Synthesis and biological evaluation of a unique heparin mimetic hexasaccharide for structure-activity relationship studies

Journal of Medicinal Chemistry

Volumn 57, Issue 11, 2014, Pages 4511-4520

  Roy, Sucharita ^a   El Hadri, Ahmed ^b,c   Richard, Sebastien ^b   Denis, Fanny ^b   Holte, Kimberly ^a   Duffner, Jay ^a   Yu, Fei ^a   Galcheva Gargova, Zoya ^a   Capila, Ishan ^a   Schultes, Birgit ^a   Petitou, Maurice ^b   Kaundinya, Ganesh V ^a  

^a Momenta Pharmaceuticals Inc   (United States)

^b Endotis Pharma   (France)

^c CarboMimetics   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GROWTH FACTOR; HEPARAN SULFATE; HEPARIN; OLIGOSACCHARIDE; SCLEROPROTEIN;

ARTICLE; DRUG ACTIVITY; DRUG STRUCTURE; DRUG SYNTHESIS; IN VITRO STUDY; STRUCTURE ACTIVITY RELATION;

CYTOKINES; GLUCURONIDASE; HEPARIN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR MIMICRY; OLIGOSACCHARIDES; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONIC ACIDS;

EID: 84902466190     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm4016069     Document Type: Article

References (37)

