EpCAM-associated claudin-7 supports lymphatic spread and drug resistance in rat pancreatic cancer

International Journal of Cancer

Volumn 133, Issue 4, 2013, Pages 855-866

  Thuma, Florian ^a   Zöller, Margot ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

apoptosis resistance; claudin 7; EpCAM; metastasis; motility; pancreatic cancer; rat

Indexed keywords

ALPHA6BETA4 INTEGRIN; CISPLATIN; CLAUDIN 7; EPITHELIAL CELL ADHESION MOLECULE; EZRIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PRESENILIN 2; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; TETRASPANIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RESISTANCE; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; LYMPH NODE METASTASIS; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SURVIVAL TIME;

ANIMALS; ANTIGENS, NEOPLASM; APOPTOSIS; BLOTTING, WESTERN; CELL ADHESION; CELL ADHESION MOLECULES; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; IMMUNOPRECIPITATION; LYMPHATIC METASTASIS; PANCREATIC NEOPLASMS; PHOSPHORYLATION; RATS;

EID: 84878870719     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28085     Document Type: Article

References (49)

1. Visvader JE,. Cells of origin in cancer. Nature 2011; 469: 314-22.
2. Chaffer CL, Weinberg RA,. A perspective on cancer cell metastasis. Science 2011; 331: 1559-64.
3. Marhaba R, Klingbeil P, Nübel T, et al. CD44 and EpCAM: cancer-initiating cell markers. Curr Mol Med 2008; 8: 784-804.
4. Münz M, Baeuerle PA, Gires O,. The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res 2009; 69: 5627-9.
5. Keysar SB, Jimeno A,. More than markers: biological significance of cancer stem cell-defining molecules. Mol Cancer Ther 2010; 9: 2450-7.
6. Balzar M, Briaire-de Bruijn IH, Rees-Bakker HA, et al. Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions. Mol Cell Biol 2001; 21: 2570-80. (Pubitemid 32222108)
7. Winter MJ, Nagelkerken B, Mertens AE, et al. Expression of Ep-CAM shifts the state of cadherin-mediated adhesions from strong to weak. Exp Cell Res 2003; 285: 50-8. (Pubitemid 36390155)
8. Yamashita T, Budhu A, Forgues M, et al. Activation of hepatic stem cell marker EpCAM by Wnt-beta-catenin signaling in hepatocellular carcinoma. Cancer Res 2007; 67: 10831-9. (Pubitemid 350145912)
9. Maghzal N, Vogt E, Reintsch W, et al. The tumor-associated EpCAM regulates morphogenetic movements through intracellular signaling. J Cell Biol 2010; 191: 645-59.
10. Denzel S, Mack B, Eggert C, et al. MMP7 is a target of the tumour-associated antigen EpCAM. Int J Exp Pathol 2012; 93: 341-53.
11. Sankpal NV, Willman MW, Fleming TP, et al. Transcriptional repression of epithelial cell adhesion molecule contributes to p53 control of breast cancer invasion. Cancer Res 2009; 69: 753-7.
12. Maetzel D, Denzel S, Mack B, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 2009; 11: 162-71.
13. Münz M, Kieu C, Mack B, et al. The carcinoma-associated antigen EpCAM upregulates c-myc and induces cell proliferation. Oncogene 2004; 23: 5748-58. (Pubitemid 39093020)
14. Lin CW, Liao MY, Lin WW, et al. Epithelial cell adhesion molecule regulates tumor initiation and tumorigenesis via activating reprogramming factors and epithelial-mesenchymal transition genes expression in colon cancer. J Biol Chem 2012; 287: 39449-59.
15. Yovchev MI, Grozdanov PN, Zhou H, et al. Identification of adult hepatic progenitor cells capable of repopulating injured rat liver. Hepatology 2008; 47: 636-47. (Pubitemid 351280732)
16. Ladwein M, Schmidt DS, Schnölzer M, et al. The cell-cell adhesion molecule EpCAM associates with the tight junction protein claudin 7. Exp Cell Res 2005; 309: 345-57. (Pubitemid 41317358)
17. Tsukita S, Yamazaki Y, Katsuno T, et al. Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 2008; 27: 6930-8.
18. Fujita H, Chiba H, Yokozaki H, et al. Differential expression and subcellular localization of claudin-7,-8,-12,-13, and -15 along the mouse intestine. J Histochem Cytochem 2006; 54: 933-44. (Pubitemid 44106871)
19. Yeaman C, Grindstaff KK, Hansen MD, et al. Cell polarity: versatile scaffolds keep things in place. Curr Biol 1999; 9: 515-17.
20. Ikari A, Ito M, Okude C, et al. Claudin-16 is directly phosphorylated by protein kinase A independently of a vasodilator-stimulated phosphoprotein- mediated pathway. J Cell Physiol 2008; 214: 221-9. (Pubitemid 350220076)
21. French AD, Fiori JL, Camilli TC, et al. PKC and PKA phosphorylation affect the subcellular localization of claudin-1 in melanoma cells. Int J Med Sci 2009; 6: 93-101.
22. Sjö A, Magnusson KE, Peterson KH,. Protein kinase C activation has distinct effects on the localization, phosphorylation and detergent solubility of the claudin protein family in tight and leaky epithelial cells. J Membr Biol 2010; 236: 181-9.
