Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity

Cancer Research

Volumn 59, Issue 14, 1999, Pages 3433-3441

  Parish, Christopher R ^a   Freeman, Craig ^a   Brown, Kathryn J ^a   Francis, Douglas J ^a   Cowden, William B ^a  

^a Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARAN SULFATE; HEPARANASE; MALTOHEXAOSE SULFATE; OLIGOSACCHARIDE; PHOSPHOMANNOPENTAOSE SULFATE; PI 88; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST ADENOCARCINOMA; CANCER INHIBITION; DRUG EFFICACY; DRUG POTENCY; ENZYME ACTIVITY; ENZYME INHIBITION; METASTASIS; NONHUMAN; PRIORITY JOURNAL; RAT; TUMOR VASCULARIZATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CARBOHYDRATE SEQUENCE; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; GLUCURONIDASE; GLYCOSIDE HYDROLASES; HUMANS; LYMPHATIC METASTASIS; MAMMARY NEOPLASMS, EXPERIMENTAL; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; OLIGOSACCHARIDES; ORGAN CULTURE TECHNIQUES; PLACENTA; RATS; RATS, INBRED F344; SULFUR;

EID: 0033565247     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Folkman, J. What is the evidence that tumors are angiogenesis dependent? J. Natl. Cancer Inst., 82: 4-6, 1990.
2. Fox, S. B., Gatter, K. C., and Harris, A. L. Tumor angiogenesis. J. Pathol., 179: 232-237, 1996.
3. Hanahan, D., and Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86: 353-364, 1996.
4. Zetter, B. R. Angiogenesis and tumor metastasis. Ann. Rev. Med., 49: 407-424, 1998.
5. Rak, J. W., St. Croix, D. V., and Kerbel, R. S. Consequences of angiogenesis for tumor progression, metastasis and cancer therapy. Anticancer Drugs, 6: 3-18, 1995.
6. Sunassee, K., and Vile, R. Hitting cancer where it hurts. Curr. Biol., 7: R282-R285, 1997.
7. Brown, K. J., Maynes, S. F., Bezos, A., Maguire, D. J., Ford, M. D., and Parish, C. R. A novel in vitro assay for human angiogenesis. Lab. Invest., 75: 539-555, 1996.
8. Yurchenco, P. D., and Schittny, J. C. Molecular architecture of basement membrane. FASEB J., 4: 1577-1590, 1990.
9. Wojtowicz-Praga, S. M., Dickson, R. B., and Hawkins, M. J. Matrix metalloproteinase inhibitors. Invest. New Drugs, 15: 61-75, 1997.
10. Nakajima, M., Irimura, T., and Nicolson, G. L. Heparanases and tumor metastasis. J. Cell. Biochem., 36: 157-167, 1988.
11. Vlodavsky, I. Eldor, A., Haimovitz-Friedman, A., Matzner, Y., Ishai-Michaeli, R., Lider, O., Naparstek, Y., Cohen, I. R., and Fuks, Z. Expression of heparanase by platelets and circulating cells of the immune system: possible involvement in diapedesis and extravasation. Invasion Metastasis., 12: 112-127, 1992.
12. Freeman, C., and Parish, C. R. Human platelet heparanase: purification, characterization and catalytic activity. Biochem. J., 330: 1-11, 1998.
13. Freeman, C., and Parish, C. R. A rapid quantitative assay for the detection of mammalian heparanase activity. Biochem. J., 326: 229-237, 1997.
14. Hulett, M. D., Freeman, C., Hamdorf, B., Baker, R. T., Harris, M. J., and Parish, C. R. Cloning of mammalian heparanase: a key enzyme in tumor invasion and metastasis. Nat. Med., in press, 1999.
15. Vlodavsky, I., Miao, H., Medalion, B., Danagher, P., and Ron, D. Involvement of heparan sulfate and related molecules in sequestration and growth promoting activity of fibroblast growth factor. Cancer Metastasis Rev., 15: 177-186, 1996.
