Replication properties of human adenovirus in vivo and in cultures of primary cells from different animal species

Journal of Virology

Volumn 80, Issue 7, 2006, Pages 3549-3558

  Jogler, Christian ^a,b   Hoffmann, Dennis ^a   Theegarten, Dirk ^a,c   Grunwald, Thomas ^a   Überla, Klaus ^a   Wildner, Oliver ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; VIRUS DNA;

ADENOVIRUS; ADENOVIRUS VECTOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; VIRUS INFECTION; VIRUS REPLICATION; VIRUS VIRULENCE;

ADENOVIRUSES, HUMAN; ANIMALS; CELL LINE; CRICETINAE; CYTOPATHOGENIC EFFECT, VIRAL; DNA, VIRAL; FEMALE; FLOW CYTOMETRY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; GUINEA PIGS; HELA CELLS; HUMANS; INFLAMMATION; INJECTIONS, INTRAVENOUS; KIDNEY; LIVER; LUNG; MARMOTA; MICE; MICE, INBRED BALB C; RABBITS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGMODONTINAE; SUS SCROFA; TRANSDUCTION, GENETIC; VIRAL LOAD; VIRUS REPLICATION;

ADENOVIRIDAE; ANIMALIA; DNA VIRUSES; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS TYPE 5; ORYCTOLAGUS CUNICULUS; RODENTIA; SUIDAE; SUS SCROFA;

EID: 33645230398     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.7.3549-3558.2006     Document Type: Article

References (69)

