The adenovirus genome contributes to the structural stability of the virion

Viruses

Volumn 6, Issue 9, 2014, Pages 3563-3583

  Saha, Bratati ^a,b   Wong, Carmen M ^a,b   Parks, Robin J ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Adenovirus; Helper dependent Ad; Viral vectors; Virion stability

Indexed keywords

ADENOVIRUS VECTOR; VIRUS DNA;

ADENOVIRUS; ADENOVIRUS INFECTION; DNA PACKAGING; GENE EXPRESSION; GENETIC STABILITY; GENOME SIZE; GENOMIC INSTABILITY; NONHUMAN; REVIEW; THERMOSTABILITY; TRANSGENE; VIRION; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME; ADENOVIRIDAE; GENE TRANSFER; GENE VECTOR; GENETICS; HUMAN; PHYSIOLOGY;

ADENOVIRIDAE;

ADENOVIRIDAE; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GENOME SIZE; GENOME, VIRAL; HUMANS; VIRION;

EID: 84907907831     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v6093563     Document Type: Review

References (149)

1. Wold, W.S.; Horwitz, M.S. Adenoviruses. In Fields Virology, 5th ed.; Knipe, D.M., Howley, P.M., Eds.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; pp. 2396–2436.
2. 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.
3. Ginn, S.L.; Alexander, I.E.; Edelstein, M.L.; Abedi, M.R.; Wixon, J. Gene therapy clinical trials worldwide to 2012—An update. J. Gene Med. 2013, 15, 65–77.
4. 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.
5. Yang, Y.; Jooss, K.U.; Su, Q.; Ertl, H.C.; Wilson, J.M. Immune responses to viral antigens versus transgene product in the elimination of recombinant adenovirus-infected hepatocytes in vivo. Gene Ther. 1996, 3, 137–144.
6. Yang, Y.; Li, Q.; Ertl, H.C.; Wilson, J.M. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J. Virol. 1995, 69, 2004–2015.
7. 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.
8. Palmer, D.J.; Ng, P. Helper-dependent adenoviral vectors for gene therapy. Hum. Gene Ther. 2005, 16, 1–16.
9. Rowe, W.P.; Huebner, R.J.; Gilmore, L.K.; Parrott, R.H.; Ward, T.G. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc. Soc. Exp. Biol. Med. 1953, 84, 570–573.
10. Hilleman, M.R.; Werner, J.H. Recovery of new agents from patients with acute respiratory illness. Proc. Soc. Exp. Biol. Med. 1954, 85, 183–188.
11. Musher, D.M. How contagious are common respiratory tract infections? N. Engl. J. Med. 2003, 348, 1256–1266.
12. Hoke, C.H., Jr.; Snyder, C.E., Jr. History of the restoration of adenovirus type 4 and type 7 vaccine, live oral (Adenovirus Vaccine) in the context of the Department of Defense acquisition system. Vaccine 2013, 31, 1623–1632.
13. Rocholl, C.; Gerber, K.; Daly, J.; Pavia, A.T.; Byington, C.L. Adenoviral infections in children: The impact of rapid diagnosis. Pediatrics 2004, 113, e51–e56.
14. Horwitz, M.A. Adenoviruses. In Fields Virology; Fields, B.N., Knipe, D.M., Howley, P.M., Eds.; Lippincott-Raven Publishers: Philadelphia, PA, USA, 1996; pp. 2149–2171.
15. Trentin, J.J.; Yabe, Y.; Taylor, G. The quest for human cancer viruses. Science 1962, 137, 835–841.
16. Yabe, Y.; Trentin, J.J.; Taylor, G. Cancer induction in hamsters by human type 12 adenovirus. Effect of age and of virus dose. Proc. Soc. Exp. Biol. Med. 1962, 111, 343–344.
17. Flint, J. Organization of the adenoviral genome. In Adenoviruses: Basic Biology to Gene Therapy; Seth, P., Ed.; R.G. Landes Company: Austin, TX, USA, 1999; pp. 17–30.
