The Interplay between Viruses and Host DNA Sensors
Language English Country Switzerland Media electronic
Document type Journal Article, Review, Research Support, Non-U.S. Gov't
PubMed
35458396
PubMed Central
PMC9027975
DOI
10.3390/v14040666
PII: v14040666
Knihovny.cz E-resources
- Keywords
- DNA sensing, DNA viruses, IFI16, IFN, STING, TLR9, cGAS, inflammasome, innate immunity, p204/Ifi-204,
- MeSH
- DNA, Viral metabolism MeSH
- Herpesviridae * genetics metabolism MeSH
- DNA Virus Infections * MeSH
- Humans MeSH
- Polyomavirus * genetics MeSH
- Immunity, Innate MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- DNA, Viral MeSH
DNA virus infections are often lifelong and can cause serious diseases in their hosts. Their recognition by the sensors of the innate immune system represents the front line of host defence. Understanding the molecular mechanisms of innate immunity responses is an important prerequisite for the design of effective antivirotics. This review focuses on the present state of knowledge surrounding the mechanisms of viral DNA genome sensing and the main induced pathways of innate immunity responses. The studies that have been performed to date indicate that herpesviruses, adenoviruses, and polyomaviruses are sensed by various DNA sensors. In non-immune cells, STING pathways have been shown to be activated by cGAS, IFI16, DDX41, or DNA-PK. The activation of TLR9 has mainly been described in pDCs and in other immune cells. Importantly, studies on herpesviruses have unveiled novel participants (BRCA1, H2B, or DNA-PK) in the IFI16 sensing pathway. Polyomavirus studies have revealed that, in addition to viral DNA, micronuclei are released into the cytosol due to genotoxic stress. Papillomaviruses, HBV, and HIV have been shown to evade DNA sensing by sophisticated intracellular trafficking, unique cell tropism, and viral or cellular protein actions that prevent or block DNA sensing. Further research is required to fully understand the interplay between viruses and DNA sensors.
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Saxena M., Yeretssian G. NOD-Like Receptors: Master Regulators of Inflammation and Cancer. Front. Immunol. 2014;5:327. doi: 10.3389/fimmu.2014.00327. PubMed DOI PMC
Drouin M., Saenz J., Chiffoleau E. C-Type Lectin-Like Receptors: Head or Tail in Cell Death Immunity. Front. Immunol. 2020;11:251. doi: 10.3389/fimmu.2020.00251. PubMed DOI PMC
Kawai T., Akira S. The Roles of TLRs, RLRs and NLRs in Pathogen Recognition. Int. Immunol. 2009;21:317–337. doi: 10.1093/intimm/dxp017. PubMed DOI PMC
Oliveira Mann C.C., Hornung V. Molecular Mechanisms of Nonself Nucleic Acid Recognition by the Innate Immune System. Eur. J. Immunol. 2021;51:1897–1910. doi: 10.1002/eji.202049116. PubMed DOI
Rehwinkel J., Gack M.U. RIG-I-like Receptors: Their Regulation and Roles in RNA Sensing. Nat. Rev. Immunol. 2020;20:537–551. doi: 10.1038/s41577-020-0288-3. PubMed DOI PMC
Caneparo V., Landolfo S., Gariglio M., De Andrea M. The Absent in Melanoma 2-Like Receptor IFN-Inducible Protein 16 as an Inflammasome Regulator in Systemic Lupus Erythematosus: The Dark Side of Sensing Microbes. Front. Immunol. 2018;9:1180. doi: 10.3389/fimmu.2018.01180. PubMed DOI PMC
