MUC1 protein induces Urokinase-type Plasminogen Activator (uPA) by forming a complex with NF-κB p65 transcription factor and binding to the uPA promoter, leading to enhanced invasiveness of cancer cells

Journal of Biological Chemistry

Volumn 289, Issue 51, 2014, Pages 35193-35204

  Mori, Yugo ^a   Akita, Kaoru ^a   Tanida, Shuhei ^a   Ishida, Akiko ^a   Toda, Munetoyo ^a   Inoue, Mizue ^a   Yashiro, Masakazu ^b   Sawada, Tetsuji ^b   Hirakawa, Kosei ^b   Nakada, Hiroshi ^a  

^a KYOTO SANGYO UNIVERSITY   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGNOSIS; DISEASES; PLANTS (BOTANY); SIGNAL TRANSDUCTION; TRANSCRIPTION;

C-TERMINAL DOMAINS; CHROMATIN IMMUNOPRECIPITATION ASSAY; MATRIX METALLOPROTEINASES; MICROARRAY ANALYSIS; NUCLEAR TRANSLOCATIONS; SIGNALING PATHWAYS; TRANSCRIPTIONAL ACTIVITY; UROKINASE-TYPE PLASMINOGEN ACTIVATOR (UPA);

CELL SIGNALING;

AMILORIDE; ANTINEOPLASTIC AGENT; GELATINASE A; GELATINASE B; ILOMASTAT; JSH 23; MUCIN 1; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; UROKINASE; 4-METHYL-N1-(3-PHENYLPROPYL)BENZENE-1,2-DIAMINE; DIPEPTIDE; MUC1 PROTEIN, HUMAN; N-(2(R)-2-(HYDROXAMIDOCARBONYLMETHYL)-4-METHYLPENTANOYL)-L-TRYPTOPHAN METHYLAMIDE; PHENYLENEDIAMINE DERIVATIVE; PROTEIN BINDING;

ARTICLE; BINDING SITE; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME LOCALIZATION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG CANCER CELL LINE; OVARIAN CANCER CELL LINE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR INVASION; UPREGULATION; ANTAGONISTS AND INHIBITORS; CELL MOTION; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HCT116 CELL LINE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; NEOPLASM; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

BINDING SITES; CELL LINE, TUMOR; CELL MOVEMENT; DIPEPTIDES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MUCIN-1; NEOPLASM INVASIVENESS; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENYLENEDIAMINES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA INTERFERENCE; TRANSCRIPTION FACTOR RELA; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84919389804     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.586461     Document Type: Article

References (54)

