Biological differences in rAAV transduction of airway epithelia in humans and in old world non-human primates

Molecular Therapy

Volumn 15, Issue 12, 2007, Pages 2114-2123

  Liu, Xiaoming ^a   Luo, Meihui ^a   Trygg, Cyndi ^b   Yan, Ziying ^a   Lei Butters, Diana C M ^a   Smith, Carolina I ^c   Fischer, Anne C ^d   Munson, Keith ^e   Guggino, William B ^c   Bunnell, Bruce A ^b   Engelhardt, John F ^a  

^a UNIVERSITY OF IOWA   (United States)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Targeted Genetics Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE ION; PARVOVIRUS VECTOR; SODIUM ION;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOENERGY; CELL CULTURE; CHLORIDE TRANSPORT; CONTROLLED STUDY; CULTURE MEDIUM; GENE THERAPY; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; REFERENCE VALUE; RESPIRATORY EPITHELIUM; RHESUS MONKEY; SEROTYPE; SODIUM TRANSPORT; SPECIES DIFFERENCE; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 36348993662     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/sj.mt.6300277     Document Type: Article

References (47)

1. Sullivan, DE, Dash, S, Du, H, Hiramatsu, N, Aydin, F, Kolls, J et al. (1997). Liver-directed gene transfer in non-human primates. Hum Gene Ther 8: 1195-1206.
2. Allocca, M, Tessitore, A, Cotugno, G and Auricchio, A (2006), AAV-mediated gene transfer for retinal diseases. Expert Opin Biol Ther 6: 1279-1294.
3. Preuss, TM, Caceres, M, Oldham, MC and Geschwind, DH (2004). Human brain evolution: Insights from microarrays. Nat Rev Genet 5: 850-860.
4. Puente, XS, Velasco, G, Gutierrez-Fernandez, A, Bertranpetit, J, King, MC and Lopez-Otin, C (2006). Comparative analysis of cancer genes in the human and chimpanzee genomes. BMC Genomics 7: 15.
5. Plopper, CG, Heidsiek, JG, Weir, AJ, George, JA and Hyde, DM (1989). Tracheobronchial epithelium in the adult rhesus monkey: A quantitative histochemical and ultrastructural study. Am J Anat 184: 31-40.
6. St George, JA, Nishio, SJ and Plopper, CG (1984). Carbohydrate cytochemistry of rhesus monkey tracheal epithelium. Anat Rec 210: 293-302.
7. Boucher, RC (2004). New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 23: 146-158.
8. Liu, X, Luo, M, Zhang, LN, Yan, Z, Zak, R, Ding, W et al. (2005). Spliceosome-mediated RNA trans-splicing with recombinant adeno-associated virus partially restores cystic fibrosis transmembrane conductance regulator function to polarized human cystic fibrosis airway epithelial cells. Hum Gene Ther 16: 1116-1123.
9. Zhang, LN, Karp, P, Gerard, CJ, Pastor, E, Laux, D, Munson, K et al. (2004). Dual therapeutic utility of proteasome modulating agents for pharmaco-gene therapy of the cystic fibrosis airway. Mol Ther 10: 990-1002.
10. Siminger, J, Muller, C, Braag, S, Tang, Q, Yue, H, Detrisac, C et al. (2004). Functional characterization of a recombinant adeno-associated virus 5-pseudotyped cystic fibrosis transmembrane conductance regulator vector. Hum Gene Ther 15: 832-841.
11. Flotte, T., Carter, B, Conrad, C, Guggino, W, Reynolds, T, Rosenstein, B et al. (1996). A phase I study of an adeno-associated virus-CFTR gene vector in adult CF patients with mild lung disease. Hum Gene Ther 7: 1145-1159.
12. Conrad, CK, Allen, SS, Afione, SA, Reynolds, TC, Beck, SE, Fee-Maki, M et al. (1996). Safety of single-dose administration of an adeno-associated virus (AAV)-CFTR vector in the primate lung. Gene Ther 3: 658-668.
