Epithelial tight junctional changes in colorectal cancer tissues

TheScientificWorldJournal

Volumn 11, Issue , 2011, Pages 826-841

  Wang, Xuexuan ^a   Tully, Owen ^a   Ngo, Benjamin ^a   Zitin, Marc ^a   Mullin, James M ^a  

^a LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Cancer; Cancer prognosis; Claudin; Colon; Inflammatory bowel disease; Occludin; Tight junction

Indexed keywords

CLAUDIN 1; CLAUDIN 12; CLAUDIN 3; CLAUDIN 4; CLAUDIN 7; CLAUDIN 8; JUNCTIONAL ADHESION PROTEIN; MEMBRANE PROTEIN; OCCLUDIN; PROTEIN DERIVATIVE; TRICELLULIN; UNCLASSIFIED DRUG;

CANCER DIAGNOSIS; CANCER SCREENING; COLORECTAL CANCER; CROHN DISEASE; DISEASE ASSOCIATION; ENTERITIS; HISTOPATHOLOGY; HUMAN; NONHUMAN; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TIGHT JUNCTION; ULCERATIVE COLITIS; UPREGULATION;

CLAUDINS; COLORECTAL NEOPLASMS; EPITHELIUM; HUMANS; INFLAMMATORY BOWEL DISEASES; PROGNOSIS; TIGHT JUNCTIONS;

ANIMALIA;

EID: 79955619149     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/tsw.2011.86     Document Type: Review

References (73)

1. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Murray, T., and Thun, M.J. (2008) Cancer statistics, 2008. CA Cancer J. Clin. 58, 71-96. (Pubitemid 351521864)
2. Levin, B., Lieberman, D.A., McFarland, B., Andrews, K.S., Brooks, D., Bond, J., Dash, C., Giardiello, F.M., Glick, S., Johnson, D., Johnson, C.D., Levin, T.R., Pickhardt, P.J., Rex, D.K., Smith, R.A., Thorson, A., and Winawer, S.J. (2008) Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 134, 1570-1595.
3. Rex, D.K., Cutler, C.S., Lemmel, G.T., Rahmani, E.Y., Clark, D.W., Helper, D.J., Lehman, G.A., and Mark, D.G. (1997) Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology 112, 24-28. (Pubitemid 27008981)
4. Meissner, H.I., Breen, N., Klabunde, C.N., and Vernon, S.W. (2006) Patterns of colorectal cancer screening uptake among men and women in the United States. Cancer Epidemiol. Biomarkers Prev. 15, 389-394. (Pubitemid 43342192)
5. Lal-Nag, M. and Morin, P.J. (2009) The claudins. Genome Biol. 10, 235.
6. Balda, M.S. and Matter, K. (2009) Tight junctions and the regulation of gene expression. Biochim. Biophys. Acta 1788, 761-767.
7. Forster, C. (2008) Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 130, 55-70.
8. Mullin, J.M., Agostino, N., Rendon-Huerta, E., and Thornton, J.J. (2005) Keynote review: epithelial and endothelial barriers in human disease. Drug Discov. Today 10, 395-408. (Pubitemid 40450271)
9. Brennan, K., Offiah, G., McSherry, E.A., and Hopkins, A.M. (2010) Tight junctions: a barrier to the initiation and progression of breast cancer? J. Biomed. Biotechnol. 2010, 460607.
10. Soler, A.P., Miller, R.D., Laughlin, K.V., Carp, N.Z., Klurfeld, D.M., and Mullin, J.M. (1999) Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis 20, 1425-1431. (Pubitemid 29385425)
11. Mullin, J.M., Snock, K.V., Shurina, R.D., Noe, J., George, K., Misner, L., Imaizumi, S., and O'Brien, T.G. (1992) Effects of acute vs. chronic phorbol ester exposure on transepithelial permeability and epithelial morphology. J. Cell Physiol. 152, 35-47.
12. Mullin, J.M., Valenzano, M.C., Trembeth, S., Allegretti, P.D., Verrecchio, J.J., Schmidt, J.D., Jain, V., Meddings, J.B., Mercogliano, G., and Thornton, J.J. (2006) Transepithelial leak in Barrett's esophagus. Dig. Dis. Sci. 51, 2326-2336.
13. Balk, S.P., Ko, Y.J., and Bubley, G.J. (2003) Biology of prostate-specific antigen. J. Clin. Oncol. 21, 383-391. (Pubitemid 46606169)
14. Mullin, J.M. (2004) Epithelial barriers, compartmentation, and cancer. Sci. STKE 2004, pe2.
15. Gregory, H., Walsh, S., and Hopkins, C.R. (1979) The identification of urogastrone in serum, saliva, and gastric juice. Gastroenterology 77, 313-318. (Pubitemid 9215618)
16. Bishop, W.P. and Wen, J.T. (1994) Regulation of Caco-2 cell proliferation by basolateral membrane epidermal growth factor receptors. Am. J. Physiol. 267, G892-900.
17. Singh, A.B., Sharma, A., and Dhawan, P. (2010) Claudin family of proteins and cancer: an overview. J. Oncol. 2010, 541957.
18. Li, D. and Mrsny, R.J. (2000) Oncogenic Raf-1 disrupts epithelial tight junctions via downregulation of occludin. J. Cell Biol. 148, 791-800.
19. Dhawan, P., Singh, A.B., Deane, N.G., No, Y., Shiou, S.R., Schmidt, C., Neff, J., Washington, M.K., and Beauchamp, R.D. (2005) Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J. Clin. Invest. 115, 1765-1776. (Pubitemid 40979715)
20. Mullin, J.M. and O'Brien, T.G. (1986) Effects of tumor promoters on LLC-PK1 renal epithelial tight junctions and transepithelial fluxes. Am. J. Physiol. 251, C597-602.
21. Mullin, J.M. (1997) Potential interplay between luminal growth factors and increased tight junction permeability in epithelial carcinogenesis. J. Exp. Zool. 279, 484-489.
22. Miwa, N., Furuse, M., Tsukita, S., Niikawa, N., Nakamura, Y., and Furukawa, Y. (2001) Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol. Res. 12, 469-476. (Pubitemid 33791807)
