Inhibitors - cellular aspects and novel approaches for tolerance

Haemophilia

Volumn 20, Issue S4, 2014, Pages 80-86

  Scott, D W ^a  

^a Uniformed Services University of the Health Sciences   (United States)

Author keywords

Factor VIII; Gene therapy; Haemophilia; Immunoglobulin fusions; Regulatory T cells

Indexed keywords

BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 8 INHIBITOR; BLOOD CLOTTING FACTOR 9; BLOOD CLOTTING INHIBITOR; IMMUNOGLOBULIN G; NANOPARTICLE; NEUTRALIZING ANTIBODY; PROCOAGULANT; ALLOANTIBODY;

ANTIBODY RESPONSE; B LYMPHOCYTE; CELL ENGINEERING; GENE MUTATION; GENE THERAPY; HEMOPHILIA; HEMOPHILIA A; HEMOPHILIA B; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOTHERAPY; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; ANIMAL; BIOLOGICAL THERAPY; BLOOD; GENETICS; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; B-LYMPHOCYTES; CELL- AND TISSUE-BASED THERAPY; FACTOR IX; FACTOR VIII; HEMOPHILIA A; HEMOPHILIA B; HUMANS; IMMUNE TOLERANCE; IMMUNOGLOBULIN G; IMMUNOTHERAPY; ISOANTIBODIES; T-LYMPHOCYTE SUBSETS;

EID: 84899528071     PISSN: 13518216     EISSN: 13652516     Source Type: Journal    
DOI: 10.1111/hae.12407     Document Type: Review

References (70)

