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Abstract

Viruses are exemplary molecular biologists and have been integral to scientific discovery for generations. It is therefore no surprise that nuclear replicating viruses have evolved to systematically take over host cell function through astoundingly specific nuclear and chromatin hijacking. In this review, we focus on nuclear replicating DNA viruses—herpesviruses and adenoviruses—as key examples of viral invasion in the nucleus. We concentrate on critical features of nuclear architecture, such as chromatin and the nucleolus, to illustrate the complexity of the virus-host battle for resources in the nucleus. We conclude with a discussion of the technological advances that have enabled the discoveries we describe and upcoming steps in this burgeoning field.

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2024-09-26
2025-06-16
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Literature Cited

  1. 1.
    Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997.. Crystal structure of the nucleosome core particle at 2.8 Å resolution. . Nature 389:(6648):25160
    [Crossref] [Google Scholar]
  2. 2.
    Bannister AJ, Kouzarides T. 2011.. Regulation of chromatin by histone modifications. . Cell Res. 21:(3):38195
    [Crossref] [Google Scholar]
  3. 3.
    Wiles ET, Selker EU. 2017.. H3K27 methylation: a promiscuous repressive chromatin mark. . Curr. Opin. Genet. Dev. 43::3137
    [Crossref] [Google Scholar]
  4. 4.
    Saksouk N, Simboeck E, Déjardin J. 2015.. Constitutive heterochromatin formation and transcription in mammals. . Epigenet. Chromatin 8:(1):3
    [Crossref] [Google Scholar]
  5. 5.
    Gamble MJ, Frizzell KM, Yang C, Krishnakumar R, Kraus WL. 2010.. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. . Gene Dev. 24:(1):2132
    [Crossref] [Google Scholar]
  6. 6.
    Trojer P, Reinberg D. 2007.. Facultative heterochromatin: Is there a distinctive molecular signature?. Mol. Cell 28:(1):113
    [Crossref] [Google Scholar]
  7. 7.
    Jenuwein T, Allis CD. 2001.. Translating the histone code. . Science 293:(5532):107480
    [Crossref] [Google Scholar]
  8. 8.
    Lee J-S, Smith E, Shilatifard A. 2010.. The language of histone crosstalk. . Cell 142:(5):68285
    [Crossref] [Google Scholar]
  9. 9.
    Kadauke S, Blobel GA. 2009.. Chromatin loops in gene regulation. . Biochim. Biophys. Acta 1789:(1):1725
    [Crossref] [Google Scholar]
  10. 10.
    Grubert F, Srivas R, Spacek DV, Kasowski M, Ruiz-Velasco M, et al. 2020.. Landscape of cohesin-mediated chromatin loops in the human genome. . Nature 583:(7818):73743
    [Crossref] [Google Scholar]
  11. 11.
    Andersson R, Sandelin A. 2020.. Determinants of enhancer and promoter activities of regulatory elements. . Nat. Rev. Genet. 21:(2):7187
    [Crossref] [Google Scholar]
  12. 12.
    Giammartino DCD, Polyzos A, Apostolou E. 2020.. Transcription factors: building hubs in the 3D space. . Cell Cycle 19:(19):2395410
    [Crossref] [Google Scholar]
  13. 13.
    Beagan JA, Phillips-Cremins JE. 2020.. On the existence and functionality of topologically associating domains. . Nat. Genet. 52:(1):816
    [Crossref] [Google Scholar]
  14. 14.
    Yu M, Ren B. 2016.. The three-dimensional organization of mammalian genomes. . Annu. Rev. Cell Dev. Biol. 33::26589
    [Crossref] [Google Scholar]
  15. 15.
    Agarwal A, Korsak S, Choudhury A, Plewczynski D. 2023.. The dynamic role of cohesin in maintaining human genome architecture. . BioEssays 45:(10):e2200240
    [Crossref] [Google Scholar]
  16. 16.
    Stephens AD. 2020.. Chromatin rigidity provides mechanical and genome protection. . Mutat. Res. Fundam. Mol. Mech. Mutagen. 821::111712
    [Crossref] [Google Scholar]
  17. 17.
    Kim S, Yu N-K, Kaang B-K. 2015.. CTCF as a multifunctional protein in genome regulation and gene expression. . Exp. Mol. Med. 47:(6):e166
    [Crossref] [Google Scholar]
  18. 18.
    Nasmyth K, Haering CH. 2009.. Cohesin: its roles and mechanisms. . Genetics 43:(1):52558
    [Crossref] [Google Scholar]
  19. 19.
    Dorner D, Gotzmann J, Foisner R. 2007.. Nucleoplasmic lamins and their interaction partners, LAP2α, Rb, and BAF, in transcriptional regulation. . FEBS J. 274:(6):136273
    [Crossref] [Google Scholar]
  20. 20.
    Bouzid T, Kim E, Riehl BD, Esfahani AM, Rosenbohm J, et al. 2019.. The LINC complex, mechanotransduction, and mesenchymal stem cell function and fate. . J. Biol. Eng. 13:(1):68
    [Crossref] [Google Scholar]
  21. 21.
