The development of anti-angiogenic heparan sulfate oligosaccharides

Biochemical Society Transactions

Volumn 42, Issue 6, 2014, Pages 1596-1600

  Jayson, Gordon C ^a   Miller, Gavin J ^a   Hansen, Steen U ^a   Barath, Marek ^b   Gardiner, John M ^a   Avizienyte, Egle ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

Angiogenesis; Heparan sulfate; Oligosaccharide

Indexed keywords

ANGIOGENESIS INHIBITOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE; HEPARIN; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; IDURONIC ACID; INTERLEUKIN 8; MESSENGER RNA; OLIGOSACCHARIDE; POLYSACCHARIDE; STROMAL CELL DERIVED FACTOR 1ALPHA; VASCULOTROPIN; VASCULOTROPIN A;

ADVANCED CANCER; ANGIOGENESIS; ANTIANGIOGENIC THERAPY; ARTICLE; BIOLOGICAL ACTIVITY; CANCER INHIBITION; CAPILLARY DENSITY; CHEMICAL MODIFICATION; HUMAN; ISOTOPE LABELING; LUNG CANCER; MEDICINAL CHEMISTRY; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; SYNTHESIS; THROMBOCYTOPENIA;

ANGIOGENESIS INHIBITORS; HEPARITIN SULFATE; HUMANS; OLIGOSACCHARIDES;

EID: 84911879033     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140229     Document Type: Article

References (42)

