The important role of von Willebrand factor in platelet-derived FVIII gene therapy for murine hemophilia A in the presence of inhibitory antibodies

Journal of Thrombosis and Haemostasis

Volumn 13, Issue 7, 2015, Pages 1301-1309

  Shi, Q ^a,b,c,d   Schroeder, J A ^a,b,c   Kuether, E L ^a,b,c   Montgomery, R R ^a,b,c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b BLOOD RESEARCH INSTITUTE   (United States)

^c Children's Hospital of Wisconsin   (United States)

^d Midwest Athletes Against Childhood Cancer Inc   (United States)

Author keywords

Gene therapy; Hemophilia A; Neutralizing antibody; Platelet; Von Willebrand factor

Indexed keywords

BLOOD CLOTTING FACTOR 8; VON WILLEBRAND FACTOR; AUTOANTIBODY; F8 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE THERAPY; HEMATOPOIETIC CELL; HEMOPHILIA A; MEGAKARYOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SURVIVAL RATE; 129 MOUSE; ANIMAL; BLOOD; BLOOD CLOTTING; BONE MARROW TRANSPLANTATION; C57BL MOUSE; DISEASE MODEL; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNIZATION; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PROCEDURES; THROMBOCYTE; TRANSGENIC MOUSE;

ANIMALS; AUTOANTIBODIES; BLOOD COAGULATION; BLOOD PLATELETS; BONE MARROW TRANSPLANTATION; DISEASE MODELS, ANIMAL; FACTOR VIII; GENETIC PREDISPOSITION TO DISEASE; GENETIC THERAPY; HEMOPHILIA A; HUMANS; IMMUNIZATION; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHENOTYPE; VON WILLEBRAND FACTOR;

EID: 84935446637     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13001     Document Type: Article

References (46)

