Role of antigen-specific regulatory CD4+ CD25+ T cells in tolerance induction after neonatal IP administration of AAV-hF.IX

Gene Therapy

Volumn 20, Issue 10, 2013, Pages 987-996

  Shi, Y ^a   Falahati, R ^a   Zhang, J ^a   Flebbe Rehwaldt, L ^a   Gaensler, K M L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AAV; hemophilia B; immuno tolerance; neonatal; Treg

Indexed keywords

BLOOD CLOTTING FACTOR 9; MESSENGER RNA; PARVOVIRUS VECTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; BLOOD CLOTTING DISORDER; C57BL 6 MOUSE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG DOSE ESCALATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE TRANSFER; HEMOPHILIA B; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; MOUSE; NEWBORN; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL; STRAIN DIFFERENCE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

MIRIDAE; MUS;

ANIMALS; ANIMALS, NEWBORN; CD4-POSITIVE T-LYMPHOCYTES; DEPENDOVIRUS; FACTOR IX; FEMALE; GENETIC THERAPY; HEMOPHILIA B; HUMANS; IMMUNE TOLERANCE; IMMUNOTHERAPY, ADOPTIVE; INJECTIONS, INTRAPERITONEAL; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, REGULATORY; TRANSGENES;

EID: 84885599195     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2013.22     Document Type: Article

References (60)

