Successful Repeated Hepatic Gene Delivery in Mice and Non-human Primates Achieved by Sequential Administration of AAV5ch and AAV1

Molecular Therapy

Volumn 25, Issue 8, 2017, Pages 1831-1842

  Majowicz, Anna ^a   Salas, David ^b   Zabaleta, Nerea ^b   Rodríguez Garcia, Estefania ^b   González Aseguinolaza, Gloria ^b   Petry, Harald ^a   Ferreira, Valerie ^a  

^a UNIQURE   (Netherlands)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

AAV; gene therapy; re administration of gene therapy

Indexed keywords

ADENOVIRUS VECTOR; ALKALINE PHOSPHATASE; DNA; NEUTRALIZING ANTIBODY; RECOMBINANT BLOOD CLOTTING FACTOR 9; BIOLOGICAL MARKER; VIRUS ANTIBODY;

ADENO ASSOCIATED VIRUS 1; ADENO ASSOCIATED VIRUS 5; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DNA DETERMINATION; FEMALE; HUMORAL IMMUNITY; LIVER; MACACA FASCICULARIS; MALE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; CLASSIFICATION; DEPENDOPARVOVIRUS; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; IMMUNOLOGY; LIVER CELL; METABOLISM; PRIMATE; TISSUE DISTRIBUTION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BIOMARKERS; CROSS REACTIONS; DEPENDOVIRUS; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HEPATOCYTES; HUMANS; IMMUNITY, HUMORAL; LIVER; MICE; PRIMATES; TISSUE DISTRIBUTION; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 85020215249     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1016/j.ymthe.2017.05.003     Document Type: Article

References (39)

