Safety of Intradiaphragmatic Delivery of Adeno-Associated Virus-Mediated Alpha-Glucosidase (rAAV1-CMV-hGAA) Gene Therapy in Children Affected by Pompe Disease

Human Gene Therapy Clinical Development

Volumn 28, Issue 4, 2017, Pages 208-218

  Corti, Manuela ^a   Liberati, Cristina ^a   Smith, Barbara K ^b   Lawson, Lee Ann ^a   Tuna, Ibrahim S ^a   Conlon, Thomas J ^a   Coleman, Kirsten E ^a   Islam, Saleem ^a   Herzog, Roland W ^a   Fuller, David D ^b   Collins, Shelley W ^a   Byrne, Barry J ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

AAV; immune response; Pompe disease; safety

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; ALPHA GLUCOSIDASE; CAPSID PROTEIN;

ANTIBODY RESPONSE; ARTICLE; CHILD; CLINICAL ARTICLE; COMPUTER ASSISTED TOMOGRAPHY; DIAPHRAGM; DRUG SAFETY; ENZYME REPLACEMENT; GENE PRODUCT; GLYCOGEN STORAGE DISEASE TYPE 2; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOMODULATION; NEUROMUSCULAR FUNCTION; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RESPIRATORY FAILURE; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS CAPSID; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; CLINICAL TRIAL; CONTROLLED STUDY; DEPENDOPARVOVIRUS; FEMALE; GENE THERAPY; GENE VECTOR; GENETICS; MALE; MOUSE; PATHOLOGY; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE; SURGERY; VIDEO ASSISTED THORACOSCOPIC SURGERY;

ALPHA-GLUCOSIDASES; ANIMALS; CHILD; DEPENDOVIRUS; DIAPHRAGM; FEMALE; GENETIC THERAPY; GENETIC VECTORS; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; IMMUNOMODULATION; MALE; MICE; MUSCLE, SKELETAL; THORACIC SURGERY, VIDEO-ASSISTED; TRANSGENES;

EID: 85038627794     PISSN: 23248637     EISSN: 23248645     Source Type: Journal    
DOI: 10.1089/humc.2017.146     Document Type: Article

References (80)

