Claudin-1 promotes TNF-α-induced epithelial-mesenchymal transition and migration in colorectal adenocarcinoma cells

Experimental Cell Research

Volumn 349, Issue 1, 2016, Pages 119-127

  Bhat, Ajaz A ^b   Ahmad, Rizwan ^a   Uppada, SrijayaPrakash B ^a   Singh, Amar B ^a   Dhawan, Punita ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Claudin 1; EMT; Migration; TNF alpha

Indexed keywords

BETA CATENIN; CLAUDIN 1; CLAUDIN 2; CLAUDIN 3; CLAUDIN 4; CLAUDIN 7; MITOGEN ACTIVATED PROTEIN KINASE 1; OCCLUDIN; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SNAIL; TUMOR NECROSIS FACTOR; UVOMORULIN; VIMENTIN; MITOGEN ACTIVATED PROTEIN KINASE; TUMOR MARKER;

ARTICLE; CARCINOGENESIS; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL MIGRATION ASSAY; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HT 29 CELL LINE; HUMAN; HUMAN CELL; INFLAMMATION; INTRACELLULAR SIGNALING; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; UPREGULATION; WOUND HEALING ASSAY; ADENOCARCINOMA; CELL MOTION; COLORECTAL TUMOR; DRUG EFFECTS; GENE SILENCING; HT-29 CELL LINE; METABOLISM; PATHOLOGY; PHOSPHORYLATION;

ADENOCARCINOMA; BIOMARKERS, TUMOR; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CLAUDIN-1; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE KNOCKDOWN TECHNIQUES; HT29 CELLS; HUMANS; PHOSPHORYLATION; SRC-FAMILY KINASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84994121222     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2016.10.005     Document Type: Article

References (49)

