Inhibition of NF-κB activation in combination with Bcl-2 expression allows for persistence of first-generation adenovirus vectors in the mouse liver

Journal of Virology

Volumn 72, Issue 11, 1998, Pages 9267-9277

  Lieber, André ^a,d   He, Chen Yi ^a,c   Meuse, Leonard ^a,c   Himeda, Charis ^a   Wilson, Christopher ^b   Kay, Mark A ^a,c  

^a Division of Medical Genetics   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; VIRUS DNA; VIRUS VECTOR; ALPHA 1 ANTITRYPSIN; DNA BINDING PROTEIN; I KAPPA B; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; PRIMER DNA;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE DELETION; GENE EXPRESSION; HUMORAL IMMUNITY; LIVER CELL; MALE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; TRANSGENIC MOUSE; ANIMAL; ANTIBODY PRODUCTION; BIOSYNTHESIS; C3H MOUSE; C57BL MOUSE; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; LIVER; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PATHOLOGY; PATHOPHYSIOLOGY; PROTO ONCOGENE; VIROLOGY; VIRUS GENE;

ADENOVIRIDAE; ALPHA 1-ANTITRYPSIN; ANIMALS; ANTIBODY FORMATION; APOPTOSIS; BASE SEQUENCE; CYTOKINES; DNA PRIMERS; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION; GENE THERAPY; GENES, BCL-2; GENES, VIRAL; GENETIC VECTORS; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION; LIVER; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B;

EID: 0031596240     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.11.9267-9277.1998     Document Type: Article

References (65)

