Improved gene delivery to intestinal mucosa by adenoviral vectors bearing subgroup B and D fibers

Journal of Virology

Volumn 80, Issue 6, 2006, Pages 2747-2759

  Lecollinet, S ^a   Gavard, F ^a   Havenga, M J E ^b   Spiller, O B ^c   Lemckert, A ^b   Goudsmit, J ^b   Eloit, M ^a   Richardson, J ^a  

^a ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^b CRUCELL HOLLAND BV   (Netherlands)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; GLYCOCONJUGATE; MEMBRANE COFACTOR PROTEIN; SIALIC ACID;

ADENOVIRUS VECTOR; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRAIN 3T3; CELL STRAIN K 562; CHO CELL; GENETIC TRANSDUCTION; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE EPITHELIUM; INTESTINE MUCOSA; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; SEROTYPE; TISSUE CULTURE; VIRAL GENE DELIVERY SYSTEM; VIRUS ADSORPTION; VIRUS FIBER;

ADENOVIRUSES, HUMAN; ANIMALS; ANTIGENS, CD46; CACO-2 CELLS; CAPSID PROTEINS; CELL LINE; CELL POLARITY; GENETIC VECTORS; HUMANS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; N-ACETYLNEURAMINIC ACID; RECEPTORS, VIRUS; SEROTYPING; TRANSDUCTION, GENETIC;

ADENOVIRIDAE; ANIMALIA; COXSACKIEVIRUS; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS TYPE 5; MURINAE; SUBGROUP B; SUBGROUP C;

EID: 33644766978     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.6.2747-2759.2006     Document Type: Article

References (83)

