Rescue of Pompe disease in mice by AAV-mediated liver delivery of secretable acid α-glucosidase

Science Translational Medicine

Volumn 9, Issue 418, 2017, Pages

  Puzzo, Francesco ^a,b   Colella, Pasqualina ^a   Biferi, Maria G ^c   Bali, Deeksha ^d   Paulk, Nicole K ^e   Vidal, Patrice ^a,c   Collaud, Fanny ^a   Simon Sola, Marcelo ^a,c   Charles, Severine ^a   Hardet, Romain ^c   Leborgne, Christian ^a   Meliani, Amine ^a,c   Cohen Tannoudji, Mathilde ^c   Astord, Stephanie ^c   Gjata, Bernard ^a   Sellier, Pauline ^a,c   Van Wittenberghe, Laetitia ^a   Vignaud, Alban ^a   Boisgerault, Florence ^a   Barkats, Martine ^c   Laforet, Pascal ^f   Kay, Mark A ^e   Koeberl, Dwight D ^g   Ronzitti, Giuseppe ^a   Mingozzi, Federico ^a,c   more..

^a UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^b UNIVERSITY OF FERRARA   (Italy)

^c SORBONNE UNIVERSITÉ   (France)

^d DUKE UNIVERSITY HEALTH SYSTEM   (United States)

^e STANFORD UNIVERSITY   (United States)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^g DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; ALPHA GLUCOSIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG RELEASE; GLYCOGEN STORAGE DISEASE TYPE 2; IMMUNOGENICITY; LIVER; LIVER CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; SURVIVAL; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ANIMAL; DEPENDOPARVOVIRUS; GENE THERAPY; GENE VECTOR; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

ALPHA-GLUCOSIDASES; ANIMALS; DEPENDOVIRUS; GENETIC THERAPY; GENETIC VECTORS; GLYCOGEN STORAGE DISEASE TYPE II; LIVER; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL;

EID: 85036608668     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aam6375     Document Type: Article

References (69)

1. A. T. van der Ploeg, A. J. J. Reuser, Pompe's disease. Lancet 372, 1342-1353 (2008).
2. P. S. Kishnani, D. Corzo, M. Nicolino, B. Byrne, H. Mandel, W. L. Hwu, N. Leslie, J. Levine, C. Spencer, M. McDonald, J. Li, J. Dumontier, M. Halberthal, Y. H. Chien, R. Hopkin, S. Vijayaraghavan, D. Gruskin, D. Bartholomew, A. van der Ploeg, J. P. Clancy, R. Parini, G. Morin, M. Beck, G. S. De la Gastine, M. Jokic, B. Thurberg, S. Richards, D. Bali, M. Davison, M. A. Worden, Y. T. Chen, J. E. Wraith, Recombinant human acid a-glucosidase: Major clinical benefits in infantile-onset Pompe disease. Neurology 68, 99-109 (2007).
3. B. Schoser, A. Stewart, S. Kanters, A. Hamed, J. Jansen, K. Chan, M. Karamouzian, A. Toscano, Survival and long-term outcomes in late-onset Pompe disease following alglucosidase alfa treatment: A systematic review and meta-analysis. J. Neurol. 264, 621-630 (2017).
4. A. T. van der Ploeg, P. R. Clemens, D. Corzo, D. M. Escolar, J. Florence, G. J. Groeneveld, S. Herson, P. S. Kishnani, P. Laforet, S. L. Lake, D. J. Lange, R. T. Leshner, J. E. Mayhew, C. Morgan, K. Nozaki, D. J. Park, A. Pestronk, B. Rosenbloom, A. Skrinar, C. I. van Capelle, N. A. van der Beek, M. Wasserstein, S. A. Zivkovic, A randomized study of alglucosidase alfa in late-onset Pompe's disease. N. Engl. J. Med. 362, 1396-1406 (2010).