Bürckstümmer T., Baumann C., Blüml S., Dixit E., Dürnberger G., Jahn H., Planyavsky M., Bilban M., Colinge J., Bennett K.L., et al. An Orthogonal Proteomic-Genomic Screen Identifies AIM2 as a Cytoplasmic DNA Sensor for the Inflammasome. Nat. Immunol. 2009;10:266–272. doi: 10.1038/ni.1702. PubMed DOI
Howard T.R., Crow M.S., Greco T.M., Lum K.K., Li T., Cristea I.M. The DNA Sensor IFIX Drives Proteome Alterations To Mobilize Nuclear and Cytoplasmic Antiviral Responses, with Its Acetylation Acting as a Localization Toggle. mSystems. 2021;6:e00397-21. doi: 10.1128/mSystems.00397-21. PubMed DOI PMC
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. doi: 10.1038/ni.1932. PubMed DOI PMC
Diner B.A., Li T., Greco T.M., Crow M.S., Fuesler J.A., Wang J., Cristea I.M. The Functional Interactome of PYHIN Immune Regulators Reveals IFIX Is a Sensor of Viral DNA. Mol. Syst. Biol. 2015;11:787. doi: 10.15252/msb.20145808. PubMed DOI PMC
Chen W., Yu S.-X., Zhou F.-H., Zhang X.-J., Gao W.-Y., Li K.-Y., Liu Z.-Z., Han W.-Y., Yang Y.-J. DNA Sensor IFI204 Contributes to Host Defense Against Staphylococcus Aureus Infection in Mice. Front. Immunol. 2019;10:474. doi: 10.3389/fimmu.2019.00474. PubMed DOI PMC
Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., et al. DAI (DLM-1/ZBP1) Is a Cytosolic DNA Sensor and an Activator of Innate Immune Response. Nature. 2007;448:501–505. doi: 10.1038/nature06013. PubMed DOI
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. doi: 10.1126/science.1229963. PubMed DOI PMC
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. doi: 10.1126/science.1232458. PubMed DOI PMC
Zhang Z., Yuan B., Bao M., Lu N., Kim T., Liu Y.-J. The Helicase DDX41 Senses Intracellular DNA Mediated by the Adaptor STING in Dendritic Cells. Nat. Immunol. 2011;12:959–965. doi: 10.1038/ni.2091. PubMed DOI PMC
Kim T., Pazhoor S., Bao M., Zhang Z., Hanabuchi S., Facchinetti V., Bover L., Plumas J., Chaperot L., Qin J., et al. Aspartate-Glutamate-Alanine-Histidine Box Motif (DEAH)/RNA Helicase A Helicases Sense Microbial DNA in Human Plasmacytoid Dendritic Cells. Proc. Natl. Acad. Sci. USA. 2010;107:15181–15186. doi: 10.1073/pnas.1006539107. PubMed DOI PMC
Ng Y.C., Chung W.-C., Kang H.-R., Cho H.-J., Park E.-B., Kang S.-J., Song M.J. A DNA-Sensing–Independent Role of a Nuclear RNA Helicase, DHX9, in Stimulation of NF-ΚB–Mediated Innate Immunity against DNA Virus Infection. Nucleic Acids Res. 2018;46:9011–9026. doi: 10.1093/nar/gky742. PubMed DOI PMC
Chiu Y.-H., MacMillan J.B., Chen Z.J. RNA Polymerase III Detects Cytosolic DNA and Induces Type I Interferons through the RIG-I Pathway. Cell. 2009;138:576–591. doi: 10.1016/j.cell.2009.06.015. PubMed DOI PMC
Kondo T., Kobayashi J., Saitoh T., Maruyama K., Ishii K.J., Barber G.N., Komatsu K., Akira S., Kawai T. DNA Damage Sensor MRE11 Recognizes Cytosolic Double-Stranded DNA and Induces Type I Interferon by Regulating STING Trafficking. Proc. Natl. Acad. Sci. USA. 2013;110:2969–2974. doi: 10.1073/pnas.1222694110. PubMed DOI PMC
Ferguson B.J., Mansur D.S., Peters N.E., Ren H., Smith G.L. DNA-PK Is a DNA Sensor for IRF-3-Dependent Innate Immunity. eLife. 2012;1:e00047. doi: 10.7554/eLife.00047. PubMed DOI PMC
