Cleavage and cell adhesion properties of human epithelial cell adhesion molecule (HEPCAM)

Journal of Biological Chemistry

Volumn 290, Issue 40, 2015, Pages 24574-24591

  Tsaktanis, Thanos ^a   Kremling, Heidi ^a   Pavšič, Miha ^c   Von Stackelberg, Ricarda ^a   Mack, Brigitte ^a   Fukumori, Akio ^d   Steiner, Harald ^b,d   Vielmuth, Franziska ^b   Spindler, Volker ^b   Huang, Zhe ^a   Jakubowski, Jasmine ^a,b   Stoecklein, Nikolas H ^e   Luxenburger, Elke ^a   Lauber, Kirsten ^b   Lenarčič, Brigita ^c   Gires, Olivier ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; CELL ADHESION; CELL CULTURE; CYTOLOGY; DIMERS; ENZYME ACTIVITY; MOLECULAR BIOLOGY; MOLECULES;

ADHESION PROPERTIES; CARCINOMA CELL LINES; CYTOPLASMIC VESICLES; HUMAN EPITHELIAL CELLS; INTRACELLULAR DOMAIN; INTRAMEMBRANE PROTEOLYSIS; THREE-DIMENSIONAL STRUCTURE; TRANSMEMBRANE HELICES;

CELLS;

ADAM PROTEIN; BETA SECRETASE 1; GAMMA SECRETASE; HUMAN EPITHELIAL CELL ADHESION MOLECULE; TUMOR ANTIGEN; UNCLASSIFIED DRUG; AMINO ACID; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; CELL ADHESION MOLECULE; EPCAM PROTEIN, HUMAN; EPITHELIAL CELL ADHESION MOLECULE; SECRETASE;

ARTICLE; CARCINOMA CELL LINE; CELL ADHESION; CELL PH; CONTROLLED STUDY; CRISPR CAS SYSTEM; CYTOPLASM; EMBRYO; ENDOCYTOSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; BINDING SITE; CELL MEMBRANE; CELL SEPARATION; CHEMISTRY; FLOW CYTOMETRY; HEK293 CELL LINE; METABOLISM; PH; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

AMINO ACIDS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANTIGENS, NEOPLASM; ASPARTIC ACID ENDOPEPTIDASES; BINDING SITES; CELL ADHESION; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELL MEMBRANE; CELL SEPARATION; ENDOCYTOSIS; EPITHELIAL CELL ADHESION MOLECULE; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS;

EID: 84943328547     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.662700     Document Type: Article

References (63)

