Characterization of the recombinant adenovirus vector AdYB-1: Implications for oncolytic vector development

Journal of Virology

Volumn 80, Issue 8, 2006, Pages 3904-3911

  Glockzin, Gabriel ^a,b   Mantwill, Klaus ^a   Jurchott, Karsten ^c   Bernshausen, Alexandra ^a   Ladhoff, Axel ^c   Royer, Hans Dieter ^d   Gansbacher, Bernd ^a   Holm, Per Sonne ^a,e  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

^e XVir Therapeutics GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

Y BOX BINDING PROTEIN 1;

ADENOVIRUS VECTOR; ADENOVIRUS VECTOR ADYB 1; ARTICLE; CANCER; CANCER THERAPY; CELL DEATH; CELL KILLING; CONTROLLED STUDY; CULTURE MEDIUM; CYTOLYSIS; DNA REPLICATION; GENE DELETION; GENE THERAPY; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; ONCOLYTIC VIRUS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR CELL LINE; VIRUS CHARACTERIZATION; VIRUS PARTICLE; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS VECTOR;

ADENOVIRIDAE; ADENOVIRUS E1B PROTEINS; ADENOVIRUS E3 PROTEINS; APOPTOSIS; CELL NUCLEUS; CYTOPATHOGENIC EFFECT, VIRAL; DNA-BINDING PROTEINS; GENETIC VECTORS; HUMANS; ONCOLYTIC VIROTHERAPY; RECOMBINATION, GENETIC; VIRION; VIRUS REPLICATION;

ADENOVIRIDAE; CYTOMEGALOVIRUS;

EID: 33645772721     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.8.3904-3911.2006     Document Type: Article

References (56)

