Design and characterization of an APC-specific serpin for the treatment of hemophilia

Blood

Volumn 129, Issue 1, 2017, Pages 105-113

  Polderdijk, Stéphanie G I ^a   Adams, Ty E ^a   Ivanciu, Lacramioara ^b   Camire, Rodney M ^b   Baglin, Trevor P ^c   Huntington, James A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; ALPHA1 TRYPSIN INHIBITOR; FIBRIN; PLASMINOGEN ACTIVATOR INHIBITOR 3; SERINE PROTEINASE INHIBITOR; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG; PROTEIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; DRUG DESIGN; DRUG SELECTIVITY; DRUG SPECIFICITY; HEMOPHILIA B; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTE; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; HUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG DESIGN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEMOPHILIA B; HUMANS; MICE; PROTEIN C; PROTEIN C INHIBITOR; SERPINS;

EID: 85014964504     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-05-718635     Document Type: Article

References (52)

1. Hoffman M, Monroe DM III. A cell-based model of hemostasis. Thromb Haemost. 2001;85(6):958-965.
2. MacFarlane RG. An Enzyme Cascade in the Blood Clotting Mechanism, and Its Function as a Biochemical Amplifier. Nature. 1964;202:498-499.
3. Davie EW, Ratnoff OD. Waterfall Sequence for Intrinsic Blood Clotting. Science. 1964;145(3638):1310-1312.
4. Lane DA, Philippou H, Huntington JA. Directing thrombin. Blood. 2005;106(8):2605-2612.
5. Davie EW, Kulman JD. An overview of the structure and function of thrombin. Semin Thromb Hemost. 2006;32(Suppl 1):3-15.
6. Esmon CT. The protein C anticoagulant pathway. Arterioscler Thromb. 1992;12(2):135-145.
7. Bolton-Maggs PH, Pasi KJ. Haemophilias A and B. Lancet. 2003;361(9371):1801-1809.
8. Mannucci PM. Hemophilia: treatment options in the twenty-first century. J Thromb Haemost. 2003;1(7):1349-1355.
9. Mannucci PM. Back to the future: a recent history of haemophilia treatment. Haemophiliaa. 2008;14(Suppl 3):10-18.
10. Dmoszynska A, Kuliczkowski K, Hellmann A, et al. Clinical assessment of Optivate®, a high-purity concentrate of factor VIII with von Willebrand factor, in the management of patients with haemophilia A. Haemophilia. 2011;17(3):456-462.
11. Schwartz RS, Abildgaard CF, Aledort LM, et al. Human recombinant DNA-derived antihemophilic factor (factor VIII) in the treatment of hemophilia A. recombinant Factor VIII Study Group. N Engl J Med. 1990;323(26):1800-1805.
12. Shapiro AD, Di Paola J, Cohen A, et al. The safety and efficacy of recombinant human blood coagulation factor IX in previously untreated patients with severe or moderately severe hemophilia B. Blood. 2005;105(2):518-525.
13. Aledort LM, Haschmeyer RH, Pettersson H; The Orthopaedic Outcome Study Group. A longitudinal study of orthopaedic outcomes for severe factor-VIII-deficient haemophiliacs. J Intern Med. 1994;236(4):391-399.
14. Knobe K, Berntorp E. Haemophilia and joint disease: pathophysiology, evaluation and management. J Comorbidity. 2011;1(1):51-59.
15. Brettler DB. Inhibitors in congenital haemophilia. Baillieres Clin Haematol. 1996;9(2):319-329.
16. DiMichele D. Inhibitor development in haemophilia B: an orphan disease in need of attention. Br J Haematol. 2007;138(3):305-315.
17. Kempton CL, Meeks SL. Toward optimal therapy for inhibitors in hemophilia. Blood. 2014;124(23):3365-3372.
18. Lindley CM, Sawyer WT, Macik BG, et al. Pharmacokinetics and pharmacodynamics of recombinant factor VIIa. Clin Pharmacol Ther. 1994;55(6):638-648.
19. Váradi K, Negrier C, Berntorp E, et al. Monitoring the bioavailability of FEIBA with a thrombin generation assay. J Thromb Haemost. 2003;1(11):2374-2380.
20. Astermark J, Donfield SM, DiMichele DM, et al; FENOC Study Group. A randomized comparison of bypassing agents in hemophilia complicated by an inhibitor: the FEIBA NovoSeven Comparative (FENOC) Study. Blood. 2007;109(2):546-551.
21. Dargaud Y, Lienhart A, Negrier C. Prospective assessment of thrombin generation test for dose monitoring of bypassing therapy in hemophilia patients with inhibitors undergoing elective surgery. Blood. 2010;116(25):5734-5737.
22. Morfini M, Haya S, Tagariello G, et al. European study on orthopaedic status of haemophilia patients with inhibitors. Haemophilia. 2007;13(5):606-612.
23. Sehgal A, Barros S, Ivanciu L, et al. An RNAi therapeutic targeting antithrombin to rebalance the coagulation system and promote hemostasis in hemophilia. Nat Med. 2015;21(5):492-497.
24. Waters EK, Genga RM, Schwartz MC, et al. Aptamer ARC19499 mediates a procoagulant hemostatic effect by inhibiting tissue factor pathway inhibitor. Blood. 2011;117(20):5514-5522.
