Deoxycholic acid causes DNA damage while inducing apoptotic resistance through NF-κ{green}b activation in benign barrett's epithelial cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 2, 2011, Pages

  Huo, Xiaofang ^a   Juergens, Stefanie ^d   Zhang, Xi ^a   Rezaei, Davood ^a   Yu, Chunhua ^a   Strauch, Eric D ^e   Wang, Jian Ying ^e,f,g   Cheng, Edaire ^b   Meyer, Frank ^d   Wang, David H ^a,c   Zhang, Qiuyang ^a   Spechler, Stuart J ^a   Souza, Rhonda F ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e Cell Biology Group   (United States)

^f UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^g BALTIMORE VA MEDICAL CENTER   (United States)

Author keywords

Barrett's esophagus; Bile salts; Gastroesophageal reflux

Indexed keywords

3 (4 TERT BUTYLPHENYLSULFONYL) 2 PROPENENITRILE; ACETYLCYSTEINE; DEOXYCHOLIC ACID; HISTONE H2AX; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITROGEN; REACTIVE OXYGEN METABOLITE; SYNAPTOTAGMIN I; URSODEOXYCHOLIC ACID;

APOPTOSIS; ARTICLE; BARRETT ESOPHAGUS; CONTROLLED STUDY; DISEASE MARKER; DNA DAMAGE; ENDOSCOPY; EPITHELIUM CELL; ESOPHAGOSCOPY; GENOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

AGED; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BARRETT ESOPHAGUS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; DEOXYCHOLIC ACID; DNA DAMAGE; EPITHELIAL CELLS; HISTONES; HUMANS; I-KAPPA B PROTEINS; MALE; MIDDLE AGED; NF-KAPPA B; RATS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; URSODEOXYCHOLIC ACID;

EID: 79960977948     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00092.2011     Document Type: Article

References (38)

