The role of chromatin in adenoviral vector function

Viruses

Volumn 5, Issue 6, 2013, Pages 1500-1515

  Wong, Carmen M ^a,b   McFall, Emily R ^a,b   Burns, Joseph K ^a,b   Parks, Robin J ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Adenovirus; Chromatin; DNA replication; Histones; Transcription

Indexed keywords

ADENOVIRUS VECTOR; CAPSID PROTEIN; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; HISTONE H3; NUCLEOPROTEIN; VIRUS DNA;

ADENOVIRUS 2; ADENOVIRUS 5; CELL NUCLEUS; CHROMATIN; CHROMATIN STRUCTURE; DNA HISTONE INTERACTION; DNA PACKAGING; DNA REPLICATION; DNA STRUCTURE; ENDOCYTOSIS; EPIGENETICS; EPISOME; EUCHROMATIN; HETEROCHROMATIN; HUMAN; INVERTED TERMINAL REPEAT; NONHUMAN; REVIEW; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRION; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ADENOVIRUSES, HUMAN; CHROMATIN; GENE EXPRESSION REGULATION, VIRAL; GENETIC THERAPY; GENETIC VECTORS; HUMANS; TRANSDUCTION, GENETIC; VIRUS REPLICATION;

ADENOVIRIDAE; PRIMATES; RODENTIA;

EID: 84879164949     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v5061500     Document Type: Review

References (103)

1. Hassell, J.A.; Lukanidin, E.; Fey, G.; Sambrook, J. The structure and expression of two defective adenovirus 2/simian virus 40 hybrids. J. Mol. Biol. 1978, 120, 209-247.
2. Tjian, R. The binding site on SV40 DNA for a T antigen-related protein. Cell 1978, 13, 165-179.
3. Graham, F.L.; Smiley, J.; Russell, W.C.; Nairn, R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 1977, 36, 59-74.
4. Giberson, A.N.; Davidson, A.R.; Parks, R.J. Chromatin structure of adenovirus DNA throughout infection. Nucleic Acids Res. 2012, 40, 2369-2376.
5. Amalfitano, A.; Parks, R.J. Separating fact from fiction: Assessing the potential of modified adenovirus vectors for use in human gene therapy. Curr. Gene Ther. 2002, 2, 111-133.
6. Bett, A.J.; Prevec, L.; Graham, F.L. Packaging capacity and stability of human adenovirus type 5 vectors. J. Virol. 1993, 67, 5911-5921.
7. Nelson, J.E.; Kay, M.A. Persistence of recombinant adenovirus in vivo is not dependent on vector DNA replication. J. Virol. 1997, 71, 8902-8907.
8. Ahi, Y.S.; Bangari, D.S.; Mittal, S.K. Adenoviral vector immunity: Its implications and circumvention strategies. Curr. Gene Ther. 2011, 11, 307-320.
9. Thaci, B.; Ulasov, I.V.; Wainwright, D.A.; Lesniak, M.S. The challenge for gene therapy: Innate immune response to adenoviruses. Oncotarget 2011, 2, 113-121.
10. Yang, Y.; Nunes, F.A.; Berencsi, K.; Furth, E.E.; Gonczol, E.; Wilson, J.M. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc. Natl. Acad. Sci. USA 1994, 91, 4407-4411.
11. Berk, A.J. Adenoviridae: The viruses and their replication. In Fields Virology, 5th ed.; Knipe, D.M.; Howley, P.M., Eds.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; pp. 2355-2394.
12. Thomas, G.P.; Mathews, M.B. DNA replication and the early to late transition in adenovirus infection. Cell 1980, 22, 523-533.
13. Parks, R.J.; Chen, L.; Anton, M.; Sankar, U.; Rudnicki, M.A.; Graham, F.L. A helper-dependent adenovirus vector system: Removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc. Natl. Acad. Sci. USA 1996, 93, 13565-13570.
14. Hardy, S.; Kitamura, M.; Harris-Stansil, T.; Dai, Y.; Phipps, M.L. Construction of adenovirus vectors through Cre-lox recombination. J. Virol. 1997, 71, 1842-1849.
