Characterization of squamous esophageal cells resistant to bile acids at acidic pH: Implication for Barrett's esophagus pathogenesis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 2, 2011, Pages

  Goldman, Aaron ^a,c   Chen, Hwu Dau Rw ^a   Roesly, Heather B ^a   Hill, Kimberly A ^a   Tome, Margaret E ^b   Dvorak, Bohuslav ^b   Bernstein, Harris ^a   Dvorak, Katerina ^a,c  

^a UNIVERSITY OF ARIZONA   (United States)

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

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Cytokeratin 8 18; Esophageal adenocarcinoma; Reactive oxygen species

Indexed keywords

BILE ACID; CYCLOOXYGENASE 2; CYTOKERATIN 18; CYTOKERATIN 8; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN MCL 1; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; TRANSCRIPTION FACTOR CDX2; VILLIN;

ACIDIFICATION; ARTICLE; BARRETT ESOPHAGUS; CARCINOGENESIS; CELL DEATH; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SQUAMOUS CELL; STOMACH ACID;

ACIDS; ADENOCARCINOMA; BARRETT ESOPHAGUS; BILE ACIDS AND SALTS; BIOLOGICAL MARKERS; CELL LINE, TRANSFORMED; DOWN-REGULATION; DRUG RESISTANCE; EPITHELIUM; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; HUMANS; HYDROGEN-ION CONCENTRATION; INTERLEUKIN-6; METAPLASIA; NF-KAPPA B; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPEROXIDE DISMUTASE; UP-REGULATION;

EID: 79251535597     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00461.2010     Document Type: Article

References (66)