23. Ding L, Lu Z, Foreman O, et al. Inflammation and disruption of the mucosal architecture in claudin-7-deficient mice. Gastroenterology 2012; 142: 305-15.
24. Lei Z, Maeda T, Tamura A, et al. EpCAM contributes to formation of functional tight junction in the intestinal epithelium by recruiting claudin proteins. Dev Biol 2012; 371: 136-45.
25. Schmidt DS, Schnölzer M, Klingbeil P, et al. CD44 variant isoforms associate with tetraspanins and selectively with EpCAM: consequences on cell cell and cell matrix adhesion. Exp Cell Res 2004; 297: 329-47.
26. Kuhn S, Koch M, Ladwein M, et al. Complex formation between CD44 variant isoforms with EpCAM and Claudin-7 in tetraspanin-enriched membrane microdomains promotes colorectal cancer progression. Mol Cancer Res 2007; 5: 553-67. (Pubitemid 46985046)
27. Nübel T, Preobraschenski J, Tuncay H, et al. Claudin-7 regulates EpCAM-mediated functions in tumor progression. Mol Cancer Res 2009; 7: 285-99.
28. Le Naour F, Zöller M,. EpCAM, tetraspanins and claudin-7. Front Biosci 2008; 13: 5847-65.
29. Thiel KW, Carpenter G,. ErbB-4 and TNF-alpha converting enzyme localization to membrane microdomains. Biochem Biophys Res Commun 2006; 350: 629-33. (Pubitemid 44550203)
30. Vetrivel KS, Cheng H, Kim SH, et al. Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J Biol Chem 2005; 280: 25892-900. (Pubitemid 40962301)
31. Matzku S, Komitowski D, Miltenberger M, et al. Characterization of BSp73, a spontaneous rat tumour and its in vivo selected variants showing different metastasizing capacity. Invasion Metast 1983; 3: 109-23. (Pubitemid 13034724)
32. Rana S, Claas C, Kretz CC, et al. Activation-induced internalization differs for the tetraspanins CD9 and Tspan8: impact on tumor cell motility. Int J Biochem Cell Biol 2011; 43: 106-19.
33. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67: 1030-7.
34. Matzku S, Wenzel A, Liu S, et al. Antigenic differences between metastatic and non-metastatic rat tumor variants characterized by monoclonal antibodies. Cancer Res 1989; 49: 1294-9. (Pubitemid 19074852)
35. Nelson GM, Padera TP, Garkavtsev I, et al. Differential gene expression of primary cultured lymphatic and blood vascular endothelial cells. Neoplasia 2007; 9: 1038-45. (Pubitemid 350255352)
36. Lingwood D, Simons K,. Lipid rafts as a membrane-organizing principle. Science 2007; 327: 46-50.
37. Wang XQ, Yan Q, Sun P, et al. Suppression of epidermal growth factor receptor signaling by protein kinase C-alpha activation requires CD82, caveolin-1, and ganglioside. Cancer Res 2007; 67: 9986-95. (Pubitemid 47621249)
38. Sjö A, Magnusson KE, Peterson KH,. Protein kinase C activation has distinct effects on the localization, phosphorylation and detergent solubility of the claudin protein family in tight and leaky epithelial cells. J Membr Biol 2010; 236: 181-9.
39. Herlevsen M, Schmidt DS, Miyazaki K, et al. The association of the tetraspanin D6.1A with the alpha6beta4 integrin supports cell motility and liver metastasis formation. J Cell Sci 2003; 116: 4373-90. (Pubitemid 37369593)
40. Hoettecke N, Ludwig A, Foro S, et al. Improved synthesis of ADAM10 inhibitor GI254023X. Neurodegener Dis 2010; 7: 232-8.
41. Klingbeil P, Marhaba R, Jung T, et al. CD44 variant isoforms promote metastasis formation by a tumor cell-matrix cross-talk that supports adhesion and apoptosis resistance. Mol Cancer Res 2009; 7: 168-79.
42. D'Souza T, Indig FE, Morin PJ,. Phosphorylation of claudin-4 by PKCepsilon regulates tight junction barrier function in ovarian cancer cells. Exp Cell Res 2007; 313: 3364-75. (Pubitemid 47284066)
43. Germain EC, Santos TM, Rabinovitz I,. Phosphorylation of a novel site on the {beta}4 integrin at the trailing edge of migrating cells promotes hemidesmosome disassembly. Mol Biol Cell 2009; 20: 56-67.
44. Feki A, Berardi P, Bellingan G, et al. Dissemination of intraperitoneal ovarian cancer: Discussion of mechanisms and demonstration of lymphatic spreading in ovarian cancer model. Crit Rev Oncol Hematol 2009; 72: 1-9.
45. Osada M, Ito E, Fermin HA, et al. The Wnt signaling antagonist Kremen1 is required for development of thymic architecture. Clin Dev Immunol 2006; 13: 299-319. (Pubitemid 44950046)
46. Murai T, Maruyama Y, Mio K, et al. Low cholesterol triggers membrane microdomain-dependent CD44 shedding and suppresses tumor cell migration. J Biol Chem 2011; 286: 1999-2007.
47. Svensson C, Part K, Künnis-Beres K, et al. Pro-survival effects of JNK and p38 MAPK pathways in LPS-induced activation of BV-2 cells. Biochem Biophys Res Commun 2011; 406: 488-92.
48. Zhang S, Yu D,. PI(3)king apart PTEN's role in cancer. Clin Cancer Res 2010; 16: 4325-30.
49. Le Naour F, André M, Boucheix C, et al. Membrane microdomains and proteomics: lessons from tetraspanin microdomains and comparison with lipid rafts. Proteomics 2006; 6: 6447-54. (Pubitemid 46048385)