5. P. S. Kishnani, A. A. Beckemeyer, New therapeutic approaches for Pompe disease: Enzyme replacement therapy and beyond. Pediatr. Endocrinol. Rev. 12 (suppl. 1), 114-124 (2014).
6. B. J. Ebbink, E. Poelman, I. Plug, M. H. Lequin, P. A. van Doorn, F. K. Aarsen, A. T. van der Ploeg, J. M. P. van den Hout, Cognitive decline in classic infantile Pompe disease: An underacknowledged challenge. Neurology 86, 1260-1261 (2016).
7. T. Fukuda, M. Ahearn, A. Roberts, R. J. Mattaliano, K. Zaal, E. Ralston, P. H. Plotz, N. Raben, Autophagy and mistargeting of therapeutic enzyme in skeletal muscle in Pompe disease. Mol. Ther. 14, 831-839 (2006).
8. P. S. Kishnani, P. C. Goldenberg, S. L. DeArmey, J. Heller, D. Benjamin, S. Young, D. Bali, S. A. Smith, J. S. Li, H. Mandel, D. Koeberl, A. Rosenberg, Y.-T. Chen, Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol. Genet. Metab. 99, 26-33 (2010).
9. J. M. de Vries, N. A. M. E. van der Beek, M. A. Kroos, L. Özkan, P. A. van Doorn, S. M. Richards, C. C. C. Sung, J.-D. C. Brugma, A. A. M. Zandbergen, A. T. van der Ploeg, A. J. J. Reuser, High antibody titer in an adult with Pompe disease affects treatment with alglucosidase alfa. Mol. Genet. Metab. 101, 338-345 (2010).
10. T. A. Kanters, I. Hoogenboom-Plug, M. P. M. H. Rutten-Van Mölken, W. K. Redekop, A. T. van der Ploeg, L. Hakkaart, Cost-effectiveness of enzyme replacement therapy with alglucosidase alfa in classic-infantile patients with Pompe disease. Orphanet J. Rare Dis. 9, 75 (2014).
11. A. C. Nathwani, E. G. D. Tuddenham, S. Rangarajan, C. Rosales, J. McIntosh, D. C. Linch, P. Chowdary, A. Riddell, A. J. Pie, C. Harrington, J. O'Beirne, K. Smith, J. Pasi, B. Glader, P. Rustagi, C. Y. Ng, M. A. Kay, J. Zhou, Y. Spence, C. L. Morton, J. Allay, J. Coleman, S. Sleep, J. M. Cunningham, D. Srivastava, E. Basner-Tschakarjan, F. Mingozzi, K. A. High, J. T. Gray, U. M. Reiss, A. W. Nienhuis, A. M. Davidoff, Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med. 365, 2357-2365 (2011).
12. A. M. Maguire, F. Simonelli, E. A. Pierce, E. N. Pugh Jr., F. Mingozzi, J. Bennicelli, S. Banfi, K. A. Marshall, F. Testa, E. M. Surace, S. Rossi, A. Lyubarsky, V. R. Arruda, B. Konkle, E. Stone, J. Sun, J. Jacobs, L. Dell'Osso, R. Hertle, J.-x. Ma, T. M. Redmond, X. Zhu, B. Hauck, O. Zelenaia, K. S. Shindler, M. G. Maguire, J. F. Wright, N. J. Volpe, J. W. McDonnell, A. Auricchio, K. A. High, J. Bennett, Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358, 2240-2248 (2008).
13. F. Mingozzi, K. A. High, Therapeutic in vivo gene transfer for genetic disease using AAV: Progress and challenges. Nat. Rev. Genet. 12, 341-355 (2011).
14. B. Sun, S. P. Young, P. Li, C. Di, T. Brown, M. Z. Salva, S. Li, A. Bird, Z. Yan, R. Auten, S. D. Hauschka, D. D. Koeberl, Correction of multiple striated muscles in murine Pompe disease through adeno-associated virus-mediated gene therapy. Mol. Ther. 16, 1366-1371 (2008).