1. Nakamori, S., Ota, D. M., Cleary, K. R., Shirotani, K., and Irimura, T. (1994)MUC1mucin expression as a marker of progression and metastasis of human colorectal carcinoma. Gastroenterology 106, 353-361
2. Kufe, D., Inghirami, G., Abe, M., Hayes, D., Justi-Wheeler, H., and Schlom, J. (1984) Differential reactivity of a novel monoclonal antibody (DF3) with human malignant versus benign breast tumors. Hybridoma 3, 223-232
3. Qu, C. F., Li, Y., Song, Y. J., Rizvi, S. M., Raja, C., Zhang, D., Samra, J., Smith, R., Perkins, A. C., Apostolidis, C., and Allen, B. J. (2004) MUC1 expression in primary and metastatic pancreatic cancer cells for in vitro treatment by (213)Bi-C595 radioimmunoconjugate. Br. J. Cancer 91, 2086-2093
4. Kufe, D. (2009) Mucins in cancer: function, prognosis and therapy. Nat. Rev. Cancer 9, 874-885
5. Ligtenberg, M. J., Kruijshaar, L., Buijs, F., van Meijer, M., Litvinov, S. V., and Hilkens, J. (1992) Cell-associated episialin is a complex containing two proteins derived from a common precursor. J. Biol. Chem. 267, 6171-6177
6. Parry, S., Silverman, H. S., McDermott, K., Willis, A., Hollingsworth, M. A., and Harris, A. (2001) Identification of MUC1 proteolytic cleavage sites in vivo. Biochem. Biophys. Res. Commun. 283, 715-720
7. Siddiqui, J., Abe, M., Hayes, D., Shani, E., Yunis, E., and Kufe, D. (1988) Isolation and sequencing of a cDNA coding for the human DF3 breast carcinoma-associated antigen. Proc. Natl. Acad. Sci. U.S.A. 85, 2320-2323
8. Gendler, S., Taylor-Papadimitriou, J., Duhig, T., Rothbard, J., and Burchell, J. (1988) A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J. Biol. Chem. 263, 12820-12823
9. Merlo, G. R., Siddiqui, J., Cropp, C. S., Liscia, D. S., Lidereau, R., Callahan, R., and Kufe, D. (1989) Frequent alteration of the DF3 tumor-associated antigen gene in primary human breast carcinomas. Cancer Res. 49, 6966-6971
10. Yamamoto, M., Bharti, A., Li, Y., and Kufe, D. (1997) Interaction of the DF3/MUC1 breast carcinoma-associated antigen and beta-catenin in cell adhesion. J. Biol. Chem. 272, 12492-12494
11. Ahmad, R., Rajabi, H., Kosugi, M., Joshi, M. D., Alam, M., Vasir, B., Kawano, T., Kharbanda, S., and Kufe, D. (2011) MUC1-C oncoprotein promotes STAT3 activation in an autoinductive regulatory loop. Sci. Signal. 4, ra9
12. Ahmad, R., Raina, D., Joshi, M. D., Kawano, T., Ren, J., Kharbanda, S., and Kufe, D. (2009) MUC1-C oncoprotein functions as a direct activator of the nuclear factor-κB p65 transcription factor. Cancer Res. 69, 7013-7021
13. Raina, D., Ahmad, R., Rajabi, H., Panchamoorthy, G., Kharbanda, S., and Kufe, D. (2012) Targeting cysteine-mediated dimerization of the MUC1-C oncoprotein in human cancer cells. Int. J. Oncol. 40, 1643-1649
14. Leng, Y., Cao, C., Ren, J., Huang, L., Chen, D., Ito, M., and Kufe, D. (2007) Nuclear import of the MUC1-C oncoprotein is mediated by nucleoporin Nup62. J. Biol. Chem. 282, 19321-19330
15. Wesseling, J., van der Valk, S. W., and Hilkens, J. (1996) A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membraneassociated mucin episialin/MUC1. Mol. Biol. Cell 7, 565-577
16. Andreasen, P. A., Kjoller, L., Christensen, L., and Duffy, M. J. (1997) The urokinase-type plasminogen activator system in cancer metastasis: a review. Int. J. Cancer 72, 1-22
17. Dano, K., Behrendt, N., Hoyer-Hansen, G., Johnsen, M., Lund, L. R., Ploug, M., and Romer, J. (2005) Plasminogen activation and cancer. Thromb. Haemost. 93, 676-681
18. Blasi, F., and Carmeliet, P. (2002) uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 3, 932-943
19. Mason, S. D., and Joyce, J. A. (2011) Proteolytic networks in cancer. Trends Cell Biol. 21, 228-237
20. Nielsen, L. S., Andreasen, P. A., Grondahl-Hansen, J., Skriver, L., and Dano, K. (1986) Plasminogen activators catalyse conversion of inhibitor from fibrosarcoma cells to an inactive form with a lower apparent molecular mass. FEBS Lett. 196, 269-273
