Caudal homeobox protein Cdx-2 cooperates with Wnt pathway to regulate claudin-1 expression in colon cancer cells

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Bhat, Ajaz A ^a   Sharma, Ashok ^a   Pope, Jillian ^a   Krishnan, Moorthy ^a   Washington, Mary K ^a   Singh, Amar B ^a   Dhawan, Punita ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CLAUDIN 1; MESSENGER RNA; TRANSCRIPTION FACTOR CDX1; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR GATA 4;

ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CLAUDIN 1 GENE; COLON CANCER; CONTROLLED STUDY; DELETION MUTANT; DNA FLANKING REGION; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; PEPTIDE MAPPING; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; WNT SIGNALING PATHWAY;

BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CLAUDIN-1; COLORECTAL NEOPLASMS; DNA; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC; WNT PROTEINS;

EID: 84862490550     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037174     Document Type: Article

References (48)

1. Tsukita S, Furuse M, (2000) The structure and function of claudins, cell adhesion molecules at tight junctions. J Cell Biol 149: 13-16.
2. Morita K, Furuse M, Fujimoto K, Tsukita S, (1999) Claudin multigene family encoding four transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96: 511-516.
3. Tsukita S, Furuse M, Itoth M, (2001) Multifunctional strands in tight junctions. Nat. Rev. Mol Cell Biol 2: 285-293.
4. Furuse M, Sasaki H, Fujimoto K, Tsukita S, (1998) A single gene product, claudin-1 or-2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143: 391-401.
5. Dhawan P, Singh AB, Deane NG, No Y, Shiou SR, et al. (2005) Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J Clin Invest 115: 1765-76.
6. Miwa N, Furuse M, Tsukita S, Niikawa N, Nakamura Y, et al. (2000) Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res 12: 469-476.
7. Charité J, de Graaff W, Consten D, Reijnen MJ, Korving J, et al. (1998) Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development 125: 4349-58.
8. Duprey P, Chowdhury K, Dressler GR, Balling R, Simon D, et al. (1988) A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev 2: 1647-54.
9. James R, Erler T, Kazenwadel J, (1994) Structure of the murine homeobox gene cdx-2. Expression in embryonic and adult intestinal epithelium. J Biol Chem 269: 15229-15237.
10. Soubeyran P, André F, Lissitzky JC, Mallo GV, Moucadel V, et al. (1999) Cdx1 promotes differentiation in a rat intestinal epithelial cell line. Gastroenterology 117: 1326-1338.
11. Lynch J, Suh ER, Silberg DG, Rulyak S, Blanchard N, et al. (2000) The caudal-related homeodomain protein Cdx1 inhibits proliferation of intestinal epithelial cells by down-regulation of D-type cyclins. J Biol Chem 275: 4499-4506.
12. Suh E, Chen L, Taylor J, Traber PG, (1994) A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol 14: 7340-7351.
13. Lambert M, Colnot S, Suh E, L'Horset F, Blin C, et al. (1996) cis-Acting elements and transcription factors involved in the intestinal specific expression of the rat calbindin-D9K gene: binding of the intestine-specific transcription factor Cdx-2 to the TATA box. Eur J Biochem 236: 778-788.
14. Troelsen JT, Mitchelmore C, Spodsberg N, Jensen AM, Norén O, et al. (1997) Regulation of lactase-phlorizin hydrolase gene expression by the caudal-related homoeodomain protein Cdx-2. Biochem J 322: 833-838.
15. Mitchelmore C, Troelsen JT, Spodsberg N, Sjöström H, Norén O, (2000) Interaction between the homeodomain proteins Cdx2 and HNF1alpha mediates expression of the lactase-phlorizin hydrolase gene. Biochem J 346: 529-535.
16. Fang R, Santiago NA, Olds LC, Sibley E, (2000) The homeodomain protein Cdx2 regulates lactase gene promoter activity during enterocyte differentiation. Gastroenterology 118: 115-127.
17. Drummond F, Sowden J, Morrison K, Edwards YH, (1996) The caudal-type homeobox protein Cdx-2 binds to the colon promoter of the carbonic anhydrase 1 gene. Eur J Biochem 236: 670-681.
18. Drummond FJ, Sowden J, Morrison K, Edwards YH, (1998) Colon carbonic anhydrase 1: transactivation of gene expression by the homeodomain protein Cdx2. FEBS Lett 423: 218-222.
19. Boudreau F, Rings EH, van Wering HM, Kim RK, Swain GP, et al. (2002) Hepatocyte nuclear factor-1 alpha, GATA-4, and caudal related homeodomain protein Cdx2 interact functionally to modulate intestinal gene transcription. Implication for the developmental regulation of the sucrase-isomaltase gene. J Biol Chem 277: 31909-31917.
20. Satake S, Semba S, Matsuda Y, Usami Y, Chiba H, et al. (2008) Cdx2 transcription factor regulates claudin-3 and claudin-4 expression during intestinal differentiation of gastric carcinoma. Pathol Int 58: 156-163.
21. Shiou SR, Singh AB, Moorthy K, Datta PK, Washington MK, et al. (2007) Smad4 Regulates Claudin-1 Expression in a Transforming Growth Factor-β-Independent Manner in Colon Cancer Cells. Cancer Res 67: 1571-1579.