15. Umana, P.; Gerdes, C.A.; Stone, D.; Davis, J.R.; Ward, D.; Castro, M.G.; Lowenstein, P.R. Efficient FLPe recombinase enables scalable production of helper-dependent adenoviral vectors with negligible helper-virus contamination. Nat. Biotechnol. 2001, 19, 582-585.
16. Ng, P.; Beauchamp, C.; Evelegh, C.; Parks, R.; Graham, F.L. Development of a FLP/frt system for generating helper-dependent adenoviral vectors. Mol. Ther. 2001, 3, 809-815.
17. Palmer, D.; Ng, P. Improved system for helper-dependent adenoviral vector production. Mol. Ther. 2003, 8, 846-852.
18. Schiedner, G.; Morral, N.; Parks, R.J.; Wu, Y.; Koopmans, S.C.; Langston, C.; Graham, F.L.; Beaudet, A.L.; Kochanek, S. Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nat. Genet. 1998, 18, 180-183.
19. Kim, I.H.; Jozkowicz, A.; Piedra, P.A.; Oka, K.; Chan, L. Lifetime correction of genetic deficiency in mice with a single injection of helper-dependent adenoviral vector. Proc. Natl. Acad. Sci. USA 2001, 98, 13282-13287.
20. Oka, K.; Pastore, L.; Kim, I.H.; Merched, A.; Nomura, S.; Lee, H.J.; Merched-Sauvage, M.; Arden-Riley, C.; Lee, B.; Finegold, M.; et al. Long-term stable correction of low-density lipoprotein receptor-deficient mice with a helper-dependent adenoviral vector expressing the very low-density lipoprotein receptor. Circulation 2001, 103, 1274-1281.
21. Toietta, G.; Mane, V.P.; Norona, W.S.; Finegold, M.J.; Ng, P.; McDonagh, A.F.; Beaudet, A.L.; Lee, B. Lifelong elimination of hyperbilirubinemia in the Gunn rat with a single injection of helper-dependent adenoviral vector. Proc. Natl. Acad. Sci. USA 2005, 102, 3930-3935.
22. Brunetti-Pierri, N.; Nichols, T.C.; McCorquodale, S.; Merricks, E.; Palmer, D.J.; Beaudet, A.L.; Ng, P. Sustained phenotypic correction of canine hemophilia B after systemic administration of helper-dependent adenoviral vector. Hum. Gene Ther. 2005, 16, 811-820.
23. Morral, N.; O'Neal, W.; Rice, K.; Leland, M.; Kaplan, J.; Piedra, P.A.; Zhou, H.; Parks, R.J.; Velji, R.; Aguilar-Cordova, E.; et al. Administration of helper-dependent adenoviral vectors and sequential delivery of different vector serotype for long-term liver-directed gene transfer in baboons. Proc. Natl. Acad. Sci. USA 1999, 96, 12816-12821.
24. Morral, N.; Parks, R.J.; Zhou, H.; Langston, C.; Schiedner, G.; Quinones, J.; Graham, F.L.; Kochanek, S.; Beaudet, A.L. High doses of a helper-dependent adenoviral vector yield supraphysiological levels of alpha1-antitrypsin with negligible toxicity. Hum. Gene Ther. 1998, 9, 2709-2716.
25. Muruve, D.A.; Cotter, M.J.; Zaiss, A.K.; White, L.R.; Liu, Q.; Chan, T.; Clark, S.A.; Ross, P.J.; Meulenbroek, R.A.; Maelandsmo, G.M.; et al. Helper-dependent adenovirus vectors elicit intact innate but attenuated adaptive host immune responses in vivo. J. Virol. 2004, 78, 5966-5972.
26. Parks, R.J. Improvements in adenoviral vector technology: Overcoming barriers for gene therapy. Clin. Genet. 2000, 58, 1-11.
27. Palmer, D.J.; Ng, P. Helper-dependent adenoviral vectors for gene therapy. Hum. Gene Ther. 2005, 16, 1-16.
28. Brunetti-Pierri, N.; Ng, P. Progress and prospects: Gene therapy for genetic diseases with helper-dependent adenoviral vectors. Gene Ther. 2008, 15, 553-560.
29. Parks, R.J.; Evelegh, C.M.; Graham, F.L. Use of helper-dependent adenoviral vectors of alternative serotypes permits repeat vector administration. Gene Ther. 1999, 6, 1565-1573.
