Functions and mechanisms of action of the adenovirus E3 proteins

International Reviews of Immunology

Volumn 23, Issue 1-2, 2004, Pages 75-111

  Lichtenstein, Drew L ^a   Toth, Karoly ^a   Doronin, Konstantin ^a   Tollefson, Ann E ^a   Wold, William S M ^a  

^a S LOUIS UNIV HLTH SCIENCES CENTER   (United States)

Author keywords

Adenovirus; Apoptosis; Fas; Immune system regulation; TRAIL; Tumor necrosis factor

Indexed keywords

ARACHIDONIC ACID; CALCIUM ION; CALNEXIN; CASPASE; CHAPERONE; CYSTEINE; CYTOCHROME C; DEATH RECEPTOR 5; EPIDERMAL GROWTH FACTOR; FAS LIGAND; IMMUNOSUPPRESSIVE AGENT; ISOPROTEIN; LYSINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; MESSENGER RNA; MONOCLONAL ANTIBODY; MUTANT PROTEIN; OLIGOSACCHARIDE; PERFORIN; RECEPTOR PROTEIN; SERINE; SOMATOMEDIN; TAPASIN; THAPSIGARGIN; THREONINE; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VIRUS PROTEIN; VIRUS VECTOR;

ADENOVIRUS; ANTIGEN PRESENTATION; APOPTOSIS; CELL KILLING; CELL LINE; CELL VIABILITY; COMPLEX FORMATION; CYTOKINE PRODUCTION; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; DISULFIDE BOND; DNA REPLICATION; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENETIC ANALYSIS; HUMAN; IMMUNE SYSTEM; INFLAMMATION; LYSOSOME; NONHUMAN; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSGENIC MOUSE; VIRUS INFECTION; VIRUS MUTANT;

EID: 1642430625     PISSN: 08830185     EISSN: None     Source Type: Journal    
DOI: 10.1080/08830180490265556     Document Type: Review

References (180)

1. M. Andersson, A. McMichael, and P.A. Peterson, Reduced allorecognition of adenovirus-2 infected cells, J. Immunol., 138: 3960-3966, 1987.
2. M. Andersson, S. Pääbo, T. Nilsson, and P.A. Peterson, Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance, Cell, 43: 215-222, 1985.
3. W.A. Andiman and G. Miller, Persistent infection with adenovirus types 5 and 6 in lymphoid cells from humans and woolly monkeys, J Infect. Dis., 145: 83-88, 1982.
4. A. Ashkenazi, Targeting death and decoy receptors of the tumour-necrosis factor superfamily, Nat. Rev. Cancer, 2: 420-430, 2002.
5. D.C. Beier, J.H. Cox, D.R. Vining, P. Cresswell, and V.H. Engelhard, Association of human class I MHC alleles with the adenovirus E3/19K protein, J. Immunol., 152: 3862-3872, 1994.
6. C. Benedict, P. Norris, T. Prigozy, J.L. Bodmer, J.A. Mahr, C. Garnett, F. Martinon, J. Tschopp, L.R. Gooding, and C.F. Ware, Three adenovirus E3 proteins cooperate to evade apoptosis by tumor necrosis factor-related apoptosis-inducing ligand receptor-1 and-2, J. Biol. Chem., 276: 3270-3278, 2001.
7. E.M. Bennett, J.R. Bennink, J.W. Yewdell, and F.M. Brodsky, Cutting edge: Adenovirus E19 has two mechanisms for affecting class I MHC expression, J. Immunol., 162: 5049-5052, 1999.
8. A.J. Bett, V. Krougliak, and F.L. Graham, DNA sequence of the deletion/insertion in early region 3 of Ad5 dl309, Virus Res., 39: 75-82, 1995.
9. B.M. Bhat, H.A. Brady, and W.S.M. Wold, Virus deletion mutants that affect a 3′ splice site in the E3 transcription unit of adenovirus 2, Mol. Cell. Biol., 5: 2405-2413, 1985.
10. M. Bouvier, Accessory proteins and the assembly of human class I MHC molecules: A molecular and structural perspective, Mol. Immunol., 39: 697-706, 2003.
11. J.T. Bruder, T. Jie, D.L. McVey, and I. Kovesdi, Expression of gp19K increases the persistence of transgene expression from an adenovirus vector in the mouse lung and liver, J. Virol., 71: 7623-7628, 1997.
12. H.-G. Burgert, Z. Ruzsics, S. Obermeier, A. Hilgendorf, M. Windheim, and A. Elsing, Subversion of host defense mechanisms by adenoviruses, Curr. Top. Microbiol. Immunol., 269: 273-318, 2002.
13. H.-G. Burgert and S. Kvist, An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens, Cell, 41: 987-997, 1985.
14. H.-G. Burgert and S. Kvist, The E3/19K protein of adenovirus type 2 binds to the domains of histocompatibility antigens required for CTL recognition, EMBO J., 6: 2019-2026, 1987.
15. H.-G. Burgert, J.L. Maryanski, and S. Kvist, "E3/19K" protein of adenovirus type 2 inhibits lysis of cytolytic T lymphocytes by blocking cell-surface expression of histocompatibility class I antigens, Proc. Natl. Acad. Sci. USA, 84: 1356-1360, 1987.
16. D.P. Cahill, L.T. da Costa, E.B. Carson-Walter, K.W. Kinzler, B. Vogelstein, and C. Lengauer, Characterization of MAD2B and other mitotic spindle checkpoint genes, Genomics, 58: 181-187, 1999.
17. C.R. Carlin, A.E. Tollefson, H.A. Brady, B.L. Hoffman, and W.S.M. Wold, Epidermal growth factor receptor is down-regulated by a 10,400 MW protein encoded by the E3 region of adenovirus, Cell, 57: 135-144, 1989.
