Comparative impact of AAV and enzyme replacement therapy on respiratory and cardiac function in adult Pompe mice

Molecular Therapy Methods and Clinical Development

Volumn 2, Issue , 2015, Pages 15007-

  Falk, Darin J ^a,b   Soustek, Meghan S ^a,b   Todd, Adrian Gary ^a,b   Mah, Cathryn S ^a,b   Cloutier, Denise A ^a,b   Kelley, Jeffry S ^a,b   Clement, Nathalie ^a,b   Fuller, David D ^b   Byrne, Barry J ^a,b  

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

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; DESMIN; DIPHENHYDRAMINE; GLUCOSIDASE; GLYCOGEN; ALPHA GLUCOSIDASE; GLYCOGEN ACID ALPHA GLUCOSIDASE; RECOMBINANT GLYCOGEN ACID ALPHA GLUCOSIDASE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANAPHYLAXIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY PLETHYSMOGRAPHY; BREATHING RATE; CARDIOVASCULAR MAGNETIC RESONANCE; COMPARATIVE STUDY; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPLACEMENT; FEMALE; GLYCOGEN STORAGE DISEASE TYPE 2; HEART FUNCTION; HEART LEFT VENTRICLE MASS; HEART SIZE; IMMUNOGENICITY; LUNG MINUTE VOLUME; MALE; MORTALITY; MOUSE; NONHUMAN; PR INTERVAL; PRIORITY JOURNAL; RESPIRATORY FAILURE; RESPIRATORY FUNCTION; TIDAL VOLUME; VIROTHERAPY; WEIGHT GAIN; ANIMAL MODEL; BIOACCUMULATION; BREATHING; CARDIOPULMONARY INSUFFICIENCY; CLINICAL ASSESSMENT; DIAPHRAGM; GLYCOGEN ANALYSIS; OUTCOME ASSESSMENT; TREATMENT DURATION; VIRAL GENE THERAPY;

EID: 85015239107     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2015.7     Document Type: Article

References (54)

