1887

Abstract

Promyelocytic leukemia (PML) proteins have been implicated in antiviral responses but PML and associated proteins are also suggested to support virus replication. One isoform, PML-II, is required for efficient transcription of interferon and interferon-responsive genes. We therefore investigated the PML-II contribution to human adenovirus 5 (Ad5) infection, using shRNA-mediated knockdown. HelaΔII cells showed a 2–3-fold elevation in Ad5 yield, reflecting an increase in late gene expression. This increase was found to be due in part to the reduced innate immune response consequent upon PML-II depletion. However, the effect was minor because the viral E4 Orf3 protein targets and inactivates this PML-II function. The major benefit to Ad5 in HelaΔII cells was exerted via an increase in HSP70; depletion of HSP70 completely reversed this replicative advantage. Increased Ad5 late gene expression was not due either to the previously described inhibition of inflammatory responses by HSP70 or to effects of HSP70 on major late promoter or L4 promoter activity, but might be linked to an observed increase in E1B 55K, as this protein is known to be required for efficient late gene expression. The induction of HSP70 by PML-II removal was specific for the HSPA1B gene among the HSP70 gene family and thus was not the consequence of a general stress response. Taken together, these data show that PML-II, through its various actions, has an overall negative effect on the Ad5 lifecycle.

Keyword(s): adenovirus, , HSP70 and PML protein,
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2016-08-01
2019-10-20
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References

  1. Ackrill A. M. , Foster G. R. , Laxton C. D. , Flavell D. M. , Stark G. R. , Kerr I. M. . ( 1991;). Inhibition of the cellular response to interferons by products of the adenovirus type 5 E1A oncogene. . Nucleic Acids Res 19: 4387–4393. [CrossRef] [PubMed]
    [Google Scholar]
  2. Agoff S. N. , Hou J. , Linzer D. , Wu B. . ( 1993;). Regulation of the human hsp70 promoter by p53. . Science 259: 84–87. [CrossRef] [PubMed]
    [Google Scholar]
  3. Au W. C. , Moore P. A. , Lowther W. , Juang Y. T. , Pitha P. M. . ( 1995;). Identification of a member of the interferon regulatory factor family that binds to the interferon-stimulated response element and activates expression of interferon-induced genes. . Proc Natl Acad Sci U S A 92: 11657–11661.[PubMed] [CrossRef]
    [Google Scholar]
  4. Bernardi R. , Pandolfi P. P. . ( 2007;). Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. . Nat Revs Mol Cell Biol 8: 1006–1016.[CrossRef]
    [Google Scholar]
  5. Berscheminski J. , Groitl P. , Dobner T. , Wimmer P. , Schreiner S. . ( 2013;). The adenoviral oncogene E1A-13S interacts with a specific isoform of the tumor suppressor PML to enhance viral transcription. . J Virol 87: 965–977. [CrossRef] [PubMed]
    [Google Scholar]
  6. Berscheminski J. , Wimmer P. , Brun J. , Ip W. H. , Groitl P. , Horlacher T. , Jaffray E. , Hay R. T. , Dobner T. , Schreiner S. . ( 2014;). Sp100 isoform-specific regulation of human adenovirus 5 gene expression. . J Virol 88: 6076–6092. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bringhurst R. M. , Schaffer P. A. . ( 2006;). Cellular stress rather than stage of the cell cycle enhances the replication and plating efficiencies of herpes simplex virus type 1 ICP0 viruses. . J Virol 80: 4528–4537. [CrossRef] [PubMed]
    [Google Scholar]
  8. Brocchieri L. , Conway de Macario E. , Macario A. J. L. . ( 2008;). Hsp70 genes in the human genome: Conservation and differentiation patterns predict a wide array of overlapping and specialized functions. . BMC Evol Biol 8: 19. [CrossRef] [PubMed]
    [Google Scholar]
  9. Burgert H. G. , Ruzsics Z. , Obermeier S. , Hilgendorf A. , Windheim M. , Elsing A. . ( 2002;). Subversion of host defense mechanisms by adenoviruses. . Curr Top Microbiol Immunol 269: 273–318.[PubMed]