1. Babiss, L. E., H. S. Ginsberg, and J. E. Darnell. 1995. Adenovirus E1B proteins are required for accumulation of late viral mRNA and for effects on cellular mRNA translation and transport. Mol. Cell. Biol. 5:2552-2558.
2. Bargou, R. C., K. Jurchott, C. Wagener, S. Bergmann, S. Metzner, K. Bommert, K. Y. Mapara, K. J. Winzer, M. Dietel, B. Doerken, and H. D. Royer. 1997. Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Nat. Med. 3:447-450.
3. Bett, A. J., V. Krougliak, and F. L. Graham. 1995. DNA sequence of the deletion/insertion in early region 3 of Ad5 dl 309. Virus Res. 39:75-82.
4. Bett, A. J., W. Haddara, L. Prevec, and F. L. Graham. 1994. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. USA 91:8802-8806.
5. Boulakia, C. A., G. Chen, F. W. Ng, J. G. Teodore, P. E. Branton, D. W. Nicholson, G. G. Poirer, and G. C. Shore. 1996. Bcl-2 and adenovirus E1B-19kDA protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene 12:529-535.
6. Chen, C. Y., R. Gherzi, J. S. Andersen, G. Gaietta, K. Jurchott, H. D. Royer, M. Mann, and M. Karin. 2000. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14:1236-1248.
7. Didier, K., J. Schiffenbauer, S. L. Woulfe, M. Zacheis, and B. D. Schwattz. 1998. Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II Y box. Proc. Natl. Acad. Sci. USA 85:7322-7326.
8. Dobner, T., N. Horikoshi, S. Rubenwolf, and T. Shenk. 1996. Blockage by adenovirus E4orf6 of transcriptional activation by the p53 tumor suppressor. Science 7:1470-1473.
9. Doronin, K., K. Toth, M. Kuppuswamy, P. Ward, A. Tollefson, and W. Wold. 2000. Tumor-specific, replication-competent adenovirus vectors overexpressing the adenovirus death protein. J. Virol. 74:6147-6155.
10. Gimenez-Bonafe, P., M. N. Fedoruk, T. G. Whitmore, M. Akbari, J. L. Ralph, S. Ettinger, M. E. Gleave, and C. C. Nelson. 2004. YB-1 is upregulated during prostate cancer progression and increases P-glycoprotein activity. Prostate 15:337-349.
11. Goldenberg, C. J., R. Rosenthal, S. Bhaduri, and H. Raskas. 1980. Coordinate regulation of two cytoplasmic RNA species transcribed from early region 2 of the adenovirus 2 genome. J. Virol. 38:932-939.
12. Halbert, D. N., J. R. Cutt, and T. Shenk. 1995. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J. Virol. 56:250-257.
13. Hawkins, L. K., and T. W. Hermiston. 2001. Gene delivery from the E3 region of replicating human adenovirus: evaluation of the ADP region. Gene Ther. 8:1132-1141.
14. Holm, P. S., H. Lage, S. Bergmann, K. Jurchott, G. Glockzin, A. Bernshausen, K. Mantwill, A. Ladhoff, A. Wichert, J. S. Mymryk, T. Ritter, M. Dietel, B. Gansbacher, and H. D. Royer. 2004. Multidrug-resistant cancer cells facilitate E1-independent adenoviral replication: impact for cancer gene therapy. Cancer Res. 64:322-328.
15. Holm, P. S., S. Bergmann, K. Jurchott, H. Lage, K. Brand, A. Ladhoff, K. Mantwill, D. T. Curiel, M. Dobbelstein, M. Dietel, B. Gansbacher, and H. D. Royer. 2002. YB-1 relocates to the nucleus in adenovirus-infected cells and facilitates viral replication by inducing E2 gene expression through the E2 late promoter. J. Biol. Chem. 277:10427-10434.
16. Huang, M., and P. Hearing. 1999. Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. J. Virol. 63:2605-2615.
17. Izumi, H., T. Imamura, G. Nagatani, T. Ise, T. Murakami, H. Uramoto, T. Torigoe, H. Ishiguchi, Y. Yoshida, M. Nomoto, T. Okamoto, T. Uchiumi, M. Kuwano, K. Funa, and K. Kohno. 2001. Y box-binding protein-1 binds preferentially to single-stranded nucleic acids and exhibits 3′-5′ exonuclease activity. Nucleic Acids Res. 29:1200-1207.
18. Janz, M., N. Harbeck, P. Dettmar, U. Berger, A. Schmidt, K. Jurchott, M. Schmitt, and H. D. Royer. 2002. Y-box factor YB-1 predicts drug resistance and patient outcome in breast cancer independent of clinically relevant tumor biologic factors HER2, uPA and PAI-1. Int. J. Cancer 98:278-282.
19. Jones, N., and T. Shenk. 1978. Isolation of deletion and substitution mutants of adenovirus type 5. Cell 13:181-188.
