Adeno-associated viral vectors for the treatment of hemophilia

Human Molecular Genetics

Volumn 25, Issue R1, 2016, Pages R36-R41

  High, Katherine A ^a   Anguela, Xavier M ^a  

^a Ophthalmology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 9;

ARTICLE; CD8+ T LYMPHOCYTE; GENE THERAPY; GENE TRANSFER; HEMOPHILIA; HEMOPHILIA A; HEMOPHILIA B; HUMAN; IMMUNE RESPONSE; NONHUMAN; PHARMACODYNAMICS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); SYSTEMATIC REVIEW; DEPENDOPARVOVIRUS; GENE VECTOR; GENETICS;

DEPENDOVIRUS; GENETIC THERAPY; GENETIC VECTORS; HEMOPHILIA A; HEMOPHILIA B; HUMANS;

EID: 85011728948     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv475     Document Type: Article

References (53)

1. Soucie, J.M., Nuss, R., Evatt, B., Abdelhak, A., Cowan, L., Hill, H., Kolakoski, M. and Wilber, N. (2000) Mortality among males with hemophilia: relations with source of medical care. The Hemophilia Surveillance System Project Investigators. Blood, 96, 437–442.
2. Aggeler, P.M., White, S.G., Glendening, M.B., Page, E.W., Leake, T.B. and Bates, G. (1952) Plasma thromboplastin component (PTC) deficiency; a new disease resembling hemophilia. Proc. Soc. Exp. Biol. Med., 79, 692–694.
3. Biggs, R., Douglas, A.S., Macfarlane, R.G., Dacie, J.V., Pitney, W.R. and Merskey, C. (1952) Christmas disease: a condition previously mistaken for haemophilia. Br. Med. J., 2, 1378–1382.
4. Soucie, J.M., Evatt, B. and Jackson, D. (1998) Occurrence of hemophilia in the United States. The Hemophilia Surveillance System Project Investigators. Am. J. Hematol., 59, 288–294.
5. Gitschier, J., Wood, W.I., Goralka, T.M., Wion, K.L., Chen, E.Y., Eaton, D.H., Vehar, G.A., Capon, D.J. and Lawn, R.M. (1984) Characterization of the human factor VIII gene. Nature, 312, 326–330.
6. Choo, K.H., Gould, K.G., Rees, D.J. and Brownlee, G.G. (1982) Molecular cloning of the gene for human anti-haemophilic factor IX. Nature, 299, 178–180.
7. Sabatino, D.E., Nichols, T.C., Merricks, E., Bellinger, D.A., Herzog, R.W. and Monahan, P.E. (2012) Animal Models of Hemophilia. In Progress in Molecular Biology and Translational Science, Elsevier, 105, 151–209.
8. Powell, J.S., Ragni, M.V., White, G.C., Lusher, J.M., Hillman-Wiseman, C., Moon, T.E., Cole, V., Ramanathan-Girish, S., Roehl, H., Sajjadi, N. et al. (2003) Phase 1 trial of FVIII gene transfer for severe hemophilia A using a retroviral construct administered by peripheral intravenous infusion. Blood, 102, 2038–2045.
9. Roth, D.A., Tawa, N.E., O’Brien, J.M., Treco, D.A. and Selden, R.F., Factor VIII Transkaryotic Therapy Study Group (2001) Nonviral transfer of the gene encoding coagulation factor VIII in patients with severe hemophilia A. N. Engl. J. Med., 344, 1735–1742.
10. Manno, C.S., Arruda, V.R., Pierce, G.F., Glader, B., Ragni, M., Rasko, J., Ozelo, M.C., Hoots, K., Blatt, P., Konkle, B. et al. (2006) Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med., 12, 342–347.
11. Hermonat, P.L. and Muzyczka, N. (1984) Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells. Proc. Natl Acad. Sci. USA, 81, 6466–6470.
12. Lisowski, L., Tay, S.S. and Alexander, I.E. (2015) ScienceDirect adeno-associated virus serotypes for gene therapeutics. Curr. Opin. Pharmacol., 24, 59–67.