1. Mannucci PM, Tuddenbam EG. The hemophilias: progress and problems. Semin Hematol 1999; 36: 104-117.
2. High KA. Gene therapy for haemophilia: a long and winding road. J Thromb Haemost 2011; 9(Suppl 1): 2-11.
3. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 2011; 12: 341-355.
4. McCarty DM, Young Jr SM, Samulski RJ. Integration of Adeno-Associated Virus (AAV) and Recombinant AAV Vectors. Annu Rev Genet 2004; 38: 819-845.
5. Stilwell JL, Samulski RJ. Adeno-associated virus vectors for therapeutic gene transfer. Biotechniques 2003; 34: 148-150 (152, 154 passim).
6. Herzog RW, Hagstrom JN. Gene therapy for hereditary hematological disorders. Am J Pharmacogenomics 2001; 1: 137-144.
7. Herzog RW, High KA. Adeno-associated virus-mediated gene transfer of factor IX for treatment of hemophilia B by gene therapy. Thromb Haemost 1999; 82: 540-546.
8. Herzog RW, Yang EY, Couto LB, Hagstrom JN, Elwell D, Fields PA et al. Long-term correction of canine hemophilia B by gene transfer of blood coagulation factor IX mediated by adeno-associated viral vector. Nat Med 1999; 5: 56-63.
9. Kay MA, Manno CS, Ragni MV, Larson PJ, Couto LB, McClelland A et al. Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat Genet 2000; 24: 257-261.
10. Mingozzi F, Liu YL, Dobrzynski E, Kaufhold A, Liu JH, Wang Y et al. Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest 2003; 111: 1347-1356.
11. Grimm D, Zhou S, Nakai H, Thomas CE, Storm TA, Fuess S et al. Preclinical in vivo evaluation of pseudotyped adeno-associated virus vectors for liver gene therapy. Blood 2003; 102: 2412-2419.
12. Arruda VR, Schuettrumpf J, Herzog RW, Nichols TC, Robinson N, Lotfi Y et al. Safety and efficacy of factor IX gene transfer to skeletal muscle in murine and canine hemophilia B models by adeno-associated viral vector serotype 1. Blood 2004; 103: 85-92.
13. Liu YL, Mingozzi F, Rodriguez-Colon SM, Joseph S, Dobrzynski E, Suzuki T et al. Therapeutic levels of factor IX expression using a muscle-specific promoter and adeno-associated virus serotype 1 vector. Hum Gene Ther 2004; 15: 783-792.
14. Louboutin JP, Wang L, Wilson JM. Gene transfer into skeletal muscle using novel AAV serotypes. J Gene Med 2005; 7: 442-451.
15. Lipshutz G, Contag C, Andriole S, Gaensler KML. In Utero AAV-mediated gene transfer to the peritoneum: comparison of gene expression after intraperitoneal delivery of EF1-alpha or CMV-directed luciferase cassettes in fetal mice. Mol Ther 2001; 3: S294.
16. Darrasse-Jeze G, Marodon G, Salomon BL, Catala M, Klatzmann D. Ontogeny of CD4CD25 regulatory/suppressor T cells in human fetuses. Blood 2005; 105: 4715-4721.
17. Manno CS, Pierce GF, Arruda VR, Glader B, Ragni M, Rasko JJ et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 2006; 12: 342-347.
18. Nayak S, Herzog RW. Progress and prospects: immune responses to viral vectors. Gene Therapy 2010; 17: 295-304.
19. Tsui LV, Kelly M, Zayek N, Rojas V, Ho K, Ge Y et al. Production of human clotting Factor IX without toxicity in mice after vascular delivery of a lentiviral vector. Nat Biotechnol 2002; 20: 53-57.
20. Chang AH, Stephan MT, Lisowski L, Sadelain M. Erythroid-specific human factor IX delivery from in vivo selected hematopoietic stem cells following nonmyeloablative conditioning in hemophilia B mice. Mol Ther 2008; 16: 1745-1752.
21. Matrai J, Cantore A, Bartholomae CC, Annoni A, Wang W, Acosta-Sanchez A et al. Hepatocyte-targeted expression by integrase-defective lentiviral vectors induces antigen-specific tolerance in mice with low genotoxic risk. Hepatology 2011; 53: 1696-1707.
22. Agudo J, Ruzo A, Kitur K, Sachidanandam R, Blander JM, Brown BD. A TLR and non-TLR mediated innate response to lentiviruses restricts hepatocyte entry and can be ameliorated by pharmacological blockade. Mol Ther 2012; 20: 2257-2267.
23. Lipshutz GS, Titre D, Brindle M, Bisconte AR, Contag CH, Gaensler KM. Comparison of gene expression after intraperitoneal delivery of AAV2 or AAV5 in utero. Mol Ther 2003; 8: 90-98.
24. Sabatino DE, Mackenzie TC, Peranteau W, Edmonson S, Campagnoli C, Liu YL et al. Persistent expression of hF. IX After tolerance induction by in utero or neonatal administration of AAV-1-F. IX in hemophilia B mice. Mol Ther 2007; 15: 1677-1685.
25. Schneider H, Muhle C, Douar AM, Waddington S, Jiang QJ, von der Mark K et al. Sustained delivery of therapeutic concentrations of human clotting factor IX-a comparison of adenoviral and AAV vectors administered in utero. J Gene Med 2002; 4: 46-53.
26. Waddington SN, Nivsarkar MS, Mistry AR, Buckley SM, Kemball-Cook G, Mosley KL et al. Permanent phenotypic correction of Hemophilia B in immunocompetent mice by prenatal gene therapy. Blood 2004; 104: 2714-2721.
27. Lipshutz GS, Flebbe-Rehwaldt L, Gaensler KM. Adenovirus-mediated gene transfer to the peritoneum and hepatic parenchyma of fetal mice in utero. Surgery 1999; 126: 171-177.
28. Lipshutz GS, Flebbe-Rehwaldt L, Gaensler KM. Reexpression following readministration of an adenoviral vector in adult mice after initial in utero adenoviral administration. Mol Ther 2000; 2: 374-380.
29. Wang L, Zoppe M, Hackeng TM, Griffin JH, Lee KF, Verma IM. A factor IX-deficient mouse model for hemophilia B gene therapy. Proc Natl Acad Sci USA 1997; 94: 11563-11566.
30. Xu L, Gao C, Sands MS, Cai SR, Nichols TC, Bellinger DA et al. Neonatal or hepatocyte growth factor-potentiated adult gene therapy with a retroviral vector results in therapeutic levels of canine factor IX for hemophilia B. Blood 2003; 101: 3924-3932.
31. Zhang J, Xu L, Haskins ME, Parker Ponder K. Neonatal gene transfer with a retroviral vector results in tolerance to human factor IX in mice and dogs. Blood 2004; 103: 143-151.