    Torvaldson E, Kochin V, Eriksson JE. 2015.. Phosphorylation of lamins determine their structural properties and signaling functions. . Nucleus 6:(3):16671
    [Crossref] [Google Scholar]
  22. 22.
    Capell BC, Collins FS. 2006.. Human laminopathies: nuclei gone genetically awry. . Nat. Rev. Genet. 7:(12):94052
    [Crossref] [Google Scholar]
  23. 23.
    Horníková L, Bruštíková K, Huérfano S, Forstová J. 2022.. Nuclear cytoskeleton in virus infection. . Int. J. Mol. Sci. 23:(1):578
    [Crossref] [Google Scholar]
  24. 24.
    O'Sullivan JM, Pai DA, Cridge AG, Engelke DR, Ganley ARD. 2013.. The nucleolus: a raft adrift in the nuclear sea or the keystone in nuclear structure?. Biomol. Concepts 4:(3):27786
    [Crossref] [Google Scholar]
  25. 25.
    Orsolic I, Jurada D, Pullen N, Oren M, Eliopoulos AG, Volarevic S. 2016.. The relationship between the nucleolus and cancer: current evidence and emerging paradigms. . Semin. Cancer Biol. 37::3650
    [Crossref] [Google Scholar]
  26. 26.
    Parlato R, Kreiner G. 2013.. Nucleolar activity in neurodegenerative diseases: a missing piece of the puzzle?. J. Mol. Med. 91:(5):54147
    [Crossref] [Google Scholar]
  27. 27.
    Zierhut C, Funabiki H. 2015.. Nucleosome functions in spindle assembly and nuclear envelope formation. . BioEssays 37:(10):107485
    [Crossref] [Google Scholar]
  28. 28.
    Tsai RYL, Pederson T. 2014.. Connecting the nucleolus to the cell cycle and human disease. . FASEB J. 28:(8):329096
    [Crossref] [Google Scholar]
  29. 29.
    Olson MOJ. 2004.. Sensing cellular stress: another new function for the nucleolus?. Sci. STKE 2004:(224):pe10
    [Crossref] [Google Scholar]
  30. 30.
    Looker KJ, Magaret AS, May MT, Turner KME, Vickerman P, et al. 2015.. Global and regional estimates of prevalent and incident herpes simplex virus type 1 infections in 2012. . PLOS ONE 10:(10):e0140765
    [Crossref] [Google Scholar]
  31. 31.
    Knipe DM, Howley P, eds. 2013.. Fields Virology. Philadelphia:: Lippincott Williams & Wilkins
    [Google Scholar]
  32. 32.
    Knipe DM, Cliffe A. 2008.. Chromatin control of herpes simplex virus lytic and latent infection. . Nat. Rev. Microbiol. 6:(3):21121
    [Crossref] [Google Scholar]
  33. 33.
    Ayoub HH, Chemaitelly H, Abu-Raddad LJ. 2019.. Characterizing the transitioning epidemiology of herpes simplex virus type 1 in the USA: model-based predictions. . BMC Med. 17:(1):57
    [Crossref] [Google Scholar]
  34. 34.
    Kennedy PGE, Chaudhuri A. 2002.. Herpes simplex encephalitis. . J. Neurol. Neurosurg. Psychiatry 73:(3):23738
    [Crossref] [Google Scholar]
  35. 35.
    Kłysik K, Pietraszek A, Nowakowska M, Karewicz A. 2018.. Acyclovir in the treatment of herpes viruses—a review. . Curr. Med. Chem. 27:(24):411837
    [Crossref] [Google Scholar]
  36. 36.
    Sirtori C, Bosisio-Bestetti M. 1967.. Nucleolar changes in KB tumor cells infected with herpes simplex virus. . Cancer Res. 27:(2):36776
    [Google Scholar]
  37. 37.
    Love R, Wildy P. 1963.. Cytochemical studies of the nucleoproteins of HeLa cells infected with herpes virus. . J. Cell Biol. 17:(2):23754
    [Crossref] [Google Scholar]
  38. 38.
    Dupuy-Coin AM, Arnoult J, Bouteille M. 1978.. Quantitative correlation of morphological alterations of the nucleus with functional events during in vitro infection of glial cells with herpes simplex hominis (HSV 2). . J. Ultrastruct. Res. 65:(1):6072
    [Crossref] [Google Scholar]
  39. 39.
    Dienes HP, Ramadori G, Falke D, Thoenes W. 1984.. Electron microscopic observations on primary hepatocyte cultures infected with herpes simplex virus types I and II. . Virchows Arch. B 46:(1):32132
    [Crossref] [Google Scholar]
  40. 40.
    Monier K, Armas JCG, Etteldorf S, Ghazal P, Sullivan KF. 2000.. Annexation of the interchromosomal space during viral infection. . Nat. Cell Biol. 2:(9):66165
    [Crossref] [Google Scholar]
  41. 41.
    Simpson-Holley M, Baines J, Roller R, Knipe DM. 2004.. Herpes simplex virus 1 UL31 and UL34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. . J. Virol. 78:(11):5591600
    [Crossref] [Google Scholar]
  42. 42.
    Simpson-Holley M, Colgrove RC, Nalepa G, Harper JW, Knipe DM. 2005.. Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. . J. Virol. 79:(20):1284051
    [Crossref] [Google Scholar]
  43. 43.