13. Wang, L., Wang, H., Bell, P., McMenamin, D. and Wilson, J.M. (2012) Hepatic gene transfer in neonatal mice by adeno-associated virus serotype 8 vector. Hum. Gene. Ther., 23, 533–539.
14. Wu, Z., Yang, H. and Colosi, P. (2009) Effect of genome size on AAV vector packaging. Mol. Ther., 18, 80–86.
15. Herzog, R.W., Yang, E.Y., Couto, L.B., Hagstrom, J.N., Elwell, D., Fields, P.A., Burton, M., Bellinger, D.A., Read, M.S., Brinkhous, K.M. et al. (1999) Long-term correction of canine hemophilia B by gene transfer of blood coagulation factor IX mediated by adeno-associated viral vector. Nat. Med., 5, 56–63.
16. Manno, C.S., Chew, A.J., Hutchison, S., Larson, P.J., Herzog, R.W., Arruda, V.R., Tai, S.J., Ragni, M.V., Thompson, A., Ozelo, M. et al. (2003) AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood, 101, 2963–2972.
17. Kay, M.A., Manno, C.S., Ragni, M.V., Larson, P.J., Couto, L.B., McClelland, A., Glader, B., Chew, A.J., Tai, S.J., Herzog, R.W. et al. (2000) Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat. Genet., 24, 257–261.
18. Buchlis, G., Podsakoff, G.M., Radu, A., Hawk, S.M., Flake, A.W., Mingozzi, F. and High, K.A. (2012) Factor IX expression in skeletal muscle of a severe hemophilia B patient 10 years after AAV-mediated gene transfer. Blood, 119, 3038–3041.
19. Mingozzi, F., Maus, M.V., Hui, D.J., Sabatino, D.E., Murphy, S.L., Rasko, J.E.J., Ragni, M.V., Manno, C.S., Sommer, J., Jiang, H. et al. (2007) CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat. Med., 13, 419–422.
20. Vandenberghe, L.H., Wang, L., Somanathan, S., Zhi, Y., Figueredo, J., Calcedo, R., Sanmiguel, J., Desai, R.A., Chen, C.S., Johnston, J. et al. (2006) Heparin binding directs activation of T cells against adeno-associated virus serotype 2 capsid. Nat. Med., 12, 967–971.
21. Li, C., Goudy, K., Hirsch, M., Asokan, A., Fan, Y., Alexander, J., Sun, J., Monahan, P., Seiber, D., Sidney, J. et al. (2009) Cellular immune response to cryptic epitopes during therapeutic gene transfer. Proc. Natl Acad. Sci. USA, 106, 10770–10774.
22. Martino, A.T., Basner-Tschakarjan, E., Markusic, D.M., Finn, J.D., Hinderer, C., Zhou, S., Ostrov, D.A., Srivastava, A., Ertl, H.C.J., Terhorst, C. et al. (2013) Engineered AAV vector minimizes in vivo targeting of transduced hepatocytes by capsid-specific CD8+ T cells. Blood, 121, 2224–2233.
23. Lisowski, L., Dane, A.P., Chu, K., Zhang, Y., Cunningham, S.C., Wilson, E.M., Nygaard, S., Grompe, M., Alexander, I.E. and Kay, M.A. (2013) Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature, doi:10.1038/nature12875.
24. Fagone, P., Wright, J.F., Nathwani, A.C., Nienhuis, A.W., Davidoff, A.M. and Gray, J.T. (2011) Systemic errors in quantitative polymerase chain reaction titration of self-complementary adeno-associated viral vectors and improved alternative methods. Hum. Gene. Ther., doi:10.1089/hum.2011.104.
25. Nathwani, A.C., Tuddenham, E.G.D., Rangarajan, S., Rosales, C., McIntosh, J., Linch, D.C., Chowdary, P., Riddell, A., Pie, A.J., Harrington, C. et al. (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med., 365, 2357–2365.
26. Nathwani, A.C., Reiss, U.M., Tuddenham, E.G.D., Rosales, C., Chowdary, P., McIntosh, J., Peruta, M.D., Lheriteau, E., Patel, N., Raj, D. et al. (2014) Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N. Engl. J. Med., 371, 1994–2004.
