The interplay between viral molecular mimicry and host chromatin dynamics

References

• Luger K, Mader AW, Richmond RK, et al. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 1997;389(6648):251–6.
   PubMed Web of Science ®Google Scholar
• Song F, Chen P, Sun D, et al. Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science. 2014;344(6182):376–380. DOI:10.1126/science.1251413
   PubMed Web of Science ®Google Scholar
• Widom J. Toward a unified model of chromatin folding. Ann Rev Biophys Biophys Chem. 1989;18(1):365–395.
   PubMedGoogle Scholar
• Li G, Reinberg D. Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev. 2011;21(2):175–186.
   PubMed Web of Science ®Google Scholar
• Martire S, Banaszynski LA. The roles of histone variants in fine-tuning chromatin organization and function. Nat Rev Mol Cell Biol. 2020;21(9):522–541.
   PubMed Web of Science ®Google Scholar
• Huang Y, Dai Y, Zhou Z. Mechanistic and structural insights into histone H2A–H2B chaperone in chromatin regulation. Biochem J. 2020;477(17):3367–3386.
   PubMed Web of Science ®Google Scholar
• Millan-Zambrano G, Burton A, Bannister AJ, et al. Histone post-translational modifications — cause and consequence of genome function. Nat Rev Genet. 2022;23(9):563–580.
   PubMed Web of Science ®Google Scholar
• Sultana S, Zarreen F, Chakraborty S. Insights into the roles of histone chaperones in nucleosome assembly and disassembly in virus infection. Virus Res. 2021;297:198395.
   PubMed Web of Science ®Google Scholar
• Tarakhovsky A, Prinjha RK. Drawing on disorder: how viruses use histone mimicry to their advantage. J Exp Med. 2018;215(7):1777–1787.
   PubMed Web of Science ®Google Scholar
• Catalano CE. Morais MC.Viral genome packaging machines: structure and enzymology. Enzymes. 2021;50:369–413.
   PubMedGoogle Scholar
• Talbert PB, Armache KJ, Henikoff S. Viral histones: pickpocket’s prize or primordial progenitor? Epigenetics Chromatin. 2022 May 28;15(1):21.
   PubMed Web of Science ®Google Scholar
• Hepat R, Song JJ, Lee D, et al. A viral histone h4 joins to eukaryotic nucleosomes and alters host gene expression. J Virol. 2013;87(20):11223–11230.
   PubMed Web of Science ®Google Scholar
• Liu Y, Bisio H, Toner CM, et al. Virus-encoded histone doublets are essential and form nucleosome-like structures. Cell. 2021;184(16):4237–50 e19. DOI:10.1016/j.cell.2021.06.032
   PubMed Web of Science ®Google Scholar
• Valencia-Sánchez MI, Abini-Agbomson S, Wang M, et al. The structure of a virus-encoded nucleosome. Nat Struct Mol Biol. 2021;28(5):413–417. DOI:10.1038/s41594-021-00585-7
   PubMed Web of Science ®Google Scholar
• Bryson TD, De Ioannes P, Valencia-Sánchez MI, et al. A giant virus genome is densely packaged by stable nucleosomes within virions. Mol Cell. 2022;82(23):4458–4470. DOI:10.1016/j.molcel.2022.10.020
   PubMed Web of Science ®Google Scholar
• Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403(6765):41–45.
   PubMed Web of Science ®Google Scholar
• Tarakhovsky A. Logic of the inflammation-associated transcriptional response. Adv Immunol. 2013;119:107–133.
   PubMed Web of Science ®Google Scholar
• Qin S, Liu Y, Tempel W, et al. Structural basis for histone mimicry and hijacking of host proteins by influenza virus protein NS1. Nat Commun. 2014;5(1):3952. DOI:10.1038/ncomms4952
   PubMedGoogle Scholar
• Chen J, Horton J, Sagum C, et al. Histone H3 N-terminal mimicry drives a novel network of methyl-effector interactions. Biochem J. 2021;478(10):1943–1958.
