Early Nuclear Events after Herpesviral Infection
<p>Herpesviral antagonism of the ATM- and DNA-PK-branch of the DDR directly after infection. After infection of target cells, the herpesviral capsid is transported to the nuclear membrane and the viral DNA released into the nucleus through nuclear pores. We propose that the cellular DDR complexes recognize the viral linear DNA by MRN- and KU70/KU80-complex binding to double-strand break resembling ends of the linear viral DNA. This results in activation of kinases ATM and DNA-PK respectively, followed by phosphorylation of H2AX (γH2AX) and CHK1/2 and activation of downstream proteins including the cell cycle regulator p53. HSV-1, HCMV and KSHV have been shown to counteract this activation as indicated in the graph, however, the viral effector proteins and mechanisms are not identified. Depletion of proteins depicted in red font has been shown to enhance herpesviral replication, indicating an inhibiting role on herpesviral replication. ? indicates an unknown mechanism.</p> "> Figure 2
<p>Herpesviral antagonism of PML-nuclear bodies. After the infection of target cells, the herpesviral capsid is transported to the nuclear membrane and the viral DNA released into the nucleus through nuclear pores. The genome rapidly associates with PML nuclear bodies (PML-NBs). PML-NBs are considered as antiviral nuclear organelles that restrict gene expression from viral genomes, and PML-NB components PML, SP100, DAXX and ATRX as well as the transiently associated proteins IFI16 and HIRA have been shown to mediate this restriction. PML is an essential structural component of PML-NBs and depletion of PML disrupts PML-NBs. Herpesviruses in contrast have evolved mechanisms to counteract this restriction, in particular viral tegument and immediate-early proteins as depicted in the graph. ? Indicates hypothetical mode of interference.</p> ">
Abstract
:1. Introduction
2. DNA Sensor Proteins
3. DNA Damage Response Proteins
4. PML Nuclear Bodies
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Pellet, P.E.; Roizman, B. Fields Virology; Wolters Kluwer: Alfon am Rhein, The Netherlands, 2013. [Google Scholar]
- Looker, K.J.; Magaret, A.S.; May, M.T.; Turner, K.M.; Vickerman, P.; Gottlieb, S.L.; Newman, L.M. Global and Regional Estimates of Prevalent and Incident Herpes Simplex Virus Type 1 Infections in 2012. PLoS ONE 2015, 10, e0140765. [Google Scholar] [CrossRef] [PubMed]
- Emery, V.C.; Clark, D.A. HHV-6A, 6B, and 7: Persistence in the population, epidemiology and transmission. In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis; Cambridge University Press: Cambridge, UK, 2007. [Google Scholar]
- Hjalgrim, H.; Friborg, J.; Melbye, M. The epidemiology of EBV and its association with malignant disease. In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis; Cambridge University Press: Cambridge, UK, 2007. [Google Scholar]
- Liu, Y.T.; Jih, J.; Dai, X.; Bi, G.Q.; Zhou, Z.H. Cryo-EM structures of herpes simplex virus type 1 portal vertex and packaged genome. Nature 2019, 570, 257–261. [Google Scholar] [CrossRef] [PubMed]
- Hornung, V.; Ablasser, A.; Charrel-Dennis, M.; Bauernfeind, F.; Horvath, G.; Caffrey, D.R.; Latz, E.; Fitzgerald, K.A. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009, 458, 514–518. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, L.; Wu, J.; Du, F.; Chen, X.; Chen, Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339, 786–791. [Google Scholar] [CrossRef] [PubMed]
- Wu, J.; Sun, L.; Chen, X.; Du, F.; Shi, H.; Chen, C.; Chen, Z.J. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013, 339, 826–830. [Google Scholar] [CrossRef] [PubMed]
- Knipe, D.M. Nuclear sensing of viral DNA, epigenetic regulation of herpes simplex virus infection, and innate immunity. Virology 2015, 479, 153–159. [Google Scholar] [CrossRef] [PubMed]
- Kobiler, O.; Drayman, N.; Butin-Israeli, V.; Oppenheim, A. Virus strategies for passing the nuclear envelope barrier. Nucleus 2012, 3, 526–539. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Orzalli, M.H.; Conwell, S.E.; Berrios, C.; DeCaprio, J.A.; Knipe, D.M. Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc. Natl. Acad. Sci. USA 2013, 110, E4492–E4501. [Google Scholar] [CrossRef]
