Galectin-3 binds to MUC1-N-terminal domain and triggers recruitment of β-catenin in MUC1-expressing mouse 3T3 cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 6, 2014, Pages 1790-1797

  Tanida, Shuhei ^a   Mori, Yugo ^a   Ishida, Akiko ^a   Akita, Kaoru ^a   Nakada, Hiroshi ^a  

^a KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

Galectin 3; MUC1; Catenin

Indexed keywords

BETA CATENIN; COMPLEMENTARY DNA; GALECTIN 3; MUCIN 1; GLUCAN SYNTHASE; GLYCOPEPTIDASE; O GLYCANASE; SIALIDASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CELL STRAIN 3T3; CELL SURFACE; CONTROLLED STUDY; FIBROBLAST; LIGAND BINDING; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; ULTRACENTRIFUGATION; WESTERN BLOTTING; BINDING AFFINITY; MOLECULAR WEIGHT; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; SIGNAL TRANSDUCTION;

GALECTIN-3; MUC1; Β-CATENIN;

ANIMALS; BETA CATENIN; GALECTIN 3; MICE; MUCIN-1; NIH 3T3 CELLS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84896989265     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.02.008     Document Type: Article

References (42)

1. A. Danguy, I. Camby, R. Kiss, Galectins and cancer, Biochim. Biophys. Acta 1572 (2002) 285-293. (Pubitemid 35246351)
2. F.T. Liu, G.A. Rabinovich, Galectins as modulators of tumour progression, Nat. Rev. Cancer 5 (2005) 29-41. (Pubitemid 40052323)
3. S. Sato, R.C. Hughes, Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages, J. Biol. Chem. 269 (1994) 4424-4430.
4. I.K. Moutsatsos, M. Wade, M. Schindler, J.L. Wang, Endogenous lectins from cultured cells: nuclear localization of carbohydrate-binding protein 35 in proliferating 3T3 fibroblasts, Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 6452-6456.
5. A. Raz, D.G. Zhu, V. Hogan, N. Shah, T. Raz, R. Karkash, G. Pazerini, P. Carmi, Evidence for the role of 34-kDa galactoside-binding lectin in transformation and metastasis, Int. J. Cancer 46 (1990) 871-877.
6. T. Fukumori, N. Oka, Y. Takenaka, P. Nangia-Makker, E. Elsamman, T. Kasai, M. Shono, H.O. Kanayama, J. Ellerhorst, R. Lotan, A. Raz, Galectin-3 regulates mitochondrial stability and antiapoptotic function in response to anticancer drug in prostate cancer, Cancer Res. 66 (2006) 3114-3119.
7. J. Dumic, S. Dabelic, M. Flögel, Galectin-3: an open-ended story, Biochim. Biophys. Acta 1760 (2006) 616-635. (Pubitemid 44382499)
8. Y. Li, D. Liu, D. Chen, S. Kharbanda, D. Kufe, Human DF3/MUC1 carcinoma-associated protein functions as an oncogene, Oncogene 22 (2003) 6107-6110. (Pubitemid 37175889)
9. M.A. Hollingsworth, B.J. Swanson, Mucins in cancer: protection and control of the cell surface, Nat. Rev. Cancer 4 (2004) 45-60 (2004).
10. M.J. Ligtenberg, L. Kruijshaar, F. Buijs, M. van Meijer, S.V. Litvinov, J. Hilkens, Cell-associated episialin is a complex containing two proteins derived from a common precursor, J. Biol. Chem. 267 (1992) 6171-6177.
11. S. Parry, H.S. Silverman, K. McDermott, A. Willis, M.A. Hollingsworth, A. Harris, Identification of MUC1 proteolytic cleavage sites in vivo, Biochem. Biophys. Res. Commun. 283 (2001) 715-720. (Pubitemid 32917949)
