Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation

Laboratory Investigation

Volumn 88, Issue 10, 2008, Pages 1110-1120

  Weber, Christopher R ^a   Nalle, Sam C ^a   Tretiakova, Maria ^a   Rubin, David T ^a   Turner, Jerrold R ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Claudin; Colon cancer; Dysplasia; Inflammatory bowel disease; Occludin; Tight junction

Indexed keywords

BETA CATENIN; CLAUDIN 1; CLAUDIN 2; CLAUDIN 4; OCCLUDIN;

ADENOMA; ADULT; AGED; ARTICLE; BIOPSY; CLINICAL ARTICLE; COLITIS; DISEASE COURSE; DISEASE MARKER; DYSPLASIA; ENTERITIS; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NEOPLASM; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING; TIGHT JUNCTION; TRANSCRIPTION INITIATION;

ADENOMA; AGED; AGED, 80 AND OVER; BETA CATENIN; COHORT STUDIES; COLITIS, ULCERATIVE; COLONIC NEOPLASMS; CROHN DISEASE; FEMALE; HUMANS; INFLAMMATION; MALE; MEMBRANE PROTEINS; MIDDLE AGED; UP-REGULATION;

EID: 52649123158     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2008.78     Document Type: Article

References (43)

1. Schmitz H, Barmeyer C, Fromm M, et al. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis,. Gastroenterology 1999;116:301-309.
2. Clayburgh DR, Shen L, Turner JR. A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 2004;84:282-291.
3. Prasad S, Mingrino R, Kaukinen K, et al. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Invest 2005;85:1139-1162.
4. Zeissig S, Burgel N, Gunzel D, et al. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 2007;56:61-72.
5. Weber CR, Turner JR. Inflammatory bowel disease: is it really just another break in the wall? Gut 2007;56:6-8.
6. Clayburgh DR, Barrett TA, Tang Y, et al. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activationinduced diarrhea in vivo. J Clin Invest 2005;115:2702-2715.
7. Graham WV, Wang F, Clayburgh DR, et al. Tumor necrosis factor-induced long myosin light chain kinase transcription is regulated by differentiation-dependent signaling events. Characterization of the human long myosin light chain kinase promoter. J Biol Chem 2006;281:26205-26215.
8. Heller F, Florian P, Bojarski C, et al. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005;129:550-564.
9. MacDonald TT, Hutchings P, Choy M-Y, et al. Tumour necrosis factor-alpha and interferon-gamma production measured at the single cell level in normal and inflamed human intestine. Clin Exp Immunol 1990;81:301-305.
10. Mankertz J, Tavalali S, Schmitz H, et al. Expression from the human occludin promoter is affected by tumor necrosis factor alpha and interferon gamma. J Cell Sci 2000;113(Part 11):2085-2090.
11. Wang F, Graham WV, Wang Y, et al. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 2005;166:409-419.
12. Wang F, Schwarz BT, Graham WV, et al. IFN-gamma-induced TNFR2 expression is required for TNF-dependent intestinal epithelial barrier dysfunction. Gastroenterology 2006;131:1153-1163.
13. Dhawan P, Singh AB, Deane NG, et al. Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J Clin Invest 2005;115:1765-1776.
14. Matter K, Balda MS. Signalling to and from tight junctions. Nat Rev Mol Cell Biol 2003;4:225-236.
15. Hewitt KJ, Agarwal R, Morin PJ. The claudin gene family: expression in normal and neoplastic tissues. BMC Cancer 2006;6:186.
16. Kominsky SL. Claudins: emerging targets for cancer therapy. Expert Rev Mol Med 2006;8:1-11.
17. Soini Y. Expression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours. Histopathology 2005;46:551-560.
18. Swisshelm K, Macek R, Kubbies M. Role of claudins in tumorigenesis. Adv Drug Deliv Rev 2005;57:919-928.
19. Morin PJ. Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res 2005;65:9603-9606.
20. Michl P, Barth C, Buchholz M, et al. Claudin-4 expression decreases invasiveness and metastatic potential of pancreatic cancer. Cancer Res 2003;63:6265-6271.
21. Gyorffy H, Holczbauer A, Nagy P, et al. Claudin expression in Barrett's esophagus and adenocarcinoma. Virchows Arch 2005;447:961-968.
22. Lee SK, Moon J, Park SW, et al. Loss of the tight junction protein claudin 4 correlates with histological growth-pattern and differentiation in advanced gastric adenocarcinoma. Oncol Rep 2005;13:193-199.
23. Grone J, Weber B, Staub E, et al. Differential expression of genes encoding tight junction proteins in colorectal cancer: frequent dysregulation of claudin-1, -8 and -12. Int J Colorectal Dis 2007;22:651-659.
24. Kinugasa T, Huo Q, Higashi D, et al. Selective up-regulation of claudin-1 and claudin-2 in colorectal cancer. Anticancer Res 2007;27:3729-3734.
25. Resnick MB, Konkin T, Routhier J, et al. Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Mod Pathol 2005;18:511-518.
26. Aung PP, Mitani Y, Sanada Y, et al. Differential expression of claudin-2 in normal human tissues and gastrointestinal carcinomas. Virchows Arch 2006;448:428-434.
27. Hahn-Stromberg V, Edvardsson H, Bodin L, et al. Disturbed expression of E-cadherin, beta-catenin and tight junction proteins in colon carcinoma is unrelated to growth pattern and genetic polymorphisms. APMIS 2008;116:253-262.
28. Miwa N, Furuse M, Tsukita S, et al. Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res 2001;12:469-476.
29. Mankertz J, Hillenbrand B, Tavalali S, et al. Functional crosstalk between Wnt signaling and Cdx-related transcriptional activation in the regulation of the claudin-2 promoter activity. Biochem Biophys Res Commun 2004;314:1001-1007.
30. Eaden J. Review article: colorectal carcinoma and inflammatory bowel disease. Aliment Pharmacol Ther 2004;20(Suppl 4):24-30.
31. von Roon AC, Reese G, Teare J, et al. The risk of cancer in patients with Crohn's disease. Dis Colon Rectum 2007;50:839-855.
32. Bernstein CN, Blanchard JF, Kliewer E, et al. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 2001;91:854-862.
33. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-G17.
34. 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.
35. Kumar NB, Nostrant TT, Appelman HD. The histopathologic spectrum of acute self-limited colitis (acute infectious-type colitis). Am J Surg Pathol 1982;6:523-529.
36. Surawicz CM. The role of rectal biopsy in infectious colitis. Am J Surg Pathol 1988;12(Suppl 1):82-88.
37. Surawicz CM, Belic L. Rectal biopsy helps to distinguish acute self-limited colitis from idiopathic inflammatory bowel disease. Gastroenterol 1984;86:104-113.
38. Surawicz CM, Haggitt RC, Husseman M, et al. Mucosal biopsy diagnosis of colitis: acute self-limited colitis and idiopathic inflammatory bowel disease. Gastroenterol 1994;107:755-763.
39. Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 2006;169:1901-1909.
40. Blair SA, Kane SV, Clayburgh DR, et al. Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest 2006;86:191-201.
41. Vagefi PA, Longo WE. Colorectal cancer in patients with inflammatory bowel disease. Clin Colorectal Cancer 2005;4:313-319.
42. Fuss IJ, Heller F, Boirivant M, et al. Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest 2004;113:1490-1497.
43. Shiou SR, Singh AB, Moorthy K, et al. Smad4 regulates claudin-1 expression in a transforming growth factor-beta-independent manner in colon cancer cells. Cancer Res 2007;67:1571-1579.