13. Flotte, TR, Zeitlin, PL, Reynolds, TC, Heald, AE, Pedersen, P, Beck S et al. (2003). Phase I trial of intranasal and endobronchial administration of a recombinant adeno-associated virus serotype 2 (rAAV2)-CFTR vector in adult cystic fibrosis patients: A two-part clinical study. Hum Gene Ther 14: 1079-1088.
14. Wagner, JA, Nepomuceno, IB, Messner, AH, Moran, ML, Batson, EP, Dimiceli, S et al. (2002). A phase II, double-blind, randomized, placebo-controlled clinical trial of tgAAVEF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum Gene Ther 13: 1349-1359.
15. Gao, G, Vandenberghe, LH and Wilson, JM (2005). New recombinant serotypes of AAV vectors. Curr Gene Ther 5: 285-297.
16. Liu, X, Yan, Z, Luo, M and Engelhardt, JF (2006). Species-specific differences in mouse and human airway epithelial biology of recombinant adeno-associated virus transduction. Am J Respir Cell Mol Biol 34: 56-64.
17. Duan, D, Yan, Z, Yue, Y, Ding, W and Engelhardt, JF (2001). Enhancement of muscle gene delivery with pseudotyped adeno-associated virus type 5 correlates with myoblast differentiation. J Virol 75: 7662-7671.
18. Yan, Z, Zak, R, Zhang, Y, Ding, W, Godwin, S, Munson, K 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.
19. Song, S, Scott-Jorgensen, M, Wang, J, Poirier, A, Crawford, J, Campbell-Thompson, M et al. (2002). Intramuscular administration of recombinant adeno-associated virus 2 alpha-1 antitrypsin (rAAV-SERPINA1) vectors in a nonhuman primate model: Safety and immunologic aspects. Mol Ther 6: 329-335.
20. Hadaczek, F, Kohutnicka, M, Krauze, MT, Bringas, J, Pivirotto, P, Cunningham, J et al. (2006). Convection-enhanced delivery of adeno-associated virus type 2 (AAV2) into the striatum and transport of AAV2 within monkey brain. Hum Gene Ther 17: 291-302.
21. Davidoff, AM, Gray, JT, Ng, CY, Zhang, Y, Zhou, J, Spence, Y et al. (2005). Comparison of the ability of adeno-associated viral vectors pseudotyped with serotype 2, 5, and 8 capsid proteins to mediate efficient transduction of the liver in murine and nonhuman primate models. Mol Ther 11: 875-888.
22. Gao, G, Lu, Y, Calcedo, R, Grant, RL, Bell, P, Wang, L et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87.
23. Moss, RB, Rodman, D, Spencer, LT, Aitken, ML, Zeitlin, PL, Waltz, D et al. (2004). Repeated adeno-associated virus serotype 2 aerosol-mediated cystic fibrosis transmembrane regulator gene transfer to the lungs of patients with cystic fibrosis: A multicenter, double-blind, placebo-controlled trial. Chest 125: 509-521.
24. Liu, X, Luo, M, Zhang, L, Ding, W, Yan, Z and Engelhardt, JF (2007). Bioelectric properties of chloride channels in human, pig, ferret, and mouse airway epithelia. Am J Respir Cell Mol Biol 36: 313-323.
25. Ballard, ST, Trout, L, Garrison, J and Inglis, SK (2006). Ionic mechanism of forskolin-induced liquid secretion by porcine bronchi. Am J Physiol Lung Cell Mol Physiol 290: L97-L104.
26. Zhang, AL and Roomans, GM (1999). Multiple intracellular pathways for regulation of chloride secretion in cultured pig tracheal submucosal gland cells. Eur Respir J 13: 571-576.
27. Thiagarajah, JR, Song, Y, Haggie, PM and Verkman, AS (2004). A small molecule CFTR inhibitor produces cystic fibrosis-like submucosal gland fluid secretions in normal airways. FASEB J 18: 875-877.