15. D. J. Falk, M. S. Soustek, A. G. Todd, C. S. Mah, D. A. Cloutier, J. S. Kelley, N. Clement, D. D. Fuller, B. J. Byrne, Comparative impact of AAV and enzyme replacement therapy on respiratory and cardiac function in adult Pompe mice. Mol. Ther. Methods Clin. Dev. 2, 15007 (2015).
16. P. A. Doerfler, A. G. Todd, N. Clement, D. J. Falk, S. Nayak, R. W. Herzog, B. J. Byrne, Copackaged AAV9 vectors promote simultaneous immune tolerance and phenotypic correction of Pompe disease. Hum. Gene Ther. 27, 43-59 (2016).
17. B. Sun, H. Zhang, L. M. Franco, T. Brown, A. Bird, A. Schneider, D. D. Koeberl, Correction of glycogen storage disease type II by an adeno-associated virus vector containing a muscle-specific promoter. Mol. Ther. 11, 889-898 (2005).
18. T. J. Fraites Jr., M. R. Schleissing, R. A. Shanely, G. A. Walter, D. A. Cloutier, I. Zolotukhin, D. F. Pauly, N. Raben, P. H. Plotz, S. K. Powers, P. D. Kessler, B. J. Byrne, Correction of the enzymatic and functional deficits in a model of Pompe disease using adeno-associated virus vectors. Mol. Ther. 5, 571-578 (2002).
19. C. Mah, K. O. Cresawn, T. J. Fraites Jr., C. A. Pacak, M. A. Lewis, I. Zolotukhin, B. J. Byrne, Sustained correction of glycogen storage disease type II using adeno-associated virus serotype 1 vectors. Gene Ther. 12, 1405-1409 (2005).
20. B. K. Smith, A. D. Martin, L. A. Lawson, V. Vernot, J. Marcus, S. Islam, N. Shafi, M. Corti, S. W. Collins, B. J. Byrne, Inspiratory muscle conditioning exercise and diaphragm gene therapy in Pompe disease: Clinical evidence of respiratory plasticity. Exp. Neurol. 287, 216-224 (2017).
21. P. I. Byrne, S. Collins, C. C. Mah, B. Smith, T. Conlon, S. D. Martin, M. Corti, B. Cleaver, S. Islam, L. A. Lawson, Phase I/II trial of diaphragm delivery of recombinant adeno-associated virus acid alpha-glucosidase (rAAV1-CMV-GAA) gene vector in patients with Pompe disease. Hum. Gene Ther. Clin. Dev. 25, 134-163 (2014).
22. M. Corti, B. Cleaver, N. Clément, T. J. Conlon, K. J. Faris, G. Wang, J. Benson, A. F. Tarantal, D. Fuller, R. W. Herzog, B. J. Byrne, Evaluation of readministration of a recombinant adeno-associated virus vector expressing acid alpha-glucosidase in Pompe disease: Preclinical to clinical planning. Hum. Gene Ther. Clin. Dev. 26, 185-193 (2015).
23. B. Sun, H. Zhang, L. M. Franco, S. P. Young, A. Schneider, A. Bird, A. Amalfitano, Y.-T. Chen, D. D. Koeberl, Efficacy of an adeno-associated virus 8-pseudotyped vector in glycogen storage disease type II. Mol. Ther. 11, 57-65 (2005).
24. F. Mingozzi, Y.-L. Liu, E. Dobrzynski, A. Kaufhold, J. H. Liu, Y. Wang, V. R. Arruda, K. A. High, R. W. Herzog, Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J. Clin. Invest. 111, 1347-1356 (2003).
25. L. M. Franco, B. Sun, X. Yang, A. Bird, H. Zhang, A. Schneider, T. Brown, S. P. Young, T. M. Clay, A. Amalfitano, Y. T. Chen, D. D. Koeberl, Evasion of immune responses to introduced human acid a-glucosidase by liver-restricted expression in glycogen storage disease type II. Mol. Ther. 12, 876-884 (2005).