27. Simioni, P., Tormene, D., Tognin, G., Gavasso, S., Bulato, C., Iacobelli, N.P., Finn, J.D., Spiezia, L., Radu, C. and Arruda, V.R. (2009) X-linked thrombophilia with a mutant factor IX (factor IX Padua). N. Engl. J. Med., 361, 1671–1675.
28. Jiang, H., Couto, L.B., Patarroyo-White, S., Liu, T., Nagy, D., Vargas, J.A., Zhou, S., Scallan, C.D., Sommer, J., Vijay, S. et al. (2006) Effects of transient immunosuppression on adenoassociated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood, 108, 3321–3328.
29. Wang, L., Bell, P., Somanathan, S., Wang, Q., He, Z., Yu, H., McMenamin, D., Goode, T., Calcedo, R. and Wilson, J.M. (2015) Comparative study of liver gene transfer with AAV vectors based on natural and engineered AAV capsids. Mol. Ther., doi:10.1038/mt.2015.179.
30. Mingozzi, F., Anguela, X.M., Pavani, G., Chen, Y., Davidson, R.J., Hui, D.J., Hinderer, C.J., Faella, A., Howard, C., Tai, A. et al. (2012) A novel strategy to circumvent pre-existing humoral immunity to AAV. ASH Annu. Meet. Abstr., 120, 2050.
31. Mingozzi, F., Chen, Y., Edmonson, S.C., Zhou, S., Thurlings, R.M., Tak, P.P., High, K.A. and Vervoordeldonk, M.J. (2012) Prevalence and pharmacological modulation of humoral immunity to AAV vectors in gene transfer to synovial tissue. Gene. Ther.,20, 417–424.
32. Monteilhet, V., Saheb, S., Boutin, S., Leborgne, C., Veron, P., Montus, M.F., Moullier, P., Benveniste, O. and Masurier, C. (2009) A 10 patient case report on the impact of plasmapheresis upon neutralizing factors against adeno-associated virus (AAV) types 1, 2, 6, and 8. Mol. Ther., 19, 2084–2091.
33. Lee, G.K., Maheshri, N., Kaspar, B. and Schaffer, D.V. (2005) PEG conjugation moderately protects adeno-associated viral vectors against antibody neutralization. Biotechnol. Bioeng., 92, 24–34.
34. Huttner, N.A., Girod, A., Perabo, L., Edbauer, D., Kleinschmidt, J.A., Buning, H. and Hallek, M. (2003) Genetic modifications of the adeno-associated virus type 2 capsid reduce the affinity and the neutralizing effects of human serum antibodies. Gene. Ther., 10, 2139–2147.
35. Mimuro, J., Mizukami, H., Hishikawa, S., Ikemoto, T., Ishiwata, A., Sakata, A., Ohmori, T., Madoiwa, S., Ono, F., Ozawa, K. et al. (2012) Minimizing the inhibitory effect of neutralizing antibody for efficient gene expression in the liver with adeno-associated virus 8 vectors. Mol. Ther., 21, 318–323.
36. György, B., Fitzpatrick, Z., Crommentuijn, M.H.W., Mu, D. and Maguire, C.A. (2014) Biomaterials. Biomaterials, 35, 7598–7609.
37. Kaeppel, C., Beattie, S.G., Fronza, R., van Logtenstein, R., Salmon, F., Schmidt, S., Wolf, S., Nowrouzi, A., Glimm, H., von Kalle, C. et al. (2013) Brief communications. Nat. Med., 19, 889–891.
38. Donsante, A., Miller, D.G., Li, Y., Vogler, C., Brunt, E.M., Russell, D.W. and Sands, M.S. (2007) AAV vector integration sites in mouse hepatocellular carcinoma. Science, 317, 477.
39. Wang, P.-R., Xu, M., Toffanin, S., Li, Y., Llovet, J.M. and Russell, D.W. (2012) Induction of hepatocellular carcinoma by in vivo gene targeting. Proc. Natl Acad. Sci. USA, 109, 11264–11269.
40. Nault, J.-C., Datta, S., Imbeaud, S., Franconi, A., Mallet, M., Couchy, G., Letouzé, E., Pilati, C., Verret, B., Blanc, J.-F. et al. (2015) Recurrent AAV2-related insertional mutagenesis in human hepatocellular carcinomas. Nat. Genet., doi:10.1038/ ng.3389.