1. Abdel-Latif MM, Kelleher D, Reynolds JV. Potential role of NF-κB in esophageal adenocarcinoma: as an emerging molecular target. J Surg Res 153: 172-180, 2009.
2. Abdel-Latif MM, O'Riordan J, Windle HJ, Carton E, Ravi N, Kelleher D, Reynolds JV. NF-κB activation in esophageal adenocarcinoma: relationship to Barrett's metaplasia, survival, and response to neoadjuvant chemoradiotherapy. Ann Surg 239: 491-500, 2004. (Pubitemid 38372765)
3. Abdel-Latif MM, O'Riordan JM, Ravi N, Kelleher D, Reynolds JV. Activated nuclear factor-κB and cytokine profiles in the esophagus parallel tumor regression following neoadjuvant chemoradiotherapy. Dis Esophagus 18: 246-252, 2005. (Pubitemid 43904793)
4. Angelo LS, Talpaz M, Kurzrock R. Autocrine interleukin-6 production in renal cell carcinoma: evidence for the involvement of p53. Cancer Res 62: 932-940, 2002. (Pubitemid 34126975)
5. Avissar NE, Toia L, Hu Y, Watson TJ, Jones C, Raymond DP, Matousek A, Peters JH. Bile acid alone, or in combination with acid, induces CDX2 expression through activation of the epidermal growth factor receptor (EGFR). J Gastrointest Surg 13: 212-222, 2009.
6. Bajpai M, Liu J, Geng X, Souza RF, Amenta PS, Das KM. Repeated exposure to acid and bile selectively induces colonic phenotype expression in a heterogeneous Barrett's epithelial cell line. Lab Invest 88: 643-651, 2008.
7. Beliveau A, Bassett E, Lo AT, Garbe J, Rubio MA, Bissell MJ, Campisi J, Yaswen P. p53-dependent integration of telomere and growth factor deprivation signals. Proc Natl Acad Sci USA 104: 4431-4436, 2007.
8. Bernstein C, Bernstein H, Payne CM, Garewal H. Field defects in progression to adenocarcinoma of the colon and esophagus. Electronic J Biotechnol 3: 167-183, 2000.
9. Bernstein H, Bernstein C, Payne CM, Dvorakova K, Garewal H. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 589: 47-65, 2005.
10. Chang CL, Lao-Sirieix P, Save V, De La Cueva Mendez G, Laskey R, Fitzgerald RC. Retinoic acid-induced glandular differentiation of the oesophagus. Gut 56: 906-917, 2007.
11. Cong Y, Shay JW. Actions of human telomerase beyond telomeres. Cell Res 18: 725-732, 2008.
12. Crowley-Weber CL, Dvorakova K, Crowley C, Bernstein H, Bernstein C, Garewal H, Payne CM. 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 145: 53-66, 2003.
13. Das KM, Kong Y, Bajpai M, Kulkarni D, Geng X, Mishra P, Banerjee D, Hirshfield K. Transformation of benign Barrett's epithelium by repeated acid and bile exposure over 65 weeks: A novel in-vitro model. Int J Cancer 128: 274-282, 2010.
14. Dhar SK, Xu Y, Chen Y, and St. Clair DK. Specificity protein 1-dependent p53-mediated suppression of human manganese superoxide dismutase gene expression. J Biol Chem 281: 21698-21709, 2006.
15. Dvorak K, Chavarria M, Payne CM, Ramsey L, Crowley-Weber C, Dvorakova B, Dvorak B, Bernstein H, Holubec H, Sampliner RE, Bernstein C, Prasad A, Green SB, Garewal H. Activation of the interleukin-6/STAT3 antiapoptotic pathway in esophageal cells by bile acids and low pH: relevance to Barrett's esophagus. Clin Cancer Res 13: 5305-5313, 2007.
16. 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.
17. Dvorakova K, Payne CM, Ramsey L, Holubec H, Sampliner R, Dominguez J, Dvorak B, Bernstein H, Bernstein C, Prasad A, Fass R, Cui H, Garewal H. Increased expression and secretion of interleukin-6 in patients with Barrett's esophagus. Clin Cancer Res 10: 2020-2028, 2004. (Pubitemid 38375562)
18. Dvorakova K, Waltmire CN, Payne CM, Tome ME, Briehl MM, Dorr RT. Induction of mitochondrial changes in myeloma cells by imexon. Blood 97: 3544-3551, 2001.
19. Glickman JN, Chen YY, Wang HH, Antonioli DA, Odze RD. Phenotypic characteristics of a distinctive multilayered epithelium suggests that it is a precursor in the development of Barrett's esophagus. Am J Surg Pathol 25: 569-578, 2001.
20. 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.
21. + exchanger: implication for Barrett's oesophagus. Gut 59: 1606-1616, 2010.