    Evilevitch A, Hohlbauch SV. 2022.. Intranuclear HSV-1 DNA ejection induces major mechanical transformations suggesting mechanoprotection of nucleus integrity. . PNAS 119:(9):e2114121119
    [Crossref] [Google Scholar]
  44. 44.
    Lewis HC, Kelnhofer-Millevolte LE, Brinkley MR, Arbach HE, Arnold EA, et al. 2023.. HSV-1 exploits host heterochromatin for nuclear egress. . J. Cell Biol. 222:(9):e202304106
    [Crossref] [Google Scholar]
  45. 45.
    Bosse JB, Hogue IB, Feric M, Thiberge SY, Sodeik B, et al. 2015.. Remodeling nuclear architecture allows efficient transport of herpesvirus capsids by diffusion. . PNAS 112:(42):E572533
    [Crossref] [Google Scholar]
  46. 46.
    Aho V, Salminen S, Mattola S, Gupta A, Flomm F, et al. 2021.. Infection-induced chromatin modifications facilitate translocation of herpes simplex virus capsids to the inner nuclear membrane. . PLOS Pathog. 17:(12):e1010132
    [Crossref] [Google Scholar]
  47. 47.
    Arii J. 2021.. Host and viral factors involved in nuclear egress of herpes simplex virus 1. . Viruses 13:(5):754
    [Crossref] [Google Scholar]
  48. 48.
    Ryckman BJ, Roller RJ. 2004.. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. . J. Virol. 78:(1):399412
    [Crossref] [Google Scholar]
  49. 49.
    Reynolds AE, Wills EG, Roller RJ, Ryckman BJ, Baines JD. 2002.. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. . J. Virol. 76:(17):893952
    [Crossref] [Google Scholar]
  50. 50.
    Bahnamiri MM, Roller RJ. 2021.. Mechanism of nuclear lamina disruption and the role of pUS3 in herpes simplex virus 1 nuclear egress. . J. Virol. 95::e02432-20
    [Google Scholar]
  51. 51.
    Park R, Baines JD. 2006.. Herpes simplex virus type 1 infection induces activation and recruitment of protein kinase C to the nuclear membrane and increased phosphorylation of lamin B. . J. Virol. 80:(1):494504
    [Crossref] [Google Scholar]
  52. 52.
    Myllys M, Ruokolainen V, Aho V, Smith EA, Hakanen S, et al. 2016.. Herpes simplex virus 1 induces egress channels through marginalized host chromatin. . Sci. Rep. 6:(1):28844
    [Crossref] [Google Scholar]
  53. 53.
    Douet J, Corujo D, Malinverni R, Renauld J, Sansoni V, et al. 2017.. MacroH2A histone variants maintain nuclear organization and heterochromatin architecture. . J. Cell Sci. 130:(9):157082
    [Crossref] [Google Scholar]
  54. 54.
    Stephens AD, Liu PZ, Banigan EJ, Almassalha LM, Backman V, et al. 2018.. Chromatin histone modifications and rigidity affect nuclear morphology independent of lamins. . Mol. Biol. Cell 29:(2):22033
    [Crossref] [Google Scholar]
  55. 55.
    Mogensen TH. 2009.. Pathogen recognition and inflammatory signaling in innate immune defenses. . Clin. Microbiol. Rev. 22:(2):24073
    [Crossref] [Google Scholar]
  56. 56.
    Schneider WM, Chevillotte MD, Rice CM. 2014.. Interferon-stimulated genes: a complex web of host defenses. . Annu. Rev. Immunol. 32::51345
    [Crossref] [Google Scholar]
  57. 57.
    Li T, Diner BA, Chen J, Cristea IM. 2012.. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. . PNAS 109:(26):1055863
    [Crossref] [Google Scholar]
  58. 58.
    Orzalli MH, Conwell SE, Berrios C, DeCaprio JA, Knipe DM. 2013.. Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. . PNAS 110:(47):E4492501
    [Crossref] [Google Scholar]
  59. 59.
    Cliffe AR, Knipe DM. 2008.. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. . J. Virol. 82:(24):1203038
    [Crossref] [Google Scholar]
  60. 60.
    Kent JR, Zeng P-Y, Atanasiu D, Gardner J, Fraser NW, Berger SL. 2004.. During lytic infection herpes simplex virus type 1 is associated with histones bearing modifications that correlate with active transcription. . J. Virol. 78:(18):1017886
    [Crossref] [Google Scholar]
  61. 61.
    Lang F, Li X, Vladimirova O, Hu B, Chen G, et al. 2017.. CTCF interacts with the lytic HSV-1 genome to promote viral transcription. . Sci. Rep. 7:(1):39861
    [Crossref] [Google Scholar]
  62. 62.
    Li X, Yu Y, Lang F, Chen G, Wang E, et al. 2021.. Cohesin promotes HSV-1 lytic transcription by facilitating the binding of RNA Pol II on viral genes. . Virol. J. 18:(1):26
    [Crossref] [Google Scholar]
  63. 63.
    Kwiatkowski DL, Thompson HW, Bloom DC. 2009.. The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. . J. Virol. 83:(16):817381
    [Crossref] [Google Scholar]
  64. 64.