1. 1 Fukuda, T, Ewan, L, Bauer, M, Mattaliano, RJ, Zaal, K, Ralston, E, et al. Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann Neurol 59 (2006), 700–708.
2. 2 Raben, N, Danon, M, Gilbert, AL, Dwivedi, S, Collins, B, Thurberg, BL, et al. Enzyme replacement therapy in the mouse model of Pompe disease. Mol Genet Metab 80 (2003), 159–169.
3. 3 Raben, N, Nagaraju, K, Lee, E, Kessler, P, Byrne, B, Lee, L, et al. Targeted disruption of the acid alpha-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 (1998), 19086–19092.
4. 4 Raben, N, Takikita, S, Pittis, MG, Bembi, B, Marie, SK, Roberts, A, et al. Deconstructing Pompe disease by analyzing single muscle fibers: to see a world in a grain of sand. Autophagy 3 (2007), 546–552.
5. 5 Raben, N, Wong, A, Ralston, E, Myerowitz, R, Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am J Med Genet C Semin Med Genet 160C (2012), 13–21.
6. 6 Xu, S, Galperin, M, Melvin, G, Horowits, R, Raben, N, Plotz, P, et al. Impaired organization and function of myofilaments in single muscle fibers from a mouse model of Pompe disease. J Appl Physiol (1985) 108 (2010), 1383–1388.
7. 7 Kishnani, PS, Hwu, WL, Mandel, H, Nicolino, M, Yong, F, Corzo, D, Infantile-Onset Pompe Disease Natural History Study Group. A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J Pediatr 148 (2006), 671–676.
8. 8 Kishnani, PS, Steiner, RD, Bali, D, Berger, K, Byrne, BJ, Case, LE, et al. Pompe disease diagnosis and management guideline. Genet Med 8 (2006), 267–288.
9. 9 Byrne, BJ, Kishnani, PS, Case, LE, Merlini, L, Müller-Felber, W, Prasad, S, et al. Pompe disease: design, methodology, and early findings from the Pompe Registry. Mol Genet Metab 103 (2011), 1–11.
10. 10 ElMallah, MK, Falk, DJ, Lane, MA, Conlon, TJ, Lee, KZ, Shafi, NI, et al. Retrograde gene delivery to hypoglossal motoneurons using adeno-associated virus serotype 9. Hum Gene Ther Methods 23 (2012), 148–156.
11. 11 Falk, DJ, Mah, CS, Soustek, MS, Lee, KZ, Elmallah, MK, Cloutier, DA, et al. Intrapleural administration of AAV9 improves neural and cardiorespiratory function in Pompe disease. Mol Ther 21 (2013), 1661–1667.
12. 12 Qiu, K, Falk, DJ, Reier, PJ, Byrne, BJ, Fuller, DD, Spinal delivery of AAV vector restores enzyme activity and increases ventilation in Pompe mice. Mol Ther 20 (2012), 21–27.
13. 13 Elmallah, MK, Falk, DJ, Nayak, S, Federico, RA, Sandhu, MS, Poirier, A, et al. Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in pompe mice. Mol Ther 22 (2014), 702–712.
14. 14 Elder, ME, Nayak, S, Collins, SW, Lawson, LA, Kelley, JS, Herzog, RW, 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, 163, 2013, 847 54.e1.
15. 15 Byrne, BJ, Falk, DJ, Pacak, CA, Nayak, S, Herzog, RW, Elder, ME, et al. Pompe disease gene therapy. Hum Mol Genet 20:R1 (2011), R61–R68.
16. 16 Mah, CS, Falk, DJ, Germain, SA, Kelley, JS, Lewis, MA, Cloutier, DA, et al. Gel-mediated delivery of AAV1 vectors corrects ventilatory function in Pompe mice with established disease. Mol Ther 18 (2010), 502–510.
17. 17 Mah, C, Cresawn, KO, Fraites, TJ Jr, Pacak, CA, Lewis, MA, Zolotukhin, I, et al. Sustained correction of glycogen storage disease type II using adeno-associated virus serotype 1 vectors. Gene Ther 12 (2005), 1405–1409.
18. 18 Mah, C, Pacak, CA, Cresawn, KO, Deruisseau, LR, Germain, S, Lewis, MA, et al. Physiological correction of Pompe disease by systemic delivery of adeno-associated virus serotype 1 vectors. Mol Ther 15 (2007), 501–507.
19. 19 Zincarelli, C, Soltys, S, Rengo, G, Rabinowitz, JE, Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16 (2008), 1073–1080.
20. 20 Pacak, CA, Mah, CS, Thattaliyath, BD, Conlon, TJ, Lewis, MA, Cloutier, DE, et al. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 99 (2006), e3–e9.
