Overexpression of the ADP (E3-11.6K) protein increases cell lysis and spread of Adenovirus

Virology

Volumn 305, Issue 2, 2003, Pages 378-387

  Doronin, Konstantin ^a   Toth, Karoly ^a   Kuppuswamy, Mohan ^a   Krajcsi, Peter ^a   Tollefson, Ann E ^a   Wold, William S M ^a,b  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VirRx Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS DEATH PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENOVIRUS; ADENOVIRUS 5; ARTICLE; CELL CULTURE; CYTOLYSIS; CYTOPATHOGENIC EFFECT; GENE FUNCTION; GENE OVEREXPRESSION; GENE STRUCTURE; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PLAQUE FORMING CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIROGENESIS; VIRUS GENE; VIRUS INFECTION; VIRUS MUTANT; VIRUS PATHOGENESIS;

ADENOVIRIDAE; HUMAN ADENOVIRUS TYPE 5;

EID: 0037455562     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.2002.1772     Document Type: Article

References (55)

1. Andersson M., Pääbo S., Nilsson T., Peterson P. A. Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell. 43:1985;215-222.
2. Benedict C., Norris P., Prigozy T., Bodmer J. L., Mahr J. A., Garnett C., Martinon F., Tschopp J., Gooding L. R., Ware C. F. Three adenovirus E3 proteins cooperate to evade apoptosis by tumor necrosis factor-related apoptosis-inducing ligand receptor-1 and -2. J. Biol. Chem. 276:2001;3270-3278.
3. Boulakia C. A., Chen G., Ng F. W., Teodoro J. G., Branton P. E., Nicholson D. W., Poirier G. G., Shore G. C. Bcl-2 and adenovirus E1B 19 kDA protein prevent E1A-induced processing of CPP32 and cleavage of poly (ADP-ribose) polymerase. Oncogene. 12:1996;529-535.
4. Branton P., Roopchand D. E. The role of adenovirus E4orf4 protein in viral replication and cell killing. Oncogene. 20:2001;7855-7865.
5. Burgert H. G., Kvist S. An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell. 41:1985;987-997.
6. Chiou S. K., White E. Inhibition of ICE-like proteases inhibits apoptosis and increases virus production during adenovirus infection. Virology. 244:1998;108-118.
7. Debbas M., White E. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:1993;546-554.
8. Devireddy L. R., Jones C. J. Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J. Virol. 73:1999;3778-3788.
9. Doronin K., Kuppuswamy M., Toth K., Tollefson A. E., Krajcsi P., Krougliak V., Wold W. S. M. Tissue-specific, tumor-selective, replication-competent adenovirus vector for cancer gene therapy. J. Virol. 75:2001;3314-3324.
10. Doronin K., Toth K., Kuppuswamy M., Ward P., Tollefson A. E., Krajcsi P., Krougliak V., Wold W. S. M. Tumor-specific, replication-competent adenovirus vectors overexpressing the Adenovirus Death Protein. J. Virol. 74:2000;6147-6155.
11. Elsing A., Burgert H.-G. The adenovirus E3/10.4K-14.5K proteins down-modulate the apoptosis receptor Fas/Apo-1 by inducing its internalization. Proc. Natl. Acad. Sci. USA. 95:1998;10072-10077.
12. Ginsberg H. S., Lundholm-Beauchamp U., Horswood R. L., Pernis B., Wold W. S. M., Chanock R. M., Prince G. A. Role of early region 3 (E3) in pathogenesis of adenovirus disease. Proc. Natl. Acad. Sci. USA. 86:1989;3823-3827.
13. Gooding L. R., Aquino L., Duerksen-Hughes P. J., Day D., Horton T. M., Yei S. P., Wold W. S. M. The E1B 19,000-molecular-weight protein of group C adenoviruses prevents tumor necrosis factor cytolysis of human cells but not of mouse cells. J. Virol. 65:1991a;3083-3094.
14. Gooding L. R., Elmore L. W., Tollefson A. E., Brady H. A., Wold W. S. M. A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor. Cell. 53:1988;341-346.
15. Gooding L. R., Ranheim T. S., Tollefson A. E., Aquino L., Duerksen-Hughes P., Horton T. M., Wold W. S. M. The 10,400- and 14,500-dalton proteins encoded by region E3 of adenovirus function together to protect many but not all mouse cell lines against lysis by tumor necrosis factor. J. Virol. 65:1991b;4114-4123.