1. Hers HG. alpha-Glucosidase deficiency in generalized glycogenstorage disease (Pompe's disease). Biochem J 1963;86:11-16.
2. Hirschhorn R, Reuser AJ. Glycogen storage disease type II: acid a-glucosidase (acid maltase) deficiency. In: Scriver CR, Beaudet AL, Sly W, et al., eds. The Metabolic and Molecular Bases of Inherited Disease. New York: McGraw Hill, 2001:3389-3420.
3. Martin JJ, de Barsy T, van Hoof F, et al. Pompe's disease: an inborn lysosomal disorder with storage of glycogen. A study of brain and striated muscle. Acta Neuropathol 1973;23:229-244.
4. Raben N, Plotz P, Byrne BJ. Acid alphaglucosidase deficiency (glycogenosis type II, Pompe disease). Curr Mol Med 2002;2:145-166.
5. Kroos M, Hoogeveen-Westerveld M, van der Ploeg A, et al. The genotype-phenotype correlation in Pompe disease. Am J Med Genet C Semin Med Genet 2012;160C:59-68.
6. ACMG Work Group on Management of Pompe Disease; Kishnani PS, Steiner RD, et al. Pompe disease diagnosis and management guideline. Genet Med 2006;8:267-288.
7. Slonim AE, Bulone L, Ritz S, et al. Identification of two subtypes of infantile acid maltase deficiency. J Pediatr 2000;137:283-285.
8. Elmallah MK, Falk DJ, Nayak S, et al. Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in pompe mice. Mol Ther 2014;22:702-712.
9. Chan J, Desai AK, Kazi ZB, et al. The emerging phenotype of late-onset Pompe disease: A systematic literature review. Mol Genet Metab 2017; 120:163-172.
10. Fernandez C, Legido A, Jethva R, et al. Correction of a short cardiac PR interval in a 12-year-old girl with late-onset Pompe disease following enzyme replacement therapy. Genet Med 2012;14:757-758.
11. van Capelle CI, van der Beek NA, Hagemans ML, et al. Effect of enzyme therapy in juvenile patients with Pompe disease: A three-year open-label study. Neuromuscul Disord 2010;20:775-782.
12. Jurecka A, Zuberuber Z, Opoka-Winiarska V, et al. Effect of rapid cessation of enzyme replacement therapy: A report of 5 cases and a review of the literature. Mol Genet Metab 2012;107:508-512.
13. Toscano A, Schoser B. Enzyme replacement therapy in late-onset Pompe disease: A systematic literature review. J Neurol 2013;260:951-959.
14. Chen CA, Chien YH, Hwu WL, et al. Left ventricular geometry, global function, and dyssynchrony in infants and children with pompe cardiomyopathy undergoing enzyme replacement therapy. J Card Fail 2011;17:930-936.
15. Byrne BJ, Kishnani PS, Case LE, et al. Pompe disease: design, methodology, and early findings from the Pompe Registry. Mol Genet Metab 2011; 103:1-11.
16. Ohashi T, Iizuka S, Shimada Y, et al. Administration of anti-CD3 antibodies modulates the immune response to an infusion of alpha-glucosidase in mice. Mol Ther 2012;20:1924-1931.
17. de Vries JM, van der Beek NA, Kroos MA, et al. High antibody titer in an adult with Pompe disease affects treatment with alglucosidase alfa. Mol Genet Metab 2010;101:338-345.
18. Kishnani PS, Dickson PI, Muldowney L, et al. Immune response to enzyme replacement therapies in lysosomal storage diseases and the role of immune tolerance induction. Mol Genet Metab 2016;117:66-83.
19. Nayak S, Sivakumar R, Cao O, et al. Mapping the T helper cell response to acid alpha-glucosidase in Pompe mice. Mol Genet Metab 2012;106:189-195.
20. Byrne BJ, Falk DJ, Pacak CA, et al. Pompe disease gene therapy. Hum Mol Genet 2011;20:R61-68.
21. Patel TT, Banugaria SG, Case LE, et al. The impact of antibodies in late-onset Pompe disease: A case series and literature review. Mol Genet Metab 2012;106:301-309.
22. Kikuchi T, Yang HW, Pennybacker M, et al. Clinical and metabolic correction of Pompe disease by enzyme therapy in acid maltase-deficient quail. J Clin Invest 1998;101:827-833.
23. Raben N, Danon M, Gilbert AL, et al. Enzyme replacement therapy in the mouse model of Pompe disease. Mol Genet Metab 2003;80:159-169.
24. DeRuisseau LR, Fuller DD, Qiu K, et al. Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc Natl Acad Sci U S A 2009; 106:9419-9424.
25. Fuller DD, ElMallah MK, Smith BK, et al. The respiratory neuromuscular system in Pompe disease. Respir Physiol Neurobiol 2013;189:241-249.
26. Todd AG, McElroy JA, Grange RW, et al. Correcting neuromuscular deficits with gene therapy in Pompe disease. Ann Neurol 2015;78:222-234.
27. Mah CS, Falk DJ, Germain SA, et al. Gel-mediated delivery of AAV1 vectors corrects ventilatory function in Pompe mice with established disease. Mol Ther 2010;18:502-510.
