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

Journal of Virology

Volumn 78, Issue 6, 2004, Pages 2863-2874

  Yan, Ziying ^a   Zak, Roman ^a   Zhang, Yulong ^a   Ding, Wei ^a   Godwin, Simon ^b   Munson, Keith ^b   Peluso, Richard ^b   Engelhardt, John F ^a  

^a UNIVERSITY OF IOWA   (United States)

^b Targeted Genetics Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACLARUBICIN; ANTHRACYCLINE DERIVATIVE; DOXORUBICIN; N ACETYLLEUCYLLEUCYLNORLEUCINE; PROTEASOME INHIBITOR; TRIPEPTIDYL ALDEHYDE PROTEASOME INHIBITOR; UNCLASSIFIED DRUG;

ADENOVIRUS 2; ADENOVIRUS 5; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POLARITY; CELL TYPE; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE THERAPY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; SEROTYPE; SIGNAL TRANSDUCTION; UBIQUITINATION; VIRUS STRAIN;

ACLARUBICIN; ANIMALS; CELL LINE; CELL POLARITY; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; CYSTIC FIBROSIS; DEPENDOVIRUS; DOXORUBICIN; EPITHELIAL CELLS; GENE THERAPY; HUMANS; LEUPEPTINS; LUNG; MICE; MICE, INBRED C57BL; MULTIENZYME COMPLEXES; PARVOVIRIDAE INFECTIONS; PROTEASOME ENDOPEPTIDASE COMPLEX; RECOMBINATION, GENETIC; TRANSDUCTION, GENETIC;

EID: 1542287505     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.6.2863-2874.2004     Document Type: Article

References (40)