16. Cohen, T., Gitay-Goren, H., Sharon, R., Shibuya, M., Halaban, R., Levi, B. Z., and Neufeld, G. VEGF121, a vascular endothelial growth factor (VEGF) isoform lacking heparin binding ability, requires cell-surface heparan sulfates for efficient binding to the VEGF receptors of human melanoma cells. J. Biol. Chem., 270: 11322-11326, 1995.
17. Glasser, J. H., and Conrad, H. E. Chick embryo liver β-glucuronidase. Comparison of activity on natural and artificial substrates. J. Biol. Chem., 254: 6588-6597, 1979.
18. Bretthauer, R. K., Kaczorowski, G. J., and Weise, M. J. Characterization of a phosphorylated pentasaccharide isolated from Hansenula holstii NRRL Y-2448 phosphomannan. Biochemistry, 12: 1251-1256, 1973.
19. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227: 680-685, 1970.
20. Parish, C. R., Jakobsen, K. B., Coombe, D. R., and Bacic, A. Isolation and characterization of cell adhesion molecules from the marine sponge, Ophlitaspongia tenuis. Biochim. Biophys. Acta, 1073: 56-64, 1991.
21. Brown, K. J., and Parish, C. R. Histidine-rich glycoprotein and platelet factor 4 mask heparan sulfate proteoglycans recognized by acidic and basic fibroblast growth factor. Biochemistry, 33: 13918-13927, 1994.
22. Coombe, D. R., Parish, C. R., Ramshaw, I. A., and Snowden, J. M. Analysis of the inhibition of tumor metastasis by sulphated polysaccharides. Int. J. Cancer, 39: 82-88, 1987.
23. Davidson, W. F., and Parish, C. R. A procedure for removing red cells and dead cells from lymphoid cell suspensions. J. Immunol. Methods, 7: 291-300, 1975.
24. Warren, H. S., and Skipsey, L. J. Phenotypic analysis of a resting subpopulation of human peripheral blood NK cells: the FcRγIII (CD16) molecule and NK cell differentiation. Immunology, 72: 150-157, 1991.
25. Glabe, C. G., Harty, P. K., and Rosen, S. D. Preparation and properties of fluorescent polysaccharides. Anal. Biochem., 130: 287-294, 1983.
26. Pesenti, E., Sola, F., Mongelli, N., Grandi, M., and Spreafico, F. Suramin prevents neovascularization and tumor growth through blocking of basic fibroblast growth factor activity. Br. J. Cancer, 66: 367-372, 1992.
27. Nakajima, M., DeChavigny, A., Johnson, C. E., Hamada, J., Stein, C. A., and Nicolson, G. L. Suramin. A potent inhibitor of melanoma heparanase and invasion. J. Biol. Chem., 266: 9661-9666, 1991.
28. La Rocca, R. V., Stein, C. A., and Myers, C. E. Suramin: prototype of a new generation of antitumor compounds. Cancer Cells, 4: 106-115, 1990.
29. Foxall, C., Wei, Z., Schaefer, M. E., Casabonne, M., Fugedi, P., Peto, C., Castellot, J. J., and Brandley, B. K. Sulfated malto-oligosaccharides bind to basic FGF, inhibit endothelial cell proliferation, and disrupt endothelial cell tube formation. J. Cell. Physiol., 168: 657-667, 1996.
30. Guimond, S., Maccarana, M., Olwin, B. B., Lindahl, U., and Rapraeger, A. C. Activating and inhibitory heparin sequences for FGF-2 (Basic FGF). Distinct requirements for FGF-1, FGF-2 and FGF-4. J. Biol. Chem., 268: 23906-23914, 1993.
31. Ishihara, M., Tyrrell, D. J., Stauber, G. B., Brown. S., Cousens, L. S., and Stack, R. J. Preparation of affinity-fractionated heparin-derived oligosaccharides and their effects on selected biological activities mediated by basic fibroblast growth factor. J. Biol. Chem., 268: 4675-4683, 1993.
32. Robertson, N. E., Discafani, C. M., Downs, E. C., Hailey, J. A., Sarre, O., Runkle, R. L., Popper, T. L., and Plunkett, M. L. A quantitative in vivo mouse model used to assay inhibitors of tumor-induced angiogenesis. Cancer Res., 51: 1339-1344, 1991.