1. Ashany, D., X. Song, E. Lacy, J. Nikolic-Zugic, S. M. Friedman, and K. B. Elkon. 1995. ThI CD4+ lymphocytes delete activated macrophages through the Fas/APO-1 pathway. Proc. Natl. Acad. Sci. USA 92:11225-11229.
2. Baeuerle, P., and D. Baltimore. 1996. NF-κB. ten years after. Cell 87:13-20.
3. Barr, D., J. Tubb, D. Ferguson, A. Scaria, A. Lieber, C. Wilson, J. Perkins, and M. Kay. 1995. Strain related variations in adenoviral mediated transgene expression from mouse hepatocytes in vivo: comparison between immunocompetent and immunodeficient inbred strains. Gene Ther. 2:151-156.
4. Beg, A. A., W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the relA component of NF-κB. Nature 376:167-170.
5. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α-induced cell death. Science 274:782-784.
6. 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.
7. Boucher, R. C. 1996. Current status of CF gene therapy. Trends Genet. 12:81-84.
8. Clesham, G. J., P. J. Adam, D. Proudfoot, P. D. Flynn, S. Efstathiou, and P. L. Weissberg. 1998. High adenoviral loads stimulate NF-κB-dependent gene expression in human vascular smooth muscle cells. Gene Ther. 5:174-180.
9. Deryckere, F., and H.-G. Burger. 1996. Tumor necrosis factor alpha induces the adenovirus early promoter by activation of NF-κB. J. Biol. Chem. 47: 30249-30255.
10. DiDonato, J., F. Mercurio, C. Rosette, J. Wu-Li, H. Suyang, S. Ghosh, and M. Karin. 1996. Mapping of the inducible IκB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 16:1295-1304.
11. Elkon, K. B., C.-C. Liu, J. G. Gall, J. Trevejo, M. W. Marino, K. A Abrahamsen, X. Song, J. L. Zhou, L. J. Old, R. G. Crystal, and E. Falck-Pedersen. 1997. Tumor necrosis factor alpha plays a central role in immune-mediated clearance of adenoviral vectors. Proc. Natl. Acad. Sci. USA 94:9814-9819.
12. Gilmore, T. D. 1997. The Rel/NF-κB signal transduction pathway. Cancer Biol. 8:61-62.
13. Gooding, L. R. 1994. Regulation of TNF-mediated cell death and inflammation by human adenoviruses. Infect. Agents Dis. 3:106-115.
14. Grimm, S., M. K. A. Bauer, P. A. Baeuerle, and K. Schulze-Osthoff. 1996. Bcl-2 down-regulates the activity of transcription factor NF-κB induced upon apoptosis. J. Cell Biol. 134:13-23.
15. Henkart, P. 1994. Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. Immunity 1:343-346.
16. Hickman, J. A. 1996. Apoptosis and chemotherapy resistance. Eur. J. Cancer 32A:921-926.
17. Hitt, M. M., C. L. Addison, and F. L. Graham. 1997. Human adenoviral vectors for gene transfer into mammalian cells. Adv. Pharmacol. 40:137-205.
18. Ilan, Y., G. Droguett, and M. S. Horwitz. 1997. Insertion of the adenoviral E3 region into a recombinant viral vector prevents antiviral humoral and cellular immune responses and permits long-term gene expression. Proc. Natl. Acad. Sci. USA 94:2587-2592.
19. Kay, M. A., F. Graham, F. Leland, and S. L. Woo. 1995. Therapeutic serum concentrations of human alphal-antitrypsin after adenoviral-mediated gene transfer into mouse hepatocytes. Hepatology 21:815-819.
20. Kay, M. A., A.-X. Holterman, L. Meuse, A. Gown, H. D. Ochs, P. S. Linsley, and C. B. Wilson. 1995. Long-term hepatic adenovirus-mediated gene expression in mice following CTLA4Ig administration. Nat. Genet. 11:191-197.
21. Kay, M. A., L. Meuse, A. M. Gown, P. Linsley, and C. B. Wilson. 1997. Transient immunomodulation with anti-CD40 ligand antibody and CTLA4Ig enhances persistence and secondary adenovirus-mediated gene transfer into mouse liver. Proc. Natl. Acad. Sci. USA 94:4686-4691.
22. Kiefer, M. C., M. J. Brauer, V. C. Powers, J. J. Wu, S. R. Umansky, L. D. Tomei, and P. J. Barr. 1995. Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 374:736-739.
23. Krajewski, S., M. Krajewska, A. Shabaik, T. Miyashita, H. G. Wang, and J. C. Reed. 1994. Immunohistochemical determination of in vivo distribution of bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145:1323-1326.