   PubMed Web of Science ®Google Scholar
• Simic R, Lindstrom DL, Tran HG, et al. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. Embo J. 2003;22(8):1846–1856. DOI:10.1093/emboj/cdg179
   PubMed Web of Science ®Google Scholar
• Abeywickrama-Samarakoon N, Cortay JC, Sureau C, et al. Hepatitis Delta Virus histone mimicry drives the recruitment of chromatin remodelers for viral RNA replication. Nat Commun. 2020;11(1):419. DOI:10.1038/s41467-020-14299-9
   PubMed Web of Science ®Google Scholar
• Schaefer U, Ho JS, Prinjha RK, et al. The “histone mimicry” by pathogens. Cold Spring Harb Symp Quant Biol. 2013;78(0):81–90.
   PubMedGoogle Scholar
• Chua MA, Schmid S, Perez JT, et al. Influenza a virus utilizes suboptimal splicing to coordinate the timing of infection. Cell Rep. 2013;3(1):23–29.
   PubMed Web of Science ®Google Scholar
• Robinson CM, Singh G, Lee JY, et al. Molecular evolution of human adenoviruses. Sci Rep. 2013;3(1):1812. DOI:10.1038/srep01812
   PubMedGoogle Scholar
• Avgousti DC, Herrmann C, Kulej K, et al. A core viral protein binds host nucleosomes to sequester immune danger signals. Nature. 2016;535(7610):173–177. DOI:10.1038/nature18317
   PubMed Web of Science ®Google Scholar
• Kee J, Thudium S, Renner DM, et al. SARS-CoV-2 disrupts host epigenetic regulation via histone mimicry. Nature. 2022;610(7931):381–388. DOI:10.1038/s41586-022-05282-z
   PubMed Web of Science ®Google Scholar
• Dai L, Xiao X, Pan L, et al. Recognition of the inherently unstable H2A nucleosome by Swc2 is a major determinant for unidirectional H2A.Z exchange. Cell Rep. 2021;35(8):109183. DOI:10.1016/j.celrep.2021.109183
   PubMed Web of Science ®Google Scholar
• McGinty RK, Tan S. Principles of nucleosome recognition by chromatin factors and enzymes. Curr Opin Struct Biol. 2021;71:16–26.
   PubMed Web of Science ®Google Scholar
• Shi L, Huang L, Long H, et al. Structural basis of nucleosomal H4K20 methylation by methyltransferase SET8. FASEB J. 2022;36(6):e22338.
   PubMed Web of Science ®Google Scholar
• Barbera AJ, Chodaparambil JV, Kelley-Clarke B, et al. The nucleosomal surface as a docking station for Kaposi’s sarcoma herpesvirus LANA. Science. 2006;311:856–861.
   PubMed Web of Science ®Google Scholar
• Mucke K, Paulus C, Bernhardt K, et al. Human cytomegalovirus major immediate early 1 protein targets host chromosomes by docking to the acidic pocket on the nucleosome surface. J Virol. 2014;88(2):1228–1248. DOI:10.1128/JVI.02606-13
   PubMed Web of Science ®Google Scholar
• Fang Q, Chen P, Wang M, et al. Human cytomegalovirus IE1 protein alters the higher-order chromatin structure by targeting the acidic patch of the nucleosome. Elife. 2016;5. DOI:10.7554/eLife.11911
   Web of Science ®Google Scholar
• Kotlar RM, Jones ND, Senavirathne G, et al. Retroviral prototype foamy virus intasome binding to a nucleosome target does not determine integration efficiency. J Biol Chem. 2021;296:100550.
   PubMed Web of Science ®Google Scholar
• Lesbats P, Serrao E, Maskell DP, et al. Structural basis for spumavirus GAG tethering to chromatin. Proc Natl Acad Sci U S A. 2017;114(21):5509–5514. DOI:10.1073/pnas.1621159114
   PubMed Web of Science ®Google Scholar
• McGinty RK, Tan S. Nucleosome structure and function. Chem Rev. 2015;115(6):2255–2273.
   PubMed Web of Science ®Google Scholar
• Vayda ME, Rogers AE, Flint SJ. The structure of nucleoprotein cores released from adenovirions. Nucleic Acids Res. 1983;11(2):441–460.
   PubMed Web of Science ®Google Scholar
• Karen KA, Hearing P. Adenovirus core protein VII protects the viral genome from a DNA damage response at early times after infection. J Virol. 2011;85(9):4135–4142.
