Postentry processing of recombinant adeno-associated virus type 1 and transduction of the ferret lung are altered by a factor in airway secretions

Human Gene Therapy

Volumn 24, Issue 9, 2013, Pages 786-796

  Yan, Ziying ^a   Sun, Xingshen ^a   Evans, Idil A ^a   Tyler, Scott R ^a   Song, Yi ^a   Liu, Xiaoming ^a   Sui, Hongshu ^a   Engelhardt, John F ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR; PROTEASOME; PROTEASOME INHIBITOR; RECOMBINANT ADENOASSOCIATED VIRUS TYPE 1 VECTOR; UNCLASSIFIED DRUG;

AIRWAY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODILY SECRETIONS; CYSTIC FIBROSIS; FERRET; HELA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG; LUNG INFECTION; NONHUMAN; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; THERMOSTABILITY; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME;

ANIMALS; CELL LINE; CYSTIC FIBROSIS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; FERRETS; GENETIC THERAPY; GENETIC VECTORS; HELA CELLS; HUMANS; LUNG; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; RESPIRATORY MUCOSA; TRANSDUCTION, GENETIC; VIRUS INTERNALIZATION;

EID: 84883725341     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2013.137     Document Type: Article

References (53)

1. Aitken, M.L., Moss, R.B., Waltz, D.A., et al. (2001). A phase I study of aerosolized administration of tgAAVCF to cystic fibrosis subjects with mild lung disease. Hum. Gene Ther 12, 1907-1916.
2. Auricchio, A., O'Connor, E., Weiner, D., et al. (2002). Noninvasive gene transfer to the lung for systemic delivery of therapeutic proteins. J. Clin. Invest. 110, 499-504.
3. Bell, C.L., Vandenberghe, L.H., Bell, P., et al. (2011). The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J. Clin. Invest. 121, 2427-2435.
4. Brennan, K., and Bowie, A.G. (2010). Activation of host pattern recognition receptors by viruses. Curr. Opin. Microbiol. 13, 503-507.
5. Carter, B.J. (2005). Adeno-associated virus vectors in clinical trials. Hum. Gene Ther. 16, 541-550.
6. Denby, L., Nicklin, S.A., and Baker, A.H. (2005). Adeno-associated virus (AAV)-7 and-8 poorly transduce vascular endothelial cells and are sensitive to proteasomal degradation. Gene Ther. 12, 1534-1538.
7. Diamond, G., Legarda, D., and Ryan, L.K. (2000). The innate immune response of the respiratory epithelium. Immunol. Rev. 173, 27-38.
8. Ding, W., Zhang, L.N., Yeaman, C., and Engelhardt, J.F. (2006). rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol. Ther. 13, 671-682.
9. Ding, J., Chou, Y.Y., and Chang, T.L. (2009). Defensins in viral infections. J. Innate Immun. 1, 413-420.
10. Driskell, R.A., and Engelhardt, J.F. (2003). Current status of gene therapy for inherited lung diseases. Annu. Rev. Physiol. 65, 585-612.
11. Duan, D., Yue, Y., Yan, Z., et al. (1998). Polarity influences the efficiency of recombinant adenoassociated virus infection in differentiated airway epithelia. Hum. Gene Ther. 9, 2761-2776.
12. Duan, D., Yue, Y., Yan, Z., et al. (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adenoassociated virus. J. Clin. Invest. 105, 1573-1587.
13. Faure, M., and Rabourdin-Combe, C. (2011). Innate immunity modulation in virus entry. Curr. Opin. Virol. 1, 6-12.
14. Finn, J.D., Hui, D., Downey, H.D., et al. (2010). Proteasome inhibitors decrease AAV2 capsid derived peptide epitope presentation on MHC class I following transduction. Mol. Ther. 18, 135-142.