23. Grone, J., Weber, B., Staub, E., Heinze, M., Klaman, I., Pilarsky, C., Hermann, K., Castanos-Velez, E., Ropcke, S., Mann, B., Rosenthal, A., and Buhr, H.J. (2007) Differential expression of genes encoding tight junction proteins in colorectal cancer: frequent dysregulation of claudin-1, -8 and -12. Int. J. Colorectal Dis. 22, 651-659. (Pubitemid 47097036)
24. Huo, Q., Kinugasa, T., Wang, L., Huang, J., Zhao, J., Shibaguchi, H., Kuroki, M., Tanaka, T., Yamashita, Y., Nabeshima, K., and Iwasaki, H. (2009) Claudin-1 protein is a major factor involved in the tumorigenesis of colorectal cancer. Anticancer Res. 29, 851-857.
25. Wodarz, A. (2000) Tumor suppressors: linking cell polarity and growth control. Curr. Biol. 10, R624-626.
26. Martin, T.A. and Jiang, W.G. (2001) Tight junctions and their role in cancer metastasis. Histol. Histopathol. 16, 1183-1195. (Pubitemid 32994462)
27. Kinzler, K.W. and Vogelstein, B. (1996) Lessons from hereditary colorectal cancer. Cell 87, 159-170. (Pubitemid 26358996)
28. Matsuda, Y., Semba, S., Ueda, J., Fuku, T., Hasuo, T., Chiba, H., Sawada, N., Kuroda, Y., and Yokozaki, H. (2007) Gastric and intestinal claudin expression at the invasive front of gastric carcinoma. Cancer Sci. 98, 1014-1019. (Pubitemid 46865385)
29. Ueda, J., Semba, S., Chiba, H., Sawada, N., Seo, Y., Kasuga, M., and Yokozaki, H. (2007) Heterogeneous expression of claudin-4 in human colorectal cancer: decreased claudin-4 expression at the invasive front correlates cancer invasion and metastasis. Pathobiology 74, 32-41. (Pubitemid 46745168)
30. Miyaki, M. and Kuroki, T. (2003) Role of Smad4 (DPC4) inactivation in human cancer. Biochem. Biophys. Res. Commun. 306, 799-804. (Pubitemid 36776201)
31. Miyaki, M., Iijima, T., Konishi, M., Sakai, K., Ishii, A., Yasuno, M., Hishima, T., Koike, M., Shitara, N., Iwama, T., Utsunomiya, J., Kuroki, T., and Mori, T. (1999) Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis. Oncogene 18, 3098-3103. (Pubitemid 29261230)
32. Hahn, S.A., Schutte, M., Hoque, A.T., Moskaluk, C.A., da Costa, L.T., Rozenblum, E., Weinstein, C.L., Fischer, A., Yeo, C.J., Hruban, R.H., and Kern, S.E. (1996) DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271, 350-353.
33. Reinacher-Schick, A., Baldus, S.E., Romdhana, B., Landsberg, S., Zapatka, M., Monig, S.P., Holscher, A.H., Dienes, H.P., Schmiegel, W., and Schwarte-Waldhoff, I. (2004) Loss of Smad4 correlates with loss of the invasion suppressor E-cadherin in advanced colorectal carcinomas. J. Pathol. 202, 412-420. (Pubitemid 38456159)
34. Shiou, S.R., Singh, A.B., Moorthy, K., Datta, P.K., Washington, M.K., Beauchamp, R.D., and Dhawan, P. (2007) Smad4 regulates claudin-1 expression in a transforming growth factor-beta-independent manner in colon cancer cells. Cancer Res. 67, 1571-1579. (Pubitemid 46383381)
35. Halder, S.K., Beauchamp, R.D., and Datta, P.K. (2005) Smad7 induces tumorigenicity by blocking TGF-beta-induced growth inhibition and apoptosis. Exp. Cell Res. 307, 231-246. (Pubitemid 40732749)
36. Halder, S.K., Rachakonda, G., Deane, N.G., and Datta, P.K. (2008) Smad7 induces hepatic metastasis in colorectal cancer. Br. J. Cancer 99, 957-965.
37. Mees, S.T., Mennigen, R., Spieker, T., Rijcken, E., Senninger, N., Haier, J., and Bruewer, M. (2009) Expression of tight and adherens junction proteins in ulcerative colitis associated colorectal carcinoma: upregulation of claudin-1, claudin-3, claudin-4, and beta-catenin. Int. J. Colorectal Dis. 24, 361-368.
38. Weber, C.R., Nalle, S.C., Tretiakova, M., Rubin, D.T., and Turner, J.R. (2008) Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab. Invest. 88, 1110-1120.
39. Oshima, T., Miwa, H., and Joh, T. (2008) Changes in the expression of claudins in active ulcerative colitis. J. Gastroenterol. Hepatol. 23(Suppl 2), S146-150.