1. Ambriovic-Ristov, A., S. Mercier, and M. Eloit. 2003. Shortening adenovirus type 5 fiber shaft decreases the efficiency of postbinding steps in CAR-expressing and nonexpressing cells. Virology 312:425-433.
2. Arcasoy, S. M., J. Latoche, M. Condor, S. C. Watkins, R. A. Henderson, R. Hughey, O. J. Finn, and J. M. Pilewski. 1997. MUC1 and other sialoglycoconjugates inhibit adenovirus-mediatcd gene transfer to epithelial cells. Am. J. Respir. Cell Mol. Biol. 17:422-435.
3. Arnberg, N., K. Edlund, A. H. Kidd, and G. Wadell. 2000. Adenovirus type 37 uses sialic acid as a cellular receptor. J. Virol. 74:42-48.
4. Arnberg, N., A. H. Kidd, K. Edlund, F. Olfat, and G. Wadell. 2000. Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus alpha(v) integrins. J. Virol. 74:7691-7693.
5. Balzar, M., F. A. Prins, H. A. Bakker, G. J. Fleuren, S. O. Warnaar, and S. V. Litvinov. 1999. The structural analysis of adhesions mediated by Ep-CAM. Exp. Cell Res. 246:108-121.
6. Bens, M., A. Bogdanova, F. Cluzeaud, L. Miquerol, S. Kerneís, J. P. Kraehenbuhl, A. Kahn, E. Pringault, and A. Vandewalle. 1996. Transimmortalized mouse intestinal cells (m-ICcl2) that maintain a crypt phenotype. Am. J. Physiol. 270:C1666-C1674.
7. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, 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.
8. Bergelson, J. M., A. Krithivas, L. Celi, G. Droguett, M. S. Horwitz, T. Wickham, R. L. Crowell, and R. W. Finberg. 1998. The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. J. Virol. 72:415-419.
9. Blixenkrone-Moller, M., A. Bernard, A. Bencsik, N. Sixt, L. E. Diamond, J. S. Logan, and T. F. Wild. 1998. Role of CD46 in measles virus infection in CD46 transgenic mice. Virology 249:238-248.
10. Casimiro, D. R., L. Chen, T. M. Fu, R. K. Evans, M. J. Caulfield, M. E. Davies, A. Tang, M. Chen, L. Huang, V. Harris, D. C. Freed, K. A. Wilson, S. Dubey, D. M. Zhu, D. Nawrocki, H. Mach, R. Troutman, L. Isopi, D. Williams, W. Hurni, Z. Xu, J. G. Smith, S. Wang, X. Liu, L. Guan, R. Long, W. Trigona, G. J. Heidecker, H. C. Perry, N. Persaud, T. J. Toner, Q. Su, X. Liang, R. Youil, M. Chastain, A. J. Bett, D. B. Volkin, E. A. Emini, and J. W. Shiver. 2003. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J. Virol. 77:6305-6313.
11. Cheng, D. Y., J. K. Kolls, D. Lei, and R. A. Noel. 1997. In vivo and in vitro gene transfer and expression in rat intestinal epithelial cells by E1-deleted adenoviral vector. Hum. Gene Ther. 8:755-764.
12. Chu, Y., D. Heistad, M. I. Cybulsky, and B. L. Davidson. 2001. Vascular cell adhesion molecule-1 augments adenovirus-mediated gene transfer. Arterioscler. Thromb. Vasc. Biol. 21:238-242.
13. Cohen, C. J., J. T. Shieh, R. J. Pickles, T. Okegawa, J. T. Hsieh, and J. M. Bergelson. 2001. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl. Acad. Sci. USA 98:15191-15196.
14. Crawford-Miksza, L., and D. P. Schnurr. 1996. Analysis of 15 adenovirus hexon proteins reveals the location and structure of seven hypervariable regions containing serotype-specific residues. J. Virol. 70:1836-1844.
15. Croyle, M. A., M. Stone, G. L. Amidon, and B. J. Roessler. 1998. In vitro and in vivo assessment of adenovirus 41 as a vector for gene delivery to the intestine. Gene Ther. 5:645-654.
16. Croyle, M. A., E. Walter, S. Janich, B. J. Roessler, and G. L. Amidon. 1998. Role of integrin expression in adenovirus-mediated gene delivery to the intestinal epithelium. Hum. Gene Ther. 9:561-573.
17. Dechecchi, M. C., P. Melotti, A. Bonizzato, M. Santacatterina, M. Chilosi, and G. Cabrini. 2001. Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5. J. Virol. 75:8772-8780.
18. Defer, C., M. T. Belin, M. L. Caillet-Boudin, and P. Boulanger. 1990. Human adenovirus-host cell interactions: comparative study with members of sub-groups B and C. J. Virol. 64:3661-3673.
19. De Jong, J. C., A. G. Wermenbol, M. W. Verweij-Uijterwaal, K. W. Slaterus, P. Wertheim-Van Dillen, G. J. Van Doornum, S. H. Khoo, and J. C. Hierholzer. 1999. Adenoviruses from human immunodeficiency virus-infected individuals, including two strains that represent new candidate serotypes Ad50 and Ad51 of species B1 and D, respectively. J. Clin. Microbiol. 37: 3940-3945.