    Bloom DC, Giordani NV, Kwiatkowski DL. 2010.. Epigenetic regulation of latent HSV-1 gene expression. . Biochim. Biophys. Acta 1799:(3–4):24656
    [Crossref] [Google Scholar]
  65. 65.
    Cliffe AR, Coen DM, Knipe DM. 2013.. Kinetics of facultative heterochromatin and polycomb group protein association with the herpes simplex viral genome during establishment of latent infection. . mBio 4:(1):e00590-12
    [Crossref] [Google Scholar]
  66. 66.
    Liang Y, Quenelle D, Vogel JL, Mascaro C, Ortega A, Kristie TM. 2013.. A novel selective LSD1/KDM1A inhibitor epigenetically blocks herpes simplex virus lytic replication and reactivation from latency. . mBio 4:(1):e00558-12
    [Crossref] [Google Scholar]
  67. 67.
    Messer HGP, Jacobs D, Dhummakupt A, Bloom DC. 2015.. Inhibition of H3K27me3-specific histone demethylases JMJD3 and UTX blocks reactivation of herpes simplex virus 1 in trigeminal ganglion neurons. . J. Virol. 89:(6):341720
    [Crossref] [Google Scholar]
  68. 68.
    Margueron R, Reinberg D. 2011.. The polycomb complex PRC2 and its mark in life. . Nature 469:(7330):34349
    [Crossref] [Google Scholar]
  69. 69.
    Arbuckle JH, Gardina PJ, Gordon DN, Hickman HD, Yewdell JW, et al. 2017.. Inhibitors of the histone methyltransferases EZH2/1 induce a potent antiviral state and suppress infection by diverse viral pathogens. . mBio 8:(4):e01141-17
    [Crossref] [Google Scholar]
  70. 70.
    Lee JS, Raja P, Pan D, Pesola JM, Coen DM, Knipe DM. 2018.. CCCTC-binding factor acts as a heterochromatin barrier on herpes simplex viral latent chromatin and contributes to poised latent infection. . mBio 9:(1):e02372-17
    [Google Scholar]
  71. 71.
    Washington SD, Edenfield SI, Lieux C, Watson ZL, Taasan SM, et al. 2018.. Depletion of the insulator protein CTCF results in herpes simplex virus 1 reactivation in vivo. . J. Virol. 92:(11):e00173-18
    [Crossref] [Google Scholar]
  72. 72.
    Washington SD, Singh P, Johns RN, Edwards TG, Mariani M, et al. 2019.. The CCCTC binding factor, CTRL2, modulates heterochromatin deposition and the establishment of herpes simplex virus 1 latency in vivo. . J. Virol. 93::e00415-19
    [Crossref] [Google Scholar]
  73. 73.
    Singh P, Neumann DM. 2021.. Cohesin subunit Rad21 binds to the herpes simplex virus 1 genome near CTCF insulator sites during latency in vivo. . J. Virol. 95::e00364-21
    [Google Scholar]
  74. 74.
    Callé A, Ugrinova I, Epstein AL, Bouvet P, Diaz J-J, Greco A. 2008.. Nucleolin is required for an efficient herpes simplex virus type 1 infection. . J. Virol. 82:(10):476273
    [Crossref] [Google Scholar]
  75. 75.
    Lymberopoulos MH, Bourget A, Abdeljelil NB, Pearson A. 2011.. Involvement of the UL24 protein in herpes simplex virus 1-induced dispersal of B23 and in nuclear egress. . Virology 412:(2):34148
    [Crossref] [Google Scholar]
  76. 76.
    Lymberopoulos MH, Pearson A. 2007.. Involvement of UL24 in herpes-simplex-virus-1-induced dispersal of nucleolin. . Virology 363:(2):397409
    [Crossref] [Google Scholar]
  77. 77.
    López MR, Schlegel EFM, Wintersteller S, Blaho JA. 2008.. The major tegument structural protein VP22 targets areas of dispersed nucleolin and marginalized chromatin during productive herpes simplex virus 1 infection. . Virus Res. 136:(1–2):17588
    [Crossref] [Google Scholar]
  78. 78.
    Greco A, Arata L, Soler E, Gaume X, Couté Y, et al. 2012.. Nucleolin interacts with US11 protein of herpes simplex virus 1 and is involved in its trafficking. . J. Virol. 86:(3):144957
    [Crossref] [Google Scholar]
  79. 79.
    Cannon MJ, Schmid DS, Hyde TB. 2010.. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. . Rev. Med. Virol. 20:(4):20213
    [Crossref] [Google Scholar]
  80. 80.
    Zanghellini F, Boppana SB, Emery VC, Griffiths PD, Pass RF. 1999.. Asymptomatic primary cytomegalovirus infection: virologic and immunologic features. . J. Infect. Dis. 180:(3):7027
    [Crossref] [Google Scholar]
  81. 81.
    Manicklal S, Emery VC, Lazzarotto T, Boppana SB, Gupta RK. 2013.. The “silent” global burden of congenital cytomegalovirus. . Clin. Microbiol. Rev. 26:(1):86102
    [Crossref] [Google Scholar]
  82. 82.
