Activation of the BMP4 Pathway and Early Expression of CDX2 Characterize Non-specialized Columnar Metaplasia in a Human Model of Barrett's Esophagus

Journal of Gastrointestinal Surgery

Volumn 16, Issue 2, 2012, Pages 227-237

  Castillo, Daniel ^a   Puig, Sonia ^a   Iglesias, Mar ^a   Seoane, Agustín ^a   de Bolós, Carme ^a   Munitiz, Vicente ^b   Parrilla, Pascual ^b   Comerma, Laura ^a   Poulsom, Richard ^c   Krishnadath, Kausilia K ^d   Grande, Luís ^a   Pera, Manuel ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Barrett's esophagus; BMP4; CDX1; CDX2; Columnar metaplasia

Indexed keywords

BIOLOGICAL MARKER; BMP4 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN 4; CDX1 PROTEIN, HUMAN; CDX2 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MUC2 PROTEIN, HUMAN; MUCIN 2; RECEPTOR REGULATED SMAD PROTEIN;

AGED; ARTICLE; BARRETT ESOPHAGUS; BIOPSY; ESOPHAGUS RESECTION; FEMALE; FOLLOW UP; GASTROESOPHAGEAL REFLUX; HUMAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; METABOLISM; METAPLASIA; MIDDLE AGED; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

AGED; BARRETT ESOPHAGUS; BIOLOGICAL MARKERS; BIOPSY; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 4; ESOPHAGECTOMY; FEMALE; FOLLOW-UP STUDIES; GASTROESOPHAGEAL REFLUX; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; METAPLASIA; MIDDLE AGED; MUCIN-2; REAL-TIME POLYMERASE CHAIN REACTION; SMAD PROTEINS, RECEPTOR-REGULATED;

EID: 84856231295     PISSN: 1091255X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11605-011-1758-5     Document Type: Article

References (40)