20. Jurchott, K., S. Bergmann, U. Stein, W. Walther, M. Janz, I. Manni, G. Piaggio, E. Fietzel, M. Dietel, and H. D. Royer. 2003. YB-1 as a cell cycle-regulated transcription factor facilitating cyclin A and cyclin B1 gene expression. J. Biol. Chem. 278:27988-27996.
21. Kamura, T., H. Yahata, S. Amada, S. Ogawa, T. Sonoda, H. Kobayashi, M. Mitsumoto, K. Kohno, M. Kuwano, and H. Nakano. 1999. Is nuclear expression of Y-box binding protein-1 a new prognostic factor in ovarian serous adenocarcinoma? Cancer 85:2450-2454.
22. Kohno, K., H. Izumi, T. Uchiumi, M. Ashizuka, and M. Kuwano. 2003. The pleiotropic functions of the Y-box-binding protein, YB-1. BioEssays 25:691-698.
23. Kovesdi, I., R. Reichel, and J. R. Nevins. 1986. Identification of a cellular transcription factor involved in E1A trans-activation. Cell 45:219-228.
24. Kuwano, M., T. Uchiumi, H. Hayakawa, M. Ono, M. Wada, H. Izumi, and K. Kohno. 2003. The basic and clinical implications of ABC transporters, Y-box-binding protein (YB-1) and angiogenesis-related factors in human malignancies. Cancer Sci. 94:9-14.
25. Lasham, A., E. Lindridge, F. Rudert, R. Onrust, and J. Watson. 2000. Regulation of the human fas promoter by YB-1, Pur-α and AP-1 transcription factors. Gene 252:1-13.
26. Lasham, A., S. Moloney, T. Hale, C. Homer, Y. F. Zhang, J. G. Murison, A. W. Braithwaite, and J. Watson. 2003. The Y-box-binding protein, YB-1, is a potential negative regulator of the p53 tumor suppressor. J. Biol. Chem. 278:35516-35523.
27. Leist, M., and M. Jaattela. 2001. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2:1-10.
28. Lillie, J. W., and M. R. Green. 1989. Transcription activation by the adenovirus E1a protein. Nature 338:39-44.
29. Marcellus, R. C., H. Chan, D. Paquette, S. Thirlwell, D. Boivin, and P. E. Branton. 2000. Induction of p53-independent apoptosis by the adenovirus E4orf4 protein requires binding to the Ba subunit of protein phosphatase 2A. J. Virol. 74:7869-7877.
30. Marcellus, R. C., J. G. Teodoro, T. Wu, D. E. Brough, G. Ketner, G. C. Shore, and P. E. Branton. 1996. Adenovirus type 5 early region 4 is responsible for E1A-induced p53-independent apoptosis. J. Virol. 70:6207-6215.
31. Marcellus, R. C., J. N. Lavoie, D. Boivin, G. C. Shore, G. Ketner, and P. E. Branton. 1999. The early region 4 orf4 protein of human adenovirus type 5 induces p53-independent cell death by apoptosis. J. Virol. 72:7144-7153.
32. Marenstein, D. R., M. Ocampo, M. K. Chan, A. Altamirano, A. K. Basu, R. J. Boorstein, R. P. Cunningham, and G. Teebor. 2001. Stimulation of human endonuclease III by Y box-binding protein 1 (DNA-binding protein B). Interaction between a base excision repair enzyme and a transcription factor. J. Biol. Chem. 276:21242-21249.
33. Martin, M., and A. Berk. 1999. Adenovirus E1B-55K represses p53 activation in vitro. J. Virol. 72:3146-3154.
34. McCormick, F. 2000. Interactions between adenovirus proteins and the p53 pathway: the development of ONYX-015. Cancer Biol. 10:453-459.
35. Mohamed Abou El Hassan, A. I., I. van der Meulen-Muileman, S. Abbas, and F. A. E. Kruyt. 2004. Conditionally replicating adenoviruses kill tumor cells via a basic apoptotic machinery-independent mechanism that resembles necrosis-like programmed cell death. J. Virol. 78:12243-12251.
36. Nelson, J. E., and M. A. Kay. 1998. Persistence of recombinant adenovirus in vivo is not dependent on vector DNA replication. J. Virol. 71:8902-8907.
37. Nevins, J. R. 1981. Mechanism of activation of early viral transcription by the adenovirus E1A gene product. Cell 26:213-220.
38. Oda, Y., A. Sakamoto, N. Shinohara, T. Ogha, T. Uchiumi, K. Kohno, M. Tsuneyoshi, M. Kuwano, and Y. Iwamoto. 1999. Nuclear expression of YB-1 correlates with P-glycoprotein expression in human osteosarcoma. Clin. Cancer Res. 4:2273-2277.