1. Hirsh, J.; Anand, S. S.; Halperin, J. L.; Fuster, V. Guide to anticoagulant therapy: Heparin: A statement for healthcare professionals from the American Heart Association Circulation 2001, 103, 2994-3018 (Pubitemid 32578141)
2. Casu, B.; Vlodavsky, I.; Sanderson, R. D. Non anti-coagulant heparins and inhibition of cancer Pathophysiol. Haemostasis Thromb. 2007, 36, 195-203
3. Tyrrell, D. J.; Horne, A. P.; Holme, K. R.; Preuss, J. M.; Page, C. P. Heparin in inflammation: Potential therapeutic applications beyond anticoagulation Adv. Pharmacol. 1999, 46, 151-208
4. Bergamaschini, L.; Donarini, C.; Rossi, E.; De Luigi, A.; Vergani, C.; De Simon, M. G. Heparin attenuates cytotoxic and inflammatory activity of Alzheimer amyloid-β in vitro Neurobiol. Aging 2002, 23, 531-536 (Pubitemid 34495463)
5. Lin, Y.-L.; Lei, H.-Y.; Lin, Y.-S.; Yeh, T.-M.; Chen, S.-H.; Liu, H.-S. Heparin inhibits dengue-2 virus infection of five human liver cell lines Antiviral Res. 2002, 56, 93-96 (Pubitemid 35248112)
6. Esko, J. D. Glycosaminoglycan binding proteins. In Essentials of Glycobiology; Varki, A., Ed.; Cold Spring Harbor Laboratory Press: Plainview, NY, 1999.
7. Powell, A. K.; Yates, E. A.; Fernig, D. G.; Turnbull, J. E. Interactions of heparin/heparan sulfate with proteins: Appraisal of structural factors and experimental approaches Glycobiology 2004, 14, 17R-30R (Pubitemid 38628108)
8. Roy, S.; Lai, H.; Zouaoui, R.; Duffner, J.; Zhou, H.; Jayaraman, L. P.; Zhao, G.; Ganguly, T.; Kishimoto, T. K.; Venkataraman, G. Bioactivity screening of partially desulfated low-molecular weight heparins: A structure/activity relationship study Glycobiology 2011, 21, 1194-1205
9. Faham, S.; Hileman, R. E.; Fromm, J. R.; Linhardt, R. J.; Rees, D. C. Heparin structure and interactions with basic fibroblast growth factor Science 1996, 271, 1116-1120 (Pubitemid 26075225)
10. DiGabriele, A. D.; Lax, I.; Chen, D. I.; Svahn, C. M.; Jaye, M.; Schlessinger, J.; Hendrickson, W. A. Structure of a heparin-linked biologically active dimer of fibroblast growth factor Nature 1998, 393, 812-817 (Pubitemid 28299496)
11. Zhao, W.; McCallum, S. A.; Xiao, Z.; Zhang, F.; Linhardt, R. J. Binding affinities of vascular endothelial growth factor (VEGF) for heparin-derived oligosaccharides Biosci. Rep. 2012, 32, 71-81
12. Hostettler, N.; Naggi, A.; Torri, G.; Casu, B.; Vlodavsky, I.; Borsig, L. P-Selectin- and heparanase-dependent antimetastatic activity of non-anticoagulant heparins FASEB J. 2007, 21, 3562-3572 (Pubitemid 350075146)
13. Liu, J.; Shriver, Z.; Pope, R. M.; Thorp, S. C.; Duncan, M. B.; Copeland, R. J.; Raska, C. S.; Yoshida, K.; Eisenberg, R. J.; Cohen, G.; Linhardt, R. J.; Sasisekharan, R. C. Characterization of a heparan sulfate octasaccharide that binds to Herpes simplex virus type 1 glycoprotein D J. Biol. Chem. 2002, 277, 33456-33467 (Pubitemid 34984869)
14. Fry, E. E.; Lea, S. M.; Jackson, T.; Newman, J. W.; Ellard, F. M.; Blakemore, W. E.; Abu-Ghazaleh, R.; Samuel, A.; King, A. M.; Stuart, D. I. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex EMBO J. 1999, 18, 543-554 (Pubitemid 29057239)
15. Petitou, M.; van Boeckel, C. A. A. A synthetic antithrombin III binding pentasaccharide is now a drug! What comes next? Angew. Chem., Int. Ed. 2004, 42, 3118-3133 (Pubitemid 39257600)
16. Schwörer, R.; Zubkova, O. V.; Turnbull, J. E.; Tyler, P. C. Synthesis of a targeted library of heparan sulfate hexa- to dodecasaccharides as inhibitors of β-secretase: Potential therapeutics for Alzheimer's disease Chem.-Eur. J. 2013, 19, 6817-6823
17. Noti, C.; de Paz, J. L.; Polito, L.; Seeberger, P. H. Preparation and use of microarrays containing synthetic heparin oligosaccharides for the rapid analysis of heparin-protein interactions Chem.-Eur. J. 2006, 12, 8664-8686 (Pubitemid 44852453)
18. Cabannes, E.; Caravano, A.; Lewandowski, D.; Motte, V.; Nancy-Portebois, V.; Petitou, M.; Pierdet, P. Oligosaccharide compounds for use in mobilizing stem cells. WO2010/29185 A1, 2010.