18. Berget, S.M.; Moore, C.; Sharp, P.A. Spliced segments at the 5' terminus of adenovirus 2 late mRNA. Proc. Natl. Acad. Sci. USA 1977, 74, 3171–3175.
19. Chow, L.T.; Gelinas, R.E.; Broker, T.R.; Roberts, R.J. An amazing sequence arrangement at the 5' ends of adenovirus 2 messenger RNA. Cell 1977, 12, 1–8.
20. Harlow, E.; Whyte, P.; Franza, B.R., Jr.; Schley, C. Association of adenovirus early-region 1A proteins with cellular polypeptides. Mol. Cell. Biol. 1986, 6, 1579–1589.
21. Davison, A.J.; Benko, M.; Harrach, B. Genetic content and evolution of adenoviruses. J. Gen. Virol. 2003, 84, 2895–2908.
22. Horwitz, M.S. Function of adenovirus E3 proteins and their interactions with immunoregulatory cell proteins. J. Gene Med. 2004, 6 (Suppl. S1), S172–S183.
23. Weitzman, M.D. Functions of the adenovirus E4 proteins and their impact on viral vectors. Front. Biosci. 2005, 10, 1106–1117.
24. Morris, S.J.; Scott, G.E.; Leppard, K.N. Adenovirus late-phase infection is controlled by a novel L4 promoter. J. Virol. 2010, 84, 7096–7104.
25. Ying, B.; Tollefson, A.E.; Wold, W.S. Identification of a previously unrecognized promoter that drives expression of the UXP transcription unit in the human adenovirus type 5 genome. J. Virol. 2010, 84, 11470–11478.
26. 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.
27. O'Malley, R.P.; Mariano, T.M.; Siekierka, J.; Mathews, M.B. A mechanism for the control of protein synthesis by adenovirus VA RNAI. Cell 1986, 44, 391–400.
28. Aparicio, O.; Razquin, N.; Zaratiegui, M.; Narvaiza, I.; Fortes, P. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 2006, 80, 1376–1384.
29. Tollefson, A.E.; Ying, B.; Doronin, K.; Sidor, P.D.; Wold, W.S. Identification of a new human adenovirus protein encoded by a novel late l-strand transcription unit. J. Virol. 2007, 81, 12918–12926.
30. Zhao, H.; Chen, M.; Pettersson, U. A new look at adenovirus splicing. Virology 2014, 456–457, 329–341.
31. Wong, C.M.; McFall, E.R.; Burns, J.K.; Parks, R.J. The role of chromatin in adenoviral vector function. Viruses 2013, 5, 1500–1515.
32. Ostapchuk, P.; Hearing, P. Control of adenovirus packaging. J. Cell. Biochem. 2005, 96, 25–35.
33. Guimet, D.; Hearing, P. The adenovirus L4–22K protein has distinct functions in the posttranscriptional regulation of gene expression and encapsidation of the viral genome. J. Virol. 2013, 87, 7688–7699.
34. Mangel, W.F.; McGrath, W.J.; Toledo, D.L.; Anderson, C.W. Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity. Nature 1993, 361, 274–275.
35. Russell, W.C. Adenoviruses: Update on structure and function. J. Gen. Virol. 2009, 90, 1–20.
36. 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.
37. 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.
38. Reddy, V.S.; Nemerow, G.R. Structures and organization of adenovirus cement proteins provide insights into the role of capsid maturation in virus entry and infection. Proc. Natl. Acad. Sci. USA 2014, 111, 11715–11720.
39. Rux, J.J.; Burnett, R.M. Adenovirus structure. Hum. Gene Ther. 2004, 15, 1167–1176.
40. Maizel, J.V., Jr.; White, D.O.; Scharff, M.D. The polypeptides of adenovirus. II. Soluble proteins, cores, top components and the structure of the virion. Virology 1968, 36, 126–136.
41. Russell, W.C.; Laver, W.G.; Sanderson, P.J. Internal components of adenovirus. Nature 1968, 219, 1127–1130.
42. 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.