18. S.R. Carlsson, J. Roth, F. Piller, and M. Fukuda, Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Major sialoglycoproteins carrying polylactosaminoglycan, J. Biol. Chem., 15: 18911-18919, 1988.
19. G. Chen and D.V. Goeddel, TNF-R1 signaling: A beautiful pathway, Science, 296: 1634-1635, 2002.
20. J. Chen and G. Fang, MAD2B is an inhibitor of the anaphase-promoting complex, Genes Dev., 15: 1765-1770, 2001.
21. P. Chen, J. Tian, I. Kovesdi, and J.B. Bruder, Interaction of the adenovirus 14.7K protein with FLICE inhibits Fas ligand-induced apoptosis, J. Biol. Chem., 273: 5815-5820, 1998.
22. L.T. Chow, T.R. Broker, and J.B. Lewis, Complex splicing patterns of RNAs from the early regions of adenovirus-2, J. Mol. Biol., 134: 265-303, 1979.
23. Y. Chu, K. Sperber, L. Mayer, and M.T. Hsu, Persistent infection of human adenovirus type 5 in human monocyte cell lines, Virology, 188: 793-800, 1992.
24. C. Cladaras, B. Bhat, and W.S. Wold, Mapping the 5′ ends, 3′ ends, and splice sites of mRNAs from the early E3 transcription unit of adenovirus 5, Virology, 140: 44-54, 1985.
25. C. Cladaras and W.S. Wold, DNA sequence of the early E3 transcription unit of adenovirus 5, Virology, 140: 28-43, 1985.
26. J.H. Cox, J.R. Bennink, and J.W. Yewdell, Retention of adenovirus E19 glycoprotein in the endoplasmic reticulum is essential to its ability to block antigen presentation, J. Exp. Med., 174: 1629-1637, 1991.
27. J.H. Cox, J.W. Yewdell, L.C. Eisenlohr, P.R. Johnson, and J.R. Bennink, Antigen presentation requires transport of MHC class I molecules from the endoplasmic reticulum, Science, 247: 715-718, 1990.
28. T. Derfuss and E. Meinl, Herpesviral proteins regulating apoptosis, Curr. Top. Microbiol. Immunol., 269: 257-272, 2002.
29. F. Deryckere and H.-G. Burgert, Tumor necrosis factor α induces the adenovirus early 3 promoter by activation of NF-κB, J. Biol. Chem., 271: 30249-30255, 1996.
30. F. Deryckere, C. Ebenau-Jehle, W.S. Wold, and H.-G. Burgert, Tumor necrosis factor alpha increases expression of adenovirus E3 proteins, Immunobiology, 193: 186-192, 1995.
31. A. Devin, A. Cook, Y. Lin, Y. Rodriguez, M. Kelliher, and Z. Liu, The distinct roles of TRAF2 and RIP in IKK activation by TNF-R1: TRAF2 recruits IKK to TNF-R1 while RIP mediates IKK activation, Immunity, 12: 419-429, 2000.
32. 2 to membranes, J. Virol., 71: 2830-2837, 1997.
33. K. Doronin, M. Kuppuswamy, K. Toth, A.E. Tollefson, P. Krajcsi, V. Krougliak, and W.S.M. Wold, Tissue-specific, tumor-selective, replication-competent adenovirus vector for cancer gene therapy, J. Virol., 75: 3314-3324, 2001.
34. K. Doronin, K. Toth, M. Kuppuswamy, P. Krajcsi, A.E. Tollefson, and W.S.M. Wold, Overexpression of the ADP (E3-11.6K) protein increases cell lysis and spread of adenovirus, Virology, 305: 378-387, 2003.
35. K. Doronin, K. Toth, M. Kuppuswamy, P. Ward, A.E. Tollefson, and W.S.M. Wold, Tumor-specific, replication-competent adenovirus vectors overexpressing the Adenovirus Death Protein, J. Virol., 74: 6147-6155, 2000.
36. N. Durepaire, J.P. Rogez, M. Verdier, S. Rogez, P. Weinbreck, and F. Denis, Detection of adenovirus DNA by polymerase chain reaction in peripheral blood lymphocytes from HIV-infected patients and a control group: Preliminary results, J. Acquir. Immune. Defic. Syndr. Hum. Retrovirol., 14: 189-190, 1997.
37. S. Efrat, G. Fejer, M. Brownlee, and M.S. Horwitz, Prolonged survival of pancreatic islet allografts mediated by adenovirus immunoregulatory transgenes, Proc. Natl. Acad. Sci. USA, 92: 6947-6951, 1995.
38. S. Efrat, D. Serreze, A. Svetlanov, C.M. Post, E.A. Johnson, K. Herold, and M. Horwitz, Adenovirus early region 3 (E3) immunomodulatory genes decrease the incidence of autoimmune diabetes in NOD mice, Diabetes, 50: 980-984, 2001.
39. B. Elangovan, D.L. Lichtenstein, A.E. Tollefson, and W.S.M. Wold, The YxxΦ motif present in the cytoplasmic tail of RID β interacts with the μ2 subunit of the AP2 complex. Manuscript in preparation, 2003.
40. A. Elsing and H.-G. Burgert, 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: 10072-10077, 1998.
41. H. Everett and G. McFadden, Poxviruses and apoptosis: A time to die, Curr. Opin. Microbiol., 5: 395-402, 2002.
42. D. Feuerbach, S. Etteldorf, C. Ebenau-Jehle, J. Abastado, D. Madden, and H.-G. Burgert, Identification of amino acids within the MHC molecule important for the interaction with the adenovirus protein E3-19K, J. Immunol., 153: 1626-1636, 1994.