1. Shi Q, Kuether EL, Schroeder JA, Perry CL, Fahs SA, Cox GJ, Montgomery RR. Factor VIII inhibitors: von Willebrand factor makes a difference invitro and invivo. J Thromb Haemost 2012; 10: 2328-37.
2. Shi Q, Wilcox DA, Fahs SA, Weiler H, Wells CW, Cooley BC, Desai D, Morateck PA, Gorski J, Montgomery RR. Factor VIII ectopically targeted to platelets is therapeutic in hemophilia A with high-titer inhibitory antibodies. J Clin Invest 2006; 116: 1974-82.
3. Haberichter SL, Shi Q, Montgomery RR. Regulated release of VWF and FVIII and the biologic implications. Pediatr Blood Cancer 2006; 46: 547-53.
4. Shi Q, Wilcox DA, Fahs SA, Fang J, Johnson BD, DU LM, Desai D, Montgomery RR. Lentivirus-mediated platelet-derived factor VIII gene therapy in murine haemophilia A. J Thromb Haemost 2007; 5: 352-61.
5. Du LM, Nurden P, Nurden AT, Nichols TC, Bellinger DA, Jensen ES, Haberichter SL, Merricks E, Raymer RA, Fang J, Koukouritaki SB, Jacobi PM, Hawkins TB, Cornetta K, Shi Q, Wilcox DA. Platelet-targeted gene therapy with human factor VIII establishes haemostasis in dogs with haemophilia A. Nat Commun 2013; 4: 2773.
6. Shi Q, Fahs SA, Wilcox DA, Kuether EL, Morateck PA, Mareno N, Weiler H, Montgomery RR. Syngeneic transplantation of hematopoietic stem cells that are genetically modified to express factor VIII in platelets restores hemostasis to hemophilia A mice with preexisting FVIII immunity. Blood 2008; 112: 2713-21.
7. Kuether EL, Schroeder JA, Fahs SA, Cooley BC, Chen Y, Montgomery RR, Wilcox DA, Shi Q. Lentivirus-mediated platelet gene therapy of murine hemophilia A with pre-existing anti-factor VIII immunity. J Thromb Haemost 2012; 10: 1570-80.
8. Shi Q, Kuether EL, Chen Y, Schroeder JA, Fahs SA, Montgomery RR. Platelet gene therapy corrects the hemophilic phenotype in immunocompromised hemophilia A mice transplanted with genetically manipulated human cord blood stem cells. Blood 2014; 123: 395-403.
9. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 1998; 67: 395-424.
10. Terraube V, O'Donnell JS, Jenkins PV. Factor VIII and von Willebrand factor interaction: biological, clinical and therapeutic importance. Haemophilia 2010; 16: 3-13.
11. Peyvandi F, Garagiola I, Baronciani L. Role of von Willebrand factor in the haemostasis. Blood Transfus 2011; 9 (Suppl. 2): s3-8.
12. Lenting PJ, Casari C, Christophe OD, Denis CV. von Willebrand factor: the old, the new and the unknown. J Thromb Haemost 2012; 10: 2428-37.
13. Flood VH, Schlauderaff AC, Haberichter SL, Slobodianuk TL, Jacobi PM, Bellissimo DB, Christopherson PA, Friedman KD, Gill JC, Hoffmann RG, Montgomery RR. Crucial role for the VWF A1 domain in binding to type IV collagen. Blood 2015; 125: 2297-304.
14. Briet E, Reisner HM, Roberts HR. Inhibitors in Christmas disease. Prog Clin Biol Res 1984; 150: 123-39.
15. Gadarowski JJ Jr, Czapek EE, Ontiveros JD, Pedraza JL. Modification of the Bethesda assay for factor VIII or IX inhibitors to improve efficiency. Acta Haematol 1988; 80: 134-8.
16. Gawryl MS, Hoyer LW. Inactivation of factor VIII coagulant activity by two different types of human antibodies. Blood 1982; 60: 1103-9.
17. Jacquemin M, Benhida A, Peerlinck K, Desqueper B, Vander EL, Lavend'homme R, d'Oiron R, Schwaab R, Bakkus M, Thielemans K, Gilles JG, Vermylen J, Saint-Remy JM. A human antibody directed to the factor VIII C1 domain inhibits factor VIII cofactor activity and binding to von Willebrand factor. Blood 2000; 95: 156-63.
18. Shima M, Scandella D, Yoshioka A, Nakai H, Tanaka I, Kamisue S, Terada S, Fukui H. A factor VIII neutralizing monoclonal antibody and a human inhibitor alloantibody recognizing epitopes in the C2 domain inhibit factor VIII binding to von Willebrand factor and to phosphatidylserine. Thromb Haemost 1993; 69: 240-6.
19. Saenko EL, Shima M, Rajalakshmi KJ, Scandella D. A role for the C2 domain of factor VIII in binding to von Willebrand factor. J Biol Chem 1994; 269: 11601-5.
20. Jacquemin M. Variable region heavy chain glycosylation determines the anticoagulant activity of a factor VIII antibody. Haemophilia 2010; 16: 16-9.
21. Nachman R, Levine R, Jaffe EA. Synthesis of factor VIII antigen by cultured guinea pig megakaryocytes. J Clin Invest 1977; 60: 914-21.
22. Jaffe EA, Hoyer LW, Nachman RL. Synthesis of antihemophilic factor antigen by cultured human endothelial cells. J Clin Invest 1973; 52: 2757-64.