1. Abdel-latif MM, O'Riordan J, Windle HJ, Carton E, Ravi N, Kelleher D, Reynolds JV. NF-κAPPA;{green}B activation in esophageal adenocarcinoma: relationship to Barrett's metaplasia, survival, and response to neoadjuvant chemoradiotherapy. Ann Surg 239: 491-500, 2004.
2. Albino AP, Huang X, Jorgensen E, Yang J, Gietl D, Traganos F, Darzynkiewicz Z. Induction of H2AX phosphorylation in pulmonary cells by tobacco smoke: a new assay for carcinogens. Cell Cycle 3: 1062-1068, 2004.
3. Bernstein C, Payne CM, Bernstein H, Garewal H. Activation of the metallothionein IIA promoter and other key stress response elements by ursodeoxycholate in HepG2 cells: relevance to the cytoprotective function of ursodeoxycholate. Pharmacology 65: 2-9, 2002.
4. Boeckxstaens GE, Smout A. Systematic review: role of acid, weakly acidic and weakly alkaline reflux in gastro-oesophageal reflux disease. Aliment Pharmacol Ther 32: 334-343, 2010.
5. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, Pommier Y.γ-H2AX and cancer. Nat Rev Cancer 8: 957-967, 2008.
6. Buttar NS, Wang KK, Leontovich O, Westcott JY, Pacifico RJ, Anderson MA, Krishnadath KK, Lutzke LS, Burgart LJ. Chemoprevention of esophageal adenocarcinoma by COX-2 inhibitors in an animal model of Barrett's esophagus. Gastroenterology 122: 1101-1112, 2002.
7. Darragh J, Hunter M, Pohler E, Nelson L, Dillon JF, Nenutil R, Vojtesek B, Ross PE, Kernohan N, Hupp TR. The calcium-binding domain of the stress protein SEP53 is required for survival in response to deoxycholic acid-mediated injury. FEBS J 273: 1930-1947, 2006.
8. Dvorak K, Payne CM, Chavarria M, Ramsey L, Dvorakova B, Bernstein H, Holubec H, Sampliner RE, Guy N, Condon A, Bernstein C, Green SB, Prasad A, Garewal HS. Bile acids in combination with low pH induce oxidative stress and oxidative DNA damage: relevance to the pathogenesis of Barrett's oesophagus. Gut 56: 763-771, 2007.
9. Dvorakova K, Payne CM, Ramsey L, Bernstein H, Holubec H, Chavarria M, Bernstein C, Sampliner RE, Riley C, Prasad A, Garewal H. Apoptosis resistance in Barrett's esophagus: ex vivo bioassay of live stressed tissues. Am J Gastroenterol 100: 424-431, 2005.
10. Fein M, Peters JH, Chandrasoma P, Ireland AP, Oberg S, Ritter MP, Bremner CG, Hagen JA, DeMeester TR. Duodenoesophageal reflux induces esophageal adenocarcinoma without exogenous carcinogen. J Gastrointest Surg 2: 260-268, 1998.
11. 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 23: 83-93, 2010.
12. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 100: 57-70, 2000.
13. Hormi-Carver K, Zhang X, Zhang HY, Whitehead RH, Terada LS, Spechler SJ, Souza RF. Unlike esophageal squamous cells, Barrett's epithelial cells resist apoptosis by activating the nuclear factor-K{green}B pathway. Cancer Res 69: 672-677, 2009.
14. Huo X, Zhang HY, Zhang XI, Lynch JP, Strauch ED, Wang JY, Melton SD, Genta RM, Wang DH, Spechler SJ, Souza RF. Acid and bile salt-induced CDX2 expression differs in esophageal squamous cells from patients with and without Barrett's esophagus. Gastroenterology 139: 194-203, 2010.
15. Jaiswal KR, Morales CP, Feagins LA, Gandia KG, Zhang X, Zhang HY, Hormi-Carver K, Shen Y, Elder F, Ramirez RD, Sarosi GA Jr, Spechler SJ, Souza RF. Characterization of telomerase-immortalized, non-neoplastic, human Barrett's cell line (BAR-T). Dis Esophagus 20: 256-264, 2007.
16. Jenkins GJ, Cronin J, Alhamdani A, Rawat N, D'Souza F, Thomas T, Eltahir Z, Griffiths AP, Baxter JN. The bile acid deoxycholic acid has a non-linear dose response for DNA damage and possibly NF-κ{green}B activation in oesophageal cells, with a mechanism of action involving ROS. Mutagenesis 23: 399-405, 2008.
17. Jenkins GJ, D'Souza FR, Suzen SH, Eltahir ZS, James SA, Parry JM, Griffiths PA, Baxter JN. 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 28: 136-142, 2007.
18. Jenkins GJ, Harries K, Doak SH, Wilmes A, Griffiths AP, Baxter JN, Parry JM. The bile acid deoxycholic acid (DCA) at neutral pH activates NF-κ{green}B and induces IL-8 expression in oesophageal cells in vitro. Carcinogenesis 25: 317-323, 2004.