30. Smith, A.C.; Poulin, K.L.; Parks, R.J. DNA genome size affects the stability of the adenovirus virion. J. Virol. 2009, 83, 2025-2028.
31. Christensen, J.B.; Byrd, S.A.; Walker, A.K.; Strahler, J.R.; Andrews, P.C.; Imperiale, M.J. Presence of the adenovirus IVa2 protein at a single vertex of the mature virion. J. Virol. 2008, 82, 9086-9093.
32. Liu, H.; Jin, L.; Koh, S.B.; Atanasov, I.; Schein, S.; Wu, L.; Zhou, Z.H. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 2010, 329, 1038-1043.
33. Reddy, V.S.; Natchiar, S.K.; Stewart, P.L.; Nemerow, G.R. Crystal structure of human adenovirus at 3.5 A resolution. Science 2010, 329, 1071-1075.
34. Russell, W.C. Adenoviruses: Update on structure and function. J. Gen. Virol. 2009, 90, 1-20.
35. Mirza, M.A.; Weber, J. Structure of adenovirus chromatin. Biochim. Biophys. Acta 1982, 696, 76-86.
36. Everitt, E.; Sundquist, B.; Pettersson, U.; Philipson, L. Structural proteins of adenoviruses. X. Isolation and topography of low molecular weight antigens from the virion of adenovirus type 2. Virology 1973, 52, 130-147.
37. Brown, D.T.; Westphal, M.; Burlingham, B.T.; Winterhoff, U.; Doerfler, W. Structure and composition of the adenovirus type 2 core. J. Virol. 1975, 16, 366-387.
38. Anderson, C.W.; Young, M.E.; Flint, S.J. Characterization of the adenovirus 2 virion protein, mu. Virology 1989, 172, 506-512.
39. Perez-Berna, A.J.; Marabini, R.; Scheres, S.H.; Menendez-Conejero, R.; Dmitriev, I.P.; Curiel, D.T.; Mangel, W.F.; Flint, S.J.; San Martin, C. Structure and uncoating of immature adenovirus. J. Mol. Biol. 2009, 392, 547-557.
40. Matsumoto, K.; Nagata, K.; Ui, M.; Hanaoka, F. Template activating factor I, a novel host factor required to stimulate the adenovirus core DNA replication. J. Biol. Chem. 1993, 268, 10582-10587.
41. Okuwaki, M.; Nagata, K. Template activating factor-I remodels the chromatin structure and stimulates transcription from the chromatin template. J. Biol. Chem. 1998, 273, 34511-34518.
42. Kennedy, M.A.; Parks, R.J. Adenovirus virion stability and the viral genome: Size matters. Mol. Ther. 2009, 17, 1664-1666.
43. Parks, R.J.; Graham, F.L. A helper-dependent system for adenovirus vector production helps define a lower limit for efficient DNA packaging. J. Virol. 1997, 71, 3293-3298.
44. Parks, R.J.; Bramson, J.L.; Wan, Y.; Addison, C.L.; Graham, F.L. Effects of stuffer DNA on transgene expression from helper-dependent adenovirus vectors. J. Virol. 1999, 73, 8027-8034.
45. Ross, P.J.; Kennedy, M.A.; Parks, R.J. Host cell detection of noncoding stuffer DNA contained in helper-dependent adenovirus vectors leads to epigenetic repression of transgene expression. J. Virol. 2009, 83, 8409-8417.
46. Bergelson, J.M.; Cunningham, J.A.; Droguett, G.; Kurt-Jones, E.A.; Krithivas, A.; Hong, J.S.; Horwitz, M.S.; Crowell, R.L.; Finberg, R.W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997, 275, 1320-1323.
47. Tomko, R.P.; Xu, R.; Philipson, L. HCAR and MCAR: The human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 1997, 94, 3352-3356.
48. Smith, T.A.; Idamakanti, N.; Rollence, M.L.; Marshall-Neff, J.; Kim, J.; Mulgrew, K.; Nemerow, G.R.; Kaleko, M.; Stevenson, S.C. Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Hum. Gene Ther. 2003, 14, 777-787.
