Heparan sulfate proteoglycans in invasion and metastasis

Seminars in Cell and Developmental Biology

Volumn 12, Issue 2, 2001, Pages 89-98

  Sanderson, Ralph D ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Adhesion; Cancer; Heparan sulfate proteoglycans; Metastasis; Motility

Indexed keywords

COMPLEMENTARY DNA; ENZYME INHIBITOR; FIBROBLAST GROWTH FACTOR 2; GLYPICAN; HEPARAN SULFATE; HEPARANASE; HEPARANASE INHIBITOR; HEPARIN DERIVATIVE; HERMES ANTIGEN; MATRIX METALLOPROTEINASE; PADGEM PROTEIN; PROTEINASE; PROTEOHEPARAN SULFATE; SYNDECAN 1; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; CANCER; CANCER INHIBITION; CANCER INVASION; CANCER SURVIVAL; CARCINOGENESIS; CELL ADHESION; CELL FUNCTION; CELL GROWTH; CELL INVASION; CELL MOTILITY; CELL SURFACE; CELLULAR DISTRIBUTION; DEVELOPMENT; DRUG EFFECT; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; METASTASIS; NONHUMAN; PATHOPHYSIOLOGY; PROGNOSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL TIME; TUMOR CELL;

EID: 0035782873     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.2000.0241     Document Type: Article

References (91)

1. Pilia G, Hughes-Benzie RM, MacKenzie A, Baybayan P, Chen EY, Huber R, Neri G, Cao A, Forabosco A, Schlessinger D (1996) Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat Genet 12:241-247
2. McCormick C, Leduc Y, Martindale D, Mattison K, Esford LE, Dyer AP, Tufaro F (1998) The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat Genet 19:158-161
3. Alexander CM, Reichsman F, Hinkes MT, Lincecum J, Becker KA, Cumberledge S, Bernfield M (2000) Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat Genet 25:329-332
4. Inki P, Jalkanen M (1996) The role of syndecan-1 in malignancies. Ann Med 28:63-67
5. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777
6. Lander AD, Selleck SB (2000) The elusive functions of proteoglycans: In vivo veritas. J Cell Biol 148:227-232
7. Tumova S, Woods A, Couchman JR (2000) Heparan sulfate proteoglycans on the cell surface: Versatile coordinators of cellular functions. Int J Biochem Cell Biol 32:269-288
8. Underhill CB, Keller JM (1975) A transformation-dependent difference in the heparan sulfate associated with the cell surface. Biochem Biophys Res Commun 63:448-454
9. Winterbourne DJ, Mora PT (1978) Altered metabolism of heparan sulphate in simian virus 40 transformed cloned mouse cells. J Biol Chem 253:5109-5120
10. David G, Van Den Berghe H (1983) Transformed mouse mammary epithelial cells synthesize undersulfated basement membrane proteoglycan. J Biol Chem 258:7338-7344
11. Robinson J, Viti M, Höök M (1984) Structure and properties of an undersulfated heparan sulfate proteoglycan synthesized by a rat hepatoma cell line. J Cell Biol 98:946-953
12. Redini F, Moczar E, Poupon MF (1986) Cell surface glycosaminoglycans of rat rhabdomyosarcoma lines with different metastatic potentials and of non-malignant rat myoblasts. Biochim Biophys Acta 883:98-105
13. Kure S, Yoshie O, Aso H (1987) Metastatic potential of murine B16 melanoma correlates with reduced surface heparan sulfate glycosaminoglycan. Jpn J Cancer Res 78:1238-1245
14. Moczar M, Caux F, Bailly M, Berthier O, Dore JF (1993) Accumulation of heparan sulfate in the culture of human melanoma cells with different metastatic ability. Clin Exp Metastasis 11:462-471
