1887

Abstract

Most currently used adenovirus vectors are based upon adenovirus serotypes 2 and 5 (Ad2 and Ad5), which have limited efficiencies for gene transfer to human neural cells. Both serotypes bind to the known adenovirus receptor, CAR (coxsackievirus and adenovirus receptor), and have restricted cell tropism. The purpose of this study was to find vector candidates that are superior to Ad5 in infecting human neural tumours. Using flow cytometry, the vector candidates Ad4p, Ad11p and Ad17p were compared to the commonly used adenovirus vector Ad5v for their binding capacity to neural cell lines derived from glioblastoma, medulloblastoma and neuroblastoma cell lines. The production of viral structural proteins and the CAR-binding properties of the different serotypes were also assessed in these cells. Computer-based models of the fibre knobs of Ad4p and Ad17 were created based upon the crystallized fibre knob structure of adenoviruses and analysed for putative receptor-interacting regions that differed from the fibre knob of Ad5. The non CAR-binding vector candidate Ad11p showed clearly the best binding capacity to all of the neural cell lines, binding more than 90% of cells of all of the neural cell lines tested, in contrast to 20% or less for the commonly used vector Ad5v. Ad4p and Ad11p were also internalized and produced viral proteins more successfully than Ad5. Ad4p showed a low binding ability but a very efficient capacity for infection in cell culture. Ad17p virions neither bound or efficiently infected any of the neural cell lines studied.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-6-1299
2002-06-01
2020-08-13
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/6/0831299a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-6-1299&mimeType=html&fmt=ahah

References

  1. Adrian T., Wadell G., Hierholzer J. C., Wigand R.. 1986; DNA restriction analysis of adenovirus prototypes 1 to 41. Archives of Virology91:277–290
    [Google Scholar]
  2. Alton E., Kitson C.. 2000; Gene therapy for cystic fibrosis. Expert Opinion on Investigational Drugs9:1523–1535
    [Google Scholar]
  3. Arnberg N., Edlund K., Kidd A. H., Wadell G.. 2000a; Adenovirus type 37 uses sialic acid as a cellular receptor. Journal of Virology74:42–48
    [Google Scholar]
  4. Arnberg N., Kidd A. H., Edlund K., Olfat F., Wadell G.. 2000b; Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus αv integrins. Journal of Virology74:7691–7693
    [Google Scholar]
  5. Asaoka K., Tada M., Sawamura Y., Ikeda J., Abe H.. 2000; Dependence of efficient adenoviral gene delivery in malignant glioma cells on the expression levels of the Coxsackievirus and adenovirus receptor. Journal of Neurosurgery92:1002–1008
    [Google Scholar]
  6. Bergelson J. M., St John N., Kawaguchi S., Chan M., Stubdal H., Modlin J., Finberg R. W.. 1993; Infection by echoviruses 1 and 8 depends on the α2 subunit of human VLA-2. Journal of Virology67:6847–6852
    [Google Scholar]
  7. Bergelson J. M., Cunningham J. A., Droguett G., Kurt-Jones E. A., Krithivas A., Hong J. S., Horwitz M. S., Crowell R. L., Finberg R. W.. 1997; Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science275:1320–1323
    [Google Scholar]
  8. Bewley M. C., Springer K., Zhang Y. B., Freimuth P., Flanagan J. M.. 1999; Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science286:1579–1583
    [Google Scholar]
  9. Byrnes A. P., Rusby J. E., Wood M. J., Charlton H. M.. 1995; Adenovirus gene transfer causes inflammation in the brain. Neuroscience66:1015–1024
    [Google Scholar]
  10. Byrnes A. P., Wood M. J., Charlton H. M.. 1996; Role of T cells in inflammation caused by adenovirus vectors in the brain. Gene Therapy3:644–651
    [Google Scholar]
  11. Chillon M., Bosch A., Zabner J., Law L., Armentano D., Welsh M. J., Davidson B. L.. 1999; Group D adenoviruses infect primary central nervous system cells more efficiently than those from group C. Journal of Virology73:2537–2540