16. Harrington E. A., Bennett M. R., Fanidi A., Evan G. I. c-MYC-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13:1994;3286-3295.
17. Hausmann J., Ortmann D., Witt M., Veit E., Seidel W. Adenovirus death protein, a transmembrane protein encoded in the E3 region, is palmitoylated at the cytoplasmic tail. Virology. 244:1998;343-351.
18. Horwitz M. Adenovirus immunoregulatory genes and their cellular targets. Virology. 279:2001;1-8.
19. Krajcsi P., Dimitrov T., Hermiston T. W., Tollefson A. E., Ranheim T. S., Vande Pol S. B., Stephenson A. H., Wold W. S. M. The adenovirus E3-14.7K protein and the E3-10.4K/14.5K complex of proteins, which independently inhibit tumor necrosis factor (TNF)-induced apoptosis, also independently inhibit TNF-induced release of arachidonic acid. J. Virol. 70:1996;4904-4913.
20. Lavoie J. N., Nguyen M., Marcellus R. C., Branton P. E., Shore G. C. E4orf4, a novel adenovirus death factor that induces p53-independent apoptosis by a pathway that is not inhibited by zVAD-fmk. J. Cell Biol. 140:1998;637-645.
21. Liljestrom P., Lusa S., Huylebroeck D., Garoff H. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest Virus: The small 6,000-molecular-weight membrane protein modulates virus release. J. Virol. 65:1991;4107-4113.
22. Loewy A., Smyth J., vonBonsdorff C.-H., Liljestrom P., Schlesinger M. J. The 6-kilodalton membrane protein of Semliki Forest Virus is involved in the budding process. J. Virol. 69:1995;469-475.
23. Lowe S. W., Ruley H. E., Housman D. E. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 74:1993;957-967.
24. Mahr J. A., Gooding L. R. Immune evasion by adenoviruses. Immunol. Rev. 168:1999;121-130.
25. Marcellus R. C., Lavoie J. N., Boivin D., Shore G. C., Ketner G., Branton P. E. The early region 4 orf4 protein of human adenovirus type 5 induces p53-independent cell death by apoptosis. J. Virol. 72:1998;7144-7153.
26. Marcellus R. C., Teodoro J. G., Wu T., Brough D. E., Ketner G., Shore G. C., Branton P. E. Adenovirus type 5 early region 4 is responsible for E1A-induced p53-independent apoptosis. J. Virol. 70:1996;6207-6215.
27. O'Brien V. Viruses and apoptosis. J. Gen. Virol. 79:1998;1833-1845.
28. Pääbo S., Bhat B. M., Wold W. S. M., Peterson P. A. A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum. Cell. 50:1987;311-317.
29. Pinto L. H., Holsinger L. J., Lamb R. A. Influenza virus M2 protein has ion channel activity. Cell. 69:1992;517-528.
30. Ramachandra M., Rahman A., Zou A., Vaillancourt M., Howe J. A., Antelman D., Sugarman B., Demers G. W., Engler H., Johnson D., Shabram P. Re-engineering adenovirus regulatory pathways to enhance oncolytic specificity and efficacy. Nature Biotech. 19:2001;1035-1041.
31. Roper R. L., Wolffe E. J., Weisberg A., Moss B. The envelope protein encoded by the A33R gene is required for formation of actin-containing microvilli and efficient cell-to-cell spread of vaccinia virus. J. Virol. 72:1998;4192-4202.
32. Ruigrok R. W. H., Hirst E. M. A., Hay A. J. The inhibition of influenza A virus maturation by amantadine: an electron microscopic examination. J. Gen. Virol. 72:1991;191-194.
33. Scaria A., Tollefson A. E., Saha S. K., Wold W. S. M. The E3-11.6K protein of adenovirus is an Asn-glycosylated integral membrane protein that localizes to the nuclear membrane. Virology. 191:1992;743-753.
34. Scaria A., Wold W. S. M. Fine-mapping of sequences that suppress splicing in the E3 complex transcription unit of adenovirus. Virology. 205:1994;406-416.
35. Shisler J., Yang C., Walter B., Ware C. F., Gooding L. R. The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J. Virol. 71:1997;8299-8306.