28. Smith BK, Collins SW, Conlon TJ, et al. Phase I/II trial of adeno-associated virus-mediated alphaglucosidase gene therapy to the diaphragm for chronic respiratory failure in Pompe disease: initial safety and ventilatory outcomes. Hum Gene Ther 2013;24:630-640.
29. Byrne PI, Collins S, Mah CC, et al. Phase I/II trial of diaphragmdelivery of recombinant adeno-associated virus acid alpha-glucosidase (rAAaV1-CMV-GAA) gene vector in patients with Pompe disease. Hum Gene Ther Clin Dev 2014;25:134-163.
30. Smith BK, Martin AD, Lawson LA, et al. Inspiratory muscle conditioning exercise and diaphragm gene therapy in Pompe disease: clinical evidence of respiratory plasticity. Exp Neurol 2017;287:216-224.
31. Mah C, Fraites TJ Jr, Cresawn KO, et al. A new method for recombinant adeno-associated virus vector delivery to murine diaphragm. Mol Ther 2004;9:458-463.
32. Conlon TJ, Erger K, Porvasnik S, et al. Preclinical toxicology and biodistribution studies of recombinant adeno-associated virus 1 human acid alpha-glucosidase. Hum Gene Ther Clin Dev 2013; 24:127-133.
33. Elder ME, Nayak S, Collins SW, et al. B-Cell depletion and immunomodulation before initiation of enzyme replacement therapy blocks the immune response to acid alpha-glucosidase in infantile-onset Pompe disease. J Pediatr 2013;163:847-854. e1.
34. Corti M, Elder M, Falk D, et al. B-Cell depletion is protective against anti-AAV capsid immune response: A human subject case study. Mol Ther Methods Clin Dev 2014;1.
35. Hobson-Webb LD, Proia AD, Thurberg BL, et al. Autopsy findings in late-onset Pompe disease: A case report and systematic review of the literature. Mol Genet Metab 2012;106:462-469.
36. Kretzschmar HA, Wagner H, Hubner G, et al. Aneurysms and vacuolar degeneration of cerebral arteries in late-onset acid maltase deficiency. J Neurol Sci 1990;98:169-183.
37. Anneser JM, Pongratz DE, Podskarbi T, et al. Mutations in the acid alpha-glucosidase gene (M. Pompe) in a patient with an unusual phenotype. Neurology 2005;64:368-370.
38. McIntosh PT, Hobson-Webb LD, Kazi ZB, et al. Neuroimaging findings in infantile Pompe patients treated with enzyme replacement therapy. Mol Genet Metab 2017 Oct 13 [Epub ahead of print]; DOI: 10. 1016/j. ymgme. 2017. 10. 005.
39. Braunsdorf WE. Fusiform aneurysm of basilar artery and ectatic internal carotid arteries associated with glycogenosis type 2 (Pompe's disease). Neurosurgery 1987;21:748-749.
40. Brettschneider J, Sperfeld AD, Ludolph AC, et al. Intracerebral hemorrhage in a patient with glycogenosis type II (Pompe disease): is there a pathophysiological relationship? Muscle Nerve 2008;38:1211-1212.
41. Garibaldi M, Sacconi S, Antonini G, et al. Long term follow-up of cerebrovascular abnormalities in late onset Pompe disease (LOPD). J Neurol 2017;264:589-590.
42. Hensel O, Hanisch F, Stock K, et al. Morphology and function of cerebral arteries in adults with pompe disease. JIMD Rep 2015;20:27-33.
43. Laforet P, Petiot P, Nicolino M, et al. Dilative arteriopathy and basilar artery dolichoectasia complicating late-onset Pompe disease. Neurology 2008; 70:2063-2066.
44. Makos MM, McComb RD, Hart MN, et al. Alphaglucosidase deficiency and basilar artery aneurysm: report of a sibship. Ann Neurol 1987;22: 629-633.
45. Matsuoka Y, Senda Y, Hirayama M, et al. Lateonset acid maltase deficiency associated with intracranial aneurysm. J Neurol 1988;235:371-373.
46. Miyamoto Y, Etoh Y, Joh R, et al. Adult-onset acid maltase deficiency in siblings. Acta Pathol Jpn 1985;35:1533-1542.
47. Peric S, Fumic K, Bilic K, et al. Rupture of the middle cerebral artery aneurysm as a presenting symptom of late-onset Pompe disease in an adult with a novel GAA gene mutation. Acta Neurol Belg 2014;114:165-166.
48. Quenardelle V, Bataillard M, Bazin D, et al. Pompe disease presenting as an isolated generalized dilative arteriopathy with repeated brain and kidney infarcts. J Neurol 2015;262:473-475.
49. Refai D, Lev R, Cross DT, et al. Thrombotic complications of a basilar artery aneurysm in a young adult with Pompe disease. Surg Neurol 2008;70: 518-520.
50. Renard D, Labauge P. Neurological picture: cerebral microbleeds in Pompe disease. J Neurol Neurosurg Psychiatry 2010;81:1217.
51. Sacconi S, Bocquet JD, Chanalet S, et al. Abnormalities of cerebral arteries are frequent in patients with late-onset Pompe disease. J Neurol 2010;257:1730-1733.
52. Sandhu D, Rizvi A, Kim J, et al. Diffuse cerebral microhemorrhages in a patient with adult-onset Pompe's disease: A case report. J Vasc Interv Neurol 2014;7:82-85.