    [Google Scholar]
  10. Carvalho T. , Seeler J. S. , Ohman K. , Jordan P. , Pettersson U. , Akusjärvi G. , Carmo-Fonseca M. , Dejean A. . ( 1995;). Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. . J Cell Biol 131: 45–56.[PubMed] [CrossRef]
    [Google Scholar]
  11. Cepko C. L. , Whetstone C. A. , Sharp P. A. . ( 1983;). Adenovirus hexon monoclonal antibody that is group specific and potentially useful as a diagnostic reagent. . J Clin Microbiol 17: 360–364.[PubMed]
    [Google Scholar]
  12. Chahal J. S. , Qi J. , Flint S. J. . ( 2012;). The human adenovirus type 5 E1B 55 kDa protein obstructs inhibition of viral replication by type I interferon in normal human cells. . PLoS Pathogens 8: e1002853. [CrossRef]
    [Google Scholar]
  13. Chee A. V. , Lopez P. , Pandolfi P. P. , Roizman B. . ( 2003;). Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. . J Virol 77: 7101–7105.[PubMed] [CrossRef]
    [Google Scholar]
  14. Chelbi-Alix M. K. , Pelicano L. , Quignon F. , Koken M. H. , Venturini L. , Stadler M. , Pavlovic J. , Degos L. , de Thé H. . ( 1995;). Induction of the PML protein by interferons in normal and APL cells. . Leukemia 9: 2027–2033.[PubMed]
    [Google Scholar]
  15. Chen Y. , Wright J. , Meng X. , Leppard K. N. . ( 2015;). Promyelocytic leukemia protein isoform II promotes transcription factor recruitment to activate interferon beta and interferon-responsive gene expression. . Mol Cell Biol 35: 1660–1672. [CrossRef] [PubMed]
    [Google Scholar]
  16. Clerico E. M. , Tilitsky J. M. , Meng W. , Gierasch L. M. . ( 2015;). How Hsp70 molecular machines interact with their substrates to mediate diverse physiological functions. . J Mol Biol 427: 1575–1588. [CrossRef] [PubMed]
    [Google Scholar]
  17. Colombo R. , Boggio R. , Seiser C. , Draetta G. F. , Chiocca S. . ( 2002;). The adenovirus protein Gam1 interferes with sumoylation of histone deacetylase 1. . EMBO Rep 3: 1062–1068. [CrossRef] [PubMed]
    [Google Scholar]
  18. Cuchet D. , Sykes A. , Nicolas A. , Orr A. , Murray J. , Sirma H. , Heeren J. , Bartelt A. , Everett R. D. . ( 2011;). PML isoforms I and II participate in PML-dependent restriction of HSV-1 replication. . J Cell Sci 124: 280–291. [CrossRef] [PubMed]
    [Google Scholar]
  19. Doucas V. , Ishov A. M. , Romo A. , Juguilon H. , Weitzman M. D. , Evans R. M. , Maul G. G. . ( 1996;). Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. . Genes Dev 10: 196–207. [CrossRef] [PubMed]
    [Google Scholar]
  20. Evans J. D. , Hearing P. . ( 2005;). Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. . J Virol 79: 6207–6215. [CrossRef] [PubMed]
    [Google Scholar]
  21. Everett R. D. , Murray J. . ( 2005;). ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. . J Virol 79: 5078–5089. [CrossRef] [PubMed]
    [Google Scholar]
  22. Everett R. D. , Parada C. , Gripon P. , Sirma H. , Orr A. . ( 2008a;). Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. . J Virol 82: 2661–2672.[CrossRef]
    [Google Scholar]
  23. Everett R. D. , Young D. F. , Randall R. E. , Orr A. . ( 2008b;). Stat-1- and IRF-3-dependent pathways are not essential for repression of ICP0-null mutant herpes simplex virus type 1 in human fibroblasts. . J Virol 82: 8871–8881.[CrossRef]
    [Google Scholar]
  24. Farley D. C. , Brown J. L. , Leppard K. N. . ( 2004;). Activation of the early-late switch in adenovirus type 5 major late transcription unit expression by L4 gene products. . J Virol 78: 1782–1791.[PubMed] [CrossRef]
    [Google Scholar]
  25. Geoffroy M. C. , Chelbi-Alix M. K. . ( 2011;). Role of promyelocytic leukemia protein in host antiviral defense. . J Interferon Cytokine Res 31: 145–158. [CrossRef] [PubMed]
    [Google Scholar]