26. B. Sun, Y.-T. Chen, A. Bird, F. Xu, Y.-X. Hou, A. Amalfitano, D. D. Koeberl, Packaging of an AAV vector encoding human acid a-glucosidase for gene therapy in glycogen storage disease type II with a modified hybrid adenovirus-AAV vector. Mol. Ther. 7, 467-477 (2003).
27. R. J. Ziegler, S. D. Bercury, J. Fidler, M. A. Zhao, J. Foley, T. V. Taksir, S. Ryan, B. L. Hodges, R. K. Scheule, L. S. Shihabuddin, S. H. Cheng, Ability of adeno-associated virus serotype 8-mediated hepatic expression of acid a-glucosidase to correct the biochemical and motor function deficits of presymptomatic and symptomatic Pompe mice. Hum. Gene Ther. 19, 609-621 (2008).
28. N. Raben, T. Jatkar, A. Lee, N. Lu, S. Dwivedi, K. Nagaraju, P. H. Plotz, Glycogen stored in skeletal but not in cardiac muscle in acid a-glucosidase mutant (Pompe) mice is highly resistant to transgene-encoded human enzyme. Mol. Ther. 6, 601-608 (2002).
29. B. Sun, H. Zhang, D. K. Benjamin Jr., T. Brown, A. Bird, S. P. Young, A. McVie-Wylie, Y.-T. Chen, D. D. Koeberl, Enhanced efficacy of an AAV vector encoding chimeric, highly secreted acid a-glucosidase in glycogen storage disease type II. Mol. Ther. 14, 822-830 (2006).
30. F. Mingozzi, K. A. High, Immune responses to AAV vectors: Overcoming barriers to successful gene therapy. Blood 122, 23-36 (2013).
31. A. C. Nathwani, U. M. Reiss, E. G. Tuddenham, C. Rosales, P. Chowdary, J. McIntosh, M. Della Peruta, E. Lheriteau, N. Patel, D. Raj, A. Riddell, J. Pie, S. Rangarajan, D. Bevan, M. Recht, Y.-M. Shen, K. G. Halka, E. Basner-Tschakarjan, F. Mingozzi, K. A. High, J. Allay, M. A. Kay, C. Y. C. Ng, J. Zhou, M. Cancio, C. L. Morton, J. T. Gray, D. Srivastava, A. W. Nienhuis, A. M. Davidoff, Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N. Engl. J. Med. 371, 1994-2004 (2014).
32. A. Hille-Rehfeld, Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta 1241, 177-194 (1995).
33. T. N. Petersen, S. Brunak, G. von Heijne, H. Nielsen, SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786 (2011).
34. G. Ronzitti, G. Bortolussi, R. van Dijk, F. Collaud, S. Charles, C. Leborgne, P. Vidal, S. Martin, B. Gjata, M. S. Sola, L. van Wittenberghe, A. Vignaud, P. Veron, P. J. Bosma, A. F. Muro, F. Mingozzi, A translationally optimized AAV-UGT1A1 vector drives safe and long-lasting correction of Crigler-Najjar syndrome. Mol. Ther. Methods Clin. Dev. 3, 16049 (2016).
35. B. Stern, A. Optun, M. Liesenfeld, C. Gey, M. Gräfe, I. F. Pryme, Enhanced protein synthesis and secretion using a rational signal-peptide library approach as a tailored tool. BMC Proc. 5 (suppl. 8), O13 (2011).
36. N. Raben, T. Fukuda, A. L. Gilbert, D. de Jong, B. L. Thurberg, R. J. Mattaliano, P. Meikle, J. J. Hopwood, K. Nagashima, K. Nagaraju, P. H. Plotz, Replacing acid a-glucosidase in Pompe disease: Recombinant and transgenic enzymes are equipotent, but neither completely clears glycogen from type II muscle fibers. Mol. Ther. 11, 48-56 (2005).
