi,D., Hinder,P.R., Bagchi,M., Perdikis,G. and McGinn,T. (1995) Reflux esophagitis in humans is mediated by oxygen derived free radicals. Am. J. Surg., 170, 552-556.
35. Jenkins,G.J.S., Doak,S.H., Griffiths,A.P., Baxter,J.N. and Parry,J.M. (2003) Early p53 mutations in non-dysplastic Barrett's tissues detected by the restriction site mutation (RSM) methodology. Br. J. Cancer, 88, 1271-1276.
36. Fenech,M. and Morley,A.A. (1986) Cytokinesis-block micronucleus method in human-lymphocytes - effect of in vivo aging and low-dose X-irradiation. Mutat. Res., 161, 193-198.
37. LeBel,C.P., Ischiropoulos,H. and Bondy,S.C. (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol., 5, 227-231.
38. Ellard,S., Mohammed,Y., Dogra,S., Wolfel,C., Doehmer,J. and Parry,J.M. (1991) The use of genetically engineered V79 Chinese-hamster cultures expressing rat-liver cyp1a1, 1a2 and 2b1 CDNAs in micronucleus assays. Mutagenesis, 6, 461-470.
39. Fenech,M., Crott,J., Turner,J. and Brown,S. (1999) Necrosis, apoptosis, cytostasis and DNA damage in human lymphocytes measured simultaneously within the cytokinesis-block micronucleus assay: Description of the method and results for hydrogen peroxide. Mutagenesis, 14, 605-612.
40. Jenkins,G.J.S. (2004) Restriction site mutation: Clinical applications. Mutagenesis, 19, 3-11.
41. Kirkland,D. and Müller,L. (2000) Interpretation of the biological relevance of genotoxicity test results: The importance of thresholds. Mutation Res., 464, 137-147.
42. Liu,L., Erguin,G., Ertan,A., Woods,K., Sachs,I. and Younes,M. (2003) Detection of oxidative DNA damage in oesophageal biopsies of patients with reflux symptoms and normal pH monitoring. Aliment. Pharmacol. Ther., 18, 693-698.
43. Washo-Stultz,D., Crowley-Weber,C.L., Dvorakova,K., Bernstein,C., Bernstein,H., Kunke,K., Waltmire,C.N., Garewal,H. and Payne,C.M. (2002) Role of mitochondrial complexes I and II, reactive oxygen species and arachidonic acid metabolism in deoxycholate induced apaoptosis. Cancer Lett., 177, 129-144.
44. Dvorakova,K., Payne,C.M., Ramsey,L. et al. (2005) Apoptosis resistance in Barrett's esophgus: Ex vivo bioassay of live stressed tissues. Am. J. Gastro., 100, 424-431.
45. Halliwell,B. (2001) Vitamin C and genomic stability. Mutat. Res., 475, 29-35.
46. Tzonou,A., Lipworth,L., Garidou,A., Signorello,L.B., Lagiou,P., Hsieh,C. and Trichopoulos,D. (1996) Diet and risk of esophageal cancer by histologic type in a low-risk population. Int. J. Cancer, 68, 300-304.
47. Terry,P., Lagergren,J., Ye,W., Nyren,O. and Wolk,A. (2000) Antioxidants and cancers of the esophagus and gastric cardia. Int. J. Cancer, 87, 750-754.
48. Jorosz,M., Dzieniszewski,J., Dabrowska-Ufniarz,E., Wartanowicz,M., Ziemlanski,S. and Reed,P.I. (1998) Effects of high dose vitamin C treatment on Helicobacter pylori infection and total vitamin C concentration in gastric juice. Eur. J. Cancer Prev., 7, 449-454.