1. Herlyn, D., Herlyn, M., Steplewski, Z., and Koprowski, H. (1979) Monoclonal antibodies in cell-mediated cytotoxicity against human melanoma and colorectal carcinoma. Eur. J. Immunol. 9, 657-659
2. Riethmüller, G., Schneider-Gädicke, E., Schlimok, G., Schmiegel, W., Raab, R., Höffken, K., Gruber, R., Pichlmaier, H., Hirche, H., and Pichlmayr, R. (1994) Randomised trial of monoclonal antibody for adjuvant therapy of resected Dukes' C colorectal carcinoma. Lancet 343, 1177-1183
3. Litvinov, S. V., and Bakker., H. A., Gourevitch, M. M., Velders, M. P., and Warnaar, S. O. (1994) Evidence for a role of the epithelial glycoprotein 40 (Ep-CAM) in epithelial cell-cell adhesion. Cell Adhes. Commun. 2, 417-428
4. Litvinov, S. V., and Velders., M. P., Bakker, H. A., Fleuren, G. J., and Warnaar, S. O. (1994) Ep-CAM: a human epithelial antigen is a homophilic cell-cell adhesion molecule. J. Cell Biol. 125, 437-446
5. Litvinov, S. V., Balzar, M., Winter, M. J., Bakker, H. A., Briaire-de Bruijn, I. H., Prins, F., Fleuren, G. J., and Warnaar, S. O. (1997) Epithelial cell adhesion molecule (Ep-CAM) modulates cell-cell interactions mediated by classic cadherins. J. Cell Biol. 139, 1337-1348
6. Nagao, K., Zhu, J., Heneghan, M. B., Hanson, J. C, Morasso, M. I., Tessarollo, L., Mackem, S., and Udey, M. C. (2009) Abnormal placental development and early embryonic lethality in EpCAM-null mice. PLoS ONE 4, e8543
7. Guerra, E., Lattanzio, R., LaSorda, R., Dini, F., and Tiboni., G. M., Piantelli, M., and Alberti, S. (2012) mTrop1/Epcam knockout mice develop congenital tufting enteropathy through dysregulation of intestinal E-cadherin/β-catenin. PLoS ONE 7, e49302
8. Lei, Z., Maeda, T., Tamura, A., Nakamura, T., Yamazaki, Y., Shiratori, H., Yashiro, K., Tsukita, S., and Hamada, H. (2012) EpCAM contributes to formation of functional tight junction in the intestinal epithelium by recruiting claudin proteins. Dev. Biol. 371, 136-145
9. Sivagnanam, M., and Mueller., J. L., Lee, H., Chen, Z., Nelson, S. F., Turner, D., Zlotkin, S. H., Pencharz, P. B., Ngan, B. Y., Libiger, O., Schork, N. J., Lavine, J. E., Taylor, S., Newbury, R. O., Kolodner, R. D., and Hoffman, H. M. (2008) Identification of EpCAM as the gene for congenital tufting enteropathy. Gastroenterology 135, 429-437
10. Slanchev, K., and Carney., T. J., Stemmler, M. P., Koschorz, B., Amsterdam, A., Schwarz, H., and Hammerschmidt, M. (2009) The epithelial cell adhesion molecule EpCAM is required for epithelial morphogenesis and integrity during zebrafish epiboly and skin development. PLoS Genet. 5, e1000563
11. Maghzal, N, Kayali, H.A., Rohani, N, and Kajava., A. V., and Fagotto, F. (2013) EpCAM controls actomyosin contractility and cell adhesion by direct inhibition of PKC. Dev. Cell 27, 263-277
12. Thuma, F., and Zöller, M. (2013) EpCAM-associated claudin-7 supports lymphatic spread and drug resistance in rat pancreatic cancer. Int. J. Cancer 133, 855-866
13. Maghzal, N, Vogt, E., Reintsch, W., Fraser, J. S., and Fagotto, F. (2010) The tumor-associated EpCAM regulates morphogenetic movements through intracellular signaling. J. Cell Biol. 191, 645-659
14. Osta, W. A., Chen, Y., Mikhitarian, K., Mitas, M., Salem, M., Hannun, Y. A., Cole, D. J., and Gillanders, W. E. (2004) EpCAM is overexpressed in breast cancer and is a potential target for breast cancer gene therapy. Cancer Res. 64, 5818-5824
15. Sankpal, N. V., and Willman., M. W., Fleming, T. P., Mayfield, J. D., and Gillanders, W. E. (2009) Transcriptional repression of epithelial cell adhesion molecule contributes to p53 control of breast cancer invasion. Cancer Res. 69, 753-757
16. Driemel, C, Kremling, H., Schumacher, S., Will, D., Wolters, J., Lindenlauf, N, Mack, B., Baldus, S. A., Hoya, V., Pietsch, J. M., Panagiotidou, P., Raba, K., Vay, C, Vallböhmer, D., Harréus, U., et al. (2014) Context-dependent adaption of EpCAM expression in early systemic esophageal cancer. Oncogene 33, 4904-4915
17. Rao, C. G., Chianese, D., Doyle, G. V., Miller, M. C., Russell, T., Sanders, R. A., Jr., and Terstappen, L. W. (2005) Expression of epithelial cell adhesion molecule in carcinoma cells present in blood and primary and metastatic tumors. Int. J. Oncol. 27, 49-57
18. Gorges, T.M., Tinhofer, I., Drosch, M., Röse, L., Zollner, T. M., Krahn, T., and von Ahsen, O. (2012) Circulating tumour cells escape from EpCAM-based detection due to epithelial-to-mesenchymal transition. BMC Cancer 12, 178