1. [1] Dhawan, P., Singh, A.B., Deane, N.G., No, Y., Shiou, S.R., Schmidt, C., et al. Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J. Clin. Investig. 115:7 (2005), 1765–1776.
2. [2] Kinugasa, T., Akagi, Y., Yoshida, T., Ryu, Y., Shiratuchi, I., Ishibashi, N., et al. Increased claudin-1 protein expression contributes to tumorigenesis in ulcerative colitis-associated colorectal cancer. Anticancer Res. 30:8 (2010), 3181–3186.
3. [3] Suren, D., Yildirim, M., Kaya, V., Alikanoglu, A.S., Bulbuller, N., Yildiz, M., et al. Loss of tight junction proteins (Claudin 1, 4, and 7) correlates with aggressive behavior in colorectal carcinoma. Med. Sci. Monit. 20 (2014), 1255–1262.
4. [4] Pope, J.L., Ahmad, R., Bhat, A.A., Washington, M.K., Singh, A.B., Dhawan, P., Claudin-1 overexpression in intestinal epithelial cells enhances susceptibility to adenamatous polyposis coli-mediated colon tumorigenesis. Mol. Cancer, 13, 2014, 167.
5. [5] Nakagawa, S., Miyoshi, N., Ishii, H., Mimori, K., Tanaka, F., Sekimoto, M., et al. Expression of CLDN1 in colorectal cancer: a novel marker for prognosis. Int. J. Oncol. 39:4 (2011), 791–796.
6. [6] Engel, M.A., Neurath, M.F., New pathophysiological insights and modern treatment of IBD. J. Gastroenterol. 45:6 (2010), 571–583.
7. [7] Grivennikov, S.I., Inflammation and colorectal cancer: colitis-associated neoplasia. Semin. Immunopathol. 35:2 (2013), 229–244.
8. [8] Weber, C.R., Nalle, S.C., Tretiakova, M., Rubin, D.T., Turner, J.R., Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Investig. 88:10 (2008), 1110–1120.
9. [9] Balkwill, F., TNF-alpha in promotion and progression of cancer. Cancer Metastasis – Rev. 25:3 (2006), 409–416.
10. [10] Popivanova, B.K., Kitamura, K., Wu, Y., Kondo, T., Kagaya, T., Kaneko, S., et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J. Clin. Investig. 118:2 (2008), 560–570.
11. [11] Grivennikov, S.I., Karin, M., Inflammatory cytokines in cancer: tumour necrosis factor and interleukin 6 take the stage. Ann. Rheum. Dis. 70:Suppl 1 (2011), S104–S108.
12. [12] Balkwill, F., Tumour necrosis factor and cancer. Nat. Rev. Cancer 9:5 (2009), 361–371.
13. [13] Moore, R.J., Owens, D.M., Stamp, G., Arnott, C., Burke, F., East, N., et al. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med. 5:7 (1999), 828–831.
14. [14] Arnott, C.H., Scott, K.A., Moore, R.J., Robinson, S.C., Thompson, R.G., Balkwill, F.R., Expression of both TNF-alpha receptor subtypes is essential for optimal skin tumour development. Oncogene 23:10 (2004), 1902–1910.
15. [15] Kitakata, H., Nemoto-Sasaki, Y., Takahashi, Y., Kondo, T., Mai, M., Mukaida, N., Essential roles of tumor necrosis factor receptor p55 in liver metastasis of intrasplenic administration of colon 26 cell. Cancer Res. 62:22 (2002), 6682–6687.
16. [16] Orosz, P., Echtenacher, B., Falk, W., Ruschoff, J., Weber, D., Mannel, D.N., Enhancement of experimental metastasis by tumor necrosis factor. J. Exp. Med. 177:5 (1993), 1391–1398.
17. [17] Balkwill, F., Tumor necrosis factor or tumor promoting factor. Cytokine Growth Factor Rev. 13:2 (2002), 135–141.
18. [18] Bates, R.C., Mercurio, A.M., Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Mol. Biol. Cell 14:5 (2003), 1790–1800.
19. [19] Bruewer, M., Luegering, A., Kucharzik, T., Parkos, C.A., Madara, J.L., Hopkins, A.M., et al. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanism. J. Immunol. 171:11 (2003), 6164–6172.
20. [20] Coyne, C.B., Vanhook, M.K., Gambling, T.M., Carson, J.L., Boucher, R.C., Johnson, L.G., Regulation of airway tight junctions by proinflammatory cytokine. Mol. Biol. Cell 13:9 (2002), 3218–3234.
21. [21] Bhat, A.A., Pope, J.L., Smith, J.J., Ahmad, R., Chen, X., Washington, M.K., et al. Claudin-7 expression induces mesenchymal to epithelial transformation (MET) to inhibit colon tumorigenesis. Oncogene 34:35 (2015), 4570–4580.
22. [22] Pope, J.L., Bhat, A.A., Sharma, A., Ahmad, R., Krishnan, M., Washington, M.K., et al. Claudin-1 regulates intestinal epithelial homeostasis through the modulation of Notch-signalling. Gut 63:4 (2014), 622–634.
23. [23] Singh, A.B., Harris, R.C., Epidermal growth factor receptor activation differentially regulates claudin expression and enhances transepithelial resistance in Madin-Darby canine kidney cell. J. Biol. Chem. 279:5 (2004), 3543–3552.
24. [24] Bhat, A.A., Sharma, A., Pope, J., Krishnan, M., Washington, M.K., Singh, A.B., et al. Caudal homeobox protein Cdx-2 cooperates with Wnt pathway to regulate claudin-1 expression in colon cancer cell. PLoS One, 7(6), 2012, e37174.
25. [25] Dhawan, P., Ahmad, R., Chaturvedi, R., Smith, J.J., Midha, R., Mittal, M.K., et al. Claudin-2 expression increases tumorigenicity of colon cancer cells: role of epidermal growth factor receptor activation. Oncogene 30:29 (2011), 3234–3247.