40. Gupta, R.B., Harpaz, N., Itzkowitz, S., Hossain, S., Matula, S., Kornbluth, A., Bodian, C., and Ullman, T. (2007) Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology 133, 1099-1105; quiz 1340-1091.
41. Ribeiro, M.B., Greenstein, A.J., Sachar, D.B., Barth, J., Balasubramanian, S., Harpaz, N., Heimann, T.M., and Aufses, A.H., Jr. (1996) Colorectal adenocarcinoma in Crohn's disease. Ann. Surg. 223, 186-193.
42. Resnick, M.B., Konkin, T., Routhier, J., Sabo, E., and Pricolo, V.E. (2005) Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Mod. Pathol. 18, 511-518. (Pubitemid 40478114)
43. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K., and Tsukita, S. (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141, 1539-1550. (Pubitemid 28309169)
44. Hewitt, K.J., Agarwal, R., and Morin, P.J. (2006) The claudin gene family: expression in normal and neoplastic tissues. BMC Cancer 6, 186.
45. Aung, P.P., Mitani, Y., Sanada, Y., Nakayama, H., Matsusaki, K., and Yasui, W. (2006) Differential expression of claudin-2 in normal human tissues and gastrointestinal carcinomas. Virchows Arch. 448, 428-434.
46. Darido, C., Buchert, M., Pannequin, J., Bastide, P., Zalzali, H., Mantamadiotis, T., Bourgaux, J.F., Garambois, V., Jay, P., Blache, P., Joubert, D., and Hollande, F. (2008) Defective claudin-7 regulation by Tcf-4 and Sox-9 disrupts the polarity and increases the tumorigenicity of colorectal cancer cells. Cancer Res. 68, 4258-4268.
47. Hahn-Stromberg, V., Edvardsson, H., Bodin, L., and Franzen, L. (2009) Tumor volume of colon carcinoma is related to the invasive pattern but not to the expression of cell adhesion proteins. APMIS 117, 205-211.
48. Soini, Y. (2005) Expression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours. Histopathology 46, 551-560.
49. Rangel, L.B., Agarwal, R., D'Souza, T., Pizer, E.S., Alo, P.L., Lancaster, W.D., Gregoire, L., Schwartz, D.R., Cho, K.R., and Morin, P.J. (2003) Tight junction proteins claudin-3 and claudin-4 are frequently overexpressed in ovarian cancer but not in ovarian cystadenomas. Clin. Cancer Res. 9, 2567-2575. (Pubitemid 36842098)
50. Nichols, L.S., Ashfaq, R., and Iacobuzio-Donahue, C.A. (2004) Claudin 4 protein expression in primary and metastatic pancreatic cancer: support for use as a therapeutic target. Am. J. Clin. Pathol. 121, 226-230. (Pubitemid 38140127)
51. de Oliveira, S.S., de Oliveira, I.M., De Souza, W., and Morgado-Diaz, J.A. (2005) Claudins upregulation in human colorectal cancer. FEBS Lett. 579, 6179-6185. (Pubitemid 41546266)
52. Furuse, M., Sasaki, H., and Tsukita, S. (1999) Manner of interaction of heterogeneous claudin species within and between tight junction strands. J. Cell Biol. 147, 891-903.
53. Sato, N., Fukushima, N., Maitra, A., Iacobuzio-Donahue, C.A., van Heek, N.T., Cameron, J.L., Yeo, C.J., Hruban, R.H., and Goggins, M. (2004) Gene expression profiling identifies genes associated with invasive intraductal papillary mucinous neoplasms of the pancreas. Am. J. Pathol. 164, 903-914. (Pubitemid 38235472)
54. Hough, C.D., Sherman-Baust, C.A., Pizer, E.S., Montz, F.J., Im, D.D., Rosenshein, N.B., Cho, K.R., Riggins, G.J., and Morin, P.J. (2000) Large-scale serial analysis of gene expression reveals genes differentially expressed in ovarian cancer. Cancer Res. 60, 6281-6287.
55. Ladwein, M., Pape, U.F., Schmidt, D.S., Schnolzer, M., Fiedler, S., Langbein, L., Franke, W.W., Moldenhauer, G., and Zoller, M. (2005) The cell-cell adhesion molecule EpCAM interacts directly with the tight junction protein claudin-7. Exp. Cell Res. 309, 345-357. (Pubitemid 41317358)
56. Li, W.Y., Huey, C.L., and Yu, A.S. (2004) Expression of claudin-7 and -8 along the mouse nephron. Am. J. Physiol. Renal Physiol. 286, F1063-1071.
57. Blackman, B., Russell, T., Nordeen, S.K., Medina, D., and Neville, M.C. (2005) Claudin 7 expression and localization in the normal murine mammary gland and murine mammary tumors. Breast Cancer Res. 7, R248-255.