- Orzalli, M.H.; DeLuca, N.A.; Knipe, D.M. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. USA 2012, 109, E3008–E3017. [Google Scholar] [CrossRef]
- Li, T.; Diner, B.A.; Chen, J.; Cristea, I.M. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc. Natl. Acad. Sci. USA 2012, 109, 10558–10563. [Google Scholar] [CrossRef] [Green Version]
- Komatsu, T.; Nagata, K.; Wodrich, H. The Role of Nuclear Antiviral Factors against Invading DNA Viruses: The Immediate Fate of Incoming Viral Genomes. Viruses 2016, 8, 290. [Google Scholar] [CrossRef] [PubMed]
- Unterholzner, L.; Keating, S.E.; Baran, M.; Horan, K.A.; Jensen, S.B.; Sharma, S.; Sirois, C.M.; Jin, T.; Latz, E.; Xiao, T.S.; et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 2010, 11, 997–1004. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ansari, M.A.; Dutta, S.; Veettil, M.V.; Dutta, D.; Iqbal, J.; Kumar, B.; Roy, A.; Chikoti, L.; Singh, V.V.; Chandran, B. Herpesvirus Genome Recognition Induced Acetylation of Nuclear IFI16 Is Essential for Its Cytoplasmic Translocation, Inflammasome and IFN-beta Responses. PLoS Pathog. 2015, 11, e1005019. [Google Scholar] [CrossRef]
- Orzalli, M.H.; Broekema, N.M.; Diner, B.A.; Hancks, D.C.; Elde, N.C.; Cristea, I.M.; Knipe, D.M. cGAS-mediated stabilization of IFI16 promotes innate signaling during herpes simplex virus infection. Proc. Natl. Acad. Sci. USA 2015, 112, E1773–E1781. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Everett, R.D. Dynamic Response of IFI16 and Promyelocytic Leukemia Nuclear Body Components to Herpes Simplex Virus 1 Infection. J. Virol. 2016, 90, 167–179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lum, K.K.; Howard, T.R.; Pan, C.; Cristea, I.M. Charge-Mediated Pyrin Oligomerization Nucleates Antiviral IFI16 Sensing of Herpesvirus DNA. MBio 2019. [Google Scholar] [CrossRef] [PubMed]
- Merkl, P.E.; Knipe, D.M. Role for a Filamentous Nuclear Assembly of IFI16, DNA, and Host Factors in Restriction of Herpesviral Infection. MBio 2019. [Google Scholar] [CrossRef]
- Gariano, G.R.; Dell’Oste, V.; Bronzini, M.; Gatti, D.; Luganini, A.; De Andrea, M.; Gribaudo, G.; Gariglio, M.; Landolfo, S. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog. 2012, 8, e1002498. [Google Scholar] [CrossRef]
- Li, T.; Chen, J.; Cristea, I.M. Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe. 2013, 14, 591–599. [Google Scholar] [CrossRef]
- Cuchet-Lourenco, D.; Anderson, G.; Sloan, E.; Orr, A.; Everett, R.D. The viral ubiquitin ligase ICP0 is neither sufficient nor necessary for degradation of the cellular DNA sensor IFI16 during herpes simplex virus 1 infection. J. Virol. 2013, 87, 13422–13432. [Google Scholar] [CrossRef]
- Diner, B.A.; Lum, K.K.; Javitt, A.; Cristea, I.M. Interactions of the Antiviral Factor Interferon Gamma-Inducible Protein 16 (IFI16) Mediate Immune Signaling and Herpes Simplex Virus-1 Immunosuppression. Mol. Cell Proteomics. 2015, 14, 2341–2356. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Orzalli, M.H.; Broekema, N.M.; Knipe, D.M. Relative Contributions of Herpes Simplex Virus 1 ICP0 and vhs to Loss of Cellular IFI16 Vary in Different Human Cell Types. J. Virol. 2016, 90, 8351–8359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roy, A.; Dutta, D.; Iqbal, J.; Pisano, G.; Gjyshi, O.; Ansari, M.A.; Kumar, B.; Chandran, B. Nuclear Innate Immune DNA Sensor IFI16 Is Degraded during Lytic Reactivation of Kaposi’s Sarcoma-Associated Herpesvirus (KSHV): Role of IFI16 in Maintenance of KSHV Latency. J. Virol. 2016, 90, 8822–8841. [Google Scholar] [CrossRef] [PubMed]
- Kerur, N.; Veettil, M.V.; Sharma-Walia, N.; Bottero, V.; Sadagopan, S.; Otageri, P.; Chandran, B. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe. 2011, 9, 363–375. [Google Scholar] [CrossRef] [PubMed]