1. Jayson, G.C., Hicklin, D.J. and Ellis, L.M. (2012) Antiangiogenic therapy: evolving view based on clinical trial results. Nat. Rev. Clin. Oncol. 9, 297-303 CrossRef PubMed
2. Hurwitz, H., Fehrenbacher, L., Novotny, W., Cartwright, T., Hainsworth, J., Heim, W., Berlin, J., Baron, A., Griffing, S., Holmgren, E. et al. (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350, 2335-2342 CrossRef PubMed
3. Perren, T.J., Swart, A.M., Pfisterer, J., Ledermann, J.A., Pujade-Lauraine, E., Kristensen, G., Carey, M.S., Beale, P., Cervantes, A., Kurzeder, C. et al. (2011) A phase 3 trial of bevacizumab in ovarian cancer. N. Engl. J. Med. 365, 2484-2496 CrossRef PubMed
4. Yang, J.C., Haworth, L., Sherry, R.M., Hwu, P., Schwartzentruber, D.J., Topalian, S.L., Steinberg, S.M., Chen, H.X. and Rosenberg, S.A. (2003) A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med. 349, 427-434 CrossRef PubMed
5. Raymond, E., Dahan, L., Raoul, J.L., Bang, Y.J., Borbath, I., Lombard-Bohas, C., Valle, J., Metrakos, P., Smith, D., Vinik, A. et al. (2011) Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N. Engl. J. Med. 364, 501-513 CrossRef PubMed
6. Miller, K.D. (2003) E2100: a phase III trial of paclitaxel versus paclitaxel/bevacizumab for metastatic breast cancer. Clin. Breast Cancer 3, 421-422 CrossRef PubMed
7. Batchelor, T.T., Sorensen, A.G., di Tomaso, E., Zhang, W.T., Duda, D.G., Cohen, K.S., Kozak, K.R., Cahill, D.P., Chen, P.J., Zhu, M. et al. (2007) AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11, 83-95 CrossRef PubMed
8. Grothey, A., Van Cutsem, E., Sobrero, A., Siena, S., Falcone, A., Ychou, M., Humblet, Y., Bouché, O., Mineur, L., Barone, C. et al. (2013) Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 381, 303-312 CrossRef PubMed
9. Karlan, B.Y., Oza, A.M., Richardson, G.E., Provencher, D.M., Hansen, V.L., Buck, M., Chambers, S.K., Ghatage, P., Pippitt, Jr, C.H, Brown, III, J.V. et al. (2012) Randomized, double-blind, placebo-controlled phase II study of AMG 386 combined with weekly paclitaxel in patients with recurrent ovarian cancer. J. Clin. Oncol. 30, 362-371 CrossRef PubMed
10. Knelson, E.H., Nee, J.C. and Blobe, G.C. (2014) Heparan sulfate signaling in cancer. Trends Biochem. Sci. 39, 277-288 CrossRef PubMed
11. Cecchi, F., Pajalunga, D., Fowler, C.A., Uren, A., Rabe, D.C., Peruzzi, B., Macdonald, N.J., Blackman, D.K., Stahl, S.J., Byrd, R.A. and Bottaro, DP. (2012) Targeted disruption of heparan sulfate interaction with hepatocyte and vascular endothelial growth factors blocks normal and oncogenic signaling. Cancer Cell 22, 250-262 CrossRef PubMed
12. Yayon, A., Klagsbrun, M., Esko, J.D., Leder, P. and Ornitz, D.M. (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848 CrossRef PubMed
13. Olwin, B.B. and Rapraeger, A. (1992) Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J. Cell Biol. 118, 631-639 CrossRef PubMed
14. Lindahl, U., Bäckström, G., Thunberg, L. and Leder, I.G. (1980) Evidence for a 3-O-sulfated D-glucosamine residue in the antithrombin-binding sequence of heparin. Proc. Natl. Acad. Sci. U.S.A. 77, 6551-6555 CrossRef PubMed
15. Turnbull, J.E., Fernig, D.G., Ke, Y., Wilkinson, M.C. and Gallagher, J.T. (1992) Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267, 10337-10341 PubMed
16. Kan, M., Wang, F., Xu, J., Crabb, J.W., Hou, J. and McKeehan, W.L. (1993) An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 259, 1918-1921 CrossRef PubMed
17. Pye, D.A., Vivès, R.R., Hyde, P. and Gallagher, J.T. (2000) Regulation of FGF-1 mitogenic activity by heparan sulfate oligosaccharides is dependent on specific structural features: differential requirements for the modulation of FGF-1 and FGF-2. Glycobiology 10, 1183-1192 CrossRef PubMed
18. 165-dependent mitogenic activity, tube formation, and its receptor phosphorylation of human endothelial cells: comparison of the effects of heparin and modified heparins. J. Biol. Chem. 280, 31508-31515 CrossRef PubMed
19. 165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by K5 lyase. J. Biol. Chem. 281, 1731-1740 CrossRef PubMed
20. 165 to its receptors. Biochem. Biophys. Res. Commun. 203, 1339-1347 CrossRef PubMed
21. Cole, C.L., Hansen, S.U., Baráth, M., Rushton, G., Gardiner, J.M., Avizienyte, E. and Jayson, G.C. (2010) Synthetic heparan sulfate oligosaccharides inhibit endothelial cell functions essential for angiogenesis. PLoS ONE 5, e11644 CrossRef PubMed
22. Sadir, R., Baleux, F., Grosdidier, A., Imberty, A. and Lortat-Jacob, H. (2001) Characterization of the stromal cell-derived factor-1α-heparin complex. J. Biol. Chem. 276, 8288-8296 CrossRef PubMed