    Azevedo LS, Pierrotti LC, Abdala E, Costa SF, Strabelli TMV, et al. 2015.. Cytomegalovirus infection in transplant recipients. . Clinics 70:(7):51523
    [Crossref] [Google Scholar]
  83. 83.
    Christensen-Quick A, Vanpouille C, Lisco A, Gianella S. 2017.. Cytomegalovirus and HIV persistence: pouring gas on the fire. . AIDS Res. Hum. Retrovir. 33:(S1):S23S-30
    [Crossref] [Google Scholar]
  84. 84.
    Lurain NS, Chou S. 2010.. Antiviral drug resistance of human cytomegalovirus. . Clin. Microbiol. Rev. 23:(4):689712
    [Crossref] [Google Scholar]
  85. 85.
    Alwine JC. 2012.. The human cytomegalovirus assembly compartment: a masterpiece of viral manipulation of cellular processes that facilitates assembly and egress. . PLOS Pathog. 8:(9):e1002878
    [Crossref] [Google Scholar]
  86. 86.
    Procter DJ, Furey C, Garza-Gongora AG, Kosak ST, Walsh D. 2020.. Cytoplasmic control of intranuclear polarity by human cytomegalovirus. . Nature 587:(7832):10914
    [Crossref] [Google Scholar]
  87. 87.
    Buchkovich NJ, Maguire TG, Alwine JC. 2010.. Role of the endoplasmic reticulum chaperone BiP, SUN domain proteins, and dynein in altering nuclear morphology during human cytomegalovirus infection. . J. Virol. 84:(14):700517
    [Crossref] [Google Scholar]
  88. 88.
    Das S, Ortiz DA, Gurczynski SJ, Khan F, Pellett PE. 2014.. Identification of human cytomegalovirus genes important for biogenesis of the cytoplasmic virion assembly complex. . J. Virol. 88:(16):908699
    [Crossref] [Google Scholar]
  89. 89.
    Camozzi D, Pignatelli S, Valvo C, Lattanzi G, Capanni C, et al. 2008.. Remodelling of the nuclear lamina during human cytomegalovirus infection: role of the viral proteins pUL50 and pUL53. . J. Gen. Virol. 89:(3):73140
    [Crossref] [Google Scholar]
  90. 90.
    Mücke K, Paulus C, Bernhardt K, Gerrer K, Schön K, et al. 2014.. Human cytomegalovirus major immediate early 1 protein targets host chromosomes by docking to the acidic pocket on the nucleosome surface. . J. Virol. 88:(2):122848
    [Crossref] [Google Scholar]
  91. 91.
    Fang Q, Chen P, Wang M, Fang J, Yang N, et al. 2016.. Human cytomegalovirus IE1 protein alters the higher-order chromatin structure by targeting the acidic patch of the nucleosome. . eLife 5::e11911
    [Crossref] [Google Scholar]
  92. 92.
    Mauch-Mücke K, Schön K, Paulus C, Nevels MM. 2020.. Evidence for tethering of human cytomegalovirus genomes to host chromosomes. . Front. Cell. Infect. Microbiol. 10::577428
    [Crossref] [Google Scholar]
  93. 93.
    Nitzsche A, Paulus C, Nevels M. 2008.. Temporal dynamics of cytomegalovirus chromatin assembly in productively infected human cells. . J. Virol. 82:(22):1116780
    [Crossref] [Google Scholar]
  94. 94.
    Albright ER, Morrison K, Ranganathan P, Carter DM, Nishikiori M, et al. 2022.. Human cytomegalovirus lytic infection inhibits replication-dependent histone synthesis and requires stem loop binding protein function. . PNAS 119:(14):e2122174119
    [Crossref] [Google Scholar]
  95. 95.
    Nitzsche A, Steinhäußer C, Mücke K, Paulus C, Nevels M. 2012.. Histone H3 lysine 4 methylation marks postreplicative human cytomegalovirus chromatin. . J. Virol. 86:(18):981727
    [Crossref] [Google Scholar]
  96. 96.
    Cuevas-Bennett C, Shenk T. 2008.. Dynamic histone H3 acetylation and methylation at human cytomegalovirus promoters during replication in fibroblasts. . J. Virol. 82:(19):952536
    [Crossref] [Google Scholar]
  97. 97.
    Groves IJ, Reeves MB, Sinclair JH. 2009.. Lytic infection of permissive cells with human cytomegalovirus is regulated by an intrinsic ‘pre-immediate-early’ repression of viral gene expression mediated by histone post-translational modification. . J. Gen. Virol. 90:(10):236474
    [Crossref] [Google Scholar]
  98. 98.
    Lieberman PM. 2013.. Keeping it quiet: chromatin control of gammaherpesvirus latency. . Nat. Rev. Microbiol. 11:(12):86375
    [Crossref] [Google Scholar]
  99. 99.
    Matthews SM, Groves IJ, O'Connor CM. 2023.. Chromatin control of human cytomegalovirus infection. . mBio 14:(4):e00326-23
    [Google Scholar]
  100. 100.
    Nevels M, Paulus C, Shenk T. 2004.. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. . PNAS 101:(49):1723439
    [Crossref] [Google Scholar]
  101. 101.
