Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer

Journal of Virology

Volumn 72, Issue 7, 1998, Pages 6014-6023

  Pickles, Raymond J ^a   McCarty, Douglas ^a   Matsui, Hirotoshi ^a   Hart, Pádraig J ^a   Randell, Scott H ^a   Boucher, Richard C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; VIRUS VECTOR;

ADENOVIRUS; ARTICLE; CELL ADHESION; CYSTIC FIBROSIS; GENE TRANSFER; HUMAN; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN BINDING; RESPIRATORY EPITHELIUM; VIRUS VIRULENCE;

EID: 0031777961     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.7.6014-6023.1998     Document Type: Article

References (37)

1. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krivithas, J. S. Hong, M. S. Horowitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
2. Boucher, R. C. 1996. Current status of CF gene therapy. Trends Genet. 12:81-84.
3. Brighton, C. T., and S. M. Albelda. 1992. Identification of cell substratum adhesion receptors of integrins on cultured rat bone cells. J. Orthop. Res. 10:766-773.
4. Comstock, K. E., N. F. Watson, and J. C. Olsen. 1996. Design of retroviral expression vectors, p. 207. In R. Tuan (ed.), Recombinant gene expression protocols. Humana Press, Inc., Totowa, N.J.
5. Crystal, R. G., A. Jaffe, S. Brody, A. Mastrangeli, N. G. McElvaney, M. E. Rosenfeld, C. Chu, C. Danel, J. Hay, and T. Eissa. 1995. A phase I study, in cystic fibrosis patients, of the safety, toxicity, and biological efficacy of a single administration of a replication-deficient, recombinant adenovirus carrying the cDNA of the normal cystic fibrosis transmembrane conductance regulator gene in the lung. Hum. Gene Ther. 6:643-666.
6. Crystal, R. G., N. G. McElvaney, M. A. Rosenfeld, C. Chu, A. Mastrangeli, J. G. Hay, S. L. Brody, H. A. Jaffe, N. T. Eissa, and C. Danel. 1994. Administration of an adenovirus containing the human CFTR cDNA to the respratory tract of individuals with cystic fibrosis. Nat. Genet. 8:42-51.
7. Damke, H., T. Baba, D. E. Warnock, and S. L. Schmid. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934
8. Dupuit, F., J. Zahm, D. Pierrot, S. Brezillion, N. Bonnet, J. Imler, A. Pavirani, and E. Puchelle. 1995. Regenerating cells in the human airway surface epithelium represent preferential targets for recombinant adenovirus. Hum. Gene Ther. 6:1185-1193.
9. Engelhardt, J. F., Y. Yang, L. D. Stratford-Perricaudet, E. D. Allen, K. Kozarsky, M. Perricaudet, J. R. Yankaskas, and J. M. Wilson. 1993. Direct gene transfer of human CFTR into human bronchial epithelia of xenografts with E1-deleted adenoviruses. Nat. Genet. 4:27-34.
10. Fasbender, A., J. Zabner, M. Chillon, T. O. Moninger, A. P. Puga, B. L. Davidson, and M. J. Welsh. 1997. Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer in vitro and in vivo. J. Biol. Chem. 272:6479-6489.
11. Fitzgerald, D. J. P., R. Padamanabhan, I. Pastan, and M. C. Willingham. 1983. Adenovirus-induced release of epidermal growth factor and Pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosi. Cell 32:607-617.
12. Freimuth, P. 1996. A human cell line selected for resistance to adenovirus infection has reduced levels of the virus receptor. J. Virol 70:4081-4085.
13. Goldman, M. J., Q. Su, and J. M. Wilson. 1996. Gradient of RGD-dependent entry of adenoviral vector in nasal and intrapulmonary epithelia: implications for gene therapy of cystic fibrosis. Gene Ther. 3:811-818.
14. 5 integrin is necessary for efficient adenovirus-mediated gene transfer in the human airway. J. Virol. 69:5951-5958.
15. Gray, T. E., K. Guzman, C. W. Davis, L. H. Abdullah, and P. Nettesheim. 1996. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 14:104-112.
16. Greber, U. F., M. Willets, P. Webster, and A. Helenius. 1993. Stepwise dismantling of adenovirus type 2 during entry into cells. Cell 75:477-486.