- Dutta, D.; Dutta, S.; Veettil, M.V.; Roy, A.; Ansari, M.A.; Iqbal, J.; Chikoti, L.; Kumar, B.; Johnson, K.E.; Chandran, B. BRCA1 Regulates IFI16 Mediated Nuclear Innate Sensing of Herpes Viral DNA and Subsequent Induction of the Innate Inflammasome and Interferon-beta Responses. PLoS Pathog. 2015, 11, e1005030. [Google Scholar] [CrossRef]
- Iqbal, J.; Ansari, M.A.; Kumar, B.; Dutta, D.; Roy, A.; Chikoti, L.; Pisano, G.; Dutta, S.; Vahedi, S.; Veettil, M.V.; et al. Histone H2B-IFI16 Recognition of Nuclear Herpesviral Genome Induces Cytoplasmic Interferon-beta Responses. PLoS Pathog. 2016, 12, e1005967. [Google Scholar] [CrossRef]
- Johnson, K.E.; Bottero, V.; Flaherty, S.; Dutta, S.; Singh, V.V.; Chandran, B. IFI16 restricts HSV-1 replication by accumulating on the hsv-1 genome, repressing HSV-1 gene expression, and directly or indirectly modulating histone modifications. PLoS Pathog. 2014, 10, e1004503. [Google Scholar] [CrossRef]
- Alandijany, T.; Roberts, A.P.E.; Conn, K.L.; Loney, C.; McFarlane, S.; Orr, A.; Boutell, C. Distinct temporal roles for the promyelocytic leukaemia (PML) protein in the sequential regulation of intracellular host immunity to HSV-1 infection. PLoS Pathog. 2018, 14, e1006769. [Google Scholar] [CrossRef]
- Komatsu, T.; Nagata, K.; Wodrich, H. An Adenovirus DNA Replication Factor, but Not Incoming Genome Complexes, Targets PML Nuclear Bodies. J. Virol. 2016, 90, 1657–1667. [Google Scholar] [CrossRef] [Green Version]
- Komatsu, T.; Will, H.; Nagata, K.; Wodrich, H. Imaging analysis of nuclear antiviral factors through direct detection of incoming adenovirus genome complexes. Biochem. Biophys. Res. Commun. 2016, 473, 200–205. [Google Scholar] [CrossRef]
- Cabral, J.M.; Oh, H.S.; Knipe, D.M. ATRX promotes maintenance of herpes simplex virus heterochromatin during chromatin stress. Elife 2018. [Google Scholar] [CrossRef] [PubMed]
- Orzalli, M.H.; Knipe, D.M. Cellular sensing of viral DNA and viral evasion mechanisms. Annu. Rev. Microbiol. 2014, 68, 477–492. [Google Scholar] [CrossRef] [PubMed]
- Stempel, M.; Chan, B.; Brinkmann, M.M. Coevolution pays off: Herpesviruses have the license to escape the DNA sensing pathway. Med. Microbiol. Immunol. 2019. [Google Scholar] [CrossRef] [PubMed]
- Weitzman, M.D.; Fradet-Turcotte, A. Virus DNA Replication and the Host DNA Damage Response. Annu. Rev. Virol. 2018, 5, 141–164. [Google Scholar] [CrossRef] [PubMed]
- Shah, G.A.; O’Shea, C.C. Viral and Cellular Genomes Activate Distinct DNA Damage Responses. Cell 2015, 162, 987–1002. [Google Scholar] [CrossRef] [Green Version]
- Stracker, T.H.; Carson, C.T.; Weitzman, M.D. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 2002, 418, 348–352. [Google Scholar] [CrossRef] [PubMed]
- Baker, A.; Rohleder, K.J.; Hanakahi, L.A.; Ketner, G. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 2007, 81, 7034–7040. [Google Scholar] [CrossRef]
- Schrank, B.; Gautier, J. Assembling nuclear domains: Lessons from DNA repair. J. Cell Biol. 2019. [Google Scholar] [CrossRef]
- Smith, S.; Reuven, N.; Mohni, K.N.; Schumacher, A.J.; Weller, S.K. Structure of the herpes simplex virus 1 genome: Manipulation of nicks and gaps can abrogate infectivity and alter the cellular DNA damage response. J. Virol. 2014, 88, 10146–10156. [Google Scholar] [CrossRef]
- Blackburn, E.H.; Epel, E.S.; Lin, J. Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science 2015, 350, 1193–1198. [Google Scholar] [CrossRef] [Green Version]
- Flamand, L. Chromosomal Integration by Human Herpesviruses 6A and 6B. Adv. Exp. Med. Biol. 2018, 1045, 209–226. [Google Scholar] [PubMed]
- Nacheva, E.P.; Ward, K.N.; Brazma, D.; Virgili, A.; Howard, J.; Leong, H.N.; Clark, D.A. Human herpesvirus 6 integrates within telomeric regions as evidenced by five different chromosomal sites. J. Med. Virol. 2008, 80, 1952–1958. [Google Scholar] [CrossRef] [PubMed]
- Arbuckle, J.H.; Medveczky, M.M.; Luka, J.; Hadley, S.H.; Luegmayr, A.; Ablashi, D.; Lund, T.C.; Tolar, J.; De Meirleir, K.; Montoya, J.G.; et al. The latent human herpesvirus-6A genome specifically integrates in telomeres of human chromosomes in vivo and in vitro. Proc. Natl. Acad. Sci. USA 2010, 107, 5563–5568. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohni, K.N.; Dee, A.R.; Smith, S.; Schumacher, A.J.; Weller, S.K. Efficient herpes simplex virus 1 replication requires cellular ATR pathway proteins. J. Virol. 2013, 87, 531–542. [Google Scholar] [CrossRef] [PubMed]
