Reduced infectivity of adenovirus type 5 particles and degradation of entering viral genomes associated with incomplete processing of the preterminal protein

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13554-13565

  Kato, Sayuri E ^a   Chahal, Jasdave S ^a   Flint, S J ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA; VIRUS FIBER PROTEIN; VIRUS PROTEIN;

ADENOVIRUS 5; ARTICLE; CELL LEVEL; CONTROLLED STUDY; CYTOSOL; DNA METABOLISM; EPITHELIUM CELL; FIBROBLAST; FRAMESHIFT MUTATION; GENE IDENTIFICATION; GENE REPLICATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; VIRION; VIRUS FIBER; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS PARTICLE;

ADENOVIRIDAE; CELL LINE; DNA, VIRAL; FLUORESCENT ANTIBODY TECHNIQUE; FRAMESHIFT MUTATION; GENOME, VIRAL; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRAL PROTEINS; VIRION; VIRULENCE;

HUMAN ADENOVIRUS TYPE 5;

EID: 84870689285     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02337-12     Document Type: Article

References (110)

1. Bai M, Harfe B, Freimuth P. 1993. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J. Virol.67:5198-5205.
2. Bailey CJ, Crystal RG, Leopold PL. 2003. Association of adenovirus with the microtubule organizing center. J. Virol. 77:13275-13287.
3. Barber GN. 2011. Cytoplasmic DNA innate immune pathways. Immunol. Rev. 243:99-108.
4. Bergelson JM, et al. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
5. Berk AJ. 2007. Adenoviridae: the viruses and their replication, p 2355-2394. In Knipe DM, Howley PM (ed), Fields virology, 5 ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
6. Bewley MC, Springer K, Zhang YB, Freimuth P, Flanagan JM. 1999. Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 286:1579-1583.
7. Blankenberg D, et al. 2010. Galaxy: a web-based genome analysis tool for experimentalists. Curr. Protoc. Mol. Biol. Chapter 19:Unit 19.10.1-21.
8. Bremner KH, et al. 2009. Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe6:523-535.
9. Burckhardt CJ, et al. 2011. Drifting motions of the adenovirus receptor CAR and immobile integrins initiate virus uncoating and membrane lytic protein exposure. Cell Host Microbe 10:105-117.
10. Cervera MM, Dreyfuss G, Penman S. 1981. Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected HeLa cells. Cell 23:113-120.
11. Chahal JS, Flint SJ. 2012. Timely synthesis of the adenovirus type 5 E1B 55-kilodalton protein is required for efficient genome replication in normal human cells. J. Virol. 86:3064-3072.
12. Chatterjee PK, Vayda ME, Flint SJ. 1986. Adenoviral protein VII packages intracellular viral DNA throughout the early phase of infection. EMBO J. 5:1633-1644.
13. Chatterjee PK, Vayda ME, Flint SJ. 1986. Identification of proteins and protein domains that contact DNA within adenovirus nucleoprotein cores by ultraviolet light crosslinking of oligonucleotides 32P-labeled in vivo. J. Mol. Biol. 188:23-37.
14. Chiu CY, Mathias P, Nemerow GR, Stewart PL. 1999. Structure of adenovirus complexed with its internalization receptor, alphavbeta5 integrin. J. Virol. 73:6759-6768.
15. Chroboczek J, Bieber F, Jacrot B. 1992. The sequence of the genome of adenovirus type 5 and its comparison with the genome of adenovirus type 2. Virology 186:280 -285.
16. Dales S, Chardonnet Y. 1973. Early events in the interaction of adenoviruses with HeLa cells. during vectorial movement of the inoculum. Virology 56:465- 483.
17. Edwards SJ, et al. 2002. Evidence that replication of the antitumor adenovirus ONYX-015 is not controlled by the p53 and p14(ARF) tumor suppressor genes. J. Virol. 76:12483-12490.
18. Einfeld DA, et al. 2001. Reducing the native tropism of adenovirus vectors requires removal of both CAR and integrin interactions. J. Virol.75:11284 -11291.
19. Engelke MF, Burckhardt CJ, Morf MK, Greber UF. 2011. The dynactin complex enhances the speed of microtubule-dependent motions of adenovirus both towards and away from the nucleus. Viruses 3:233-253.
20. Field J, Gronostajski RM, Hurwitz J. 1984. Properties of the adenovirus DNA polymerase. J. Biol. Chem. 259:9487-9495.
21. Gastaldelli M, et al. 2008. Infectious adenovirus type 2 transport through early but not late endosomes. Traffic 9:2265-2278.
22. Giardine B, et al. 2005. Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 15:1451-1455.