28. Ma, T, Thiagarajah, JR, Yang, H, Sonawane, ND, Folli, C, Galietta, LJ et al. (2002). Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 110: 1651-1658.
29. Muanprasat, C, Sonawane, ND, Salinas, D, Taddei, A, Galietta, LJ and Verkman, AS (2004). Discovery of glycine hydrazide pore-occluding CFTR inhibitors: Mechanism, structure-activity analysis, and in vivo efficacy. J Gen Physiol 124: 125-137.
30. Yan, Z, Lei-Butters, DC, Liu, X, Zhang, Y, Zhang, L, Luo, M et al. (2006). Unique biologic properties of recombinant AAV1 transduction in polarized human airway epithelia. J Biol Chem 281: 29684-29692.
31. Jiang, Q and Engelhardt, JF (1998). Cellular heterogeneity of CFTR expression and function in the Jung: Implications for gene therapy of cystic fibrosis. Eur J Hum Genet 6: 12-31.
32. Duan, D, Yue, Y, Yan, Z, Yang, J and Engelhardt, JF (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 105: 1573-1587.
33. Hansen, J, Qing, K and Srivastava, A (2001). Adeno-associated virus type 2-mediated gene transfer: Altered endocytic processing enhances transduction efficiency in murine fibroblasts. J Virol 75: 4080-4090.
34. Ding, W, Yan, Z, Zak, R, Saavedra, M, Rodman, DM and Engelhardt, JF (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.
35. Zhao, W, Zhong, L, Wu, J, Chen, L, Qing, K, Weigel-Kelley, KA et al. (2006). Role of cellular FKBP52 protein in intracellular trafficking of recombinant adeno-associated virus 2 vectors. Virology 353 283-293.
36. Wu, Z, Miller, E, Agbandje-McKenna, M and Samulski, RJ (2006). Alpha2,3 and alpha2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol 80: 9093-9103.
37. Summerford, C and Samulski, RJ (1998). Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445.
38. Summerford, C, Bartlett, JS and Samulski, RJ (1999). AlphaVbeta5 integrin: A co-receptor for adeno-associated virus type 2 infection. Nat Med 5: 78-82.
39. Qing, K, Mah, C, Hansen, J, Zhou, S, Dwarki, V and Srivastava, A (1999). Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat Med 5: 71-77.
40. Kashiwakura, Y, Tamayose, K, Iwabuchi, K, Hirai, Y, Shimada, T, Matsumoto, K et al. (2005). Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J Virol 79: 609-614.
41. Walters, RW, Yi, SM, Keshavjee, S, Brown, KE, Welsh, MJ, Chiorini, JA et al. (2001). Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J Biol Chem 276: 20610-20616.
42. Di Pasquale, G, Davidson, BL, Stein, CS, Martins, I, Scudiero, D, Monks, A et al. (2003). Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med 9: 1306-1312.
43. Duan, D, Yue, Y and Engelhardt, JF (1999). Response to "polarity influences the efficiency of recombinant adeno-associated virus infection in differentiated airway epithelia." Hum Gene Ther 10: 1553-1557.
44. Seiler, MP, Miller, AD, Zabner, J and Halbert, CL (2006). Adeno-associated virus types 5 and 6 use distinct receptors for cell entry. Hum Gene Ther 17: 10-19.
45. Ding, W, Zhang, LN, Yeaman, C and Engelhardt, JF (2006). rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol Ther 13: 671-682.
46. Liu, X, Driskell, RR and Engelhardt, JF (2006). Stem cells in the lung. Methods Enzymol 419: 285-321.
47. Karp, PH, Moninger, TO, Weber, SP, Nesselhauf, TS, Launspach, JL, Zabner, J et al. (2002). An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures. Methods Mol Biol 188: 115-137.