37. N. Raben, V. Hill, L. Shea, S. Takikita, R. Baum, N. Mizushima, E. Ralston, P. Plotz, Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease. Hum. Mol. Genet. 17, 3897-3908 (2008).
38. A. C. Nascimbeni, M. Fanin, E. Masiero, C. Angelini, M. Sandri, The role of autophagy in the pathogenesis of glycogen storage disease type II (GSDII). Cell Death Differ. 19, 1698-1708 (2012).
39. L. R. DeRuisseau, D. D. Fuller, K. Qiu, K. C. DeRuisseau, W. H. Donnelly Jr., C. Mah, P. J. Reier, B. J. Byrne, Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc. Natl. Acad. Sci. U.S.A. 106, 9419-9424 (2009).
40. S. M. F. Turner, A. K. Hoyt, M. K. ElMallah, D. J. Falk, B. J. Byrne, D. D. Fuller, Neuropathology in respiratory-related motoneurons in young Pompe (Gaa-/-) mice. Respir. Physiol. Neurobiol. 227, 48-55 (2016).
41. X. Li, E. M. Eastman, R. J. Schwartz, R. Draghia-Akli, Synthetic muscle promoters: Activities exceeding naturally occurring regulatory sequences. Nat. Biotechnol. 17, 241-245 (1999).
42. M. Nielsen, C. Lundegaard, O. Lund, Prediction of MHC class II binding affinity using SMM-align, a novel stabilization matrix alignment method. BMC Bioinformatics 8, 238 (2007).
43. J. B. Nietupski, G. D. Hurlbut, R. J. Ziegler, Q. Chu, B. L. Hodges, K. M. Ashe, M. Bree, S. H. Cheng, R. J. Gregory, J. Marshall, R. K. Scheule, Systemic administration of AAV8-a-galactosidase A induces humoral tolerance in nonhuman primates despite low hepatic expression. Mol. Ther. 19, 1999-2011 (2011).
44. S. Li, C. Ling, L. Zhong, M. Li, Q. Su, R. He, Q. Tang, D. L. Greiner, L. D. Shultz, M. A. Brehm, T. R. Flotte, C. Mueller, A. Srivastava, G. Gao, Efficient and targeted transduction of nonhuman primate liver with systemically delivered optimized AAV3B vectors. Mol. Ther. 23, 1867-1876 (2015).
45. L. Lisowski, A. P. Dane, K. Chu, Y. Zhang, S. C. Cunningham, E. M. Wilson, S. Nygaard, M. Grompe, I. E. Alexander, M. A. Kay, Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature 506, 382-386 (2014).
46. N. K. Paulk, K. Pekrun, E. Zhu, S. Nygaard, B. Li, J. Xu, K. Chu, C. Leborgne, A. P. Dane, A. Haft, Y. Zhang, F. Zhang, C. Morton, M. B. Valentine, A. M. Davidoff, A. C. Nathwani, F. Mingozzi, M. Grompe, I. E. Alexander, L. Lisowski, M. A. Kay, Bioengineered AAV capsids with combined high human liver transduction in vivo and unique humoral seroreactivity. Mol. Ther. in press (2017).
47. R. J. Desnick, Enzyme replacement and enhancement therapies for lysosomal diseases. J. Inherit. Metab. Dis. 27, 385-410 (2004).
48. A. Amalfitano, A. J. McVie-Wylie, H. Hu, T. L. Dawson, N. Raben, P. Plotz, Y. T. Chen, Systemic correction of the muscle disorder glycogen storage disease type II after hepatic targeting of a modified adenovirus vector encoding human acid-a-glucosidase. Proc. Natl. Acad. Sci. U.S.A. 96, 8861-8866 (1999).