22. Hodge DR, Peng B, Pompeia C, Thomas S, Cho E, Clausen PA, Marquez VE, Farrar WL. Epigenetic silencing of manganese superoxide dismutase (SOD-2) in KAS 6/1 human multiple myeloma cells increases cell proliferation. Cancer Biol Ther 4: 585-592, 2005.
23. Hodge DR, Xiao W, Peng B, Cherry JC, Munroe DJ, Farrar WL. Enforced expression of superoxide dismutase 2/manganese superoxide dismutase disrupts autocrine interleukin-6 stimulation in human multiple myeloma cells and enhances dexamethasone-induced apoptosis. Cancer Res 65: 6255-6263, 2005.
24. Hu Y, Williams VA, Gellersen O, Jones C, Watson TJ, Peters JH. The pathogenesis of Barrett's esophagus: secondary bile acids upregulate intestinal differentiation factor CDX2 expression in esophageal cells. J Gastrointest Surg 11: 827-834, 2007.
25. 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 e191, 2010.
26. Inayama M, Hashimoto N, Tokoro T, Shiozaki H. Involvement of oxidative stress in experimentally induced reflux esophagitis and esophageal cancer. Hepatogastroenterology 54: 761-765, 2007.
27. Iqbal J, Whitney P. Use of cyanide and diethyldithiocarbamate in the assay of superoxide dismutases. Free Radic Biol Med 10: 69-77, 1991.
28. Jankowski JA, Harrison RF, Perry I, Balkwill F, Tselepis, C. Barrett's metaplasia. Lancet 356: 2079-2085, 2000.
29. Jenkins GJ, Doak SH, Parry JM, D'Souza FR, Griffiths AP, Baxter JN. Genetic pathways involved in the progression of Barrett's metaplasia to adenocarcinoma. Br J Surg 89: 824-837, 2002.
30. 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-κB and induces IL-8 expression in oesophageal cells in vitro. Carcinogenesis 25: 317-323, 2004.
31. Kinnula VL, Crapo JD. Superoxide dismutases in malignant cells and human tumors. Free Radic Biol Med 36: 718-744, 2004.
32. Kong J, Nakagawa H, Isariyawongse BK, Funakoshi S, Silberg DG, Rustgi AK, Lynch JP. Induction of intestinalization in human esophageal keratinocytes is a multistep process. Carcinogenesis 30: 122-130, 2009.
33. Kwak EL, Jankowski J, Thayer SP, Lauwers GY, Brannigan BW, Harris PL, Okimoto RA, Haserlat SM, Driscoll DR, Ferry D, Muir B, Settleman J, Fuchs CS, Kulke MH, Ryan DP, Clark JW, Sgroi DC, Haber DA, Bell DW. Epidermal growth factor receptor kinase domain mutations in esophageal and pancreatic adenocarcinomas. Clin Cancer Res 12: 4283-4287, 2006.
34. Lao-Sirieix P, Corovic A, Jankowski J, Lowe A, Triadafilopoulos G, Fitzgerald RC. Physiological and molecular analysis of acid loading mechanisms in squamous and columnar-lined esophagus. Dis Esophagus 21: 529-538, 2008.
35. Li Y, Reuter NP, Li X, Liu Q, Zhang J, Martin RC. Colocalization of MnSOD expression in response to oxidative stress. Mol Carcinog 49: 44-53, 2010.
36. Li Y, Wo JM, Ray MB, Jones W, Su RR, Ellis S, Martin RC. Cyclooxygenase-2 and epithelial growth factor receptor up-regulation during progression of Barrett's esophagus to adenocarcinoma. World J Gastroenterol 12: 928-934, 2006.
37. Li Y, Wo JM, Su RR, Ray MB, Martin RC. Loss of manganese superoxide dismutase expression and activity in rat esophagus with external esophageal perfusion. Surgery 141: 359-367, 2007.
38. MacLennan AJ, Orringer MB, Beer DG. Identification of intestinal-type Barrett's metaplasia by using the intestine-specific protein villin and esophageal brush cytology. Mol Carcinog 24: 137-143, 1999.
39. + exchanger. Eur J Med Chem 38: 547-554, 2003.
40. 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. (Pubitemid 29195903)
41. Nielsen M, Kaltoft K, Nordahl M, Ropke C, Geisler C, Mustelin T, Dobson P, Svejgaard A, Odum N. Constitutive activation of a slowly migrating isoform of Stat3 in mycosis fungoides: tyrphostin AG490 inhibits Stat3 activation and growth of mycosis fungoides tumor cell lines. Proc Natl Acad Sci USA 94: 6764-6769, 1997. (Pubitemid 27281938)
42. 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-κB expression along the inflammation-metaplasia- dysplasia-adenocarcinoma sequence in the esophagus. Am J Gastroenterol 100: 1257-1264, 2005.
43. Paoletti F, Aldinucci D, Mocali A, Caparrini A. A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154: 536-541, 1986.