1. Aitken, M. L., R. B. Moss, D. A. Waltz, M. E. Dovey, M. R. Tonelli, S. C. McNamara, R. L. Gibson, B. W. Ramsey, B. J. Carter, and T. C. Reynolds. 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., E. O'Connor, D. Weiner, G. Gao, M. Hildinger, L. Wang, R. Calcedo, and J. Wilson. 2002. Noninvasive gene transfer to the lung for systemic delivery of therapeutic proteins. J. Clin. Investig. 110:499-504.
3. Bals, R., W. Xiao, N. Sang, D. J. Weiner, R. L. Meegalla, and J. M. Wilson. 1999. Transduction of well-differentiated airway epithelium by recombinant adeno-associated virus is limited by vector entry. J. Virol. 73:6085-6088.
4. Bartlett, J. S., R. Wilcher, and R. J. Samulski. 2000. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74: 2777-2785.
5. Berns, K. I., and C. Giraud. 1996. Adeno-associated virus (AAV) vectors in gene therapy. Springer, Berlin, Germany.
6. Burstein, H. J., M. J. Ramirez, W. P. Petros, K. D. Clarke, M. A. Warmuth, P. K. Marcom, U. A. Matulonis, L. M. Parker, L. N. Harris, and E. P. Winer. 1999. Phase I study of Doxil and vinorelbine in metastatic breast cancer. Ann. Oncol. 10:1113-1116.
7. Carter, B. J., H. B. Burnstein, and R. W. Peluso. AAV vectors for gene therapy, in press. Marcel Dekker, Inc., New York, N.Y.
8. Casper, E. S., R. J. Gralla, and C. W. Young. 1981. Clinical phase I study of aclacinomycin A by evaluation of an intermittent intravenous administration schedule. Cancer Res. 41:2417-2420.
9. Davidson, B. L., C. S. Stein, J. A. Heth, I. Martins, R. M. Kotin, T. A. Derksen, J. Zabner, A. Ghodsi, and J. A. Chiorini. 2000. Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc. Natl. Acad. Sci. USA 97:3428-3432.
10. Ding, W., Z. Yan, R. Zak, M. Saavedra, D. M. Rodman, and J. F. Engelhardt. 2003. Second-strand genome conversion of adeno-associated virus type 2 (AAV-2) and AAV-5 is not rate limiting following apical infection of polarized human airway epithelia. J. Virol. 77:7361-7366.
11. Dong, J., M. Naito, T. Tatsuta, H. Seimiya, O. Johdo, and T. Tsuruo. 1995. Difference between the resistance mechanisms of aclacinomycin- and adriamycin-resistant P388 cell lines. Oncol. Res. 7:245-252.
12. Duan, D., Y. Yue, and J. F. Engelhardt. 2002. Adeno-associated virus. Marcel Dekker, Inc., New York, N.Y.
13. Duan, D., Y. Yue, Z. Yan, P. B. McCray, and J. F. Engelhardt. 1998. Polarity influences the efficiency of recombinant adeno-associated virus infection in differentiated airway epithelia. Hum. Gene Ther. 9:2761-2776.
14. Duan, D., Y. Yue, Z. Yan, J. Yang, and J. F. Engelhardt. 2000. Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J. Clin. Investig. 105:1573-1587.
15. Duan, D., Y. Zhang, and J. F. Engelhardt. 1998. Gene delivery to the airway, p. 13.9.1-13.9.34. In N. C. Dracopoli, J. L. Haines, B. R. Korf, D. T. Moir, C. C. Morton, C. E. Seidman, J. G. Seidman, and D. R. Smith (ed.), Current protocols in human genetics. John Wiley & Sons, Inc., New York, N.Y.
16. Figueiredo-Pereira, M. E., W. E. Chen, J. Li, and O. Johdo. 1996. The antitumor drug aclacinomycin A, which inhibits the degradation of ubiquitinated proteins, shows selectivity for the chymotrypsin-like activity of the bovine pituitary 20 S proteasome. J. Biol. Chem. 271:16455-16459.
17. Gabizon, A., H. Shmeeda, and Y. Barenholz. 2003. Pharmacokinetics of pegylated liposomal Doxorubicin: review of animal and human studies. Clin. Pharmacokinet. 42:419-436.
18. Gao, G. P., M. R. Alvira, L. Wang, R. Calcedo, J. Johnston, and J. M. Wilson. 2002. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. USA 99:11854-11859.
19. Hansen, J., K. Qing, H. J. Kwon, C. Mah, and A. Srivastava. 2000. Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J. Virol. 74:992-996.
20. Hansen, J., K. Qing, and A. Srivastava. 2001. Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J. Virol. 75:4080-4090.
21. Kaludov, N., B. Handelman, and J. A. Chiorini. 2002. Scalable purification of adeno-associated virus type 2, 4, or 5 using ion-exchange chromatography. Hum. Gene Ther. 13:1235-1243.
22. Keizer, H. G., H. M. Pinedo, G. J. Schuurhuis, and H. Joenje. 1990. Doxorubicin (adriamycin): a critical review of free radical-dependent mechanisms of cytotoxicity. Pharmacol. Ther. 47:219-231.
23. Kisselev, A. F., T. N. Akopian, K. M. Woo, and A. L. Goldberg. 1999. The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem. 274:3363-3371.
24. Kiyomiya, K., M. Kurebe, H. Nakagawa, and S. Matsuo. 2002. The role of the proteasome in apoptosis induced by anthracycline anticancer agents. Int. J. Oncol. 20:1205-1209.
25. Kiyomiya, K., S. Matsuo, and M. Kurebe. 1998. Proteasome is a carrier to translocate doxorubicin from cytoplasm into nucleus. Life Sci. 62:1853-1860.
26. Lee, D. H., and A. L Goldberg. 1998. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8:397-403.
27. McCarty, D. M., P. E. Monahan, and R. J. Samulski. 2001. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 8:1248-1254.
28. Mellgren, R. L. 1997. Specificities of cell permeant peptidyl inhibitors for the proteinase activities of mu-calpain and the 20 S proteasome. J. Biol. Chem. 272:29899-29903.
29. Muller, I., D. Niethammer, and G. Bruchelt. 1998. Anthracycline-derived chemotherapeutics in apoptosis and free radical cytotoxicity. Int. J. Mol. Med. 1:491-494.
30. Ros, C., C. J. Burckhardt, and C. Kempf. 2002. Cytoplasmic trafficking of minute virus of mice: low-pH requirement, routing to late endosomes, and proteasome interaction. J. Virol. 76:12634-12645.
31. Singal, P. K., and N. Iliskovic. 1998. Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 339:900-905.
32. Stebbing, J., and A. Gaya. 2002. Pegylated liposomal doxorubicin (Caelyx) in recurrent ovarian cancer. Cancer Treat. Rev. 28:121-125.
33. Vinitsky, A., C. Michaud, J. C. Powers, and M. Orlowski. 1992. Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex. Biochemistry 31:9421-9428.
34. Wagner, J. A., A. H. Messner, M. L. Moran, R. Daifuku, K. Kouyama, J. K. Desch, S. Manley, A. M. Norbash, C. K. Conrad, S. Friborg, T. Reynolds, W. B. Guggino, R. B. Moss, B. J. Carter, J. J. Wine, T. R. Flotte, and P. Gardner. 1999. Safety and biological efficacy of an adeno-associated virus vector-cystic fibrosis transmembrane regulator (AAV-CFTR) in the cystic fibrosis maxillary sinus. Laryngoscope 109:266-274.
35. Wagner, J. A., M. L. Moran, A. H. Messner, R. Daifuku, C. K. Conrad, T. Reynolds, W. B. Guggino, R. B. Moss, B. J. Carter, J. J. Wine, T. R. Flotte, and P. Gardner. 1998. A phase I/II study of tgAAV-CF for the treatment of chronic sinusitis in patients with cystic fibrosis. Hum. Gene Ther. 9:889-909.
36. Wagner, J. A., I. B. Nepomuceno, A. H. Messner, M. L. Moran, E. P. Batson, S. Dimiceli, B. W. Brown, J. K. Desch, A. M. Norbash, C. K. Conrad, W. B. Guggino, T. R. Flotte, J. J. Wine, B. J. Carter, T. C. Reynolds, R. B. Moss, and P. Gardner. 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.
37. Xiao, W., K. H. Warrington, Jr., P. Hearing, J. Hughes, and N. Muzyczka. 2002. Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J. Virol. 76:11505-11517.
38. Yan, Z., T. C. Ritchie, D. Duan, and J. F. Engelhardt. 2002. Recombinant AAV-mediated gene delivery using dual vector heterodimerization. Methods Enzymol. 346:334-357.
39. Yan, Z., R. Zak, G. W. Luxton, T. C. Ritchie, U. Bantel-Schaal, and J. F. Engelhardt. 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.
40. Zabner, J., M. Seiler, R. Walters, R. M. Kotin, W. Fulgeras, B. L. Davidson, and J. A. Chiorini. 2000. Adeno-associated virus type 5 (AAV5) but not AAV2 binds to the apical surfaces of airway epithelia and facilitates gene transfer. J. Virol. 74:3852-3858.