25. Vianello F, Belvini D, Dal Bello F, et al. Mild bleeding diathesis in a boy with combined severe haemophilia B (C(10400)->T) and heterozygous factor V Leiden. Haemophilia. 2001;7(5):511-514.
26. Nichols WC, Amano K, Cacheris PM, et al. Moderation of hemophilia A phenotype by the factor V R506Q mutation. Blood. 1996;88(4):1183-1187.
27. Escuriola Ettingshausen C, Halimeh S, Kurnik K, et al. Symptomatic onset of severe hemophilia A in childhood is dependent on the presence of prothrombotic risk factors. Thromb Haemost. 2001;85(2):218-220.
28. Gettins PG. Serpin structure, mechanism, and function. Chem Rev. 2002;102(12):4751-4804.
29. Huntington JA, Read RJ, Carrell RW. Structure of a serpin-protease complex shows inhibition by deformation. Nature. 2000;407(6806):923-926.
30. Heeb MJ, Bischoff R, Courtney M, Griffin JH. Inhibition of activated protein C by recombinant alpha 1-antitrypsin variants with substitution of arginine or leucine for methionine358. J Biol Chem. 1990;265(4):2365-2369.
31. Rezaie AR. Vitronectin functions as a cofactor for rapid inhibition of activated protein C by plasminogen activator inhibitor-1. Implications for the mechanism of profibrinolytic action of activated protein C. J Biol Chem. 2001;276(19):15567-15570.
32. Suzuki K, Nishioka J, Kusumoto H, Hashimoto S. Mechanism of inhibition of activated protein C by protein C inhibitor. J Biochem. 1984;95(1):187-195.
33. Fortenberry YM, Hlavacek AC, Church FC. Protein C inhibitor inhibits factor VIIa when bound to tissue factor. J Thromb Haemost. 2011;9(4):861-863.
34. Li W, Adams TE, Nangalia J, Esmon CT, Huntington JA. Molecular basis of thrombin recognition by protein C inhibitor revealed by the 1.6-A structure of the heparin-bridged complex. Proc Natl Acad Sci USA. 2008;105(12):4661-4666.
35. Ivanciu L, Toso R, Margaritis P, et al. A zymogen-like factor Xa variant corrects the coagulation defect in hemophilia. Nat Biotechnol. 2011;29(11):1028-1033.
36. Schechter I, Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun. 1967;27(2):157-162.
37. Stubbs MT, Bode W. A player of many parts: the spotlight falls on thrombin's structure. Thromb Res. 1993;69(1):1-58.
38. Dickson I, Alper CA. Changes in serum proteinase inhibitor levels following bone surgery. Clin Chim Acta. 1974;54(3):381-385.
39. Ward AM, White PA, Wild G. Reference ranges for serum alpha 1 antitrypsin. Arch Dis Child. 1985;60(3):261-262.
40. Owen MC, Brennan SO, Lewis JH, Carrell RW. Mutation of antitrypsin to antithrombin. alpha 1-antitrypsin Pittsburgh (358 Met leads to Arg), a fatal bleeding disorder. N Engl J Med. 1983;309(12):694-698.
41. Zhou A, Carrell RW, Huntington JA. The serpin inhibitory mechanism is critically dependent on the length of the reactive center loop. J Biol Chem. 2001;276(29):27541-27547.
42. Bode W, Mayr I, Baumann U, Huber R, Stone SR, Hofsteenge J. The refined 1.9 A crystal structure of human alpha-thrombin: interaction with D-Phe- Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 1989;8(11):3467-3475.
43. Bah A, Chen Z, Bush-Pelc LA, Mathews FS, Di Cera E. Crystal structures of murine thrombin in complex with the extracellular fragments of murine protease-activated receptors PAR3 and PAR4. Proc Natl Acad Sci USA. 2007;104(28):11603-11608.
44. Mather T, Oganessyan V, Hof P, et al. The 2.8 A crystal structure of Gla-domainless activated protein C. EMBO J. 1996;15(24):6822-6831.
45. Falati S, Liu Q, Gross P, et al. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med. 2003;197(11):1585-1598.
46. Schlachterman A, Schuettrumpf J, Liu JH, et al. Factor V Leiden improves in vivo hemostasis in murine hemophilia models. J Thromb Haemost. 2005;3(12):2730-2737.
47. Cantin AM, Woods DE, Cloutier D, Dufour EK, Leduc R. Polyethylene glycol conjugation at Cys232 prolongs the half-life of alpha1 proteinase inhibitor. Am J Respir Cell Mol Biol. 2002;27(6):659-665.
48. Lusch A, Kaup M, Marx U, Tauber R, Blanchard V, Berger M. Development and analysis of alpha 1-antitrypsin neoglycoproteins: the impact of additional N-glycosylation sites on serum half-life. Mol Pharm. 2013;10(7):2616-2629.
49. Laurell CB, Nosslin B, Jeppsson JO. Catabolic rate of alpha1-antitrypsin of Pi type M and Z in man. Clin Sci Mol Med. 1977;52(5):457-461.
50. Arora V, Pamarthi M, Scuderi P. Method, composition, and article of manufacture for providing alpha-1 antitrypsin EP 2214699 A4. Patent application. http://www.google.co.za/patents/EP2214699A4?cl=en.
51. Goodnow CC. Transgenic mice and analysis of B-cell tolerance. Annu Rev Immunol. 1992;10:489-518.
52. Haribhai D, Engle D, Meyer M, et al. A threshold for central T cell tolerance to an inducible serum protein. J Immunol. 2003;170(6):3007-3014.