15. Timar J, Ladanyi A, Lapis K, Moczar M (1992) Differential expression of proteoglycans on the surface of human melanoma cells characterized by altered experimental metastatic potential. Am J Pathol 141:467-474
16. Day RM, Hao X, Ilyas M, Daszak P, Talbot IC, Forbes A (1999) Changes in the expression of syndecan-1 in the colorectal adenoma-carcinoma sequence. Virchows Arch 434:121-125
17. Kumar-Singh S, Jacobs W, Dhaene K, Weyn B, Bogers J, Weyler J, Van Marck E (1998) Syndecan-1 expression in malignant mesothelioma: Correlation with cell differentiation, WT1 expression, and clinical outcome. J Pathol 186:300-305
18. Nackaerts K, Verbeken E, Deneffe G, Vanderschueren B, Demedts M, David G (1997) Heparan sulfate proteoglycan expression in human lung-cancer cells. Int J Cancer 74:335-345
19. Matsumoto A, Ono M, Fujimoto Y, Gallo RL, Bernfield M, Kohgo Y (1997) Reduced expression of syndecan-1 in human hepatocellular carcinoma with high metastatic potential. Int J Cancer 74:482-491
20. Stanley MJ, Stanley MW, Sanderson RD, Zera R (1999) Syndecan-1 expression is induced in the stroma of infiltrating breast carcinoma. Am J Clin Pathol 112:377-383
21. Inki P, Joensuu H, Grenman R, Klemi P, Jalkanen M (1994) Association between syndecan-1 expression and clinical outcome in squamous cell carcinoma of the head and neck. Br J Cancer 70:319-323
22. Leppa S, Harkonen P, Jalkanen M (1991) Steroid-induced epithelial-fibroblastic conversion associated with syndecan suppression in S115 mouse mammary tumor cells. Cell Regul 2:1-11
23. Leppa S, Mali M, Miettinen HM, Jalkanen M (1992) Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc Natl Acad Sci USA 89:932-936
24. Kato M, Saunders S, Nguyen H, Bernfield M (1995) Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol Biol Cell 6:559-576
25. Numa F, Hirabayashi K, Tsunaga N, Kato H, O'Rourke K, Shao H, Stechmann-Lebakken C, Varani J, Rapraeger A, Dixit VM (1995) Elevated levels of syndecan-1 expression confer potent serum-dependent growth in human 293t cells. Cancer Res 55:4676-4680
26. Ohtake T, Fujimoto Y, Ikuta K, Saito H, Ohhira M, Ono M, Kohgo Y (1999) Proline-rich antimicrobial peptide, PR-39 gene transduction altered invasive activity and actin structure in human hepatocellular carcinoma cells. Br J Cancer 81:393-403
27. Liebersbach BF, Sanderson RD (1994) Expression of syndecan-1 inhibits cell invasion into type I collagen. J Biol Chem 269:20013-20019
28. Liu W, Litwack ED, Stanley MJ, Langford JK, Lander AD, Sanderson RD (1998) Heparan sulfate proteoglycans as adhesive and anti-invasive molecules: Syndecans and glypican have distinct functions. J Biol Chem 273:22825-22832
29. Steinfeld R, Van Den Berghe H, David G (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J Cell Biol 133:405-416
30. Bernfield M, Hinkes MT, Gallo RL (1993) Developmental expression of the syndecans: Possible function and regulation. Dev Suppl:205-212
31. Sun D, McAlmon KR, Davies JA, Bernfield M, Hay ED (1998) Simultaneous loss of expression of syndecan-1 and E-cadherin in the embryonic palate during epithelial-mesenchymal transformation. Int J Dev Biol 42:733-736
32. Leppa S, Vleminckx K, Van Roy F, Jalkanen M (1996) Syndecan-1 expression in mammary epithelial tumor cells is E-cadherin-dependent. J Cell Sci 109:1393-1403
33. Conejo JR, Kleeff J, Koliopanos A, Matsuda K, Zhu ZW, Goeke H, Bicheng N, Zimmermann A, Korc M, Friess H, Buchler MW (2000) Syndecan-1 expression is up-regulated in pancreatic but not in other gastrointestinal cancers. Int J Cancer 88:12-20