Sui H., Hao M., Chang W., Imamichi T. The Role of Ku70 as a Cytosolic DNA Sensor in Innate Immunity and Beyond. Front. Cell. Infect. Microbiol. 2021;11:761983. doi: 10.3389/fcimb.2021.761983. PubMed DOI PMC
Johnstone R.W., Wei W., Greenway A., Trapani J.A. Functional Interaction between P53 and the Interferon-Inducible Nucleoprotein IFI 16. Oncogene. 2000;19:6033–6042. doi: 10.1038/sj.onc.1204005. PubMed DOI
Johnstone R.W., Kerry J.A., Trapani J.A. The Human Interferon-Inducible Protein, IFI 16, Is a Repressor of Transcription. J. Biol. Chem. 1998;273:17172–17177. doi: 10.1074/jbc.273.27.17172. PubMed DOI
Roy A., Ghosh A., Kumar B., Chandran B. IFI16, a Nuclear Innate Immune DNA Sensor, Mediates Epigenetic Silencing of Herpesvirus Genomes by Its Association with H3K9 Methyltransferases SUV39H1 and GLP. eLife. 2019;8:e49500. doi: 10.7554/eLife.49500. PubMed DOI PMC
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. doi: 10.1371/journal.ppat.1004503. PubMed DOI PMC
Jiang H., Xue X., Panda S., Kawale A., Hooy R.M., Liang F., Sohn J., Sung P., Gekara N.O. Chromatin-bound cGAS Is an Inhibitor of DNA Repair and Hence Accelerates Genome Destabilization and Cell Death. EMBO J. 2019;38:e102718. doi: 10.15252/embj.2019102718. PubMed DOI PMC
Liu H., Zhang H., Wu X., Ma D., Wu J., Wang L., Jiang Y., Fei Y., Zhu C., Tan R., et al. Nuclear CGAS Suppresses DNA Repair and Promotes Tumorigenesis. Nature. 2018;563:131–136. doi: 10.1038/s41586-018-0629-6. PubMed DOI
Zierhut C., Yamaguchi N., Paredes M., Luo J.-D., Carroll T., Funabiki H. The Cytoplasmic DNA Sensor CGAS Promotes Mitotic Cell Death. Cell. 2019;178:302–315.e23. doi: 10.1016/j.cell.2019.05.035. PubMed DOI PMC
Cui S., Yu Q., Chu L., Cui Y., Ding M., Wang Q., Wang H., Chen Y., Liu X., Wang C. Nuclear CGAS Functions Non-Canonically to Enhance Antiviral Immunity via Recruiting Methyltransferase Prmt5. Cell Rep. 2020;33:108490. doi: 10.1016/j.celrep.2020.108490. PubMed DOI
Ablasser A., Goldeck M., Cavlar T., Deimling T., Witte G., Röhl I., Hopfner K.-P., Ludwig J., Hornung V. CGAS Produces a 2′-5′-Linked Cyclic Dinucleotide Second Messenger That Activates STING. Nature. 2013;498:380–384. doi: 10.1038/nature12306. PubMed DOI PMC
Sui H., Zhou M., Imamichi H., Jiao X., Sherman B.T., Lane H.C., Imamichi T. STING Is an Essential Mediator of the Ku70-Mediated Production of IFN-Λ1 in Response to Exogenous DNA. Sci. Signal. 2017;10:eaah5054. doi: 10.1126/scisignal.aah5054. PubMed DOI
Burleigh K., Maltbaek J.H., Cambier S., Green R., Gale M., James R.C., Stetson D.B. Human DNA-PK Activates a STING-Independent DNA Sensing Pathway. Sci. Immunol. 2020;5:eaba4219. doi: 10.1126/sciimmunol.aba4219. PubMed DOI PMC
Yang P., An H., Liu X., Wen M., Zheng Y., Rui Y., Cao X. The Cytosolic Nucleic Acid Sensor LRRFIP1 Mediates the Production of Type I Interferon via a β-Catenin-Dependent Pathway. Nat. Immunol. 2010;11:487–494. doi: 10.1038/ni.1876. PubMed DOI
Liu Y., Zou Z., Zhu B., Hu Z., Zeng P., Wu L. LRRFIP1 Inhibits Hepatitis C Virus Replication by Inducing Type I Interferon in Hepatocytes. Hepat. Mon. 2015;15:e28473. doi: 10.5812/hepatmon.15(5)2015.28473. PubMed DOI PMC