    [Google Scholar]
  12. Choi-Lundberg D., Rosenthal A.. 1999; Autotransplantation for Parkinson’s disease goes a step further. Neuron22:635–636
    [Google Scholar]
  13. Chroboczek J., Ruigrok R. W., Cusack S.. 1995; Adenovirus fiber. Current Topics in Microbiology and Immunology199:163–200
    [Google Scholar]
  14. Ebihara S., Guibinga G. H., Gilbert R., Nalbantoglu J., Massie B., Karpati G., Petrof B. J.. 2000; Differential effects of dystrophin and utrophin gene transfer in immunocompetent muscular dystrophy (mdx) mice. Physiological Genomics3:133–144
    [Google Scholar]
  15. Ehrengruber M. U., Hennou S., Bueler H., Naim H. Y., Deglon N., Lundstrom K.. 2001; Gene transfer into neurons from hippocampal slices: comparison of recombinant Semliki Forest virus, adenovirus, adeno-associated virus, lentivirus, and measles Virus. Molecular and Cellular Neurosciences17:855–871
    [Google Scholar]
  16. Fasbender A., Zabner J., Chillon M., Moninger T. O., Puga A. P., Davidson B. L., Welsh M. J.. 1997; Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer in vitro and in vivo . Journal of Biological Chemistry272:6479–6489
    [Google Scholar]
  17. Fasbender A., Lee J. H., Walters R. W., Moninger T. O., Zabner J., Welsh M. J.. 1998; Incorporation of adenovirus in calcium phosphate precipitates enhances gene transfer to airway epithelia in vitro and in vivo . Journal of Clinical Investigation102:184–193
    [Google Scholar]
  18. Fenner F., McAuslan B. R., Mims C. A., Sambrook J., White D. O.. 1974; The biology of animal viruses. In The Biology of Human Viruses pp191–198 Edited by Fenner F.. New York: Academic Press;
    [Google Scholar]
  19. Fisher K. J., Choi H., Burda J., Chen S. J., Wilson J. M.. 1996; Recombinant adenovirus deleted of all viral genes for gene therapy of cystic fibrosis. Virology217:11–22
    [Google Scholar]
  20. Fox J. P., Hall C. E.. (editors) 1980; Viruses in Families p–318 Littleton, MA: PSG Publishing;
    [Google Scholar]
  21. Graham F. L.. 1984; Covalently closed circles of human adenovirus DNA are infectious. EMBO Journal3:2917–2922
    [Google Scholar]
  22. Graham F. L., Rudy J., Brinkley P.. 1989; Infectious circular DNA of human adenovirus type 5: regeneration of viral DNA termini from molecules lacking terminal sequences. EMBO Journal8:2077–2085
    [Google Scholar]
  23. Gruber W. C., Russell D. J., Tibbetts C.. 1993; Fiber gene and genomic origin of human adenovirus type 4. Virology196:603–611
    [Google Scholar]
  24. Guex N., Peitsch M. C.. 1997; SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis18:2714–2723
    [Google Scholar]
  25. Guex N., Diemand A., Peitsch M. C.. 1999; Protein modelling for all. Trends in Biochemical Sciences24:364–367
    [Google Scholar]
  26. Habib N. A., Hodgson H. J., Lemoine N., Pignatelli M.. 1999; A phase I/II study of hepatic artery infusion with wtp53-CMV-Ad in metastatic malignant liver tumours. Human Gene Therapy10:2019–2034
    [Google Scholar]
  27. Hermens W. T., Verhaagen J.. 1998; Viral vectors, tools for gene transfer in the nervous system. Progress in Neurobiology55:399–432
    [Google Scholar]
  28. Honda T., Saitoh H., Masuko M., Katagiri-Abe T., Tominaga K., Kozakai I., Kobayashi K., Kumanishi T., Watanabe Y. G., Odani S., Kuwano R.. 2000; The coxsackievirus–adenovirus receptor protein as a cell adhesion molecule in the developing mouse brain. Brain research: Molecular Brain Research77:19–28
    [Google Scholar]
  29. Hong S. S., Karayan L., Tournier J., Curiel D. T., Boulanger P. A.. 1997; Adenovirus type 5 fiber knob binds to MHC class I α2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO Journal16:2294–2306
    [Google Scholar]
  30. Kajiwara K., Byrnes A. P., Ohmoto Y., Charlton H. M., Wood M. J., Wood K. J.. 2000; Humoral immune responses to adenovirus vectors in the brain. Journal of Neuroimmunology103:8–15
    [Google Scholar]
