Bio-inspired liposomal thrombomodulin conjugate through bio-orthogonal chemistry

Bioconjugate Chemistry

Volumn 24, Issue 4, 2013, Pages 550-559

  Zhang, Hailong ^a   Weingart, Jacob ^a   Jiang, Rui ^a   Peng, Jianhao ^b   Wu, Qingyu ^a,b   Sun, Xue Long ^a,b  

^a CLEVELAND STATE UNIVERSITY   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CYTOLOGY; ENDOTHELIAL CELLS; ESCHERICHIA COLI; GLYCOPROTEINS; RATIONAL FUNCTIONS; RECOMBINANT PROTEINS;

C-TERMINUS; CHEMOSELECTIVE; COFACTORS; ENDOTHELIAL-CELLS; MEMBRANE PROTEINS; MIMETICS; ORTHOGONAL CHEMISTRIES; SITE-SPECIFIC; STRUCTURAL FEATURE; THROMBOMODULIN;

CHEMICAL ACTIVATION;

LIPOSOME; PROTEIN C; THROMBOMODULIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CLICK CHEMISTRY; CONJUGATE; CONTROLLED STUDY; ESCHERICHIA COLI; LIPID MEMBRANE; PROTEIN FUNCTION; PROTEIN SYNTHESIS; WESTERN BLOTTING;

EID: 84876477487     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc300399f     Document Type: Article

References (42)