- Mohni, K.N.; Livingston, C.M.; Cortez, D.; Weller, S.K. ATR and ATRIP are recruited to herpes simplex virus type 1 replication compartments even though ATR signaling is disabled. J. Virol. 2010, 84, 12152–12164. [Google Scholar] [CrossRef] [PubMed]
- Edwards, T.G.; Bloom, D.C.; Fisher, C. The ATM and Rad3-Related (ATR) Protein Kinase Pathway Is Activated by Herpes Simplex Virus 1 and Required for Efficient Viral Replication. J. Virol. 2018. [Google Scholar] [CrossRef] [PubMed]
- Albright, B.S.; Kosinski, A.; Szczepaniak, R.; Cook, E.A.; Stow, N.D.; Conway, J.F.; Weller, S.K. The putative herpes simplex virus 1 chaperone protein UL32 modulates disulfide bond formation during infection. J. Virol. 2015, 89, 443–453. [Google Scholar] [CrossRef] [PubMed]
- Mohni, K.N.; Smith, S.; Dee, A.R.; Schumacher, A.J.; Weller, S.K. Herpes simplex virus type 1 single strand DNA binding protein and helicase/primase complex disable cellular ATR signaling. PLoS Pathog. 2013, 9, e1003652. [Google Scholar] [CrossRef] [PubMed]
- Wilkinson, D.E.; Weller, S.K. Herpes simplex virus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 2006, 119, 2695–2703. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lilley, C.E.; Carson, C.T.; Muotri, A.R.; Gage, F.H.; Weitzman, M.D. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 2005, 102, 5844–5849. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lilley, C.E.; Schwartz, R.A.; Weitzman, M.D. Using or abusing: Viruses and the cellular DNA damage response. Trends. Microbiol. 2007, 15, 119–126. [Google Scholar] [CrossRef] [PubMed]
- Dembowski, J.A.; Dremel, S.E.; DeLuca, N.A. 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. 2017, 13, e1006166. [Google Scholar] [CrossRef] [PubMed]
- Hollingworth, R.; Horniblow, R.D.; Forrest, C.; Stewart, G.S.; Grand, R.J. Localization of Double-Strand Break Repair Proteins to Viral Replication Compartments following Lytic Reactivation of Kaposi’s Sarcoma-Associated Herpesvirus. J. Virol. 2017. [Google Scholar] [CrossRef] [PubMed]
- Hollingworth, R.; Skalka, G.L.; Stewart, G.S.; Hislop, A.D.; Blackbourn, D.J.; Grand, R.J. Activation of DNA Damage Response Pathways during Lytic Replication of KSHV. Viruses 2015, 7, 2908–2927. [Google Scholar] [CrossRef] [PubMed]
- O’Dowd, J.M.; Zavala, A.G.; Brown, C.J.; Mori, T.; Fortunato, E.A. HCMV-infected cells maintain efficient nucleotide excision repair of the viral genome while abrogating repair of the host genome. PLoS Pathog. 2012, 8, e1003038. [Google Scholar] [CrossRef] [PubMed]
- Luo, M.H.; Rosenke, K.; Czornak, K.; Fortunato, E.A. Human cytomegalovirus disrupts both ataxia telangiectasia mutated protein (ATM)- and ATM-Rad3-related kinase-mediated DNA damage responses during lytic infection. J. Virol. 2007, 81, 1934–1950. [Google Scholar] [CrossRef] [PubMed]
- Castillo, J.P.; Frame, F.M.; Rogoff, H.A.; Pickering, M.T.; Yurochko, A.D.; Kowalik, T.F. Human cytomegalovirus IE1-72 activates ataxia telangiectasia mutated kinase and a p53/p21-mediated growth arrest response. J. Virol. 2005, 79, 11467–11475. [Google Scholar] [CrossRef] [PubMed]
- Xiaofei, E.; Pickering, M.T.; Debatis, M.; Castillo, J.; Lagadinos, A.; Wang, S.; Lu, S.; Kowalik, T.F. An E2F1-mediated DNA damage response contributes to the replication of human cytomegalovirus. PLoS Pathog. 2011, 7, e1001342. [Google Scholar] [CrossRef]
- Xiaofei, E.; Savidis, G.; Chin, C.R.; Wang, S.; Lu, S.; Brass, A.L.; Kowalik, T.F. A novel DDB2-ATM feedback loop regulates human cytomegalovirus replication. J. Virol. 2014, 88, 2279–2290. [Google Scholar]
- Xiaofei, E.; Kowalik, T.F. The DNA damage response induced by infection with human cytomegalovirus and other viruses. Viruses 2014, 6, 2155–2185. [Google Scholar]
