Tyrosine-phosphorylated galectin-3 protein is resistant to prostate-specific antigen (PSA) cleavage

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5192-5198

  Balan, Vitaly ^a   Nangia Makker, Pratima ^a   Kho, Dhong Hyo ^a   Wang, Yi ^a   Raz, Avraham ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; BIOLOGICAL PROCESS; CARBOHYDRATE BINDING; CARBOHYDRATE-RECOGNITION DOMAINS; CELL SURFACES; EXTRACELLULAR MATRICES; GLYCOCONJUGATES; HOMODIMERS; LIGAND-RECEPTOR BINDING; MULTIVALENCY; N-TERMINAL DOMAINS; PENTAMERS; PHOSPHATASE AND TENSIN HOMOLOGUE DELETED ON CHROMOSOME 10; POST-TRANSLATIONAL MODIFICATIONS; PROSTATE CANCERS; PROSTATE CELLS; PROSTATE SPECIFIC ANTIGEN; SELF-ASSOCIATIONS; SERINE PROTEASE; THERAPEUTIC TARGETS; TUMOR CELLS; TUMOR PROGRESSIONS; UNIQUE FEATURES;

AMINO ACIDS; ANTIGENS; ASSOCIATION REACTIONS; CELL MEMBRANES; DISEASES; LIGANDS; OLIGOMERIZATION; OLIGOMERS; PHOSPHORYLATION; TUMORS; UROLOGY;

CARBOHYDRATES;

ABELSON KINASE; GALECTIN 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROSTATE SPECIFIC ANTIGEN;

ARTICLE; BINDING AFFINITY; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; LIGAND BINDING; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

CELL LINE, TUMOR; CHEMOTAXIS; EXTRACELLULAR SPACE; GALECTIN 3; HUMANS; MODELS, MOLECULAR; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROSTATE-SPECIFIC ANTIGEN; PROTEIN CONFORMATION; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-ABL; PTEN PHOSPHOHYDROLASE; TYROSINE;

EID: 84863147748     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C111.331686     Document Type: Article

References (45)