49. Shayakhmetov, D.M.; Gaggar, A.; Ni, S.; Li, Z.Y.; Lieber, A. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J. Virol. 2005, 79, 7478-7491.
50. Waddington, S.N.; McVey, J.H.; Bhella, D.; Parker, A.L.; Barker, K.; Atoda, H.; Pink, R.; Buckley, S.M.K.; Greig, J.A.; Denby, L.; et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 2008, 132, 397-409.
51. Kalyuzhniy, O.; Di Paolo, N.C.; Silvestry, M.; Hofherr, S.E.; Barry, M.A.; Stewart, P.L.; Shayakhmetov, D.M. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc. Natl. Acad. Sci. USA 2008, 105, 5483-5488.
52. Wickham, T.J.; Mathias, P.; Cheresh, D.A.; Nemerow, G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73, 309-319.
53. Leopold, P.L.; Ferris, B.; Grinberg, I.; Worgall, S.; Hackett, N.R.; Crystal, R.G. Fluorescent virions: Dynamic tracking of the pathway of adenoviral gene transfer vectors in living cells. Hum. Gene Ther. 1998, 9, 367-378.
54. Wiethoff, C.M.; Wodrich, H.; Gerace, L.; Nemerow, G.R. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 2005, 79, 1992-2000.
55. Greber, U.F.; Willetts, M.; Webster, P.; Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75, 477-486.
56. Chatterjee, P.K.; Vayda, M.E.; Flint, S.J. Identification of proteins and protein domains that contact DNA within adenovirus nucleoprotein cores by ultraviolet light crosslinking of oligonucleotides 32P-labelled in vivo. J. Mol. Biol. 1986, 188, 23-37.
57. Strunze, S.; Engelke, M.F.; Wang, I.H.; Puntener, D.; Boucke, K.; Schleich, S.; Way, M.; Schoenenberger, P.; Burckhardt, C.J.; Greber, U.F. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 2011, 10, 210-223.
58. Greber, U.F.; Puntener, D. DNA-tumor virus entry-From plasma membrane to the nucleus. Semin. Cell Dev. Biol. 2009, 20, 631-642.
59. Gabriel, R.; Schmidt, M.; von Kalle, C. Integration of retroviral vectors. Curr. Opin. Immunol. 2012, 24, 592-597.
60. Hacein-Bey-Abina, S.; von Kalle, C.; Schmidt, M.; Le Deist, F.; Wulffraat, N.; McIntyre, E.; Radford, I.; Villeval, J.L.; Fraser, C.C.; Cavazzana-Calvo, M.; et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. New Engl. J. Med. 2003, 348, 255-256.
61. Hacein-Bey-Abina, S.; Von Kalle, C.; Schmidt, M.; McCormack, M.P.; Wulffraat, N.; Leboulch, P.; Lim, A.; Osborne, C.S.; Pawliuk, R.; Morillon, E.; et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003, 302, 415-419.
62. Harui, A.; Suzuki, S.; Kochanek, S.; Mitani, K. Frequency and stability of chromosomal integration of adenovirus vectors. J. Virol. 1999, 73, 6141-6146.
63. Hillgenberg, M.; Tonnies, H.; Strauss, M. Chromosomal integration pattern of a helperdependent minimal adenovirus vector with a selectable marker inserted into a 27.4-kilobase genomic stuffer. J. Virol. 2001, 75, 9896-9908.
64. Stephen, S.L.; Montini, E.; Sivanandam, V.G.; Al-Dhalimy, M.; Kestler, H.A.; Finegold, M.; Grompe, M.; Kochanek, S. Chromosomal integration of adenoviral vector DNA in vivo. J. Virol. 2010, 84, 9987-9994.
65. Jager, L.; Ehrhardt, A. Persistence of high-capacity adenoviral vectors as replication-defective monomeric genomes in vitro and in murine liver. Hum. Gene Ther. 2009, 20, 883-896.
66. Ehrhardt, A.; Xu, H.; Kay, M.A. Episomal persistence of recombinant adenoviral vector genomes during the cell cycle in vivo. J. Virol. 2003, 77, 7689-7695.
67. Rauschhuber, C.; Noske, N.; Ehrhardt, A. New insights into stability of recombinant adenovirus vector genomes in mammalian cells. Eur. J. Cell Biol. 2012, 91, 2-9.