23. Axelsson, J., Xu, D., Kang, B.N., Nussbacher, J.K., Handel, T.M., Ley, K., Sriramarao, P. and Esko, J.D. (2012) Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 120, 1742-1751 CrossRef PubMed
24. Spillmann, D., Witt, D. and Lindahl, U. (1998) Defining the interleukin-8-binding domain of heparan sulfate. J. Biol. Chem. 273, 15487-15493 CrossRef PubMed
25. Wang, S., Ai, X., Freeman, S.D., Pownall, M.E., Lu, Q., Kessler, D.S. and Emerson, Jr, C.P. (2004) QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 4833-4838 CrossRef PubMed
26. Jayson, G.C., Lyon, M., Paraskeva, C., Turnbull, J.E., Deakin, J.A. and Gallagher, J.T. (1998) Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 273, 51-57 CrossRef PubMed
27. Jayson, G.C., Vives, C., Paraskeva, C., Schofield, K., Coutts, J., Fleetwood, A. and Gallagher, J.T. (1999) Coordinated modulation of the fibroblast growth factor dual receptor mechanism during transformation from human colon adenoma to carcinoma. Int. J. Cancer 82, 298-304 CrossRef PubMed
28. Jayson, G.C., Evans, G.S., Pemberton, P.W., Lobley, R.W. and Allen, T. (1994) Basic fibroblast growth factor increases the multiplication and migration of a serum-free derivative of CACO-2 but does not affect differentiation. Cancer Res. 54, 5718-5723 PubMed
29. Davies, E.J., Blackhall, F.H., Shanks, J.H., David, G., McGown, A.T., Swindell, R., Slade, R.J., Martin-Hirsch, P., Gallagher, J.T. and Jayson, G.C. (2004) Distribution and clinical significance of heparan sulfate proteoglycans in ovarian cancer. Clin. Cancer Res. 10, 5178-5186 CrossRef PubMed
30. Whitworth, M.K., Backen, A.C., Clamp, A.R., Wilson, G., McVey, R., Friedl, A., Rapraeger, A.C., David, G., McGown, A., Slade, R.J. et al. (2005) Regulation of fibroblast growth factor-2 activity by human ovarian cancer tumor endothelium. Clin. Cancer Res. 11, 4282-4288 CrossRef PubMed
31. Backen, A.C., Cole, C.L., Lau, S.C., Clamp, A.R., McVey, R., Gallagher, J.T. and Jayson, G.C. (2007) Heparan sulphate synthetic and editing enzymes in ovarian cancer. Br. J. Cancer 96, 1544-1548 CrossRef PubMed
32. Ferreras, C., Rushton, G., Cole, C.L., Babur, M., Telfer, B.A., van Kuppevelt, T.H., Gardiner, J.M., Williams, K.J., Jayson, G.C. and Avizienyte, E. (2012) Endothelial heparan sulfate 6-O-sulfation levels regulate angiogenic responses of endothelial cells to fibroblast growth factor 2 and vascular endothelial growth factor. J. Biol. Chem. 287, 36132-36146 CrossRef PubMed
33. Cole, C.L., Rushton, G., Jayson, G.C. and Avizienyte, E. (2014) Ovarian cancer cell heparan sulfate 6-O-sulfotransferases regulate an angiogenic program induced by heparin-binding epidermal growth factor (EGF)-like growth factor/EGF receptor signaling. J. Biol. Chem. 289, 10488-10501 CrossRef PubMed
34. Pellegrini, L., Burke, D.F., von Delft, F., Mulloy, B. and Blundell, T.L. (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407, 1029-1034 CrossRef PubMed
35. Schlessinger, J., Plotnikov, A.N., Ibrahimi, O.A., Eliseenkova, A.V., Yeh, B.K., Yayon, A., Linhardt, R.J. and Mohammadi, M. (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell 6, 743-750 CrossRef PubMed
36. Hasan, J., Shnyder, S.D., Clamp, A.R., McGown, A.T., Bicknell, R., Presta, M., Bibby, M., Double, J., Craig, S., Leeming, D. et al. (2005) Heparin octasaccharides inhibit angiogenesis in vivo. Clin. Cancer Res. 11, 8172-8179 CrossRef PubMed
37. Fuster, M.M., Wang, L., Castagnola, J., Sikora, L., Reddi, K., Lee, P.H., Radek, K.A., Schuksz, M., Bishop, J.R., Gallo, R.L. et al. (2007) Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis. J. Cell Biol. 177, 539-549 CrossRef PubMed
38. Hansen, S.U., Baráth, M., Salameh, B.A., Pritchard, R.G., Stimpson, W.T., Gardiner, J.M. and Jayson, G.C. (2009) Scalable synthesis of L-iduronic acid derivatives via stereocontrolled cyanohydrin reaction for synthesis of heparin-related disaccharides. Org. Lett. 11, 4528-4531 CrossRef PubMed
39. Hansen, S.U., Miller, G.J., Baráth, M., Broberg, K.R., Avizienyte, E., Helliwell, M., Raftery, J., Jayson, G.C. and Gardiner, J.M. (2012) Synthesis and scalable conversion of L-iduronamides to heparin-related di-and tetrasaccharides. J. Org. Chem. 77, 7823-7843 CrossRef PubMed
40. Hansen, S.U., Miller, G.J., Jayson, G.C. and Gardiner, J.M. (2013) First gram-scale synthesis of a heparin-related dodecasaccharide. Org. Lett. 15, 88-91 CrossRef PubMed
41. 165-mediated endothelial cell functions. Chem. Sci. 4, 3218-3222 CrossRef
42. Rosenthal, M.A., Rischin, D., McArthur, G., Ribbons, K., Chong, B., Fareed, J., Toner, G., Green, M.D. and Basser, R.L. (2002) Treatment with the novel anti-angiogenic agent PI-88 is associated with immune-mediated thrombocytopenia. Ann. Oncol. 13, 770-776 CrossRef PubMed