    Martínez FP, Cruz R, Lu F, Plasschaert R, Deng Z, et al. 2014.. CTCF binding to the first intron of the major immediate early (MIE) gene of human cytomegalovirus (HCMV) negatively regulates MIE gene expression and HCMV replication. . J. Virol. 88:(13):7389401
    [Crossref] [Google Scholar]
  102. 102.
    Elder EG, Krishna BA, Poole E, Perera M, Sinclair J. 2021.. Regulation of host and viral promoters during human cytomegalovirus latency via US28 and CTCF. . J. Gen. Virol. 102:(5):001609
    [Crossref] [Google Scholar]
  103. 103.
    Abraham CG, Kulesza CA. 2013.. Polycomb repressive complex 2 silences human cytomegalovirus transcription in quiescent infection models. . J. Virol. 87:(24):13193205
    [Crossref] [Google Scholar]
  104. 104.
    Cavallo T, Graves K, Cole NL, Albrecht T. 1981.. Cytomegalovirus: an ultrastructural study of the morphogenesis of nuclear inclusions in human cell culture. . J. Gen. Virol. 56:(1):97104
    [Crossref] [Google Scholar]
  105. 105.
    Villinger C, Neusser G, Kranz C, Walther P, Mertens T. 2015.. 3D analysis of HCMV induced-nuclear membrane structures by FIB/SEM tomography: insight into an unprecedented membrane morphology. . Viruses 7:(11):5686704
    [Crossref] [Google Scholar]
  106. 106.
    Strang BL, Boulant S, Coen DM. 2010.. Nucleolin associates with the human cytomegalovirus DNA polymerase accessory subunit UL44 and is necessary for efficient viral replication. . J. Virol. 84:(4):177184
    [Crossref] [Google Scholar]
  107. 107.
    Westdorp KN, Sand A, Moorman NJ, Terhune SS. 2017.. Cytomegalovirus late protein pUL31 alters pre-rRNA expression and nuclear organization during infection. . J. Virol. 91::e00593-17
    [Crossref] [Google Scholar]
  108. 108.
    Al-Heeti OM, Cathro HP, Ison MG. 2022.. Adenovirus infection and transplantation. . Transplantation 106:(5):92027
    [Crossref] [Google Scholar]
  109. 109.
    Majorant D, Qiu F, Kalil AC, Wilson N, Florescu DF. 2018.. Adenovirus—a deadly disease in the solid organ transplant population: risk factors and outcomes. . Transplant Proc. 50:(10):376974
    [Crossref] [Google Scholar]
  110. 110.
    Marsh K, Tayler R, Pollock L, Roy K, Lakha F, et al. 2022.. Investigation into cases of hepatitis of unknown aetiology among young children, Scotland, 1 January 2022 to 12 April 2022. . Eurosurveillance 27:(15):2200318
    [Crossref] [Google Scholar]
  111. 111.
    Baker JM, Buchfellner M, Britt W, Sanchez V, Potter JL, et al. 2022.. Acute hepatitis and adenovirus infection among children—Alabama, October 2021–February 2022. . Morb. Mortal. Wkly. Rep. 71:(18):63840
    [Crossref] [Google Scholar]
  112. 112.
    Hoke CH, Snyder CE. 2013.. 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 31:(12):162332
    [Crossref] [Google Scholar]
  113. 113.
    Sandkovsky U, Vargas L, Florescu DF. 2014.. Adenovirus: current epidemiology and emerging approaches to prevention and treatment. . Curr. Infect. Dis. Rep. 16:(8):416
    [Crossref] [Google Scholar]
  114. 114.
    Avgousti DC, Herrmann C, Kulej K, Pancholi NJ, Sekulic N, et al. 2016.. A core viral protein binds host nucleosomes to sequester immune danger signals. . Nature 535:(7610):17377
    [Crossref] [Google Scholar]
  115. 115.
    Lynch KL, Dillon MR, Bat-Erdene M, Lewis HC, Kaai RJ, et al. 2021.. A viral histone-like protein exploits antagonism between linker histones and HMGB proteins to obstruct the cell cycle. . Curr. Biol. 31:(23):522737
    [Crossref] [Google Scholar]
  116. 116.
    Charman M, Weitzman MD. 2020.. Replication compartments of DNA viruses in the nucleus: location, location, location. . Viruses 12:(2):151
    [Crossref] [Google Scholar]
  117. 117.
    Pfitzner S, Hofmann-Sieber H, Bosse JB, Franken LE, Grünewald K, Dobner T. 2020.. Fluorescent protein tagging of adenoviral proteins pV and pIX reveals ‘late virion accumulation compartment. .’ PLOS Pathog. 16:(6):e1008588
    [Crossref] [Google Scholar]
  118. 118.
    Lynch KL, Gooding LR, Garnett-Benson C, Ornelles DA, Avgousti DC. 2019.. Epigenetics and the dynamics of chromatin during adenovirus infections. . FEBS Lett. 593:(24):355170
    [Crossref] [Google Scholar]
  119. 119.