19. Vannier, C, Mock, K., Brabletz, T., and Driever, W. (2013) Zeb1 regulates E-cadherin and Epcam expression to control cell behavior in early zebrafish development. J. Biol. Chem. 288, 18643-18659
20. Gires, O., and Stoecklein, N. H. (2014) Dynamic EpCAM expression on circulating and disseminating tumor cells: causes and consequences. Cell. Mol. Life Sci. 71, 4393-4402
21. Schön, M. P., Schön, M., Klein, C. E., Blume, U., Bisson, S., and Orfanos, C. E. (1994) Carcinoma-associated 38-kD membrane glycoprotein MH 99/KS 1/4 is related to proliferation and age of transformed epithelial cell lines. J. Invest. Dermatol. 102, 987-991
22. Litvinov, S. V., van Driel, W., van Rhijn, C M., and Bakker., H. A., van Krieken, H., Fleuren, G. J., and Warnaar, S. O. (1996) Expression of Ep-CAM in cervical squamous epithelia correlates with an increased proliferation and the disappearance of markers for terminal differentiation. Am. J. Pathol. 148, 865-875
23. Münz, M., Kieu, C, Mack, B., Schmitt, B., Zeidler, R., and Gires, O. (2004) The carcinoma-associated antigen EpCAM upregulates c-myc and induces cell proliferation. Oncogene 23, 5748-5758
24. Brown, M. S., Ye, J., Rawson, R. B., and Goldstein, J. L. (2000) Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391-398
25. Wolfe, M. S., and Kopan, R. (2004) Intramembrane proteolysis: theme and variations. Science 305, 1119-1123
26. Mumm, J. S., and Kopan, R. (2000) Notch signaling: from the outside in. Dev. Biol. 228, 151-165
27. Lichtenthaler, S. F., Haass, C, and Steiner, H. (2011) Regulated intramembrane proteolysis-lessons from amyloid precursor protein processing. J. Neurochem. 117, 779-796
28. Kopan, R., and Ilagan, M. X. (2004) γ-Secretase: proteasome of the membrane? Nat. Rev. Mol. Cell Biol. 5, 499-504
29. Maetzel, D., Denzel, S., Mack, B., Canis, M., Went, P., Benk, M., Kieu, C, Papior, P., and Baeuerle., P. A., Munz, M., and Gires, O. (2009) Nuclear signalling by tumour-associated antigen EpCAM. Nat. Cell Biol. 11, 162-171
30. Chaves-Pérez, A., Mack, B., Maetzel, D., Kremling, H., Eggert, C, Harréus, U., and Gires, O. (2013) EpCAM regulates cell cycle progression via control of cyclin D1 expression. Oncogene 32, 641-650
31. Hachmeister, M., and Bobowski., K. D., Hogl, S., Dislich, B., Fukumori, A., Eggert, C, Mack, B., Kremling, H, Sarrach, S., Coscia, F., Zimmermann, W., Steiner, H., and Lichtenthaler., S. F., and Gires, O. (2013) Regulated intramembrane proteolysis and degradation of murine epithelial cell adhesion molecule mEpCam. PLoS ONE 8, e71836
32. Akeson, A. L., and Woods, C. W. (1993) A fluorometric assay for the quantitation of cell adherence to endothelial cells. J. Immunol. Methods 163, 181-185
33. Sastre, M., Steiner, H., Fuchs, K., Capell, A., Multhaup, G., Condron, M. M., Teplow, D. B., and Haass, C. (2001) Presenilin-dependent γ-secretase processing of β-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep. 2, 835-841
34. Pavsic, M., Guncar, G., Djinovic-Carugo, K., and Lenarčič, B. (2014) Crystal structure and its bearing towards an understanding of key biological functions of EpCAM. Nat Commun. 5, 4764
35. Kim, D. E., Chivian, D., and Baker, D. (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32, W526-W531
36. Raman, S., Vernon, R., Thompson, J., Tyka, M., Sadreyev, R., Pei, J., Kim, D., Kellogg, E., DiMaio, F., Lange, O., Kinch, L., Sheffler, W., Kim, B. H., Das, R., Grishin, N. V., and Baker, D. (2009) Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins 77, 89-99
37. Waschke, J., Bruggeman, P., Baumgartner, W., Zillikens, D., and Drenckhahn, D. (2005) Pemphigus foliaceus IgG causes dissociation of desmoglein 1-containing junctions without blocking desmoglein 1 transinteraction. J. Clin. Invest. 115, 3157-3165
38. Monteiro, A. C, Luissint, A.-C, Sumagin, R., Lai, C, Vielmuth, F., Wolf, M. F., Laur, O., Reiss, K., Spindler, V., Stehle, T., Dermody, T. S., Nusrat, A., and Parkos, C. A. (2014) Trans-dimerization of JAM-A regulates Rap2 and is mediated by a domain that is distinct from the cis-dimerization interface. Mol. Biol. Cell 25, 1574-1585
39. Wildling, L., Unterauer, B., Zhu, R., Rupprecht, A., Haselgrübler, T., Rankl, C., Ebner, A., Vater, D., Pollheimer, P., and Pohl., E. E., Hinterdorfer, P., and Gruber, H. J. (2011) Linking of sensor molecules with amino groups to amino-functionalized AFM tips. Bioconjug. Chem. 22, 1239-1248