20. De Jong, J. C., R. Wigand, A. H. Kidd, G. Wadell, J. G. Kapsenberg, C. J. Muzerie, A. G. Wermenbol, and R. G. Firtzlaff. 1983. Candidate adenoviruses 40 and 41: fastidious adenoviruses from human infant stool. J. Med. Virol. 11:215-231.
21. Favier, A. L., W. P. Burmeister, and J. Chroboczek. 2004. Unique physicochemical properties of human enteric Ad41 responsible for its survival and replication in the gastrointestinal tract. Virology 322:93-104.
22. Fogh, J., J. M. Fogh, and T. Orfeo. 1977. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J. Natl. Cancer Inst. 59:221-226.
23. Foreman, P. K., M. J. Wainwright, B. Alicke, I. Kovesdi, T. J. Wickham, J. G. Smith, S. Meier-Davis, J. A. Fix, P. Daddona, P. Gardner, and M. T. Huang. 1998. Adenovirus-mediated transduction of intestinal cells in vivo. Hum. Gene Ther. 9:1313-1321.
24. Gaden, F., L. Franqueville, S. S. Hong, V. Legrand, C. Figarella, and P. Boulanger. 2002. Mechanism of restriction of normal and cystic fibrosis transmembrane conductance regulator-deficient human tracheal gland cells to adenovirus infection and ad-mediated gene transfer. Am. J. Respir. Cell Mol. Biol. 27:628-640.
25. Gaggar, A., D. M. Shayakhmetov, and A. Lieber. 2003. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9:1408-1412.
26. Gall, J., A. Kass-Eisler, L. Leinwand, and E. Falck-Pedersen. 1996. Adenovirus type 5 and 7 capsid chimera: fiber replacement alters receptor tropism without affecting primary immune neutralization epitopes. J. Virol. 70:2116-2123.
27. Gao, G., L. H. Vandenberghe, and J. M. Wilson. 2005. New recombinant serotypes of AAV vectors. Curr. Gene Ther. 5:285-297.
28. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-74.
29. Hamilton, T., R. DeMatteo, S. McClane, C. Burke, J. Rombeau, and S. Raper. 1997. Adenoviral-mediated gene transfer to murine small intestine is more efficient in neonates than adults. J. Pediatr. Surg. 32:373-377.
30. Havenga, M. J., A. A. Lemckert, O. J. Ophorst, M. van Meijer, W. T. Germeraad, J. Grimbergen, M. A. van Den Doel, R. Vogels, J. van Deutekom, A. A. Janson, J. D. de Bruijn, F. Uytdehaag, P. H. Quax, T. Logtenberg, M. Mehtali, and A. Bout. 2002. Exploiting the natural diversity in adenovirus tropism for therapy and prevention of disease. J. Virol. 76:4612-4620.
31. 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.
32. Hierholzer, J. C. 1992. Adenoviruses in the immunocompromised host. Clin. Microbiol. Rev. 5:262-274.
33. Hong, S. S., M. Bardy, M. Monteil, B. Gay, C. Denesvre, J. Tournier, G. Martin, M. Eloit, and P. Boulanger. 2000. Immunoreactive domains and integrin-binding motifs in adenovirus penton base capsomer. Viral Immunol. 13:353-371.
34. Hong, S. S., L. Karayan, J. Tournier, D. T. Curiel, and P. A. Boulanger. 1997. Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J. 16:2294-2306.
35. Horwitz, M. 1990. Adenoviruses, p. 1723-1740. In B. N. Fields and D. M. Knipe (ed.), Raven Press, New York, N.Y.
36. Huang, S., T. Kamata, Y. Takada, Z. M. Ruggeri, and G. R. Nemerow. 1996. Adenovirus interaction with distinct integrins mediates separate events in cell entry and gene delivery to hematopoietic cells. J. Virol. 70:4502-4508.
37. Kidd, A. H., J. Chroboczek, S. Cusack, and R. W. Ruigrok. 1993. Adenovirus type 40 virions contain two distinct fibers. Virology 192:73-84.
38. Krasnykh, V. N., G. V. Mikheeva, J. T. Douglas, and D. T. Curiel. 1996. Generation of recombinant adenovirus vectors with modified fibers for altering viral tropism. J. Virol. 70:6839-6846.
39. Lozahic, S., D. Christiansen, S. Manie, D. Gerlier, M. Billard, C. Boucheix, and E. Rubinstein. 2000. CD46 (membrane cofactor protein) associates with multiple beta1 integrins and tetraspans. Eur. J. Immunol. 30:900-907.
40. Maisner, A., M. K. Liszewski, J. P. Atkinson, R. Schwartz-Albiez, and G. Herrler. 1996. Two different cytoplasmic tails direct isoforms of the membrane cofactor protein (CD46) to the basolateral surface of Madin-Darby canine kidney cells. J. Biol. Chem. 271:18853-18858.