58. Fujita, H., Chiba, H., Yokozaki, H., Sakai, N., Sugimoto, K., Wada, T., Kojima, T., Yamashita, T., and Sawada, N. (2006) Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine. J. Histochem. Cytochem. 54, 933-944. (Pubitemid 44106871)
59. Kominsky, S.L., Argani, P., Korz, D., Evron, E., Raman, V., Garrett, E., Rein, A., Sauter, G., Kallioniemi, O.P., and Sukumar, S. (2003) Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 22, 2021-2033. (Pubitemid 36523639)
60. Lioni, M., Brafford, P., Andl, C., Rustgi, A., El-Deiry, W., Herlyn, M., and Smalley, K.S. (2007) Dysregulation of claudin-7 leads to loss of E-cadherin expression and the increased invasion of esophageal squamous cell carcinoma cells. Am. J. Pathol. 170, 709-721. (Pubitemid 47342407)
61. Choi, Y.D., Kim, K.S., Ryu, S., Park, Y., Cho, N.H., Rha, S.H., Jang, J.J., Ro, J.Y., Juhng, S.W., and Choi, C. (2007) Claudin-7 is highly expressed in chromophobe renal cell carcinoma and renal oncocytoma. J. Korean Med. Sci. 22, 305-310.
62. Johnson, A.H., Frierson, H.F., Zaika, A., Powell, S.M., Roche, J., Crowe, S., Moskaluk, C.A., and El-Rifai, W. (2005) Expression of tight-junction protein claudin-7 is an early event in gastric tumorigenesis. Am. J. Pathol. 167, 577-584. (Pubitemid 43026111)
63. Bastide, P., Darido, C., Pannequin, J., Kist, R., Robine, S., Marty-Double, C., Bibeau, F., Scherer, G., Joubert, D., Hollande, F., Blache, P., and Jay, P. (2007) Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J. Cell Biol. 178, 635-648. (Pubitemid 47267275)
64. Kuhn, S., Koch, M., Nubel, T., Ladwein, M., Antolovic, D., Klingbeil, P., Hildebrand, D., Moldenhauer, G., Langbein, L., Franke, W.W., Weitz, J., and Zoller, M. (2007) A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol. Cancer Res. 5, 553-567. (Pubitemid 46985046)
65. Basak, S., Speicher, D., Eck, S., Wunner, W., Maul, G., Simmons, M.S., and Herlyn, D. (1998) Colorectal carcinoma invasion inhibition by CO17-1A/GA733 antigen and its murine homologue. J. Natl. Cancer Inst. 90, 691-697. (Pubitemid 28222143)
66. Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., and Tsukita, S. (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123, 1777-1788. (Pubitemid 24012933)
67. Tsukita, S., Furuse, M., and Itoh, M. (2001) Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293. (Pubitemid 33676971)
68. Wang, Z., Mandell, K.J., Parkos, C.A., Mrsny, R.J., and Nusrat, A. (2005) The second loop of occludin is required for suppression of Raf1-induced tumor growth. Oncogene 24, 4412-4420. (Pubitemid 40961764)
69. Kimura, Y., Shiozaki, H., Hirao, M., Maeno, Y., Doki, Y., Inoue, M., Monden, T., Ando-Akatsuka, Y., Furuse, M., Tsukita, S., and Monden, M. (1997) Expression of occludin, tight-junction-associated protein, in human digestive tract. Am. J. Pathol. 151, 45-54. (Pubitemid 27283956)
70. Tobioka, H., Isomura, H., Kokai, Y., Tokunaga, Y., Yamaguchi, J., and Sawada, N. (2004) Occludin expression decreases with the progression of human endometrial carcinoma. Hum. Pathol. 35, 159-164. (Pubitemid 38240897)
71. Zeissig, S., Burgel, N., Gunzel, D., Richter, J., Mankertz, J., Wahnschaffe, U., Kroesen, A.J., Zeitz, M., Fromm, M., and Schulzke, J.D. (2007) 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 56, 61-72. (Pubitemid 46044890)
72. Laukoetter, M.G., Nava, P., Lee, W.Y., Severson, E.A., Capaldo, C.T., Babbin, B.A., Williams, I.R., Koval, M., Peatman, E., Campbell, J.A., Dermody, T.S., Nusrat, A., and Parkos, C.A. (2007) JAM-A regulates permeability and inflammation in the intestine in vivo. J. Exp. Med. 204, 3067-3076.
73. Krug, S.M., Amasheh, S., Richter, J.F., Milatz, S., Gunzel, D., Westphal, J.K., Huber, O., Schulzke, J.D., and Fromm, M. (2009) Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol. Biol. Cell 20, 3713-3724.