- Spector, D.H. Human cytomegalovirus riding the cell cycle. Med. Microbiol. Immunol. 2015, 204, 409–419. [Google Scholar] [CrossRef] [PubMed]
- Trigg, B.J.; Lauer, K.B.; Fernandes Dos Santos, P.; Coleman, H.; Balmus, G.; Mansur, D.S.; Ferguson, B.J. The Non-Homologous End Joining Protein PAXX Acts to Restrict HSV-1 Infection. Viruses 2017, 9, 342. [Google Scholar] [CrossRef] [PubMed]
- Reichel, A.; Stilp, A.C.; Scherer, M.; Reuter, N.; Lukassen, S.; Kasmapour, B.; Schreiner, S.; Cicin-Sain, L.; Winterpacht, A.; Stamminger, T. Chromatin-Remodeling Factor SPOC1 Acts as a Cellular Restriction Factor against Human Cytomegalovirus by Repressing the Major Immediate Early Promoter. J. Virol. 2018. [Google Scholar] [CrossRef] [PubMed]
- Schreiner, S.; Kinkley, S.; Burck, C.; Mund, A.; Wimmer, P.; Schubert, T.; Groitl, P.; Will, H.; Dobner, T. SPOC1-mediated antiviral host cell response is antagonized early in human adenovirus type 5 infection. PLoS Pathog. 2013, 9, e1003775. [Google Scholar] [CrossRef] [PubMed]
- Mund, A.; Schubert, T.; Staege, H.; Kinkley, S.; Reumann, K.; Kriegs, M.; Fritsch, L.; Battisti, V.; Ait-Si-Ali, S.; Hoffbeck, A.S.; et al. SPOC1 modulates DNA repair by regulating key determinants of chromatin compaction and DNA damage response. Nucleic. Acids. Res. 2012, 40, 11363–11379. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jackson, S.A.; DeLuca, N.A. Relationship of herpes simplex virus genome configuration to productive and persistent infections. Proc. Natl. Acad. Sci. USA 2003, 100, 7871–7876. [Google Scholar] [CrossRef] [Green Version]
- Strang, B.L.; Stow, N.D. Circularization of the herpes simplex virus type 1 genome upon lytic infection. J. Virol. 2005, 79, 12487–12494. [Google Scholar] [CrossRef]
- Skaliter, R.; Lehman, I.R. Rolling circle DNA replication in vitro by a complex of herpes simplex virus type 1-encoded enzymes. Proc. Natl. Acad. Sci. USA 1994, 91, 10665–10669. [Google Scholar] [CrossRef]
- Skaliter, R.; Makhov, A.M.; Griffith, J.D.; Lehman, I.R. Rolling circle DNA replication by extracts of herpes simplex virus type 1-infected human cells. J. Virol. 1996, 70, 1132–1136. [Google Scholar] [Green Version]
- Zhang, X.; Efstathiou, S.; Simmons, A. Identification of novel herpes simplex virus replicative intermediates by field inversion gel electrophoresis: Implications for viral DNA amplification strategies. Virology 1994, 202, 530–539. [Google Scholar] [CrossRef]
- Severini, A.; Morgan, A.R.; Tovell, D.R.; Tyrrell, D.L. Study of the structure of replicative intermediates of HSV-1 DNA by pulsed-field gel electrophoresis. Virology 1994, 200, 428–435. [Google Scholar] [CrossRef]
- Severini, A.; Scraba, D.G.; Tyrrell, D.L. Branched structures in the intracellular DNA of herpes simplex virus type 1. J. Virol. 1996, 70, 3169–3175. [Google Scholar] [PubMed]
- Wilkinson, D.E.; Weller, S.K. The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 2003, 55, 451–458. [Google Scholar] [CrossRef] [PubMed]
- Dembowski, J.A.; DeLuca, N.A. Temporal Viral Genome-Protein Interactions Define Distinct Stages of Productive Herpesviral Infection. MBio 2018. [Google Scholar] [CrossRef] [PubMed]
- Ligasova, A.; Liboska, R.; Friedecky, D.; Micova, K.; Adam, T.; Ozdian, T.; Rosenberg, I.; Koberna, K. Dr Jekyll and Mr Hyde: A strange case of 5-ethynyl-2’-deoxyuridine and 5-ethynyl-2’-deoxycytidine. Open Biol. 2016. [Google Scholar] [CrossRef] [PubMed]
- Kohlmeier, F.; Maya-Mendoza, A.; Jackson, D.A. EdU induces DNA damage response and cell death in mESC in culture. Chromosome. Res. 2013, 21, 87–100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parkinson, J.; Lees-Miller, S.P.; Everett, R.D. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 1999, 73, 650–657. [Google Scholar] [PubMed]
- Lees-Miller, S.P.; Long, M.C.; Kilvert, M.A.; Lam, V.; Rice, S.A.; Spencer, C.A. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 1996, 70, 7471–7477. [Google Scholar] [PubMed]
- Taylor, T.J.; Knipe, D.M. Proteomics of herpes simplex virus replication compartments: Association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J. Virol. 2004, 78, 5856–5866. [Google Scholar] [CrossRef] [PubMed]
