Activation of the interleukin-6/STAT3 antiapoptotic pathway in esophageal cells by bile acids and low pH: Relevance to Barrett's esophagus

Clinical Cancer Research

Volumn 13, Issue 18, 2007, Pages 5305-5313

  Dvorak, Katerina ^a,b,c,d   Chavarria, Melissa ^a   Payne, Claire M ^a,b,c   Ramsey, Lois ^c   Crowley Weber, Cara ^a   Dvorakova, Barbora ^a   Dvorak, Bohuslav ^a   Bernstein, Harris ^a,b   Holubec, Hana ^a   Sampliner, Richard E ^b,c   Bernstein, Carol ^a,c   Prasad, Anil ^b,c   Green, Sylvan B ^b   Garewal, Harinder ^b,c  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c SOUTHERN ARIZONA VA HEALTH CARE SYSTEM   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; PROTEIN BCL XL; PROTEIN MCL 1; STAT3 PROTEIN;

ADULT; AGED; APOPTOSIS; ARTICLE; BARRETT ESOPHAGUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DYSPLASIA; ESOPHAGEAL ADENOCARCINOMA; FEMALE; GASTROESOPHAGEAL REFLUX; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; MAJOR CLINICAL STUDY; MALE; MOLECULAR BIOLOGY; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; BARRETT ESOPHAGUS; BCL-X PROTEIN; BILE ACIDS AND SALTS; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; FEMALE; GASTRIC ACID; HUMANS; HYDROGEN-ION CONCENTRATION; INTERLEUKIN-6; MALE; MIDDLE AGED; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED;

EID: 34848856813     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-07-0483     Document Type: Article

References (50)