23. Wagner DD. The Weibel-Palade body: the storage granule for von Willebrand factor and P-selectin. Thromb Haemost 1993; 70: 105-10.
24. Bowie EJ, Solberg LA Jr, Fass DN, Johnson CM, Knutson GJ, Stewart ML, Zoecklein LJ. Transplantation of normal bone marrow into a pig with severe von Willebrand's disease. J Clin Invest 1986; 78: 26-30.
25. Yarovoi H, Nurden AT, Montgomery RR, Nurden P, Poncz M. Intracellular interaction of von Willebrand factor and factor VIII depends on cellular context: lessons from platelet-expressed factor VIII. Blood 2005; 105: 4674-6.
26. Bi L, Lawler AM, Antonarakis SE, High KA, Gearhart JD, Kazazian HH Jr. Targeted disruption of the mouse factor VIII gene produces a model of haemophilia A. Nat Genet 1995; 10: 119-21.
27. Shi Q, Fahs SA, Kuether EL, Cooley BC, Weiler H, Montgomery RR. Targeting FVIII expression to endothelial cells regenerates a releasable pool of FVIII and restores hemostasis in a mouse model of hemophilia A. Blood 2010; 116: 3049-57.
28. Hoyer LW. The factor VIII complex: structure and function. Blood 1981; 58: 1-13.
29. Andersson LO, Brown JE. Interaction of factor VIII-von Willebrand Factor with phospholipid vesicles. Biochem J 1981; 200: 161-7.
30. Nogami K, Shima M, Nishiya K, Hosokawa K, Saenko EL, Sakurai Y, Shibata M, Suzuki H, Tanaka I, Yoshioka A. A novel mechanism of factor VIII protection by von Willebrand factor from activated protein C-catalyzed inactivation. Blood 2002; 99: 3993-8.
31. Kaufman RJ, Wasley LC, Davies MV, Wise RJ, Israel DI, Dorner AJ. Effect of von Willebrand factor coexpression on the synthesis and secretion of factor VIII in Chinese hamster ovary cells. Mol Cell Biol 1989; 9: 1233-42.
32. Weiss HJ, Sussman II, Hoyer LW. Stabilization of factor VIII in plasma by the von Willebrand factor. Studies on posttransfusion and dissociated factor VIII and in patients with von Willebrand's disease. J Clin Invest 1977; 60: 390-404.
33. Fulcher CA, de Graaf MS, Roberts JR, Kasper CK, Zimmerman TS. Localization of human factor FVIII inhibitor epitopes to two polypeptide fragments. Proc Natl Acad Sci USA 1985; 82: 7728-32.
34. Scandella D, DeGraaf MS, Mattingly M, Roeder D, Timmons L, Fulcher CA. Epitope mapping of human factor VIII inhibitor antibodies by deletion analysis of factor VIII fragments expressed in Escherichia coli. Proc Natl Acad Sci USA 1988; 85: 6152-6.
35. Healey JF, Parker ET, Barrow RT, Langley TJ, Church WR, Lollar P. The humoral response to human factor VIII in hemophilia A mice. J Thromb Haemost 2007; 5: 512-9.
36. Jacquemin MG, Desqueper BG, Benhida A, Vander EL, Hoylaerts MF, Bakkus M, Thielemans K, Arnout J, Peerlinck K, Gilles JG, Vermylen J, Saint-Remy JM. Mechanism and kinetics of factor VIII inactivation: study with an IgG4 monoclonal antibody derived from a hemophilia A patient with inhibitor. Blood 1998; 92: 496-506.
37. Kanaji S, Fahs SA, Shi Q, Haberichter SL, Montgomery RR. Contribution of platelet vs. endothelial VWF to platelet adhesion and hemostasis. J Thromb Haemost 2012; 10: 1646-52.
38. Takakura N, Watanabe T, Suenobu S, Yamada Y, Noda T, Ito Y, Satake M, Suda T. A role for hematopoietic stem cells in promoting angiogenesis. Cell 2000; 102: 199-209.
39. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP. Evidence for circulating bone marrow-derived endothelial cells. Blood 1998; 92: 362-7.
40. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 2002; 8: 403-9.
41. Bailey AS, Jiang S, Afentoulis M, Baumann CI, Schroeder DA, Olson SB, Wong MH, Fleming WH. Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood 2004; 103: 13-9.
42. Schick PK, Walker J, Profeta B, Denisova L, Bennett V. Synthesis and secretion of von Willebrand factor and fibronectin in megakaryocytes at different phases of maturation. Arterioscler Thromb Vasc Biol 1997; 17: 797-801.
43. Ruggeri ZM. The role of von Willebrand factor in thrombus formation. Thromb Res 2007; 120 (Suppl. 1): S5-9.
44. Williams SB, McKeown LP, Krutzsch H, Hansmann K, Gralnick HR. Purification and characterization of human platelet von Willebrand factor. Br J Haematol 1994; 88: 582-91.
45. Kagami K, Williams S, Horne M, Gralnick H. A preliminary analysis of platelet von Willebrand factor oligosaccharides. Nagoya J Med Sci 2000; 63: 51-6.
46. McGrath RT, McRae E, Smith OP, O'Donnell JS. Platelet von Willebrand factor-structure, function and biological importance. Br J Haematol 2010; 148: 834-43.