  26. Glotzer J. B. , Saltik M. , Chiocca S. , Michou A. I. , Moseley P. , Cotten M. . ( 2000;). Activation of heat-shock response by an adenovirus is essential for virus replication. . Nature 407: 207–211. [CrossRef] [PubMed]
    [Google Scholar]
  27. Gooding L. R. , Elmore L. W. , Tollefson A. E. , Brady H. A. , Wold W. S. . ( 1988;). A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor. . Cell 53: 341–346. [CrossRef] [PubMed]
    [Google Scholar]
  28. Halford W. P. , Weisend C. , Grace J. , Soboleski M. , Carr D. J. , Balliet J. W. , Imai Y. , Margolis T. P. , Gebhardt B. M. . ( 2006;). ICP0 antagonizes Stat 1-dependent repression of herpes simplex virus: implications for the regulation of viral latency. . Virol J 3: 44. [CrossRef] [PubMed]
    [Google Scholar]
  29. Hartman Z. C. , Black E. P. , Amalfitano A. . ( 2007;). Adenoviral infection induces a multi-faceted innate cellular immune response that is mediated by the toll-like receptor pathway in A549 cells. . Virology 358: 357–372. [CrossRef] [PubMed]
    [Google Scholar]
  30. Hendrickx R. , Stichling N. , Koelen J. , Kuryk L. , Lipiec A. , Greber U. F. . ( 2014;). Innate immunity to adenovirus. . Hum Gene Ther 25: 265–284. [CrossRef] [PubMed]
    [Google Scholar]
  31. Higginbotham J. N. , Seth P. , Blaese R. M. , Ramsey W. J. . ( 2002;). The release of inflammatory cytokines from human peripheral blood mononuclear cells in vitro following exposure to adenovirus variants and capsid. . Hum Gene Ther 13: 129–141. [CrossRef] [PubMed]
    [Google Scholar]
  32. Hoppe A. , Beech S. J. , Dimmock J. , Leppard K. N. . ( 2006;). Interaction of the adenovirus type 5 E4 Orf3 protein with promyelocytic leukemia protein isoform II is required for ND10 disruption. . J Virol 80: 3042–3049. [CrossRef] [PubMed]
    [Google Scholar]
  33. Huang M.-M. , Hearing P. . ( 1989;). Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. . J Virol 63: 2605–2615.[PubMed]
    [Google Scholar]
  34. Imperiale M. J. , Kao H. T. , Feldman L. T. , Nevins J. R. , Strickland S. . ( 1984;). Common control of the heat shock gene and early adenovirus genes: evidence for a cellular E1A-like activity. . Mol Cell Biol 4: 867–874. [PubMed] [CrossRef]
    [Google Scholar]
  35. Ishov A. M. , Maul G. G. . ( 1996;). The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. . J Cell Biol 134: 815–826.[PubMed] [CrossRef]
    [Google Scholar]
  36. Jensen K. , Shiels C. , Freemont P. S. . ( 2001;). PML protein isoforms and the RBCC/TRIM motif. . Oncogene 20: 7223–7233. [CrossRef] [PubMed]
    [Google Scholar]
  37. Kim Y.-E. , Ahn J.-H. . ( 2015;). Positive role of promyelocytic leukemia protein in type I interferon response and its regulation by human cytomegalovirus. . PLoS Pathog 11: e1004785. [CrossRef] [PubMed]
    [Google Scholar]
  38. King P. , Goodbourn S. . ( 1994;). The beta-interferon promoter responds to priming through multiple independent regulatory elements. . J Biol Chem 269: 30609–30615.[PubMed]
    [Google Scholar]
  39. Kitajewski J. , Schneider R. J. , Safer B. , Munemitsu S. M. , Samuel C. E. , Thimmappaya B. , Shenk T. . ( 1986;). Adenovirus VAI RNA antagonizes the antiviral action of interferon by preventing activation of the interferon-induced eIF-2 alpha kinase. . Cell 45: 195–200. [CrossRef] [PubMed]
    [Google Scholar]
  40. Kumar P. P. , Bischof O. , Purbey P. K. , Notani D. , Urlaub H. , Dejean A. , Galande S. . ( 2007;). Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. . Nat Cell Biol 9: 45–56. [CrossRef] [PubMed]
    [Google Scholar]
  41. Leib D. A. , Harrison T. E. , Laslo K. M. , Machalek M. A. , Moorman N. J. , Virgin H. W. . ( 1999;). Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. . J Exp Med 189: 663–672.[PubMed] [CrossRef]
    [Google Scholar]
  42. Leppard K. N. , Dimmock J. . ( 2006;). Virus interactions with PML nuclear bodies. . In Viruses and the Nucleus , pp. 213–245. Edited by Hiscox J. , Wiley J. .
