Development of rAAV2-CFTR: History of the First rAAV Vector Product to be Used in Humans

Human Gene Therapy Methods

Volumn 27, Issue 2, 2016, Pages 49-58

  Loring, Heather S ^a   Elmallah, Mai K ^a   Flotte, Terence R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA; PARVOVIRUS VECTOR; RECOMBINANT ADENOASSOCIATED VIRUS VECTOR; UNCLASSIFIED DRUG;

AEROSOL; ANTROSTOMY; CHLORIDE TRANSPORT; CLINICAL EFFECTIVENESS; COMPARATIVE STUDY; CYSTIC FIBROSIS; DRUG BINDING; GENE REPLACEMENT THERAPY; GENE THERAPY; GENE TRANSFER; HISTORY OF MEDICINE; HUMAN; HUMORAL IMMUNITY; LUNG ALVEOLUS EPITHELIUM; LUNG DISEASE; MAXILLARY SINUS; NONHUMAN; NOSE MUCOSA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; RESPIRATORY EPITHELIUM; REVIEW; SEROTYPE; SURGERY; VIRAL GENE DELIVERY SYSTEM; VIRAL TROPISM; ANIMAL; DEPENDOPARVOVIRUS; GENE VECTOR; GENETICS; RESPIRATORY MUCOSA;

ANIMALS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEPENDOVIRUS; GENETIC THERAPY; GENETIC VECTORS; HUMANS; RESPIRATORY MUCOSA;

EID: 84964888283     PISSN: 19466536     EISSN: 19466544     Source Type: Journal    
DOI: 10.1089/hgtb.2015.150     Document Type: Review

References (61)

