Genetic modification of adeno-associated viral vector type 2 capsid enhances gene transfer efficiency in polarized human airway epithelial cells

Human Gene Therapy

Volumn 19, Issue 12, 2008, Pages 1407-1414

  White, April F ^a   Mazur, Marina ^b   Sorscher, Eric J ^b   Zinn, Kurt R ^b   Ponnazhagan, Selvarangan ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOASSOCIATED VIRUS VECTOR TYPE 2; CAPSID PROTEIN; PARVOVIRUS VECTOR; PEPTIDE; THREONYLHISTIDYLALANYLLEUCYLTRYPTOPHYLHISTIDYLTHREONINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; GENE TRANSFER; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; NONHUMAN; RESPIRATORY EPITHELIUM; VIRUS STRAIN;

BASE SEQUENCE; BRONCHI; CAPSID; CELLS, CULTURED; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEPENDOVIRUS; DNA PRIMERS; EPITHELIAL CELLS; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; TRANSDUCTION, GENETIC;

MIRIDAE;

EID: 57749190573     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2008.117     Document Type: Article

References (45)

1. Aitken, M.L., Moss, R.B., Waltz, D.A., Dovey, M.E., Tonelli, M.R., McNamara, S.C., Gibson, R.L., Ramsey, B.W., Carter, B.J., and Reynolds, T.C. (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. Auger, R., Robin, P., Camier, B., Vial, G., Rossignol, B., Tenu, J.P., and Raymond, M.N. (1999). Relationship between phosphatidic acid level and regulation of protein transit in colonic epithelial cell line HT29-cl19A. J. Biol. Chem. 274, 28652-28659.
3. Augeron, C., and Laboisse, C.L. (1984). Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res. 44, 3961-3969.
4. Auricchio, A., O'Connor, E., Weiner, D., Gao, G.P., Hildinger, M., Wang, L., Calcedo, R., and Wilson, J.M. (2002). Noninvasive gene transfer to the lung for systemic delivery of therapeutic proteins. J. Clin. Invest. 110, 499-504.
5. Bals, R., Xiao, W., Sang, N., Weiner, D.J., Meegalla, R.L., and Wilson, J.M. (1999). Transduction of well-differentiated airway epithelium by recombinant adeno-associated virus is limited by vector entry. J. Virol. 73, 6085-6088.
6. Büning, H., Ried, M., Perabo, L., Gerner, F., Huttner, N., Enssle, J., and Hallek, M. (2003). Receptor targeting of adeno-associated virus. Gene Ther. 10, 1142-1151.
7. Büning, H., Braun-Falco, M., and Hallek, M. (2004). Progress in the use of adenoassociated viral vectors for gene therapy. Cells Tissues Organs 177, 139-150.
8. Carter, B.J. (2005). Adeno-associated virus vectors in clinical trials. Hum. Gene Ther. 16, 541-550.
9. Cozens, A.L., Yezzi, M.J., Kunzelmann, K., Ohrui, T., Chin, L., Eng, K., Finkbeiner, W.E., Widdicombe, J.H., and Gruenert, D.C. (1994). CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 10, 38-47.
10. Ding, W., Yan, Z., Zak, R., Saavedra, M., Rodman, D.M., and Engelhardt, J.F. (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. Dragomir, A., Bjorstad, J., Hjelde, L., and Roomans, G.M. (2004). Curcumin does not stimulate cAMP-mediated chloride transport in cystic fibrosis airway epithelial cells. Biochem. Biophys. Res. Commun. 322, 447-451.
12. Duan, D., Yue, Y., Yan, Z., McCray, P.B., and Engelhardt, J.F. (1998). Polarity influences the efficiency of recombinant adeno-associated virus infection in differentiated airway epithelia. Hum. Gene Ther. 9, 2761-2776.
13. Duan, D., Yue, Y., Yan, Z., Yang, J., and Engelhardt, J.F. (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associted virus. J. Clin. Invest. 105, 1573-1587.
14. Finkbeiner, W.E., Carrier, S.D., and Teresi, C.E. (1993). Reverse transcription-polymerase chain reaction (RT-PCR) phenotypic analysis of cell cultures of human tracheal epithelium, tracheobronchial glands, and lung carcinomas. Am. J. Respir. Cell Mol. Biol. 9, 547-556.
15. Foster, K.A., Avery, M.L., Yazdanian, M., and Audus, K.L. (2000). Characterization of the Calu-3 cell line as a tool to screen pulmonary drug delivery. Int. J. Pharm. 208, 1-11.
16. Gao, G., Alvira, M.R., Somanathan, S., Lu, Y., Vandenberghe, L.H., Rux, J.J., Calcedo, R., Sanmiguel, J., Abbas, Z., and Wilson, J.M. (2003). Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc. Natl. Acad. Sci. U.S.A. 100, 6081-6086.
17. Gao, G.P., Alvira, M.R., Wang, L., Calcedo, R., Johnston, J., and Wilson, J.M. (2002). Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. U.S.A. 99, 11854-11859.
18. 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 with that of AAV2 vectors. J. Virol. 75, 6615-6624.
19. Halbert, C.L., Allen, J.M., and Miller, A.D. (2002). Efficient mouse airway transduction following recombination between AAV vectors carrying parts of a larger gene. Nat. Biotechnol. 20, 697-701.
20. Jost, P.J., Harbottle, R.P., Knight, A., Miller, A.D., Coutelle, C., and Schneider, H. (2001). A novel peptide, THALWHT, for the targeting of human airway epithelia. FEBS Lett. 489, 263-269.
