Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells

Journal of Cell Biology

Volumn 171, Issue 4, 2005, Pages 729-738

  Ding, Kan ^a   Lopez Burks, Martha ^a   Sánchez Duran, José Antonio ^a   Korc, Murray ^b   Lander, Arthur D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GLYPICAN; MATRILYSIN; SYNDECAN 1;

ARTICLE; BREAST CANCER; CANCER CELL; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MITOGENESIS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION;

CELL LINE, TUMOR; CELL MEMBRANE; CULTURE MEDIA, SERUM-FREE; DISEASE PROGRESSION; DNA; ENZYME ACTIVATION; ENZYME INHIBITORS; FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCANS; GROWTH SUBSTANCES; HEPARAN SULFATE PROTEOGLYCANS; HEPARITIN SULFATE; HUMANS; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 7; MEMBRANE GLYCOPROTEINS; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; PROTEOGLYCANS; SYNDECAN-1; SYNDECANS; TIME FACTORS; TRANSFECTION; TRYPSIN; UP-REGULATION;

EID: 27944469616     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200508010     Document Type: Article

References (72)

1. Alexander, C.M., F. Reichsman, M.T. Hinkes, J. Lincecum, K.A. Becker, S. Cumberledge, and M. Bernfield. 2000. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet. 25:329-332.
2. Asundi, V.K., R. Erdman, R.C. Stahl, and D.J. Carey. 2003. Matrix metalloproteinase-dependent shedding of syndecan-3, a transmembrane heparan sulfate proteoglycan, in Schwann cells. J. Neurosci. Res. 73:593-602.
3. Aviezer, D., and A. Yayon. 1994. Heparin-dependent binding and autophosphorylation of epidermal growth factor (EGF) receptor by heparin-binding EGF-like growth factor but not by EGF. Proc. Natl. Acad. Sci. USA. 91:12173-12177.
4. Barbareschi, M., P. Maisonneuve, D. Aldovini, M.G. Cangi, L. Pecciarini, F. Angelo Mauri, S. Veronese, O. Caffo, A. Lucenti, P.D. Palma, et al. 2003. High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer. 98:474-483.
5. Bellaiche, Y., I. The, and N. Perrimon. 1998. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature. 394:85-88.
6. Bellin, R., I. Capila, J. Lincecum, P.W. Park, O. Reizes, and M.R. Bernfield. 2002. Unlocking the secrets of syndecans: transgenic organisms as a potential key. Glycoconj. J. 19:295-304.
7. Bernfield, M., M. Götte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:729-777.
8. Bhanot, P., and V. Nussenzweig. 2002. Plasmodium yoelii sporozoites infect syndecan-1 deficient mice. Mol. Biochem. Parasitol. 123:143-144.
9. Brandan, E., D.J. Carey, J. Larrain, F. Melo, and A. Campos. 1996. Synthesis and processing of glypican during differentiation of skeletal muscle cells. Eur. J. Cell Biol. 71:170-176.
10. Conejo, J.R., J. Kleeff, A. Koliopanos, K. Matsuda, Z.W. Zhu, H. Goecke, N. Bicheng, A. Zimmermann, M. Korc, H. Friess, and M.W. Buchler. 2000. Syndecan-1 expression is up-regulated in pancreatic but not in other gastrointestinal cancers. Int. J. Cancer. 88:12-20.
11. Crabbe, T., F. Willenbrock, D. Eaton, P. Hynds, A.F. Carne, G. Murphy, and A.J. Docherty. 1992. Biochemical characterization of matrilysin. Activation conforms to the stepwise mechanisms proposed for other matrix metalloproteinases. Biochemistry. 31:8500-8507.
12. Crawford, H.C., C.R. Scoggins, M.K. Washington, L.M. Matrisian, and S.D. Leach. 2002. Matrix metalloproteinase-7 is expressed by pancreatic cancer precursors and regulates acinar-to-ductal metaplasia in exocrine pancreas. J. Clin. Invest. 109:1437-1444.
13. Desbordes, S.C., and B. Sanson. 2003. The glypican Dally-like is required for Hedgehog signalling in the embryonic epidermis of Drosophila. Development. 130:6245-6255.
14. Endo, K., T. Takino, H. Miyamori, H. Kinsen, T. Yoshizaki, M. Furukawa, and H. Sato. 2003. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278:40764-40770.