1. Playfair JH. A cellular basis for auto-immunity. Essays Fundam Immunol 1973; 44-56.
2. Singh NJ, Schwartz RH. Primer: mechanisms of immunologic tolerance. Nat Clin Pract Rheumatol 2006; 2: 44-52.
3. Westerberg LS, Klein C, Snapper SB. Breakdown of T cell tolerance and autoimmunity in primary immunodeficiency-lessons learned from monogenic disorders in mice and men. Curr Opin Immunol 2008; 20: 646-54.
4. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8: 523-32.
5. Aledort LM, Evatt BL, Lusher JM, Brownstein AP. HIV and hemophilia. J Thromb Haemost 2007; 5: 607-10.
6. Bray GL, Kroner BL, Arkin S et al. Loss of high-responder inhibitors in patients with severe hemophilia A and human immunodeficiency virus type 1 infection: a report from the Multi-Center Hemophilia Cohort Study. Am J Hematol 1993; 42: 375-9.
7. Qian J, Collins M, Sharpe AH, Hoyer LW. Prevention and treatment of factor VIII inhibitors in murine hemophilia A. Blood 2000; 95: 1324-9.
8. Qian J, Burkly LC, Smith EP et al. Role of CD154 in the secondary immune response: the reduction of pre-existing splenic germinal centers and anti-factor VIII inhibitor titer. Eur J Immunol 2000; 30: 2548-54.
9. Qian J, Borovok M, Bi L, Kazazian HH, Hoyer LW. Inhibitor antibody development and T cell response to human factor VIII in murine hemophilia A. Thromb Haemost 1999; 81: 240-4.
10. Liu M-C, Ettinger RA, Gunasekera D, James EA, Lewis KB, Pratt KP. Identification of potential T-cell epitopes in factor VIII using peptide microarrays. Haemophilia 2012; 18 (Suppl 3): 94.
11. Moise L, Skupsky J, Tassone R et al. De-immunization of human factor VIII: identification of pitopes in the C2 domain. ASH Annual Meeting Abstracts 2008; 112: 1030.
12. Ettinger R, Epstein M, Puranik K et al. Sequence-modified factor VIII variants having reduced immunogenicity. ASH Annual Meeting Abstracts 2012; 120: 39.
13. DiMichele DM, Kroner BL. The North American immune tolerance registry: practices, outcomes, outcome predictors. Thromb Haemost 2002; 87: 52-7.
14. Mariani G, Kroner B. Immune tolerance in hemophilia with factor VIII inhibitors: predictors of success. Haematologica 2001; 86: 1186-93.
15. High KA. The gene therapy journey for hemophilia: are we there yet? Blood 2012; 120: 4482-7.
16. Nathwani AC, Rosales C, McIntosh J et al. Long-term safety and efficacy following systemic administration of a self-complementary AAV vector encoding human FIX pseudotyped with serotype 5 and 8 capsid proteins. Mol Ther 2011; 19: 876-85.
17. Matsui H, Hegadorn C, Ozelo M et al. A microRNA-regulated and GP64-pseudotyped lentiviral vector mediates stable expression of FVIII in a murine model of Hemophilia A. Mol Ther 2011; 19: 723-30.
18. Annoni A, Brown BD, Cantore A, Sergi LS, Naldini L, Roncarolo MG. In vivo delivery of a microRNA-regulated transgene induces antigen-specific regulatory T cells and promotes immunologic tolerance. Blood 2009; 114: 5152-61.
19. Vandendriessche T, Chuah MK. Clinical progress in gene therapy: sustained partial correction of the bleeding disorder in patients suffering from severe hemophilia B. Hum Gene Ther 2012; 23: 4-6.
20. Scott DW, Lozier JN. Gene therapy for haemophilia: prospects and challenges to prevent or reverse inhibitor formation. Br J Haematol 2012; 156: 295-302.
21. High KA. Gene therapy for haemophilia: a long and winding road. J Thromb Haemost 2011; 9(Suppl 1): 2-11.
22. Chuah MK, Nair N, VandenDriessche T. Recent progress in gene therapy for hemophilia. Hum Gene Ther 2012; 23: 557-65.
23. Miao CH. Advances in overcoming immune responses following hemophilia gene therapy. J Genet Syndr Gene Ther; 2011: 18(Suppl 1): 1-17.
24. Peng B, Ye P, Rawlings DJ, Ochs HD, Miao CH. Anti-CD3 antibodies modulate anti-factor VIII immune responses in hemophilia A mice after factor VIII plasmid-mediated gene therapy. Blood 2009; 114: 4373-82.
25. Scott DW, Pratt KP, Miao CH. Progress toward inducing immunologic tolerance to factor VIII. Blood 2013; 121: 4449-56.
