Immunohistochemical expression of CDX2, β-catenin, and TP53 in inflammatory bowel disease-associated colorectal cancer

Inflammatory Bowel Diseases

Volumn 17, Issue 1, 2011, Pages 232-240

  Laurent, Camille ^a,b   Svrcek, Magali ^c   Flejou, Jean François ^c   Chenard, Marie Pierre ^a   Duclos, Bernard ^a,d   Freund, Jean Noël ^b   Reimund, Jean Marie ^e,f  

^a HÔPITAL DE HAUTEPIERRE   (France)

^b INSERM   (France)

^c HÔPITAL SAINT ANTOINE   (France)

^d Biology and Innovative Therapeutics for Ovarian Cancers group   (France)

^e CAEN UNIVERSITY HOSPITAL   (France)

^f Laboratoired'Anatomiecytologiepathologiques   (France)

Author keywords

catenin; CDX2; colorectal cancer; Crohn's disease; inflammatory bowel disease; small bowel adenocarcinoma; TP53; ulcerative colitis

Indexed keywords

BETA CATENIN; PROTEIN P53; TRANSCRIPTION FACTOR CDX2;

ADULT; ARTICLE; CANCER INVASION; CELL MEMBRANE; COLORECTAL CANCER; CONTROLLED STUDY; CROHN DISEASE; DISEASE ASSOCIATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL BOWEL ADENOCARCINOMA; SMALL INTESTINE CARCINOMA; TUMOR DIFFERENTIATION;

ADENOCARCINOMA; ADULT; BETA CATENIN; COLON; COLORECTAL NEOPLASMS; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; INFLAMMATORY BOWEL DISEASES; MALE; MIDDLE AGED; MUTATION; RISK FACTORS; TUMOR SUPPRESSOR PROTEIN P53; YOUNG ADULT;

EID: 78650162662     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21451     Document Type: Article

References (59)