43. P. Flomenberg, E. Gutierrez, and K.T. Hogan, Identification of class I MHC regions which bind to the adenovirus E3-19k protein, Mol. Immunol., 31: 1277-1284, 1994.
44. P. Flomenberg, E. Gutierrez, V. Piaskowski, and J.T. Casper, Detection of adenovirus DNA in peripheral blood mononuclear cells by polymerase chain reaction assay, J. Med. Virol., 51: 182-188, 1997.
45. P. Flomenberg, V. Piaskowski, R.L. Truitt, and J.T. Casper, Human adenovirus-specific CD8+ T-cell responses are not inhibited by E3-19K in the presence of gamma interferon, J. Virol, 70: 6314-6322, 1996.
46. J.P. Fox, C.D. Brandt, F.E. Wassermann, C.E. Hall, I. Spigland, A. Kogon, and L.R. Elveback, The virus watch program: A continuing surveillance of viral infections in metropolitan New York families. VI. Observations of adenovirus infections: virus excretion patterns, antibody response, efficiency of surveillance, patterns of infections, and relation to illness, Am. J. Epidemiol., 89: 25-50, 1969.
47. J.P. Fox, C.E. Hall, and M.K. Cooney, The Seattle Virus Watch. VII. Observations of adenovirus infections, Am. J. Epidemiol., 105: 362-386, 1977.
48. J.M. Friedman and M.S. Horwitz, Inhibition of tumor necrosis factor alpha-induced NF-κB activation by the adenovirus E3-10.4/14.5K complex, J. Virol., 76: 5515-5521, 2002.
49. R. Gabathuler and S. Kvist, The endoplasmic reticulum retention signal of the E3/19K protein of adenovirus type 2 consists of three separate amino acid segments at the carboxy terminus, J. Cell. Biol., 111: 1803-1810, 1990.
50. R. Gabathuler, F. Levy, and S. Kvist, Requirements for the association of adenovirus type 2 E3/19K wild-type and mutant proteins with HLA antigens, J. Virol., 64: 3679-3685, 1990.
51. M. Gantzer, E. Spitz, N. Accard, and R. Rooke, Constitutive expression of the adenovirus E3-14.7K protein does not prolong adenovirus vector DNA persistence but protects mice against lipopolysaccharide-induced acute hepatitis, Hum. Gene Ther., 13: 921-933, 2002.
52. J. Garcia, F. Wu, and R. Gaynor, Upstream regulatory regions required to stabilize binding to the TATA sequence in an adenovirus early promoter, Nucleic Acids Res., 15: 8367-8385, 1987.
53. C.T. Garnett, D. Erdman, W. Xu, and L.R. Gooding, Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes, J. Virol., 76: 10608-10616, 2002.
54. K. Ghosh and H.P. Ghosh, Role of the membrane anchoring and cytoplasmic domains in intracellular transport and localization of viral glycoproteins, J. Biochem. Cell Biol., 77: 165-178, 1999.
55. H.S. Ginsberg, R.L. Horswood, R.M. Chanock, and G.A. Prince, Role of early genes in pathogenesis of adenovirus pneumonia. Proc. Nat. Acad. Sci. USA, 87: 6191-6195, 1990.
56. H.S. Ginsberg, U. Lundholm-Beauchamp, R.L. Horswood, B. Pernis, W.S.M. Wold, R.M. Chanock, and G.A. Prince, Role of early region 3 (E3) in pathogenesis of adenovirus disease, Proc. Natl. Acad. Sci. USA, 86: 3823-3827, 1989.
57. H.S. Ginsberg, L.L. Moldawer, P.B. Sehgal, M. Redington, P.L. Kilian, R.M. Chanock, and G.A. Prince, A mouse model for investigating the molecular pathogenesis of adenovirus pneumonia, Proc. Natl. Acad. Sci. USA, 88: 1651-1655, 1991.
58. L.R. Gooding, L. Aquino, P.J. Duerksen-Hughes, D. Day, T.M. Horton, S.P. Yei, and W.S.M. Wold, 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: 3083-3094, 1991.
59. L.R. Gooding, L.W. Elmore, A.E. Tollefson, H.A. Brady, and W.S.M. Wold, A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor, Cell, 53: 341-346, 1988.
60. L.R. Gooding, T.S. Ranheim, A.E. Tollefson, L. Aquino, P. Duerksen-Hughes, T.M. Horton, and W.S.M. Wold, 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: 4114-4123, 1991.
61. L.R. Gooding, I.O. Sofola, A.E. Tollefson, P. Duerksen-Hughes, and W.S.M. Wold, The adenovirus E3-14.7K protein is a general inhibitor of tumor necrosis factor-mediated cytolysis, J. Immunol., 145: 3080-3086, 1990.
62. A. Grunhaus, S. Cho, and M.S. Horwitz, Association of vaccinia virus-expressed adenovirus E3-19K glycoprotein with class I MHC and its effects on virulence in a murine pneumonia model, Virology, 200: 535-546, 1994.
63. K. Hattula and J. Peränen, FIP-2, a coiled-coil protein, links Huntingtin to Rab8 and modulates cellular morphogenesis, Curr. Biol., 10: 1603-1606, 2000.
64. J. Hausmann, D. Ortmann, M. Witt, E. Veit, and W. Seidel, Adenovirus death protein, a transmembrane protein encoded in the E3 region, is palmitoylated at the cytoplasmic tail, Virology, 244: 343-351, 1998.