44. Richter JE. Importance of bile reflux in Barrett's esophagus. Dig Dis 18: 208-216, 2000.
45. Rosati A, Ammirante M, Gentilella A, Basile A, Festa M, Pascale M, Marzullo L, Belisario MA, Tosco A, Franceschelli S, Moltedo O, Pagliuca G, Lerose R, Turco MC. Apoptosis inhibition in cancer cells: a novel molecular pathway that involves BAG3 protein. Int J Biochem Cell Biol 39: 1337-1342, 2007.
46. Rosati A, Di Salle E, Luberto L, Quinto I, Scala G, Turco MC, Pascale M. Identification of a Btk-BAG3 complex induced by oxidative stress. Leukemia 23: 823-824, 2009.
47. Rosati A, Leone A, Del Valle L, Amini S, Khalili K, Turco MC. Evidence for BAG3 modulation of HIV-1 gene transcription. J Cell Physiol 210: 676-683, 2007.
48. Salo JA, Kivilaakso EO, Kiviluoto TA, Virtanen IO. Cytokeratin profile suggests metaplastic epithelial transformation in Barrett's oesophagus. Ann Med 28: 305-309, 1996.
49. - exchanger. Am J Physiol Gastrointest Liver Physiol 289: G991-G997, 2005.
50. + exchanger-1. Am J Physiol Renal Physiol 295: F625-F632, 2008.
51. Shahidullah M, Mandal A, Delamere NA. Responses of sodium-hydrogen exchange to nitric oxide in porcine cultured nonpigmented ciliary epithelium. Invest Ophthalmol Vis Sci 50: 5851-5858, 2009.
52. Shukla S, Shukla M, Maclennan GT, Fu P, Gupta S. Deregulation of FOXO3A during prostate cancer progression. Int J Oncol 34: 1613-1620, 2009.
53. Sihvo EI, Ruohtula T, Auvinen MI, Koivistoinen A, Harjula AL, Salo JA. Simultaneous progression of oxidative stress and angiogenesis in malignant transformation of Barrett esophagus. J Thorac Cardiovasc Surg 126: 1952-1957, 2003.
54. Sihvo EI, Salminen JT, Rantanen TK, Ramo OJ, Ahotupa M, Farkkila M, Auvinen MI, Salo JA. Oxidative stress has a role in malignant transformation in Barrett's oesophagus. Int J Cancer 102: 551-555, 2002.
55. Smith LL, Coller HA, Roberts JM. Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nat Cell Biol 5: 474-479, 2003. (Pubitemid 36592272)
56. Souza RF, Shewmake K, Terada LS, Spechler SJ. Acid exposure activates the mitogen-activated protein kinase pathways in Barrett's esophagus. Gastroenterology 122: 299-307, 2002. (Pubitemid 34126346)
57. Spechler SJ, Fitzgerald RC, Prasad GA, Wang KK. History, molecular mechanisms, and endoscopic treatment of Barrett's esophagus. Gastroenterology 138: 854-869, 2010.
58. Stewart SA, Hahn WC, O'Connor BF, Banner EN, Lundberg AS, Modha P, Mizuno H, Brooks MW, Fleming M, Zimonjic DB, Popescu NC, Weinberg RA. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc Natl Acad Sci USA 99: 12606-12611, 2002.
59. Stoner GD, Kaighn ME, Reddel RR, Resau JH, Bowman D, Naito Z, Matsukura N, You M, Galati AJ, Harris CC. Establishment and characterization of SV40 T-antigen immortalized human esophageal epithelial cells. Cancer Res 51: 365-371, 1991.
60. Tong X, Yin L, Washington R, Rosenberg DW, Giardina C. The p50-p50 NF-κB complex as a stimulus-specific repressor of gene activation. Mol Cell Biochem 265: 171-183, 2004. (Pubitemid 41461877)
61. Vaezi MF, Richter JE. Role of acid and duodenogastroesophageal reflux in gastroesophageal reflux disease. Gastroenterology 111: 1192-1199, 1996.
62. Wilson KT, Fu S, Ramanujam KS, Meltzer SJ. Increased expression of inducible nitric oxide synthase and cyclooxygenase-2 in Barrett's esophagus and associated adenocarcinomas. Cancer Res 58: 2929-2934, 1998.
63. Wu J, Gong J, Geng J, Song Y. Deoxycholic acid induces the overexpression of intestinal mucin, MUC2, via NF-κB signaling pathway in human esophageal adenocarcinoma cells. BMC Cancer 8: 333, 2008.
64. + exchange. Annu Rev Physiol 67: 411-443, 2005.
65. Zhang HY, Zhang X, Huo X, Hormi-Carver K, Spechler SJ, Souza RF. Increased expression, secretion and activation of IL-6 during the neoplastic progression of Barrett's esophagus (Abstract). Gastroenterology 136: A-92, 2009.
66. Zhou G, Sun YG, Wang HB, Wang WQ, Wang XW, Fang DC. Acid and bile salt up-regulate BMP4 expression in human esophageal epithelium cells. Scand J Gastroenterol 44: 926-932, 2009.