- Lilley, C.E.; Chaurushiya, M.S.; Boutell, C.; Everett, R.D.; Weitzman, M.D. The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog. 2011, 7, e1002084. [Google Scholar] [CrossRef]
- Lilley, C.E.; Chaurushiya, M.S.; Boutell, C.; Landry, S.; Suh, J.; Panier, S.; Everett, R.D.; Stewart, G.S.; Durocher, D.; Weitzman, M.D. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J. 2010, 29, 943–955. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mattiroli, F.; Vissers, J.H.; van Dijk, W.J.; Ikpa, P.; Citterio, E.; Vermeulen, W.; Marteijn, J.A.; Sixma, T.K. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 2012, 150, 1182–1195. [Google Scholar] [CrossRef] [PubMed]
- Lallemand-Breitenbach, V.; de Thé, H. PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2010. [Google Scholar] [CrossRef] [PubMed]
- Lallemand-Breitenbach, V.; de Thé, H. PML nuclear bodies: From architecture to function. Curr. Opin. Cell Biol. 2018, 52, 154–161. [Google Scholar] [CrossRef] [PubMed]
- Tavalai, N.; Stamminger, T. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta. 2008, 1783, 2207–2221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Full, F.; Hahn, A.S.; Grosskopf, A.K.; Ensser, A. Gammaherpesviral Tegument Proteins, PML-Nuclear Bodies and the Ubiquitin-Proteasome System. Viruses 2017, 9, 308. [Google Scholar] [CrossRef] [PubMed]
- Scherer, M.; Schilling, E.M.; Stamminger, T. The Human CMV IE1 Protein: An Offender of PML Nuclear Bodies. Adv. Anat. Embryol. Cell Biol. 2017, 223, 77–94. [Google Scholar] [PubMed]
- Schreiner, S.; Burck, C.; Glass, M.; Groitl, P.; Wimmer, P.; Kinkley, S.; Mund, A.; Everett, R.D.; Dobner, T. Control of human adenovirus type 5 gene expression by cellular Daxx/ATRX chromatin-associated complexes. Nucleic. Acids. Res. 2013, 41, 3532–3550. [Google Scholar] [CrossRef] [Green Version]
- Albright, E.R.; Kalejta, R.F. Canonical and Variant Forms of Histone H3 Are Deposited onto the Human Cytomegalovirus Genome during Lytic and Latent Infections. J. Virol. 2016, 90, 10309–10320. [Google Scholar] [CrossRef] [Green Version]
- Tsai, K.; Chan, L.; Gibeault, R.; Conn, K.; Dheekollu, J.; Domsic, J.; Marmorstein, R.; Schang, L.M.; Lieberman, P.M. Viral reprogramming of the Daxx histone H3.3 chaperone during early Epstein-Barr virus infection. J. Virol. 2014, 88, 14350–14363. [Google Scholar] [CrossRef] [PubMed]
- McFarlane, S.; Orr, A.; Roberts, A.P.E.; Conn, K.L.; Iliev, V.; Loney, C.; da Silva Filipe, A.; Smollett, K.; Gu, Q.; Robertson, N.; et al. The histone chaperone HIRA promotes the induction of host innate immune defences in response to HSV-1 infection. PLoS Pathog. 2019, 15, e1007667. [Google Scholar] [CrossRef] [PubMed]
- Rai, T.S.; Glass, M.; Cole, J.J.; Rather, M.I.; Marsden, M.; Neilson, M.; Brock, C.; Humphreys, I.R.; Everett, R.D.; Adams, P.D. Histone chaperone HIRA deposits histone H3.3 onto foreign viral DNA and contributes to anti-viral intrinsic immunity. Nucleic. Acids. Res. 2017, 45, 11673–11683. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, J.S.; Raja, P.; Knipe, D.M. Herpesviral ICP0 Protein Promotes Two Waves of Heterochromatin Removal on an Early Viral Promoter during Lytic Infection. MBio 2016, 7, e02007–e02015. [Google Scholar] [CrossRef] [PubMed]
- Ishov, A.M.; Stenberg, R.M.; Maul, G.G. Human cytomegalovirus immediate early interaction with host nuclear structures: Definition of an immediate transcript environment. J. Cell Biol. 1997, 138, 5–16. [Google Scholar] [CrossRef] [PubMed]
- Nitzsche, A.; Paulus, C.; Nevels, M. Temporal dynamics of cytomegalovirus chromatin assembly in productively infected human cells. J. Virol. 2008, 82, 11167–11180. [Google Scholar] [CrossRef] [PubMed]
- Woodhall, D.L.; Groves, I.J.; Reeves, M.B.; Wilkinson, G.; Sinclair, J.H. Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J. Biol. Chem. 2006, 281, 37652–37660. [Google Scholar] [CrossRef] [PubMed]
- Maul, G.G.; Ishov, A.M.; Everett, R.D. Nuclear domain 10 as preexisting potential replication start sites of herpes simplex virus type-1. Virology 1996, 217, 67–75. [Google Scholar] [CrossRef]