Rathinam V.A.K., Sharma S., Fitzgerald K.A. Catenin’ on to Nucleic Acid Sensing. Nat. Immunol. 2010;11:466–468. doi: 10.1038/ni0610-466. PubMed DOI
Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., et al. A Toll-like Receptor Recognizes Bacterial DNA. Nature. 2000;408:740–745. doi: 10.1038/35047123. PubMed DOI
Kadowaki N., Ho S., Antonenko S., de Waal Malefyt R., Kastelein R.A., Bazan F., Liu Y.-J. Subsets of Human Dendritic Cell Precursors Express Different Toll-like Receptors and Respond to Different Microbial Antigens. J. Exp. Med. 2001;194:863–870. doi: 10.1084/jem.194.6.863. PubMed DOI PMC
Hornung V., Rothenfusser S., Britsch S., Krug A., Jahrsdörfer B., Giese T., Endres S., Hartmann G. Quantitative Expression of Toll-Like Receptor 1–10 MRNA in Cellular Subsets of Human Peripheral Blood Mononuclear Cells and Sensitivity to CpG Oligodeoxynucleotides. J. Immunol. 2002;168:4531–4537. doi: 10.4049/jimmunol.168.9.4531. PubMed DOI
Botos I., Segal D.M., Davies D.R. The Structural Biology of Toll-like Receptors. Structure. 2011;19:447–459. doi: 10.1016/j.str.2011.02.004. PubMed DOI PMC
Avalos A.M., Kirak O., Oelkers J.M., Pils M.C., Kim Y.-M., Ottinger M., Jaenisch R., Ploegh H.L., Brinkmann M.M. Cell-Specific TLR9 Trafficking in Primary APCs of Transgenic TLR9-GFP Mice. J. Immunol. 2013;190:695–702. doi: 10.4049/jimmunol.1202342. PubMed DOI PMC
Chockalingam A., Brooks J.C., Cameron J.L., Blum L.K., Leifer C.A. TLR9 Traffics through the Golgi Complex to Localize to Endolysosomes and Respond to CpG DNA. Immunol. Cell Biol. 2009;87:209–217. doi: 10.1038/icb.2008.101. PubMed DOI PMC
Kagan J.C., Barton G.M. Emerging Principles Governing Signal Transduction by Pattern-Recognition Receptors. Cold Spring Harb. Perspect. Biol. 2014;7:a016253. doi: 10.1101/cshperspect.a016253. PubMed DOI PMC
Kumar H., Kawai T., Akira S. Toll-like Receptors and Innate Immunity. Biochem. Biophys. Res. Commun. 2009;388:621–625. doi: 10.1016/j.bbrc.2009.08.062. PubMed DOI
Ohto U., Ishida H., Shibata T., Sato R., Miyake K., Shimizu T. Toll-like Receptor 9 Contains Two DNA Binding Sites That Function Cooperatively to Promote Receptor Dimerization and Activation. Immunity. 2018;48:649–658.e4. doi: 10.1016/j.immuni.2018.03.013. PubMed DOI
Latz E., Verma A., Visintin A., Gong M., Sirois C.M., Klein D.C.G., Monks B.G., McKnight C.J., Lamphier M.S., Duprex W.P., et al. Ligand-Induced Conformational Changes Allosterically Activate Toll-like Receptor 9. Nat. Immunol. 2007;8:772–779. doi: 10.1038/ni1479. PubMed DOI
Häcker H., Redecke V., Blagoev B., Kratchmarova I., Hsu L.-C., Wang G.G., Kamps M.P., Raz E., Wagner H., Häcker G., et al. Specificity in Toll-like Receptor Signalling through Distinct Effector Functions of TRAF3 and TRAF6. Nature. 2006;439:204–207. doi: 10.1038/nature04369. PubMed DOI
Kawai T., Sato S., Ishii K.J., Coban C., Hemmi H., Yamamoto M., Terai K., Matsuda M., Inoue J., Uematsu S., et al. Interferon-α Induction through Toll-like Receptors Involves a Direct Interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 2004;5:1061–1068. doi: 10.1038/ni1118. PubMed DOI