68. Trotman, L.C.; Mosberger, N.; Fornerod, M.; Stidwill, R.P.; Greber, U.F. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 2001, 3, 1092-1100.
69. Chatterjee, P.K.; Vayda, M.E.; Flint, S.J. Adenoviral protein VII packages intracellular viral DNA throughout the early phase of infection. EMBO J. 1986, 5, 1633-1644.
70. Xue, Y.; Johnson, J.S.; Ornelles, D.A.; Lieberman, J.; Engel, D.A. Adenovirus protein VII functions throughout early phase and interacts with cellular proteins SET and pp32. J. Virol. 2005, 79, 2474-2483.
71. Chen, J.; Morral, N.; Engel, D.A. Transcription releases protein VII from adenovirus chromatin. Virology 2007, 369, 411-422.
72. Karen, K.A.; Hearing, P. Adenovirus core protein VII protects the viral genome from a DNA damage response at early times after infection. J. Virol. 2011, 85, 4135-4142.
73. Walkiewicz, M.P.; Morral, N.; Engel, D.A. Accurate single-day titration of adenovirus vectors based on equivalence of protein VII nuclear dots and infectious particles. J. Virol. Methods 2009, 159, 251-258.
74. Komatsu, T.; Haruki, H.; Nagata, K. Cellular and viral chromatin proteins are positive factors in the regulation of adenovirus gene expression. Nucleic Acids Res. 2011, 39, 889-901.
75. Haruki, H.; Gyurcsik, B.; Okuwaki, M.; Nagata, K. Ternary complex formation between DNAadenovirus core protein VII and TAF-Ibeta/SET, an acidic molecular chaperone. FEBS Lett. 2003, 555, 521-527.
76. Ross, P.J.; Kennedy, M.A.; Christou, C.; Risco Quiroz, M.; Poulin, K.L.; Parks, R.J. Assembly of helper-dependent adenovirus DNA into chromatin promotes efficient gene expression. J. Virol. 2011, 85, 3950-3958.
77. Komatsu, T.; Nagata, K. Replication-uncoupled histone deposition during adenovirus DNA replication. J. Virol. 2012, 86, 6701-6711.
78. Kawase, H.; Okuwaki, M.; Miyaji, M.; Ohba, R.; Handa, H.; Ishimi, Y.; Fujii-Nakata, T.; Kikuchi, A.; Nagata, K. NAP-I is a functional homologue of TAF-I that is required for replication and transcription of the adenovirus genome in a chromatin-like structure. Gene. Cell. 1996, 1, 1045-1056.
79. Okuwaki, M.; Iwamatsu, A.; Tsujimoto, M.; Nagata, K. Identification of nucleophosmin/B23, an acidic nucleolar protein, as a stimulatory factor for in vitro replication of adenovirus DNA complexed with viral basic core proteins. J. Mol. Biol. 2001, 311, 41-55.
80. Gyurcsik, B.; Haruki, H.; Takahashi, T.; Mihara, H.; Nagata, K. Binding modes of the precursor of adenovirus major core protein VII to DNA and template activating factor I: Implication for the mechanism of remodeling of the adenovirus chromatin. Biochemistry 2006, 45, 303-313.
81. Johnson, J.S.; Osheim, Y.N.; Xue, Y.; Emanuel, M.R.; Lewis, P.W.; Bankovich, A.; Beyer, A.L.; Engel, D.A. Adenovirus protein VII condenses DNA, represses transcription, and associates with transcriptional activator E1A. J. Virol. 2004, 78, 6459-6468.
82. Tagami, H.; Ray-Gallet, D.; Almouzni, G.; Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004, 116, 51-61.
83. Smith, S.; Stillman, B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 1989, 58, 15-25.
84. Drane, P.; Ouararhni, K.; Depaux, A.; Shuaib, M.; Hamiche, A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 2010, 24, 1253-1265.
85. Lewis, P.W.; Elsaesser, S.J.; Noh, K.M.; Stadler, S.C.; Allis, C.D. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. USA 2010, 107, 14075-14080.