33. 9-bradykinin inhibits the angiogenic effect of bradykinin and interleukin-1 in rats. Br. J. Pharmacol., 109: 14-17, 1993.
34. Hu, D. E., Hiley, C. R., Smither, R. L., Gresham, G. A., and Fan, T. P. Correlation of 133Xe clearance, blood flow and histology in the rat sponge model for angiogenesis. Further studies with angiogenic modifiers. Lab. Invest., 72: 601-610, 1995.
35. Mühlhauser, J., Pili, R., Merrill, M. J., Maeda, H., Passaniti, A., Crystal, R. G., and Capogrossi, M. C. In vivo angiogenesis induced by recombinant adenovirus vectors coding either for secreted or nonsecreted forms of acidic fibroblast growth factor. Hum. Gene Ther., 6: 1457-1465, 1995.
36. Okada, N., Fushimi, M., Nagata, Y., Fukunaga, T., Tsutsumi, Y., Nakagawa, S., and Mayumi, T. Evaluation of angiogenic inhibitors with an in vivo quantitative angiogenesis method using agarose microencapsulation and mouse hemoglobin enzyme-linked immunosorbent assay. Jpn. J. Cancer Res., 87: 952-957, 1996.
37. Ornitz, D. M., Herr, A. B., Nilsson, M., Westman, J., Svahn, C. M., and Waksman, G. FGF binding and FGF receptor activation by synthetic heparan-de rived di-and trisaccharides. Science (Washington DC), 268: 432-436, 1995.
38. Folkman, J., Langer, R., Linhardt, R. J., Haudenschild, C., and Taylor, S. Angiogenesis inhibition and tumor regression caused by heparin or a heparin fragment in the presence of cortisone. Science (Washington DC), 221: 719-725, 1983.
39. Folkman, J., Weisz, P. B., Jouille, M. M., Li, W. W., and Ewing, W. R. Control of angiogenesis with synthetic heparin substitutes. Science (Washington DC), 243: 1490-1493, 1989.
40. Tressler, R. J., Wei, Z., Storm, N., Fugedi, P., Stack, R., Tyrrell, D. J., and Killion, J. J. A heparinase inhibitory, basic-FGF binding sulfated oligosaccharide that inhibits angiogenesis ex vivo has potent anti-tumor and anti-metastatic activity in vivo. In: M. E. Maragoudakis (ed.), Molecular, Cellular and Clinical Aspects of Angiogenesis. New York: Plenum Press, 1996.
41. Zioncheck, T. F., Richardson, L., Liu, J., Chang, L., King, K. L., Bennett, G. L., Fügedi, P., Chamow, S. M., Schwall, R. H., and Stack, R. J. Sulfated oligosaccharides promote hepatocyte growth factor association and govern its mitogenic activity. J. Biol. Chem., 270: 16871-16878, 1995.
42. Lapierre, F., Holme, K., Lam, L., Tressler, R. J., Storm, N., Wee, J., Stack, R. J., Castellot, J., and Tyrrell, D. J. Chemical modifications of heparin that diminish its anticoagulant but preserve its heparanase-inhibitory, angiostatic, anti-tumor and anti-metastatic properties. Glycobiology, 6: 355-366, 1996.
43. Sciumbata, T., Caretto, P., Pirovano, P., Pozzi, P., Cremonesi, P., Galimberti, G., Leoni, F., and Marcucci, F. Treatment with modified heparins inhibits experimental metastasis formation and leads, in some animals, to long-term survival. Invasion Metastasis, 16: 132-143, 1996.
44. Vlodavsky, I., Mohsen, M., Lider, O., Svahn, C. M., Ekre, H. P., Vigoda, M., Ishaimichaeli, R., and Peretz, T. Inhibition of tumor metastasis by heparanase inhibiting species of heparin. Invasion Metastasis, 14: 290-302, 1994.
45. Parish, C. R., Coombe, D. R., Jakobsen, K. B., Bennet, F. A., and Underwood, P. A. Evidence that sulphated polysaccharides inhibit tumor metastasis by blocking tumor-cell-derived heparanase. Int. J. Cancer. 40: 511-518, 1987.