    Stein RW, Corrigan M, Yaciuk P, Whelan J, Moran E. 1990.. Analysis of E1A-mediated growth regulation functions: binding of the 300-kilodalton cellular product correlates with E1A enhancer repression function and DNA synthesis-inducing activity. . J. Virol. 64:(9):442127
    [Crossref] [Google Scholar]
  120. 120.
    Arany Z, Newsome D, Oldread E, Livingston DM, Eckner R. 1995.. A family of transcriptional adaptor proteins targeted by the E1A oncoprotein. . Nature 374:(6517):8184
    [Crossref] [Google Scholar]
  121. 121.
    Horwitz GA, Zhang K, McBrian MA, Grunstein M, Kurdistani SK, Berk AJ. 2008.. Adenovirus small e1a alters global patterns of histone modification. . Science 321:(5892):108485
    [Crossref] [Google Scholar]
  122. 122.
    Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ, Kurdistani SK. 2008.. Epigenetic reprogramming by adenovirus e1a. . Science 321:(5892):108688
    [Crossref] [Google Scholar]
  123. 123.
    Ferrari R, Su T, Li B, Bonora G, Oberai A, et al. 2012.. Reorganization of the host epigenome by a viral oncogene. . Genome Res. 22:(7):121221
    [Crossref] [Google Scholar]
  124. 124.
    Ferrari R, Gou D, Jawdekar G, Johnson SA, Nava M, et al. 2014.. Adenovirus small e1a employs the lysine acetylases p300/CBP and tumor suppressor Rb to repress select host genes and promote productive virus infection. . Cell Host Microbe 16:(5):66376
    [Crossref] [Google Scholar]
  125. 125.
    Johnson JS, Osheim YN, Xue Y, Emanuel MR, Lewis PW, et al. 2004.. Adenovirus protein VII condenses DNA, represses transcription, and associates with transcriptional activator E1A. . J. Virol. 78:(12):645968
    [Crossref] [Google Scholar]
  126. 126.
    Haruki H, Okuwaki M, Miyagishi M, Taira K, Nagata K. 2006.. Involvement of template-activating factor I/SET in transcription of adenovirus early genes as a positive-acting factor. . J. Virol. 80:(2):794801
    [Crossref] [Google Scholar]
  127. 127.
    Haruki H, Gyurcsik B, Okuwaki M, Nagata K. 2003.. Ternary complex formation between DNA-adenovirus core protein VII and TAF-Iβ/SET, an acidic molecular chaperone. . FEBS Lett. 555:(3):52127
    [Crossref] [Google Scholar]
  128. 128.
    Tang D, Kang R, Zeh HJ, Lotze MT. 2023.. The multifunctional protein HMGB1: 50 years of discovery. . Nat. Rev. Immunol. 23:(12):82441
    [Crossref] [Google Scholar]
  129. 129.
    Arnold EA, Kaai RJ, Leung K, Brinkley MR, Kelnhofer-Millevolte LE, et al. 2023.. Adenovirus protein VII binds the A-box of HMGB1 to repress interferon responses. . PLOS Pathog. 19:(9):e1011633
    [Crossref] [Google Scholar]
  130. 130.
    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:(4):247483
    [Crossref] [Google Scholar]
  131. 131.
    Carvalho T, Seeler JS, Ohman K, Jordan P, Pettersson U, et al. 1995.. Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. . J. Cell Biol. 131:(1):4556
    [Crossref] [Google Scholar]
  132. 132.
    Ullman AJ, Reich NC, Hearing P. 2007.. Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. . J. Virol. 81:(9):474452
    [Crossref] [Google Scholar]
  133. 133.
    Stracker TH, Carson CT, Weitzman MD. 2002.. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. . Nature 418:(6895):34852
    [Crossref] [Google Scholar]
  134. 134.
    Soriano AM, Crisostomo L, Mendez M, Graves D, Frost JR, et al. 2019.. Adenovirus 5 E1A interacts with E4orf3 to regulate viral chromatin organization. . J. Virol. 93::e00157-19
    [Crossref] [Google Scholar]
  135. 135.
    Lawrence FJ, McStay B, Matthews DA. 2006.. Nucleolar protein upstream binding factor is sequestered into adenovirus DNA replication centres during infection without affecting RNA polymerase I location or ablating rRNA synthesis. . J. Cell Sci. 119:(12):262131
    [Crossref] [Google Scholar]
  136. 136.
    Lam YW, Evans VC, Heesom KJ, Lamond AI, Matthews DA. 2010.. Proteomics analysis of the nucleolus in adenovirus-infected cells. . Mol. Cell. Proteom. 9:(1):11730
    [Crossref] [Google Scholar]
  137. 137.
    Reyes ED, Kulej K, Pancholi NJ, Akhtar LN, Avgousti DC, et al. 2017.. Identifying host factors associated with DNA replicated during virus infection. . Mol. Cell. Proteom. 16:(12):207997
    [Crossref] [Google Scholar]
  138. 138.
    Genoveso MJ, Hisaoka M, Komatsu T, Wodrich H, Nagata K, Okuwaki M. 2020.. Formation of adenovirus DNA replication compartments and viral DNA accumulation sites by host chromatin regulatory proteins including NPM1. . FEBS J. 287:(1):20517
    [Crossref] [Google Scholar]
  139. 139.
