Immune deviation by mucosal antigen administration suppresses gene-transfer-induced inhibitor formation to factor IX

Blood

Volumn 108, Issue 2, 2006, Pages 480-486

  Cao, Ou ^b   Armstrong, Elina ^b   Schlachterman, Alexander ^b   Wang, Lixin ^b   Okita, David K ^b   Conti Fine, Bianca ^b   High, Katherine A ^b   Herzog, Roland W ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ANTIGEN; BLOOD CLOTTING FACTOR 9; CYTOKINE; EPITOPE; FACTOR 9 ANTIGEN; IMMUNOGLOBULIN G; INTERLEUKIN 10; PEPTIDE; PROTEIN HFIX; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOTTING DISORDER; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; GENE DELETION; GENE EXPRESSION; GENE MAPPING; GENE THERAPY; GENE TRANSFER; HEMOPHILIA B; IMMUNITY; MALE; MOUSE; MUCOSA; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH2 CELL; TH3 CELL;

EID: 33745939120     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-11-4668     Document Type: Article

References (44)

1. Gianelli F, Green PM. The molecular basis of hemophilia A and B. In: Lee CA, ed. Clinical Hematology: Haemophilia. Vol 9. London, United Kingdom: Bailliere Tindall; 1996:211-228.
2. Key NS. Inhibitors in congenital coagulation disorders. Br J Haematol. 2004;127:379-391.
3. Fields PA, Kowalczyk DW, Arruda VR, et al. Choice of vector determines T cell subsets involved in immune responses against the secreted transgene product factor IX. Mol Ther. 2000;1:225-235.
4. Ljung R, Petrini P, Tengborn L, Sjorin E. Haemophilia B mutations in Sweden: a population-based study of mutational heterogeneity. Br J Haematol. 2001;113:81-86.
5. Qian J, Borovok M, Bi L, Kazazian HH Jr, Hoyer LW. Inhibitor antibody development and T cell response to human factor VIII in murine hemophilia A. Thromb Haemost. 1999;81:240-244.
6. Qian J, Collins M, Sharpe AH, Hoyer LW. Prevention and treatment of factor VIII inhibitors in murine hemophilia A. Blood. 2000;95:1324-1329.
7. Wu H, Reding M, Qian J, et al. Mechanism of the immune response to human factor VIII in murine hemophilia A. Thromb Haemost. 2001;85:125-133.
8. High KA. Clinical gene transfer studies for hemophilia B. Semin Thromb Hemost. 2004;30:257-267.
9. Manno CS, Chew AJ, Hutchison S, et al. AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood. 2003;101:2963-2972.
10. Mount JD, Herzog RW, Tillson DM, et al. Sustained phenotype correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood. 2002;99:2670-2676.
11. Snyder RO, Miao C, Meuse L, et al. Correction of hemophilia B in canine and murine models using recombinant adeno-associated viral vectors. Nat Med. 1999;5:64-70.
12. Wang L, Takabe K, Bidlingmaier SM, Ill CR, Verma IM. Sustained correction of bleeding disorder in hemophilia B mice by gene therapy. Proc Natl Acad Sci U S A. 1999;96:3906-3910.
13. Mingozzi F, Liu Y-L, Dobrzynski E, et al. Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest. 2003;111:1347-1356.
14. Nathwani AC, Davidoff A, Hanawa H, Zhou J, Vanin EF, Nienhuis AW. Factors influencing in vivo transduction by recombinant adeno-associated viral vectors expressing the human factor IX cDNA. Blood. 2001;97:1258-1265.
15. Dobrzynski E, Herzog RW. Tolerance induction by viral in vivo gene transfer. Clin Med Res. 2005;3:234-240.
16. Dobrzynski E, Mingozzi F, Liu Y-L, Cao O, Wang L, Herzog RW. Induction of antigen-specific CD4+ T cell anergy and deletion by in vivo viral gene transfer. Blood. 2004;104:969-977.
17. Ziegler RJ, Lonning SM, Armentano D, et al. AAV2 vector harboring a liver-restricted promoter facilitates sustained expression of therapeutic levels of alpha-galactosidase A and the induction of immune tolerance in fabry mice. Mol Ther. 2004;9:231-240.
18. Faria AM, Weiner HL. Oral tolerance. Immunol Rev. 2005;206:232-259.
19. Weiner HL. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev. 2001;182:207-214.
20. Liu YL, Wagner K, Robinson N, et al. Optimized production of high-titer recombinant adeno-associated virus in roller bottles. Biotechniques. 2003;34:184-189.
21. Lin HF, Maeda N, Smithies O, Straight DL, Stafford DW. A coagulation factor IX-deficient mouse model for human hemophilia B. Blood. 1997;90:3962-3966.