21. 21 Pacak, CA, Sakai, Y, Thattaliyath, BD, Mah, CS, Byrne, BJ, Tissue specific promoters improve specificity of AAV9 mediated transgene expression following intra-vascular gene delivery in neonatal mice. Genet Vaccines Ther, 6, 2008, 13.
22. 22 Nayak, S, Doerfler, PA, Porvasnik, SL, Cloutier, DD, Khanna, R, Valenzano, KJ, et al. Immune responses and hypercoagulation in ERT for Pompe disease are mutation and rhGAA dose dependent. PLoS One, 9, 2014, e98336.
23. 23 van Gelder, CM, Hoogeveen-Westerveld, M, Kroos, MA, Plug, I, van der Ploeg, AT, Reuser, AJ, Enzyme therapy and immune response in relation to CRIM status: the Dutch experience in classic infantile Pompe disease. J Inherit Metab Dis 38 (2014), 305–314.
24. 24 Banugaria, SG, Patel, TT, Mackey, J, Das, S, Amalfitano, A, Rosenberg, AS, et al. Persistence of high sustained antibodies to enzyme replacement therapy despite extensive immunomodulatory therapy in an infant with Pompe disease: need for agents to target antibody-secreting plasma cells. Mol Genet Metab 105 (2012), 677–680.
25. 25 Pacak, CA, Mah, CS, Thattaliyath, BD, Conlon, TJ, Lewis, MA, Cloutier, DE, et al. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 99 (2006), e3–e9.
26. 26 Sun, B, Young, SP, Li, P, Di, C, Brown, T, Salva, MZ, et al. Correction of multiple striated muscles in murine Pompe disease through adeno-associated virus-mediated gene therapy. Mol Ther 16 (2008), 1366–1371.
27. 27 Reuser, AJ, Kroos, MA, Ponne, NJ, Wolterman, RA, Loonen, MC, Busch, HF, et al. Uptake and stability of human and bovine acid alpha-glucosidase in cultured fibroblasts and skeletal muscle cells from glycogenosis type II patients. Exp Cell Res 155 (1984), 178–189.
28. 28 Chien, YH, Hwu, WL, Lee, NC, Pompe disease: early diagnosis and early treatment make a difference. Pediatr Neonatol 54 (2013), 219–227.
29. 29 Toscano, A, Schoser, B, Enzyme replacement therapy in late-onset Pompe disease: a systematic literature review. J Neurol 260 (2013), 951–959.
30. 30 Fuller, DD, ElMallah, MK, Smith, BK, Corti, M, Lawson, LA, Falk, DJ, et al. The respiratory neuromuscular system in Pompe disease. Respir Physiol Neurobiol 189 (2013), 241–249.
31. 31 Van der Ploeg, AT, Kroos, MA, Willemsen, R, Brons, NH, Reuser, AJ, Intravenous administration of phosphorylated acid alpha-glucosidase leads to uptake of enzyme in heart and skeletal muscle of mice. J Clin Invest 87 (1991), 513–518.
32. 32 Yang, HW, Kikuchi, T, Hagiwara, Y, Mizutani, M, Chen, YT, Van Hove, JL, Recombinant human acid alpha-glucosidase corrects acid alpha-glucosidase-deficient human fibroblasts, quail fibroblasts, and quail myoblasts. Pediatr Res 43 (1998), 374–380.
33. 33 Maga, JA, Zhou, J, Kambampati, R, Peng, S, Wang, X, Bohnsack, RN, et al. Glycosylation-independent lysosomal targeting of acid α-glucosidase enhances muscle glycogen clearance in pompe mice. J Biol Chem 288 (2013), 1428–1438.
34. 34 Koeberl, DD, Austin, S, Case, LE, Smith, EC, Buckley, AF, Young, SP, et al. Adjunctive albuterol enhances the response to enzyme replacement therapy in late-onset Pompe disease. FASEB J 28 (2014), 2171–2176.
35. 35 Li, S, Sun, B, Nilsson, MI, Bird, A, Tarnopolsky, MA, Thurberg, BL, et al. Adjunctive β2-agonists reverse neuromuscular involvement in murine Pompe disease. FASEB J 27 (2013), 34–44.
36. 36 DeRuisseau, LR, Fuller, DD, Qiu, K, DeRuisseau, KC, Donnelly, WH Jr, Mah, C, et al. Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc Natl Acad Sci USA 106 (2009), 9419–9424.
37. 37 Falk, DJ, Mah, CS, Soustek, MS, Lee, KZ, Elmallah, MK, Cloutier, DA, et al. Intrapleural administration of AAV9 improves neural and cardiorespiratory function in Pompe disease. Mol Ther 21 (2013), 1661–1667.