17. Griffiths, M., X. Huang, J. F. Wu, R. Driscoll, and D. Sheppard. 1997 Inactivation of the b5 integrin subunit gene does not prevent expression of adenovirus genes in mouse airway epithelium. Respir. Crit. Care Med. 155: A459. (Abstract.)
18. Grubb, B. R., R. J. Pickles, H. Ye, J. R. Yankaskas, R. N. Vick, J. F. Engelhardt, J. M. Wilson, L. G. Johnson, and R. C. Boucher. 1994. Inefficient gene transfer by adenovirus vector to cystic fibrosis airway epithelia of mice and humans. Nature 371:802-806.
19. Henry, L. J., D. Xia, M. E. Wilke, J. Deisenhofer, and R. D. Gerard. 1994. Characterization of the knob domain of the adenovirus type 5 fiber protein expressed in Escherichia coli. J. Virol. 68:5239-5246.
20. Hsu, K. L., K. Lonberg-Holm, B. Alstein, and R. L. Crowell. 1988. A monoclonal antibody specific for the cellular receptor for the group B coxsackieviruses. J. Virol. 62:1647-1652.
21. Kaartinen, L., P. Nettesheim, K. B. Adler, and S. H. Randell. 1993. Rat tracheal epithelial cell differentiation in vitro. In Vitro Cell. Dev. Biol. 29:481-492.
22. Lechner, J. F., and M. A. LaVeck. 1985. A serum-free method for culturing normal human bronchial epithelial cells at clonal density. J. Tissue Cult. Methods 9:43-48.
23. Leopold, P. L., B. Ferris, I. Grinberg, S. Worgall, N. R. Hackett, and R. G. Crystal. 1998. Fluorescent virions: dynamic tracking of the pathway of adenoviral gene transfer vectors in living cells. Hum. Gene Ther. 9:367-378.
24. Matsui, H., L. G. Johnson, S. H. Randell, and R. C. Boucher. 1997. Loss of binding and entry of liposomal-DNA complexes decreases transfection efficiency in differentiated airway epithelial cells. J. Biol. Chem. 272:1117-1126.
25. Olsen, J. Personal communication.
26. Pickles, R. J., P. M. Barker, H. Ye, and R. C. Boucher. 1996. Efficient adenovirus-mediated gene transfer to basal but not columnar cells of cartilaginous airway epithelia. Hum. Gene Ther. 7:921-931.
27. Pickles, R. J., D. McCarty, S. H. Randell, and R. C. Boucher. 1997. Internalisation, not attachment is the rate limiting step responsible for the inefficiency of adenoviral-mediated gene transfer to well differentiated respiratory epithelium. Pediatr. Pulmonol. 14:A193. (Abstract.)
28. Piedimonte, G., R. J. Pickles, J. R. Lehmann, D. McCarty, D. L. Costa, and R. C. Boucher. 1997. Replication-deficient adenoviral vector for gene transfer potentiates airway neurogenic inflammation. Am. J. Respir. Cell Mol. Biol. 16:250-258.
29. Robinson, G., and T. Gray. 1996. Electron microscopy 2: practical procedures, p. 585-627. In J. D. Bancroft and A. Stevens (ed.), Theory and practice of histological techniques. Churchill Livingstone, Inc., New York, N.Y.
30. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94:3352-3356.
31. Varga, M. J., C. Weibull, and E. Everitt. 1991. Infectious entry pathway of adenovirus type 2. J. Virol. 65:6061-6070.
32. von Bonsdorff, C., S. D. Fuller, and K. Simons. 1985. Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitro-cellulose filters. EMBO J. 4:2781-2792.
33. 5 promote adenovirus internalisation but not virus attachment. Cell 73:309-319.
34. Wickham, T. J., P. W. Roelvink, D. E. Brough, and I. Kovesdi. 1996. Adenovirus targeted to heparan-containing receptors increases its gene delivery efficiency to multiple cell-types. Nat. Biotechnol. 14:1570-1573.
35. Wu, R., J. Yankaskas, E. Cheng, M. R. Knowles, and R. C. Boucher. 1985. Growth and differentiation of human nasal epithelial cells in culture. Serum-free, hormone-supplemented medium and proteoglycan synthesis. Am. Rev. Respir. Dis. 132:311-320.
36. Zabner, J., P. Freimuth, A. Puga, A. Fabrega, and M. J. Welsh. 1997. Lack of high affinity fiber receptor activity explains the resistance of ciliated airway epithelia to adenovirus infection. J. Clin. Invest. 100:1144-1149.
37. Zabner, J., B. G. Zeiher, E. Friedman, and M. J. Welsh. 1996. Adenovirus-mediated gene transfer to ciliated airway epithelia requires prolonged incubation times. J. Virol. 70:6994-7003.