23. Goecks J, Nekrutenko A, Taylor J. 2010. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 11:R86.
24. Gonzalez R, Huang W, Finnen R, Bragg C, Flint SJ. 2006. Adenovirus E1B 55-kilodalton protein is required for both regulation of mRNA export and efficient entry into the late phase of infection in normal human fibroblasts. J. Virol. 80:964 -974.
25. Gonzalez RA, Flint SJ. 2002. Effects of mutations in the adenoviral E1B 55 kDa protein coding sequence on viral latemRNAmetabolism. J. Virol.76:4507- 4519.
26. Goodrum FD, Ornelles DA. 1998. p53 status does not determine outcome of E1B 55-kilodalton mutant adenovirus lytic infection. J. Virol. 72:9479 -9490.
27. Graham FL, Prevec L. 1991. Manipulation of adenovirus vectors. Methods Mol. Biol. 7:109 -128.
28. Graham FL, Smiley J, Russell WC, Nairn R. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59 -72.
29. Greber UF, et al. 1997. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16:5998-6007.
30. Greber UF, Willetts M, Webster P, Helenius A. 1993. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75:477- 486.
31. Grosshans BL, Ortiz D, Novick P. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. U. S. A.103:11821-11827.
32. Harada JN, Berk AJ. 1999. p53-Independent and -dependent requirements for E1B-55K in adenovirus type 5 replication. J. Virol. 73:5333-5344.
33. Harlow E, Franza B, Jr, Schley C. 1985. Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J. Virol. 55:533-546.
34. Harrison TJ, Graham F, Williams JF. 1977. Host range mutants of adenovirus type 5 defective for growth on HeLa cells. Virology 77:319- 329.
35. Haruki H, Gyurcsik B, Okuwaki M, Nagata K. 2003. Ternary complex formation between DNA-adenovirus core protein VII and TAF-Ibeta/SET, an acidic molecular chaperone. FEBS Lett. 555:521-527.
36. Hay RT, Freeman A, Leith I, Monaghan A, Webster A. 1995. Molecular interactions during adenovirus DNA replication. Curr. Top. Microbiol. Immunol. 199(Pt 2):31-48.
37. He TC, et al. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. U. S. A. 95:2509-2514.
38. Henaff D, Salinas S, Kremer EJ. 2011. An adenovirus traffic update: from receptor engagement to the nuclear pore. Future Microbiol. 6:179-192.
39. Hindley CE, Lawrence FJ, Matthews DA. 2007. A role for transportin in the nuclear import of adenovirus core proteins and DNA. Traffic 8:1313-1322.
40. Imelli N, Ruzsics Z, Puntener D, Gastaldelli M, Greber UF. 2009. Genetic reconstitution of the human adenovirus type 2 temperaturesensitive 1 mutant defective in endosomal escape. Virol. J. 6:174.
41. Jakubczak JL, et al. 2001. Adenovirus type 5 viral particles pseudotyped with mutagenized fiber proteins show diminished infectivity of coxsackie B-adenovirus receptor-bearing cells. J. Virol. 75:2972-2981.
42. Johnson JS, et al. 2004. Adenovirus protein VII condenses DNA, represses transcription, and associates with transcriptional activator E1A. J. Virol. 78:6459-6468.
43. Kato SE, Huang W, Flint SJ. 2011. Role of the RNA recognition motif of the E1B 55kDa protein in the adenovirus type 5 infectious cycle. Virology 417:9-17.
44. Kelkar SA, Pfister KK, Crystal RG, Leopold PL. 2004. Cytoplasmic dynein mediates adenovirus binding to microtubules. J. Virol. 78:10122-10132.
45. Kirby I, et al. 2000. Identification of contact residues and definition of the CAR-binding site of adenovirus type 5 fiber protein. J. Virol. 74: 2804-2813.
46. Lassam NJ, Bayley ST, Graham FL. 1979. Tumor antigens of human Ad5 in transformed cells and in cells infected with transformation defective host range mutants. Cell 18:781-791.
47. Leissner P, et al. 2001. Influence of adenoviral fiber mutations on viral encapsidation, infectivity and in vivo tropism. Gene Ther. 8:49-57.
48. Lenk R, Penman S. 1979. The cytoskeletal framework and poliovirus metabolism. Cell 16:289 301.
49. Leopold PL, et al. 2000. Dynein-and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Hum. Gene Ther. 11:151-165.
50. Li E, et al. 2001. Integrin alpha(v)beta1 is an adenovirus coreceptor. J. Virol. 75:5405-5409.
51. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
52. Liu H, Naismith JH, Hay RT. 2003. Adenovirus DNA replication. Curr. Top. Microbiol. Immunol. 272:131-164.
53. Lunt R, Vayda ME, Young M, Flint SJ. 1988. Isolation and characterization of monoclonal antibodies against the adenovirus core proteins. Virology 164:275-279.