43. Mirza, M.A.; Weber, J. Structure of adenovirus chromatin. Biochim. Biophys. Acta 1982, 696, 76–86.
44. Newcomb, W.W.; Boring, J.W.; Brown, J.C. Ion etching of human adenovirus 2: Structure of the core. J. Virol. 1984, 51, 52–56.
45. 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.
46. 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.
47. Perez-Vargas, J.; Vaughan, R.C.; Houser, C.; Hastie, K.M.; Kao, C.C.; Nemerow, G.R. Isolation and characterization of the DNA and protein binding activities of adenovirus core protein V. J. Virol. 2014, 88, 9287–9296.
48. Everitt, E.; Lutter, L.; Philipson, L. Structural proteins of adenoviruses. XII. Location and neighbor relationship among proteins of adenovirion type 2 as revealed by enzymatic iodination, immunoprecipitation and chemical cross-linking. Virology 1975, 67, 197–208.
49. Fabry, C.M.; Rosa-Calatrava, M.; Moriscot, C.; Ruigrok, R.W.; Boulanger, P.; Schoehn, G. The C-terminal domains of adenovirus serotype 5 protein IX assemble into an antiparallel structure on the facets of the capsid. J. Virol. 2009, 83, 1135–1139.
50. Chatterjee, P.K.; Vayda, M.E.; Flint, S.J. Interactions among the three adenovirus core proteins. J. Virol. 1985, 55, 379–386.
51. Stewart, P.L.; Fuller, S.D.; Burnett, R.M. Difference imaging of adenovirus: Bridging the resolution gap between X-ray crystallography and electron microscopy. EMBO J. 1993, 12, 2589–2599.
52. Saban, S.D.; Silvestry, M.; Nemerow, G.R.; Stewart, P.L. Visualization of alpha-helices in a 6-angstrom resolution cryoelectron microscopy structure of adenovirus allows refinement of capsid protein assignments. J. Virol. 2006, 80, 12049–12059.
53. Anderson, C.W.; Young, M.E.; Flint, S.J. Characterization of the adenovirus 2 virion protein, mu. Virology 1989, 172, 506–512.
54. 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.
55. Fabry, C.M.; Rosa-Calatrava, M.; Conway, J.F.; Zubieta, C.; Cusack, S.; Ruigrok, R.W.; Schoehn, G. A quasi-atomic model of human adenovirus type 5 capsid. EMBO J. 2005, 24, 1645–1654.
56. Booy, F.P.; Newcomb, W.W.; Trus, B.L.; Brown, J.C.; Baker, T.S.; Steven, A.C. Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 1991, 64, 1007–1015.
57. Lepault, J.; Dubochet, J.; Baschong, W.; Kellenberger, E. Organization of double-stranded DNA in bacteriophages: A study by cryo-electron microscopy of vitrified samples. EMBO J. 1987, 6, 1507–1512.
58. Hearing, P.; Samulski, R.J.; Wishart, W.L.; Shenk, T. Identification of a repeated sequence element required for efficient encapsidation of the adenovirus type 5 chromosome. J. Virol. 1987, 61, 2555–2558.
59. Daniell, E. Genome structure of incomplete particles of adenovirus. J. Virol. 1976, 19, 685–708.
60. Morsy, M.A.; Gu, M.C.; Zhao, J.Z.; Holder, D.J.; Rogers, I.T.; Pouch, W.J.; Motzel, S.L.; Klein, H.J.; Gupta, S.K.; Liang, X. et al. Leptin gene therapy and daily protein administration: A comparative study in the ob/ob mouse. Gene Ther. 1998, 5, 8–18.
61. 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.
62. Gilbert, R.; Dudley, R.W.; Liu, A.B.; Petrof, B.J.; Nalbantoglu, J.; Karpati, G. Prolonged dystrophin expression and functional correction of mdx mouse muscle following gene transfer with a helper-dependent (gutted) adenovirus-encoding murine dystrophin. Hum. Mol. Genet. 2003, 12, 1287–1299.
63. Ostapchuk, P.; Hearing, P. Minimal cis-acting elements required for adenovirus genome packaging. J. Virol. 2003, 77, 5127–5135.