24. Kroemer, G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 6:614-620.
25. Lacronique, V., A. Mignon, M. Fabre, B. Viollet, N. Rouquet, T. Molina, A. Porteu, A. Henrion, D. Bouscary, P. Varlet, V. Joulin, and A. Kahn. 1996. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat. Med. 2:80-86.
26. Langer, S. J., and J. Schaak. 1996. 293 cell lines that inducibly express high level adenovirus type 5 precurser terminal protein. Virology 221:172-179.
27. Li, Y., J. Kang, and M. S. Horwitz. 1997. Interaction of an adenovirus 14.7-kilodalton protein inhibitor of tumor necrosis factor alpha cytolysis with a new member of the GTPase superfamily of signal transducers. J. Virol. 71:1576-1582.
28. Lieber, A., C.-Y. He, I. Kirillova, and M. A. Kay. 1996. Recombinant adenoviruses with large deletions generated by Cre-mediated excision exhibit different biological properties compared with first-generation vectors in vitro and in vivo. J. Virol. 70:8944-8960.
29. Lieber, A., C.-Y. He, L. Meuse, D. Schowalter, I. Kirillova, B. Winther, and M. A. Kay. 1997. The role of Kupfer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J. Virol. 71:8798-8807.
30. Lin, K., S.-H. Lee, R. Narayanan, J. M. Baraban, J. M. Hardwick, and R. R. Ratan. 1995. Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-κB. J. Cell Biol. 131:1149-1161.
31. Loeser, P., G. S. Jennings, M. Strauss, and V. Sandig. 1998. Reactivation of the previously silenced cytomegalovirus promoter in the mouse liver: involvement of NF-κB. J. Virol. 72:180-190.
32. Luque, I., and C. Gelinas. 1997. Rel/NF-κB and IκB factors in oncogenesis. Cancer Biol. 8:103-111.
33. Morral, N., W. O'Neal, H. Zbou, C. Langston, and A. Beaudet. 1997. Immune responses to reporter proteins and high viral dose limit duration of expression with adenoviral vectors: comparison of E2a wildtype and E2a deleted vectors. Hum. Gene Ther. 8:1275-1286.
34. Mosialos, G. 1997. The role of rel/NF-κB proteins in viral oncogenesis and the regulation of viral transcription. Cancer Biol. 8:121-129.
35. Neumann, B., T. Machleidt, A. Lifka, K. Pfeffer, D. Vesrweber, T. W. Mak, B. Holzmann, and M. Kronke. 1996. Crucial role of 55-kDa TNF receptor in TNF induced adhesion molecule expression and leukocyte organ infiltration. J. Immunol. 156:1587-1593.
36. Pezzella, F., A. G. Tse, J. L. Cordell, K. A. Pulford, K. C. Gatter, and D. Y. Mason. 1990. Expression of the Bcl-2 oncogene protein is not specific for the 14;18 chromosomal translocation. Am. J. Pathol. 137:225-232.
37. Pftzenmaier, K., H. Wajant, and M. Grell. 1996. Tumor necrosis factor in 1996. Cytokine Growth Factor Rev. 3:271-277.
38. Quin, L. H., Y. Z. Ding, D. R. Pahud, E. Chang, M. J. Imperiale, and J. S. Bromberg. 1997. Promoter attenuation in gene therapy: interferon-gamma and tumor necrosis factor-alpha inhibit transgene expression. Hum. Gene Ther. 8:2019-2029.
39. Rodriguez, I., K. Matsuura, K. Khatib, J. C. Reed, S. Nagata, and P. Vassalli. 1996. A bcl-2 transgene expressed in hepatocytes protects mice from fulminant liver destruction but not from rapid death induced by anti-Fas antibody injection. J. Exp. Med. 183:1031-1036.
40. Roth, S., J. Schurek, and A. M. Gressner. 1997. Expression and release of the latent transforming growth factor beta binding protein by hepatocytes from rat liver. Hepatology 25:1398-1405.
41. Rowell, D. L., L. Eckmann, M. B. Dwinell, S. P. Carpenter, J. L. Raucy, S. K. Yang, and M. F. Kagnoff. 1997. Human hepatocytes express an array of proinflammatory cytokines after agonist stimulation or bacterial invasion. Am. J. Physiol. 273:G322-G332.
42. Scallan, M., T. E. Allsopp, and J. K. Fazakerley. 1997. Bcl-2 acts early to restrict Semliki Forest virus replication and delays virus-induced programmed cell death. J. Virol. 71:1583-1590.