Marongiu L., Gornati L., Artuso I., Zanoni I., Granucci F. Below the Surface: The Inner Lives of TLR4 and TLR9. J. Leukoc. Biol. 2019;106:147–160. doi: 10.1002/JLB.3MIR1218-483RR. PubMed DOI PMC
Hoshino K., Sasaki I., Sugiyama T., Yano T., Yamazaki C., Yasui T., Kikutani H., Kaisho T. Cutting Edge: Critical Role of IκB Kinase α in TLR7/9-Induced Type I IFN Production by Conventional Dendritic Cells. J.I. 2010;184:3341–3345. doi: 10.4049/jimmunol.0901648. PubMed DOI
Schmitz F., Heit A., Guggemoos S., Krug A., Mages J., Schiemann M., Adler H., Drexler I., Haas T., Lang R., et al. Interferon-Regulatory-Factor 1 Controls Toll-like Receptor 9-Mediated IFN-β Production in Myeloid Dendritic Cells. Eur. J. Immunol. 2007;37:315–327. doi: 10.1002/eji.200636767. PubMed DOI
Cridland J.A., Curley E.Z., Wykes M.N., Schroder K., Sweet M.J., Roberts T.L., Ragan M.A., Kassahn K.S., Stacey K.J. The Mammalian PYHIN Gene Family: Phylogeny, Evolution and Expression. BMC Evol. Biol. 2012;12:140. doi: 10.1186/1471-2148-12-140. PubMed DOI PMC
Zhao H., Gonzalezgugel E., Cheng L., Richbourgh B., Nie L., Liu C. The Roles of Interferon-Inducible P200 Family Members IFI16 and P204 in Innate Immune Responses, Cell Differentiation and Proliferation. Genes Dis. 2015;2:46–56. doi: 10.1016/j.gendis.2014.10.003. PubMed DOI PMC
Gray E.E., Winship D., Snyder J.M., Child S.J., Geballe A.P., Stetson D.B. The AIM2-like Receptors Are Dispensable for the Interferon Response to Intracellular DNA. Immunity. 2016;45:255–266. doi: 10.1016/j.immuni.2016.06.015. PubMed DOI PMC
Nakaya Y., Lilue J., Stavrou S., Moran E.A., Ross S.R. AIM2-Like Receptors Positively and Negatively Regulate the Interferon Response Induced by Cytosolic DNA. mBio. 2017;8:e00944-17. doi: 10.1128/mBio.00944-17. PubMed DOI PMC
Shaw N., Liu Z.-J. Role of the HIN Domain in Regulation of Innate Immune Responses. Mol. Cell. Biol. 2014;34:2–15. doi: 10.1128/MCB.00857-13. PubMed DOI PMC
Morrone S.R., Wang T., Constantoulakis L.M., Hooy R.M., Delannoy M.J., Sohn J. Cooperative Assembly of IFI16 Filaments on DsDNA Provides Insights into Host Defense Strategy. Proc. Natl. Acad. Sci. USA. 2014;111:E62–E71. doi: 10.1073/pnas.1313577111. PubMed DOI PMC
Jin T., Perry A., Jiang J., Smith P., Curry J.A., Unterholzner L., Jiang Z., Horvath G., Rathinam V.A., Johnstone R.W., et al. Structures of the HIN Domain:DNA Complexes Reveal Ligand Binding and Activation Mechanisms of the AIM2 Inflammasome and IFI16 Receptor. Immunity. 2012;36:561–571. doi: 10.1016/j.immuni.2012.02.014. PubMed DOI PMC
Jin T., Perry A., Smith P., Jiang J., Xiao T.S. Structure of the Absent in Melanoma 2 (AIM2) Pyrin Domain Provides Insights into the Mechanisms of AIM2 Autoinhibition and Inflammasome Assembly. J. Biol. Chem. 2013;288:13225–13235. doi: 10.1074/jbc.M113.468033. PubMed DOI PMC
Morrone S.R., Matyszewski M., Yu X., Delannoy M., Egelman E.H., Sohn J. Assembly-Driven Activation of the AIM2 Foreign-DsDNA Sensor Provides a Polymerization Template for Downstream ASC. Nat. Commun. 2015;6:7827. doi: 10.1038/ncomms8827. PubMed DOI PMC