1. Souza RF, Krishnan K, Spechler SJ. Acid, bile, and CDX: the ABCs of making Barrett's metaplasia. Am J Physiol Gastrointest Liver Physiol 2008; 295: G211-218.
2. Spechler SJ, Fitzgerald RC, Prasad GA, Wang KK. History, molecular mechanisms, and endoscopic treatment of Barrett's esophagus. Gastroenterology 2010; 138: 854-869.
3. Wang KK, Sampliner RE. Updated guidelines 2008 for the diagnosis, surveillance and therapy of Barrett's esophagus. Am J Gastroenterol 2008; 103: 788-797.
4. Fitzgerald RC. Molecular basis of Barrett's oesophagus and oesophageal adenocarcinoma. Gut 2006; 55: 1810-1820.
5. Tosh D, Slack JM. How cells change their phenotype. Nat Rev Mol Cell Biol 2002; 3: 187-194.
6. Krishnadath KK. Novel findings in the pathogenesis of esophageal columnar metaplasia or Barrett's esophagus. Curr Opin Gastroenterol 2007; 23: 440-445.
7. Lord RV, Wickramasinghe K, Johansson JJ, DeMeester SR, Brabender J, DeMeester TR. Cardiac mucosa in the remnant esophagus after esophagectomy is an acquired epithelium with Barrett's-like features. Surgery 2004; 136: 633-640.
8. D'Journo XB, Martin J, Rakovich G, Brigand C, Gaboury L, Ferraro P, Duranceau A. Mucosal damage in the esophageal remnant after esophagectomy and gastric transposition. Ann Surg 2009; 249: 262-268.
9. Dresner SM, Griffin SM, Wayman J, Bennett MK, Hayes N, Raimes SA. Human model of duodenogastro-oesophageal reflux in the development of Barrett's metaplasia. Br J Surg 2003; 90: 1120-1128.
10. Hamilton SR, Yardley JH. Regenerative of cardiac type mucosa and acquisition of Barrett mucosa after esophagogastrostomy. Gastroenterology 1977; 72: 669-675.
11. O'Riordan JM, Tucker ON, Byrne PJ, McDonald GS, Ravi N, Keeling PW, Reynolds JV. Factors influencing the development of Barrett's epithelium in the esophageal remnant postesophagectomy. Am J Gastroenterol 2004; 99: 205-211.
12. Oberg S, Johansson J, Wenner J, Walther B. Metaplastic columnar mucosa in the cervical esophagus after esophagectomy. Ann Surg 2002; 235: 338-345.
13. Peitz U, Vieth M, Ebert M, Kahl S, Schulz HU, Roessner A, Malfertheiner P. Small-bowel metaplasia arising in the remnant esophagus after esophagojejunostomy--a [corrected] prospective study in patients with a history of total gastrectomy. Am J Gastroenterol 2005; 100: 2062-2070.
14. Milano F, van Baal JW, Buttar NS, Rygiel AM, de Kort F, DeMars CJ, Rosmolen WD, Bergman JJ, J VAM, Wang KK, Peppelenbosch MP, Krishnadath KK. Bone morphogenetic protein 4 expressed in esophagitis induces a columnar phenotype in esophageal squamous cells. Gastroenterology 2007; 132: 2412-2421.
15. Wang DH, Clemons NJ, Miyashita T, Dupuy AJ, Zhang W, Szczepny A, Corcoran-Schwartz IM, Wilburn DL, Montgomery EA, Wang JS, Jenkins NA, Copeland NA, Harmon JW, Phillips WA, Watkins DN. Aberrant epithelial-mesenchymal Hedgehog signaling characterizes Barrett's metaplasia. Gastroenterology 2010; 138: 1810-1822.
16. Milano F, Pacha A, Buttar NS, Krishnadath KK. The synergistic cooperative interaction of the BMP4 and CDX-2 enhance transcription of intestine specific genes during development of intestinal type of metaplasia or Barrett's esophagus. Gastroenterology 2009; 136: A83.
17. Guo RJ, Suh ER, Lynch JP. The role of Cdx proteins in intestinal development and cancer. Cancer Biol Ther 2004; 3: 593-601.
18. Groisman GM, Amar M, Meir A. Expression of the intestinal marker Cdx2 in the columnar-lined esophagus with and without intestinal (Barrett's) metaplasia. Mod Pathol 2004; 17: 1282-1288.
19. Hahn HP, Blount PL, Ayub K, Das KM, Souza R, Spechler S, Odze RD. Intestinal differentiation in metaplastic, nongoblet columnar epithelium in the esophagus. Am J Surg Pathol 2009; 33: 1006-1015.
20. Kerkhof M, Bax DA, Moons LM, van Vuuren AJ, van Dekken H, Steyerberg EW, Kuipers EJ, Kusters JG, Siersema PD. Does CDX2 expression predict Barrett's metaplasia in oesophageal columnar epithelium without goblet cells? Aliment Pharmacol Ther 2006; 24: 1613-1621.
21. Phillips RW, Frierson HF, Jr., Moskaluk CA. Cdx2 as a marker of epithelial intestinal differentiation in the esophagus. Am J Surg Pathol 2003; 27: 1442-1447.
22. van Baal JW, Bozikas A, Pronk R, Ten Kate FJ, Milano F, Rygiel AM, Rosmolen WD, Peppelenbosch MP, Bergman JJ, Krishnadath KK. Cytokeratin and CDX-2 expression in Barrett's esophagus. Scand J Gastroenterol 2008; 43: 132-140.
23. Vallbohmer D, DeMeester SR, Peters JH, Oh DS, Kuramochi H, Shimizu D, Hagen JA, Danenberg KD, Danenberg PV, DeMeester TR, Chandrasoma PT. Cdx-2 expression in squamous and metaplastic columnar epithelia of the esophagus. Dis Esophagus 2006; 19: 260-266.
24. 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.
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 2010; 139: 194-203.
26. Moons LM, Bax DA, Kuipers EJ, van Dekken H, Haringsma J, van Vliet AH, Siersema PD, Kusters JG. The homeodomain protein CDX2 is an early marker of Barrett's oesophagus. J Clin Pathol 2004; 57: 1063-1068.
27. Odze RD. Barrett esophagus: histology and pathology for the clinician. Nat Rev Gastroenterol Hepatol 2009; 6: 478-490.
28. Paull A, Trier JS, Dalton MD, Camp RC, Loeb P, Goyal RK. The histologic spectrum of Barrett's esophagus. N Engl J Med 1976; 295: 476-480.
29. Zandvliet DW, Hanby AM, Austin CA, Marsh KL, Clark IB, Wright NA, Poulsom R. Analysis of foetal expression sites of human type II DNA topoisomerase alpha and beta mRNAs by in situ hybridisation. Biochim Biophys Acta 1996; 1307: 239-247.
30. 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 2007; 11: 827-834.
31. Kazumori H, Ishihara S, Rumi MA, Kadowaki Y, Kinoshita Y. Bile acids directly augment caudal related homeobox gene Cdx2 expression in oesophageal keratinocytes in Barrett's epithelium. 2006; Gut 55: 16-25.
32. Liu T, Zhang X, So CK, 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: 488-496.
33. Marchetti M, Caliot E, Pringault E. Chronic acid exposure leads to activation of the cdx2 intestinal homeobox gene in a long-term culture of mouse esophageal keratinocytes. J Cell Sci 2003; 116: 1429-1436.
34. Vaninetti N, Williams L, Geldenhuys L, Porter GA, Guernsey DL, Casson AG. Regulation of CDX2 expression in esophageal adenocarcinoma. Mol Carcinog 2009; 48: 965-974.
35. Pera M, Pera M, de Bolos C, Brito MJ, Palacin A, Grande L, Cardesa A, Poulsom R. Duodenal-content reflux into the esophagus leads to expression of Cdx2 and Muc2 in areas of squamous epithelium in rats. J Gastrointest Surg 2007; 11: 869-874.
36. Ji J, Yamashita T, Budhu A, Forgues M, Jia HL, Li C, Deng C, Wauthier E, Reid LM, Ye QH, Qin LX, Yang W, Wang HY, Tang ZY, Croce CM, Wang XW. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 2009; 50: 472-480.
37. Rotkrua P, Akiyama Y, Hashimoto Y, Otsubo T, Yuasa Y. MiR-9 down-regulates CDX2 expression in gastric cancer cells. Int J Cancer 2011 Jan 10. [Epub ahead of print].
38. Bax D, Siersema PD, Moons LM, Dekken H, Tilanus HW, Kusters JG, Kuipers EJ. CDX2 expression in columnar metaplasia of the remnant esophagus in patients who underwent esophagectomy. J Clin Gastroenterol 2007; 41: 375-379.
39. Mesquita P, Jonckheere N, Almeida R, Ducourouble MP, Serpa J, Silva E, Pigny P, Silva FS, Reis C, Silberg D, van Seuningen I, David L. Human MUC2 mucin gene is transcriptionally regulated by Cdx homeodomain proteins in gastrointestinal carcinoma cell lines. J Biol Chem 2003; 278: 51549-51556.
40. Almeida R, Silva E, Santos-Silva F, Silberg DG, Wang J, De Bolos C, David L. Expression of intestine-specific transcription factors, CDX1 and CDX2, in intestinal metaplasia and gastric carcinomas. J Pathol 2003; 199: 36-40.