43. Scaria, A., J. A. St-George, R. J. Gregory, R. J. Noelle, S. C. Wadsworth, A. E. Smith, and J. M. Kaplan. 1997. Antibody to CD40 ligand inhibits both humoral and cellular immune responses to adenoviral vectors and facilitates repeated administration to mouse airway. Gene Ther. 4:611-617.
44. Schiedner, G., N. Morral, R. J. Parks, Y. Wu, S. C. Koopmans, C. Langston, F. L. Graham, A. L. Beaudet, and S. Kochanek. 1998. Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nat. Genet. 18:180-183.
45. Schowalter, D. B., L. Meuse, C. B. Wilson, P. S. Linsley, and M. A. Kay. 1997. Constitutive expression of murine CTLA4Ig from a recombinant adenovirus vector results in prolonged transgene expression. Gene Ther. 4:853-860.
46. Schowalter, D. B., C. L. Himeda, B. L. Winther, C. B. Wilson, and M. A. Kay. 1998. Unpublished data.
47. Schroeder, R. A., J. S. Gu, and P. C. Kuo. 1998. Interleukin 1beta-stimulated production of nitric oxide in rat hepatocytes is mediated through endogenous synthesis of interferon gamma. Hepatology 27:711-719.
48. Shenk, T. 1996. Adenoviridae, p. 2111-2148. In B. N. Fields, D. M. Knipe, and P. M. Howley, (ed.), Fields virology, vol. 2. Lippincott-Raven Publisher, Philadelphia, Pa.
49. Shishler, J., C. Yang, B. Walter, C. F. Ware, and L. R. Gooding. 1997. The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J. Virol. 71:8299-8306.
50. Shtrichman, R., and T. Kleinberger. 1998. Adenovirus type 5 E4 open reading frame 4 protein induces apoptosis in transformed cells. J. Virol. 72:2975-2983.
51. Sonenshein, G. E. 1997. Rel/NF-κB transcription factors and the control of apoptosis. Cancer Biol. 8:113-119.
52. Stancovski, I., and D. Baltimore. 1997. NF-κB activation: the IκB kinase revealed. Cell 91:299-302.
53. Strasser, A., and L. O'Connor. 1998. Fas-ligand - caught between Scylla and Charybdis. Nat. Med. 4:21-22.
54. Sueoka, E., N. Soeoka, S. Okabe, T. Kozu, A. Komori, T. Ohta, M. Suganuma, S. J. Kim, I. K. Lim, and H. Fujiki. 1997. Expression of the tumor necrosis factor alpha gene and early response genes by nodularin, a liver tumor promoter, in primary cultured rat hepatocytes. J. Cancer Res. Clin. Oncol. 123:413-419.
55. Teodoro, J. G., and P. E. Branton. 1997. Regulation of apoptosis by viral gene products. J. Virol. 71:1739-1746.
56. Tollefson, A. E., A. Scaria, T. W. Hermiston, J. S. Ryerse, L. J. Wold, and W. S. M. 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.
57. Tripathy, S., H. Black, E. Goldwasser, and O. Leiden. 1996. Immune responses to transgene-encoded proteins limit the stability of gene expression after injection of replication-defective adenovirus vectors. Nat. Med. 2:545-550.
58. Tsui, L. V., L. G. Guidotti, T. Ishikawa, and F. V. Chrisari. 1995. Post-transcriptional clearance of hepatitis B virus RNA by cytotoxic T lymphocyte-activated hepatocytes. Proc. Natl. Acad. Sci. USA 92:12398-12402.
59. Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-induced apoptosis by NF-κB. Science 274:787-789.
60. Vrancken Peeters, M.-J., A. Lieber, J. Perkins, and M. A. Kay. 1996. Method for multiple portal vein infusions in mice: quantification of adenovirus-mediated hepatic gene transfer. BioTechniques 20:278-285.
61. Vrancken Peeters, M.-J., G. A. Patjin, A. Lieber, L. Meuse, and M.-A. Kay. 1996. Adenovirus-mediated hepatic gene transfer in mice: comparison of intravascular and biliary administration. Hum. Gene Ther. 7:1693-1699.
62. Wang, C.-Y., M. W. Mayo, and A. S. Baldwin. 1996. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science 274:784-787.
63. Yang, Y., Q. Su, I. S. Grewal, R. Schilz, R. A. Flavell, and J. M. Wilson. 1996. Transient subversion of CD40 ugand function diminishes immune responses to adenovirus vectors in mouse liver and lung tissues. J. Virol. 70:6370-6377.
64. Yang, Y., and J. M. Wilson. 1996. CD40 ligand-dependent T cell activation: requirement of B7-CD28 signaling through CD40. Science 273:1862-1864.
65. Yang, X.-Z., H. C. Ertl, and J. M. Wilson. 1995. Upregulation of class I MHC 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.