64. Grable, M.; Hearing, P. Adenovirus type 5 packaging domain is composed of a repeated element that is functionally redundant. J. Virol. 1990, 64, 2047–2056.
65. Zhang, W.; Imperiale, M.J. Interaction of the adenovirus IVa2 protein with viral packaging sequences. J. Virol. 2000, 74, 2687–2693.
66. Ostapchuk, P.; Anderson, M.E.; Chandrasekhar, S.; Hearing, P. The L4 22-kilodalton protein plays a role in packaging of the adenovirus genome. J. Virol. 2006, 80, 6973–6981.
67. Ewing, S.G.; Byrd, S.A.; Christensen, J.B.; Tyler, R.E.; Imperiale, M.J. Ternary complex formation on the adenovirus packaging sequence by the IVa2 and L4 22-kilodalton proteins. J. Virol. 2007, 81, 12450–12457.
68. Wu, K.; Orozco, D.; Hearing, P. The adenovirus L4–22K protein is multifunctional and is an integral component of crucial aspects of infection. J. Virol. 2012, 86, 10474–10483.
69. Ali, H.; LeRoy, G.; Bridge, G.; Flint, S.J. The adenovirus L4 33-kilodalton protein binds to intragenic sequences of the major late promoter required for late phase-specific stimulation of transcription. J. Virol. 2007, 81, 1327–1338.
70. Hasson, T.B.; Soloway, P.D.; Ornelles, D.A.; Doerfler, W.; Shenk, T. Adenovirus L1 52-and 55-kilodalton proteins are required for assembly of virions. J. Virol. 1989, 63, 3612–3621.
71. Gustin, K.E.; Imperiale, M.J. Encapsidation of viral DNA requires the adenovirus L1 52/55-kilodalton protein. J. Virol. 1998, 72, 7860–7870.
72. Perez-Romero, P.; Tyler, R.E.; Abend, J.R.; Dus, M.; Imperiale, M.J. Analysis of the interaction of the adenovirus L1 52/55-kilodalton and IVa2 proteins with the packaging sequence in vivo and in vitro. J. Virol. 2005, 79, 2366–2374.
73. Ma, H.C.; Hearing, P. Adenovirus structural protein IIIa is involved in the serotype specificity of viral DNA packaging. J. Virol. 2011, 85, 7849–7855.
74. Stilwell, J.L.; McCarty, D.M.; Negishi, A.; Superfine, R.; Samulski, R.J. Development and characterization of novel empty adenovirus capsids and their impact on cellular gene expression. J. Virol. 2003, 77, 12881–12885.
75. Muruve, D.A.; Petrilli, V.; Zaiss, A.K.; White, L.R.; Clark, S.A.; Ross, P.J.; Parks, R.J.; Tschopp, J. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 2008, 452, 103–107.
76. Wu, K.; Guimet, D.; Hearing, P. The adenovirus L4–33K protein regulates both late gene expression patterns and viral DNA packaging. J. Virol. 2013, 87, 6739–6747.
77. Ostapchuk, P.; Hearing, P. Regulation of adenovirus packaging. Curr. Top. Microbiol. Immunol. 2003, 272, 165–185.
78. Ostapchuk, P.; Hearing, P. Adenovirus IVa2 protein binds ATP. J. Virol. 2008, 82, 10290–10294.
79. Giberson, A.N.; Davidson, A.R.; Parks, R.J. Chromatin structure of adenovirus DNA throughout infection. Nucleic Acids Res. 2012, 40, 2369–2376.
80. 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.
81. 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.
82. 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.
83. 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.
84. 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.
85. 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.
86. 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.
87. 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.
88. 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.
89. Greber, U.F.; Willetts, M.; Webster, P.; Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75, 477–486.
90. 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.
91. 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.
92. Komatsu, T.; Nagata, K. Replication-uncoupled histone deposition during adenovirus DNA replication. J. Virol. 2012, 86, 6701–6711.
93. 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.
94. Bett, A.J.; Prevec, L.; Graham, F.L. Packaging capacity and stability of human adenovirus type 5 vectors. J. Virol. 1993, 67, 5911–5921.