34. Kleeff J, Ishiwata T, Kumbasar A, Friess H, Buchler MW, Lander AD, Korc M (1998) The cell-surface heparan sulfate proteoglycan glypican-1 regulates growth factor action in pancreatic carcinoma cells and is overexpressed in human pancreatic cancer. J Clin Invest 102:1662-1673
35. Dhodapkar MV, Sanderson RD (1999) Syndecan-1 (CD 138) in myeloma and lymphoid malignancies: A multifunctional regulator of cell behavior within the tumor microenvironment. Leuk Lymphoma 34:35-43
36. Fitzgerald ML, Wang Z, Park PW, Murphy G, Bernfield M (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
37. David G, Bai XM, Van der Schueren B, Cassiman J-J, Van den Berghe H (1992) Developmental changes in heparan sulfate expression: In situ detection with mAbs. J Cell Biol 119:961-975
38. van Kuppevelt TH, Dennissen MA, van Venrooij WJ, Hoet RM, Veerkamp JH (1998) Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology. Further evidence for heparan sulfate heterogeneity in the kidney. J Biol Chem 273:12960-12966
39. Sanderson RD, Bernfield M (1988) Molecular polymorphism of a cell surface proteoglycan: Distinct structures on simple and stratified epithelia. Proc Natl Acad Sci USA 85:9562-9566
40. Langford JK, Stanley MJ, Cao D, Sanderson RD (1998) Multiple heparan sulfate chains are required for optimal syndecan-1 function. J Biol Chem 273:29965-29971
41. Salmivirta M, Lidholt K, Lindahl U (1996) Heparan sulfate: A piece of information. FASEB J 10:1270-1279
42. Lindahl U, Kusche-Gullberg M, Kjellen L (1998) Regulated diversity of heparan sulfate. J Biol Chem 273:24979-24982
43. Gallagher JT (1997) Structure-activity relationship of heparan sulphate. Biochem Soc Trans 25:1206-1209
44. Schubert D, LaCorbiere M (1980) A role of secreted glycosaminoglycans in cell-substratum adhesion. J Biol Chem 255:11564-11569
45. Stamatoglou SC, Keller JM (1983) Correlation between cell substrate attachment in vitro and cell surface heparan sulfate affinity for fibronectin and collagen. J Cell Biol 96:1820-1823
46. Sanderson RD, Turnbull JE, Gallagher JT, Lander AD (1994) Fine structure of heparan sulfate regulates syndecan-1 function and cell behavior. J Biol Chem 269:13100-13106
47. Kishibe J, Yamada S, Okada Y, Sato J, Ito A, Miyazaki K, Sugahara K (2000) Structural requirements of heparan sulfate for the binding to the tumor-derived adhesion factor/angiomodulin that induces cord-like structures to ECV-304 human carcinoma cells. J Biol Chem 275:15321-15329
48. Jayson GC, Lyon M, Paraskeva C, Turnbull JE, Deakin JA, Gallagher JT (1998) Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J Biol Chem 273:51-57
49. Safaiyan F, Lindahl U, Salmivirta M (1998) Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells. Eur J Biochem 252:576-582
50. Merry CL, Lyon M, Deakin JA, Hopwood JJ, Gallagher JT (1999) Highly sensitive sequencing of the sulfated domains of heparan sulfate. J Biol Chem 274:18455-18462
51. Turnbull JE, Hopwood JJ, Gallagher JT (1999) A strategy for rapid sequencing of heparan sulfate and heparin saccharides. Proc Natl Acad Sci USA 96:2698-2703
52. Venkataraman G, Shriver Z, Raman R, Sasisekharan R (1999) Sequencing complex polysaccharides. Science 286:537-542
53. Nakajima M, Irimura T, Nicolson GL (1988) Heparanases and tumor metastasis. J Cell Biochem 36:157-167