  31. Kaplan J. M., Pennington S. E., St George J. A., Woodworth L. A., Fasbender A., Marshall J., Cheng S. H., Wadsworth S. C., Gregory R. J., Smith A. E.. 1998; Potentiation of gene transfer to the mouse lung by complexes of adenovirus vector and polycations improves therapeutic potential. Human Gene Therapy9:1469–1479
    [Google Scholar]
  32. Kaplitt M. G., Makimura H.. 1997; Defective viral vectors as agents for gene transfer in the nervous system. Journal of Neuroscience Methods71:125–132
    [Google Scholar]
  33. Kochanek S., Clemens P. R., Mitani K., Chen H. H., Chan S., Caskey C. T.. 1996; A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and β-galactosidase. Proceedings of the National Academy of Sciences, USA93:5731–5736
    [Google Scholar]
  34. Kremer E. J., Boutin S., Chillon M., Danos O.. 2000; Canine adenovirus vectors: an alternative for adenovirus-mediated gene transfer. Journal of Virology74:505–512
    [Google Scholar]
  35. Lang F. F., Yung W. K., Sawaya R., Tofilon P. J.. 1999; Adenovirus-mediated p53 gene therapy for human gliomas. Neurosurgery45:1093–1104
    [Google Scholar]
  36. Ludwig S. L., Brundage J. F., Kelley P. W., Nang R., Towle C., Schnurr D. P., Crawford-Miksza L., Gaydos J. C.. 1998; Prevalence of antibodies to adenovirus serotypes 4 and 7 among unimmunized US Army trainees: results of a retrospective nationwide seroprevalence survey. Journal of Infectious Diseases178:1776–1778
    [Google Scholar]
  37. Marini F. C.III., Yu Q., Wickham T., Kovesdi I., Andreeff M.. 2000; Adenovirus as a gene therapy vector for hematopoietic cells. Cancer Gene Therapy7:816–825
    [Google Scholar]
  38. Mei Y. F., Lindman K., Wadell G.. 1998; Two closely related adenovirus genome types with kidney or respiratory tract tropism differ in their binding to epithelial cells of various origins. Virology240:254–266
    [Google Scholar]
  39. Miller C. R., Buchsbaum D. J., Reynolds P. N., Douglas J. T., Gillespie G. Y., Mayo M. S., Raben D., Curiel D. T.. 1998; Differential susceptibility of primary and established human glioma cells to adenovirus infection: targeting via the epidermal growth factor receptor achieves fiber receptor-independent gene transfer. Cancer Research58:5738–5748
    [Google Scholar]
  40. Miyazawa N., Leopold P. L., Hackett N. R., Ferris B., Worgall S., Falck-Pedersen E., Crystal R. G.. 1999; Fiber swap between adenovirus subgroups B and C alters intracellular trafficking of adenovirus gene transfer vectors. Journal of Virology73:6056–6065
    [Google Scholar]
  41. Miyazawa N., Crystal R. G., Leopold P. L.. 2001; Adenovirus serotype 7 retention in a late endosomal compartment prior to cytosol escape is modulated by fiber protein. Journal of Virology75:1387–1400
    [Google Scholar]
  42. Mori T., Arakawa H., Tokino T., Mineura K., Nakamura Y.. 1999; Significant increase of adenovirus infectivity in glioma cell lines by extracellular domain of hCAR. Oncology Research11:513–521
    [Google Scholar]
  43. Musgrave D. S., Bosch P., Lee J. Y., Pelinkovic D., Ghivizzani S. C., Whalen J., Niyibizi C., Huard J.. 2000; Ex vivo gene therapy to produce bone using different cell types. Clinical Orthopaedics Research378:290–305
    [Google Scholar]
  44. Peitsch M. C.. 1995; Protein modeling by e-mail. Biotechnology13:658–660
    [Google Scholar]
  45. Pickles R. J., Fahrner J. A., Petrella J. M., Boucher R. C., Bergelson J. M.. 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. Journal of Virology74:6050–6057
    [Google Scholar]
  46. Piedra P. A., Poveda G. A., Ramsey B., McCoy K., Hiatt P. W.. 1998; Incidence and prevalence of neutralizing antibodies to the common adenoviruses in children with cystic fibrosis: implication for gene therapy with adenovirus vectors. Pediatrics101:1013–1019
    [Google Scholar]
  47. Rebel V. I., Hartnett S., Denham J., Chan M., Finberg R., Sieff C. A.. 2000; Maturation and lineage-specific expression of the coxsackie and adenovirus receptor in hematopoietic cells. Stem Cells18:176–182
    [Google Scholar]