41. Chandler, R.J., LaFave, M.C., Varshney, G.K., Trivedi, N.S., Carrillo-Carrasco, N., Senac, J.S., Wu, W., Hoffmann, V., Elkahloun, A.G., Burgess, S.M. et al. (2015) Vector design influences hepatic genotoxicity after adeno-associated virus gene therapy. J. Clin. Invest., doi:10.1172/JCI79213DS1.
42. Wellman, J.A., Mingozzi, F., Ozelo, M.C., Arruda, V., Podsakoff, G., Chen, Y., Konkle, B.A., Blatt, P.M., Hoots, K., Raffini, L.J. et al. (2012) Results from long-term follow-up of severe hemophilia B subjects previously enrolled in a clinical study of AAV2-FIX gene transfer to the liver. Mol. Ther., 20(Suppl. 1), 28–29.
43. Lynch, C.M., Israel, D.I., Kaufman, R.J. and Miller, A.D. (1993) Sequences in the coding region of clotting factor VIII act as dominant inhibitors of RNA accumulation and protein production. Hum. Gene. Ther.,4, 259–272.
44. Ward, N.J., Buckley, S.M.K., Waddington, S.N., Vanden Driessche, T., Chuah, M.K.L., Nathwani, A.C., Mcintosh, J., Tuddenham, E.G.D., Kinnon, C. and Thrasher, A.J. et al. (2011) Codon optimization of human factor VIII cDNAs leads to high-level expression. Blood, 117, 798–807.
45. Mcintosh, J., Lenting, P.J., Rosales, C., Lee, D., Rabbanian, S., Raj, D., Patel, N., Tuddenham, E.G.D., Christophe, O.D., McVey, J.H. et al. (2013) Therapeutic levels of FVIII following a single peripheral vein administration of rAAV vector encoding a novel human factor VIII variant. Blood, 121, 3335–3344.
46. Wight, J. and Paisley, S. (2003) The epidemiology of inhibitors in haemophilia A: a systematic review. Haemophilia, 9, 418–435.
47. Rocino, A., Cortesi, P.A., Scalone, L., Mantovani, L.G., Crea, R. and Gringeri, A., European Haemophilia Therapy Strategy Board (EHTSB) (2015) Immune tolerance induction in patients with haemophilia a and inhibitors: effectiveness and cost analysis in an European Cohort (The ITER Study). Haemophilia, doi:10.1111/hae.12780.
48. Finn, J.D., Ozelo, M.C., Sabatino, D.E., Franck, H.W.G., Merricks, E.P., Crudele, J.M., Zhou, S., Kazazian, H.H., Lillicrap, D., Nichols, T.C. et al. (2010) Eradication of neutralizing antibodies to factor VIII in canine hemophilia A after liver gene therapy. Blood, 116, 5842–5848.
49. Stocker, J.T., Dehner, L.P. and Husain, A.N. (2012) Stocker and Dehner’s Pediatric Pathology Lippincott Williams & Wilkins.
50. Cantore, A., Ranzani, M., Bartholomae, C.C., Volpin, M., Valle, P.D., Sanvito, F., Sergi, L.S., Gallina, P., Benedicenti, F., Bellinger, D. et al. (2015) Liver-directed lentiviral gene therapy in a dog model of hemophilia B. Sci. Transl. Med., 7, 277ra28.
51. Li, H., Haurigot, V., Doyon, Y., Li, T., Wong, S.Y., Bhagwat, A.S., Malani, N., Anguela, X.M., Sharma, R., Ivanciu, L. et al. (2011) In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature, 475, 217–U128.
52. Sharma, R., Anguela, X.M., Doyon, Y., Wechsler, T., DeKelver, R.C., Sproul, S., Paschon, D.E., Miller, J.C., Davidson, R.J., Shivak, D. et al. (2015) In vivo genome editing of the albumin locus as a platform for protein replacement therapy. Blood, 126, 1777–1784.
53. Urnov, F.D. (2014) Taking it to the clinic: genome editing for blood disorders. Blood, 124, SCI12–SCI12.