1. Akusjarvi, G., and U. Pettersson. 1978. Nucleotide sequence at the junction between the coding region of the adenovirus 2 hexon messenger RNA and its leader sequence. Proc. Natl. Acad. Sci. USA 75:5822-5826.
2. Alemany, R., K. Suzuki, and D. T. Curiel. 2000. Blood clearance rates of adenovirus type 5 in mice. J. Gen. Virol. 81:2605-2609.
3. Arola, M., O. Ruuskanen, T. Ziegler, and T. T. Salmi. 1995. Respiratory virus infections during anticancer treatment in children. Pediatr. Infect. Dis. J. 14:690-694.
4. Batshaw, M. L., J. M. Wilson, S. Raper, M. Yudkoff, and M. B. Robinson. 1999. Recombinant adenovirus gene transfer in adults with partial ornithine transcarbamylase deficiency (OTCD). Hum. Gene Ther. 10:2419-2437.
5. Blair, G. E., S. C. Dixon, S. A. Griffiths, and M. E. Zajdel. 1989. Restricted replication of human adenovirus type 5 in mouse cell lines. Virus Res. 14:339-346.
6. Blanke, C., C. Clark, E. R. Broun, G. Tricot, I. Cunningham, K. Cornetta, A. Hedderman, and R. Hromas. 1995. Evolving pathogens in allogeneic bone marrow transplantation: increased fatal adenoviral infections. Am. J. Med. 99:326-328.
7. Braithwaite, A. W., J. D. Murray, and A. J. Bellett. 1981. Alterations to controls of cellular DNA synthesis by adenovirus infection. J. Virol. 39:331-340.
8. Brann, T., D. Kayda, R. M. Lyons, P. Shirley, S. Roy, M. Kaleko, and T. Smith. 1999. Adenoviral vector-mediated expression of physiologic levels of human factor VIII in nonhuman primates. Hum. Gene Ther. 10:2999-3011.
9. Cames, B., J. Rahier, G. Burtomboy, d. G. de Ville, R. Reding, M. Lamy, J. B. Otte, and E. M. Sokal. 1992. Acute adenovirus hepatitis in liver transplant recipients. J. Pediatr. 120:33-37.
10. Carrigan, D. R. 1997. Adenovirus infections in immunocompromised patients. Am. J. Med. 102:71-74.
11. Dobbelstein, M. 2004. Replicating adenoviruses in cancer therapy. Curr. Top. Microbiol. Immunol. 273:291-334.
12. Duncan, S. J., F. C. Gordon, D. W. Gregory, J. L. McPhie, R. Postlethwaite, R. White, and H. N. Willcox. 1978. Infection of mouse liver by human adenovirus type 5. J. Gen. Virol. 40:45-61.
13. Edwards, K. M., J. Thompson, J. Paolini, and P. F. Wright. 1985. Adenovirus infections in young children. Pediatrics 76:420-424.
14. Flomenberg, P., J. Babbitt, W. R. Drobyski, R. C. Ash, D. R. Carrigan, G. V. Sedmak, T. McAuliffe, B. Camitta, M. M. Horowitz, and N. Bunin. 1994. Increasing incidence of adenovirus disease in bone marrow transplant recipients. J. Infect. Dis. 169:775-781.
15. Freytag, S. O., H. Stricker, J. Pegg, D. Paielli, D. G. Pradhan, J. Peabody, M. Peralta-Venturina, X. Xia, S. Brown, M. Lu, and J. H. Kim. 2003. Phase I study of replication-competent adenovirus-mediated double-suicide gene therapy in combination with conventional-dose three-dimensional conformal radiation therapy for the treatment of newly diagnosed, intermediate- to high-risk prostate cancer. Cancer Res. 63:7497-7506.
16. Fueyo, J., C. Gomez-Manzano, R. Alemany, P. S. Lee, T. J. McDonnell, P. Mitlianga, Y. X. Shi, V. A. Levin, W. K. Yung, and A. P. Kyritsis. 2000. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene 19:2-12.
17. Ganly, I., V. Mautner, and A. Balmain. 2000. Productive replication of human adenoviruses in mouse epidermal cells. J. Virol. 74:2895-2899.
18. Ginsberg, H. S., R. L. Horswood, R. M. Chanock, and G. A. Prince. 1990. Role of early genes in pathogenesis of adenovirus pneumonia. Proc. Natl. Acad. Sci. USA 87:6191-6195.
19. Ginsberg, H. S., U. Lundholm-Beauchamp, R. L. Horswood, B. Pernis, W. S. Wold, R. M. Chanock, and G. A. Prince. 1989. Role of early region 3 (E3) in pathogenesis of adenovirus disease. Proc. Natl. Acad. Sci. USA 86:3823-3827.
20. Ginsberg, H. S., L. L. Moldawer, P. B. Sehgal, M. Redington, P. L. Kilian, R. M. Chanock, and G. A. Prince. 1991. A mouse model for investigating the molecular pathogenesis of adenovirus pneumonia. Proc. Natl. Acad. Sci. USA 88:1651-1655.
21. Graham, F. L., and L. Prevec. 1995. Methods for construction of adenovirus vectors. Mol. Biotechnol. 3:207-220.
22. Graham, F. L., and L. Prevec. 1992. Adenovirus-based expression vectors and recombinant vaccines. Biotechnology 20:363-390.
23. 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.
24. Green, N. K., C. W. Herbert, S. J. Hale, A. B. Hale, V. Mautner, R. Harkins, T. Hermiston, K. Ulbrich, K. D. Fisher, and L. W. Seymour. 2004. Extended plasma circulation time and decreased toxicity of polymer-coated adenovirus. Gene Ther. 11:1256-1263.