95. Wellington, C.L.; Brunham, L.R.; Zhou, S.; Singaraja, R.R.; Visscher, H.; Gelfer, A.; Ross, C.; James, E.; Liu, G.; Huber, M.T. et al. Alterations of plasma lipids in mice via adenoviral-mediated hepatic overexpression of human ABCA1. J. Lipid Res. 2003, 44, 1470–1480.
96. Hubberstey, A.V.; Pavliv, M.; Parks, R.J. Cancer therapy utilizing an adenoviral vector expressing only E1A. Cancer Gene Ther. 2002, 9, 321–329.
97. Mizuguchi, H.; Funakoshi, N.; Hosono, T.; Sakurai, F.; Kawabata, K.; Yamaguchi, T.; Hayakawa, T. Rapid construction of small interfering RNA-expressing adenoviral vectors on the basis of direct cloning of short hairpin RNA-coding DNAs. Hum. Gene Ther. 2007, 18, 74–80.
98. 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.
99. 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.
100. Mitani, K.; Graham, F.L.; Caskey, C.T.; Kochanek, S. Rescue, propagation, and partial purification of a helper virus-dependent adenovirus vector. Proc. Natl. Acad. Sci. USA 1995, 92, 3854–3858.
101. Fisher, K.J.; Choi, H.; Burda, J.; Chen, S.J.; Wilson, J.M. Recombinant adenovirus deleted of all viral genes for gene therapy of cystic fibrosis. Virology 1996, 217, 11–22.
102. Haecker, S.E.; Stedman, H.H.; Balice-Gordon, R.J.; Smith, D.B.; Greelish, J.P.; Mitchell, M.A.; Wells, A.; Sweeney, H.L.; Wilson, J.M. In vivo expression of full-length human dystrophin from adenoviral vectors deleted of all viral genes. Hum. Gene Ther. 1996, 7, 1907–1914.
103. Kumar-Singh, R.; Chamberlain, J.S. Encapsidated adenovirus minichromosomes allow delivery and expression of a 14 kb dystrophin cDNA to muscle cells. Hum. Mol. Genet. 1996, 5, 913–921.
104. Kumar-Singh, R.; Farber, D.B. Encapsidated adenovirus mini-chromosome-mediated delivery of genes to the retina: Application to the rescue of photoreceptor degeneration. Hum. Mol. Genet. 1998, 7, 1893–1900.
105. Kochanek, S.; Clemens, P.R.; Mitani, K.; Chen, H.H.; Chan, S.; Caskey, C.T. A new adenoviral vector: Replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and beta-galactosidase. Proc. Natl. Acad. Sci. USA 1996, 93, 5731–5736.
106. Lieber, A.; He, C.Y.; Kirillova, I.; Kay, M.A. 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. 1996, 70, 8944–8960.
107. 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.
108. 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.
109. 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.
110. 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.
111. Palmer, D.; Ng, P. Improved system for helper-dependent adenoviral vector production. Mol. Ther. 2003, 8, 846–852.
112. Sandig, V.; Youil, R.; Bett, A.J.; Franlin, L.L.; Oshima, M.; Maione, D.; Wang, F.; Metzker, M.L.; Savino, R.; Caskey, C.T. Optimization of the helper-dependent adenovirus system for production and potency in vivo. Proc. Natl. Acad. Sci. USA 2000, 97, 1002–1007.
113. Morsy, M.A.; Gu, M.; Motzel, S.; Zhao, J.; Lin, J.; Su, Q.; Allen, H.; Franlin, L.; Parks, R.J.; Graham, F.L. et al. An adenoviral vector deleted for all viral coding sequences results in enhanced safety and extended expression of a leptin transgene. Proc. Natl. Acad. Sci. USA 1998, 95, 7866–7871.
114. 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.
115. 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.
116. 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.
117. Parks, R.J. Improvements in adenoviral vector technology: Overcoming barriers for gene therapy. Clin. Genet. 2000, 58, 1–11.