53. Zhang B, Zhao Y, Liu J, et al. Late-onset Pompe disease with complicated intracranial aneurysm: A Chinese case report. Neuropsychiatr Dis Treat 2016;12:713-717.
54. Pichiecchio A, Sacco S, De Filippi P, et al. Lateonset Pompe disease: A genetic-radiological correlation on cerebral vascular anomalies. J Neurol 2017 Oct;264:2110-2118.
55. Montagnese F, Barca E, Musumeci O, et al. Clinical and molecular aspects of 30 patients with lateonset Pompe disease (LOPD): unusual features and response to treatment. J Neurol 2015;262:968-978.
56. Wens SC, Kuperus E, Mattace-Raso FU, Kruijshaar ME, Brusse E, van Montfort KC, de Boer MS, Sijbrands EJ, van der Ploeg AT, van Doorn PA. Increased aortic stiffness and blood pressure in non-classic Pompe disease. J Inherit Metab Dis 2014;37:391-397.
57. Schuller A, Wenninger S, Strigl-Pill N, et al. Toward deconstructing the phenotype of late-onset Pompe disease. Am J Med Genet C Semin Med Genet2012;160C:80-88.
58. Calcedo R, Wilson JM. Humoral immune response to AAV. Front Immunol 2013;4:341.
59. Masat E, Pavani G, Mingozzi F. Humoral immunity to AAV vectors in gene therapy: challenges and potential solutions. Discov Med2013;15:379-389.
60. Mingozzi F, High KA. Immune responses to AAV vectors: overcoming barriers to successful gene therapy. Blood 2013;122:23-36.
61. Ferreira V, Twisk J, Kwikkers K, et al. Immune responses to intramuscular administration of alipogene tiparvovec (AAV1-LPL(S447X) in a Phase II clinical trial of lipoprotein lipase deficiency gene therapy. Hum Gene Ther 2014;25:180-188.
62. Scallan CD, Jiang H, Liu T, et al. Human immunoglobulin inhibits liver transduction by AAV vectors at low AAV2 neutralizing titers in SCID mice. Blood 2006;107:1810-1817.
63. Murphy SL, Li H, Zhou S, et al. Prolonged susceptibility to antibody-mediated neutralization for adeno-associated vectors targeted to the liver. Mol Ther 2008;16:138-145.
64. Jiang H, Couto LB, Patarroyo-White 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 2006;108: 3321-3328.
65. Manno CS, Pierce GF, Arruda VR, 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.
66. Corti M, Cleaver B, Clement N, et al. 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 2015;26:185-193.
67. Kozarsky KF, McKinley DR, Austin LL, et al. In vivo correction of low density lipoprotein receptor deficiency in the Watanabe heritable hyperlipidemic rabbit with recombinant adenoviruses. J Biol Chem 1994;269:13695-13702.
68. Gao GP, Lu F, Sanmiguel JC, et al. Rep/Cap gene amplification and high-yield production of AAV in an A549 cell line expressing Rep/Cap. Mol Ther 2002;5:644-649.
69. Unzu C, Hervas-Stubbs S, Sampedro A, et al. Transient and intensive pharmacological immunosuppression fails to improve AAV-based liver gene transfer in nonhuman primates. J Transl Med 2012;10:122.
70. Sack BK, Merchant S, Markusic DM, 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.
71. Mingozzi F, Chen Y, Murphy SL, et al. Pharmacological modulation of humoral immunity in a nonhuman primate model of AAV gene transfer for hemophilia B. Mol Ther 2012;20:1410-1416.
72. Fontanellas A, Hervas-Stubbs S, Mauleon I, et al. Intensive pharmacological immunosuppression allows for repetitive liver gene transfer with recombinant adenovirus in nonhuman primates. Mol Ther 2010;18:754-765.
73. Limon JJ, Fruman DA. Akt and mTOR in B cell activation and differentiation. Front Immunol 2012;3:228.
74. Nayak S, Cao O, Hoffman BE, et al. Prophylactic immune tolerance induced by changing the ratio of antigen-specific effector to regulatory T cells. J Thromb Haemost 2009;7:1523-1532.
75. Moghimi B, Sack BK, Nayak S, et al. Induction of tolerance to factor VIII by transient co-administration with rapamycin. J Thromb Haemost 2011;9:1524-1533.
76. Bestard O, Cassis L, Cruzado JM, et al. Costimulatory blockade with mTor inhibition abrogates effector T-cell responses allowing regulatory Tcell survival in renal transplantation. Transpl Int 2011;24:451-460.
77. Battaglia M, Stabilini A, Roncarolo MG. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 2005;105:4743-4748.
78. Nayak S, Sarkar D, Perrin GQ, et al. Prevention and reversal of antibody responses against Factor IX in gene therapy for hemophilia B. Front Microbiol 2011;2:244.
79. Liu CL, Ye P, Lin J, et al. Anti-CD20 as the B-cell targeting agent in a combined therapy to modulate anti-Factor VIII immune responses in hemophilia A inhibitor mice. Front Immunol 2014;4:502.
80. Mendell JR, Al-Zaidy S, Shell R, et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med 2017;377:1713-1722.