- Scherer, M.; Stamminger, T. Emerging Role of PML Nuclear Bodies in Innate Immune Signaling. J. Virol. 2016, 90, 5850–5854. [Google Scholar] [CrossRef] [Green Version]
- Cliffe, A.R.; Knipe, D.M. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J. Virol. 2008, 82, 12030–12038. [Google Scholar] [CrossRef]
- Herrera, F.J.; Triezenberg, S.J. VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J. Virol. 2004, 78, 9689–9696. [Google Scholar] [CrossRef]
- Maul, G.G.; Everett, R.D. 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. 1994, 75, 1223–1233. [Google Scholar] [CrossRef] [PubMed]
- Everett, R.D.; Freemont, P.; Saitoh, H.; Dasso, M.; Orr, A.; Kathoria, M.; Parkinson, J. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. J. Virol. 1998, 72, 6581–6591. [Google Scholar] [PubMed]
- Glass, M.; Everett, R.D. Components of promyelocytic leukemia nuclear bodies (ND10) act cooperatively to repress herpesvirus infection. J. Virol. 2013, 87, 2174–2185. [Google Scholar] [CrossRef] [PubMed]
- Everett, R.D.; Rechter, S.; Papior, P.; Tavalai, N.; Stamminger, T.; Orr, A. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 2006, 80, 7995–8005. [Google Scholar] [CrossRef] [PubMed]
- Boutell, C.; Cuchet-Lourenco, D.; Vanni, E.; Orr, A.; Glass, M.; McFarlane, S.; Everett, R.D. A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathog. 2011, 7, e1002245. [Google Scholar] [CrossRef] [PubMed]
- Hofmann, H.; Sindre, H.; Stamminger, T. Functional interaction between the pp71 protein of human cytomegalovirus and the PML-interacting protein human Daxx. J. Virol. 2002, 76, 5769–5783. [Google Scholar] [CrossRef] [PubMed]
- Ishov, A.M.; Vladimirova, O.V.; Maul, G.G. Daxx-mediated accumulation of human cytomegalovirus tegument protein pp71 at ND10 facilitates initiation of viral infection at these nuclear domains. J. Virol. 2002, 76, 7705–7712. [Google Scholar] [CrossRef] [PubMed]
- Korioth, F.; Maul, G.G.; Plachter, B.; Stamminger, T.; Frey, J. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp. Cell Res. 1996, 229, 155–158. [Google Scholar] [CrossRef]
- Schilling, E.M.; Scherer, M.; Reuter, N.; Schweininger, J.; Muller, Y.A.; Stamminger, T. The Human Cytomegalovirus IE1 Protein Antagonizes PML Nuclear Body-Mediated Intrinsic Immunity via the Inhibition of PML De Novo SUMOylation. J. Virol. 2017, 91, e02049-16. [Google Scholar] [CrossRef]
- Ensser, A.; Pflanz, R.; Fleckenstein, B. Primary structure of the alcelaphine herpesvirus 1 genome. J. Virol. 1997, 71, 6517–6525. [Google Scholar] [Green Version]
- Full, F.; Jungnickl, D.; Reuter, N.; Bogner, E.; Brulois, K.; Scholz, B.; Sturzl, M.; Myoung, J.; Jung, J.U.; Stamminger, T.; et al. Kaposi’s sarcoma associated herpesvirus tegument protein ORF75 is essential for viral lytic replication and plays a critical role in the antagonization of ND10-instituted intrinsic immunity. PLoS Pathog. 2014, 10, e1003863. [Google Scholar] [CrossRef] [PubMed]
- Full, F.; Reuter, N.; Zielke, K.; Stamminger, T.; Ensser, A. Herpesvirus saimiri antagonizes nuclear domain 10-instituted intrinsic immunity via an ORF3-mediated selective degradation of cellular protein Sp100. J. Virol. 2012, 86, 3541–3553. [Google Scholar] [CrossRef] [PubMed]
- Hahn, A.S.; Grosskopf, A.K.; Jungnickl, D.; Scholz, B.; Ensser, A. Viral FGARAT Homolog ORF75 of Rhesus Monkey Rhadinovirus Effects Proteasomal Degradation of the ND10 Components SP100 and PML. J. Virol. 2016, 90, 8013–8028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsai, K.; Thikmyanova, N.; Wojcechowskyj, J.A.; Delecluse, H.J.; Lieberman, P.M. EBV tegument protein BNRF1 disrupts DAXX-ATRX to activate viral early gene transcription. PLoS Pathog. 2011, 7, e1002376. [Google Scholar] [CrossRef] [PubMed]
- He, S.; Zhao, J.; Song, S.; He, X.; Minassian, A.; Zhou, Y.; Zhang, J.; Brulois, K.; Wang, Y.; Cabo, J.; et al. Viral pseudo-enzymes activate RIG-I via deamidation to evade cytokine production. Mol. Cell 2015, 58, 134–146. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.; Li, J.; Xu, S.; Feng, P. Emerging Roles of Protein Deamidation in Innate Immune Signaling. J. Virol. 2016, 90, 4262–4268. [Google Scholar] [CrossRef] [Green Version]