1. Huflejt, M. E., Turck, C. W., Lindstedt, R., Barondes, S. H., and Leffler, H. (1993) L-29, a soluble lactose-binding lectin, is phosphorylated on serine 6 and serine 12 in vivo and by casein kinase I. J. Biol. Chem. 268, 26712-26718 (Pubitemid 23361758)
2. Balan, V., Nangia-Makker, P., Jung, Y. S., Wang, Y., and Raz, A. (2010) Galectin-3: a novel substrate for c-Abl kinase. Biochim. Biophys. Acta 1803, 1198-1205
3. Barondes, S. H., Cooper, D. N., Gitt, M. A., and Leffler, H. (1994) Galectins: structure and function of a large family of animal lectins. J. Biol. Chem. 269, 20807-20810
4. Ahmad, N., Gabius, H. J., André, S., Kaltner, H., Sabesan, S., Roy, R., Liu, B., Macaluso, F., and Brewer, C. F. (2004) Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J. Biol. Chem. 279, 10841-10847 (Pubitemid 38401573)
5. Barondes, S. H., Castronovo, V., Cooper, D. N., Cummings, R. D., Drickamer, K., Feizi, T., Gitt, M. A., Hirabayashi, J., Hughes, C., and Kasai, K. (1994) Galectins: a family of animal β-galactoside-binding lectins. Cell 76, 597-598 (Pubitemid 24070645)
6. Mazurek, N., Conklin, J., Byrd, J. C., Raz, A., and Bresalier, R. S. (2000) Phosphorylation of the β-galactoside-binding protein galectin-3 modulates binding to its ligands. J. Biol. Chem. 275, 36311-36315
7. Mazurek, N., Sun, Y. J., Liu, K. F., Gilcrease, M. Z., Schober, W., Nangia-Makker, P., Raz, A., and Bresalier, R. S. (2007) Phosphorylated galectin-3 mediates tumor necrosis factor-related apoptosis-inducing ligand signaling by regulating phosphatase and tensin homologue deleted on chromosome 10 in human breast carcinoma cells. J. Biol. Chem. 282, 21337-21348 (Pubitemid 47099965)
8. Mazurek, N., Sun, Y. J., Price, J. E., Ramdas, L., Schober, W., Nangia-Makker, P., Byrd, J. C., Raz, A., and Bresalier, R. S. (2005) Phosphorylation of galectin-3 contributes to malignant transformation of human epithelial cells via modulation of unique sets of genes. Cancer Res. 65, 10767-10775 (Pubitemid 41713345)
9. Yoshii, T., Fukumori, T., Honjo, Y., Inohara, H., Kim, H. R., and Raz, A. (2002) Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J. Biol. Chem. 277, 6852-6857 (Pubitemid 34953068)
10. Nangia-Makker, P., Balan, V., and Raz, A. (2008) Regulation of tumor progression by extracellular galectin-3. Cancer Microenviron. 1, 43-51
11. Nangia-Makker, P., Raz, T., Tait, L., Hogan, V., Fridman, R., and Raz, A. (2007) Galectin-3 cleavage: a novel surrogate marker for matrix metalloproteinase activity in growing breast cancers. Cancer Res. 67, 11760-11768
12. Nangia-Makker, P., Wang, Y., Raz, T., Tait, L., Balan, V., Hogan, V., and Raz, A. (2010) Cleavage of galectin-3 by matrix metalloproteases induces angiogenesis in breast cancer. Int. J. Cancer 127, 2530-2541
13. Rabinovich, G. A., Toscano, M. A., Jackson, S. S., and Vasta, G. R. (2007) Functions of cell surface galectin-glycoprotein lattices. Curr. Opin. Struct. Biol. 17, 513-520 (Pubitemid 350019014)
14. Ochieng, J., Green, B., Evans, S., James, O., and Warfield, P. (1998) Modulation of the biological functions of galectin-3 by matrix metalloproteinases. Biochim. Biophys. Acta 1379, 97-106 (Pubitemid 28045559)
15. Ochieng, J., Fridman, R., Nangia-Makker, P., Kleiner, D. E., Liotta, L. A., Stetler-Stevenson, W. G., and Raz, A. (1994) Galectin-3 is a novel substrate for human matrix metalloproteinases-2 and -9. Biochemistry 33, 14109-14114 (Pubitemid 24382354)
16. Pelletier, I., and Sato, S. (2002) Specific recognition and cleavage of galectin-3 by Leishmania major through species-specific polygalactose epitope. J. Biol. Chem. 277, 17663-17670 (Pubitemid 34967570)
17. Karlsson, A., Follin, P., Leffler, H., and Dahlgren, C. (1998) Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils. Blood 91, 3430-3438 (Pubitemid 28193896)
18. Hughes, R. C. (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473, 172-185
19. Menon, R. P., and Hughes, R. C. (1999) Determinants in the N-terminal domains of galectin-3 for secretion by a novel pathway circumventing the endoplasmic reticulum-Golgi complex. Eur. J. Biochem. 264, 569-576 (Pubitemid 29424464)
20. Nakahara, S., Oka, N., Wang, Y., Hogan, V., Inohara, H., and Raz, A. (2006) Characterization of the nuclear import pathways of galectin-3. Cancer Res. 66, 9995-10006 (Pubitemid 44672052)
21. Nakahara, S., Hogan, V., Inohara, H., and Raz, A. (2006) Importin-mediated nuclear translocation of galectin-3. J. Biol. Chem. 281, 39649-39659 (Pubitemid 46041924)
22. Merseburger, A. S., Kramer, M. W., Hennenlotter, J., Simon, P., Knapp, J., Hartmann, J. T., Stenzl, A., Serth, J., and Kuczyk, M. A. (2008) Involvement of decreased galectin-3 expression in the pathogenesis and progression of prostate cancer. Prostate 68, 72-77