86. Goldberg, A.D.; Banaszynski, L.A.; Noh, K.M.; Lewis, P.W.; Elsaesser, S.J.; Stadler, S.; Dewell, S.; Law, M.; Guo, X.; Li, X.; et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140, 678-691.
87. Schneiderman, J.I.; Orsi, G.A.; Hughes, K.T.; Loppin, B.; Ahmad, K. Nucleosome-depleted chromatin gaps recruit assembly factors for the H3.3 histone variant. Proc. Natl. Acad. Sci. USA 2012, 109, 19721-19726.
88. Placek, B.J.; Huang, J.; Kent, J.R.; Dorsey, J.; Rice, L.; Fraser, N.W.; Berger, S.L. The histone variant H3.3 regulates gene expression during lytic infection with herpes simplex virus type 1. J. Virol. 2009, 83, 1416-1421.
89. Pastore, L.; Morral, N.; Zhou, H.; Garcia, R.; Parks, R.J.; Kochanek, S.; Graham, F.L.; Lee, B.; Beaudet, A.L. Use of a liver-specific promoter reduces immune response to the transgene in adenoviral vectors. Hum. Gene Ther. 1999, 10, 1773-1781.
90. Schiedner, G.; Hertel, S.; Johnston, M.; Biermann, V.; Dries, V.; Kochanek, S. Variables affecting in vivo performance of high-capacity adenovirus vectors. J. Virol. 2002, 76, 1600-1609.
91. Jenuwein, T.; Allis, C.D. Translating the histone code. Science 2001, 293, 1074-1080.
92. Smith, C.L.; Hager, G.L. Transcriptional regulation of mammalian genes in vivo. A tale of two templates. J. Biol. Chem. 1997, 272, 27493-27496.
93. Jiang, C.; Pugh, B.F. Nucleosome positioning and gene regulation: Advances through genomics. Nat. Rev. Genet. 2009, 10, 161-172.
94. Lomvardas, S.; Thanos, D. Modifying gene expression programs by altering core promoter chromatin architecture. Cell 2002, 110, 261-271.
95. Schreiner, S.; Wimmer, P.; Sirma, H.; Everett, R.D.; Blanchette, P.; Groitl, P.; Dobner, T. Proteasome-dependent degradation of Daxx by the viral E1B-55K protein in human adenovirusinfected cells. J. Virol. 2010, 84, 7029-7038.
96. Ullman, A.J.; Hearing, P. Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. J. Virol. 2008, 82, 7325-7335.
97. Schreiner, S.; Burck, C.; Glass, M.; Groitl, P.; Wimmer, P.; Kinkley, S.; Mund, A.; Everett, R.D.; Dobner, T. Control of human adenovirus type 5 gene expression by cellular Daxx/ATRX chromatin-associated complexes. Nucleic Acids Res. 2013, 41, 3532-3550.
98. Schreiner, S.; Martinez, R.; Groitl, P.; Rayne, F.; Vaillant, R.; Wimmer, P.; Bossis, G.; Sternsdorf, T.; Marcinowski, L.; Ruzsics, Z.; et al. Transcriptional activation of the adenoviral genome is mediated by capsid protein VI. PLoS Path. 2012, 8, e1002549.
99. Suzuki, M.; Cerullo, V.; Bertin, T.K.; Cela, R.; Clarke, C.; Guenther, M.; Brunetti-Pierri, N.; Lee, B. MyD88-dependent silencing of transgene expression during the innate and adaptive immune response to helper-dependent adenovirus. Hum. Gene Ther. 2010, 21, 325-336.
100. Cerullo, V.; Seiler, M.P.; Mane, V.; Brunetti-Pierri, N.; Clarke, C.; Bertin, T.K.; Rodgers, J.R.; Lee, B. Toll-like receptor 9 triggers an innate immune response to helper-dependent adenoviral vectors. Mol. Ther. 2007, 15, 378-385.
101. Brestovitsky, A.; Sharf, R.; Mittelman, K.; Kleinberger, T. The adenovirus E4orf4 protein targets PP2A to the ACF chromatin-remodeling factor and induces cell death through regulation of SNF2h-containing complexes. Nucleic Acids Res. 2011, 39, 6414-6427.
102. 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. 1998, 140, 637-645.
103. 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. 1998, 72, 7144-7153.