15. Fitzgerald, M.L., Z. Wang, P.W. Park, G. Murphy, and M. Bernfield. 2000. Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148:811-824.
16. Friess, H., P. Berberat, M. Schilling, J. Kunz, M. Korc, and M.W. Buchler. 1996. Pancreatic cancer: the potential clinical relevance of alterations in growth factors and their receptors. J. Mol. Med. 74:35-42.
17. Fujimoto, Y., and Y. Kohgo. 1998. Alteration of genomic structure and/or expression of cancer associated genes in hepatocellular carcinoma. Rinsho Byori. 46:9-14.
18. Fujise, M., S. Takeo, K. Kamimura, T. Matsuo, T. Aigaki, S. Izumi, and H. Nakato. 2003. Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development. 130:1515-1522.
19. Fukushima, H., H. Yamamoto, F. Itoh, H. Nakamura, Y. Min, S. Horiuchi, S. Iku, S. Sasaki, and K. Imai. 2001. Association of matrilysin mRNA expression with K-ras mutations and progression in pancreatic ductal adenocarcinomas. Carcinogenesis. 22:1049-1052.
20. Galli, A., A. Roure, R. Zeller, and R. Dono. 2003. Glypican 4 modulates FGF signalling and regulates dorsoventral forebrain patterning in Xenopus embryos. Development. 130:4919-4929.
21. Grisaru, S., D. Cano-Gauci, J. Tee, J. Filmus, and N.D. Rosenblum. 2001. Glypican-3 modulates BMP- and FGF-mediated effects during renal branching morphogenesis. Dev. Biol. 231:31-46.
22. Haddad, R., K.E. Lipson, and C.P. Webb. 2001. Hepatocyte growth factor expression in human cancer and therapy with specific inhibitors. Anticancer Res. 21:4243-4252.
23. Harada, K., S. Masuda, M. Hirano, and Y. Nakanuma. 2003. Reduced expression of syndecan-1 correlates with histologic dedifferentiation, lymph node metastasis, and poor prognosis in intrahepatic cholangiocarcinoma. Hum. Pathol. 34:857-863.
24. Holen, I., N.L. Drury, P.G. Hargreaves, and P.I. Croucher. 2001. Evidence of a role for a non-matrix-type metalloproteinase activity in the shedding of syndecan-1 from human myeloma cells. Br. J. Haematol. 114:414-421.
25. Ishiguro, K., T. Kojima, and T. Muramatsu. 2002. Syndecan-4 as a molecule involved in defense mechanisms. Glycoconj. J. 19:315-318.
26. Jackson, S.M., H. Nakato, M. Sugiura, A. Jannuzi, R. Oakes, V. Kaluza, C. Golden, and S.B. Selleck. 1997. dally, a Drosophila glypican, controls cellular responses to the TGF-β-related morphogen, Dpp. Development. 124:4113-4120.
27. Kainulainen, V., H. Wang, C. Schick, and M. Bernfield. 1998. Syndecans, heparan sulfate proteoglycans, maintain the proteolytic balance of acute wound fluids. J. Biol. Chem. 273:11563-11569.
28. Kaksonen, M., I. Pavlov, V. Voikar, S.E. Lauri, A. Hienola, R. Riekki, M. Lakso, T. Taira, and H. Rauvala. 2002. Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol. Cell. Neurosci. 21:158-172.
29. Kleeff, J., T. Ishiwata, A. Kumbasar, H. Friess, M.W. Büchler, A.D. Lander, and M. Korc. 1998. The cell surface heparan sulfate proteoglycan glypican-1 is an essential regulator of growth factor action in pancreatic carcinoma cells, and is overexpressed in human pancreatic cancer. J. Clin. Invest. 102:1662-1673.
30. Kleeff, J., S. Wildi, A. Kumbasar, H. Friess, A.D. Lander, and M. Korc. 1999. Stable transfection of a glypican-1 antisense construct decreases tumorigenicity in PANC-1 pancreatic carcinoma cells. Pancreas. 19:281-288.
31. Lander, A.D., and S.B. Selleck. 2000. The elusive functions of proteoglycans: in vivo veritas. J. Cell Biol. 148:227-232.
32. Langford, J.K., Y. Yang, T. Kieber-Emmons, and R.D. Sanderson. 2005. Identification of an invasion regulatory domain within the core protein of syndecan-1. J. Biol. Chem. 280:3467-3473.
33. Larrain, J., J. Alvarez, J.R. Hassell, and E. Brandan. 1997. Expression of perlecan, a proteoglycan that binds myogenic inhibitory basic fibroblast growth factor, is down regulated during skeletal muscle differentiation. Exp. Cell Res. 234:405-412.