32. Ogura T, Mizukami H, Mimuro J, Madoiwa S, Okada T, Matsushita T et al. Utility of intraperitoneal administration as a route of AAV serotype 5 vector-mediated neonatal gene transfer. J Gene Med 2006; 8: 990-997.
33. Wang L, Calcedo R, Nichols TC, Bellinger DA, Dillow A, Verma IM et al. Sustained correction of disease in naive and AAV2-pretreated hemophilia B dogs: AAV2/8-mediated, liver-directed gene therapy. Blood 2005; 105: 3079-3086.
34. Hartung SD, Frandsen JL, Pan D, Koniar BL, Graupman P, Gunther R et al. Correction of metabolic, craniofacial, and neurologic abnormalities in MPS I mice treated at birth with adeno-associated virus vector transducing the human alpha-L-iduronidase gene. Mol Ther 2004; 9: 866-875.
35. Ponder KP. Immunology of neonatal gene transfer. Curr Gene Ther 2007; 7: 403-410.
36. Cao O, Dobrzynski E, Wang L, Nayak S, Mingle B, Terhorst C et al. Induction and role of regulatory CD4CD25 T cells in tolerance to the transgene product following hepatic in vivo gene transfer. Blood 2007; 110: 1132-1140.
37. Fisson S, Darrasse-Jeze G, Litvinova E, Septier F, Klatzmann D, Liblau R et al. Continuous activation of autoreactive CD4 CD25 regulatory T cells in the steady state. J Exp Med 2003; 198: 737-746.
38. Renda MC, Fecarotta E, Dieli F, Markling L, Westgren M, Damiani G et al. Evidence of alloreactive T lymphocytes in fetal liver: implications for fetal hematopoietic stem cell transplantation. Bone Marrow Transplant 2000; 25: 135-141.
39. Asano M, Toda M, Sakaguchi N, Sakaguchi S. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 1996; 184: 387-396.
40. Kung SH, Hagstrom JN, Cass D, Tai SJ, Lin HF, Stafford DW et al. Human factor IX corrects the bleeding diathesis of mice with hemophilia B. Blood 1998; 91: 784-790.
41. Fields PA, Armstrong E, Hagstrom JN, Arruda VR, Murphy ML, Farrell JP et al. Intravenous administration of an E1/E3-deleted adenoviral vector induces tolerance to factor IX in C57BL/6 mice. Gene Therapy 2001; 8: 354-361.
42. Kelly ME, Zhuo J, Bharadwaj AS, Chao H. Induction of immune tolerance to FIX following muscular AAV gene transfer is AAV-dose/FIX-level dependent. Mol Ther 2009; 17: 857-863.
43. Cao O, Furlan-Freguia C, Arruda VR, Herzog RW. Emerging role of regulatory T cells in gene transfer. Curr Gene Ther 2007; 7: 381-390.
44. Lipshutz GS, Gruber CA, Cao Y, Hardy J, Contag CH, Gaensler KM. In utero delivery of adeno-associated viral vectors: intraperitoneal gene transfer produces long-term expression. Mol Ther 2001; 3: 284-292.
45. Cao Z, Zheng P, Lin Y. A comparative study of hFIX expression mediated by rAAV8 and rAAV1 administrated intramuscularly. Cytotherapy 2007; 9: 593-599.
46. Kelly M, Bharadwaj AS, Tacke F, Chao HJ. Regulatory T cells and immune tolerance to coagulation factor IX in the context of intramuscular AAV1 gene transfer. Mol Ther 2010; 18: 361-369.
47. Garza KM, Agersborg SS, Baker E, Tung KS. Persistence of physiological self antigen is required for the regulation of self tolerance. Journal of Immunology 2000; 164: 3982-3989.
48. Hacke K, Falahati R, Flebbe-Rehwaldt L, Kasahara N, Gaensler KM. Suppression of HLA expression by lentivirus-mediated gene transfer of siRNA cassettes and in vivo chemoselection to enhance hematopoietic stem cell transplantation. Immunol Res 2009; 44: 112-126.
49. David AL, McIntosh J, Peebles DM, Cook T, Waddington S, Weisz B et al. Recombinant adeno-associated virus-mediated in utero gene transfer gives therapeutic transgene expression in the sheep. Hum Gene Ther 2011; 22: 419-426.
50. Haurigot V, Mingozzi F, Buchlis G, Hui DJ, Chen Y, Basner-Tschakarjan E et al. Safety of AAV factor IX peripheral transvenular gene delivery to muscle in hemophilia B dogs. Mol Ther 2010; 18: 1318-1329.
51. Arruda VR, Stedman HH, Haurigot V, Buchlis G, Baila S, Favaro P et al. Peripheral transvenular delivery of adeno-associated viral vectors to skeletal muscle as a novel therapy for hemophilia B. Blood 2010; 115: 4678-4688.
52. Finn JD, Hui D, Downey HD, Dunn D, Pien GC, Mingozzi F et al. Proteasome inhibitors decrease AAV2 capsid derived peptide epitope presentation on MHC class I following transduction. Mol Ther 2010; 18: 135-142.
53. Monahan PE, Lothrop CD, Sun J, Hirsch ML, Kafri T, Kantor B et al. Proteasome inhibitors enhance gene delivery by AAV virus vectors expressing large genomes in hemophilia mouse and dog models: a strategy for broad clinical application. Mol Ther 18: 1907-1916.
54. Mingozzi F, Hasbrouck NC, Basner-Tschakarjan E, Edmonson SA, Hui DJ, Sabatino DE et al. Modulation of tolerance to the transgene product in a nonhuman primate model of AAV-mediated gene transfer to liver. Blood 2007; 110: 2334-2341.
55. Sack BK, Merchant S, Markusic DM, Nathwani AC, Davidoff AM, Byrne BJ et al. Transient B cell depletion or improved transgene expression by codon optimization promote tolerance to factor VIII in gene therapy. PLoS One 2012; 7: e37671.
56. Goudy KS, Annoni A, Naldini L, Roncarolo MG. Manipulating Immune Tolerance with Micro-RNA Regulated Gene Therapy. Front Microbiol 2011; 2: 221.
57. Shevach EM. Regulatory T cells in autoimmmunity*. Annu Rev Immunol 2000; 18: 423-449.
58. Chatenoud L, Salomon B, Bluestone JA. Suppressor T cells-they're back and critical for regulation of autoimmunity! Immunol Rev 2001; 182: 149-163.
59. Nathwani AC, Rosales C, McIntosh J, Rastegarlari G, Nathwani D, Raj D 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: 876-885.
60. Cohn EF, Zhuo J, Kelly ME, Chao HJ. Efficient induction of immune tolerance to coagulation factor IX following direct intramuscular gene transfer. J Thromb Haemost 2007; 5: 1227-1236.