65. L.K. Hawkins and W.S.M. Wold, A 12,500 MW protein is coded by region E3 of adenovirus, Virology, 188: 486-494, 1992.
66. J. Herisse, G. Courtois, and F. Galibert, Nucleotide sequence of the EcoRI D fragment of adenovirus 2 genome, Nucleic Acids Res., 8: 2173-2192, 1980.
67. J. Herisse and F. Galibert, Nucleotide sequence of the EcoRI E fragment of adenovirus 2 genome, Nucleic Acids Res., 9: 1229-1240, 1981.
68. T.W. Hermiston, R.A. Tripp, T. Sparer, L.R. Gooding, and W.S.M. Wold, Deletion mutation analysis of the adenovirus type 2 E3-gp19K protein: Identification of sequences within the endoplasmic reticulum lumenal domain that are required for class I antigen binding and protection from adenovirus-specific cytotoxic T lymphocytes, J. Virol., 67: 5289-5298, 1993.
69. P. Hoffman, P. Rajakumar, B. Hoffman, R. Heuertz, W.S. Wold, and C.R. Carlin, Evidence for intracellular down-regulation of the epidermal growth factor (EGF) receptor during adenovirus infection by an EGF-independent mechanism, J. Virol., 66: 197-203, 1992.
70. P. Hoffman, M.B. Yaffe, B.L. Hoffman, S. Yei, W.S.M. Wold, and C. Carlin, Characterization of the adenovirus E3 protein that down-regulates the epidermal growth factor receptor. Evidence for intermolecular disulfide bonding and plasma membrane localization, J. Biol. Chem., 267: 13480-13487, 1992.
71. T.M. Horton, T.S. Ranheim, L. Aquino, D.I. Kusher, S.K. Saha, C.F. Ware, W.S.M. Wold, and L.R. Gooding, Adenovirus E3 14.7K protein functions in the absence of other adenovirus proteins to protect transfected cells from tumor necrosis factor cytolysis, J. Virol., 65: 2629-2639, 1991.
72. J. Horvath, L. Palkonyay, and J. Weber, Group C adenovirus DNA sequences in human lymphoid cells, J. Virol., 59: 189-192, 1986.
73. M. Horwitz, Adenovirus immunoregulatory genes and their cellular targets, Virology, 279: 1-8, 2001.
74. H.C. Hurst and N.C. Jones, Identification of factors that interact with the E1A-inducible adenovirus E3 promoter, Genes Dev., 1: 1132-1146, 1987.
75. Y. Ilan, G. Droguett, N.R. Chowdhury, Y. Li, K. Sengupta, N.R. Thummala, A. Davidson, J.R. Chowdhury, and M.S. Horwitz, 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, 1997.
76. M.R. Jackson, T. Nilsson, and P.A. Peterson, Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum, EMBO J., 9: 3153-3162, 1990.
77. W.A. Jefferies and H.-G. Burgert, E3/19K from adenovirus 2 is an immunosubversive protein that binds to a structural motif regulating the intracellular transport of major histocompatibility complex class I proteins. J. Exp. Med., 172: 1653-1664, 1990.
78. O. Kampe, D. Bellgrau, U. Hammerling, P. Lind, S. Pääbo, L. Severinsson, and P.A. Peterson, Complex formation of class I transplantation antigens and a viral glycoprotein, J. Biol. Chem., 258: 10594-10598, 1983.
79. J.M. Kaplan, D. Armentano, T.E. Sparer, S.G. Wynn, P.A. Peterson, S.C. Wadsworth, K.K. Couture, S.E. Pennington, J.A. St George, L.R. Gooding, and A.E. Smith, Characterization of factors involved in modulating persistence of transgene expression from recombinant adenovirus in the mouse lung, Hum. Gene Ther., 8: 45-56, 1997.
80. M. Karin and Y. Ben Neriah, Phosphorylation meets ubiquitination: The control of NF-[κ]B activity, Annu. Rev. Immunol., 18: 621-663, 2000.
81. M. Karin and A. Lin, NF-kappaB at the crossroads of life and death, Nat. Immunol., 3: 221-227, 2002.
82. T.J. Kelly Jr., and A.M. Lewis Jr., Use of nondefective adenovirus-simian virus 40 hybrids for mapping the simian virus 40 genome, J. Virol., 12: 643-652, 1973.
83. [82a] H.-J. Kim and M.P. Foster, Characterization of Ad5 E3-14.7K, an adenoviral inhibitor of apoptosis: Structure, oligometric state, and metal binding. Protein Science, 11: 1117-1128, 2002.
84. T. Kirchhausen, Adaptors for clathrin-mediated traffic, Annu. Rev. Cell Dev. Biol., 15: 705-732, 1999.
85. H. Korner, U. Fritzsche, and H.-G. Burgert, Tumor necrosis factor alpha stimulates expression of adenovirus early region 3 proteins: Implications for viral persistence, Proc. Natl. Acad. Sci. USA, 89: 11857-11861, 1992.
86. R. Kornfeld and W.S.M. Wold, Structures of the oligosaccharides of the glycoprotein coded by early region E3 of adenovirus 2, J. Virol., 40: 440-449, 1981.
87. M. Kornuc, S. Kliewer, J. Garcia, D. Harrich, C. Li, and R. Gaynor, Adenovirus early region 3 promoter regulation by E1A/E1B is independent of alterations in DNA binding and gene activation of CREB/ATF and AP1, J. Virol., 64: 2004-2013, 1990.
88. P. Krajcsi, T. Dimitrov, T.W. Hermiston, A.E. Tollefson, T.S. Ranheim, S.B. Vande Pol, A.H. Stephenson, and W.S.M. Wold, 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: 4904-4913, 1996.
89. cyt orientation, Virology, 187: 131-144, 1992.