34. Leask, A., and T. Stearns. 1998. Expression of amino- and carboxyl-terminal gamma- and alpha-tubulin mutants in cultured epithelial cells. J. Biol. Chem. 273:2661-2668.
35. LeRoith, D., and C.T. Roberts Jr. 2003. The insulin-like growth factor system and cancer. Cancer Lett. 195:127-137.
36. Li, Q., and J.A. Loeb. 2001. Neuregulin-heparan-sulfate proteoglycan interactions produce sustained erbB receptor activation required for the induction of acetylcholine receptors in muscle. J. Biol. Chem. 276:38068-38075.
37. Li, Q., P.W. Park, C.L. Wilson, and W.C. Parks. 2002. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell. 111:635-646.
38. Liu, W., E.D. Litwack, M.J. Stanley, J.K. Langford, A.D. Lander, and R.D. Sanderson. 1996. Heparan sulfate proteoglycans as anti-invasive molecules. Syndecans and glypican have distinct functions. J. Biol. Chem. 273:22825-22832.
39. Lobb, R.R., and J.W. Fett. 1984. Purification of two distinct growth factors from bovine neural tissue by heparin affinity chromatography. Biochemistry. 23:6295-6299.
40. Matsuda, K., H. Maruyama, F. Guo, J. Kleeff, J. Itakura, Y. Matsumoto, A.D. Lander, and M. Korc. 2001. Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res. 61:5562-5569.
41. Mendelsohn, J., and J. Baselga. 2000. The EGF receptor family as targets for cancer therapy. Oncogene. 19:6550-6565.
42. Nackaerts, K., E. Verbeken, G. Deneffe, B. Vanderschueren, M. Demedts, and G. David. 1997. Heparan sulfate proteoglycan expression in human lung-cancer cells. Int. J. Cancer. 74:335-345.
43. Nakamura, H., S. Horita, N. Senmaru, Y. Miyasaka, T. Gohda, Y. Inoue, M. Fujita, T. Meguro, T. Morita, and K. Nagashima. 2002. Association of matrilysin expression with progression and poor prognosis in human pancreatic adenocarcinoma. Oncol. Rep. 9:751-755.
44. Nakatsura, T., T. Kageshita, S. Ito, K. Wakamatsu, M. Monji, Y. Ikuta, S. Senju, T. Ono, and Y. Nishimura. 2004. Identification of glypican-3 as a novel tumor marker for melanoma. Clin. Cancer Res. 10:6612-6621.
45. Park, P.W., O. Reizes, and M. Bernfield. 2000. Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J. Biol. Chem. 275:29923-29926.
46. Perrimon, N., and M. Bernfield. 2000. Specificities of heparan sulphate proteoglycans in developmental processes. Nature. 404:725-728.
47. Pilia, G., R.M. Hughes-Benzie, A. MacKenzie, P. Baybayan, E.Y. Chen, R. Huber, G. Neri, A. Cao, A. Foarabosco, and D. Schlessinger. 1996. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel over-growth syndrome. Nat. Genet. 12:241-247.
48. Pulkkinen, J.O., M. Penttinen, M. Jalkanen, P. Klemi, and R. Grenman. 1997. Syndecan-1: a new prognostic marker in laryngeal cancer. Acta Otolaryngol. 117:312-315.
49. Qiao, D., K. Meyer, C. Mundhenke, S.A. Drew, and A. Friedl. 2003. Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 signaling in brain endothelial cells. Specific role for glypican-1 in glioma angiogenesis. J. Biol. Chem. 278:16045-16053.
50. Rapraeger, A., A. Krufka, and B.B. Olwin. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science. 252:1705-1708.
51. Reizes, O., S.C. Benoit, A.D. Strader, D.J. Clegg, S. Akunuru, and R.J. Seeley. 2003. Syndecan-3 modulates food intake by interacting with the melanocortin/AgRP pathway. Ann. NY Acad. Sci. 994:66-73.
52. Steigemann, P., A. Molitor, S. Fellert, H. Jackle, and G. Vorbruggen. 2004. Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol. 14:225-230.
53. Steinfeld, R., H. Van Den Berghe, and G. David. 1996. Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol. 133:405-416.
54. Subramanian, S.V., M.L. Fitzgerald, and M. Bernfield. 1997. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J. Biol. Chem. 272:14713-14720.