22. Nakai H, Herzog RW, Hagstrom JN, et al. Adeno-associated viral vector-mediated gene transfer of human blood coagulation factor IX into mouse liver. Blood. 1998;91:4600-4607.
23. Fields PA, Arruda VR, Armstrong E, et al. Risk and prevention of anti-factor IX formation in AAV-mediated gene transfer in the context of a large deletion of F9. Mol Ther. 2001;4:201-210.
24. Wang L, Cao O, Swalm B, Dobrzynski E, Herzog RW. Major role of local immune responses in antibody formation to factor IX in viral gene transfer to skeletal muscle. Gene Ther. 2005;12:1453-1464.
25. Greenwood R, Wang B, Midkiff K, White GC 2nd, Lin HF, Frelinger JA. Identification of T-cell epitopes in clotting factor IX and lack of tolerance in inbred mice. J Thromb Haemost. 2003;1:95-102.
26. Karachunski PI, Ostlie NS, Okita DK, Conti-Fine BM. Prevention of experimental myasthenia gravis by nasal administration of synthetic acetylcholine receptor T epitope sequences. J Clin Invest. 1997;100:3027-3035.
27. Shevach EM, McHugh RS, Piccirillo CA, Thornton AM. Control of T-cell activation by CD4+ CD25+ suppressor T cells. Immunol Rev. 2001;182:58-67.
28. Sakaguchi S, Sakaguchi N, Shimizu J, et al. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev. 2001;182:18-32.
29. Vigouroux S, Yvon E, Biagi E, Brenner MK. Antigen-induced regulatory T cells. Blood. 2004;104:26-33.
30. Reding MT, Wu H, Krampf M, et al. CD4+ T cells specific for factor VIII as a target for specific suppression of inhibitor production. Adv Exp Med Biol. 2001;489:119-134.
31. Wang L, Dobrzynski E, Schlachterman A, Cao O, Herzog RW. Systemic protein delivery by muscle-gene transfer is limited by a local immune response. Blood. 2005;105:4226-4234.
32. Herzog RW, Dobrzynski E. Immune implications of gene therapy for hemophilia. Semin Thromb Hemost. 2004;30:215-226.
33. Shi FD, Li H, Wang H, et al. Mechanisms of nasal tolerance induction in experimental autoimmune myasthenia gravis: identification of regulatory cells. J Immunol. 1999;162:5757-5763.
34. Monfardini C, Milani M, Ostlie N, et al. Adoptive protection from experimental myasthenia gravis with T cells from mice treated nasally with acetylcholine receptor epitopes. J Neuroimmunol. 2002;123:123-134.
35. Zhang X, Izikson L, Liu L, Weiner HL. Activation of CD25(+)CD4(+) regulatory T cells by oral antigen administration. J Immunol. 2001;167:4245-4253.
36. Peng Y, Laouar Y, Li MO, Green EA, Flavell RA. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc Natl Acad Sci U S A. 2004;101:4572-4577.
37. Zheng SG, Wang JH, Gray JD, Soucier H, Horwitz DA. Natural and induced CD4+CD25+ cells educate CD4+CD25- cells to develop suppressive activity: the role of IL-2, TGF-beta, and IL-10. J Immunol. 2004;172:5213-5221.
38. Goudy KS, Burkhardt BR, Wasserfall C, et al. Systemic overexpression of IL-10 induces CD4+CD25+ cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion. J Immunol. 2003;171:2270-2278.
39. Zhang J, Xu LF, Haskins ME, Ponder KP. Neonatal gene transfer with a retroviral vector results in tolerance to human factor IX in mice and dogs. Blood. 2004;103:143-151.
40. Lei TC, Scott DW. Induction of tolerance to factor VIII inhibitors by gene therapy with immunodominant A2 and C2 domains presented by B cells as Ig fusion proteins. Blood. 2005;105:4865-4870.
41. Herzog RW, Mount JD, Arruda VR, High KA, Lothrop CD Jr. Muscle-directed gene transfer and transient immune suppression result in sustained partial correction of canine hemophilia B caused by a null mutation. Mol Ther. 2001;4:192-199.
42. Rossi G, Sarkar J, Scandella D. Long-term induction of immune tolerance after blockade of CD40-CD40L interaction in a mouse model of hemophilia A. Blood. 2001;97:2750-2757.
43. Alpan O, Kamala T, Velander W, et al. Milky way: an inexpensive and easy method of inducing tolerance to human F.IX [abstract]. Blood. 2001;98:825a. Abstract 3430.
44. Rawle FEM, Labelle AD, Davie E, Pratt K, Lillicrap DP. Prevention of anti-FVIII inhibitor formation post protein infusion in hemophilic mice by prior feeding of the FVIII-C2 domain [abstract]. Blood. 2004;104:15a. Abstract 39.