118. Brunetti-Pierri, N.; Ng, T.; Iannitti, D.; Cioffi, W.; Stapleton, G.; Law, M.; Breinholt, J.; Palmer, D.; Grove, N.; Rice, K. et al. Transgene expression up to 7 years in nonhuman primates following hepatic transduction with helper-dependent adenoviral vectors. Hum. Gene Ther. 2013, 24, 761–765.
119. Sargent, K.; Ng, P.; Evelegh, C.; Graham, F.L.; Parks, R.J. Development of a size restricted pIX deleted helper virus for amplificaton of helper dependent adenovirus vectors. Gene Ther. 2004, 11, 504–511.
120. GhoshChoudhury, G.; Haj-Ahmad, Y.; Graham, F.L. Protein IX, a minor component of the human adenovirus capsid, is essential for the packaging of full length genomes. EMBO J. 1987, 6, 1733–1739.
121. Parks, R.J. Adenovirus protein IX: A new look at an old protein. Mol. Ther. 2005, 11, 19–25.
122. Colby, W.W.; Shenk, T. Adenovirus type 5 virions can be assembled in vivo in the absence of detectable polypeptide IX. J. Virol. 1981, 39, 977–980.
123. Louis, N.; Evelegh, C.; Graham, F.L. Cloning and sequencing of the cellular-viral junctions from the human adenovirus type 5 transformed 293 cell line. Virology 1997, 233, 423–429.
124. Sargent, K.; Meulenbroek, R.A.; Parks, R.J. Activation of adenoviral gene expression by protein IX is not required for efficient virus replication. J. Virol. 2004, 78, 5032–5037.
125. 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.
126. Kennedy, M.A.; Parks, R.J. Adenovirus virion stability and the viral genome: Size matters. Mol. Ther. 2009, 17, 1664–1666.
127. Shayakhmetov, D.M.; Li, Z.Y.; Gaggar, A.; Gharwan, H.; Ternovoi, V.; Sandig, V.; Lieber, A. Genome size and structure determine efficiency of postinternalization steps and gene transfer of capsid-modified adenovirus vectors in a cell-type-specific manner. J. Virol. 2004, 78, 10009–10022.
128. Benevento, M.; Di Palma, S.; Snijder, J.; Moyer, C.L.; Reddy, V.S.; Nemerow, G.R.; Heck, A.J. Adenovirus composition, proteolysis, and disassembly studied by in-depth qualitative and quantitative proteomics. J. Biol. Chem. 2014, 289, 11421–11430.
129. Ivanovska, I.; Wuite, G.; Jonsson, B.; Evilevitch, A. Internal DNA pressure modifies stability of WT phage. Proc. Natl. Acad. Sci. USA 2007, 104, 9603–9608.
130. Tzlil, S.; Kindt, J.T.; Gelbart, W.M.; Ben-Shaul, A. Forces and pressures in DNA packaging and release from viral capsids. Biophys. J. 2003, 84, 1616–1627.
131. Evilevitch, A.; Roos, W.H.; Ivanovska, I.L.; Jeembaeva, M.; Jonsson, B.; Wuite, G.J. Effects of salts on internal DNA pressure and mechanical properties of phage capsids. J. Mol. Biol. 2011, 405, 18–23.
132. Ortega-Esteban, A.; Perez-Berna, A.J.; Menendez-Conejero, R.; Flint, S.J.; San Martin, C.; de Pablo, P.J. Monitoring dynamics of human adenovirus disassembly induced by mechanical fatigue. Sci. Rep. 2013, 3, 1434.
133. Snijder, J.; Reddy, V.S.; May, E.R.; Roos, W.H.; Nemerow, G.R.; Wuite, G.J. Integrin and defensin modulate the mechanical properties of adenovirus. J. Virol. 2013, 87, 2756–2766.
134. Carrasco, C.; Carreira, A.; Schaap, I.A.; Serena, P.A.; Gomez-Herrero, J.; Mateu, M.G.; de Pablo, P.J. DNA-mediated anisotropic mechanical reinforcement of a virus. Proc. Natl. Acad. Sci. USA 2006, 103, 13706–13711.