22. Guo RJ, Funakoshi S, Lee HH, Kong J, Lynch JP, (2010) The intestine-specific transcription factor Cdx2 inhibits beta-catenin/TCF transcriptional activity by disrupting the beta-catenin-TCF protein complex. Carcinogenesis 31: 159-66.
23. Dang LH, Chen F, Ying C, Chun SY, Knock SA, et al. (2006) CDX2 has tumorigenic potential in the human colon cancer cell lines LOVO and SW48. Oncogene 25: 2264-72.
24. Singh AB, Sharma A, Smith JJ, Krishnan M, Chen X, et al. (2011) Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology 141: 2140-53.
25. Krishnan M, Singh AB, Smith JJ, Sharma A, Chen X, et al. (2010) HDAC inhibitors regulate claudin-1 expression in colon cancer cells through modulation of mRNA stability. Oncogene 14 (2): 305-12.
26. James R, Kazenwadel J, (1991) Homeobox gene expression in the intestinal epithelium of adult mice. J Biol Chem 266: 3246-3251.
27. James R, Erler T, Kazenwadel J, (1994) Structure of the murine homeobox gene Cdx-2. Expression in embryonic and adult intestinal epithelium. J Biol Chem 269: 15229-15237.
28. Suh E, Traber PG, (1996) An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol 16: 619-625.
29. Silberg DG, Swain GP, Suh ER, Traber PG, (2000) Cdx1 and Cdx2 expression during intestinal development. Gastroenterology 119: 961-971.
30. Miller CT, Moy JR, Lin L, Schipper M, Normolle D, et al. (2003) Gene amplification in esophageal adenocarcinomas and Barrett's with high-grade dysplasia. Clin Cancer Res 15: 4819-25.
31. Hellebrekers DM, Lentjes MH, van den Bosch SM, Melotte V, Wouters KA, et al. (2009) GATA4 and GATA5 are potential tumor suppressors and biomarkers in colorectal cancer. Clin Cancer Res 15 (12): 3990-7.
32. Chawengsaksophak K, James R, Hammond VE, Köntgen F, Beck F, (1997) Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386: 84-7.
33. Tamai Y, Nakajima R, Ishikawa T, Takaku K, Seldin MF, et al. (1999) Colonic hamartoma development by anomalous duplication in Cdx2 knockout mice. Cancer Res 59: 2965-70.
34. Bonhomme C, Duluc I, Martin E, Chawengsaksophak K, Chenard MP, et al. (2003) The Cdx2 homeobox gene has a tumour suppressor function in the distal colon in addition to a homeotic role during gut development. Gut 52: 1465-71.
35. Aoki K, Tamai Y, Horiike S, Oshima M, Taketo MM, (2003) Colonic polyposis caused by mTOR-mediated chromosomal instability in Apc+/Delta716 Cdx2+/- compound mutant mice. Nat Genet 35: 323-30.
36. Dang LH, Chen F, Ying C, Chun SY, Knock SA, et al. (2006) CDX2 has tumorigenic potential in the human colon cancer cell lines LOVO and SW48. Oncogene 25: 2264-2272.
37. Chun SY, Chen F, Washburn JG, MacDonald JW, Innes KL, et al. (2007) CDX2 promotes anchorage-independent growth by transcriptional repression of IGFBP-3. Oncogene 26: 4725-4729.
38. Moskaluk CA, Zhang H, Powell SM, Cerilli LA, Hampton GM, et al. (2003) Cdx2 protein expression in normal and malignant human tissues: an immunohistochemical survey using tissue microarrays Mod Pathol 16: 913-9.
39. Kaimaktchiev V, Terracciano L, Tornillo L, Spichtin H, Stoios D, et al. (2004) The homeobox intestinal differentiation factor CDX2 is selectively expressed in gastrointestinal adenocarcinomas. Mod Pathol 17: 1392-9.
40. Sakaguchi T, Gu X, Golden HM, Suh E, Rhoads DB, et al. (2002) Cloning of the human claudin-2 5/-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1alpha. J Biol Chem 277: 21361-21370.
41. Escaffit F, Boudreau F, Beaulieu JF, (2005) Differential expression of claudin-2 along the human intestine: Implication of GATA-4 in the maintenance of claudin-2 in differentiating cells. J Cell Physiol 203: 15-26.
42. Dhawan P, Ahmad R, Chaturvedi R, Smith JJ, Midha R, et al. (2011) Claudin-2 expression increases tumorigenicity of colon cancer cells: role of epidermal growth factor receptor activation. Oncogene 21 (29): 3234-47.
43. McLin VA, Rankin SA, Zorn AM, (2007) Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134: 2207-2217.
44. Kahler RA, Westendorf JJ, (2003) Lymphoid enhancer factor-1 and beta-catenin inhibit Runx2-dependent transcriptional activation of the osteocalcin promoter. J Biol Chem 278: 11937-11944.
45. Lickert H, Domon C, Huls G, Wehrle C, Duluc I, et al. (2000) Wnt/(beta)-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 127: 3805-3813.
46. Verzi MP, Hatzis P, Sulahian R, Philips J, Schuijers J, et al. (2010) TCF4 and CDX2, major transcription factors for intestinal function, converge on the same cis-regulatory regions. Proc Natl Acad Sci U S A 107: 15157-62.
47. Wong V, Gumbiner BM, (1997) A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 136: 399-409.
48. Vietor I, Bader T, Paiha K, Huber LA, (2001) Perturbation of the tight junction permeability barrier by occludin loop peptides activates beta-catenin/TCF/LEF-mediated transcription. EMBO 2: 306-312.