1. Esmon, C. T., Esmon, N. L., and Harris, K. W. (1982) Complex formation between thrombin and thrombomodulin inhibits both thrombin-catalyzed fibrin formation and factor V activation J. Biol. Chem. 257, 7944-7947
2. Esmon, C. T. (1989) The roles of protein C and thrombomodulin in the regulation of blood coagulation J. Biol. Chem. 264, 4743-4746
3. Dittman, W. A. and Majerus, P. W. (1990) Structure and function of thrombomodulin: a natural anticoagulant Blood 75, 329-335
4. Wu, Q., Sheehan, J. P., Tsiang, M., Lentz, S. R., Birktoft, J. J., and Sadler, J. E. (1991) Single amino acid substitutions dissociate fibrinogen-clotting and thrombomodulin-binding activities of human thrombin Proc. Natl. Acad. Sci. U.S.A. 88, 6775-6779
5. Ohlin, A. K. and Marlar, R. A. (1995) The first mutation identified in the thrombomodulin gene in a 45-year-old man presenting with thromboembolic disease Blood 85, 330-336
6. Rosenberg, R. D. and Aird, W. C. (1999) Vascular-bed-specific hemostasis and hypercoagulable states N. Engl. J. Med. 340, 1555-1564
7. Kumada, T., Dittman, W. A., and Majerus, P. W. (1988) A role for thrombomodulin in the pathogenesis of thrombin-induced thromboembolism in mice Blood 71, 728-733
8. Gresele, P. and Agnelli, G. (2002) Novel approaches to the treatment of thrombosis Trends Pharmacol. Sci. 23, 25-30
9. Parkinson, J. F., Grinnell, B. W., Moore, R. E., Hoskins, J., Vlahost, C. J., and Bang, N. U. (1990) Stable expression of a secretable deletion mutant of recombinant human thrombomodulin in mammalian cells J. Biol. Chem. 265, 12602-12610
10. Gomi, K., Zushi, M., Honda, G., Kawahara, S., Matsuzaki, O., Kanabayashi, T., Yamamoto, S., Maruyama, I., and Suzuki, K. (1990) Antithrombotic effect of recombinant human thrombomodulin on thrombin-induced thromboembolism in mice Blood 75, 1396-1399
11. Saito, H., Maruyama, I., Shimazaki, S., Yamamoto, Y., Aikawa, N., Ohno, R., Hirayama, A., Matsuda, T., Asakura, H., Nakashima, M., and Aoki, N. (2007) Efficacy and safety of recombinant human soluble thrombomodulin (ART-123) in disseminated intravascular coagulation: results of a phase III, randomized, double-blind clinical trial J. Thromb. Haemost. 5, 31-41
12. Ding, B. -S., Hong, N., Christofidou-Solomidou, M., Gottstein, C. S., Albelda, M., Cines, D. B., Fisher, A. B., and Muzykantou, V. R. (2009) Anchoring fusion thrombomodulin to the endothelial lumen protects against injury-induced lung thrombosis and inflammation Am. J. Respir. Crit. Care Med. 180, 247-256
13. Moll, S., Lindley, C., Pescatore, S., Morrison, D., Tsuruta, K., Mohri, M., Serada, M., Sata, M., Shimizu, H., Yamada, K., and White, G. C. (2004) Phase I study of a novel recombinant human soluble thrombomodulin, ART-123 J. Thromb. Haemost. 2, 1745-51
14. Ito, I. and Maruyama, I. (2011) Thrombomodulin: protectorate God of the vasculature in thrombosis and inflammation J. Thromb. Haemost. 9, 168-173
15. Bajzar, L., Morser, J., and Nesheim, M. (1996) TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex J. Biol. Chem. 271, 16603-16608
16. Bajzar, L., Manuel, R., and Nesheim, M. E. (1995) Purification and characterization of TAFI, a thrombin-activable fibrinolysis inhibitor J. Biol. Chem. 270, 14477-14484
17. Zushi, M., Gomi, K., Yamamoto, S., Maruyama, I., Hayashi, T., and Suzuki, H. (1989) The last three consecutive epidermal growth factor-like structures of human thrombomodulin comprise the minimum functional domain for protein C-activating cofactor activity and anticoagulant activity J. Biol. Chem. 264, 10351-10353
18. Parkinson, J. F., Nagashima, M. M., Kuhn, I., Leonard, J., and Morser, J. (1992) Structure-function studies of the epidermal growth factor domains of human thrombomodulin Biochem. Biophys. Res. Commun. 185, 567-576
19. Adams, T. E., Li, W., and Huntington, J. A. (2009) Molecular basis of thrombomodulin activation of slow thrombin J. Thromb. Haemost. 7, 1688-1695
20. Cazalis, C. S., Haller, C. A., Sease-Cargo, L., and Chaikof, E. L. (2004) C-terminal site-specific PEGylation of a truncated thrombomodulin mutant with retention of full bioactivity Bioconjugate Chem. 15, 1005-1009
21. Susuki, M., Mohri, M., and Yamamoto, S. (1998) In vitro anticoagulant properties of a minimum functional fragment of human thrombomodulin and in vivo demonstration of its benefit as an anticoagulant in extracorporeal circulation using a monkey model Thromb. Haemost. 79, 417-422
22. Tseng, P. -Y., Rele, S. S., Sun, X. -L., and Chaikof, E. L. (2006) Membrane-mimetic films containing thrombomodulin and heparin inhibit tissue factor-induced thrombin generation in a flow model Biomaterials 27, 2637-2650
23. Torchilin, V. P. (2005) Recent advances with liposomes as pharmaceutical carriers Nat. Rev. Drug Discovery 4, 145-160
24. Katre, N. V. (1993) The conjugation of proteins with polyethylene glycol and other polymers: Altering properties of proteins to enhance their therapeutic potential Adv. Drug Delivery Rev. 10, 91-114
25. Monkarsh, S. P., Ma, Y. M., Aglione, A., Bailon, P., Ciolek, D., DeBarbieri, B., Graves, M. C., Hollfelder, K., Michel, H., Palleroni, A., Porter, J. E., Russoman, E., Roy, S., and Pan, Y. C. E. (1997) Positional isomers of monopegylated interferon α2a: Isolation, characterization, and biological activity Anal. Biochem. 247, 434-440
26. Strømgaard, A., Jensen, A. A., and Strømgaard, K. (2004) Site-specific incorporation of unnatural amino acids into proteins ChemBioChem 5, 909-916
27. Kiick, K. L., Saxon, E., Tirrell, D. A., and Bertozzi, C. R. (2002) Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation Proc. Natl. Acad. Sci. U.S.A. 99, 19-24
28. Wang, Q., Chan, T. R., Hilgraf, R., Fokin, V. V., Sharpless, K. B., and Finn, M. G. (2003) Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition J. Am. Chem. Soc. 125, 3192-3193
29. Agard, N. J., Prescher, J. A., and Bertozzi, C. R. (2004) A strain-promoted [3 + 2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems J. Am. Chem. Soc. 126, 15046-15047
30. Sun, X. -L., Stabler, C., Cazalis, C., and Chaikof, E. L. (2006) Carbohydrate and protein immobilization onto solid surfaces by sequential Diels-Alder and azide-alkyne cycloadditions Bioconjugate Chem. 17, 52-57
31. van Dijk, M., Rijkers, D. T. S., Liskamp, R. M. J., van Nostrum, C. F., and Hennink, W. E. (2009) Synthesis and applications of biomedical and pharmaceutical polymers via click chemistry methodologies Bioconjugate Chem. 20, 2001-2016
32. Gaetke, L. M. and Chow, C. K. (2003) Copper toxicity, oxidative stress, and antioxidant nutrients Toxicology 189, 147-163
33. Debets, M. F., van Berkel, S. S., Dommerholt, J., Dirks, A. J., Rutjes, F. P. J. T., and van Delft, F. L. (2011) Bioconjugation with strained alkenes and alkynes Acc. Chem. Res. 44, 805-815
34. Debets, M. F., van der Doelen, C. W. J., Rutjes, F. P. J. T., and van Delft, F. L (2010) Azide: a unique dipole for metal-free bioorthogonal ligations ChemBioChem 11, 1168-1184
35. Ning, X., Guo, J., Wolfert, M. A., and Boons, G.-J. (2008) Visualizing metabolically labeled glycoconjugates of living cells by copper-free and fast huisgen cycloadditions Angew. Chem., Int. Ed. 47, 2253-2255
36. Bostic, H. E., Smith, M. D., Poloukhtine, A. A., Popik, V. V., and Best, M. D. (2012) Membrane labeling and immobilization via copper-free click chemistry Chem. Commun. 48, 1431-3
37. Agard, N. J., Baskin, J. M., Prescher, J. A., Lo, A., and Bertozzi, C. R. (2006) A Comparative study of bioorthogonal reactions with azides ACS Chem. Biol. 1, 644-648
38. Ma, Y., Zhang, H., and Sun, X. -L. (2010) Surface-bound cytomimetic assembly based on chemoselective and biocompatible immobilization and further modification of intact liposome Bioconjugate Chem 21, 1994-1999
39. Zhang, H., Ma, Y., and Sun, X. -L. (2009) Chemical selective surface glyco-functionalization of liposome through staudinger ligation Chem. Commun. 3032-3034
40. Esmon, N. L., DeBault, L. E., and Esmon, C. T. (1983) Proteolytic formation and properties of gamma-carboxyglutamic acid-domainless protein C J. Biol. Chem. 258, 5548-5553
41. Davie, E. W., Fujikawa, K., and Kisiel, W. (1991) The coagulation cascade: initiation, maintenance, and regulation Biochemistry 30, 10363-10370
42. Galvin, J., B., Kurosawa, S., Moore, K., Esmon, C. T., and Esmon, N. J. (1987) Reconstitution of rabbit thrombomodulin into phospholipid vesicles J. Biol. Chem. 262, 2199-2205