135. Reguera, J.; Grueso, E.; Carreira, A.; Sanchez-Martinez, C.; Almendral, J.M.; Mateu, M.G. Functional relevance of amino acid residues involved in interactions with ordered nucleic acid in a spherical virus. J. Biol. Chem. 2005, 280, 17969–17977.
136. Carrasco, C.; Castellanos, M.; de Pablo, P.J.; Mateu, M.G. Manipulation of the mechanical properties of a virus by protein engineering. Proc. Natl. Acad. Sci. USA 2008, 105, 4150–4155.
137. Li, T.; Chen, Z.; Johnson, J.E.; Thomas, G.J., Jr. Conformations, interactions, and thermostabilities of RNA and proteins in bean pod mottle virus: Investigation of solution and crystal structures by laser Raman spectroscopy. Biochemistry 1992, 31, 6673–6682.
138. Da Poian, A.T.; Johnson, J.E.; Silva, J.L. Protein-RNA interactions and virus stability as probed by the dynamics of tryptophan side chains. J. Biol. Chem. 2002, 277, 47596–47602.
139. Michel, J.P.; Ivanovska, I.L.; Gibbons, M.M.; Klug, W.S.; Knobler, C.M.; Wuite, G.J.; Schmidt, C.F. Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc. Natl. Acad. Sci. USA 2006, 103, 6184–6189.
140. Horowitz, E.D.; Rahman, K.S.; Bower, B.D.; Dismuke, D.J.; Falvo, M.R.; Griffith, J.D.; Harvey, S.C.; Asokan, A. Biophysical and ultrastructural characterization of adeno-associated virus capsid uncoating and genome release. J. Virol. 2013, 87, 2994–3002.
141. Allocca, M.; Doria, M.; Petrillo, M.; Colella, P.; Garcia-Hoyos, M.; Gibbs, D.; Kim, S.R.; Maguire, A.; Rex, T.S.; Di Vicino, U. et al. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J. Clin. Invest. 2008, 118, 1955–1964.
142. Dong, B.; Nakai, H.; Xiao, W. Characterization of genome integrity for oversized recombinant AAV vector. Mol. Ther. 2010, 18, 87–92.
143. Lai, Y.; Yue, Y.; Duan, D. Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome > or = 8.2 kb. Mol. Ther. 2010, 18, 75–79.
144. Wu, Z.; Yang, H.; Colosi, P. Effect of genome size on AAV vector packaging. Mol. Ther. 2010, 18, 80–86.
145. de Vrij, J.; van den Hengel, S.K.; Uil, T.G.; Koppers-Lalic, D.; Dautzenberg, I.J.; Stassen, O.M.; Barcena, M.; Yamamoto, M.; de Ridder, C.M.; Kraaij, R. et al. Enhanced transduction of CAR-negative cells by protein IX-gene deleted adenovirus 5 vectors. Virology 2011, 410, 192–200.
146. Yamaguchi, T.; Kawabata, K.; Koizumi, N.; Sakurai, F.; Nakashima, K.; Sakurai, H.; Sasaki, T.; Okada, N.; Yamanishi, K.; Mizuguchi, H. Role of MyD88 and TLR9 in the innate immune response elicited by serotype 5 adenoviral vectors. Hum. Gene Ther. 2007, 18, 753–762.
147. Appledorn, D.M.; Patial, S.; McBride, A.; Godbehere, S.; Van Rooijen, N.; Parameswaran, N.; Amalfitano, A. Adenovirus vector-induced innate inflammatory mediators, MAPK signaling, as well as adaptive immune responses are dependent upon both TLR2 and TLR9 in vivo. J. Immunol. 2008, 181, 2134–2144.
148. Fejer, G.; Drechsel, L.; Liese, J.; Schleicher, U.; Ruzsics, Z.; Imelli, N.; Greber, U.F.; Keck, S.; Hildenbrand, B.; Krug, A. et al. Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog. 2008, 4, e1000208.
149. Teigler, J.E.; Kagan, J.C.; Barouch, D.H. Late endosomal trafficking of alternative serotype adenovirus vaccine vectors augments antiviral innate immunity. J. Virol. 2014, 88, 10354–10363.