41. Mallegol, J., G. van Niel, and M. Heyman. 2005. Phenotypic and functional characterization of intestinal epithelial exosomes. Blood Cells Mol. Dis. 35:11-16.
42. Mei, Y. F., K. Lindman, and G. Wadell. 2002. Human adenoviruses of subgenera B, C, and E with various tropisms differ in both binding to and replication in the epithelial A549 and 293 cells. Virology 295:30-43.
43. Meier, O., and U. F. Greber. 2003. Adenovirus endocytosis. J. Gene Med. 5:451-462.
44. Miyazawa, N., P. L. Leopold, N. R. Hackett, B. Ferris, S. Worgall, E. Falck-Pedersen, and R. G. Crystal. 1999. Fiber swap between adenovirus sub-groups B and C alters intracellular trafficking of adenovirus gene transfer vectors. J. Virol. 73:6056-6065.
45. Nakamura, T., K. Sato, and H. Hamada. 2003. Reduction of natural adenovirus tropism to the liver by both ablation of fiber-coxsackievirus and adenovirus receptor interaction and use of replaceable short fiber. J. Virol. 77:2512-2521.
46. Pickles, R. J., J. A. Fahrner, J. M. Petrella, R. C. Boucher, and J. M. Bergelson. 2000. Retargeting the coxsackievirus and adenovirus receptor to the apical surface of polarized epithelial cells reveals the glycocalyx as a barrier to adenovirus-mediated gene transfer. J. Virol. 74:6050-6057.
47. Pickles, R. J., D. McCarty, H. Matsui, P. J. Hart, S. H. Randell, and R. C. Boucher. 1998. Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer. J. Virol. 72: 6014-6023.
48. Rea, D., M. J. Havenga, A. M. van Den, R. P. Sutmuller, A. Lemckert, R. C. Hoeben, A. Bout, C. J. Melief, and R. Offringa. 2001. Highly efficient transduction of human monocyte-derived dendritic cells with subgroup B fiber-modified adenovirus vectors enhances transgene-uncoded antigen presentation to cytotoxic T cells. J. Immunol. 166:5236-5244.
49. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty per cent endpoint. Am. J. Hyg. 27:493-497.
50. Rescigno, M., G. Rotta, B. Valzasina, and P. Ricciardi-Castagnoli. 2001. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 204:572-581.
51. Roelvink, P. W., A. Lizonova, J. G. Lee, Y. Li, J. M. Bergelson, R. W. Finberg, D. E. Brough, I. Kovesdi, and T. J. Wickham. 1998. The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J. Virol. 72:7909-7915.
52. Roelvink, P. W., L. G. Mi, D. A. Einfeld, I. Kovesdi, and T. J. Wickham. 1999. Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286:1568-1571.
53. Sandberg, J. W., C. Lau, M. Jacomino, M. Finegold, and S. J. Henning. 1994. Improving access to intestinal stem cells as a step toward intestinal gene transfer. Hum. Gene Ther. 5:323-329.
54. Schoggins, J. W., J. G. Gall, and E. Falck-Pedersen. 2003. Subgroup B and F fiber chimeras eliminate normal adenovirus type 5 vector transduction in vitro and in vivo. J. Virol. 77:1039-1048.
55. Segerman, A., J. P. Atkinson, M. Marttila, V. Dennerquist, G. Wadell, and N. Arnberg. 2003. Adenovirus type 11 uses CD46 as a cellular receptor. J. Virol. 77:9183-9191.
56. Sferra, T. J., D. McNeely, and P. R. Johnson. 1997. Gene transfer to the intestinal tract: a new approach using selective injection of the superior mesenteric artery. Hum. Gene Ther. 8:681-687.
57. Shayakhmetov, D. M., A. M. Eberly, Z. Y. Li, and A. Lieber. 2005. Deletion of penton RGD motifs affects the efficiency of both the internalization and the endosome escape of viral particles containing adenovirus serotype 5 or 35 fiber knobs. J. Virol. 79:1053-1061.
58. Shayakhmetov, D. M., Z. Y. Li, V. Ternovoi, A. Gaggar, H. Gharwan, and A. Lieber. 2003. The interaction between the fiber knob domain and the cellular attachment receptor determines the intracellular trafficking route of adenoviruses. J. Virol. 77:3712-3723.
59. Shayakhmetov, D. M., and A. Lieber. 2000. Dependence of adenovirus infectivity on length of the fiber shaft domain. J. Virol. 74:10274-10286.
60. Shiver, J. W., and E. A. Emini. 2004. Recent advances in the development of HIV-1 vaccines using replication-incompetent adenovirus vectors. Annu. Rev. Med. 55:355-372.
61. Short, J. J., A. V. Pereboev, Y. Kawakami, C. Vasu, M. J. Holterman, and D. T. Curiel. 2004. Adenovirus serotype 3 utilizes CD80 (B7.1) and CD86 (B7.2) as cellular attachment receptors. Virology 322:349-359.