23. Wang, Y., Nangia-Makker, P., Tait, L., Balan, V., Hogan, V., Pienta, K. J., and Raz, A. (2009) Regulation of prostate cancer progression by galectin-3. Am. J. Pathol. 174, 1515-1523
24. Kim, J., and Coetzee, G. A. (2004) Prostate-specific antigen gene regulation by androgen receptor. J. Cell Biochem. 93, 233-241 (Pubitemid 44264201)
25. Liang, C. C., Park, A. Y., and Guan, J. L. (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2, 329-333 (Pubitemid 47040047)
26. Li, X., Ma, Q., Wang, J., Liu, X., Yang, Y., Zhao, H., Wang, Y., Jin, Y., Zeng, J., Li, J., Song, L., Li, X., Li, P., Qian, X., and Cao, C. (2010) c-Abl and Arg tyrosine kinases regulate lysosomal degradation of the oncoprotein galectin-3. Cell Death Differ. 17, 1277-1287
27. Yamazaki, K., Kawai, A., Kawaguchi, M., Hibino, Y., Li, F., Sasahara, M., Tsukada, K., and Hiraga, K. (2001) Simultaneous induction of galectin-3 phosphorylated on tyrosine residue, p21WAF1/Cip1/Sdi1 and the proliferating cell nuclear antigen at a distinctive period of repair of hepatocytes injured by CCl4. Biochem. Biophys. Res. Commun. 280, 1077-1084 (Pubitemid 32924450)
28. Menon, S., Kang, C. M., and Beningo, K. A. (2011) Galectin-3 secretion and tyrosine phosphorylation is dependent on the calpain small subunit, calpain 4. Biochem. Biophys. Res. Commun. 410, 91-96
29. Saraswati, S., Block, A. S., Davidson, M. K., Rank, R. G., Mahadevan, M., and Diekman, A. B. (2011) Galectin-3 is a substrate for prostate-specific antigen (PSA) in human seminal plasma. Prostate 71, 197-208
30. Yang, R. Y., Hill, P. N., Hsu, D. K., and Liu, F. T. (1998) Role of the C-terminal lectin domain in self-association of galectin-3. Biochemistry 37, 4086-4092 (Pubitemid 28166430)
31. Rabinovich, G. A., and Toscano, M. A. (2009) Turning "sweet" on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 9, 338-352
32. Barboni, E. A., Bawumia, S., Henrick, K., and Hughes, R. C. (2000) Molecular modeling and mutagenesis studies of the N-terminal domains of galectin-3: evidence for participation with the C-terminal carbohydrate recognition domain in oligosaccharide binding. Glycobiology 10, 1201-1208
33. Sirvent, A., Benistant, C., and Roche, S. (2008) Cytoplasmic signaling by the c-Abl tyrosine kinase in normal and cancer cells. Biol. Cell 100, 617-631
34. Davoodpour, P., Landström, M., and Welsh, M. (2007) Reduced tumor growth in vivo and increased c-Abl activity in PC3 prostate cancer cells overexpressing the Shb adapter protein. BMC Cancer 7, 161
35. Mulholland, D. J., Dedhar, S., Wu, H., and Nelson, C. C. (2006) PTEN and GSK3β: key regulators of progression to androgen-independent prostate cancer. Oncogene 25, 329-337 (Pubitemid 43117618)
36. Dong, J. T. (2006) Prevalent mutations in prostate cancer. J. Cell Biochem. 97, 433-447
37. Chow, L. M., and Baker, S. J. (2006) PTEN function in normal and neoplastic growth. Cancer Lett. 241, 184-196 (Pubitemid 44163047)
38. Nangia-Makker, P., Honjo, Y., Sarvis, R., Akahani, S., Hogan, V., Pienta, K. J., and Raz, A. (2000) Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am. J. Pathol. 156, 899-909 (Pubitemid 30626949)
39. Newlaczyl, A. U., and Yu, L. G. (2011) Galectin-3: a jack-of-all-trades in cancer. Cancer Lett. 313, 123-128
40. Zhao, Q., Guo, X., Nash, G. B., Stone, P. C., Hilkens, J., Rhodes, J. M., and Yu, L. G. (2009) Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res. 69, 6799-6806
41. Lehr, J. E., and Pienta, K. J. (1998) Preferential adhesion of prostate cancer cells to a human bone marrow endothelial cell line. J. Natl. Cancer Inst. 90, 118-123 (Pubitemid 28114412)
42. Glinsky, V. V., Glinsky, G. V., Glinskii, O. V., Huxley, V. H., Turk, J. R., Mossine, V. V., Deutscher, S. L., Pienta, K. J., and Quinn, T. P. (2003) Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Cancer Res. 63, 3805-3811 (Pubitemid 36793070)
43. Geiger, B., and Yamada, K. M. (2011) Molecular architecture and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 3, pii: a005033
44. Thijssen, V. L., Postel, R., Brandwijk, R. J., Dings, R. P., Nesmelova, I., Satijn, S., Verhofstad, N., Nakabeppu, Y., Baum, L. G., Bakkers, J., Mayo, K. H., Poirier, F., and Griffioen, A. W. (2006) Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc. Natl. Acad. Sci. U.S.A. 103, 15975-15980 (Pubitemid 44657577)
45. Stillman, B. N., Hsu, D. K., Pang, M., Brewer, C. F., Johnson, P., Liu, F. T., and Baum, L. G. (2006) Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J. Immunol. 176, 778-789 (Pubitemid 43099674)