   PubMed Web of Science ®Google Scholar
• Lynch KL, Dillon MR, Bat-Erdene M, et al. A viral histone-like protein exploits antagonism between linker histones and HMGB proteins to obstruct the cell cycle. Curr Biol. 2021;31(23):5227–5237. DOI:10.1016/j.cub.2021.09.050
   PubMed Web of Science ®Google Scholar
• Chodaparambil JV, Barbera AJ, Lu X, et al. A charged and contoured surface on the nucleosome regulates chromatin compaction. Nat Struct Mol Biol. 2007;14(11):1105–1107.
   PubMed Web of Science ®Google Scholar
• Chen J, Lu Z, Gong W, et al. Epstein-Barr virus protein BKRF4 restricts nucleosome assembly to suppress host antiviral responses. Proc Natl Acad Sci U S A. 2022;119(37):e2203782119. DOI:10.1073/pnas.2203782119
   PubMed Web of Science ®Google Scholar
• Ho TH, Sitz J, Shen Q, et al. A screen for Epstein-Barr virus proteins that inhibit the DNA damage response reveals a novel histone binding protein. J Virol. 2018;92(14).
   Web of Science ®Google Scholar
• Wang HC, Wang HC, Ko TP, et al. White spot syndrome virus protein ICP11: a histone-binding DNA mimic that disrupts nucleosome assembly. Proc Natl Acad Sci U S A. 2008;105(52):20758–20763. DOI:10.1073/pnas.0811233106
   PubMed Web of Science ®Google Scholar
• Gibson BA, Doolittle LK, Schneider MWG, et al. Organization of chromatin by intrinsic and regulated phase separation. Cell. 2019;179(2):470–84 e21. DOI:10.1016/j.cell.2019.08.037
   PubMed Web of Science ®Google Scholar
• Boija A, Klein IA, Sabari BR, et al. Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell. 2018;175:1842–55 e16.
   PubMed Web of Science ®Google Scholar
• Peng Q, Wang L, Qin Z, et al. Phase separation of Epstein-Barr virus EBNA2 and its coactivator EBNALP controls gene expression. J Virol. 2020;94(7):e01771–19.
   PubMed Web of Science ®Google Scholar
• Yang Y, Ye X, Dai R, et al. Phase separation of Epstein-Barr virus EBNA2 protein reorganizes chromatin topology for epigenetic regulation. Commun Biol. 2021;4(1):967. DOI:10.1038/s42003-021-02501-7
   PubMed Web of Science ®Google Scholar
• Xu G, Liu C, Zhou S, et al. Viral tegument proteins restrict Cgas-DNA phase separation to mediate immune evasion. Mol Cell. 2021;81(13):2823–2837. DOI:10.1016/j.molcel.2021.05.002
   PubMed Web of Science ®Google Scholar
• Bhowmik D, Du M, Tian Y, et al. Cooperative DNA binding mediated by KicGAS/ORF52 oligomerization allows inhibition of DNA-induced phase separation and activation of cGAS. Nucleic Acids Res. 2021;49(16):9389–9403. DOI:10.1093/nar/gkab689
   PubMed Web of Science ®Google Scholar
• Ma X, Chen T, Peng Z, et al. Histone chaperone CAF-1 promotes HIV-1 latency by leading the formation of phase-separated suppressive nuclear bodies. Embo J. 2021;40(10).
   Web of Science ®Google Scholar
• Wu Y, Ma L, Cai S, et al. RNA-induced liquid phase separation of SARS-CoV-2 nucleocapsid protein facilitates NF-κB hyper-activation and inflammation. Signal Transduct Target Ther. 2021;6(1):167. DOI:10.1038/s41392-021-00575-7
   PubMed Web of Science ®Google Scholar
• Wang S, Dai T, Qin Z, et al. Targeting liquid-liquid phase separation of SARS-CoV-2 nucleocapsid protein promotes innate antiviral immunity by elevating MAVS activity. Nat Cell Biol. 2021;23(7):718–732. DOI:10.1038/s41556-021-00710-0
   PubMed Web of Science ®Google Scholar
• Majumder K, Morales AJ. Utilization of host cell chromosome conformation by viral pathogens: knowing when to hold and when to fold. Front Immunol. 2021;12:633762.
   PubMed Web of Science ®Google Scholar