54. Mabit H, et al. 2002. Intact microtubules support adenovirus and herpes simplex virus infections. J. Virol. 76:9962-9971.
55. Magnusson MK, Hong SS, Boulanger P, Lindholm L. 2001. Genetic retargeting of adenovirus: novel strategy employing "deknobbing" of the fiber. J. Virol. 75:7280-7289.
56. Maier O, Galan DL, Wodrich H, Wiethoff CM. 2010. An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature. Virology 402:11-19.
57. Martin-Fernandez M, et al. 2004. Adenovirus type-5 entry and disassembly followed in living cells by FRET, fluorescence anisotropy, and FLIM. Biophys. J. 87:1316-1327.
58. Miller DL, Rickards B, Mashiba M, Huang W, Flint SJ. 2009. The adenoviral E1B 55-kilodalton protein controls expression of immune response genes but not p53-dependent transcription. J. Virol. 83:3591-3603.
59. Moyer CL, Nemerow GR. 2012. Disulfide-bond formation by a single cysteine mutation in adenovirus protein VI impairs capsid release and membrane lysis. Virology 428:41-47.
60. Moyer CL, Wiethoff CM, Maier O, Smith JG, Nemerow GR. 2011. Functional genetic and biophysical analyses of membrane disruption by human adenovirus. J. Virol. 85:2631-2641.
61. Murti KG, Davis DS, Kitchingman GR. 1990. Localization of adenovirus- encoded DNA replication proteins in the nucleus by immunogold electron microscopy. J. Gen. Virol. 71(Pt 12):2847-2857.
62. Nakano MY, Greber UF. 2000. Quantitative microscopy of fluorescent adenovirus entry. J. Struct. Biol. 129:57-68.
63. O'Shea C, et al. 2004. Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell 6:611-623.
64. Pérez-Berná AJ, et al. 2009. Structure and uncoating of immature adenovirus. J. Mol. Biol. 392:547-557.
65. Puntener D, et al. 2011. Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J. Virol. 85:481-496.
66. Puvion-Dutilleul F, Puvion E, Icard-Liepkalns C, Macieira-Coelho A. 1984. Chromatin structure, DNA synthesis and transcription through the lifespan of human embryonic lung fibroblasts. Exp. Cell Res. 151: 283-298.
67. Rancourt C, Keyvani-Amineh H, Sircar S, Labrecque P, Weber JM. 1995. Proline 137 is critical for adenovirus protease encapsidation and activation but not enzyme activity. Virology 209:167-173.
68. Reich NC, Sarnow P, Duprey E, Levine AJ. 1983. Monoclonal antibodies which recognise native and denatured forms of the adenovirus DNAbinding protein. Virology 128:480-484.
69. Robinson JT, et al. 2011. Integrative genomics viewer. Nat. Biotechnol. 29:24-26.
70. Roelvink PW, Mi Lee G, Einfeld DA, Kovesdi I, Wickham TJ. 1999. Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286:1568-1571.
71. Rothmann T, Hengstermann A, Whitaker NJ, Scheffner M, zur Hausen H. 1998. Replication of ONYX-015, a potential anticancer adenovirus,is independent of p53 status in tumor cells. J. Virol.72:9470-9478.
72. San Martín C. 2012. Latest insights on adenovirus structure and assembly.Viruses 4:847-877.
73. Schaack J, Ho WJ-W, Frimuth P, Shenk T. 1990. Adenovirus terminal protein mediates both nuclear matrix attachment and efficient transcription of adenovirus DNA. Genes Dev. 4:1197-1208.
74. Seki T, et al. 2002. Artificial extension of the adenovirus fiber shaft inhibits infectivity in coxsackievirus and adenovirus receptor-positive cell lines. J. Virol. 76:1100 -1108.
75. Shayakhmetov DM, Lieber A. 2000. Dependence of adenovirus infectivity on length of the fiber shaft domain. J. Virol. 74:10274 -10286.
76. Silvestry M, et al. 2009. Cryo-electron microscopy structure of adenovirus type 2 temperature-sensitive mutant 1 reveals insight into the cell entry defect. J. Virol. 83:7375-7383.
77. Smart JE, Stillman BW. 1982. Adenovirus terminal protein precursor. Partial amino acid sequence and the site of covalent linkage to virus DNA. J. Biol. Chem. 257:13499 -13506.
78. Smith JG, Cassany A, Gerace L, Ralston R, Nemerow GR. 2008.Neutralizing antibody blocks adenovirus infection by arresting microtubule-dependent cytoplasmic transport. J. Virol. 82:6492- 6500.
79. Smith JG, Nemerow GR. 2008. Mechanism of adenovirus neutralization by human alpha-defensins. Cell Host Microbe 3:11-19.
80. Smith JG, Wiethoff CM, Stewart PL, Nemerow GR. 2010. Adenovirus. Curr. Top. Microbiol. Immunol. 343:195-224.
81. Somsel Rodman J, Wandinger-Ness A. 2000. Rab GTPases coordinate endocytosis. J. Cell Sci. 113(Pt. 2):183-192.