19. Jacquinet, J.-C.; Petitou, M.; Duchaussoy, P.; Lederman, I.; Choay, J.; Torri, G.; Sinay, P. Synthesis of heparin fragments. A chemical synthesis of the trisaccharide O -(2-deoxy-2-sulfamido-3,6-di- O -sulfo-α- d -glucopyranosyl)-(1→4)- O -(2- O -sulfo-α- l -idopyranosyluronic acid)-(1→4)-2-deoxy-2-sulfamido-6- O -sulfo- d -glucopyranose heptasodium salt Carbohydr. Res. 1984, 130, 221-242
20. Reinold, V. N.; Carr, S. A.; Green, B. N.; Petitou, M.; Choay, J.; Sinay, P. Structural characterization of sulfated glycosaminoglycans by fast atom bombardment mass spectrometry: Application to heparin fragments prepared by chemical synthesis Carbohydr. Res. 1987, 161, 305-313
21. Jaurand, G.; Tabeur, C.; Petitou, M. Synthesis of the basic disaccharide unit of heparin Carbohydr. Res. 1994, 255, 295-302
22. Petitou, M.; Duchaussoy, P.; Jaurand, G.; Gourvenec, F.; Lederman, I.; Strassel, J.-M.; Bârzu, T.; Crépon, B.; Hérault, J.-P.; Lormeau, J.-C.; Bernat, A.; Herbert, J.-M. Synthesis and pharmacological properties of a close analogue of an antithrombotic pentasaccharide SR 90107A/ORG 31540 J. Med. Chem. 1997, 40, 1600-1607 (Pubitemid 27231463)
23. Paz, J. L.; Martin-Lomas, M. Synthesis and biological evaluation of a heparin-like hexasaccharide with the structural motifs for binding to FGF and FGFR Eur. J. Org. Chem. 2005, 9, 1849-1858 (Pubitemid 40669533)
24. Lubineau, A.; Lortat-Jacob, H.; Gavard, O.; Sarrazin, S.; Bonnaffe, D. Synthesis of tailor-made glycoconjugate mimetics of heparan sulfate that bind IFN-γ in the nanomolar range Chem.-Eur. J. 2004, 10, 4265-4282
25. Hu, Y.-P.; Lin, S.-Y.; Huang, C.-Y.; Zulueta, M. M. L.; Liu, J.-Y.; Chang, W.; Hung, S.-H. Synthesis of 3- O -sulfonated heparan sulfate octasaccharides that inhibit the Herpes simplex virus type 1 host-cell interaction Nat. Chem. 2011, 3, 557-563
26. Hamza, D.; Lucas, R.; Feizi, T.; Chai, W.; Bonnaffe, D.; Lubineau, A. First synthesis of heparan sulfate tetrasaccharides containing both N -acetylated and N -unsubstituted glucosamine: Search for putative 10E4 epitopes ChemBioChem 2006, 7, 1856-1858 (Pubitemid 44893513)
27. Tabeur, C.; Mallet, J. M.; Bono, F.; Herbert, J. M.; Petitou, M.; Sinaÿ, P. Oligosaccharides corresponding to the regular sequence of heparin: Chemical synthesis and interaction with FGF-2 Bioorg. Med. Chem. 1999, 7, 2003-2012 (Pubitemid 29457698)
28. Yin, J.; Seeberger, P. H. Applications of heparin and heparan sulfate microarrays Methods Enzymol. 2010, 478, 197-218
29. Arungundram, S.; Al-Mafraji, K.; Asong, J.; Venot, A.; Boons, G.-J.; Leach, F. E., III; Amster, I. J.; Turnbull, J. E. Modular synthesis of heparan sulfate oligosaccharides for structure-activity relationship studies J. Am. Chem. Soc. 2009, 131, 17394-17405
30. Boons, G.-J. Heparan sulfate synthesis. WO2010/117803 A2, 2010.
31. Tabeur, C.; Machetto, F.; Mallet, J.-M.; Duchaussoy, P.; Petitou, M.; Sinay, P. l -Iduronic acid derivatives as glycosyl donors Carbohydr. Res. 1996, 281, 253-276 (Pubitemid 26070015)
32. Zhang, F.; McLellan, J. S.; Ayala, A. M.; Leahy, D. J.; Linhardt, R. J. Kinetic and structural studies on interactions between heparin or heparan sulfate and proteins of the hedgehog signaling pathway Biochemistry 2007, 46, 3933-3941 (Pubitemid 46536057)
33. Zhong, X.; Desilva, T.; Lin, L.; Bodine, P.; Bhat, R. A.; Presman, E.; Pocas, J.; Stahl, M.; Kriz, R. Regulation of secreted frizzled-related protein-1 by heparin J. Biol. Chem. 2007, 282, 20523-20533 (Pubitemid 47099992)
34. Angulo, J.; Nieto, P. M. STD-NMR: Application to transient interactions between biomolecules-a quantitative approach Eur. Biophys. J. 2011, 40, 1357-1369
35. Kreuger, J.; Salmivirta, M.; Sturiale, L.; Giménez-Gallego, G.; Lindahl, U. Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2 J. Biol. Chem. 2001, 276, 30744-30752
36. Faham, S.; Hileman, R. E.; Fromm, J. R.; Linhardt, R. J.; Rees, D. C. Heparin structure and interactions with basic fibroblast growth factor Science 1996, 271, 1116-1120 (Pubitemid 26075225)
37. Yu, F.; Roy, S.; Arevalo, E.; Schaeck, J.; Wang, J.; Holte, K.; Duffner, J.; Gunay, N. S.; Capila, I.; Kaundinya, G. V. Characterization of heparin-protein interaction by saturation transfer difference (STD) NMR Anal. Bioanal. Chem. 2014, 406, 3079-3089