25. Hallden, G., R. Hill, Y. Wang, A. Anand, T. C. Liu, N. R. Lemoine, J. Francis, L. Hawkins, and D. Kim. 2003. Novel immunocompetent murine tumor models for the assessment of replication-competent oncolytic adenovirus efficacy. Mol. Ther. 8:412-424.
26. Hemminki, A., A. Kanerva, E. J. Kremer, G. J. Bauerschmitz, B. F. Smith, B. Liu, M. Wang, R. A. Desmond, A. Keriel, B. Barnett, H. J. Baker, G. P. Siegal, and D. T. Curiel. 2003. A canine conditionally replicating adenovirus for evaluating oncolytic virotherapy in a syngeneic animal model. Mol. Ther. 7:163-173.
27. Hierholzer, J. C. 1992. Adenoviruses in the immunocompromised host. Clin. Microbiol. Rev. 5:262-274.
28. Hilleman, M. R., and J. H. Werner. 1954. Recovery of new agents from patients with acute respiratory illness. Proc. Soc. Exp. Biol. Med. 85:183-188.
29. Janner, D., A. M. Petru, D. Belchis, and P. H. Azimi. 1990. Fatal adenovirus infection in a child with acquired immunodeficiency syndrome. Pediatr. Infect. Dis. J. 9:434-436.
30. Kelly, T. J., Jr., and A. M. Lewis, Jr. 1973. Use of nondefective adenovirus-simian virus 40 hybrids for mapping the simian virus 40 genome. J. Virol. 12:643-652.
31. Khuri, F. R., J. Nemunaitis, I. Ganly, J. Arseneau, I. F. Tannock, L. Romel, M. Gore, J. Ironside, R. H. MacDougall, C. Heise, B. Randlev, A. M. Gillenwater, P. Bruso, S. B. Kaye, W. K. Hong, and D. H. Kirn. 2000. A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat. Med. 6:879-885.
32. Krilov, L. R., M. H. Kaplan, M. Frogel, and L. G. Rubin. 1990. Fatal adenovirus disease and human immunodeficiency virus infection. Pediatr. Infect. Dis. J. 9:753.
33. Kvist, S., L. Ostberg, H. Persson, L. Philipson, and P. A Peterson. 1978. Molecular association between transplantation antigens and cell surface antigen in adenovirus-transformed cell line. Proc. Natl. Acad. Sci. USA 75:5674-5678.
34. Lichtenstein, D. L., and W. S. Wold. 2004. Experimental infections of humans with wild-type adenoviruses and with replication-competent adenovirus vectors: replication, safety, and transmission. Cancer Gene Ther. 11:819-829.
35. Lieber, A., C. Y. He, L. Meuse, D. Schowalter, I. Kirillova, B. Winther, and M. A. Kay. 1997. The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J. Virol. 71:8798-8807.
36. Lieber, M., B. Smith, A. Szakal, W. Nelson-Rees, and G. Todaro. 1976. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int. J. Cancer 17:62-70.
37. Lozier, J. N., G. Csako, T. H. Mondoro, D. M. Krizek, M. E. Metzger, R. Costello, J. G. Vostal, M. E. Rick, R. E. Donahue, and R. A. Morgan. 2002. Toxicity of a first-generation adenoviral vector in rhesus macaques. Hum. Gene Ther. 13:113-124.
38. Michaels, M. G., M. Green, E. R. Wald, and T. E. Starzl. 1992. Adenovirus infection in pediatric liver transplant recipients. J. Infect. Dis. 165:170-174.
39. Mittereder, N., K. L. March, and B. C. Trapnell. 1996. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J. Virol. 70:7498-7509.
40. Morral, N., W. K. O'Neal, K. Rice, M. M. Leland, P. A. Piedra, E. guilar-Cordova, K. D. Carey, A. L. Beaudet, and C. Langston. 2002. Lethal toxicity, severe endothelial injury, and a threshold effect with high doses of an adenoviral vector in baboons. Hum. Gene Ther. 13:143-154.
41. Morris, J. C., and O. Wildner. 2000. Therapy of head and neck squamous cell carcinoma with an oncolytic adenovirus depressing HSV-tk. Mol. Ther. 1:56-62.
42. Myerowitz, R. L., H. Stalder, M. N. Oxman, M. J. Levin, M. Moore, J. D. Leith, N. M. Gantz, J. C. Hierholzer, and J. C. Hierholzer. 1975. Fatal disseminated adenovirus infection in a renal transplant recipient. Am. J. Med. 59:591-598.
43. Nemunaitis, J., F. Khuri, I. Ganly, J. Arseneau, M. Posner, E. Vokes, J. Kuhn, T. McCarty, S. Landers, A. Blackburn, L. Romel, B. Randlev, S. Kaye, and D. Kirn. 2001. Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer. J. Clin. Oncol. 19:289-298.
44. Odio, C., G. H. McCracken, Jr., and J. D. Nelson. 1984. Disseminated adenovirus infection: a case report and review of the literature. Pediatr. Infect. Dis. 3:46-49.
45. Prince, G. A., D. D. Porter, A. B. Jenson, R. L. Horswood, R. M. Chanock, and H. S. Ginsberg. 1993. Pathogenesis of adenovirus type 5 pneumonia in cotton rats (Sigmodon hispidus). J. Virol. 67:101-111.
46. Ram, Z., K. W. Culver, E. M. Oshiro, J. J. Viola, H. L. DeVroom, E. Otto, Z. Long, Y. Chiang, G. J. McGarrity, L. M. Muul, D. Katz, R. M. Blaese, and E. H. Oldfield. 1997. Therapy of malignant brain tumors by intratumoral implantation of retroviral vector-producing cells. Nat. Med. 3:1354-1361.