1. Gaudet, D., Méthot, J., Déry, S., Brisson, D., Essiembre, C., Tremblay, G., Tremblay, K., de Wal, J., Twisk, J., van den Bulk, N., et al. Efficacy and long-term safety of alipogene tiparvovec (AAV1-LPLS447X) gene therapy for lipoprotein lipase deficiency: an open-label trial. Gene Ther. 20 (2013), 361–369.
2. Grimm, D., Zhou, S., Nakai, H., Thomas, C.E., Storm, T.A., Fuess, S., Matsushita, T., Allen, J., Surosky, R., Lochrie, M., et al. Preclinical in vivo evaluation of pseudotyped adeno-associated virus vectors for liver gene therapy. Blood 102 (2003), 2412–2419.
3. Nathwani, A.C., Tuddenham, E.G., Rangarajan, S., Rosales, C., McIntosh, J., Linch, D.C., Chowdary, P., Riddell, A., Pie, A.J., Harrington, C., et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med. 365 (2011), 2357–2365.
4. Halbert, C.L., Rutledge, E.A., Allen, J.M., Russell, D.W., Miller, A.D., Repeat transduction in the mouse lung by using adeno-associated virus vectors with different serotypes. J. Virol. 74 (2000), 1524–1532.
5. Halbert, C.L., Standaert, T.A., Aitken, M.L., Alexander, I.E., Russell, D.W., Miller, A.D., Transduction by adeno-associated virus vectors in the rabbit airway: efficiency, persistence, and readministration. J. Virol. 71 (1997), 5932–5941.
6. Rivière, C., Danos, O., Douar, A.M., Long-term expression and repeated administration of AAV type 1, 2 and 5 vectors in skeletal muscle of immunocompetent adult mice. Gene Ther. 13 (2006), 1300–1308.
7. Xiao, W., Chirmule, N., Berta, S.C., McCullough, B., Gao, G., Wilson, J.M., Gene therapy vectors based on adeno-associated virus type 1. J. Virol. 73 (1999), 3994–4003.
8. Jacobs, F., Gordts, S.C., Muthuramu, I., De Geest, B., The liver as a target organ for gene therapy: state of the art, challenges, and future perspectives. Pharmaceuticals (Basel) 5 (2012), 1372–1392.
9. Kok, C.Y., Cunningham, S.C., Carpenter, K.H., Dane, A.P., Siew, S.M., Logan, G.J., Kuchel, P.W., Alexander, I.E., Adeno-associated virus-mediated rescue of neonatal lethality in argininosuccinate synthetase-deficient mice. Mol. Ther. 21 (2013), 1823–1831.
10. Boutin, S., Monteilhet, V., Veron, P., Leborgne, C., Benveniste, O., Montus, M.F., Masurier, C., Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum. Gene Ther. 21 (2010), 704–712.
11. Gao, G.P., Alvira, M.R., Wang, L., Calcedo, R., Johnston, J., Wilson, J.M., Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. USA 99 (2002), 11854–11859.
12. McIntosh, J.H., Cochrane, M., Cobbold, S., Waldmann, H., Nathwani, S.A., Davidoff, A.M., Nathwani, A.C., Successful attenuation of humoral immunity to viral capsid and transgenic protein following AAV-mediated gene transfer with a non-depleting CD4 antibody and cyclosporine. Gene Ther. 19 (2012), 78–85.
13. Mingozzi, F., Chen, Y., Edmonson, S.C., Zhou, S., Thurlings, R.M., Tak, P.P., High, K.A., Vervoordeldonk, M.J., Prevalence and pharmacological modulation of humoral immunity to AAV vectors in gene transfer to synovial tissue. Gene Ther. 20 (2013), 417–424.
14. Mingozzi, F., Chen, Y., Murphy, S.L., Edmonson, S.C., Tai, A., Price, S.D., Metzger, M.E., Zhou, S., Wright, J.F., Donahue, R.E., et al. Pharmacological modulation of humoral immunity in a nonhuman primate model of AAV gene transfer for hemophilia B. Mol. Ther. 20 (2012), 1410–1416.
15. Unzu, C., Hervás-Stubbs, S., Sampedro, A., Mauleón, I., Mancheño, U., Alfaro, C., de Salamanca, R.E., Benito, A., Beattie, S.G., Petry, H., et al. Transient and intensive pharmacological immunosuppression fails to improve AAV-based liver gene transfer in non-human primates. J. Transl. Med., 10, 2012, 122.
16. Urabe, M., Nakakura, T., Xin, K.Q., Obara, Y., Mizukami, H., Kume, A., Kotin, R.M., Ozawa, K., Scalable generation of high-titer recombinant adeno-associated virus type 5 in insect cells. J. Virol. 80 (2006), 1874–1885.
17. D'Avola, D., López-Franco, E., Sangro, B., Pañeda, A., Grossios, N., Gil-Farina, I., Benito, A., Twisk, J., Paz, M., Ruiz, J., et al. Phase I open label liver-directed gene therapy clinical trial for acute intermittent porphyria. J. Hepatol. 65 (2016), 776–783.
18. Mendell, J.R., Sahenk, Z., Malik, V., Gomez, A.M., Flanigan, K.M., Lowes, L.P., Alfano, L.N., Berry, K., Meadows, E., Lewis, S., et al. A phase 1/2a follistatin gene therapy trial for becker muscular dystrophy. Mol. Ther. 23 (2015), 192–201.
19. Pañeda, A., Vanrell, L., Mauleon, I., Crettaz, J.S., Berraondo, P., Timmermans, E.J., Beattie, S.G., Twisk, J., van Deventer, S., Prieto, J., et al. Effect of adeno-associated virus serotype and genomic structure on liver transduction and biodistribution in mice of both genders. Hum. Gene Ther. 20 (2009), 908–917.
20. Tseng, Y.S., Gurda, B.L., Chipman, P., McKenna, R., Afione, S., Chiorini, J.A., Muzyczka, N., Olson, N.H., Baker, T.S., Kleinschmidt, J., Agbandje-McKenna, M., Adeno-associated virus serotype 1 (AAV1)- and AAV5-antibody complex structures reveal evolutionary commonalities in parvovirus antigenic reactivity. J. Virol. 89 (2015), 1794–1808.