21. Naldini, L., Tamagnone, L., Vigna, E., Sachs, M., Hartmann, G., Birchmeier, W., Daikuhara, Y., Tsubouchi, H., Blasi, F., and Comoglio, P. M. (1992) Extracellular proteolytic cleavage by urokinase is required for activation of hepatocyte growth factor/scatter factor.EMBO J. 11, 4825-4833
22. Ustach, C. V., and Kim, H. R. (2005) Platelet-derived growth factor D is activated by urokinase plasminogen activator in prostate carcinoma cells. Mol. Cell Biol. 25, 6279-6288
23. Waltz, D. A., and Chapman, H. A. (1994) Reversible cellular adhesion to vitronectin linked to urokinase receptor occupancy. J. Biol. Chem. 269, 14746-14750
24. Wei, Y., Czekay, R. P., Robillard, L., Kugler, M. C., Zhang, F., Kim, K. K., Xiong, J. P., Humphries, M. J., and Chapman, H. A. (2005) Regulation of α5β1 integrin conformation and function by urokinase receptor binding. J. Cell Biol. 168, 501-511
25. Wei, Y., Eble, J. A., Wang, Z., Kreidberg, J. A., and Chapman, H. A. (2001) Urokinase receptors promote β1 integrin function through interactions with integrin α3β1. Mol. Biol. Cell 12, 2975-2986
26. Gondi, C. S., Kandhukuri, N., Dinh, D. H., Gujrati, M., and Rao, J. S. (2007) Down-regulation of uPAR and uPA activates caspase-mediated apoptosis and inhibits the PI3K/AKT pathway. Int. J. Oncol. 31, 19-27
27. Aguirre Ghiso, J. A. (2002) Inhibition of FAK signaling activated by urokinase receptor induces dormancy in human carcinoma cells in vivo. Oncogene 21, 2513-2524
28. Sidenius, N., and Blasi, F. (2003) The urokinase plasminogen activator system in cancer: recent advances and implication for prognosis and therapy. Cancer Metastasis Rev. 22, 205-222
29. Irigoyen, J. P., Muñoz-Cánoves, P., Montero, L., Koziczak, M., and Nagamine, Y. (1999) The plasminogen activator system: biology and regulation. Cell Mol. Life Sci. 56, 104-132
30. Novak, U., Cocks, B. G., and Hamilton, J. A. (1991) A labile repressor acts through the NFkB-like binding sites of the human urokinase gene. Nucleic Acids Res. 19, 3389-3393
31. Cicek, M., Fukuyama, R., Cicek, M. S., Sizemore, S., Welch, D. R., Sizemore, N., and Casey, G. (2009) BRMS1 contributes to the negative regulation of uPA gene expression through recruitment of HDAC1 to the NF-κB binding site of the uPA promoter. Clin. Exp. Metastasis 26, 229-237
32. Hayden, M. S., and Ghosh, S. (2008) Shared principles in NF-κB signaling. Cell 132, 344-362
33. Ahmad, R., Raina, D., Trivedi, V., Ren, J., Rajabi, H., Kharbanda, S., and Kufe, D. (2007) MUC1 oncoprotein activates the IκB kinase beta complex and constitutive NF-κB signalling. Nat. Cell Biol. 9, 1419-1427
34. Li, Y., Ren, J., Yu, W., Li, Q., Kuwahara, H., Yin, L., Carraway, K. L., 3rd, and Kufe D. (2001) The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and beta-catenin. J. Biol. Chem. 276, 35239-35242
35. Shang, Y., Hu, X., DiRenzo, J., Lazar, M. A., and Brown, M. (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103, 843-852
36. He, Y., Liu, X. D., Chen, Z. Y., Zhu, J., Xiong, Y., Li, K., Dong, J. H., and Li, X. (2007) Interaction between cancer cells and stromal fibroblasts is required for activation of the uPAR-uPA-MMP-2 cascade in pancreatic cancer metastasis. Clin. Cancer Res. 13, 3115-3124
37. Toupance, S., Brassart, B., Rabenoelina, F., Ghoneim, C., Vallar, L., Polette, M., Debelle, L., and Birembaut, P. (2012) Elastin-derived peptides increase invasive capacities of lung cancer cells by post-transcriptional regulation of MMP-2 and uPA. Clin. Exp. Metastasis 29, 511-522
38. Hiendlmeyer, E., Regus, S., Wassermann, S., Hlubek, F., Haynl, A., Dimmler, A., Koch, C., Knoll, C., van Beest, M., Reuning, U., Brabletz, T., Kirchner, T., and Jung, A. (2004) Beta-catenin up-regulates the expression of the urokinase plasminogen activator in human colorectal tumors. Cancer Res. 64, 1209-1214
39. Tanida, S., Akita, K., Ishida, A., Mori, Y., Toda, M., Inoue, M., Ohta, M., Yashiro, M., Sawada, T., Hirakawa, K., and Nakada, H. (2013) Binding of the sialic acid-binding lectin, Siglec-9, to the membrane mucin, MUC1, induces recruitment of β-catenin and subsequent cell growth. J. Biol. Chem. 288, 31842-31852