82. Stenmark H, Olkkonen VM. 2001. The Rab GTPase family. Genome Biol. 2:REVIEWS3007.
83. Stetson DB, Ko JS, Heidmann T, Medzhitov R. 2008. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134:587-598.
84. Stewart PL, et al. 1997. Cryo-EM visualization of an exposed RGD epitope on adenovirus that escapes antibody neutralization. EMBO J.16:1189 -1198.
85. Strunze S, et al. 2011. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10:210 -223.
86. Sugarman BJ, Hutchins BM, McAllister DL, Lu F, Thomas KB. 2003.The complete nucleic acid sequence of the adenovirus type 5 reference material (ARM) genome. Bioprocessing J. 2:27-32.
87. Sugawara K, Gilead Z, Wold WSM, Green M. 1977. Immunofluorescence study of the adenovirus type 2 single-stranded DNA binding protein in infected and transformed cells. J. Virol. 22:527-539.
88. Suomalainen M, et al. 1999. Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144:657-672.
89. Tomko RP, Xu R, Philipson L. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses.Proc. Natl. Acad. Sci. U. S. A. 94:3352-3356.
90. Trotman LC, Mosberger N, Fornerod M, Stidwill RP, Greber UF.2001. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3:1092-1100.
91. Turnell AS, Grand RJ, Gallimore PH. 1999. The replicative capacities of large E1B-null group A and group C adenoviruses are independent of host cell p53 status. J. Virol. 73:2074 -2083.
92. Ugai H, Borovjagin AV, Le LP, Wang M, Curiel DT. 2007. Thermostability/infectivity defect caused by deletion of the core proteinVgene in human adenovirus type 5 is rescued by thermo-selectable mutations in the core protein X precursor. J. Mol. Biol. 366:1142-1160.
93. van Raaij MJ, Louis N, Chroboczek J, Cusack S. 1999. Structure of the human adenovirus serotype 2 fiber head domain at 1.5 A resolution.Virology 262:333-343.
94. Vilaysane A, Muruve DA. 2009. The innate immune response to DNA.Semin. Immunol. 21:208 -214.
95. Voelkerding K, Klessig DF. 1986. Identification of two nuclear subclasses of the adenovirus type 5-encoded DNA-binding protein. J. Virol.60:353-362.
96. Von Seggern DJ, Chiu CY, Fleck SK, Stewart PL, Nemerow GR. 1999.A helper-independent adenovirus vector with E1, E3, and fiber deleted:structure and infectivity of fiberless particles. J. Virol. 73:1601-1608.
97. Weber J. 1976. Genetic analysis of adenovirus type 2 III. Temperature sensitivity of processing of viral proteins. J. Virol. 17:462- 471.
98. Webster A, Leith IR, Hay RT. 1994. Activation of adenovirus-coded protease and processing of preterminal protein. J. Virol. 68:7292-7300.
99. Webster A, Leith .IR, Hay RT. 1997. Domain organization of the adenovirus preterminal protein. J. Virol. 71:539-547.
100. Webster A, Leith IR, Nicholson J, Hounsell J, Hay RT. 1997. Role of preterminal protein processing in adenovirus replication. J. Virol. 71:6381-6389.
101. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. 1993. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73:309 -319.
102. Wiethoff CM, Wodrich H, Gerace L, Nemerow GR. 2005. Adenovirus protein VI mediates membrane disruption following capsid disassembly.J. Virol. 79:1992-2000.
103. Williams J, et al. 1986. The adenovirus E1B 495R protein plays a role in regulating the transport and stability of the viral late messages. Cancer Cells. 4:275-284.
104. Williams JF. 1970. Enhancement of adenovirus plaque formation on HeLa cells by magnesium chloride. J. Gen. Virol. 9:251-253.
105. Wodrich H, et al. 2010. A capsid-encoded PPxY-motif facilitates adenovirus entry. PLoS Pathog. 6:e1000808. doi:10.1371/journal.ppat.1000808.
106. Wold WSM, Horwitz MS. 2007. Adenoviruses, p 2395-2436. In Knipe DM, Howley PM (ed), Fields virology, 5 ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
107. Xue Y, Johnson JS, Ornelles DA, Lieberman J, Engel DA. 2005.Adenovirus protein VII functions throughout early phase and interacts with cellular proteins SET and pp32. J. Virol. 79:2474 -2483.
108. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. 2010. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol.11:1005-1013.
109. Yang U-C, Huang W, Flint SJ. 1996. mRNA export correlates with activation of transcription in human subgroup C adenovirus-infected cells. J. Virol. 70:4071- 4080.
110. Yang YG, Lindahl T, Barnes DE. 2007. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease.Cell 131:873- 886.