49. N. P. van Til, M. Stok, F. S. F. Aerts Kaya, M. C. de Waard, E. Farahbakhshian, T. P. Visser, M. A. Kroos, E. H. Jacobs, M. A. Willart, P. van der Wegen, B. J. Scholte, B. N. Lambrecht, D. J. Duncker, A. T. van der Ploeg, A. J. J. Reuser, M. M. Verstegen, G. Wagemaker, Lentiviral gene therapy of murine hematopoietic stem cells ameliorates the Pompe disease phenotype. Blood 115, 5329-5337 (2010).
50. C. S. Manno, A. J. Chew, S. Hutchison, P. J. Larson, R. W. Herzog, V. R. Arruda, S. J. Tai, M. V. Ragni, A. Thompson, M. Ozelo, L. B. Couto, D. G. B. Leonard, F. A. Johnson, A. McClelland, C. Scallan, E. Skarsgard, A. W. Flake, M. A. Kay, K. A. High, B. Glader, AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101, 2963-2972 (2003).
51. D. L. Mack, K. Poulard, M. A. Goddard, V. Latournerie, J. M. Snyder, R. W. Grange, M. R. Elverman, J. Denard, P. Veron, L. Buscara, C. Le Bec, J.-Y. Hogrel, A. G. Brezovec, H. Meng, L. Yang, F. Liu, M. O'Callaghan, N. Gopal, V. E. Kelly, B. K. Smith, J. L. Strande, F. Mavilio, A. H. Beggs, F. Mingozzi, M. W. Lawlor, A. Buj-Bello, M. K. Childers, Systemic AAV8-mediated gene therapy drives whole-body correction of myotubular myopathy in dogs. Mol. Ther. 25, 839-854 (2017).
52. J. Ramos, J. S. Chamberlain, Gene therapy for Duchenne muscular dystrophy. Expert Opin. Orphan Drugs 3, 1255-1266 (2015).
53. N. Raben, K. Nagaraju, E. Lee, P. Kessler, B. Byrne, L. Lee, M. LaMarca, C. King, J. Ward, B. Sauer, P. Plotz, Targeted disruption of the acid a-glucosidase gene in mice causes an illness with critical features of both infantile and adult human glycogen storage disease type II. J. Biol. Chem. 273, 19086-19092 (1998).
54. G. Parenti, S. Fecarotta, G. la Marca, B. Rossi, S. Ascione, M. A. Donati, L. O. Morandi, S. Ravaglia, A. Pichiecchio, D. Ombrone, M. Sacchini, M. B. Pasanisi, P. De Filippi, C. Danesino, R. Della Casa, A. Romano, C. Mollica, M. Rosa, T. Agovino, E. Nusco, C. Porto, G. Andria, A chaperone enhances blood a-glucosidase activity in Pompe disease patients treated with enzyme replacement therapy. Mol. Ther. 22, 2004-2012 (2014).
55. A. Ruzo, M. Garcia, A. Ribera, P. Villacampa, V. Haurigot, S. Marcó, E. Ayuso, X. M. Anguela, C. Roca, J. Agudo, D. Ramos, J. Ruberte, F. Bosch, Liver production of sulfamidase reverses peripheral and ameliorates CNS pathology in mucopolysaccharidosis IIIA mice. Mol. Ther. 20, 254-266 (2012).
56. P. A. Gonzales, T. Pisitkun, J. D. Hoffert, D. Tchapyjnikov, R. A. Star, R. Kleta, N. S. Wang, M. A. Knepper, Large-scale proteomics and phosphoproteomics of urinary exosomes. J. Am. Soc. Nephrol. 20, 363-379 (2009).
57. N. W. Andrews, Regulated secretion of conventional lysosomes. Trends Cell Biol. 10, 316-321 (2000).
58. B. Sun, A. Bird, S. P. Young, P. S. Kishnani, Y.-T. Chen, D. D. Koeberl, Enhanced response to enzyme replacement therapy in Pompe disease after the induction of immune tolerance. Am. J. Hum. Genet. 81, 1042-1049 (2007).