Lu A., Magupalli V.G., Ruan J., Yin Q., Atianand M.K., Vos M.R., Schröder G.F., Fitzgerald K.A., Wu H., Egelman E.H. Unified Polymerization Mechanism for the Assembly of ASC-Dependent Inflammasomes. Cell. 2014;156:1193–1206. doi: 10.1016/j.cell.2014.02.008. PubMed DOI PMC
Ni X., Ru H., Ma F., Zhao L., Shaw N., Feng Y., Ding W., Gong W., Wang Q., Ouyang S., et al. New Insights into the Structural Basis of DNA Recognition by HINa and HINb Domains of IFI16. J. Mol. Cell Biol. 2016;8:51–61. doi: 10.1093/jmcb/mjv053. PubMed DOI
Fan X., Jiang J., Zhao D., Chen F., Ma H., Smith P., Unterholzner L., Xiao T.S., Jin T. Structural Mechanism of DNA Recognition by the P204 HIN Domain. Nucleic Acids Res. 2021;49:2959–2972. doi: 10.1093/nar/gkab076. PubMed DOI PMC
Ishikawa H., Ma Z., Barber G.N. STING Regulates Intracellular DNA-Mediated, Type I Interferon-Dependent Innate Immunity. Nature. 2009;461:788–792. doi: 10.1038/nature08476. PubMed DOI PMC
Liu S., Cai X., Wu J., Cong Q., Chen X., Li T., Du F., Ren J., Wu Y.-T., Grishin N.V., et al. Phosphorylation of Innate Immune Adaptor Proteins MAVS, STING, and TRIF Induces IRF3 Activation. Science. 2015;347:aaa2630. doi: 10.1126/science.aaa2630. PubMed DOI
Tanaka Y., Chen Z.J. STING Specifies IRF3 Phosphorylation by TBK1 in the Cytosolic DNA Signaling Pathway. Sci. Signal. 2012;5:ra20. doi: 10.1126/scisignal.2002521. PubMed DOI PMC
Zhang C., Shang G., Gui X., Zhang X., Bai X., Chen Z.J. Structural Basis of STING Binding with and Phosphorylation by TBK1. Nature. 2019;567:394–398. doi: 10.1038/s41586-019-1000-2. PubMed DOI PMC
Zhong B., Yang Y., Li S., Wang Y.-Y., Li Y., Diao F., Lei C., He X., Zhang L., Tien P., et al. The Adaptor Protein MITA Links Virus-Sensing Receptors to IRF3 Transcription Factor Activation. Immunity. 2008;29:538–550. doi: 10.1016/j.immuni.2008.09.003. PubMed DOI
Parker Z.M., Murphy A.A., Leib D.A. Role of the DNA Sensor STING in Protection from Lethal Infection Following Corneal and Intracerebral Challenge with Herpes Simplex Virus 1. J. Virol. 2015;89:11080–11091. doi: 10.1128/JVI.00954-15. PubMed DOI PMC
Reinert L.S., Lopušná K., Winther H., Sun C., Thomsen M.K., Nandakumar R., Mogensen T.H., Meyer M., Vægter C., Nyengaard J.R., et al. Sensing of HSV-1 by the CGAS–STING Pathway in Microglia Orchestrates Antiviral Defence in the CNS. Nat. Commun. 2016;7:13348. doi: 10.1038/ncomms13348. PubMed DOI PMC
Stetson D.B., Medzhitov R. Recognition of Cytosolic DNA Activates an IRF3-Dependent Innate Immune Response. Immunity. 2006;24:93–103. doi: 10.1016/j.immuni.2005.12.003. PubMed DOI
Stratmann S.A., Morrone S.R., van Oijen A.M., Sohn J. The Innate Immune Sensor IFI16 Recognizes Foreign DNA in the Nucleus by Scanning along the Duplex. eLife. 2015;4:e11721. doi: 10.7554/eLife.11721. PubMed DOI PMC
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-β Responses. PLoS Pathog. 2015;11:e1005019. doi: 10.1371/journal.ppat.1005019. PubMed DOI PMC
Lum K.K., Howard T.R., Pan C., Cristea I.M. Charge-Mediated Pyrin Oligomerization Nucleates Antiviral IFI16 Sensing of Herpesvirus DNA. mBio. 2019;10:e01428-19. doi: 10.1128/mBio.01428-19. PubMed DOI PMC
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. doi: 10.1073/pnas.1424637112. PubMed DOI PMC