90. P. Krajcsi, A.E. Tollefson, C.W. Anderson, and W.S.M. Wold, The adenovirus E3 14.5-kilodalton protein, which is required for downregulation of the epidermal growth factor receptor and prevention of tumor necrosis factor cytolysis, is an integral membrane protein oriented with its C terminus in the cytoplasm, J. Virol., 66: 1665-1673, 1992.
91. P. Krajcsi, A.E. Tollefson, and W.S.M. Wold, The E3-14.5K integral membrane protein of adenovirus that is required for downregulation of the EGF receptor and for prevention of TNF cytolysis is O-glycosylated but not N-glycosylated., Virology, 188: 570-579, 1992.
92. P. Krajcsi and W.S.M. Wold, The adenovirus E3-14.5K protein which is required for prevention of TNF cytolysis and for downregulation of the EGF receptor contains phosphoserine, Virology, 187: 492-498, 1992.
93. E. Kuivinen, B.L. Hoffman, P.A. Hoffman, and C.R. Carlin, Structurally related class I and class II receptor protein tyrosine kinases are down-regulated by the same E3 protein coded for by human group C adenoviruses, J. Cell. Biol., 120: 1271-1279, 1993.
94. S. Kvist, L. Ostberg, H. Persson, L. Philipson, and P.A. Peterson, Molecular association between transplantation antigens and cell surface antigen in adenovirus-transformed cell line, Proc. Natl. Acad. Sci. USA, 75: 5674-5678, 1978.
95. - adenoviral vectors strongly reduces the host cytotoxic T cell response against the vector, Gene Therapy, 2: 256-262, 1995.
96. R. Li and A.W. Murray, Feedback control of mitosis in budding yeast, Cell, 66: 519-531, 1991.
97. Y. Li, J. Kang, J. Friedman, L. Tarassishin, J. Ye, A. Kovalenko, D. Wallach, and M.S. Horwitz, Identification of a cell protein (FIP-3) as a modulator of NF-κB activity and as a target of an adenovirus inhibitor of tumor necrosis factor α-induced apoptosis, Proc. Natl. Acad. Sci. USA, 96: 1042-1047, 1999.
98. Y. Li, J. Kang, and M.S. Horwitz, 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, 1997.
99. Y. Li, J. Kang, and M.S. Horwitz, Interaction of an adenovirus E3 14.7-kilodalton protein with a novel tumor necrosis factor alpha-inducible cellular protein containing leucine zipper domains, Mol. Cell. Biol., 18: 1601-1610, 1998.
100. Y. Li and W.S. Wold, Identification and characterization of a 30K protein (Ad4E3-30K) encoded by the E3 region of human adenovirus type 4, Virology, 273: 127-138, 2000.
101. D.L. Lichtenstein, P. Krajcsi, D.J. Esteban, A.E. Tollefson, and W.S.M. Wold, The adenovirus RIDβ subunit contains a tyrosine residue that is critical for RID-mediated receptor internalization and inhibition of Fas- and TRAIL-induced apoptosis, J. Virol., 76: 11329-11342, 2002.
102. S. Lukashok, L. Tarassishin, Y. Li, and M. Horwitz, An adenovirus inhibitor of tumor necrosis factor alpha-induced apoptosis complexes with dynein and a small GTPase, J. Virol., 74: 4705-4709, 2000.
103. M. MacFarlane, TRAIL-induced signalling and apoptosis, Toxicol. Lett., 139: 89-97, 2003.
104. J. A. Mahr, J.M. Boss, and L.R. Gooding, The adenovirus E3 promoter is sensitive to activation signals in human T cells, J. Virol., 77: 1112-1119, 2003.
105. J.A. Mahr and L.R. Gooding, Immune evasion by adenoviruses, Immunol. Rev., 168: 121-130, 1999.
106. A.L. McNees, C.T. Garnett, and L.R. Gooding, The adenovirus E3 RID complex protects some cultured human T and B lymphocytes from Fas-induced apoptosis, J. Virol., 76: 9716-9723, 2002.
107. F. Mercurio, B.W. Murray, A. Shevchenko, B.L. Bennett, D.B. Young, J.W. Li, G. Pascual, A. Motiwala, H. Zhu, M. Mann, and A.M. Manning, IkappaB kinase (IKK)-associated protein 1, a common component of the heterogeneous IKK complex, Mol. Cell Biol., 19: 1526-1538, 1999.
108. A.R. Moise, J.R. Grant, T.Z. Vitalis, and W.A. Jefferies, Adenovirus E3-6.7K maintains calcium homeostasis and prevents apoptosis and arachidonic acid release, J. Virol., 76: 1578-1587, 2002.
109. J.E. Morin, M.D. Lubeck, J.E. Barton, A.J. Conley, A.R. Davis, and P.P. Hung, Recombinant adenovirus induces antibody response to hepatitis B virus surface antigen in hamsters, Proc. Natl. Acad. Sci. USA, 84: 4626-4630, 1987.
110. Y. Murakumo, T. Roth, H. Ishii, D. Rasio, S. Numata, C.M. Croce, and R. Fishel, A human REV7 homolog that interacts with the polymerase zeta catalytic subunit hREV3 and the spindle assembly checkpoint protein hMAD2, J. Biol. Chem., 275: 4391-4397, 2000.
111. K.K. Nelson, J. Schlondorff, and C.P. Blobel, Evidence for an interaction of the metalloprotease-disintegrin tumour necrosis factor alpha convertase (TACE) with mitotic arrest deficient 2 (MAD2), and of the metalloprotease-disintegrin MDC9 with a novel MAD2-related protein, MAD2beta, Biochem. J., 343: 673-680, 1999.
112. T. Nilsson, M. Jackson, and P.A. Peterson, Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum, Cell, 58: 707-718, 1989.