    [Google Scholar]
  43. Leppard K. N. , Everett R. D. . ( 1999;). The adenovirus type 5 E1b 55K and E4 Orf3 proteins associate in infected cells and affect ND10 components. . J Gen Virol 80: 997–1008. [CrossRef] [PubMed]
    [Google Scholar]
  44. Leppard K. N. , Wright J. . ( 2012;). Targeting of promyelocytic leukaemia proteins and promyelocytic leukaemia nuclear bodies by DNA tumour viruses. . In Small DNA Tumour Viruses , pp. 255–280. Edited by Gaston K. . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  45. Leppard K. N. . ( 1998;). Regulated RNA processing and RNA transport during adenovirus infection. . Semin Virol 8: 301–307.[CrossRef]
    [Google Scholar]
  46. Leppard K. N. , Emmott E. , Cortese M. S. , Rich T. . ( 2009;). Adenovirus type 5 E4 Orf3 protein targets promyelocytic leukaemia (PML) protein nuclear domains for disruption via a sequence in PML isoform II that is predicted as a protein interaction site by bioinformatic analysis. . J Gen Virol 90: 95–104. [CrossRef] [PubMed]
    [Google Scholar]
  47. Lethbridge K. J. , Scott G. E. , Leppard K. N. . ( 2003;). Nuclear matrix localization and SUMO-1 modification of adenovirus type 5 E1b 55K protein are controlled by E4 Orf6 protein. . J Gen Virol 84: 259–268. [CrossRef] [PubMed]
    [Google Scholar]
  48. Lum L. S. , Hsu S. , Vaewhongs M. , Wu B. . ( 1992;). The hsp70 gene CCAAT-binding factor mediates transcriptional activation by the adenovirus E1a protein. . Mol Cell Biol 12: 2599–2605.[PubMed] [CrossRef]
    [Google Scholar]
  49. Macejak D. G. , Luftig R. B. . ( 1991;). Association of HSP70 with the adenovirus type 5 fiber protein in infected HEp-2 cells. . Virology 180: 120–125. [CrossRef] [PubMed]
    [Google Scholar]
  50. Madara J. , Krewet J. A. , Shah M. . ( 2005;). Heat shock protein 72 expression allows permissive replication of oncolytic adenovirus dl1520 (ONYX-015) in rat glioblastoma cells. . Mol Cancer 4: 12. [CrossRef] [PubMed]
    [Google Scholar]
  51. Maul G. G. , Everett R. D. . ( 1994;). The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. . J Gen Virol 75: 1223–1233. [CrossRef] [PubMed]
    [Google Scholar]
  52. McFadden G. , Mohamed M. R. , Rahman M. M. , Bartee E. . ( 2009;). Cytokine determinants of viral tropism. . Nat Revs Immunol 9: 645–655. [CrossRef]
    [Google Scholar]
  53. Meng X. Z. , Harken A. H. . ( 2002;). The interaction between Hsp70 and TNF-alpha expression: a novel mechanism for protection of the myocardium against post-injury depression. . Shock 17: 345–353. [CrossRef] [PubMed]
    [Google Scholar]
  54. Mitchell A. M. , Hirsch M. L. , Li C. , Samulski R. J. . ( 2014;). Promyelocytic leukemia protein is a cell-intrinsic factor inhibiting parvovirus DNA replication. . J Virol 88: 925–936. [CrossRef] [PubMed]
    [Google Scholar]
  55. Moffat J. , Grueneberg D. A. , Yang X. , Kim S. Y. , Kloepfer A. M. , Hinkle G. , Piqani B. , Eisenhaure T. M. , Luo B. et al. ( 2006;). A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. . Cell 124: 1283–1298. [CrossRef] [PubMed]
    [Google Scholar]
  56. Moore M. , Schaack J. , Baim S. B. , Morimoto R. I. , Shenk T. . ( 1987;). Induced heat shock mRNAs escape the nucleocytoplasmic transport block in adenovirus-infected HeLa cells. . Mol Cell Biol 7: 4505–4512.[PubMed] [CrossRef]
    [Google Scholar]
  57. Morris S. J. , Leppard K. N. . ( 2009;). Adenovirus serotype 5 L4-22K and L4-33K proteins have distinct functions in regulating late gene expression. . J Virol 83: 3049–3058. [CrossRef] [PubMed]
    [Google Scholar]
  58. Morris S. J. , Scott G. E. , Leppard K. N. . ( 2010;). Adenovirus late-phase infection is controlled by a novel L4 promoter. . J Virol 84: 7096–7104. [CrossRef] [PubMed]
    [Google Scholar]
  59. Nevins J. R. . ( 1982;). Induction of the synthesis of a 70,000 dalton mammalian heat shock protein by the adenovirus E1A gene product. . Cell 29: 913–919. [CrossRef] [PubMed]