Almine J.F., O’Hare C.A.J., Dunphy G., Haga I.R., Naik R.J., Atrih A., Connolly D.J., Taylor J., Kelsall I.R., Bowie A.G., et al. IFI16 and CGAS Cooperate in the Activation of STING during DNA Sensing in Human Keratinocytes. Nat. Commun. 2017;8:14392. doi: 10.1038/ncomms14392. PubMed DOI PMC
Jønsson K.L., Laustsen A., Krapp C., Skipper K.A., Thavachelvam K., Hotter D., Egedal J.H., Kjolby M., Mohammadi P., Prabakaran T., et al. IFI16 Is Required for DNA Sensing in Human Macrophages by Promoting Production and Function of CGAMP. Nat. Commun. 2017;8:14391. doi: 10.1038/ncomms14391. PubMed DOI PMC
Ishikawa H., Barber G.N. STING Is an Endoplasmic Reticulum Adaptor That Facilitates Innate Immune Signalling. Nature. 2008;455:674–678. doi: 10.1038/nature07317. PubMed DOI PMC
Gentili M., Lahaye X., Nadalin F., Nader G.P.F., Puig Lombardi E., Herve S., De Silva N.S., Rookhuizen D.C., Zueva E., Goudot C., et al. The N-Terminal Domain of CGAS Determines Preferential Association with Centromeric DNA and Innate Immune Activation in the Nucleus. Cell Rep. 2019;26:2377–2393.e13. doi: 10.1016/j.celrep.2019.01.105. PubMed DOI PMC
Barnett K.C., Coronas-Serna J.M., Zhou W., Ernandes M.J., Cao A., Kranzusch P.J., Kagan J.C. Phosphoinositide Interactions Position CGAS at the Plasma Membrane to Ensure Efficient Distinction between Self- and Viral DNA. Cell. 2019;176:1432–1446.e11. doi: 10.1016/j.cell.2019.01.049. PubMed DOI PMC
Li T., Huang T., Du M., Chen X., Du F., Ren J., Chen Z.J. Phosphorylation and Chromatin Tethering Prevent CGAS Activation during Mitosis. Science. 2021;371:eabc5386. doi: 10.1126/science.abc5386. PubMed DOI PMC
Wu X., Wu F.-H., Wang X., Wang L., Siedow J.N., Zhang W., Pei Z.-M. Molecular Evolutionary and Structural Analysis of the Cytosolic DNA Sensor CGAS and STING. Nucleic Acids Res. 2014;42:8243–8257. doi: 10.1093/nar/gku569. PubMed DOI PMC
Xie W., Lama L., Adura C., Tomita D., Glickman J.F., Tuschl T., Patel D.J. Human CGAS Catalytic Domain Has an Additional DNA-Binding Interface That Enhances Enzymatic Activity and Liquid-Phase Condensation. Proc. Natl. Acad. Sci. USA. 2019;116:11946–11955. doi: 10.1073/pnas.1905013116. PubMed DOI PMC
Kranzusch P.J. CGAS and CD-NTase Enzymes: Structure, Mechanism, and Evolution. Curr. Opin. Struct. Biol. 2019;59:178–187. doi: 10.1016/j.sbi.2019.08.003. PubMed DOI PMC
Zhou W., Whiteley A.T., de Oliveira Mann C.C., Morehouse B.R., Nowak R.P., Fischer E.S., Gray N.S., Mekalanos J.J., Kranzusch P.J. Structure of the Human CGAS–DNA Complex Reveals Enhanced Control of Immune Surveillance. Cell. 2018;174:300–311.e11. doi: 10.1016/j.cell.2018.06.026. PubMed DOI PMC
Li X.-D., Wu J., Gao D., Wang H., Sun L., Chen Z.J. Pivotal Roles of CGAS-CGAMP Signaling in Antiviral Defense and Immune Adjuvant Effects. Science. 2013;341:1390–1394. doi: 10.1126/science.1244040. PubMed DOI PMC
Andreeva L., Hiller B., Kostrewa D., Lässig C., de Oliveira Mann C.C., Jan Drexler D., Maiser A., Gaidt M., Leonhardt H., Hornung V., et al. CGAS Senses Long and HMGB/TFAM-Bound U-Turn DNA by Forming Protein–DNA Ladders. Nature. 2017;549:394–398. doi: 10.1038/nature23890. PubMed DOI