55. Tanaka, A., K. Miyamoto, N. Minamino, M. Takeda, B. Sato, H. Matsuo, and K. Matsumoto. 1992. Cloning and characterization of an androgen-induced growth factor essential for the androgen-dependent growth of mouse mammary carcinoma cells. Proc. Natl. Acad. Sci. USA. 89:8928-8932.
56. Tsuda, M., K. Kamimura, H. Nakato, M. Archer, W. Staatz, B. Fox, M. Humphrey, S. Olson, T. Futch, V. Kaluza, et al. 1999. The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature. 400:276-280.
57. Tumova, S., A. Woods, and J.R. Couchman. 2000. Heparan sulfate chains from glypican and syndecans bind the Hep II domain of fibronectin similarly despite minor structural differences. J. Biol. Chem. 275:9410-9417.
58. Vince, G.H., S. Wagner, T. Pietsch, R. Klein, R.H. Goldbrunner, K. Roosen, and J.C. Tonn. 1999. Heterogeneous regional expression patterns of matrix metalloproteinases in human malignant gliomas. Int. J. Dev. Neurosci. 17:437-445.
59. Wiksten, J.P., J. Lundin, S. Nordling, A. Kokkola, and C. Haglund. 2000. A prognostic value of syndecan-1 in gastric cancer. Anticancer Res. 20:4905-4907.
60. Wiksten, J.P., J. Lundin, S. Nordling, M. Lundin, A. Kokkola, K. von Boguslawski, and C. Haglund. 2001. Epithelial and stromal syndecan-1 expression as predictor of outcome in patients with gastric cancer. Int. J. Cancer. 95:1-6.
61. Wilson, C.L., K.J. Heppner, P.A. Labosky, B.L. Hogan, and L.M. Matrisian. 1997. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc. Natl. Acad. Sci. USA. 94:1402-1407.
62. Woods, A., and J.R. Couchman. 2001. Syndecan-4 and focal adhesion function. Curr. Opin. Cell Biol. 13:578-583.
63. Wroblewski, L.E., P.J. Noble, A. Pagliocca, D.M. Pritchard, C.A. Hart, F. Campbell, A.R. Dodson, G.J. Dockray, and A. Varro. 2003. Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J. Cell Sci. 116:3017-3026.
64. Yamamoto, H., F. Itoh, S. Iku, Y. Adachi, H. Fukushima, S. Sasaki, M. Mukaiya, K. Hirata, and K. Imai. 2001. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human pancreatic adenocarcinomas: clinicopathologic and prognostic significance of matrilysin expression. J. Clin. Oncol. 19:1118-1127.
65. Yang, Y., S. Yaccoby, W. Liu, J.K. Langford, C.Y. Pumphrey, A. Theus, J. Epstein, and R.D. Sanderson. 2002. Soluble syndecan-1 promotes growth of myeloma tumors in vivo. Blood. 100:610-617.
66. Yu, J., C. Ustach, and H.R. Kim. 2003. Platelet-derived growth factor signaling and human cancer. J. Biochem. Mol. Biol. 36:49-59.
67. Yu, W.H., and J.F. Woessner Jr. 2000. Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J. Biol. Chem. 275:4183-4191.
68. Zako, M., J. Dong, O. Goldberger, M. Bernfield, J.T. Gallagher, and J.A. Deakin. 2003. Syndecan-1 and -4 synthesized simultaneously by mouse mammary gland epithelial cells bear heparan sulfate chains that are apparently structurally indistinguishable. J. Biol. Chem. 278:13561-13569.
69. Zhang, Z., C. Coomans, and G. David. 2001. Membrane heparan sulfate proteoglycan-supported FGF2-FGFR1 signaling: evidence in support of the "cooperative end structures" model. J. Biol. Chem. 276:41921-41929.
70. Zhou, W., L.J. Sokoll, D.J. Bruzek, L. Zhang, V.E. Velculescu, S.B. Goldin, R.H. Hruban, S.E. Kern, S.R. Hamilton, D.W. Chan, et al. 1998. Identifying markers for pancreatic cancer by gene expression analysis. Cancer Epidemiol. Biomarkers Prev. 7:109-112.
71. Zhu, Z.W., H. Friess, L. Wang, M. Abou-Shady, A. Zimmermann, A.D. Lander, M. Korc, J. Kleeff, and M.W. Buchler. 2001. Enhanced glypican-3 expression differentiates the majority of hepatocellular carcinomas from benign hepatic disorders. Gut. 48:558-564.
72. Zioncheck, T.F., L. Richardson, J. Liu, L. Chang, K.L. King, G.L. Bennett, P. Fugedi, S.M. Chamow, R.H. Schwall, and R.J. Stack. 1995. Sulfated oligosaccharides promote hepatocyte growth factor association and govern its mitogenic activity. J. Biol. Chem. 270:16871-16878.