26. Weiner HL, da Cunha AP, Quintana F, Wu H. Oral tolerance. Immunol Rev 2011; 241: 241-59.
27. Rawle FE, Pratt KP, Labelle A, Weiner HL, Hough C, Lillicrap D. Induction of partial immune tolerance to factor VIII through prior mucosal exposure to the factor VIII C2 domain. J Thromb Haemost 2006; 4: 2172-9.
28. Kwon KC, Verma D, Singh ND, Herzog R, Daniell H. Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv Drug Deliv Rev 2012; 65: 782-99.
29. Miao CH. Immunomodulation for inhibitors in hemophilia A: the important role of Treg cells. Expert Rev Hematol 2010; 3: 469-83.
30. Liu CL, Ye P, Yen BC, Miao CH. In vivo expansion of regulatory T cells with IL-2/IL-2 mAb complexes prevents anti-factor VIII immune responses in hemophilia A mice treated with factor VIII plasmid-mediated gene therapy. Mol Ther 2011; 19: 1511-20.
31. Skupsky J, Saltis M, Song C, Rossi R, Nelson D, Scott DW. Gene therapy for tolerance and vice versa: a case for hemophilia. Curr Opin Mol Ther 2010; 12: 509-18.
32. Paley RS, Leskowitz S, Borel Y. Effect on tolerance induction of the mode of attachment of the hapten the carrier. J Immunol 1975; 115: 1409-13.
33. Venkataraman M, Aldo-Benson M, Borel Y, Scott DW. Persistence of antigen-binding cells with surface tolerogen: isologous versus heterologous immunoglobulin carriers. J Immunol 1977; 119: 1006-9.
34. Borel Y, Kilham L, Hyslop N, Borel H. Isologous IgG-induced tolerance to benzyl penicilloyl. Nature 1976; 261: 49-50.
35. Borel Y, Lewis RM, Stollar BD. Prevention of murine lupus nephritis by carrier-dependent induction of immunologic tolerance to denatured DNA. Science 1973; 182: 76-8.
36. Borel Y. Haptens bound to self IgG induce immunologic tolerance, while when coupled to syngeneic spleen cells they induce immune suppression. Immunol Rev 1980; 50: 71-104.
37. Zambidis ET, Scott DW. Epitope-specific tolerance induction with an engineered immunoglobulin. Proc Natl Acad Sci U S A 1996; 93: 5019-24.
38. Eynon EE, Parker DC. Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigens. J Exp Med 1992; 175: 131-8.
39. Fuchs EJ, Matzinger P. B cells turn off virgin but not memory T cells. Science 1992; 258: 1156-9.
40. Gilbert KM, Weigle WO. Tolerogenicity of resting and activated B cells. J Exp Med 1994; 179: 249-58.
41. Zambidis ET, Kurup A, Scott DW. Genetically transferred central and peripheral immune tolerance via retroviral-mediated expression of immunogenic epitopes in hematopoietic progenitors or peripheral B lymphocytes. Mol Med 1997; 3: 212-24.
42. Zambidis ET, Barth RK, Scott DW. Both resting and activated B lymphocytes expressing engineered peptide-Ig molecules serve as highly efficient tolerogenic vehicles in immunocompetent adult recipients. J Immunol 1997; 158: 2174-82.
43. Melo ME, Qian J, El-Amine M et al. Gene transfer of Ig-fusion proteins into B cells prevents and treats autoimmune diseases. J Immunol 2002; 168: 4788-95.
44. Song L, Wang J, Wang R et al. Retroviral delivery of GAD-IgG fusion construct induces tolerance and modulates diabetes: a role for CD4 + regulatory T cells and TGF-beta? Gene Ther 2004; 11: 1487-96.
45. Soukhareva N, Jiang Y, Scott DW. Treatment of diabetes in NOD mice by gene transfer of Ig-fusion proteins into B cells: role of T regulatory cells. Cell Immunol 2006; 240: 41-6.
46. Xu B, Haviernik P, Wolfraim LA, Bunting KD, Scott DW. Bone marrow transplantation combined with gene therapy to induce antigen-specific tolerance and ameliorate EAE. Mol Ther 2006; 13: 42-8.
47. Xu B, Scott DW. A novel retroviral gene therapy approach to inhibit specific antibody production and suppress experimental autoimmune encephalomyelitis induced by MOG and MBP. Clin Immunol 2004; 111: 47-52.
48. Satpute SR, Soukhareva N, Scott DW, Moudgil KD. Mycobacterial Hsp65-IgG-expressing tolerogenic B cells confer protection against adjuvant-induced arthritis in Lewis rats. Arthritis Rheum 2007; 56: 1490-6.
