Cystic fibrosis gene therapy: A mutationindependent treatment

Current Opinion in Pulmonary Medicine

Volumn 22, Issue 6, 2016, Pages 602-609

  Griesenbach, Uta ^a   Davies, Jane C ^a   Alton, Eric ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cystic fibrosis; Cystic fibrosis transmembrane conductance regulator (CFTR); Gene therapy; Gene transfer; Lung

Indexed keywords

LENTIVIRUS VECTOR;

AIRWAY EPITHELIAL CELL; CYSTIC FIBROSIS; FIRST IN HUMAN STUDY; GENE MUTATION; GENE THERAPY; GENE TRANSFER; HUMAN; LUNG FIBROSIS; LUNG FUNCTION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; OUTCOME ASSESSMENT; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; GENE VECTOR; LUNG; MUTATION;

CYSTIC FIBROSIS; GENETIC THERAPY; GENETIC VECTORS; HUMANS; LUNG; MUTATION;

EID: 84984697904     PISSN: 10705287     EISSN: 15316971     Source Type: Journal    
DOI: 10.1097/MCP.0000000000000327     Document Type: Review

References (47)

1. Boucher RC. Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu Rev Med 2007; 58:157-170.
2. Stoltz DA, Meyerholz DK, Welsh MJ. Origins of cystic fibrosis lung disease. N Engl J Med 2015; 372:1574-1575.
3. Shamsuddin AK, Quinton PM. Native small airways secrete bicarbonate. Am J Respir Cell Mol Biol 2014; 50:796-804.
4. Wang Y, Wrennall JA, Cai Z, et al. Understanding how cystic fibrosis mutations disrupt CFTR function: from single molecules to animal models. Int J Biochem Cell Biol 2014; 52:47-57.
5. McKone EF, Borowitz D, Drevinek P, et al. Long-term safety and efficacy of ivacaftor in patients with cystic fibrosis who have the Gly551Asp-CFTR mutation: a phase 3, open-label extension study (PERSIST). Lancet Respir Med 2014; 2:902-910.
6. 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.
7. Griesenbach U, Pytel KM, Alton EW. Cystic fibrosis gene therapy in the UK and elsewhere. Hum Gene Ther 2015; 26:266-275.
8. Drumm ML, Pope HA, Cliff WH, et al. Correction of the cystic fibrosis defect in vitro by retrovirus-mediated gene transfer. Cell 1990; 62:1227-1233.
9. Rosenfeld MA, Yoshimura K, Trapnell BC, et al. In vivo transfer of the human cystic fibrosis transmembrane conductance regulator gene to the airway epithelium. Cell 1992; 68:143-155.
10. Hyde SC, Gill DR, Higgins CF, et al. Correction of the ion transport defect in cystic fibrosis transgenic mice by gene therapy. Nature 1993; 362:250-255.
11. Zabner J, Couture LA, Gregory RJ, et al. Adenovirus-mediated gene transfer transiently corrects the chloride transport defect in nasal epithelia of patients with cystic fibrosis. Cell 1993; 75:207-216.
12. Crystal RG, McElvaney NG, Rosenfeld MA, et al. Administration of an adenovirus containing the human CFTR cDNA to the respiratory tract of individuals with cystic fibrosis. Nat Genet 1994; 8:42-51.
13. Caplen NJ, Alton EW, Middleton PG, et al. Liposome-mediated CFTR gene transfer to the nasal epithelium of patients with cystic fibrosis. Nat Med 1995; 1:39-46.
14. Alton EW, Stern M, Farley R, et al. Cationic lipid-mediated CFTR gene transfer to the lungs and nose of patients with cystic fibrosis: a double-blind placebo-controlled trial. Lancet 1999; 353:947-954.
15. Alton EW, Armstrong DK, Ashby D, et al. Repeated nebulisation of nonviral CFTR gene therapy in patients with cystic fibrosis: a randomised, double-blind, placebo-controlled, phase 2b trial. Lancet Respir Med 2015; 3:684-691.
16. Stern M, Ulrich K, Geddes DM, Alton EW. Poly (D, L-lactide-co-glycolide)/DNA microspheres to facilitate prolonged transgene expression in airway epithelium in vitro, ex vivo and in vivo. Gene Ther 2003; 10:1282-1288.
17. Yonemitsu Y, Kitson C, Ferrari S, et al. Efficient gene transfer to airway epithelium using recombinant Sendai virus. Nat Biotechnol 2000; 18:970-973.
18. Schuster BS, Kim AJ, Kays JC, et al. Overcoming the cystic fibrosis sputum barrier to leading adeno-associated virus gene therapy vectors. Mol Ther 2014; 22:1484-1493.
19. Xia E, Munegowda MA, Cao H, Hu J. Lung gene therapy: how to capture illumination from the light already present in the tunnel. Genes Dis 2014; 1:40-52.
20. Hyde SC, Southern KW, Gileadi U, et al. Repeat administration of DNA/liposomes to the nasal epithelium of patients with cystic fibrosis. Gene Ther 2000; 7:1156-1165.
21. McLachlan G, Davidson H, Holder E, et al. Preclinical evaluation of three nonviral gene transfer agents for cystic fibrosis after aerosol delivery to the ovine lung. Gene Ther 2011; 18:996-1005.