113. S. Pääbo, B.M. Bhat, W.S.M. Wold, and P.A. Peterson, A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum, Cell, 50: 311-317, 1987.
114. S. Pääbo, F. Weber, O. Kampe, W. Schaffner, and P.A. Peterson, Association between transplantation antigens and a viral membrane protein synthesized from a mammalian expression vector, Cell, 33: 445-453, 1983.
115. S. Pääbo, F. Weber, T. Nilsson, W. Schaffner, and P.A. Peterson, Structural and functional dissection of an MHC class I antigen-binding adenovirus glycoprotein, EMBO J., 5: 1921-1927, 1986.
116. D.L. Pacini, E.J. Dubovi, and W.A. Clyde, Jr., A new animal model for human respiratory tract disease due to adenovirus, J. Infect. Dis., 150: 92-97, 1984.
117. H. Persson, M. Jansson, and L. Philipson, Synthesis and genomic site for an adenovirus type 2 early glycoprotein, J. Mol. Biol., 136: 375-394, 1980.
118. H. Persson, H. Jornvall, and J. Zabielski, Multiple mRNA species for the precursor to an adenovirus-encoded glycoprotein: identification and structure of the signal sequence, Proc. Natl. Acad. Sci. USA, 77: 6349-6353, 1980.
119. H. Persson, B. Oberg, and L. Philipson, Purification and characterization of an early protein (E14K) from adenovirus type 2-infected cells, J. Virol., 28: 119-139, 1978.
120. C.M. Pfleger, A. Salic, E. Lee, and M.W. Kirschner, Inhibition of Cdh1-APC by the MAD2-related protein MAD2L2: A novel mechanism for regulating Cdh1, Genes Dev., 15: 1759-1764, 2001.
121. W. Poller, S. Schneider-Rasp, U. Liebert, F. Merklein, P. Thalheimer, A. Haack, R. Schwaab, C. Schmitt, and H.H. Brackmann, Stabilization of transgene expression by incorporation of E3 region genes into an adenoviral factor IX vector and by transient anti-CD4 treatment of the host, Gene Ther., 3: 521-530, 1996.
122. M. Ramachandra, A. Rahman, A. Zou, M. Vaillancourt, J. A. Howe, D. Antelman, B. Sugarman, G.W. Demers, H. Engler, D. Johnson, and P. Shabram, Re-engineering adenovirus regulatory pathways to enhance oncolytic specificity and efficacy, Nature Biotech., 19: 1035-1041, 2001.
123. T.S. Ranheim, J. Shisler, T.M. Horton, L.J. Wold, L.R. Gooding, and W.S.M. Wold, Characterization of mutants within the gene for the adenovirus E3 14.7-kilodalton protein which prevents cytolysis by tumor necrosis factor, J. Virol., 67:2159-2167, 1993.
124. k mice, J. Immunol., 146: 3977-3984, 1991.
125. F.C. Rawle, A.E. Tollefson, W.S.M. Wold, and L.R. Gooding, Mouse anti-adenovirus cytotoxic T lymphocytes. Inhibition of lysis by E3 gp19K but not E3 14.7K, J. Immunol., 143: 2031-2037, 1989.
126. D.M. Rothwarf, E. Zandi, G. Natoli, and M. Karin, IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex, Nature, 395: 297-300, 1998.
127. U. Sartorius, I. Schmitz, and P.H. Krammer, Molecular mechanisms of death-receptor-mediated apoptosis, Chembiochem., 2: 20-29, 2001.
128. A. Scaria, A.E. Tollefson, S.K Saha, and W.S.M. Wold, The E3-11.6K protein of adenovirus is an Asn-glycosylated integral membrane protein that localizes to the nuclear membrane, Virology, 191: 743-753, 1992.
129. D.B. Schowalter, J.C. Tubb, M. Liu, C.B. Wilson, and M.A. Kay, Heterologous expression of adenovirus E3-gp19K in an E1a-deleted adenovirus vector inhibits MHC I expression in vitro, but does not prolong transgene expression in vivo, Gene Ther., 4: 351-360, 1997.
130. A. Schurmann, A. Brauers, S. Massmann, W. Becker, and H.G. Joost, Cloning of a novel family of mammalian GTP-binding proteins (RagA, RagBs, RagB1) with remote similarity to the Ras-related GTPases, J. Biol. Chem., 270: 28982-28988, 1995.
131. K. Schwamborn, R. Weil, G. Courtois, S.T. Whiteside, and A. Israël, Phorbol esters and cytokines regulate the expression of the NEMO-related protein, a molecule involved in a NF-kappa B-independent pathway, J. Biol. Chem., 275: 22780-22789, 2000.
132. M. Sester, and H.-G. Burgert, Conserved cysteine residues within the E3/19K protein of adenovirus type 2 are essential for binding to major histocompatibility complex antigens, J. Virol., 68: 5423-5432, 1994.
133. L. Severinsson, I. Martens, and P.A. Peterson, Differential association between two human MHC class I antigens and an adenoviral glycoprotein, J. Immunol., 137: 1003-1009, 1986.
134. T. Shenk, Adenoviridae: The viruses and their replication, In D.M. Knipe and P.M. Howley, (Eds.), Fields Virology. Philadelphia: Lippincott, Williams & Wilkins, pp. 2265-2300, 2001.
135. J. Shisler, C. Yang, B. Walter, C.F. Ware, and L.R. Gooding, 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, 1997.
136. C. Signas, M.G. Katze, H. Persson, and L. Philipson, An adenovirus glycoprotein binds heavy chains of class I transplantation antigens from man and mouse, Nature, 299: 175-178, 1982.