49. Liang W, Karabekian Z, Mattapallil M et al. B-cell delivered gene transfer of human S-Ag-Ig fusion protein protects from experimental autoimmune uveitis. Clin Immunol 2006; 118: 35-41.
50. Agarwal RK, Kang Y, Zambidis E, Scott DW, Chan CC, Caspi RR. Retroviral gene therapy with an immunoglobulin-antigen fusion construct protects from experimental autoimmune uveitis. J Clin Invest 2000; 106: 245-52.
51. 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: 4865-70.
52. Skupsky J, Su Y, Lei TC, Scott DW. Tolerance induction by gene transfer to lymphocytes. Curr Gene Ther 2007; 7: 369-80.
53. Wang XM, Moghimi B, Zolotukhin I, Cao C, Herzog RW. Immune tolerance induction to factor IX through B cell gene transfer - delineating between tolerogenic and immunogenic B cells. Blood 2012; 120: 14.
54. Dierselhuis MP, Schrama E, Scott DW, Spierings E. Gene therapy with IgG-HY fusion proteins to reduce male-specific T-cell reactivity in vitro. Hum Gene Ther 2011; 22: 44-54.
55. Cavazzana-Calvo M, André-Schmutz I, Fischer A. Haematopoietic stem cell transplantation for SCID patients: where do we stand? Br J Haematol 2013; 160: 146-52.
56. De Groot AS, Moise L, McMurry JA et al. Activation of natural regulatory T cells by IgG Fc-derived peptide 'Tregitopes'. Blood 2008; 112: 3303-11.
57. Su Y, Rossi R, De Groot AS, Scott DW. Regulatory T cell epitopes (Tregitopes) in IgG induce tolerance in vivo and lack immunogenicity per se. J Leukoc Biol 2013 94: 377-83.
58. Cousens LP, Su Y, McClaine E et al. Application of IgG-derived natural Treg epitopes (IgG Tregitopes) to antigen-specific tolerance induction in a murine model of type 1 diabetes. J Diabetes Res 2013; 2013: 621693.
59. Cousens LP, Najafian N, Mingozzi F et al. In vitro and in vivo studies of IgG-derived Treg epitopes (Tregitopes): a promising new tool for tolerance induction and treatment of autoimmunity. J Clin Immunol 2013; 33(Suppl 1): S43-9.
60. Skupsky J, Zhang AH, Su Y, Scott DW. B-cell-delivered gene therapy induces functional T regulatory cells and leads to a loss of antigen-specific effector cells. Mol Ther 2010; 18: 1527-35.
61. Kang Y, Melo M, Deng E, Tisch R, El-Amine M, Scott DW. Induction of hyporesponsiveness to intact foreign protein via retroviral-mediated gene expression: the IgG scaffold is important for induction and maintenance of immune hyporesponsiveness. Proc Natl Acad Sci U S A 1999; 96: 8609-14.
62. Lei TC, Su Y, Scott DW. Tolerance induction via a B-cell delivered gene therapy-based protocol: optimization and role of the Ig scaffold. Cell Immunol 2005; 235: 12-20.
63. Cousens LP, Tassone R, Mazer BD, Ramachandiran V, Scott DW, De Groot AS. Tregitope update: mechanism of action parallels IVIg. Autoimmun Rev 2013; 12: 436-43.
64. McCoy ME, Golden HE, Doll TA et al. Mechanisms of protective immune responses induced by the Plasmodium falciparum circumsporozoite protein-based, self-assembling protein nanoparticle vaccine. Malar J 2013; 12: 357.
65. Getts DR, Martin AJ, McCarthy DP et al. Microparticles bearing encephalitogenic peptides induce T-cell tolerance and ameliorate experimental autoimmune encephalomyelitis. Nat Biotechnol 2012; 30: 1217-24.
66. Shevach EM. Biological functions of regulatory T cells. Adv Immunol 2011; 112: 137-76.
67. Ohkura N, Kitagawa Y, Sakaguchi S. Development and maintenance of regulatory T cells. Immunity 2013; 38: 414-23.
68. Bluestone JA. Regulatory T-cell therapy: is it ready for the clinic? Nat Rev Immunol 2005; 5: 343-9.
69. James EA, van Haren SD, Ettinger RA et al. T-cell responses in two unrelated hemophilia A inhibitor subjects include an epitope at the factor VIII R593C missense site. J Thromb Haemost 2011; 9: 689-99.
70. Ettinger RA, James EA, Kwok WW, Thompson AR, Pratt KP. HLA-DR-restricted T-cell responses to factor VIII epitopes in a mild haemophilia A family with missense substitution A2201P. Haemophilia 2010; 16: 44-55.