15. Fisher, J.T., Zhang, Y., and Engelhardt, J.F. (2011). Comparative biology of cystic fibrosis animal models. Methods Mol. Biol. 742, 311-334.
16. Flotte, T.R. (2001). Recombinant adeno-associated virus vectors for cystic fibrosis gene therapy. Curr. Opin. Mol. Ther. 3, 497-502.
17. Flotte, T.R., Fischer, A.C., Goetzmann, J., et al. (2010). Dual reporter comparative indexing of rAAV pseudotyped vectors in chimpanzee airway. Mol. Ther. 18, 594-600.
18. Gaiha, G.D., Dong, T., Palaniyar, N., et al. (2008). Surfactant protein a binds to HIV and inhibits direct infection of CD4( + ) cells, but enhances dendritic cell-mediated viral transfer. J. Immunol. 181, 601-609.
19. Gao, G., and Luo, H. (2006). The ubiquitin-proteasome pathway in viral infections. Can. J. Physiol. Pharmacol. 84, 5-14.
20. Griesenbach, U., and Alton, E.W. (2009). Gene transfer to the lung: lessons learned from more than 2 decades of CF gene therapy. Adv. Drug Deliv. Rev. 61, 128-139.
21. Griesenbach, U., Inoue, M., Hasegawa, M., and Alton, E.W. (2010). Viral vectors for cystic fibrosis gene therapy: what does the future hold? Virus Adaptation Treat. 2, 159-171.
22. Grubb, B.R., and Boucher, R.C. (1999). Pathophysiology of genetargeted mouse models for cystic fibrosis. Physiol. Rev. 79, S193-S214.
23. Guilbault, C., Saeed, Z., Downey, G.P., and Radzioch, D. (2007). Cystic fibrosis mouse models. Am. J. Respir. Cell Mol. Biol. 36, 1-7.
24. Halbert, C.L., Allen, J.M., and Miller, A.D. (2001). Adeno-associated virus type 6 (AAV6) vectors mediate efficient transduction of airway epithelial cells in mouse lungs compared to that of AAV2 vectors. J. Virol. 75, 6615-6624.
25. Jennings, K., Miyamae, T., Traister, R., et al. (2005). Proteasome inhibition enhances AAV-mediated transgene expression in human synoviocytes in vitro and in vivo. Mol. Ther. 11, 600-607.
26. Keiser, N.W., and Engelhardt, J.F. (2011). New animal models of cystic fibrosis: what are they teaching us? Curr. Opin. Pulm. Med. 17, 478-483.
27. Knowles, M.R., and Boucher, R.C. (2002). Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109, 571-577.
28. Leigh, M.W., Gambling, T.M., Carson, J.L., et al. (1986). Postnatal development of tracheal surface epithelium and submucosal glands in the ferret. Exp. Lung Res. 10, 153-169.
29. Li, W., Zhang, L., Wu, Z., et al. (2011). AAV-6 mediated efficient transduction of mouse lower airways. Virology 417, 327-333.
30. Liu, X., Driskell, R.R., and Engelhardt, J.F. (2004). Airway glandular development and stem cells. Curr. Top. Dev. Biol. 64, 33-56.
31. Liu, X., Yan, Z., Luo, M., and Engelhardt, J.F. (2006). Speciesspecific differences in mouse and human airway epithelial biology of recombinant adeno-associated virus transduction. Am. J. Respir. Cell Mol. Biol. 34, 56-64.
32. Liu, X., Luo, M., Guo, C., et al. (2007a). Comparative biology of rAAV transduction in ferret, pig and human airway epithelia. Gene Ther. 14, 1543-1548.
33. Liu, X., Luo, M., Zhang, L., et al. (2007b). Bioelectric properties of chloride channels in human, pig, ferret, and mouse airway epithelia. Am. J. Respir. Cell Mol. Biol. 36, 313-323.
34. Matalon, S., and Wright, J.R. (2004). Surfactant proteins and inflammation-The Yin and Yang. Am. J. Respir. Cell Mol. Biol. 31, 585-586.
