The roles of Versican V1 and V2 isoforms in cell proliferation and apoptosis

Molecular Biology of the Cell

Volumn 16, Issue 3, 2005, Pages 1330-1340

  Sheng, Wang ^a,b   Wang, Guizhi ^a,b   Wang, Yelina ^a,b   Liang, Jiyong ^a,b   Wen, Jianping ^a   Zheng, Peng Sheng ^a,b   Wu, Yaojiong ^a,b   Lee, Vivian ^a,b   Slingerland, Joyce ^a,b   Dumont, Dan ^a,b   Yang, Burton B ^a,b  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; CYCLIN E; EPIDERMAL GROWTH FACTOR RECEPTOR; HYALURONIC ACID; PHOSPHATASE; PROTEIN BAD; PROTEIN P27; PROTEOCHONDROITIN SULFATE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VERSICAN; VERSICAN V1; VERSICAN V2;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROBLAST; FLOW CYTOMETRY; GENE SILENCING; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTO ONCOGENE; UBIQUITINATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CERCOPITHECUS AETHIOPS; COS CELLS; CULTURE MEDIA, SERUM-FREE; CYCLIN E; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DNA PRIMERS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXTRACELLULAR MATRIX; FIBROBLASTS; FLOW CYTOMETRY; HYALURONIC ACID; IMMUNOPRECIPITATION; LECTINS, C-TYPE; MICE; MODELS, GENETIC; NIH 3T3 CELLS; ONCOGENE PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEOCHONDROITIN SULFATES; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN; VERSICANS;

EID: 20044368972     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-04-0295     Document Type: Article

References (38)