    [Google Scholar]
  60. Niewiarowska J. , D'Halluin J. C. , Belin M.-T. . ( 1992;). Adenovirus capsid proteins interact with HSP70 proteins after penetration in human or rodent cells. . Exp Cell Res 201: 408–416. [CrossRef] [PubMed]
    [Google Scholar]
  61. Ou H. D. , Kwiatkowski W. , Deerinck T. J. , Noske A. , Blain K. Y. , Land H. S. , Soria C. , Powers C. J. , May A. P . ( 2012;). A structural basis for the assembly and functions of a viral polymer that inactivates multiple tumor suppressors. . Cell 151: 304–319. [CrossRef] [PubMed]
    [Google Scholar]
  62. Pahl H. L. , Sester M. , Burgert H. G. , Baeuerle P. A. . ( 1996;). Activation of transcription factor NF-kappaB by the adenovirus E3/19K protein requires its ER retention. . J Cell Biol 132: 511–522.[PubMed] [CrossRef]
    [Google Scholar]
  63. Patsalo V. , Yondola M. A. , Luan B. , Shoshani I. , Kisker C. , Green D. F. , Raleigh D. P. , Hearing P. . ( 2012;). Biophysical and functional analyses suggest that adenovirus E4-ORF3 protein requires higher-order multimerization to function against promyelocytic leukemia protein nuclear bodies. . J Biol Chem 287: 22573–22583. [CrossRef] [PubMed]
    [Google Scholar]
  64. Phillips B. , Abravaya K. , Morimoto R. I. . ( 1991;). Analysis of the specificity and mechanism of transcriptional activation of the human hsp70 gene during infection by DNA viruses. . J Virol 65: 5680–5692.[PubMed]
    [Google Scholar]
  65. Reich N. C. , Sarnow P. , Duprey E. , Levine A. J. . ( 1983;). Monoclonal antibodies which recognize native and denatured forms of the adenovirus DNA-binding protein. . Virology 128: 480–484. [CrossRef] [PubMed]
    [Google Scholar]
  66. Reich N. , Pine R. , Levy D. , Darnell J. E. . ( 1988;). Transcription of interferon-stimulated genes is induced by adenovirus particles but is suppressed by E1A gene products. . J Virol 62: 114–119.[PubMed]
    [Google Scholar]
  67. Santoro M. G. , Amici C. , Rossi A. . ( 2010;). Role of heat shock proteins in viral infection. . In Prokaryotic and Eukaryotic Heat Shock Proteins in Infectious Disease , pp. 51–84. Edited by Pockley A. G. , Calderwood S. K. , Santoro M. G. . New York:: Springer;.[CrossRef]
    [Google Scholar]
  68. Saphire A. C. , Guan T. , Schirmer E. C. , Nemerow G. R. , Gerace L. . ( 2000;). Nuclear import of adenovirus DNA in vitro involves the nuclear protein import pathway and hsc70. . J Biol Chem 275:.[PubMed] [CrossRef]
    [Google Scholar]
  69. Sarnow P. , Sullivan C. A. , Levine A. J. . ( 1982;). A monoclonal antibody detecting the adenovirus type 5-E1b-58Kd tumor antigen: characterization of the E1b-58Kd tumor antigen in adenovirus-infected and -transformed cells. . Virology 120: 510–517. [CrossRef] [PubMed]
    [Google Scholar]
  70. Schmitz M. L. , Indorf A. , Limbourg F. P. , Städtler H. , Traenckner E. B. , Baeuerle P. A. . ( 1996;). The dual effect of adenovirus type 5 E1A 13S protein on NF-kappaB activation is antagonized by E1B 19K. . Mol Cell Biol 16: 4052–4063.[PubMed] [CrossRef]
    [Google Scholar]
  71. Schreiner S. , Bürck C. , Glass M. , Groitl P. , Wimmer P. , Kinkley S. , Mund A. , Everett R. D. , Dobner T. . ( 2013;). Control of human adenovirus type 5 gene expression by cellular Daxx/ATRX chromatin-associated complexes. . Nucleic Acids Res 41: 3532–3550. [CrossRef] [PubMed]
    [Google Scholar]
  72. Simon M. C. , Fisch T. M. , Benecke B. J. , Nevins J. R. , Heintz N. . ( 1988;). Definition of multiple, functionally distinct TATA elements, one of which is a target in the hsp70 promoter for E1A regulation. . Cell 52: 723–729. [CrossRef] [PubMed]
    [Google Scholar]
  73. Singh I. S. , Shah N. G. , Almutairy E. , Hasday J. D. . ( 2010;). Role of HSF1 in infectious disease. . In Prokaryotic and Eukaryotic Heat Shock Proteins in Infectious Disease , pp. 1–31. Edited by Pockley A. G. , Calderwood S. K. , Santoro M. G. . New York:: Springer;.