137. L. Silver and C.W. Anderson, Interaction of human adenovirus serotype 2 with human lymphoid cells, Virology, 165: 377-387, 1988.
138. T. Sparer, R.A. Tripp, D.L. Dillehay, T.W. Hermiston, W.S.M. Wold, and L.R. Gooding, The role of adenovirus early region 3 proteins (gp19K, 10.4K, 14.5K, and 14.7K) in a murine pneumonia model, J. Virol., 70: 2431-2439, 1996.
139. T.E. Sparer and L.R. Gooding, Suppression of MHC class I antigen presentation by human adenoviruses, Curr. Top. Microbiol. Immunol., 232: 135-147, 1998.
140. T.E. Sparer, S.G. Wynn, D.J. Clark, J.M. Kaplan, L.M. Cardoza, S.C. Wadsworth, A.E. Smith, and L.R. Gooding, Generation of cytotoxic T lymphocytes against immunorecessive epitopes after multiple immunizations with adenovirus vectors is dependent on haplotype, J. Virol., 71: 2277-2284, 1997.
141. + T-cell-deficient mice survive inoculation with high doses of vaccinia virus and exhibit altered IgG responses, Proc. Natl. Acad. Sci. USA, 89: 6070-6074, 1992.
142. A.R. Stewart, A.E. Tollefson, P. Krajcsi, S.P. Yei, and W.S.M. Wold, The adenovirus E3 10.4K and 14.5K proteins, which function to prevent cytolysis by tumor necrosis factor and to down-regulate the epidermal growth factor receptor, are localized in the plasma membrane, J. Virol., 69: 172-181, 1995.
143. K. Suzuki, R. Alemany, M. Yamamoto, and D.T. Curiel, The presence of the adenovirus E3 region improves the oncolytic potency of conditionally replicative adenoviruses, Clin. Cancer Res., 8: 3348-3359, 2002.
144. K. Tada, T. Okazaki, S. Sakon, T. Kobarai, K. Kurosawa, S. Yamaoka, H. Hashimoto, T.W. Mak, H. Yagita, K. Okumura, W.C. Yeh, and H. Nakano, Critical roles of TRAF2 and TRAF5 in tumor necrosis factor-induced NF-kappa B activation and protection from cell death, J. Biol. Chem., 276: 36530-36534, 2001.
145. M.M. Taketo and M. Sonoshita, Phospolipase A2 and apoptosis, Biochim. Biophys. Acta, 1585: 72-76, 2002.
146. b-restricted SV40-specific CTL-mediated lysis, Virology, 165: 357-366, 1988.
147. 2 is required for the lysis of adenovirus-infected cells by tumor necrosis factor, J. Virol., 70: 8502-8507, 1996.
148. A.E. Tollefson, T.W. Hermiston, D.L. Lichtenstein, C.F. Colle, R.A. Tripp, T. Dimitrov, K. Toth, C.E. Wells, P.C. Doherty, and W.S.M. Wold, Forced degradation of Fas inhibits apoptosis in adenovirus-infected cells, Nature, 392: 726-730, 1998.
149. A.E. Tollefson, P. Krajcsi, M.H. Pursley, L.R. Gooding, and W.S.M. Wold, A 14,500 MW protein is coded by region E3 of group C human adenoviruses, Virology, 175: 19-29, 1990.
150. A.E. Tollefson, P. Krajcsi, S.P. Yei, C.R. Carlin, and W.S.M. Wold, A 10,400-molecular-weight membrane protein is coded by region E3 of adenovirus, J. Virol., 64: 794-801, 1990.
151. A.E. Tollefson, J.S. Ryerse, A. Scaria, T.W. Hermiston, and W.S.M. Wold, The E3-11.6 kDa Adenovirus Death Protein (ADP) is required for efficient cell death: Characterization of cells infected with adp mutants, Virology, 220: 152-162, 1996.
152. A.E. Tollefson, A. Scaria, T.W. Hermiston, J.S. Ryerse, L.J. Wold, and W.S.M. Wold, 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, 1996.
153. A.E. Tollefson, A. Scaria, S.K. Saha, and W.S.M. Wold, 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: 3633-3642, 1992.
154. A.E. Tollefson, A. Scaria, B. Ying, and W.S.M. Wold, Mutations within the adenovirus death protein (ADP) alter the Kinetics of cell death of adenovirus infected cells, J. Virol., 77: 7764-7778, 2003.
155. A.E. Tollefson, A.R. Stewart, S.P. Yei, S.K. Saha, and W.S.M. Wold, The 10,400-and 14,500-dalton proteins encoded by region E3 of adenovirus form a complex and function together to down-regulate the epidermal growth factor receptor, J. Virol., 65: 3095-3105, 1991.
156. A.E. Tollefson, K. Toth, K. Doronin, M. Kuppuswamy, O.A. Doronina, D.L. Lichtenstein, T.W. Hermiston, C.A. Smith, and W.S.M. Wold, Inhibition of TRAIL-induced apoptosis and forced internalization of TRAIL receptor 1 by adenovirus proteins, J. Virol., 75: 8875-8887, 2001.
157. A.E. Tollefson, and W.S.M. Wold, Identification and gene mapping of a 14,700-molecular-weight protein encoded by region E3 of group C adenoviruses, J. Virol., 62: 33-39, 1988.
158. K. Toth, M. Kuppuswamy, K. Doronin, O. Doronina, D.L. Lichtenstein, A.E. Tollefson, and W.S.M. Wold, Construction and characterization of E1-minus replication-defective adenovirus vectors that express E3 proteins from the E1 region, Virology, 301: 99-108, 2002.