35. Monahan, P.E., Lothrop, C.D., Sun, J., et al. (2010). Proteasome inhibitors enhance gene delivery by AAV virus vectors expressing large genomes in hemophilia mouse and dog models: a strategy for broad clinical application. Mol. Ther. 18, 1907-1916.
36. Moss, R.B., Milla, C., Colombo, J., et al. (2007). Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: a randomized placebo-controlled phase 2B trial. Hum. Gene Ther. 18, 726-732.
37. Ros, C., and Kempf, C. (2004). The ubiquitin-proteasome machinery is essential for nuclear translocation of incoming minute virus of mice. Virology 324, 350-360.
38. Rowe, S.M., Miller, S., and Sorscher, E.J. (2005). Cystic fibrosis. N. Engl. J. Med. 352, 1992-2001.
39. See, H., and Wark, P. (2008). Innate immune response to viral infection of the lungs. Paediatr. Respir. Rev. 9, 243-250.
40. Sun, X., Yan, Z., Yi, Y., et al. (2008). Adeno-associated virustargeted disruption of the CFTR gene in cloned ferrets. J. Clin. Invest. 118, 1578-1583.
41. Sun, X., Sui, H., Fisher, J.T., et al. (2010). Disease phenotype of a ferret CFTR-knockout model of cystic fibrosis. J. Clin. Invest. 120, 3149-3160.
42. Virella-Lowell, I., Poirier, A., Chesnut, K.A., et al. (2000). Inhibition of recombinant adeno-associated virus (rAAV) transduction by bronchial secretions from cystic fibrosis patients. Gene Ther. 7, 1783-1789.
43. Viswanathan, K., Fruh, K., and Defilippis, V. (2010). Viral hijacking of the host ubiquitin system to evade interferon responses. Curr. Opin. Microbiol. 13, 517-523.
44. Wagner, J.A., Nepomuceno, I.B., Messner, A.H., et al. (2002). A phase II, double-blind, randomized, placebo-controlled clinical trial of tgAAVCF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum. Gene Ther. 13, 1349-1359.
45. Welsh, M.J., Ramsey, B.W., Accurso, F., and Cutting, G.R. (2001). The Metabolic and Molecular Basis of Inherited Disease (McGraw-Hill, New York).
46. Weyer, C., Sabat, R., Wissel, H., et al. (2000). Surfactant protein A binding to cytomegalovirus proteins enhances virus entry into rat lung cells. Am. J. Respir. Cell Mol. Biol. 23, 71-78.
47. Wilke, M., Buijs-Offerman, R.M., Aarbiou, J., et al. (2011). Mouse models of cystic fibrosis: phenotypic analysis and research applications. J. Cyst. Fibros. 10 Suppl 2, S152-S171.
48. Yan, Z., Zak, R., Luxton, G.W., et al. (2002). Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J. Virol. 76, 2043-2053.
49. Yan, Z., Zak, R., Zhang, Y., et al. (2004). Distinct classes of proteasome-modulating agents cooperatively augment recombinant adeno-associated virus type 2 and type 5-mediated transduction from the apical surfaces of human airway epithelia. J. Virol. 78, 2863-2874.
50. Yan, Z., Lei-Butters, D.C., Liu, X., et al. (2006). Unique biologic properties of recombinant AAV1 transduction in polarized human airway epithelia. J. Biol. Chem. 281, 29684-29692.
51. Yan, Z., Lei-Butters, D.C., Keiser, N.W., and Engelhardt, J.F. (2013). Distinct transduction difference between adenoassociated virus type 1 and type 6 vectors in human polarized airway epithelia. Gene Ther. 20, 328-337.
52. Yang, J., Zhou, W., Zhang, Y., et al. (1999). Concatamerization of adeno-associated virus circular genomes occurs through intermolecular recombination. J. Virol. 73, 9468-9477.
53. Yu, G.Y., and Lai, M.M. (2005). The ubiquitin-proteasome system facilitates the transfer of murine coronavirus from endosome to cytoplasm during virus entry. J. Virol. 79, 644-648.