1. Jess T, Gamborg M, Matzen P, et al. Increased risk of intestinal cancer in Crohn's disease. Am J Gastroenterol. 2005; 2724-2729.
2. Canavan C, Abrams KR, Mayberry J., Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn's disease. Aliment Pharmacol Ther. 2006; 23: 1097-1104.
3. Eaden JA, Abrams KR, Mayberry J., The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001; 48: 526-535.
4. Schlemper RJ, Riddell RH, Kato Y, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000; 47: 251-255.
5. Geboes K., Review article: what are the important endoscopic lesions for detection of dysplasia in inflammatory bowel disease? Aliment Pharmacol Ther. 2006; 24 (suppl 3): 50-55.
6. Itzkowitz SH., Molecular biology of dysplasia and cancer in inflammatory bowel disease. Gastroenterol Clin North Am. 2006; 35: 553-571.
7. Rubin DT, Cruz-Correa MR, Gasche C, et al. Colorectal cancer prevention in inflammatory bowel disease and the role of 5-aminosalicylic acid: a clinical review and update. Inflamm Bowel Dis. 2008; 14: 265-274.
8. Viennot S, Deleporte A, Moussata D, et al. Colon cancer in inflammatory bowel disease: recent trends, questions and answers. Gastroenterol Clin Biol. 2009; 33 (suppl 3): S190-S201.
9. Beck F, Chawengsaksophak K, Waring P, et al. Reprogramming of intestinal differentiation and intercalary regeneration in cdx2 mutant mice. Proc Natl Acad Sci U S A. 1999; 96: 7318-7323.
10. Gao N, White P, Kaestner KH., Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev Cell. 2009; 16: 588-599.
11. Lorentz O, Duluc I, De Arcangelis A, et al. Key role of the Cdx2 homeobox gene in extra-cellular matrix-mediated intestinal cell differentiation. J Cell Biol. 1997; 139: 1553-1565.
12. Suh E, Traber PG., An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol. 1996; 16: 619-625.
13. Ee HC, Erler T, Bhathal PS, et al. Cdx-2 homeodomain protein expression in human and rat colorectal adenoma and carcinoma. Am J Pathol. 1995; 147: 586-592.
14. Kaimaktchiev V, Terracciano L, Tornillo L, et al. The homeobox intestinal differentiation factor CDX2 is selectively expressed in gastrointestinal adenocarcinomas. Mod Pathol. 2004; 17: 1392-1399.
15. Subtil C, Guérin E, Schneider A, et al. Frequent rearrangements and amplification of the CDX2 homeobox gene in human sporadic colorectal cancers with chromosomal instability. Cancer Lett. 2007; 247: 197-203.
16. Brabletz T, Spaderna S, Kolb J, et al. Down-regulation of the homeodomain factor Cdx2 in colorectal cancer by collagen type I: an active role for the tumor environment in malignant tumor progression. Cancer Res. 2004; 64: 6973-6977.
17. Hinoi T, Tani M, Lucas PC, et al. Loss of CDX2 expression and microsatellite instability are prominent features of large cell minimally differentiated carcinomas of the colon. Am J Pathol. 2001; 159-2239-2248.
18. Lugli A, Tzankov A, Zlobec I, et al. Differential diagnostic and functional role of the multi-marker phenotype CDX2/CK20/CK7 in colorectal cancer stratified by mismatch repair status. Mod Pathol. 2008; 21: 1403-1412.
19. Bonhomme C, Duluc I, Martin E, et al. The Cdx2 homeobox gene has a tumour suppressor function in the distal colon in addition to a homeotic role during gut development. Gut. 2003; 52: 1465-1471.
20. Aoki K, Tamai Y, Horiike S, et al. Colonic polyposis caused by mTOR-mediated chromosomal instability in Apc+/Î716Cdx2+/- compound mutant mice. Nat Genet. 2003; 35: 323-330.
21. Gross I, Duluc I, Benameur T, et al. The intestine-specific homeobox gene Cdx2 decreases motility and antagonizes dissemination of colon cancer cells. Oncogene. 2008; 27: 107-115.
22. Calon A, Gross I, Lhermitte B, et al. Different effects of the Cdx1 and Cdx2 homeobox genes in a murine model of intestinal inflammation. Gut. 2007; 56: 1688-1695.
23. Svrcek M, El-Bchiri J, Chalastanis A, et al. Specific clinical and biological features characterize inflammatory bowel disease associated colorectal cancers showing microsatellite instability. J Clin Oncol. 2007; 25: 4231-4238.
24. Moskaluk CA, Zhang H, Powell SM, et al. Cdx2 protein expression in normal and malignant human tissues: an immunohistochemical survey using tissue microarrays. Mod Pathol. 2003; 16: 913-919.
25. Barbareschi M, Murer B, Colby TV, et al. CDX2 homeobox gene expression is a reliable marker of colorectal adenocarcinoma metastases to the lungs. Am J Surg Pathol. 2003; 27: 141-149.
26. Werling RW, Yaziji H, Bacchi CE, et al. CDX2, a highly sensitive and specific marker of colorectal adenocarcinomas of intestinal origin: an immunohistochemical survey of 476 primary and metastatic carcinomas. Am J Surg Pathol. 2003; 27: 303-310.
27. Benhamed F, Gross I, Gaunt SJ, et al. Multiple regulatory regions control the complex expression pattern of the mouse Cdx2 homeobox gene. Gastroenterology. 2008; 135: 1238-1247.
28. Blache P, van de Wetering M, Duluc I, et al. SOX9 is an intestine crypt transcription factor, is regulated by Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol. 2004; 166: 37-47.
29. Baba Y, Nosho K, Shima K, et al. Relationship of CDX2 loss with molecular features and prognosis in colorectal cancer. Clin Cancer Res. 2009; 15: 4665-4673.