40. Doedens, J. R., and Mahimkar., R. M., and Black, R. A. (2003) TACE/ADAM-17 enzymatic activity is increased in response to cellular stimulation. Biochem. Biophys. Res. Commun. 308, 331-338
41. Cole, S. L., and Vassar, R. (2007) The Alzheimer's disease β-secretase enzyme, BACE1. Mol. Neurodegeneration 2, 22
42. Munz, M., Fellinger, K., Hofmann, T., Schmitt, B., and Gires, O. (2008) Glycosylation is crucial for stability of tumour and cancer stem cell antigen EpCAM. Front. Biosci. 13, 5195-5201
43. Balzar, M., Briaire-de Bruijn, I. H, Rees-Bakker, H. A., Prins, F. A., Helfrich, W., de Leij, L., Riethmüller, G., Alberti, S., Warnaar, S. O., Fleuren, G. J., and Litvinov, S. V. (2001) Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions. Mol. Cell. Biol. 21, 2570-2580
44. Hinterdorfer, P., and Dufrêne, Y. F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3, 347-355
45. Waschke, J. (2008) The desmosome and pemphigus. Histochem. Cell Biol. 130, 21-54
46. Vielmuth, F., Hartlieb, E., Kugelmann, D., Waschke, J., and Spindler, V. (2015) Atomic force microscopy identifies regions of distinct desmoglein 3 adhesive properties on living keratinocytes. Nanomedicine 11, 511-520
47. Went, P. T., Lugli, A., Meier, S., Bundi, M., Mirlacher, M., Sauter, G., and Dirnhofer, S. (2004) Frequent EpCam protein expression in human carcinomas. Hum. Pathol. 35, 122-128
48. Baeuerle, P. A., and Gires, O. (2007) EpCAM (CD326) finding its role in cancer. Br. J. Cancer 96, 417-423
49. Imrich, S., Hachmeister, M., and Gires, O. (2012) EpCAM and its potential role in tumor-initiating cells. CellAdh. Migr. 6, 30-38
50. Patriarca, C, and Macchi., R. M., Marschner, A. K., and Mellstedt, H. (2012) Epithelial cell adhesion molecule expression (CD326) in cancer: a short review. Cancer Treat. Rev. 38, 68-75
51. Ng, V. Y., Ang, S. N, Chan, J. X., and Choo, A. B. (2009) Characterization of epithelial cell adhesion molecule as a surface marker on undifferentiated human embryonic stem cells. Stem Cells 28, 29-35
52. González, B., Denzel, S., Mack, B., Conrad, M., and Gires, O. (2009) EpCAM is involved in maintenance of the murine embryonic stem cell phenotype. Stem Cells 27, 1782-1791
53. Dollé, L., and Theise., N. D., Schmelzer, E., Boulter, L., Gires, O., and van Grunsven, L. A. (2015) EpCAM and the biology of hepatic stem/progenitor cells. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G233-G250
54. Trzpis, M., and McLaughlin., P. M., van Goor, H., Brinker, M. G., van Dam, G. M., de Leij, L. M., Popa, E. R., and Harmsen, M. C. (2008) Expression of EpCAM is up-regulated during regeneration of renal epithelia. J. Pathol. 216, 201-208
55. Lu, T. Y., and Lu., R. M., Liao, M. Y., Yu, J., Chung, C. H., Kao, C. F., and Wu, H. C. (2010) Epithelial cell adhesion molecule regulation is associated with the maintenance of the undifferentiated phenotype of human embryonic stem cells. J. Biol. Chem. 285, 8719-8732
56. Joachim, C. L., and Selkoe, D. J. (1992) The seminal role of β-amyloid in the pathogenesis of Alzheimer disease. Alzheimer Dis. Assoc. Disord. 6, 7-34
57. Haass, C, Kaether, C, Thinakaran, G., and Sisodia, S. (2012) Trafficking and proteolytic processing of APP. Cold Spring Harb. Perspect. Med. 2, a006270
58. Simon, M., Stefan, N, Plückthun, A., and Zangemeister-Wittke, U. (2013) Epithelial cell adhesion molecule-targeted drug delivery for cancer therapy. Expert Opin. Drug Deliv. 10, 451-468
59. Balzar, M., and Winter., M. J., de Boer, C. J., and Litvinov, S. V. (1999) The biology of the 17-1A antigen (Ep-CAM). J. Mol. Med. 77, 699-712
60. Pavšič, M., and Lenarčič, B. (2011) Expression, crystallization and preliminary x-ray characterization of the human epithelial cell-adhesion molecule ectodomain. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 1363-1366
61. Kuhn, S., Koch, M., Nübel, T., Ladwein, M., Antolovic, D., Klingbeil, P., Hildebrand, D., Moldenhauer, G., Langbein, L., Franke, W. W., Weitz, J., and Zöller, M. (2007) A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol. Cancer Res. 5, 553-567
62. Ladwein, M., and Pape., U. F., Schmidt, D. S., Schnölzer, M., Fiedler, S., Langbein, L., Franke, W. W., Moldenhauer, G., and Zöller, M. (2005) The cell-cell adhesion molecule EpCAM interacts directly with the tight junction protein claudin-7. Exp. Cell Res. 309, 345-357
63. Philip, R., Heiler, S., Mu, W., Büchler, M. W., Zöller, M., and Thuma, F. (2015) Claudin-7 promotes the epithelial-mesenchymal transition in human colorectal cancer. Oncotarget 6, 2046-2063