  48. Reynolds P. N., Zinn K. R., Gavrilyuk V. D., Balyasnikova I. V., Rogers B. E., Buchsbaum D. J., Wang M. H., Miletich D. J., Grizzle W. E., Douglas J. T., Danilov S. M., Curiel D. T.. 2000; A targetable, injectable adenoviral vector for selective gene delivery to pulmonary endothelium in vivo . Molecular Therapy2:562–578
    [Google Scholar]
  49. Roelvink P. W., Lizonova A., Lee J. G., Li Y., Bergelson J. M., Finberg R. W., Brough D. E., Kovesdi I., Wickham T. J.. 1998; The coxsackievirus–adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. Journal of Virology72:7909–7915
    [Google Scholar]
  50. Roelvink P. W., Lee G. M., Einfeld D. A., Kovesdi I., Wickham T. J.. 1999; Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing Adenoviridae . Science286:1568–1571
    [Google Scholar]
  51. Russell W. C.. 2000; Update on adenovirus and its vectors. Journal of General Virology81:2573–2604
    [Google Scholar]
  52. Russell D. W., Hirata R. K.. 1998; Human gene targeting by viral vectors. Nature Genetics18:325–330
    [Google Scholar]
  53. Schiedner G., Morral N., Parks R. J., Wu Y., Koopmans S. C., Langston C., Graham F. L., Beaudet A. L., Kochanek S.. 1998; Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nature Genetics18:180–183
    [Google Scholar]
  54. Segerman A., Mei Y. F., Wadell G.. 2000; Adenovirus types 11p and 35p show high binding efficiencies for committed hematopoietic cell lines and are infective to these cell lines. Journal of Virology74:1457–1467
    [Google Scholar]
  55. Shayakhmetov D. M., Lieber A.. 2000; Dependence of adenovirus infectivity on length of the fiber shaft domain. Journal of Virology74:10274–10286
    [Google Scholar]
  56. Thomas C. E., Schiedner G., Kochanek S., Castro M. G., Lowenstein P. R.. 2000; Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases. Proceedings of the National Academy of Sciences, USA97:7482–7487
    [Google Scholar]
  57. Tomko R. P., Johansson C. B., Totrov M., Abagyan R., Frisen J., Philipson L.. 2000; Expression of the adenovirus receptor and its interaction with the fiber knob. Experimental Cell Research255:47–55
    [Google Scholar]
  58. Toyoda K., Ooboshi H., Chu Y., Fasbender A., Davidson B. L., Welsh M. J., Heistad D. D.. 1998; Cationic polymer and lipids enhance adenovirus-mediated gene transfer to rabbit carotid artery. Stroke29:2181–2188
    [Google Scholar]
  59. Trask T. W., Trask R. P., Aguilar-Cordova E., Shine H. D., Wyde P. R., Goodman J. C., Hamilton W. J., Rojas-Martinez A., Chen S. H., Woo S. L., Grossman R. G.. 2000; Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. Molecular Therapy1:195–203
    [Google Scholar]
  60. Wadell G.. 1999; Adenoviruses ( Adenoviridae ): general features. In Encyclopaedia of Virology pp1–7 Edited by Webster R. G., Granoff A.. London: Academic Press;
    [Google Scholar]
  61. van Raaij M. J., Louis N., Chroboczek J., Cusack S.. 1999; Structure of the human adenovirus serotype 2 fiber head domain at 1·5 Å resolution. Virology262:333–343
    [Google Scholar]
  62. Wickham T. J., Mathias P., Cheresh D. A., Nemerow G. R.. 1993; Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment. Cell73:309–319
    [Google Scholar]
  63. Wood M. J., Charlton H. M., Wood K. J., Kajiwara K., Byrnes A. P.. 1996; Immune responses to adenovirus vectors in the nervous system. Trends in Neuroscience19:497–501
    [Google Scholar]
  64. Xia D., Henry L. J., Gerard R. D., Deisenhofer J.. 1994; Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1·7 Å resolution. Structure2:1259–1270
    [Google Scholar]
  65. Zabner J., Chillon M., Grunst T., Moninger T. O., Davidson B. L., Gregory R., Armentano D.. 1999; A chimeric type 2 adenovirus vector with a type 17 fiber enhances gene transfer to human airway epithelia. Journal of Virology73:8689–8695
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-6-1299
Loading
/content/journal/jgv/10.1099/0022-1317-83-6-1299
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error