59. B. Sun, M. D. Kulis, S. P. Young, A. C. Hobeika, S. Li, A. Bird, H. Zhang, Y. Li, T. M. Clay, W. Burks, P. S. Kishnani, D. D. Koeberl, Immunomodulatory gene therapy prevents antibody formation and lethal hypersensitivity reactions in murine Pompe disease. Mol. Ther. 18, 353-360 (2010).
60. D. M. Markusic, B. E. Hoffman, G. Q. Perrin, S. Nayak, X. Wang, P. A. LoDuca, K. A. High, R. W. Herzog, Effective gene therapy for haemophilic mice with pathogenic factor IX antibodies. EMBO Mol. Med. 5, 1698-1709 (2013).
61. J. M. Crudele, J. D. Finn, J. I. Siner, N. B. Martin, G. P. Niemeyer, S. Zhou, F. Mingozzi, C. D. Lothrop Jr., V. R. Arruda, AAV liver expression of FIX-Padua prevents and eradicates FIX inhibitor without increasing thrombogenicity in hemophilia B dogs and mice. Blood 125, 1553-1561 (2015).
62. G. Bortolussi, L. Zentillin, J. Vaníkova, L. Bockor, C. Bellarosa, A. Mancarella, E. Vianello, C. Tiribelli, M. Giacca, L. Vitek, A. F. Muro, Life-long correction of hyperbilirubinemia with a neonatal liver-specific AAV-mediated gene transfer in a lethal mouse model of Crigler-Najjar Syndrome. Hum. Gene Ther. 25, 844-855 (2014).
63. A. Meliani, F. Boisgerault, G. Ronzitti, F. Collaud, C. Leborgne, T. K. Kishimoto, F. Mingozzi, Antigen-specific modulation of capsid immunogenicity with tolerogenic nanoparticles results in successful AAV vector readministration. Mol. Ther. 24, pS34 (2016).
64. A. Meliani, C. Leborgne, S. Triffault, L. Jeanson-Leh, P. Veron, F. Mingozzi, Determination of anti-adeno-associated virus vector neutralizing antibody titer with an in vitro reporter system. Hum. Gene. Ther. Methods 26, 45-53 (2015).
65. E. Ayuso, F. Mingozzi, J. Montane, X. Leon, X. M. Anguela, V. Haurigot, S. A. Edmonson, L. Africa, S. Zhou, K. A. High, F. Bosch, J. F. Wright, High AAV vector purity results in serotype- and tissue-independent enhancement of transduction efficiency. Gene Ther. 17, 503-510 (2010).
66. E. Masat, P. Laforêt, M. De Antonio, G. Corre, B. Perniconi, N. Taouagh, K. Mariampillai, D. Amelin, W. Mauhin, J.-Y. Hogrel, C. Caillaud, G. Ronzitti, F. Puzzo, K. Kuranda, P. Colella, R. Mallone, O. Benveniste, F. Mingozzi; French Pompe Registry Study Group, Long-term exposure to Myozyme results in a decrease of anti-drug antibodies in late-onset Pompe disease patients. Sci. Rep. 6, 36182 (2016).
67. P. Zhang, B. Sun, T. Osada, R. Rodriguiz, X. Y. Yang, X. Luo, A. R. Kemper, T. M. Clay, D. D. Koeberl, Immunodominant liver-specific expression suppresses transgenedirected immune responses in murine Pompe disease. Hum. Gene Ther. 23, 460-472 (2012).
68. R. J. Moreland, X. Jin, X. K. Zhang, R. W. Decker, K. L. Albee, K. L. Lee, R. D. Cauthron, K. Brewer, T. Edmunds, W. M. Canfield, Lysosomal acid a-glucosidase consists of four different peptides processed from a single chain precursor. J. Biol. Chem. 280, 6780-6791 (2005).
69. D. T. Deming, in Molecular Genetics and Metabolism (Elsevier, 2016), vol. 117, pp. S14-S124.