26. [26] Nishiyama, R., Sakaguchi, T., Kinugasa, T., Gu, X., MacDermott, R.P., Podolsky, D.K., et al. Interleukin-2 receptor beta subunit-dependent and -independent regulation of intestinal epithelial tight junction. J. Biol. Chem. 276:38 (2001), 35571–35580.
27. [27] Baker, O.J., Camden, J.M., Redman, R.S., Jones, J.E., Seye, C.I., Erb, L., et al. Proinflammatory cytokines tumor necrosis factor-alpha and interferon-gamma alter tight junction structure and function in the rat parotid gland Par-C10 cell line. Am. J. Physiol. Cell Physiol. 295:5 (2008), C1191–C1201.
28. [28] Huo, Q., Kinugasa, T., Wang, L., Huang, J., Zhao, J., Shibaguchi, H., et al. Claudin-1 protein is a major factor involved in the tumorigenesis of colorectal cancer. Anticancer Res. 29:3 (2009), 851–857.
29. [29] Wang, K., Karin, M., Chapter five – tumor-elicited inflammation and colorectal cancer. Xiang-Yang, W., Paul, B.F., (eds.) Advances in Cancer Research, 128, 2015, Academic Press, 173–196.
30. [30] Ben-Neriah, Y., Karin, M., Inflammation meets cancer, with NF-[kappa]B as the matchmaker. Nat. Immunol. 12:8 (2011), 715–723.
31. [31] Terzić, J., Grivennikov, S., Karin, E., Karin, M., Inflammation and colon cancer. Gastroenterology, 138(6), 2010 (2101-14.e5).
32. [32] Turner, J.R., Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9:11 (2009), 799–809.
33. [33] Peyrin-Biroulet, L., Anti-TNF therapy in inflammatory bowel diseases: a huge review. Minerva Gastroenterol. Dietol. 56:2 (2010), 233–243.
34. [34] Kinugasa, T., Akagi, Y., Ochi, T., Tanaka, N., Kawahara, A., Ishibashi, Y., et al. Increased claudin-1 protein expression in hepatic metastatic lesions of colorectal cancer. Anticancer Res. 32:6 (2012), 2309–2314.
35. [35] Suh, Y., Yoon, C.H., Kim, R.K., Lim, E.J., Oh, Y.S., Hwang, S.G., et al. Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cell. Oncogene 32:41 (2013), 4873–4882.
36. [36] Stebbing, J., Filipovic, A., Giamas, G., Claudin-1 as a promoter of EMT in hepatocellular carcinom. Oncogene 32:41 (2013), 4871–4872.
37. [37] Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., et al. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol. 156:6 (2002), 1099–1111.
38. [38] Singh, A.B., Sharma, A., Dhawan, P., Claudin-1 expression confers resistance to anoikis in colon cancer cells in a Src-dependent manner. Carcinogenesis 33:12 (2012), 2538–2547.
39. [39] Smith, B.N., Burton, L.J., Henderson, V., Randle, D.D., Morton, D.J., Smith, B.A., et al. Snail promotes epithelial mesenchymal transition in breast cancer cells in part via activation of nuclear ERK. PLoS One, 9(8), 2014, e104987.
40. [40] Amoozadeh, Y., Dan, Q., Xiao, J., Waheed, F., Szászi, K., Tumor necrosis factor-α induces a biphasic change in claudin-2 expression in tubular epithelial cells: role in barrier function. Am. J. Physiol. – Cell Physiol. 309:1 (2015), C38–C50.
41. [41] Shiozaki, A., Shimizu, H., Ichikawa, D., Konishi, H., Komatsu, S., Kubota, T., et al. Claudin 1 mediates tumor necrosis factor alpha-induced cell migration in human gastric cancer cell. World J. Gastroenterol.: WJG 20:47 (2014), 17863–17876.
42. [42] Iitaka, D., Moodley, S., Shimizu, H., Bai, X.-H., Liu, M., PKCδ–iPLA2–PGE2–PPARγ signaling cascade mediates TNF-α induced Claudin 1 expression in human lung carcinoma cell. Cell. Signal. 27:3 (2015), 568–577.
43. [43] Shiozaki, A., Bai, X.-h., Shen-Tu, G., Moodley, S., Takeshita, H., Fung, S.-Y., et al. Claudin 1 mediates TNFα-induced gene expression and cell migration in human lung carcinoma cell. PLoS ONE, 7(5), 2012, e38049.
44. [44] Chua, H.L., Bhat-Nakshatri, P., Clare, S.E., Morimiya, A., Badve, S., Nakshatri, H., NF-[kappa]B represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-. Oncogene 26:5 (2006), 711–724.
45. [45] Ikenouchi, J., Matsuda, M., Furuse, M., Tsukita, S., Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by snail. J. Cell Sci. 116:10 (2003), 1959–1967.
46. [46] Ohkubo, T., Ozawa, M., The transcription factor snail downregulates the tight junction components independently of E-cadherin downregulation. J. Cell Sci. 117:9 (2004), 1675–1685.
47. [47] Baker, O.J., Camden, J.M., Redman, R.S., Jones, J.E., Seye, C.I., Erb, L., et al. Proinflammatory cytokines tumor necrosis factor-α and interferon-γ alter tight junction structure and function in the rat parotid gland Par-C10 cell line. Am. J. Physiol. – Cell Physiol. 295:5 (2008), C1191–C1201.
48. [48] Poritz, L.S., Garver, K.I., Tilberg, A.F., Koltun, W.A., Tumor necrosis factor alpha disrupts tight junction assembly1,2. J. Surg. Res. 116:1 (2004), 14–18.
49. [49] Fujita, H., Chalubinski, M., Rhyner, C., Indermitte, P., Meyer, N., Ferstl, R., et al. Claudin-1 expression in airway smooth muscle exacerbates airway remodeling in asthmatic subjects. J. Allergy Clin. Immunol., 127(6), 2011 (1612-21.e8).