159. J. Tufariello, S. Cho, and M.S. Horwitz, The adenovirus E3 14.7-kilodalton protein which inhibits cytolysis by tumor necrosis factor increases the virulence of vaccinia virus in a murine pneumonia model, J. Virol., 68: 453-462, 1994.
160. J.M. Tufariello, S. Cho, and M.S. Horwitz, Adenovirus E3 14.7-kilodalton protein, an antagonist of tumor necrosis factor cytolysis, increases the virulence of vaccinia virus in severe combined immunodeficient mice, Proc. Natl. Acad. Sci. USA, 91: 10987-10991, 1994.
161. J. van der Veen and M. Lambriex, Relationship of adenovirus to lymphocytes in naturally infected human tonsils and adenoids, Infect. Immun., 7: 604-609, 1973.
162. M.G. von Herrath, S. Efrat, M.B.A. Oldstone, and M.S. Horwitz, Expression of adenovirus E3 transgenes in β cells prevents autoimmune diabetes, Proc. Natl. Acad. Sci. USA, 94: 9808-9813, 1997.
163. R.E. Wallace, Susceptibility of human lymphoblasts (RPMI 7466) to viral infections in vitro, Proc. Soc Exp. Biol Med., 130: 702-710, 1969.
164. E.W. Wang, M.O. Scott, and R.P. Ricciardi, An adenovirus mRNA which encodes a 14,700-Mr protein that maps to the last open reading frame of region E3 is expressed during infection, J. Virol., 62: 1456-1459, 1988.
165. S. Wen, R.M. Driscoll, D.B. Schneider, and D.A. Dichek, Inclusion of the E3 region in an adenoviral vector decreases inflammation and neointima formation after arterial gene transfer. Arterioscler. Thromb. Vasc. Biol., 21: 1777-1782, 2001.
166. J.L. Williams, J. Garcia, D. Harrich, L. Pearson, F. Wu, and R. Gaynor, Lymphoid specific gene expression of the adenovirus early region 3 promoter is mediated by NF-kappa B binding motifs, EMBO J., 9: 4435-4442, 1990.
167. J. Wilson-Rawls, S.K. Saha, P. Krajcsi, A.E. Tollefson, L.R. Gooding, and W.S.M. Wold., A 6700 MW membrane protein is encoded by region E3 of adenovirus type 2, Virology, 178: 204-212, 1990.
168. J. Wilson-Rawls and W.S.M. Wold, The E3-6.7K protein of adenovirus is an Asn-linked integral membrane glycoprotein localized in the endoplasmic reticulum, Virology, 195: 6-15, 1993.
169. W.S.M. Wold and G. Chinnadurai, Adenovirus proteins that regulate apoptosis., p. 200-232. In A.J. Cann (Ed.), DNA Virus Replication: Frontiers in Molecular Biology, Oxford, Oxford University Press, 2000.
170. W.S.M. Wold, C. Cladaras, S.L. Deutscher, and Q.S. Kapoor, The 19-kDa glycoprotein coded by region E3 of adenovirus. Purification, characterization, and structural analysis, J. Biol. Chem., 260: 2424-2431, 1985.
171. W.S.M. Wold, C. Cladaras, S.C. Magie, and N. Yacoub, Mapping a new gene that encodes an 11,600-molecular-weight protein in the E3 transcription unit of adenovirus 2, J. Virol., 52: 307-313, 1984.
172. W.S.M. Wold, K. Doronin, K. Toth, M. Kuppuswamy, D.L. Lichtenstein, and A.E. Tollefson, Immune responses to adenoviruses: Viral evasion mechanisms and their implications for the clinic, Curr. Opin. Immunol., 11: 380-386, 1999.
173. W.S.M. Wold, A.E. Tollefson, and T.W. Hermiston, E3 transcription unit of adenovirus, p. 237-274. In W. Doerfler and P. Bohm (Eds.), The Molecular Repertoire of Adenoviruses, Springer-Verlag, Heidelberg, 1995.
174. S. Yamaoka, G. Courtois, C. Bessia, S.T. Whiteside, R. Weil, F. Agou, H.E. Kirk, R.J. Kay, and A. Israël, Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation, Cell, 93: 1231-1240, 1998.
175. J. Ye, X. Xie, L. Tarassishin, and M. Horwitz, Regulation of the NF-κB activation pathway by isolated domains of FIP3/IKKγ, a component of the IκB-α kinase complex, J. Biol. Chem., 275: 9882-9889, 2000.
176. B. Ying and W.S.M. Wold, Adenovirus ADP protein (E3-11.6K), which is required for efficient cell lysis and virus release, interacts with human MAD2B, Virology, 313: 224-234, 2003.
177. D.-C. Yu, Y. Chen, M. Seng, J. Dilley, and D.R. Henderson, The addition of adenovirus type 5 region E3 enables Calydon virus 787 to eliminate distant prostate tumor xenografts, Cancer Res., 59: 4200-4203, 1999.
178. T.A. Zanardi, S. Yei, D.L. Lichtenstein, Tollefson A.E., and W.S.M. Wold, Distinct domains in the adenovirus E3 RIDα protein are required for degradation of Fas and the epidermal growth factor receptor, J. Virol., 77: 11685-11696, 2003.
179. S.Q. Zhang, A. Kovalenko, G. Cantarella, and D. Wallach, Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to NEMO (IKKgamma) upon receptor stimulation, Immunity, 12: 301-311, 2000.
180. Z.K. Zsengeller, S.E. Wert, W.M. Hull, X. Hu, S. Yei, B.C. Trapnell, and J.A. Whitsett, Persistence of replication-deficient adenovirus-mediated gene transfer in lungs of immune-deficient (nu/nu) mice, Hum. Gene Ther., 6: 457-467, 1995.