19. Jolly AJ, Wild CP, Hardie LJ. Sodium deoxycholate causes nitric oxide mediated DNA damage in oesophageal cells. Free Radic Res 43: 234-240, 2009.
20. Kauer WK, Peters JH, DeMeester TR, Feussner H, Ireland AP, Stein HJ, Siewert RJ. Composition and concentration of bile acid reflux into the esophagus of patients with gastroesophageal reflux disease. Surgery 122: 874-881, 1997.
21. Kowdley KV. Ursodeoxycholic acid therapy in hepatobiliary disease. Am J Med 108: 481-486, 2000.
22. Mills KD, Ferguson DO, Alt FW. The role of DNA breaks in genomic instability and tumorigenesis. Immunol Rev 194: 77-95, 2003.
23. Nehra D, Howell P, Williams CP, Pye JK, Beynon J. Toxic bile acids in gastro-oesophageal reflux disease: influence of gastric acidity. Gut 44: 598-602, 1999.
24. 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 _B expression along the inflammationmetaplasia- dysplasia-adenocarcinoma sequence in the esophagus. Am J Gastroenterol 100: 1257-1264, 2005.
25. Pohl H, Welch HG. The role of overdiagnosis and reclassification in the marked increase of esophageal adenocarcinoma incidence. J Natl Cancer Inst 97: 142-146, 2005.
26. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, Wright WE. Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 15: 398-403, 2001.
27. Richter JE, Bradley LA, DeMeester TR, Wu WC. Normal 24-hr ambulatory esophageal pH values. Influence of study center, pH electrode, age, and gender. Dig Dis Sci 37: 849-856, 1992.
28. Sarosi G, Brown G, Jaiswal K, Feagins LA, Lee E, Crook TW, Souza RF, Zou YS, Shay JW, Spechler SJ. Bone marrow progenitor cells contribute to esophageal regeneration and metaplasia in a rat model of Barrett's esophagus. Dis Esophagus 21: 43-50, 2008.
29. Sital RR, Kusters JG, De Rooij FW, Kuipers EJ, Siersema PD. Bile acids and Barrett's oesophagus: a sine qua non or coincidence? Scand J Gastroenterol Suppl 11-17, 2006.
30. Souza RF, Shewmake KL, Shen Y, Ramirez RD, Bullock JS, Hladik CL, Lee EL, Terada LS, Spechler SJ. Differences in ERK activation in squamous mucosa in patients who have gastroesophageal reflux disease with and without Barrett's esophagus. Am J Gastroenterol 100: 551-559, 2005.
31. Spechler SJ, Fitzgerald RC, Prasad GA, Wang KK. History, molecular mechanisms, and endoscopic treatment of Barrett's esophagus. Gastroenterology 138: 854-869, 2010.
32. Theisen J, Nehra D, Citron D, Johansson J, Hagen JA, Crookes PF, DeMeester SR, Bremner CG, DeMeester TR, Peters JH. Suppression of gastric acid secretion in patients with gastroesophageal reflux disease results in gastric bacterial overgrowth and deconjugation of bile acids. J Gastrointest Surg 4: 50-54, 2000.
33. Toledo A, Yamaguchi J, Wang JY, Bass BL, Turner DJ, Strauch ED. Taurodeoxycholate stimulates intestinal cell proliferation and protects against apoptotic cell death through activation of NF-κ{green}B. Dig Dis Sci 49: 1664-1671, 2004.
34. Tung BY, Emond MJ, Haggitt RC, Bronner MP, Kimmey MB, Kowdley KV, Brentnall TA. Ursodiol use is associated with lower prevalence of colonic neoplasia in patients with ulcerative colitis and primary sclerosing cholangitis. Ann Intern Med 134: 89-95, 2001.
35. Vaezi MF, Richter JE. Role of acid and duodenogastroesophageal reflux in gastroesophageal reflux disease. Gastroenterology 111: 1192-1199, 1996.
36. Zhang HY, Hormi-Carver K, Zhang X, Spechler SJ, Souza RF. In benign Barrett's epithelial cells, acid exposure generates reactive oxygen species that cause DNA double-strand breaks. Cancer Res 69: 9083-9089, 2009.
37. Zhang HY, Zhang X, Hormi-Carver K, Feagins LA, Spechler SJ, Souza RF. In non-neoplastic Barrett's epithelial cells, acid exerts early antiproliferative effects through activation of the Chk2 pathway. Cancer Res 67: 8580-8587, 2007.
38. Zhang X, Yu C, Wilson K, Zhang H, Melton SD, Huo X, Wang DH, Genta RM, Spechler SJ, Souza RF. Malignant transformation of nonneoplastic Barrett's epithelial cells through well-defined genetic manipulations. PLoS One 5: e13093, 2010.