1. Di Sant'Agnese PA, Darling RC, Perera GA, et al. Abnormal electrolyte composition of sweat in cystic fibrosis of the pancreas; clinical significance and relationship to the disease. Pediatrics 1953;12:549-563.
2. Flotte TR, Carter BJ. Adeno-associated virus vectors for gene therapy of cystic fibrosis. Methods Enzymol 1998;292:717-732.
3. Flotte TR. Gene therapy for cystic fibrosis. Curr Opin Mol Ther 1999;1:510-516.
4. Davis PB. Cystic fibrosis since 1938. Am J Resp Crit Care Med 2006;173:475-482.
5. Kerem B, Rommens JM, Buchanan JA, et al. Identification of the cystic fibrosis gene: Genetic analysis. Science 1989;245:1073-1080.
6. Riordan JR, Rommens JM, Kerem B, et al. Identification of the cystic fibrosis gene: Cloning and characterization of complementary DNA. Science 1989;245:1066-1073.
7. Rommens JM, Iannuzzi MC, Kerem B, et al. Identification of the cystic fibrosis gene: Chromosome walking and jumping. Science 1989;245:1059-1065.
8. Egan M, Flotte T, Afione S, et al. Defective regulation of outwardly rectifying Cl-channels by protein kinase A corrected by insertion of CFTR. Nature 1992;358:581-584.
9. Flotte TR, Carter BJ. In vivo gene therapy with adeno-associated virus vectors for cystic fibrosis. Adv Pharmacol 1997;40:85-101.
10. Carroll TP, Morales MM, Fulmer SB, et al. Alternate translation initiation codons can create functional forms of cystic fibrosis transmembrane conductance regulator. J Biol Chem 1995;270:11941-11946.
11. Cutting GR. Spectrum of mutations in cystic fibrosis. J Bioenerg Biomembr 1993;25:7-10.
12. Swiatecka-Urban A, Brown A, Moreau-Marquis S, et al. The short apical membrane half-life of rescued {Delta}F508-cystic fibrosis transmembrane conductance regulator (CFTR) results from accelerated endocytosis of {Delta}F508-CFTR in polarized human airway epithelial cells. J Biol Chem 2005;280:36762-36772.
13. Rowe SM, Miller S, Sorscher EJ. Cystic fibrosis. N Engl J Med 2005;352:1992-2001.
14. Carter BJ, Flotte TR. Development of adenoassociated virus vectors for gene therapy of cystic fibrosis. Curr Top Microbiol Immunol 1996;218:119-144.
15. Mueller C, Torrez D, Braag S, et al. Partial correction of the CFTR-dependent ABPA mouse model with recombinant adeno-associated virus gene transfer of truncated CFTR gene. J Gene Med 2008;10:51-60.
16. MacLusky IB, Gold R, Corey M, et al. Long-term effects of inhaled tobramycin in patients with cystic fibrosis colonized with Pseudomonas aeruginosa. Pediatr Pulmonol 1989;7:42-48.
17. FitzSimmons SC. The changing epidemiology of cystic fibrosis. Curr Probl Pediatr 1994;24:171-179.
18. Flotte TR, Carter BJ. Adeno-associated virus vectors for gene therapy. Gene Ther 1995;2:357-362.
19. Cutting GR. Cystic fibrosis genetics: From molecular understanding to clinical application. Nat Rev Genet 2015;16:45-56.
20. Pohl K, Hayes E, Keenan J, et al. A neutrophil intrinsic impairment affecting Rab27a and de-granulation in cystic fibrosis is corrected by CFTR potentiator therapy. Blood 2014;124:999-1009.
21. Moriceau S, Lenoir G, Witko-Sarsat V. In cystic fibrosis homozygotes and heterozygotes, neutrophil apoptosis is delayed and modulated by diamide or roscovitine: Evidence for an innate neutrophil disturbance. J Innate Immun 2010;2: 260-266.
22. Yu H, Zeidan YH, Wu BX, et al. Defective acid sphingomyelinase pathway with Pseudomonas aeruginosa infection in cystic fibrosis. Am J Resp Cell Mol Biol 2009;41:367-375.
23. Martino AT, Mueller C, Braag S, et al. Nglycosylation augmentation of the cystic fibrosis epithelium improves Pseudomonas aeruginosa clearance. Am J Resp Cell Mol Biol 2011;44:824-830.
24. Stalvey MS, Brusko TM, Mueller C, et al. CFTR mutations impart elevated immune reactivity in a murine model of cystic fibrosis related diabetes. Cytokine 2008;44:154-159.
25. Ramsey BW, Davies J, McElvaney NG, et al. A CFTR potentiator in patients with cystic fibrosis and the G551D mutation. N Engl J Med 2011;365:1663-1672.
26. Wainwright CE, Elborn JS, Ramsey BW, et al. Lumacaftor-Ivacaftor in patients with cystic fibrosis homozygous for Phe508del CFTR. N Engl J Med 2015;373:220-231.
27. Rich DP, Anderson MP, Gregory RJ, et al. Expression of cystic fibrosis transmembrane conductance regulator corrects defective chloride channel regulation in cystic fibrosis airway epithelial cells. Nature 1990;347:358-363.
28. Drumm ML, Pope HA, Cliff WH, et al. Correction of the cystic fibrosis defect in vitro by retrovirusmediated gene transfer. Cell 1990;62:1227-1233.
29. Kartner N, Hanrahan JW, Jensen TJ, et al. Expression of the cystic fibrosis gene in nonepithelial invertebrate cells produces a regulated anion conductance. Cell 1991;64:681-691.
30. Carter BJ, Antoni BA, Klessig DF. Adenovirus containing a deletion of the early region 2A gene allows growth of adeno-associated virus with decreased efficiency. Virology 1992;191:473-476.
31. Flotte TR, Afione SA, Conrad C, et al. Stable in vivo expression of the cystic fibrosis transmembrane conductance regulator with an adenoassociated virus vector. Proc Natl Acad Sci USA 1993;90:10613-10617.
32. Flotte TR, Afione SA, Solow R, et al. Expression of the cystic fibrosis transmembrane conductance regulator from a novel adeno-associated virus promoter. J Biol Chem 1993;268:3781-3790.