- Zhao, J.; Zeng, Y.; Xu, S.; Chen, J.; Shen, G.; Yu, C.; Knipe, D.; Yuan, W.; Peng, J.; Xu, W.; et al. A Viral Deamidase Targets the Helicase Domain of RIG-I to Block RNA-Induced Activation. Cell Host Microbe. 2016, 20, 770–784. [Google Scholar] [CrossRef] [Green Version]
- Clynes, D.; Jelinska, C.; Xella, B.; Ayyub, H.; Scott, C.; Mitson, M.; Taylor, S.; Higgs, D.R.; Gibbons, R.J. Suppression of the alternative lengthening of telomere pathway by the chromatin remodelling factor ATRX. Nat. Commun. 2015. [Google Scholar] [CrossRef]
- Wang, Z.; Deng, Z.; Tutton, S.; Lieberman, P.M. The Telomeric Response to Viral Infection. Viruses 2017, 9, 218. [Google Scholar] [CrossRef]
- Merkl, P.E.; Orzalli, M.H.; Knipe, D.M. Mechanisms of Host IFI16, PML, and Daxx Protein Restriction of Herpes Simplex Virus 1 Replication. J. Virol. 2018. [Google Scholar] [CrossRef]
- Dunphy, G.; Flannery, S.M.; Almine, J.F.; Connolly, D.J.; Paulus, C.; Jonsson, K.L.; Jakobsen, M.R.; Nevels, M.M.; Bowie, A.G.; Unterholzner, L. Non-canonical Activation of the DNA Sensing Adaptor STING by ATM and IFI16 Mediates NF-kappaB Signaling after Nuclear DNA Damage. Mol. Cell 2018, 71, 745–760. [Google Scholar] [CrossRef] [PubMed]
- Shire, K.; Wong, A.I.; Tatham, M.H.; Anderson, O.F.; Ripsman, D.; Gulstene, S.; Moffat, J.; Hay, R.T.; Frappier, L. Identification of RNF168 as a PML nuclear body regulator. J. Cell Sci. 2016, 129, 580–591. [Google Scholar] [CrossRef] [PubMed]
- Schierling, K.; Stamminger, T.; Mertens, T.; Winkler, M. Human cytomegalovirus tegument proteins ppUL82 (pp71) and ppUL35 interact and cooperatively activate the major immediate-early enhancer. J. Virol. 2004, 78, 9512–9523. [Google Scholar] [CrossRef] [PubMed]
- Salsman, J.; Wang, X.; Frappier, L. Nuclear body formation and PML body remodeling by the human cytomegalovirus protein UL35. Virology 2011, 414, 119–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salsman, J.; Jagannathan, M.; Paladino, P.; Chan, P.K.; Dellaire, G.; Raught, B.; Frappier, L. Proteomic profiling of the human cytomegalovirus UL35 gene products reveals a role for UL35 in the DNA repair response. J. Virol. 2012, 86, 806–820. [Google Scholar] [CrossRef] [PubMed]
- Schilling, M.; Bulli, L.; Weigang, S.; Graf, L.; Naumann, S.; Patzina, C.; Wagner, V.; Bauersfeld, L.; Goujon, C.; Hengel, H.; et al. Human MxB Protein Is a Pan-herpesvirus Restriction Factor. J. Virol. 2018. [Google Scholar] [CrossRef] [PubMed]
- Kane, M.; Yadav, S.S.; Bitzegeio, J.; Kutluay, S.B.; Zang, T.; Wilson, S.J.; Schoggins, J.W.; Rice, C.M.; Yamashita, M.; Hatziioannou, T.; et al. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 2013, 502, 563–566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Goujon, C.; Moncorge, O.; Bauby, H.; Doyle, T.; Ward, C.C.; Schaller, T.; Hue, S.; Barclay, W.S.; Schulz, R.; Malim, M.H. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 2013, 502, 559–562. [Google Scholar] [CrossRef]
- Crameri, M.; Bauer, M.; Caduff, N.; Walker, R.; Steiner, F.; Franzoso, F.D.; Gujer, C.; Boucke, K.; Kucera, T.; Zbinden, A.; et al. MxB is an interferon-induced restriction factor of human herpesviruses. Nat. Commun. 2018. [Google Scholar] [CrossRef]
- Jaguva Vasudevan, A.A.; Bahr, A.; Grothmann, R.; Singer, A.; Haussinger, D.; Zimmermann, A.; Munk, C. MXB inhibits murine cytomegalovirus. Virology 2018, 522, 158–167. [Google Scholar] [CrossRef]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Full, F.; Ensser, A. Early Nuclear Events after Herpesviral Infection. J. Clin. Med. 2019, 8, 1408. https://doi.org/10.3390/jcm8091408
Full F, Ensser A. Early Nuclear Events after Herpesviral Infection. Journal of Clinical Medicine. 2019; 8(9):1408. https://doi.org/10.3390/jcm8091408
Chicago/Turabian StyleFull, Florian, and Armin Ensser. 2019. "Early Nuclear Events after Herpesviral Infection" Journal of Clinical Medicine 8, no. 9: 1408. https://doi.org/10.3390/jcm8091408