22. Ruiz FE, Clancy JP, Perricone MA, et al. A clinical inflammatory syndrome attributable to aerosolized lipid-DNA administration in cystic fibrosis. Hum Gene Ther 2001; 12:751-761.
23. Hyde SC, Pringle IA, Abdullah S, et al. CpG-free plasmids confer reduced inflammation and sustained pulmonary gene expression. Nat Biotechnol 2008; 26:549-551.
24. Alton EW, Boyd AC, Cheng SH, et al. Toxicology study assessing efficacy and safety of repeated administration of lipid/DNA complexes to mouse lung. Gene Ther 2014; 21:89-95.
25. Alton EW, Baker A, Baker E, et al. The safety profile of a cationic lipid-mediated cystic fibrosis gene transfer agent following repeated monthly aerosol administration to sheep. Biomaterials 2013; 34:10267-10277.
26. Alton EW, Boyd AC, Porteous DJ, et al. A phase I/IIa safety and efficacy study of nebulized liposome-mediated gene therapy for cystic fibrosis supports a multidose trial. Am J Respir Crit Care Med 2015; 192:1389-1392.
27. Rivat C, Santilli G, Gaspar HB, Thrasher AJ. Gene therapy for primary immunodeficiencies. Hum Gene Ther 2012; 23:668-675.
28. Aiuti A, Cossu G, de FP, et al. The committee for advanced therapies' of the European Medicines Agency reflection paper on management of clinical risks deriving from insertional mutagenesis. Hum Gene Ther Clin Dev 2013; 24:47-54.
29. Biffi A, Montini E, Lorioli L, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 2013; 341:1233158.
30. Palfi S, Gurruchaga JM, Ralph GS, et al. Long-term safety and tolerability of ProSavin, a lentiviral vector-based gene therapy for Parkinson's disease: a dose escalation, open-label, phase 1/2 trial. Lancet 2014; 383:1138-1146.
31. Cmielewski P, Anson DS, Parsons DW. Lysophosphatidylcholine as an adjuvant for lentiviral vector mediated gene transfer to airway epithelium: effect of acyl chain length. Respir Res 2010; 11:84.
32. Sinn PL, Cooney AL, Oakland M, et al. Lentiviral vector gene transfer to porcine airways. Mol Ther Nucleic Acids 2012; 1:e56.
33. Kobinger GP, Weiner DJ, Yu QC, Wilson JM. Filovirus-pseudotyped lentiviral vector can efficiently and stably transduce airway epithelia in vivo. Nat Biotechnol 2001; 19:225-230.
34. Patel M, Giddings AM, Sechelski J, Olsen JC. High efficiency gene transfer to airways of mice using influenza hemagglutinin pseudotyped lentiviral vectors. J Gene Med 2013; 15:51-62.
35. Kobayashi M, Iida A, Ueda Y, Hasegawa M. Pseudotyped lentivirus vectors derived from simian immunodeficiency virus SIVagm with envelope glycopro-teins from paramyxovirus. J Virol 2003; 77:2607-2614.
36. Mitomo K, Griesenbach U, Inoue M, et al. Toward gene therapy for cystic fibrosis using a lentivirus pseudotyped with Sendai virus envelopes. Mol Ther 2010; 18:1173-1182.
37. Griesenbach U, Inoue M, Meng C, et al. Assessment of F/HN-pseudotyped lentivirus as a clinically relevant vector for lung gene therapy. Am J Respir Crit Care Med 2012; 186:846-856.
38. Alton Eric WFW, Beekman Jeffery M, Christopher Boyd A, et al. Preparation for a first-in-man lentivirus trial in cystic fibrosis patients. Thorax 2016. (in press).
39. Griesenbach U, Alton EW. Gene transfer to the lung: lessons learned from more than 2 decades of CF gene therapy. Adv Drug Deliv Rev 2009; 61:128-139.
40. Kariko K, Muramatsu H, Ludwig J, Weissman D. Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, protein-encoding mRNA. Nucleic Acids Res 2011; 39:e142.
41. Kormann MS, Hasenpusch G, Aneja MK, et al. Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 2011; 29:154-157.
42. Lee CM, Flynn R, Hollywood JA, et al. Correction of the DF508 mutation in the cystic fibrosis transmembrane conductance regulator gene by zinc-finger nuclease homology-directed repair. Biores Open Access 2012; 1:99-108.
43. 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.
44. Crane AM, Kramer P, Bui JH, et al. Targeted correction and restored function of the CFTR gene in cystic fibrosis induced pluripotent stem cells. Stem Cell Reports 2015; 4:569-577.
45. Firth AL, Menon T, Parker GS, et al. Functional gene correction for cystic fibrosis in lung epithelial cells generated from patient iPSCs. Cell Rep 2015; 12:1385-1390.
46. Alton EWFW, Boyd AC, Davies JC, et al. Genetic medicines for CF: hype versus reality. Pediatr Pulmonol 2016. (in press).
47. Shoseyov D, Cohen-Cymberknoh M, Wilschanski M. Ataluren for the treatment of cystic fibrosis. Expert Rev Respir Med 2016. [Epub ahead of print]