39. Oda, Y., Y. Ohishi, T. Saito, E. Hinoshita, T. Schiumi, N. Kinukawa, Y. Iwamoto, K. Kohno, M. Kuwano, and M. Tsuneyoshi. 2003. Nuclear expression of Y-box-binding protein-1 correlates with P-glycoprotein and topoisomerase IIα expression, and with poor prognosis in synovial sarcoma. J. Pathol. 199:251-258.
40. Okamoto, T., H. Izumi, T. Imamura, H. Takano, T. Ise, T. Uchiumi, M. Kuwano, and K. Kohno. 2000. Direct interaction of p53 with the Y-box binding protein, YB-1: a mechanism for regulation of the human gene expression. Oncogene 19:6194-6202.
41. Ornelles, D. A., and T. Shenk. 1991. Localization of the adenovirus early region 1B 55-kilodalton protein during lytic infection: association with nuclear viral inclusions requires the early region 4 34-kilodalton protein. J. Virol. 65:424-439.
42. Puvion-Dutilleul, F., J. Pedron, and C. Cajean-Feroldi. 1984. Identification of intranuclear structures containing the 72K DNA-binding protein of human adenovirus type 5. Eur. J. Cell Biol. 34:313-322.
43. Querido, E., M. R. Morrison, H. Chu-Pham-Dang, H. Thirlwell, D. Boivin, and P. E. Branton. 2001. Identification of three functions of the adenovirus E4orf6 protein that mediate p53 degradation by the E4orf6-E1B55K complex. J. Virol. 75:699-709.
44. Shen, Y., G. Kitzes, J. A. Nye, A. Fattaey, and T. Hermiston. 2001. Analysis of single-amino-acid substitution mutants of adenovirus type 5 E1B-55K protein. J. Virol. 75:4298-4307.
45. Shenk, T. 1996. Adenoviridae: the viruses and their replication, p. 2111-2147. In D. M. Knipe, B. Roizman, P. M. Howley, T. P. Monath, S. E. Straus, R. M. Chanock, J. L. Melnick, and B. N. Fields (ed.), Fields virology, 3rd ed. Lippincott Williams and Wilkins, Baltimore, Md.
46. Shibahara, K., K. Sugio, T. Osaki, T. Uchiumi, Y. Maehara, K. Kohno, K. Yasumoto, K. Sugimachi, and M. Kuwano. 2001. Nuclear expression of the Y-box binding protein, YB-1, as a novel marker of disease progression in non-small cell lung cancer. Clin. Cancer Res. 7:3151-3155.
47. Shibao, K., H. Takano, Y. Nakayama, K. Okazaki, N. Nagata, H. Izumi, T. Uchiumi, M. Kuwano, K. Kohno, and H. Itoh. 1999. Enhanced coexpression of YB-1 and DNA topoisomerase IIα genes in human colorectal carcinomas. Int. J. Cancer 83:732-737.
48. Swaminathan, S., and B. Thimmapaya. 1995. Regulation of adenovirus E2 transcription unit. Curr. Top. Microbiol. Immunol. 199:177-194.
49. Teodoro, J. G., and P. E. Branton. 1998. Regulation of p53-dependent apoptosis, transcriptional repression, and cell transformation by phosphorylation of the 55-kilodalton E1B protein of human adenovirus type 5. J. Virol. 71:3620-3627.
50. Teodoro, J. G., G. C. Shore, and P. E. Branton. 1995. Adenovirus E1A proteins induce apoptosis by both p53-dependent and p53-independent mechanisms. Oncogene 11:467-474.
51. 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.
52. Toth, K., H. Djeha, B. Ying, A. E. Tollefson, M. Kuppuswamy, K. Doronin, P. Krajcsi, K. Lipinski, C. J. Wrighton, and W. S. Wold. 2004. An oncolytic vector combining enhanced cell-to-cell spreading, mediated by the ADP cytolytic protein, with selective replication in cancer cells with deregulated wnt signaling. Cancer Res. 64:3638-3644.
53. Toth, K., V. Tarakanova, K. Doronin, P. Ward, M. Kuppuswamy, J. E. Locke, J. E. Dawson, H. J. Kim, and W. S. Wold. 2003. Radiation increases the activity of oncolytic adenovirus cancer gene therapy vectors that overexpress the ADP (E3-11.6K) protein. Cancer Gene Ther. 10:193-200.
54. Weinberg, D. H., and G. Ketner. 1996. Adenoviral early region 4 is required for efficient viral DNA replication and for late gene expression. J. Virol. 57:833-838.
55. Wienzek, S., J. Roth, and M. Dobbelstein. 2000. E1B 55-kilodalton oncoproteins of adenovirus type 5 and 12 inactivate and relocalize p53, but not p51 or p73, and cooperate with E4orf6 proteins to destabilize p53. J. Virol. 74:193-202.
56. Yu, D. C., Y. Chen, J. Dilley, and D. R. Henderson. 1999. The addition of adenovirus type 5 region E3 enables calydon virus 787 to eliminate distant prostate tumor xenografts. Cancer Res. 59:4200-4203.