    [Google Scholar]
  74. Sohn S. Y. , Hearing P. . ( 2011;). Adenovirus sequesters phosphorylated STAT1 at viral replication centers and inhibits STAT dephosphorylation. . J Virol 85: 7555–7562. [CrossRef] [PubMed]
    [Google Scholar]
  75. Stadler M. , Chelbi-Alix M. K. , Koken M. H. , Venturini L. , Lee C. , Saïb A. , Quignon F. , Pelicano L. , Guillemin M. C. , Schindler C. . ( 1995;). Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element. . Oncogene 11: 2565–2573.[PubMed]
    [Google Scholar]
  76. Tanaka K. , Namba T. , Arai Y. , Fujimoto M. , Adachi H. , Sobue G. , Takeuchi K. , Nakai A. , Mizushima T. . ( 2007;). Genetic evidence for a protective role for heat shock factor 1 and heat shock protein 70 against colitis. . J Biol Chem 282: 23240–23252. [CrossRef] [PubMed]
    [Google Scholar]
  77. Tobe M. , Isobe Y. , Tomizawa H. , Nagasaki T. , Takahashi H. , Hayashi H. . ( 2003;). A novel structural class of potent inhibitors of NF-kappa B activation: structure-activity relationships and biological effects of 6-aminoquinazoline derivatives. . Bioorg Med Chem 11: 3869–3878. [CrossRef] [PubMed]
    [Google Scholar]
  78. Ullman A. J. , Hearing P. . ( 2008;). Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. . J Virol 82: 7325–7335. [CrossRef] [PubMed]
    [Google Scholar]
  79. Ullman A. J. , Reich N. C. , Hearing P. . ( 2007;). Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. . J Virol 81: 4744–4752. [CrossRef] [PubMed]
    [Google Scholar]
  80. Van Damme E. , Laukens K. , Dang T. H. , Van Ostade X. . ( 2010;). A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. . Int J Biol Sci 6: 51–67.[PubMed] [CrossRef]
    [Google Scholar]
  81. Weidtkamp-Peters S. , Lenser T. , Negorev D. , Gerstner N. , Hofmann T. G. , Schwanitz G. , Hoischen C. , Maul G. , Dittrich P. , Hemmerich P. . ( 2008;). Dynamics of component exchange at PML nuclear bodies. . J Cell Sci 121: 2731–2743. [CrossRef] [PubMed]
    [Google Scholar]
  82. White E. , Spector D. , Welch W. . ( 1988;). Differential distribution of the adenovirus E1A proteins and colocalization of E1A with the 70-kilodalton cellular heat shock protein in infected cells. . J Virol 62: 4153–4166.[PubMed]
    [Google Scholar]
  83. Wright J. , Atwan Z. , Morris S. J. , Leppard K. N. . ( 2015;). The human adenovirus type 5 L4 promoter is negatively regulated by TFII-I and L4-33K. . J Virol 89: 7053–7063. [CrossRef] [PubMed]
    [Google Scholar]
  84. Wu B. J. , Hurst H. C. , Jones N. C. , Morimoto R. I. . ( 1986;). The E1A 13S product of adenovirus 5 activates transcription of the cellular human HSP70 gene. . Mol Cell Biol 6: 2994–2999.[PubMed] [CrossRef]
    [Google Scholar]
  85. Xu Z. X. , Zou W. X. , Lin P. , Chang K. S. . ( 2005;). A role for PML3 in centrosome duplication and genome stability. . Mol Cell 17: 721–732. [CrossRef] [PubMed]
    [Google Scholar]
  86. Zhao H. X. , Granberg F. , Elfineh L. , Pettersson U. , Svensson C. . ( 2003;). Strategic attack on host cell gene expression during adenovirus infection. . J Virol 77: 11006–11015. [CrossRef] [PubMed]
    [Google Scholar]
  87. Zhu J. , Huang X. , Yang Y. . ( 2007;). Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. . J Virol 81: 3170–3180. [CrossRef] [PubMed]
    [Google Scholar]
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