54. Nakajima M, Irimura T, Di Ferrante D, Di Ferrante N, Nicolson GL (1983) Heparan sulfate degradation: Relation to tumor invasive and metastatic properties of mouse B16 melanoma sublines. Science 220:611-613
55. Vlodavsky I, Eldor A, Haimovitz-Friedman A, Matzner Y, Ishai-Michaeli R, Lider O, Naparstek Y, Cohen IR, Fuks Z (1992) Expression of heparanase by platelets and circulating cells of the immune system - Possible involvement in diapedesis and extravasation. Invasion Metastasis 12:112-127
56. Nicolson GL, Nakajima M, Wakabayashi H, Boyd DD, Diaz D, Irimura T (1998) Cancer cell heparanase activity associated with invasion and metastasis. Adv Enzyme Regul 38:19-32
57. Parish CR, Freeman C, Brown KJ, Francis DJ, Cowden WB (1999) Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity. Cancer Res 59:3433-3441
58. Hulett MD, Freeman C, Hamdorf BJ, Baker RT, Harris MJ, Parish CR (1999) Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat Med 5:803-809
59. Vlodavsky I, Friedmann Y, Elkin M, Aingorn H, Atzmon R, Ishai-Michaeli R, Bitan M, Pappo O, Peretz T, Michal I, Spector L, Peeker I (1999) Mammalian heparanase: Gene cloning, expression and function in tumor progression and metastasis. Nat Med 5:793-802
60. Kussie PH, Hulmes JD, Ludwig DL, Patel S, Navarro EC, Seddon AP, Giorgio NA, Bohlen P (1999) Cloning and functional expression of a human heparanase gene. Biochem Biophys Res Commun 261:183-187
61. Toyoshima M, Nakajima M (1999) Human heparanase. Purification, characterization, cloning, and expression. J Biol Chem 274:24153-24160
62. Vlodavsky I, Elkin M, Pappo O, Aingorn H, Atzmon R, Ishai-Michaeli R, Aviv A, Pecker I, Friedmann Y (2000) Mammalian heparanase as mediator of tumor metastasis and angiogenesis. Isr Med Assoc J 2 Suppl:37-45
63. Ishai-Michaeli R, Eldor A, Vlodavsky I (1990) Heparanase activity expressed by platelets, neutrophils, and lymphoma cells releases active fibroblast growth factor from extracellular matrix. Cell Regul 1:833-842
64. Whitelock JM, Murdoch AD, Iozzo RV, Underwood PA (1996) The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J Biol Chem 271:10079-10086
65. Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM, Bernfield M (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 4:691-697
66. Blood CH, Zetter BR (1990) Tumor interactions with the vasculature: Angiogenesis and tumor metastasis. Biochim Biophys Acta 1032:89-118
67. Ihrcke NS, Parker W, Reissner KJ, Platt JL (1998) Regulation of platelet heparanase during inflammation: Role of pH and proteinases. J Cell Physiol 175:255-267
68. Dempsey LA, Plummer TB, Coombes SL, Platt JL (2000) Heparanase expression in invasive trophoblasts and acute vascular damage. Glycobiology 10:467-475
69. Iozzo RV, Cohen IR, Grassel S, Murdoch AD (1994) The biology of perlecan: The multifaceted heparan sulphate pro-teoglycan of basement membranes and pericellular matrices. Biochem J 302:625-639
70. Adatia R, Albini A, Carlone S, Giunciuglio D, Benelli R, Santi L, Noonan DM (1997) Suppression of invasive behavior of melanoma cells by stable expression of anti-sense perlecan cDNA. Ann Oncol 8:1257-1261
71. Sharma B, Handler M, Eichstetter I, Whitelock JM, Nugent MA, Iozzo RV (1998) Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo. J Clin Invest 102:1599-1608
72. Mathiak M, Yenisey C, Grant DS, Sharma B, Iozzo RV (1997) A role for perlecan in the suppression of growth and invasion in fibrosarcoma cells. Cancer Res 57:2130-2136