21. Harbison, C.E., Weichert, W.S., Gurda, B.L., Chiorini, J.A., Agbandje-McKenna, M., Parrish, C.R., Examining the cross-reactivity and neutralization mechanisms of a panel of mAbs against adeno-associated virus serotypes 1 and 5. J. Gen. Virol. 93 (2012), 347–355.
22. Nathwani, A.C., Gray, J.T., McIntosh, J., Ng, C.Y., Zhou, J., Spence, Y., Cochrane, M., Gray, E., Tuddenham, E.G., Davidoff, A.M., Safe and efficient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 109 (2007), 1414–1421.
23. 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. Effects of transient immunosuppression on adenoassociated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood 108 (2006), 3321–3328.
24. Kim, C.Y., Lee, H.S., Han, S.C., Heo, J.D., Kwon, M.S., Ha, C.S., Han, S.S., Hematological and serum biochemical values in cynomolgus monkeys anesthetized with ketamine hydrochloride. J. Med. Primatol. 34 (2005), 96–100.
25. Mingozzi, F., Hasbrouck, N.C., Basner-Tschakarjan, E., Edmonson, S.A., Hui, D.J., Sabatino, D.E., Zhou, S., Wright, J.F., Jiang, H., Pierce, G.F., et al. Modulation of tolerance to the transgene product in a nonhuman primate model of AAV-mediated gene transfer to liver. Blood 110 (2007), 2334–2341.
26. Wang, M., Crosby, A., Hastie, E., Samulski, J.J., McPhee, S., Joshua, G., Samulski, R.J., Li, C., Prediction of adeno-associated virus neutralizing antibody activity for clinical application. Gene Ther. 22 (2015), 984–992.
27. Pañeda, A., Lopez-Franco, E., Kaeppel, C., Unzu, C., Gil-Royo, A.G., D'Avola, D., Beattie, S.G., Olagüe, C., Ferrero, R., Sampedro, A., et al. Safety and liver transduction efficacy of rAAV5-cohPBGD in nonhuman primates: a potential therapy for acute intermittent porphyria. Hum. Gene Ther. 24 (2013), 1007–1017.
28. Park, F., Ohashi, K., Kay, M.A., The effect of age on hepatic gene transfer with self-inactivating lentiviral vectors in vivo. Mol. Ther. 8 (2003), 314–323.
29. Sack, B.K., Herzog, R.W., Evading the immune response upon in vivo gene therapy with viral vectors. Curr. Opin. Mol. Ther. 11 (2009), 493–503.
30. Davidoff, A.M., Gray, J.T., Ng, C.Y., Zhang, Y., Zhou, J., Spence, Y., Bakar, Y., Nathwani, A.C., Comparison of the ability of adeno-associated viral vectors pseudotyped with serotype 2, 5, and 8 capsid proteins to mediate efficient transduction of the liver in murine and nonhuman primate models. Mol. Ther. 11 (2005), 875–888.
31. Nathwani, A.C., Davidoff, A.M., Hanawa, H., Hu, Y., Hoffer, F.A., Nikanorov, A., Slaughter, C., Ng, C.Y., Zhou, J., Lozier, J.N., et al. Sustained high-level expression of human factor IX (hFIX) after liver-targeted delivery of recombinant adeno-associated virus encoding the hFIX gene in rhesus macaques. Blood 100 (2002), 1662–1669.
32. Nathwani, A.C., Gray, J.T., Ng, C.Y., Zhou, J., Spence, Y., Waddington, S.N., Tuddenham, E.G., Kemball-Cook, G., McIntosh, J., Boon-Spijker, M., et al. Self-complementary adeno-associated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood 107 (2006), 2653–2661.
33. Nathwani, A.C., Rosales, C., McIntosh, J., Rastegarlari, G., Nathwani, D., Raj, D., Nawathe, S., Waddington, S.N., Bronson, R., Jackson, S., 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. 19 (2011), 876–885.
34. Mendell, J.R., Campbell, K., Rodino-Klapac, L., Sahenk, Z., Shilling, C., Lewis, S., Bowles, D., Gray, S., Li, C., Galloway, G., et al. Dystrophin immunity in Duchenne's muscular dystrophy. N. Engl. J. Med. 363 (2010), 1429–1437.
35. Flotte, T.R., Trapnell, B.C., Humphries, M., Carey, B., Calcedo, R., Rouhani, F., Campbell-Thompson, M., Yachnis, A.T., Sandhaus, R.A., McElvaney, N.G., et al. Phase 2 clinical trial of a recombinant adeno-associated viral vector expressing α1-antitrypsin: interim results. Hum. Gene Ther. 22 (2011), 1239–1247.
36. Urabe, M., Ding, C., Kotin, R.M., Insect cells as a factory to produce adeno-associated virus type 2 vectors. Hum. Gene Ther. 13 (2002), 1935–1943.
37. Nelson, E.K., Piehler, B., Eckels, J., Rauch, A., Bellew, M., Hussey, P., Ramsay, S., Nathe, C., Lum, K., Krouse, K., et al. LabKey Server: an open source platform for scientific data integration, analysis and collaboration. BMC Bioinformatics, 12, 2011, 71.
38. Piehler, B., Nelson, E.K., Eckels, J., Ramsay, S., Lum, K., Wood, B., Greene, K.M., Gao, H., Seaman, M.S., Montefiori, D.C., Igra, M., LabKey Server NAb: a tool for analyzing, visualizing and sharing results from neutralizing antibody assays. BMC Immunol., 12, 2011, 33.
39. Hui, D.J., Edmonson, S.C., Podsakoff, G.M., Pien, G.C., Ivanciu, L., Camire, R.M., Ertl, H., Mingozzi, F., High, K.A., Basner-Tschakarjan, E., AAV capsid CD8+ T-cell epitopes are highly conserved across AAV serotypes. Mol. Ther. Methods Clin. Dev., 2, 2015, 15029.