36. Subramanian T., Kuppuswamy M., Gysbers J., Mak S., Chinnadurai G. 19-kDa tumor antigen coded by early region E1b of adenovirus 2 is required for efficient synthesis and for protection of viral DNA. J. Biol. Chem. 259:1984;11777-11783.
37. Subramanian T., Tarodi B., Chinnadurai G. p53-independent apoptotic and necrotic cell deaths induced by adenovirus infection: suppression by E1B 19K and Bcl-2 proteins. Cell Growth Differ. 6:1995;131-137.
38. Teodoro J. G., Branton P. E. Regulation of apoptosis by viral gene products. J. Virol. 71:1997;1739-1746.
39. Teodoro J. G., Shore G. C., Branton P. E. Adenovirus E1A proteins induce apoptosis by both p53-dependent and p53-independent mechanisms. Oncogene. 11:1995;467-474.
40. Tollefson A. E., Hermiston T. W., Lichtenstein D. L., Colle C. F., Tripp R. A., Dimitrov T., Toth K., Wells C. E., Doherty P. C., Wold W. S. M. Forced degradation of Fas inhibits apoptosis in adenovirus-infected cells. Nature. 392:1998a;726-730.
41. Tollefson A. E., Hermiston T. W., Wold W. S. M. Preparation and titration of CsCl-banded adenovirus stocks. Wold W. S. M. Adenovirus Methods and Protocols. 1998b;1-9 Humana Press, Totowa.
42. Tollefson A. E., Ryerse J. S., Scaria A., Hermiston T. W., Wold W. S. M. The E3-11.6kDa Adenovirus Death Protein (ADP) is required for efficient cell death: Characterization of cells infected with adp mutants. Virology. 220:1996a;152-162.
43. Tollefson A. E., Scaria A., Hermiston T. W., Ryerse J. S., Wold L. J., Wold W. S. M. 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. 70:1996b;2296-2306.
44. Tollefson A. E., Scaria A., Saha S. K., Wold W. S. M. The 11,600-MW protein encoded by region E3 of adenovirus is expressed early but is greatly amplified at late stages of infection. J. Virol. 66:1992;3633-3642.
45. Tollefson A. E., Toth K., Doronin K., Kuppuswamy M., Doronina O. A., Lichtenstein D. L., Hermiston T. W., Smith C. A., Wold W. S. M. Inhibition of TRAIL-induced apoptosis and forced internalization of TRAIL receptor 1 by adenovirus proteins. J. Virol. 75:2001;8875-8887.
46. van den Heuvel S. J., van Laar T., The I., Van der Eb A. J. Large E1B proteins of adenovirus types 5 and 12 have different effects on p53 and distinct roles in cell transformation. J. Virol. 67:1993;5226-5234.
47. van Kuppeveld F. J. M., Hoenderop J. G. J., Smeets R. L. L., Willems P. H., Dijkman H. B., Galama J. M., Melchers W. J. Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. EMBO J. 16:1997;3519-3532.
48. Vazquez M.-I., Esteban M. Identification of functional domains in the 14-kilodalton envelope protein (A27L) of vaccinia virus. J. Virol. 73:1999;9098-9109.
49. White E. Regulation of the cell cycle and apoptosis by the oncogenes of adenovirus. Oncogene. 20:2001;7836-7846.
50. Wold W. S. M., Chinnadurai G. Adenovirus proteins that regulate apoptosis. Cann A. J. DNA Virus Replication: Frontiers in Molecular Biology. 2000;200-232 Oxford Univ. Press, Oxford.
51. Wold W. S. M., Cladaras C., Magie S. C., Yacoub N. Mapping a new gene that encodes an 11,600-molecular-weight protein in the E3 transcription unit of adenovirus 2. J. Virol. 52:1984;307-313.
52. Wold W. S. M., Doronin K., Toth K., Kuppuswamy M., Lichtenstein D. L., Tollefson A. E. Immune responses to adenoviruses: Viral evasion mechanisms and their implications for the clinic. Curr. Opin. Immunol. 11:1999;380-386.
53. Wolffe E. J., Isaacs S. N., Moss B. Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. J. Virol. 67:1993;4732-4147.
54. Yamada T., Yamaoka S., Goto T., Nakai M., Tsujimoto Y., Hatanaka M. The human T-cell leukemia virus Type 1 tax protein induces apoptosis which is blocked by the Bcl-2 protein. J. Virol. 68:1994;3374-3379.
55. Yew P. R., Liu X., Berk A. J. Adenovirus E1B oncoprotein tethers a transcriptional repression domain to p53. Genes Dev. 8:1994;190-202.