62. Sirena, D., B. Lilienfeld, M. Eisenhut, S. Kalin, K. Boucke, R. R. Beerli, L. Vogt, C. Ruedl, M. F. Bachmann, U. F. Greber, and S. Hemmi. 2004. The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3. J. Virol. 78:4454-4462.
63. Spiller, O. B., I. G. Goodfellow, D. J. Evans, S. J. Hinchliffe, and B. P. Morgan. 2002. Coxsackie B viruses that use human DAF as a receptor infect pig cells via pig CAR and do not use pig DAF. J. Gen. Virol. 83:45-52.
64. Stevenson, S. C., M. Rollence, J. Marshall-Neff, and A. McClelland. 1997. Selective targeting of human cells by a chimeric adenovirus vector containing a modified fiber protein. J. Virol. 71:4782-4790.
65. Stevenson, S. C., M. Rollence, B. White, L. Weaver, and A. McClelland. 1995. Human adenovirus serotypes 3 and 5 bind to two different cellular receptors via the fiber head domain. J. Virol. 69:2850-2857.
66. Sullivan, N. J., A. Sanchez, P. E. Rollin, Z. Y. Yang, and G. J. Nabel. 2000. Development of a preventive vaccine for Ebola virus infection in primates. Nature 408:605-609.
67. Sweeney, J. A., and J. P. Hennessey, Jr. 2002. Evaluation of accuracy and precision of adenovirus absorptivity at 260 nm under conditions of complete DNA disruption. Virology 295:284-288.
68. 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.
69. Tsujimura, A., K. Shida, M. Kitamura, M. Nomura, J. Takeda, H. Tanaka, M. Matsumoto, K. Matsumiya, A. Okuyama, Y. Nishimune, M. Okabe, and T. Seya. 1998. Molecular cloning of a murine homologue of membrane cofactor protein (CD46): preferential expression in testicular germ cells. Biochem. J. 330(Pt. 1):163-168.
70. Uhnoo, I., G. Wadell, L. Svensson, and M. E. Johansson. 1984. Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children. J. Clin. Microbiol. 20:365-372.
71. Wadell, G., A. Allard, and J. C. Hierholzer. 1999. Adenoviruses, p. 970-982. In P. R. Murray, E. J. Baron, M. A. Pfaller, F. C. Tenover, and R. H. Yolken (ed.), Manual of clinical microbiology, 7th ed. ASM Press, Washington, D.C.
72. Walter, E., M. A. Croyle, B. J. Roessler, and G. L. Amidon. 1997. The absence of accessible vitronectin receptors in differentiated tissue hinders adenoviral-mediated gene transfer to the intestinal epithelium in vitro. Pharm. Res. 14:1216-1222.
73. Walters, R. W., P. Freimuth, T. O. Moninger, I. Ganske, J. Zabner, and M. J. Welsh. 2002. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110:789-799.
74. Walters, R. W., T. Grunst, J. M. Bergelson, R. W. Finberg, M. J. Welsh, and J. Zabner. 1999. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J. Biol. Chem. 274:10219-10226.
75. Wickham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
76. Wu, E., J. Fernandez, S. K. Fleck, D. J. Von Seggern, S. Huang, and G. R. Nemerow. 2001. A 50-kDa membrane protein mediates sialic acid-independent binding and infection of conjunctival cells by adenovirus type 37. Virology 279:78-89.
77. Wu, E., L. Pache, D. J. Von Seggern, T. M. Mullen, Y. Mikyas, P. L. Stewart, and G. R. Nemerow. 2003. Flexibility of the adenovirus fiber is required for efficient receptor interaction. J. Virol. 77:7225-7235.
78. Wu, E., S. A. Trauger, L. Pache, T. M. Mullen, D. J. Von Seggern, G. Siuzdak, and G. R. Nemerow. 2004. Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. J. Virol. 78:3897-3905.
79. Xiang, Z. Q., Y. Yang, J. M. Wilson, and H. C. Ertl. 1996. A replication-defective human adenovirus recombinant serves as a highly efficacious vaccine carrier. Virology 219:220-227.
80. Xu, R., J. G. Mohanty, and R. L. Crowell. 1995. Receptor proteins on newborn BALB/c mouse brain cells for coxsackievirus B3 are immunologically distinct from those on HeLa cells. Virus Res. 35:323-340.
81. Yeh, H. Y., N. Pieniazek, D. Pieniazek, H. Gelderblom, and R. B. Luftig. 1994. Human adenovirus type 41 contains two fibers. Virus Res. 33:179-198.
82. Zabner, J., M. Chillon, T. Grunst, T. O. Moninger, B. L. Davidson, R. Gregory, and D. Armentano. 1999. A chimeric type 2 adenovirus vector with a type 17 fiber enhances gene transfer to human airway epithelia. J. Virol. 73:8689-8695.
83. 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. Investig. 100:1144-1149.