De novo design of self-assembling foldamers that inhibit heparin-protein interactions

ACS Chemical Biology

Volumn 9, Issue 4, 2014, Pages 967-975

  Montalvo, Geronda L ^a   Zhang, Yao ^b   Young, Trevor M ^d   Costanzo, Michael J ^d   Freeman, Katie B ^d   Wang, Jun ^c   Clements, Dylan J ^d   Magavern, Emma ^a   Kavash, Robert W ^d   Scott, Richard W ^d   Liu, Dahui ^d   Degrado, William F ^a,b,c  

^a Department of Biochemistry and Biophysics ^*  (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PolyMedix Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; AMYLOID; ANTICOAGULANT AGENT; ANTITHROMBIN III; BLOOD CLOTTING FACTOR 10A; DIMER; FOLDAMER; FONDAPARINUX; HEPARIN; HEPARIN DERIVATIVE; MONOMER; POLYMER; PROTEIN; SALICYLAMIDE; UNCLASSIFIED DRUG; FIBRINOLYTIC AGENT; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CHEMICAL MODIFICATION; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; DISSOCIATION; DRUG DESIGN; DRUG STRUCTURE; HYDROPHOBICITY; IONIC STRENGTH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CARBOHYDRATE INTERACTION; ULTRACENTRIFUGATION; ULTRAVIOLET SPECTROSCOPY; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; IC50; PROTEIN CONFORMATION; SYNTHESIS;

CIRCULAR DICHROISM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DESIGN; FIBRINOLYTIC AGENTS; HEPARIN; INHIBITORY CONCENTRATION 50; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84899072740     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500026x     Document Type: Article

References (43)