12. J. Siddiqui, M. Abe, D. Hayes, E. Shani, E. Yunis, D. Kufe, Isolation and sequencing of a cDNA coding for the human DF3 breast carcinoma-associated antigen, Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 2320-2323. (Pubitemid 24315883)
13. L.G. Yu, N. Andrews, Q. Zhao, D. McKean, J.F. Williams, L.J. Connor, O.V. Gerasimenko, J. Hilkens, J. Hirabayashi, K. Kasai, J.M. Rhodes, Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion, J. Biol. Chem. 282 (2007) 773-781. (Pubitemid 47076627)
14. S. Ramasamy, S. Duraisamy, S. Barbashov, T. Kawano, S. Kharbanda, D. Kufe, The MUC1 and galectin-3 oncoproteins function in a microRNA-dependent regulatory loop, Mol. Cell 27 (2007) 992-1004. (Pubitemid 47488189)
15. Q. Zhao, M. Barclay, J. Hilkens, X. Guo, H. Barrow, J.M. Rhodes, L.G. Yu, Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis, Mol. Cancer 9 (2010) 154.
16. Q. Zhao, X. Guo, G.B. Nash, P.C. Stone, J. Hilkens, J.M. Rhodes, L.G. Yu, Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface, Cancer Res. 69 (2009) 6799-6806.
17. L. Huang, D. Chen, D. Liu, L. Yin, S. Kharbanda, D. Kufe, MUC1 oncoprotein blocks glycogen synthase kinase 3beta-mediated phosphorylation and degradation of beta-catenin, Cancer Res. 65 (2005) 10413-10422. (Pubitemid 41743735)
18. Y. Li, W.H. Yu, J. Ren, W. Chen, L. Huang, S. Kharbanda, M. Loda, D. Kufe, Heregulin targets gamma-catenin to the nucleolus by a mechanism dependent on the DF3/MUC1 oncoprotein, Mol. Cancer Res. 1 (2003) 765-775. (Pubitemid 37025595)
19. J. Ren, A. Bharti, D. Raina, W. Chen, R. Ahmad, D. Kufe, MUC1 oncoprotein is targeted to mitochondria by heregulin-induced activation of c-Src and themolecular chaperone HSP90, Oncogene 25 (2006) 20-31. (Pubitemid 43050000)
20. L. Huang, J. Ren, D. Chen, Y. Li, S. Kharbanda, D. Kufe, MUC1 cytoplasmic domain coactivates Wnt target gene transcription and confers transformation, Cancer Biol. Ther. 2 (2003) 702-706.
21. D. Raina, S. Kharbanda, D. Kufe, The MUC1 oncoprotein activates the anti-apoptotic phosphoinositide 3-kinase/Akt and Bcl-xL pathways in rat 3Y1 fibroblasts, J. Biol. Chem. 279 (2004) 20607-20612. (Pubitemid 38656454)
22. Y. Li, J. Ren, W. Yu, Q. Li, H. Kuwahara, L. Yin, K.L. Carraway, D. Kufe, The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and beta-catenin, J. Biol. Chem. 276 (2001) 35239-35242.
23. M.S. Lan, S.K. Batra, W.N. Qi, R.S. Metzgar, M.A. Hollingsworth, Cloning and sequencing of a human pancreatic tumor mucin cDNA, J. Biol. Chem. 265 (1990) 15294-15299.
24. J. Merlin, L. Stechly, S. de Beaucé, D. Monté, E. Leteurtre, I. van Seuningen, G. Huet, P. Pigny, Galectin-3 regulates MUC1 and EGFR cellular distribution and EGFR downstream pathways in pancreatic cancer cells, Oncogene 30 (2011) 2514-2525.
25. C.F. Roff, J.L. Wang, Endogenous lectins from cultured cells. Isolation and characterization of carbohydrate-binding proteins from 3T3 fibroblasts, J. Biol. Chem. 258 (1983) 10657-10663. (Pubitemid 14244326)
26. J. Nieminen, A. Kuno, J. Hirabayashi, S. Sato, Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer, J. Biol. Chem. 282 (2007) 1374-1383. (Pubitemid 47076550)
27. J.J. Rahn, Q. Shen, B.K. Mah, J.C. Hugh, MUC1 initiates a calcium signal after ligation by intercellular adhesion molecule-1, J. Biol. Chem. 279 (2004) 29386-29390. (Pubitemid 38915817)