47. Roth, J. A., and R. J. Cristiano. 1997. Gene therapy for cancer: what have we done and where are we going? J. Natl. Cancer Inst. 89:21-39.
48. Rowe, W. P., R. J. Huebner, L. K. Gilmore, R. H. Parrot, and T. G. Ward. 1953. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc. Soc. Exp. Biol. Med. 84:570-573.
49. Scherer, W. F., J. T. Syverton, and G. O. Gey. 1953. Studies on the propagation in vitro of poliomyelitis viruses. J. Exp. Med. 97:695-709.
50. Shu, S. Y., and S. A. Rosenberg. 1985. Adoptive immunotherapy of newly induced murine sarcomas. Cancer Res. 45:1657-1662.
51. Sterman, D. H., J. Treat, L. A. Litzky, K. M. Amin, L. Coonrod, K. Molnar-Kimber, A. Recio, L. Knox, J. M. Wilson, S. M. Albelda, and L. R. Kaiser. 1998. Adenovirus-mediated herpes simplex virus thymidine kinase/ganciclovir gene therapy in patients with localized malignancy: results of a phase 1 clinical trial in malignant mesothelioma. Hum. Gene Ther. 9:1083-1092.
52. Suzuki, K., R. Alemany, M. Yamamoto, and D. T. Curiel. 2002. The presence of the adenovirus E3 region improves the oncolytic potency of conditionally replicative adenoviruses. Clin. Cancer Res. 8:3348-3359.
53. Todaro, G. J., and H. Green. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313.
54. Tollefson, A. E., A. Scaria, T. W. Hermiston, J. S. Ryerse, L. J. Wold, and W. S. Wold. 1996. The adenovirus death protein (E3-11.6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. J. Virol. 70:2296-2306.
55. Torres, J. M., C. Alonso, A. Ortega, S. Mittal, F. Graham, and L. Enjuanes. 1996. Tropism of human adenovirus type 5-based vectors in swine and their ability to protect against transmissible gastroenteritis coronavirus. J. Virol. 70:3770-3780.
56. Wadler, S., B. Yu, J. Y. Tan, R. Kaleya, A. Rozenblit, D. Makower, M. Edelman, M. Lane, E. Hyjek, and M. Horwitz. 2003. Persistent replication of the modified chimeric adenovirus ONYX-015 in both tumor and stromal cells from a patient with gall bladder carcinoma implants. Clin. Cancer Res. 9:33-43.
57. Wein, L. M., J. T. Wu, and D. H. Kirn. 2003. Validation and analysis of a mathematical model of a replication-competent oncolytic virus for cancer treatment: implications for virus design and delivery. Cancer Res. 63:1317-1324.
58. Wildner, O., R. M. Blaese, and J. C. Morris. 1999. Therapy of colon cancer with oncolytic adenovirus is enhanced by the addition of HSV-tk. Cancer Res. 59:410-413.
59. Wildner, O., D. Hoffmann, C. Jogler, and K. Uberla. 2003. Comparison of HSV-1 thymidine kinase-dependent and -independent inhibition of replication-competent adenoviral vectors by a panel of drugs. Cancer Gene Ther. 10:791-802.
60. Wildner, O., and J. C. Morris. 2000. The Role of the E1B 55 kDa gene in oncolytic adenoviral vectors expressing HSV-tk: assessment of anti-tumor efficacy and toxicity. Cancer Res. 60:4167-4174.
61. Wilson, J. M. 1996. Adenoviruses as gene-delivery vehicles. N. Engl. J. Med. 334:1185-1187.
62. Wolff, G., S. Worgall, R. N. van, W. R. Song, B. G. Harvey, and R. G. Crystal. 1997. Enhancement of in vivo adenovirus-mediated gene transfer and expression by prior depletion of tissue macrophages in the target organ. J. Virol. 71:624-629.
63. Wood, M., P. Perrotte, E. Onishi, M. E. Harper, C. Dinney, L. Pagliaro, and D. R. Wilson. 1999. Biodistribution of an adenoviral vector carrying the luciferase reporter gene following intravesical or intravenous administration to a mouse. Cancer Gene Ther. 6:367-372.
64. Worgall, S., G. Wolff, E. Falck-Pedersen, and R. G. Crystal. 1997. Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum. Gene Ther. 8:37-44.
65. Yang, Y., H. C. Ertl, and J. M. Wilson. 1994. MHC class I-restricted cytotoxic T lymphocytes to viral antigens destroy hepatocytes in mice infected with E1-deleted recombinant adenoviruses. Immunity 1:433-442.
66. Yang, Y., Q. Li, H. C. Ertl, and J. M. Wilson. 1995. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J. Virol. 69:2004-2015.
67. Yang, Y., and J. M. Wilson. 1995. Clearance of adenovirus-infected hepatocytes by MHC class I-restricted CD4+ CTLs in vivo. J. Immunol. 155:2564-2570.
68. Yang, Y., Z. Xiang, H. C. Ertl, and J. M. Wilson. 1995. Upregulation of class I major histocompatibility complex antigens by interferon gamma is necessary for T-cell-mediated elimination of recombinant adenovirus-infected hepatocytes in vivo. Proc. Natl. Acad. Sci. USA 92:7257-7261.
69. Yver, A. 2001. Does detection of circulating ONYX-015 genome by polymerase chain reaction indicate vector replication? J. Clin. Oncol. 19:3155-3157.