38. 38 Lee, KZ, Qiu, K, Sandhu, MS, Elmallah, MK, Falk, DJ, Lane, MA, et al. Hypoglossal neuropathology and respiratory activity in pompe mice. Front Physiol, 2, 2011, 31.
39. 39 Bockstael, O, Foust, KD, Kaspar, B, Tenenbaum, L, Recombinant AAV delivery to the central nervous system. Methods Mol Biol 807 (2011), 159–177.
40. 40 Hester, ME, Foust, KD, Kaspar, RW, Kaspar, BK, AAV as a gene transfer vector for the treatment of neurological disorders: novel treatment thoughts for ALS. Curr Gene Ther 9 (2009), 428–433.
41. 41 Foust, KD, Nurre, E, Montgomery, CL, Hernandez, A, Chan, CM, Kaspar, BK, Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27 (2009), 59–65.
42. 42 Bevan, AK, Duque, S, Foust, KD, Morales, PR, Braun, L, Schmelzer, L, et al. Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol Ther 19 (2011), 1971–1980.
43. 43 Amalfitano, A, McVie-Wylie, AJ, Hu, H, Dawson, TL, Raben, N, Plotz, P, et al. Systemic correction of the muscle disorder glycogen storage disease type II after hepatic targeting of a modified adenovirus vector encoding human acid-alpha-glucosidase. Proc Natl Acad Sci USA 96 (1999), 8861–8866.
44. 44 Ding, EY, Hodges, BL, Hu, H, McVie-Wylie, AJ, Serra, D, Migone, FK, et al. Long-term efficacy after [E1-, polymerase-] adenovirus-mediated transfer of human acid-alpha-glucosidase gene into glycogen storage disease type II knockout mice. Hum Gene Ther 12 (2001), 955–965.
45. 45 Khanna, R, Flanagan, JJ, Feng, J, Soska, R, Frascella, M, Pellegrino, LJ, et al. The pharmacological chaperone AT2220 increases recombinant human acid α-glucosidase uptake and glycogen reduction in a mouse model of Pompe disease. PLoS One, 7, 2012, e40776.
46. 46 van Gelder, MKC, Ozkan, L, Plug, I, Reuser, A, van der Ploeg, A, Antibody formation to enzyme therapy in classic infantile Pompe disease: implications of patient age. BMC Musculoskelet Disord, 14 (suppl 2), 2013, 18.
47. 47 Franco, LM, Sun, B, Yang, X, Bird, A, Zhang, H, Schneider, A, et al. Evasion of immune responses to introduced human acid alpha-glucosidase by liver-restricted expression in glycogen storage disease type II. Mol Ther 12 (2005), 876–884.
48. 48 Zhang, P, Sun, B, Osada, T, Rodriguiz, R, Yang, XY, Luo, X, et al. Immunodominant liver-specific expression suppresses transgene-directed immune responses in murine pompe disease. Hum Gene Ther 23 (2012), 460–472.
49. 49 Sun, B, Bird, A, Young, SP, Kishnani, PS, Chen, YT, Koeberl, DD, Enhanced response to enzyme replacement therapy in Pompe disease after the induction of immune tolerance. Am J Hum Genet 81 (2007), 1042–1049.
50. 50 Sun, B, Kulis, MD, Young, SP, Hobeika, AC, Li, S, Bird, A, et al. Immunomodulatory gene therapy prevents antibody formation and lethal hypersensitivity reactions in murine pompe disease. Mol Ther 18 (2010), 353–360.
51. 51 Han, SO, Li, S, Brooks, ED, Masat, E, Leborgne, C, Banugaria, S, et al. Enhanced efficacy from gene therapy in pompe disease using coreceptor blockade. Hum Gene Ther 26 (2015), 26–35.
52. 52 Zolotukhin, S, Potter, M, Zolotukhin, I, Sakai, Y, Loiler, S, Fraites, TJ Jr, et al. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28 (2002), 158–167.
53. 53 Fraites, TJ Jr, Schleissing, MR, Shanely, RA, Walter, GA, Cloutier, DA, Zolotukhin, I, et al. Correction of the enzymatic and functional deficits in a model of Pompe disease using adeno-associated virus vectors. Mol Ther 5:5 Pt 1 (2002), 571–578.
54. 54 Mah, C, Pacak, CA, Cresawn, KO, Deruisseau, LR, Germain, S, Lewis, MA, et al. Physiological correction of Pompe disease by systemic delivery of adeno-associated virus serotype 1 vectors. Mol Ther 15 (2007), 501–507.