73. Lyon M, Gallagher JT (1994) Hepatocyte growth factor/scatter factor: a heparan sulphate-binding pleiotropic growth factor. Biochem Soc Trans 22:365-370
74. Date K, Matsumoto K, Kuba K, Shimura H, Tanaka M, Nakamura T (1998) Inhibition of tumor growth and invasion by a four-kringle antagonist (HGF/NK4) for hepatocyte growth factor. Oncogene 17:3045-3054
75. Robertson NP, Starkey JR, Hamner S, Meadows GG (1989) Tumor cell invasion of three-dimensional matrices of defined composition: Evidence for a specific role for heparan sulfate in rodent cell lines. Cancer Res 49:1816-1823
76. Engelberg H (1999) Actions of heparin that may affect the malignant process. Cancer 85:257-272
77. Ma YQ, Geng JG (2000) Heparan sulfate-like proteoglycans mediate adhesion of human malignant melanoma A375 cells to P-selectin under flow. J Immunol 165:558-565
78. Hirabayashi K, Numa F, Suminami Y, Murakami A, Murakami T, Kato H (1998) Altered proliferative and metastatic potential associated with increased expression of syndecan-1. Tumour Biol 19:454-463
79. Yu WH, Woessner JF Jr (2000) Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J Biol Chem 275:4183-4191
80. Kelly T, Mueller SC, Yeh Y, Chen WT (1994) Invadopodia promote proteolysis of a wide variety of extracellular matrix proteins. J Cell Physiol 158:299-308
81. Kelly T, Yan Y, Osborne RL, Athota AB, Rozypal TL, Colclasure JC, Chu WS (1998) Proteolysis of extracellular matrix by invadopodia facilitates human breast cancer cell invasion and is mediated by matrix metalloproteinases. Clin Exp Metastasis 16:501-512
82. Perrimon N, Bernfield M (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404:725-728
83. van der Voort R, Taher TE, Wielenga VJ, Spaargaren M, Prevo R, Smit L, David G, Hartmann G, Gherardi E, Pals ST (1999) Heparan sulfate-modified CD44 promotes hepatocyte growth factor/scatter factor-induced signal transduction through the receptor tyrosine kinase c-Met. J Biol Chem 274:6499-6506
84. Borset M, Hjertner O, Jaccoby S, Epstein J, Sanderson RD (2000) Syndecan-1 is targeted to the uropods of polarized myeloma cells where it sequesters heparin-binding proteins. Blood 96:2528-2536
85. Miyake H, Hara I, Yoshimura K, Eto H, Arakawa S, Wada S, Chihara K, Kamidono S (1996) Introduction of basic fibroblast growth factor gene into mouse renal cell carcinoma cell line enhances its metastatic potential. Cancer Res 56:2440-2445
86. Rahmoune H, Turnbull JE, Gallagher JT, Rudland PS, Fernig DG (1996) Heparan sulphate in breast cancer cells. Biochem Soc Trans 24:355S
87. Dhodapkar MV, Kelly T, Theus A, Athotha AP, Barlogie B, Sanderson RD (1997) Elevated levels of shed syndecan-1 correlate with tumor mass and decreased matrix metalloproteinase-9 activity in the serum of patients with multiple myeloma. Br J Haematol 99:368-371
88. Seidel C, Sundan A, Hjorth M, Turesson I, Dahl IM, Abildgaard N, Waage A, Borset M (2000) Serum syndecan-1: A new independent prognostic marker in multiple myeloma. Blood 95:388-392
89. Oh ES, Woods A, Couchman JR (1997) Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem 272:8133-8136
90. McFall AJ, Rapraeger AC (1998) Characterization of the high affinity cell-binding domain in the cell surface proteoglycan syndecan-4. J Biol Chem 273:28270-28276
91. Mongiat M, Taylor K, Otto J, Aho S, Uitto J, Whitelock JM, Iozzo RV (2000) The protein core of the proteoglycan perlecan binds specifically to fibroblast growth factor-7. J Biol Chem 275:7095-7100