28. Q. Shen, J.J. Rahn, J. Zhang, N. Gunasekera, X. Sun, A.R. Shaw, M.J. Hendzel, P. Hoffman, A. Bernier, J.C. Hugh, MUC1 initiates Src-CrkL-Rac1/Cdc42- mediated actin cytoskeletal protrusive motility after ligating intercellular adhesion molecule-1, Mol. Cancer Res. 6 (2008) 555-567. (Pubitemid 351521837)
29. E.P. Lillehoj, H. Kim, E.Y. Chun, K.C. Kim, Pseudomonas aeruginosa stimulates phosphorylation of the airway epithelial membrane glycoprotein Muc1 and activates MAP kinase, Am. J. Physiol. Lung Cell. Mol. Physiol. 287 (2004) L809-L815. (Pubitemid 39249394)
30. Y. Li, H. Kuwahara, J. Ren, G. Wen, D. Kufe, The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3 beta and beta-catenin, J. Biol. Chem. 276 (2001) 6061-6064.
31. J.A. Schroeder, M.C. Thompson, M.M. Gardner, S.J. Gendler, Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland, J. Biol. Chem. 276 (2001) 13057-13064.
32. M.R. Pochampalli, R.M. el Bejjani, J.A. Schroeder, MUC1 is a novel regulator of ErbB1 receptor trafficking, Oncogene 26 (2007) 1693-1701. (Pubitemid 46426203)
33. T.M. Connolly, J.W. Jacobs, C. Condra, An inhibitor of collagen-stimulated platelet activation from the salivary glands of the Haementeria officinalis leech. I. Identification, isolation, and characterization, J. Biol. Chem. 267 (1992) 6893-6898.
34. H. Inohara, S. Akahani, A. Raz, Galectin-3 stimulates cell proliferation, Exp. Cell Res. 245 (1998) 294-302. (Pubitemid 28565771)
35. J. Kopitz, C. von Reitzenstein, S. André, H. Kaltner, J. Uhl, V. Ehemann, M. Cantz, H.J. Gabius, Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3, J. Biol. Chem. 276 (2001) 35917-35923.
36. N. Maeda, N. Kawada, S. Seki, T. Arakawa, K. Ikeda, H. Iwao, H. Okuyama, J. Hirabayashi, K. Kasai, K. Yoshizato, Stimulation of proliferation of rat hepatic stellate cells by galectin-1 and galectin-3 through different intracellular signaling pathways, J. Biol. Chem. 278 (2003) 18938-18944. (Pubitemid 36799277)
37. V. Furtak, F. Hatcher, J. Ochieng, Galectin-3 mediates the endocytosisof beta-1 integrins by breast carcinoma cells, Biochem. Biophys. Res. Commun. 289 (2001) 845-850. (Pubitemid 34060081)
38. E.A. Partridge, C. Le Roy, G.M. Di Guglielmo, J. Pawling, P. Cheung, M. Granovsky, I.R. Nabi, J.L. Wrana, J.W. Dennis, Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis, Science 306 (2004) 120-124. (Pubitemid 39451953)
39. T. Tadokoro, M. Ikekita, T. Toda, H. Ito, T. Sato, R. Nakatani, Y. Hamaguchi, K. Furukawa, Involvement of Galectin-3 with vascular cell adhesion molecule-1 in growth regulation ofmouse BALB/3T3 cells, J. Biol. Chem. 284 (2009) 35556-35563.
40. J. Ochieng, D. Platt, L. Tait, V. Hogan, T. Raz, P. Carmi, A. Raz, Structure-function relationship of a recombinant human galactoside-binding protein, Biochemistry 32 (1993) 4455-4460. (Pubitemid 23137756)
41. S.H. Barondes, D.N. Cooper, M.A. Gitt, H. Leffler, Galectins. Structure and function of a large family of animal lectins, J. Biol. Chem. 269 (1994) 20807-20810.
42. N. Ahmad, H.J. Gabius, S. André, H. Kaltner, S. Sabesan, R. Roy, B. Liu, F. Macaluso, C.F. Brewer, Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes, J. Biol. Chem. 279 (2004) 10841-10847. (Pubitemid 38401573)