1. Gellman, S. H. (1998) Foldamers: a manifesto Acc. Chem. Res. 31, 173-180
2. Goodman, C. M., Choi, S., Shandler, S., and DeGrado, W. F. (2007) Foldamers as versatile frameworks for the design and evolution of function Nat. Chem. Biol. 3, 252-262
3. Guichard, G. and Huc, I. (2011) Synthetic foldamers Chem. Commun. 47, 5933-5941
4. Hill, D. J., Mio, M. J., Prince, R. B., Hughes, T. S., and Moore, J. S. (2001) A field guide to foldamers Chem. Rev. 101, 3893-4012
5. Choi, S., Clements, D. J., Pophristic, V., Ivanov, I., Vemparala, S., Bennett, J. S., Klein, M. L., Winkler, J. D., and DeGrado, W. F. (2005) The design and evaluation of heparin-binding foldamers Angew. Chem., Int. Ed. 44, 6685-6689
6. Choi, S., Isaacs, A., Clements, D., Liu, D., Kim, H., Scott, R. W., Winkler, J. D., and DeGrado, W. F. (2009) De novo design and in vivo activity of conformationally restrained antimicrobial arylamide foldamers Proc. Natl. Acad. Sci. U.S.A. 106, 6968-6973
7. Kritzer, J. A., Hodsdon, M. E., and Schepartz, A. (2005) Solution structure of a peptide ligand for hDM2 J. Am. Chem. Soc. 127, 4118-4119
8. Lee, E. F., Sadowsky, J. D., Smith, B. J., Czabotar, P. E., Peterson-Kaufman, K. J., Colman, P. M., Gellman, S. H., and Fairlie, W. D. (2009) High-resolution structural characterization of a helical α/peptide foldamer bound to the anti-apoptotic protein Bcl-xL Angew. Chem., Int. Ed. 48, 4318-4322
9. Liu, D., Choi, S., Chen, B., Doerksen, R. J., Clements, D. J., Winkler, J. D., Klein, M. L., and DeGrado, W. F. (2004) Nontoxic membrane-active antimicrobial arylamide oligomers Angew. Chem., Int. Ed. 43, 1158-1162
10. Cheng, P. N., Liu, C., Zhao, M., Eisenberg, D., and Nowick, J. S. (2012) Amyloid sheet mimics that antagonize protein aggregation and reduce amyloid toxicity Nat. Chem. 4, 927-933
11. Gong, B., Yan, Y., Zeng, H., Skrzypczak-Jankunn, E., Kim, Y. W., Zhu, J., and Ickes, H. (1999) A new approach for the design of supramolecular recognition units: hydrogen-bonded molecular duplexes J. Am. Chem. Soc. 121, 5607-5608
12. Haldar, D., Jiang, H., Leger, J. M., and Huc, I. (2006) Interstrand interactions between side chains in a double-helical foldamer Angew. Chem., Int. Ed. 45, 5483-5486
13. Huc, I. (2004) Aromatic oligoamide foldamers Eur. J. Org. Chem. 2004, 17-29
14. Maurizot, V., Dolain, C., and Huc, I. (2005) Intramolecular versus intermolecular induction of helical handedness in pyridinedicarboxamide oligomers Eur. J. Org. Chem. 1293-1301
15. Nowick, J. S. (2008) Exploring sheet structure and interactions with chemical model systems Acc. Chem. Res. 41, 1319-1330
16. Sanford, A. R., Yamato, K., Yang, X., Yuan, L., Han, Y., and Gong, B. (2004) Well-defined secondary structures Eur. J. Biochem. 271, 1416-1425
17. Price, J. L., Horne, W. S., and Gellman, S. H. (2010) Structural consequences of amino acid preorganization in a self-assembling α/peptide: fundamental studies of foldameric helix bundles J. Am. Chem. Soc. 132, 12378-12387
18. Daniels, D. S., Petersson, E. J., Qiu, J. X., and Schepartz, A. (2007) High-resolution structure of a peptide bundle J. Am. Chem. Soc. 129, 1532-1533
19. Giuliano, M. W., Horne, W. S., and Gellman, S. H. (2009) An α/-peptide helix bundle with a pure 3-amino acid core and a distinctive quaternary structure J. Am. Chem. Soc. 131, 9860-9861
20. Petersson, E. J. and Schepartz, A. (2008) Toward -amino acid proteins: design, synthesis, and characterization of a fifteen kilodalton peptide tetramer J. Am. Chem. Soc. 130, 821-823
21. Capila, I. and Linhardt, R. J. (2002) Heparin-Protein Interactions Angew. Chem., Int. Ed. 41, 391-412
22. Jin, L., Abrahams, J. P., Skinner, R., Petitou, M., Pike, R. N., and Carrell, R. W. (1997) The anticoagulant activation of antithrombin by heparin Proc. Natl. Acad. Sci. U.S.A. 94, 14683-14688
23. Johnson, D. J. and Huntington, J. A. (2003) Crystal structure of antithrombin in a heparin-bound intermediate state Biochemistry (Moscow) 42, 8712-8719
24. Olson, S. T. and Chuang, Y. J. (2002) Heparin activates antithrombin anticoagulant function by generating new interaction sites (exosites) for blood clotting proteinases Trends Cardiovasc. Med. 12, 331-338
25. Rosenberg, R. D. and Damus, P. S. (1973) The purification and mechanism of action of human antithrombin-heparin cofactor J. Biol. Chem. 248, 6490-6505
26. Lever, R. and Page, C. P. (2002) Novel drug development opportunities for heparin Nat. Rev. Drug Discovery 1, 140-148
27. Jones, G. R., Hashim, R., and Power, D. M. (1986) A comparison of the strength of binding of antithrombin-III, protamine and poly(L-lysine) to heparin samples of different anticoagulant activities Biochim. Biophys. Acta 883, 69-76
28. Mecca, T., Consoli, G. M. L., Geraci, C., La Spina, R., and Cunsolo, F. (2006) Polycationic calix[8]arenes able to recognize and neutralize heparin Org. Biomol. Chem. 4, 3763-3768
29. Cardin, A. D. and Weintraub, H. J. (1989) Molecular modeling of protein-glycosaminoglycan interactions Arteriosclerosis 9, 21-32
30. Fromm, J. R., Hileman, R. E., Caldwell, E. E., Weiler, J. M., and Linhardt, R. J. (1997) Pattern and spacing of basic amino acids in heparin binding sites Arch. Biochem. Biophys. 343, 92-100
31. Margalit, H., Fischer, N., and Ben-Sasson, S. A. (1993) Comparative analysis of structurally defined heparin binding sequences reveals a distinct spatial distribution of basic residues J. Biol. Chem. 268, 19228-19231
32. Chang, L. C., Liang, J. F., Lee, H. F., Lee, L. M., and Yang, V. C. (2001) Low molecular weight protamine (LMWP) as nontoxic heparin/low molecular weight heparin antidote (II): in vitro evaluation of efficacy and toxicity AAPS PharmSci. 3, E18
33. Lee, L. M., Chang, L. C., Wrobleski, S., Wakefield, T. W., and Yang, V. C. (2001) Low molecular weight protamine as nontoxic heparin/low molecular weight heparin antidote (III): preliminary in vivo evaluation of efficacy and toxicity using a canine model AAPS PharmSci. 3, E19
34. Choay, J., Petitou, M., Lormeau, J. C., Sinay, P., Casu, B., and Gatti, G. (1983) Structure-activity relationship in heparin: a synthetic pentasaccharide with high affinity for antithrombin III and eliciting high anti-factor Xa activity Biochem. Biophys. Res. Commun. 116, 492-499
35. Zeng, H., Miller, R. S., Flowers, R. A., and Gong, B. (2000) A highly stable, six-hydrogen-bonded molecular duplex J. Am. Chem. Soc. 122, 2635-2644
36. Zeng, H., Yang, X., Flowers, R. A., and Gong, B. (2002) A noncovalent approach to antiparallel sheet formation J. Am. Chem. Soc. 124, 2903-2910
37. Lindahl, U., Backstrom, G., Hook, M., Thunberg, L., Fransson, L. A., and Linker, A. (1979) Structure of the antithrombin-binding site in heparin Proc. Natl. Acad. Sci. U.S.A. 76, 3198-3202
38. Lindahl, U., Backstrom, 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
39. Lindahl, U., Thunberg, L., Backstrom, G., Riesenfeld, J., Nordling, K., and Bjork, I. (1984) Extension and structural variability of the antithrombin-binding sequence in heparin J. Biol. Chem. 259, 12368-12376
40. Thunberg, L., Backstrom, G., and Lindahl, U. (1982) Further characterization of the antithrombin-binding sequence in heparin Carbohydr. Res. 100, 393-410
41. Fromm, J. R., Hileman, R. E., Caldwell, E. E., Weiler, J. M., and Linhardt, R. J. (1995) Differences in the interaction of heparin with arginine and lysine and the importance of these basic amino acids in the binding of heparin to acidic fibroblast growth factor Arch. Biochem. Biophys. 323, 279-287
42. Schedin-Weiss, S., Arocas, V., Bock, S. C., Olson, S. T., and Bjork, I. (2002) Specificity of the basic side chains of Lys114, Lys125, and Arg129 of antithrombin in heparin binding Biochemistry (Moscow) 41, 12369-12376
43. Udit, A. K., Everett, C., Gale, A. J., Reiber Kyle, J., Ozkan, M., and Finn, M. G. (2009) Heparin antagonism by polyvalent display of cationic motifs on virus-like particles ChemBioChem 10, 503-510