33. Flotte TR, Schwiebert EM, Zeitlin PL, et al. Correlation between DNA transfer and cystic fibrosis airway epithelial cell correction after recombinant adeno-associated virus serotype 2 gene therapy. Hum Gene Ther 2005;16:921-928.
34. Johnson LG, Olsen JC, Sarkadi B, et al. Efficiency of gene transfer for restoration of normal airway epithelial function in cystic fibrosis. Nat Genet 1992;2:21-25.
35. Flotte TR, Afione SA, Zeitlin PL. Adeno-associated virus vector gene expression occurs in nondividing cells in the absence of vector DNA integration. Am J Resp Cell Mol Biol 1994;11:517-521.
36. Conrad CK, Allen SS, Afione SA, et al. Safety of single-dose administration of an adenoassociated virus (AAV)-CFTR vector in the primate lung. Gene Ther 1996;3:658-668.
37. Afione SA, Conrad CK, Kearns WG, et al. In vivo model of adeno-associated virus vector persistence and rescue. J Virol 1996;70:3235-3241.
38. Kotin RM, Siniscalco M, Samulski RJ, et al. Sitespecific integration by adeno-associated virus. Proc Natl Acad Sci USA 1990;87:2211-2215.
39. Kearns WG, Afione SA, Fulmer SB, et al. Recombinant adeno-associated virus (AAV-CFTR) vectors do not integrate in a site-specific fashion in an immortalized epithelial cell line. Gene Ther 1996;3:748-755.
40. Sirninger J, Muller C, Braag S, et al. Functional characterization of a recombinant adeno-associated virus 5-pseudotyped cystic fibrosis transmembrane conductance regulator vector. Hum Gene Ther 2004; 15:832-841.
41. Rubenstein RC, McVeigh U, Flotte TR, et al. CFTR gene transduction in neonatal rabbits using an adeno-associated virus (AAV) vector. Gene Ther 1997;4:384-392.
42. Beck SE, Jones LA, Chesnut K, et al. Repeated delivery of adeno-associated virus vectors to the rabbit airway. J Virol 1999;73:9446-9455.
43. Beck SE, Laube BL, Barberena CI, et al. Deposition and expression of aerosolized rAAV vectors in the lungs of Rhesus macaques. Mol Ther 2002;6:546-554.
44. Flotte TR, Zeitlin PL, Reynolds TC, et al. Phase I trial of intranasal and endobronchial administration of a recombinant adeno-associated virus serotype 2 (rAAV2)-CFTR vector in adult cystic fibrosis patients: A two-part clinical study. Hum Gene Ther 2003;14:1079-1088.
45. Fischer AC, Smith CI, Cebotaru L, et al. Expression of a truncated cystic fibrosis transmembrane conductance regulator with an AAV5-pseudotyped vector in primates. Mol Ther 2007;15:756-763.
46. Virella-Lowell I, Zusman B, Foust K, et al. Enhancing rAAV vector expression in the lung. J Gene Med 2005;7:842-850.
47. Zabner J, Seiler M, Walters R, et al. Adenoassociated virus type 5 (AAV5) but not AAV2 binds to the apical surfaces of airway epithelia and facilitates gene transfer. J Virol 2000;74:3852-3858.
48. Flotte TR, Fischer AC, Goetzmann J, et al. Dual reporter comparative indexing of rAAV pseudotyped vectors in chimpanzee airway. Mol Ther 2010;18:594-600.
49. Duan D, Yue Y, Yan Z, et al. Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 2000;105:1573-1587.
50. Liu X, Luo M, Trygg C, et al. Biological differences in rAAV transduction of airway epithelia in humans and in Old World non-human primates. Mol Ther 2007;15:2114-2123.
51. Liu X, Yan Z, Luo M, et al. Species-specific differences in mouse and human airway epithelial biology of recombinant adeno-associated virus transduction. Am J Resp Cell Mol Biol 2006;34: 56-64.
52. Flotte T, Carter B, Conrad C, et al. A phase I study of an adeno-associated virus-CFTR gene vector in adult CF patients with mild lung disease. Hum Gene Ther 1996;7:1145-1159.
53. Virella-Lowell I, Poirier A, Chesnut KA, et al. Inhibition of recombinant adeno-associated virus (rAAV) transduction by bronchial secretions from cystic fibrosis patients. Gene Ther 2000;7:1783-1789.
54. Fasbender A, Zabner J, Zeiher BG, et al. A low rate of cell proliferation and reduced DNA uptake limit cationic lipid-mediated gene transfer to primary cultures of ciliated human airway epithelia. Gene Ther 1997;4:1173-1180.
55. Wagner JA, Reynolds T, Moran ML, et al. Efficient and persistent gene transfer of AAV-CFTR in maxillary sinus. Lancet 1998;351:1702-1703.
56. Wagner JA, Messner AH, Moran ML, et al. Safety and biological efficacy of an adeno-associated virus vector-cystic fibrosis transmembrane regulator (AAV-CFTR) in the cystic fibrosis maxillary sinus. Laryngoscope 1999;109:266-274.
57. Wagner JA, Nepomuceno IB, Messner AH, et al. A phase II, double-blind, randomized, placebocontrolled clinical trial of tgAAVCF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum Gene Ther 2002;13:1349-1359.
58. Moss RB, Rodman D, Spencer LT, et al. Repeated adeno-associated virus serotype 2 aerosolmediated cystic fibrosis transmembrane regulator gene transfer to the lungs of patients with cystic fibrosis: A multicenter, double-blind, placebocontrolled trial. Chest 2004;125:509-521.
59. Moss RB, Milla C, Colombo J, et al. Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: A randomized placebo-controlled phase 2B trial. Hum Gene Ther 2007;18:726-732.
60. Armstrong DK, Cunningham S, Davies JC, et al. Gene therapy in cystic fibrosis. Arch Disease Child 2014;99:465-468.
61. Schwank G, Koo BK, Sasselli V, et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 2013;13:653-658.