1. Ang, L. C., Zhang, Y., Cao, L., Yang, B. L., Young, B., Kiani, C., Lee, V., Allan, K., and Yang, B. B. (1999). Versican enhances locomotion of astrocytoma cells and reduces cell adhesion through its G1 domain. J. Neuropathol. Exp. Neurol. 58, 597-605.
2. Blain, S. W., Scher, H. I., Cordon-Cardo, C., and Koff, A. (2003). p27 as a target for cancer therapeutics. Cancer Cell 3, 111-115.
3. Carrano, A. C., Eytan, E., Hershko, A., and Pagano, M. (1999). SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1, 193-199.
4. Cattaruzza, S., Schiappacassi, M., Kimata, K., Colombatti, A., and Perris, R. (2004). The globular domains of PG-M/versican modulate the proliferation-apoptosis equilibrium and invasive capabilities of tumor cells. FASEB J. 18, 779-781.
5. Cattaruzza, S., Schiappacassi, M., Ljungberg-Rose, A., Spessotto, P., Perissinotto, D., Morgelin, M., Mucignat, M. T., Colombatti, A., and Perris, R. (2002). Distribution of PG-M/versican variants in human tissues and de novo expression of isoform V3 upon endothelial cell activation, migration, and neo-angiogenesis in vitro. J. Biol. Chem. 277, 47626-47635.
6. Catzavelos, C. et al. (1997). Decreased levels of the cell-cycle inhibitor p27Kip1 protein: prognostic implications in primary breast cancer. Nat. Med. 3, 227-230.
7. Chen, J., Freeman, A., Liu, J., Dai, Q., and Lee, R. M. (2002a). The apoptotic effect of HA14-1, a Bcl-2-interacting small molecular compound, requires Bax translocation and is enhanced by PK11195. Mol. Cancer Ther. 1, 961-967.
8. Chen, L., Wu, Y., Lee, V., Kiani, C., Adams, M. E., Yao, Y., and Yang, B. B. (2002b). The folded modules of aggrecan G3 domain exert two separable functions in glycosaminoglycan modification and product secretion. J. Biol. Chem. 277, 2657-2665.
9. Chen, L., Yang, B. L., Wu, Y., Yee, A., and Yang, B. B. (2003). G3 domains of aggrecan and PG-M/versican form intermolecular disulfide bonds that stabilize cell-matrix interaction. Biochemistry 42, 8332-8341.
10. Chiarle, R. et al. (2000). Increased proteasome degradation of cyclin-dependent kinase inhibitor p27 is associated with a decreased overall survival in mantle cell lymphoma. Blood 95, 619-626.
11. Di Fiore, P. P., Pierce, J. H., Kraus, M. H., Segatto, O., King, C. R., and Aaronson, S. A. (1987). erbB-2 is a potent oncogene when overexpressed in N1H/3T3 cells. Science 237, 178-182.
12. Fukuda, M., Gotoh, I., Adachi, M., Gotoh, Y., and Nishida, E. (1997). A novel regulatory mechanism in the mitogen-activated protein (MAP) kinase cascade. Role of nuclear export signal of MAP kinase kinase. J. Biol. Chem. 272, 32642-32648.
13. Henderson, D. J., Ybot-Gonzalez, P., and Copp, A. J. (1997). Over-expression of the chondroitin sulphate proteoglycan versican is associated with defective neural crest migration in the Pax3 mutant mouse (splotch). Mech. Dev. 69, 39-51.
14. Ingber, D. E., and Folkman, J. (1989). Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J. Cell Biol. 109, 317-330.
15. Ito, K., Shinomura, T., Zako, M., Ujita, M., and Kimata, K. (1995). Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J. Biol. Chem. 270, 958-965.
16. Kiani, C., Chen, L., Lee, V., Zheng, P. S., Wu, Y., Wen, J., Cao, L., Adams, M. E., Sheng, W., and Yang, B. B. (2003). Identification of the motifs and amino acids in aggrecan G1 and G2 domains involved in product secretion. Biochemistry 42, 7226-7237.
17. Landolt, R. M., Vaughan, L., Winterhalter, K. H., and Zimmermann, D. R. (1995). Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development 121, 2303-2312.
18. Lee, V., Cao, L., Zhang, Y., Kiani, C., Adams, M. E., and Yang, B. B. (2000). The roles of matrix molecules in mediating chondrocyte aggregation, attachment, and spreading. J. Cell. Biochem. 79, 322-333.
19. Lemire, J. M., Braun, K. R., Maurel, P., Kaplan, E. D., Schwartz, S. M., and Wight, T. N. (1999). Versican/PG-M isoforms in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 19, 1630-1639.
20. Maruta, H., and Burgess, A. W. (1994). Regulation of the Ras signalling network. Bioessays 16, 489-496.
21. Merlino, G. T., Xu, Y. H., Kichert, N., Clark, A. J., Ishii, S., Banks-Schlegel, S., and Pastan, I. (1985). Elevated EGF receptor gene copy number and expression in a squamous carcinoma cell line. J. Clin. Invest. 75, 1077-1079.
22. Ricciardelli, C., Brooks, J. H., Suwiwat, S., Sakko, A. J., Mayne, K., Raymond, W. A., Seshadri, R., LeBaron, R. G., and Horsfall, D. J. (2002). Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with node-negative primary breast cancer. Clin. Cancer Res. 8, 1054-1060.
23. Sandhu, C., Garbe, J., Bhattacharya, N., Daksis, J., Pan, C. H., Yaswen, P., Koh, J., Slingerland, J. M., and Stampfer, M. R. (1997). Transforming growth factor beta stabilizes p15INK4B protein, increases p15INK4B-cdk4 complexes, and inhibits cyclin D1-cdk4 association in human mammary epithelial cells. Mol. Cell. Biol. 17, 2458-2467.
24. Sandy, J. D. et al. (2001). Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J. Biol. Chem. 276, 13372-13378.
25. Schmalfeldt, M., Bandtlow, C. E., Dours-Zimmermann, M. T., Winterhalter, K. H., and Zimmermann, D. R. (2000). Brain derived versican V2 is a potent inhibitor of axonal growth. J. Cell Sci. 113, 807-816.
26. Schmalfeldt, M., Dours-Zimmermann, M. T., Winterhalter, K. H., and Zimmermann, D. R. (1998). Versican V2 is a major extracellular matrix component of the mature bovine brain. J. Biol. Chem. 273, 15758-15764.
27. Sheaff, R. J., Groudine, M., Gordon, M., Roberts, J. M., and Clurman, B. E. (1997). Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 11, 1464-1478.
28. Shinomura, T., Nishida, Y., Ito, K., and Kimata, K. (1993). cDNA cloning of PG-M, a large chondroitin sulfate proteoglycan expressed during chondrogenesis in chick limb buds. Alternative spliced multiforms of PG-M and their relationships to versican. J. Biol. Chem. 268, 14461-14469.
29. Slingerland, J. M., Hengst, L., Pan, C. H., Alexander, D., Stampfer, M. R., and Reed, S. I. (1994). A novel inhibitor of cyclin-Cdk activity detected in transforming growth factor beta-arrested epithelial cells. Mol. Cell. Biol. 24, 3683-3694.
30. Touab, M., Villena, J., Barranco, C., Arumi-Uria, M., and Bassols, A. (2002). Versican is differentially expressed in human melanoma and may play a role in tumor development. Am. J. Pathol. 260, 549-557.
31. Wu, Y., Chen, L., Cao, L., Sheng, W., and Yang, B. B. (2004a). Overexpression of the C-terminal PG-M/versican domain impairs growth of tumor cells by intervening in the interaction between EGF receptor and {beta}1-integrin. J. Cell Sci. 227, 2227-2237.
32. Wu, Y., Chen, L., Zheng, P. S., and Yang, B. B. (2002). beta 1-Integrin-mediated glioma cell adhesion and free radical-induced apoptosis are regulated by binding to a C-terminal domain of PG-M/versican. J. Biol. Chem. 277, 12294-12301.
33. Wu, Y., Sheng, W., Chen, L., Dong, H., Lee, V., Lu, F., Wong, C. S., Lu, W. Y., and Yang, B. B. (2004b). Versican V1 isoform induces neuronal differentiation and promotes neurite outgrowth. Mol. Biol. Cell 25, 2093-2104.
34. Yang, B. L., Cao, L., Kiani, C, Lee, V., Zhang, Y., Adams, M. E., and Yang, B. B. (2000). Tandem repeats are involved in G1 domain inhibition of versican expression and secretion and the G3 domain enhances glycosaminoglycan modification and product secretion via the complement-binding protein-like motif. J. Biol. Chem. 275, 21255-21261.
35. Zhang, Y., Cao, L., Kiani, C. G., Yang, B. L., and Yang, B. B. (1998a). The G3 domain of versican inhibits mesenchymal chondrogenesis via the EGF-like motifs. J. Biol. Chem. 273, 33054-33063.
36. Zhang, Y., Cao, L., Yang, B. L., and Yang, B. B. (1998b). The G3 domain of versican enhances cell proliferation via epidermal growth factor-like motifs. J. Biol. Chem. 273, 21342-21351.
37. Zheng, P. S., Vais, D., Lapierre, D., Liang, Y. Y., Lee, V., Yang, B. L., and Yang, B. B. (2004a). PG-M/versican binds to P-selectin glycoprotein ligand-1 and mediates leukocyte aggregation. J. Cell Sci. 117, 5887-5895.
38. Zheng, P. S., Wen, J., Ang, L. C., Sheng, W., Viloria-Petit, A., Wang, Y., Wu, Y., Kerbel, R. S., and Yang, B. B. (2004b). Versican/PG-M G3 domain promotes tumor growth and angiogenesis. FASEB J. 18, 754-756.