30. Gross I, Lhermitte B, Domon-Dell C, et al. Phosphorylation of the homeotic tumor suppressor Cdx2 mediates its ubiquitin-dependent proteasome degradation. Oncogene. 2005; 24: 7955-7963.
31. Rings EH, Boudreau F, Taylor JK, et al. Phosphorylation of the serine 60 residue within the cdx2 activation domain mediates its transactivation capacity. Gastroenterology. 2001; 121: 1437-1450.
32. Polakis P., The many ways of Wnt in cancer. Curr Opin Genet Dev. 2007; 17: 45-51.
33. Lai S-L, Chien AJ, Moon RT., Wnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis. Cell Res. 2009; 19: 532-545.
34. Kikuchi A, Yamamoto H., Tumor formation due to abnormalities in the β-catenin-independent pathways of Wnt signaling. Cancer Sci. 2008; 99: 202-208.
35. Dejmek J, Dejmek A, Säfholm A, et al. Wnt-5a protein expression in primary dukes B colon cancers identifies a subgroup of patients with good prognosis. Cancer Res. 2005; 65: 9142-9146.
36. Ying J, Li H, Yu J, et al. WNT5A exhibits tumor-suppressive activity through antagonizing the Wnt/beta-catenin signaling, and is frequently methylated in colorectal cancer. Clin Cancer Res. 2008; 14: 55-61.
37. Eaden J, Abrams K, Ekbom A, et al. Colorectal cancer prevention in ulcerative colitis: a case-control study. Aliment Pharmacol Ther. 2000; 14: 145-153.
38. Velayos FS, Terdiman JP, Walsh JM., Effect of 5-aminosalicylates use on colorectal cancer and dysplasia risk: a systematic review and metaanalysis of observational studies. Am J Gastroenterol. 2005; 100: 1345-1353.
39. Castellone MD, Teramoto H, Gutkind JS., Cyclooxygenase-2 and colorectal cancer chemoprevention: the β-catenin connection. Cancer Res. 2006; 66: 11085-11088.
40. Rousseaux C, Lefebvre B, Dubucquoy L, et al. Intestinal anti-inflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator- activated receptor-γ. J Exp Med. 2005; 201: 1205-1215.
41. Schwab M, Reynders V, Loitsch S, et al. PPARγ is involved in mesalazine-mediated induction of apoptosis and inhibition of cell growth in colon cancer cells. Carcinogenesis. 2008; 29: 1407-1414.
42. Allgayer H., Review article: mechanisms of action of mesalazine in preventing colorectal carcinoma in inflammatory bowel disease. Aliment Pharmacol Ther. 2003; 18 (suppl 2): 10-14.
43. Greenwald BD, Harpaz N, Yin J, et al. Loss of heterozygosity affecting the p53, Rb, and mcc/apc tumor suppressor gene loci in dysplastic and cancerous ulcerative colitis. Cancer Res. 1992; 52: 741-745.
44. Brentnall TA, Crispin DA, Rabinovitch PS, et al. Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology. 1994; 107: 369-378.
45. Leedham SJ, Graham TA, Oukrif D, et al. Clonality, founder mutations, and field cancerization in human ulcerative colitis-associated neoplasia. Gastroenterology. 2009; 136: 542-550.
46. Lashner RA, Shapiro BD, Husain A, et al. Evaluation of the usefulness of testing for p53 mutations in colorectal surveillance for ulcerative colitis. Am J Gastroenterol. 1999; 94: 456-462.
47. Nathanson JW, Yadron NE, Farnan J, et al. p53 mutations are associated with dysplasia and progression of dysplasia in patients with Crohn's disease. Dig Dis Sci. 2008; 53: 474-480.
48. Rutter M, Saunders B, Wilkinson K, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 2004; 126: 451-459.
49. Gupta RB, Harpaz N, Itzkowitz S, et al. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology. 2007; 133: 1099-1105.
50. Popivanova BK, Kitamura K, Wu Y, et al. Blocking TNF-α in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest. 2008; 118: 560-570.
51. Palascak-Juif V, Bouvier AM, Cosnes J, et al. Small bowel adenocarcinoma in patients with Crohn's disease compared with small bowel adenocarcinoma de novo. Inflamm Bowel Dis. 2005; 11: 828-832.
52. Jess T, Gamborg M, Matzen P, et al. Increased risk of intestinal cancer in Crohn's disease: a meta-analysis of population-based cohort studies. Am J Gastroenterol. 2005; 100: 2724-2729.
53. Canavan C, Abrams KR, Mayberry J., Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn's disease. Aliment Pharmacol Ther. 2006; 23: 1097-1104.
54. Zhang MQ, Lin F, Hui P, et al. Expression of mucins, SIMA, villin, and CDX2 in small-intestinal adenocarcinoma. Am J Clin Pathol. 2007; 128: 808-816.
55. Wheeler JMD, Warren BF, Mortensen NJMC, et al. An insight into the genetic pathway of adenocarcinoma of the small intestine. Gut. 2002; 50: 218-223.
56. Zhang MQ, Chen Z-M E, Wang HL., Immunohistochemical investigation of tumorigenic pathways in small intestinal adenocarcinoma: a comparison with colorectal adenocarcinoma. Mod Pathol. 2006; 19: 573-580.
57. Bläker H, Helmchen B, Bönisch A, et al. Mutational activation of the RAS-RAF-MAPK and the Wnt pathway in small intestinal adenocarcinomas. Scand J Gastroenterol. 2004; 39: 748-753.
58. Svrcek M, Jourdan F, Sebbagh N, et al. Immunohistochemical analysis of adenocarcinoma of the small intestine: a tissue microarray study. J Clin Pathol. 2003; 56: 898-903.
59. Nishiyama K, Yao T, Yonemasu H, et al. Overexpression of p53 protein and point mutation of K-ras gene in primary carcinoma of the small intestine. Oncol Rep. 2002; 9: 293-300.