40. Ren, J., Raina, D., Chen, W., Li, G., Huang, L., and Kufe, D. (2006) MUC1 oncoprotein functions in activation of fibroblast growth factor receptor signaling. Mol. Cancer Res. 4, 873-883
41. Huang, L., Chen, D., Liu, D., Yin, L., Kharbanda, S., and Kufe, D. (2005) MUC1 oncoprotein blocks glycogen synthase kinase 3β-mediated phosphorylation and degradation of beta-catenin. Cancer Res. 65, 10413-10422
42. Rahn, J. J., Shen, Q., Mah, B. K., and Hugh, J. C. (2004) MUC1 initiates a calcium signal after ligation by intercellular adhesion molecule-1. J. Biol. Chem. 279, 29386-29390
43. Shen, Q., Rahn, J. J., Zhang, J., Gunasekera, N., Sun, X., Shaw, A. R., Hendzel, M. J., Hoffman, P., Bernier, A., and Hugh, J. C. (2008) MUC1 initiates Src-CrkL-Rac1/Cdc42-mediated actin cytoskeletal protrusive motility after ligating intercellular adhesion molecule-1. Mol. Cancer Res. 6, 555-567
44. Sahraei, M., Roy, L. D., Curry, J. M., Teresa, T. L., Nath, S., Besmer, D., Kidiyoor, A., Dalia, R., Gendler, S. J., and Mukherjee, P. (2012) MUC1 regulates PDGFA expression during pancreatic cancer progression. Oncogene 31, 4935-4945
45. Singh, P. K., Wen, Y., Swanson, B. J., Shanmugam, K., Kazlauskas, A., Cerny, R. L., Gendler, S. J., and Hollingsworth, M. A. (2007) Platelet-derived growth factor receptor β-mediated phosphorylation of MUC1 enhances invasiveness in pancreatic adenocarcinoma cells. Cancer Res. 67, 5201-5210
46. Rajabi, H., Alam, M., Takahashi, H., Kharbanda, A., Guha, M., Ahmad, R., and Kufe, D. (2014) MUC1-C oncoprotein activates the ZEB1/miR-200c regulatory loop and epithelial-mesenchymal transition. Oncogene 33, 1680-1689
47. Cantero, D., Friess, H., Deflorin, J., Zimmermann, A., Bründler, M. A., Riesle, E., Korc, M., and Büchler, M. W. (1997) Enhanced expression of urokinase plasminogen activator and its receptor in pancreatic carcinoma. Br. J. Cancer 75, 388-395
48. Memarzadeh, S., Kozak, K. R., Chang, L., Natarajan, S., Shintaku, P., Reddy, S. T., and Farias-Eisner, R. (2002) Urokinase plasminogen activator receptor: Prognostic biomarker for endometrial cancer. Proc. Natl. Acad. Sci. U.S.A. 99, 10647-10652
49. Hemsen, A., Riethdorf, L., Brünner, N., Berger, J., Ebel, S., Thomssen, C., Jänicke, F., and Pantel, K. (2003) Comparative evaluation of urokinase-type plasminogen activator receptor expression in primary breast carcinomas and on metastatic tumor cells. Int. J. Cancer 107, 903909
50. Mann, B., Gelos, M., Siedow, A., Hanski, M. L., Gratchev, A., Ilyas, M., Bodmer, W. F., Moyer, M. P., Riecken, E. O., Buhr, H. J., and Hanski, C. (1999) Target genes of beta-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc. Natl. Acad. Sci. U.S.A. 96, 1603-1608
51. Wang, Q., Sun, Z. X., Allgayer, H., and Yang, H. S. (2010) Downregulation of E-cadherin is an essential event in activating beta-catenin/Tcf-dependent transcription and expression of its target genes in Pdcd4 knockdown cells. Oncogene 29, 128-138
52. Farina, A. R., Tacconelli, A., Vacca, A., Maroder, M., Gulino, A., and Mackay, A. R. (1999) Transcriptional up-regulation of matrix metalloproteinase-9 expression during spontaneous epithelial to neuroblast phenotype conversion by SK-N-SH neuroblastoma cells, involved in enhanced invasivity, depends upon GT-box and nuclear factor κB elements. Cell Growth Differ. 10, 353-367
53. Tanida, S., Mori, Y., Ishida, A., Akita, K., and Nakada, H. (2014) Galectin-3 binds to MUC1-N-terminal domain and triggers recruitment of β-catenin in MUC1-expressing mouse 3T3 cells. Biochim. Biophys. Acta 1840, 1790-1797
54. Raina, D., Kosugi, M., Ahmad, R., Panchamoorthy, G., Rajabi, H., Alam, M., Shimamura, T., Shapiro, G. I., Supko, J., Kharbanda, S., and Kufe, D. (2011) Dependence on the MUC1-C oncoprotein in non-small cell lung cancer cells. Mol. Cancer Ther. 10, 806-816