1. Drewitz DJ, Sampliner RE, Garewal HS. The incidence of adenocarcinoma in Barrett's esophagus: a prospective study of 170 patients followed 4.8 years. Am J Gastroenterol 1997;92:212-5.
2. Falk GW. Barrett's esophagus. Gastroenterology 2002;122:1569-91.
3. Devesa SS, Blot WJ, Fraumeni JF, Jr. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer 1998;83:2049-53.
4. DeMeester TR. Management of adenocarcinoma arising in Barrett's esophagus. Semin Thorac Cardiovasc Surg 1997;9:290-301.
5. Richter JE. Importance of bile reflux in Barrett's esophagus. Dig Dis 2000;18:208-16.
6. Vaezi MF, Richter JE. Role of acid and duodenogastroesophageal reflux in gastroesophageal reflux disease. Gastroenterology1996;111:1192-9.
7. Iftikhar SY, Ledingham S, Steele RJ, et al. Bile reflux in columnar-lined Barrett's oesophagus. Ann R Coll Surg Engl 1993;75:411-6.
8. 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.
9. Seto Y, Kobori O. Role of reflux oesophagitis and acid in the development of columnar epithelium in the rat oesophagus. Br J Surg 1993;80:467-70.
10. Bernstein H, Payne CM, Bernstein C, Schneider J, Beard SE, Crowley CL. Activation of the promoters of genes associated with DNA damage, oxidative stress, ER stress and protein malfolding by the bile salt, deoxycholate. Toxicol Lett 1999;108:37-46.
11. Sokol RJ, Winklhofer-Roob BM, Devereaux MW, McKim JM, Jr. Generation of hydroperoxides in isolated rat hepatocytes and hepaticmitochondria exposed to hydrophobic bile acids. Gastroenterology 1995;109:1249-56.
12. Venturi M, Hambly RJ, Glinghammar B, Rafter JJ, Rowland IR. Genotoxic activity in human faecal water and the role of bile acids: a study using the alkaline comet assay. Carcinogenesis 1997;18:2353-9.
13. Washo-Stultz D, Crowley-Weber CL, Dvorakova K, et al. Role of mitochondrial complexes I and II, reactive oxygen species and arachidonic acid metabolism in deoxycholate-induced apoptosis. Cancer Lett 2002;177:129-44.
14. Payne CM, Weber C, Crowley-Skillicorn C, et al. Deoxycholate induces mitochondrial oxidative stress and activates NF-κB through multiple mechanisms in HCT-116 colon epithelial cells. Carcinogenesis 2007;28:215-22.
15. Bernstein H, Bernstein C, Payne CM, Dvorakova K, Garewal H. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 2005;589:47-65.
16. Shirvani VN, Ouatu-Lascar R, Kaur BS, Omary MB, Triadafilopoulos G. Cyclooxygenase 2 expression in Barrett's esophagus and adenocarcinoma: Ex vivo induction by bile salts and acid exposure. Gastroenterology 2000;118:487-96.
17. Kaur BS, Triadafilopoulos G. Acid- and bile-induced PGE(2) release and hyperproliferation in Barrett's esophagus are COX-2 and PKC-epsilon dependent. Am J Physiol Gastrointest Liver Physiol 2002;283:G327-34.
18. Souza RF, Shewmake K, Terada LS, Spechler SJ. Acid exposure activates themitogen-activated protein kinase pathways in Barrett's esophagus. Gastroenterology 2002;122:299-307.
19. Abdel-Latif MM, O'Riordan J, Windle HJ, et al. NF-κB activation in esophageal adenocarcinoma: relationship to Barrett's metaplasia, survival, and response to neoadjuvant chemoradiotherapy. Ann Surg 2004;239:491-500.
20. Qiao L, Studer E, Leach K, et al. Deoxycholic acid (DCA) causes ligand-independent activation of epidermal growth factor receptor (EGFR) and FAS receptor in primary hepatocytes: inhibition of EGFR/mitogen-activated protein kinase-signaling module enhances DCA-induced apoptosis. Mol Biol Cell 2001;12:2629-45.
21. Dvorakova K, Payne CM, Ramsey L, et al. Apoptosis resistance in Barrett's esophagus: ex vivo bioassay of live stressed tissues. Am J Gastroenterol 2005;100:424-31.
22. Dvorakova K, Payne CM, Ramsey L, et al. Increased expression and secretion of interleukin-6 in patients with Barrett's esophagus. Clin Cancer Res 2004;10:2020-8.
23. Kauer WK, Peters JH, DeMeester TR, et al. Composition and concentration of bile acid reflux into the esophagus of patients with gastroesophageal reflux disease. Surgery 1997;122:874-81.
24. Theisen J, Nehra D, Citron D, et al. Suppression of gastric acid secretion in patients with gastroesophageal reflux disease results in gastric bacterial overgrowth and deconjugation of bile acids. J Gastrointest Surg 2000;4:50-4.
25. Garewal H, Ramsey L, Sharma P, Kraus K, Sampliner R, Fass R. Biomarker studies in reversed Barrett's esophagus. Am J Gastroenterol 1999;94:2829-33.
26. Dvorakova K, Waltmire CN, Payne CM, Tome ME, Briehl MM, Dorr RT. Induction of mitochondrial changes in myeloma cells by imexon. Blood 2001;97:3544-51.
27. Halpern MD, Holubec H, Dominguez JA, et al. Upregulation of IL-18 and IL-12 in the ileum of neonatal rats with necrotizing enterocolitis. Pediatr Res 2002;51:733-9.
28. Crowley-Weber CL, Dvorakova K, Crowley C, et al. Nicotine increases oxidative stress, activates NF-κB and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem Biol Interact 2003;145:53-66.
29. Payne CM, Bernstein H, Bernstein C, Garewal H. Role of apoptosis in biology and pathology: resistance to apoptosis in colon carcinogenesis. Ultrastruct Pathol 1995;19:221-48.
30. Hirano T. Interleukin 6 and its receptor: ten years later. Int Rev Immunol 1998;16:249-84.
31. Grad JM, Zeng XR, Boise LH. Regulation of Bcl-xL: a little bit of this and a little bit of STAT. Curr Opin Oncol 2000;12:543-9.
32. Lauta VM. Interleukin-6 and the network of several cytokines in multiple myeloma: an overview of clinical and experimental data. Cytokine 2001;16:79-86.
33. Hobisch A, Rogatsch H, Hittmair A, et al. Immunohistochemical localization of interleukin-6 and its receptor in benign, premalignant and malignant prostate tissue. J Pathol 2000;191:239-44.
34. Basolo F, Fiore L, Fontanini G, et al. Expression of and response to interleukin 6 (IL6) in human mammary tumors. Cancer Res 1996;56:3118-22.
35. Hoheisel G, Izbicki G, Roth M, et al. Proinflammatory cytokine levels in patients with lung cancer and carcinomatous pleurisy. Respiration 1998;65:183-6.
36. Konig B, Steinbach F, Janocha B, et al. The differential expression of proinflammatory cytokines IL-6, IL-8 and TNF-α in renal cell carcinoma. Anticancer Res 1999;19:1519-24.
37. Watson JM, Sensintaffar JL, Berek JS, Martinez-Maza O. Constitutive production of interleukin 6 by ovarian cancer cell lines and by primary ovarian tumor cultures. Cancer Res 1990;50:6959-65.
38. Kirnbauer R, Kock A, Schwarz T, et al. IFN-α 2, B cell differentiation factor 2, or hybridoma growth factor (IL-6) is expressed and released by human epidermal cells and epidermoid carcinoma cell lines. J Immunol 1989;142:1922-8.
39. Dvorak K, Payne CM, Chavarria M, et al. Bile acids in combination with low pH induce oxidative stress and oxidative DNA damage: Relevance to the pathogenesis of Barrett's Oesophagus. Gut 2007;56:763-71.
40. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 1996;271:736-41.
41. Epling-Burnette PK, Zhong B, Bai F, et al. Cooperative regulation of Mcl-1 by Janus kinase/stat and phosphatidylinositol 3-kinase contribute to granulocyte-macrophage colony-stimulating factor-delayed apoptosis in human neutrophils. J Immunol 2001;166:7486-95.
42. Puthier D, Bataille R, Amiot M. IL-6 up-regulates mcl-1 in human myeloma cells through JAK/STAT rather than ras/MAP kinase pathway. Eur J Immunol 1999;29:3945-50.
43. Baud V, Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 2001;11:372-7.
44. Catlett-Falcone R, Landowski TH, Oshiro MM, et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999;10:105-15.
45. Taga T, Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 1997;15:797-819.
46. Niu G, Wright KL, Huang M, et al. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 2002;21:2000-8.
47. Shaheen N, Ransohoff DF. Gastroesophageal reflux, Barrett esophagus, and esophageal cancer: clinical applications. JAMA 2002;287:1982-6.
48. Verselis SJ, Olson KA, Fett JW. Regulation of angiogenin expression in human HepG2 hepatoma cells by mediators of the acute-phase response. Biochem Biophys Res Commun 1999;259:178-84.
49. Kovalovich K, Li W, DeAngelis R, Greenbaum LE, Ciliberto G, Taub R. Interleukin-6 protects against Fas-mediated death by establishing a critical level of anti-apoptotic hepatic proteins FLIP, Bcl-2, and Bcl-xL. J Biol Chem 2001;276:26605-13.
50. Buettner R, Mora LB, Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin Cancer Res 2002;8:945-54.