    Ugai H, Dobbins GC, Wang M, Le LP, Matthews DA, Curiel DT. 2012.. Adenoviral protein V promotes a process of viral assembly through nucleophosmin 1. . Virology 432:(2):28395
    [Crossref] [Google Scholar]
  140. 140.
    Samad MA, Komatsu T, Okuwaki M, Nagata K. 2012.. B23/nucleophosmin is involved in regulation of adenovirus chromatin structure at late infection stages, but not in virus replication and transcription. . J. Gen. Virol. 93:(Part 6):132838
    [Crossref] [Google Scholar]
  141. 141.
    Samad MA, Okuwaki M, Haruki H, Nagata K. 2007.. Physical and functional interaction between a nucleolar protein nucleophosmin/B23 and adenovirus basic core proteins. . FEBS Lett. 581:(17):328388
    [Crossref] [Google Scholar]
  142. 142.
    Box JK, Paquet N, Adams MN, Boucher D, Bolderson E, et al. 2016.. Nucleophosmin: from structure and function to disease development. . BMC Mol. Biol. 17:(1):19
    [Crossref] [Google Scholar]
  143. 143.
    Pfitzner S, Bosse JB, Hofmann-Sieber H, Flomm F, Reimer R, et al. 2021.. Human adenovirus type 5 infection leads to nuclear envelope destabilization and membrane permeability independently of adenovirus death protein. . Int. J. Mol. Sci. 22:(23):13034
    [Crossref] [Google Scholar]
  144. 144.
    Tollefson AE, Scaria A, Hermiston TW, Ryerse JS, Wold LJ, Wold WS. 1996.. The adenovirus death protein (E3-11.6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. . J. Virol. 70:(4):2296306
    [Crossref] [Google Scholar]
  145. 145.
    Doan PTB, Nio K, Shimakami T, Kuroki K, Li Y-Y, et al. 2023.. Super-resolution microscopy analysis of hepatitis B viral cccDNA and host factors. . Viruses 15:(5):1178
    [Crossref] [Google Scholar]
  146. 146.
    Moreau P, Cournac A, Palumbo GA, Marbouty M, Mortaza S, et al. 2018.. Tridimensional infiltration of DNA viruses into the host genome shows preferential contact with active chromatin. . Nat. Commun. 9:(1):4268
    [Crossref] [Google Scholar]
  147. 147.
    Porter SS, Liddle JC, Browne K, Pastrana DV, Garcia BA, et al. 2021.. Histone modifications in papillomavirus virion minichromosomes. . mBio 12:(1):e03274-20
    [Crossref] [Google Scholar]
  148. 148.
    Wang R, Lee J-H, Kim J, Xiong F, Hasani LA, et al. 2023.. SARS-CoV-2 restructures host chromatin architecture. . Nat. Microbiol. 8:(4):67994
    [Crossref] [Google Scholar]
  149. 149.
    Washington SD, Musarrat F, Ertel MK, Backes GL, Neumann DM. 2018.. CTCF binding sites in the herpes simplex virus 1 genome display site-specific CTCF occupation, protein recruitment, and insulator function. . J. Virol. 92:(8):e00156-18
    [Crossref] [Google Scholar]
  150. 150.
    Kaya-Okur HS, Wu SJ, Codomo CA, Pledger ES, Bryson TD, et al. 2019.. CUT&Tag for efficient epigenomic profiling of small samples and single cells. . Nat. Commun. 10:(1):1930
    [Crossref] [Google Scholar]
  151. 151.
    Boftsi M, Whittle FB, Wang J, Shepherd P, Burger LR, et al. 2021.. The adeno-associated virus 2 genome and Rep 68/78 proteins interact with cellular sites of DNA damage. . Hum. Mol. Genet. 31:(6):98598
    [Crossref] [Google Scholar]
  152. 152.
    Majumder K, Boftsi M, Pintel DJ. 2019.. Viral chromosome conformation capture (V3C) assays for identifying trans-interaction sites between lytic viruses and the cellular genome. . Bio-Protocol 9:(6):e3198
    [Crossref] [Google Scholar]
  153. 153.
    Vu A, Poyzer C, Roller R. 2016.. Extragenic suppression of a mutation in herpes simplex virus 1 UL34 that affects lamina disruption and nuclear egress. . J. Virol. 90:(23):1073851
    [Crossref] [Google Scholar]
  154. 154.
    Dembowski JA, DeLuca NA. 2018.. Temporal viral genome-protein interactions define distinct stages of productive herpesviral infection. . mBio 9:(4):e01182-18
    [Crossref] [Google Scholar]
  155. 155.
    Kulej K, Avgousti DC, Sidoli S, Herrmann C, Fera AND, et al. 2017.. Time-resolved global and chromatin proteomics during herpes simplex virus type 1 (HSV-1) infection. . Mol. Cell. Proteom. 16:(4):S92107
    [Crossref] [Google Scholar]
  156. 156.
    Dembowski JA, Dremel SE, DeLuca NA. 2017.. Replication-coupled recruitment of viral and cellular factors to herpes simplex virus type 1 replication forks for the maintenance and expression of viral genomes. . PLOS Pathog. 13:(1):e1006166
    [Crossref] [Google Scholar]
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