21. Kern, A., Schmidt, K., Leder, C., Muller, O.J., Wobus, C.E., Bettinger, K., von der Lieth, C.W., King, J.A., and Kleinschmidt, J.A. (2003). Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J. Virol. 77, 11072-11081.
22. Limberis, M.P., and Wilson, J.M. (2006). Adeno-associated virus serotype 9 vectors transduce murine alveolar and nasal epithelia and can be readministered. Proc. Natl. Acad. Sci. U.S.A. 103, 12993-12998.
23. Mathia, N.R., Timoszyk, J., Stetsko, P.I., Megill, J.R., Smith, R.L., and Wall, D.A. (2002). Permeability characteristics of calu-3 human bronchial epithelial cells: In vitro-in vivo correlation to predict lung absorption in rats. J. Drug Target. 10, 31-40.
24. - secretion in colonic epithelial cells expressing high levels of cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 267, 5575-5583.
25. - secretion in epithelial cells. Am. J. Physiol. 266, C254-C268.
26. Nakai, H., Storm, T.A., and Kay, M.A. (2000). Increasing the size of rAAV-mediated expression cassettes in vivo by intermolecular joining of two complementary vectors. Nat. Biotechnol. 18, 527-532.
27. Opie, S.R., Warrington, K., Agbandje-McKenna, M., Zolotukhin, S., and Muzyczka, N. (2003). Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding. J. Virol. 77, 6995-7006.
28. Ostedgaard, L.S., Rokhlina, T., Karp, P.H., Lashmit, P., Afione, S., Schmidt, M., Zabner, J., Stinski, M.F., Chiorini, J.A., and Welsh, M.J. (2005). A shortened adeno-associated virus expression cassette for CFTR gene transfer to cystic fibrosis airway epithelia. Proc. Natl. Acad. Sci. U.S.A. 102, 2952-2957.
29. Pergolizzi, R.G., Ropper, A.E., Dragos, R., Reid, A.C., Nakayama, K., Tan, Y., Ehteshami, J.R., Coleman, S.H., Silver, R.B., Hackett, N.R., Menez, A., and Crystal, R.G. (2003). In vivo trans-splicing of 5′ and 3′ segments of pre-mRNA directed by corresponding DNA sequences delivered by gene transfer. Mol. Ther. 8, 999-1008.
30. Ren, C., White, A.F., and Ponnazhagan, S. (2007). Notch-1 augments intracellular trafficking of adeno-associated virus 2. J. Virol. 81, 2069-2073.
31. Rosenecker, J., Huth, S., and Rudolph, C. (2006). Gene therapy for cystic fibrosis lung disease: Current status and future perspectives. Curr. Opin. Mol. Ther. 8, 439-445.
32. Rosseau, S., Selhorst, J., Wiechmann, K., Leissner, K., Maus, U.K., Mayer, K., Grimminger, F., Seeger, W., and Lohmeyer, J. (2000). Monocyte migration through the alveolar epithelial barrier: Adhesion molecule mechanisms and impact of chemokines. J. Immunol. 164, 427-435.
33. 1-integrins. FEBS Lett. 429, 269-273.
34. - secretion. Am. J. Physiol. 266, 493-501.
35. Subramanian, S., Parthasarathy, R., Sen, S., Boder, E.T., and Discher, D.E. (2006). Species- and cell type-specific interactions between CD47 and human SIRPα. Blood 107, 2548-2556.
36. Subramanian, S., Boder, E.T., and Discher, D.E. (2007). Phylogenetic divergence of CD47 interactions with human signal regulatory protein α reveals locus of species specificity: Implications for the binding site. J. Biol. Chem. 282, 1805-1818.
37. Summerford, C., and Samulski, R.J. (1998). Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72, 1438-1445.
38. Varga, K., Jurkuvenaite, A., Wakefield, J., Hong, J.S., Guimbellot, J.S., Venglarik, C.J., Niraj, A., Mazur, M., Sorscher, E.J., Collawn, J.F., and Bebök, Z. (2004). Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J. Biol. Chem. 279, 22578-22584.
39. Wagner, J.A., Moran, M.L., Messner, A.H., Daifuku, R., Conrad, C.K., Reynolds, T., Guggino, W.B., Moss, R.B., Carter, B.J., Wine, J.J., Flotte, T.R., and Gardner, P. (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.
40. Weber, E., Berta, G., Tousson, A., St John, P., Green, M.W., Gopalokrishnan, U., Jilling, T., Sorscher, E.J., Elton, T.S., Abrahamson, D.R., and Kirk, K.L. (1994). Expression and polarized targeting of a rab3 isoform in epithelial cells. J. Cell. Biol. 125, 583-594.
41. Wistuba, A., Kern, A., Weger, S., Grimm, D., and Kleinschmidt, J.A. (1997). Subcellular compartmentalization of adeno-associated virus type 2 assembly. J. Virol. 71, 1341-1352.
42. Wobus, C.E., Hugle-Dorr, B., Girod, A., Petersen, G., Hallek, M., and Kleinschmidt, J.A. (2000). Monoclonal antibodies against the adeno-associated virus type 2 (AAV-2) capsid: Epitope mapping and identification of capsid domains involved in AAV-2-cell interaction and neutralization of AAV-2 infection. J. Virol. 74, 9281-9293.
43. Yan, Z., Zhang, Y., Duan, D., and Engelhardt, J.F. (2000). Trans-splicing vectors expand the utility of adeno-associated virus for gene therapy. Proc. Natl. Acad. Sci. U.S.A. 97, 6716-6721.
44. Yan, Z., Zak, R., Zhang, Y., Ding, W., Godwin, S., Munson, K., Peluso, R., and Engelhardt, J.F. (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, 2861-2874.
45. Zabner, J., Seiler, M., Walters, R., Kotin, R.M., Fulgeras, W., Davidson, B.L., and Chiorini, J.A. (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.