Du M., Chen Z.J. DNA-Induced Liquid Phase Condensation of CGAS Activates Innate Immune Signaling. Science. 2018;361:704–709. doi: 10.1126/science.aat1022. PubMed DOI PMC
Liu Z.-S., Cai H., Xue W., Wang M., Xia T., Li W.-J., Xing J.-Q., Zhao M., Huang Y.-J., Chen S., et al. G3BP1 Promotes DNA Binding and Activation of CGAS. Nat. Immunol. 2019;20:18–28. doi: 10.1038/s41590-018-0262-4. PubMed DOI PMC
Srikanth S., Woo J.S., Wu B., El-Sherbiny Y.M., Leung J., Chupradit K., Rice L., Seo G.J., Calmettes G., Ramakrishna C., et al. The Ca2+ Sensor STIM1 Regulates the Type I Interferon Response by Retaining the Signaling Adaptor STING at the Endoplasmic Reticulum. Nat. Immunol. 2019;20:152–162. doi: 10.1038/s41590-018-0287-8. PubMed DOI PMC
Burdette D.L., Monroe K.M., Sotelo-Troha K., Iwig J.S., Eckert B., Hyodo M., Hayakawa Y., Vance R.E. STING Is a Direct Innate Immune Sensor of Cyclic Di-GMP. Nature. 2011;478:515–518. doi: 10.1038/nature10429. PubMed DOI PMC
Diner E.J., Burdette D.L., Wilson S.C., Monroe K.M., Kellenberger C.A., Hyodo M., Hayakawa Y., Hammond M.C., Vance R.E. The Innate Immune DNA Sensor CGAS Produces a Noncanonical Cyclic Dinucleotide That Activates Human STING. Cell Rep. 2013;3:1355–1361. doi: 10.1016/j.celrep.2013.05.009. PubMed DOI PMC
Cheng Z., Dai T., He X., Zhang Z., Xie F., Wang S., Zhang L., Zhou F. The Interactions between CGAS-STING Pathway and Pathogens. Sig. Transduct. Target. Ther. 2020;5:91. doi: 10.1038/s41392-020-0198-7. PubMed DOI PMC
Shang G., Zhang C., Chen Z.J., Bai X., Zhang X. Cryo-EM Structures of STING Reveal Its Mechanism of Activation by Cyclic GMP–AMP. Nature. 2019;567:389–393. doi: 10.1038/s41586-019-0998-5. PubMed DOI PMC
Gui X., Yang H., Li T., Tan X., Shi P., Li M., Du F., Chen Z.J. Autophagy Induction via STING Trafficking Is a Primordial Function of the CGAS Pathway. Nature. 2019;567:262–266. doi: 10.1038/s41586-019-1006-9. PubMed DOI PMC
Stempel M., Chan B., Juranić Lisnić V., Krmpotić A., Hartung J., Paludan S.R., Füllbrunn N., Lemmermann N.A., Brinkmann M.M. The Herpesviral Antagonist M152 Reveals Differential Activation of STING -dependent IRF and NF -κB Signaling and STING ’s Dual Role during MCMV Infection. EMBO J. 2019;38:e100983. doi: 10.15252/embj.2018100983. PubMed DOI PMC
Tsuchida T., Zou J., Saitoh T., Kumar H., Abe T., Matsuura Y., Kawai T., Akira S. The Ubiquitin Ligase TRIM56 Regulates Innate Immune Responses to Intracellular Double-Stranded DNA. Immunity. 2010;33:765–776. doi: 10.1016/j.immuni.2010.10.013. PubMed DOI
Wang Q., Liu X., Cui Y., Tang Y., Chen W., Li S., Yu H., Pan Y., Wang C. The E3 Ubiquitin Ligase AMFR and INSIG1 Bridge the Activation of TBK1 Kinase by Modifying the Adaptor STING. Immunity. 2014;41:919–933. doi: 10.1016/j.immuni.2014.11.011. PubMed DOI
Zhang J., Hu M.-M., Wang Y.-Y., Shu H.-B. TRIM32 Protein Modulates Type I Interferon Induction and Cellular Antiviral Response by Targeting MITA/STING Protein for K63-Linked Ubiquitination. J. Biol. Chem. 2012;287:28646–28655. doi: 10.1074/jbc.M112.362608. PubMed DOI PMC
Yu X., Zhang L., Shen J., Zhai Y., Jiang Q., Yi M., Deng X., Ruan Z., Fang R., Chen Z., et al. The STING Phase-Separator Suppresses Innate Immune Signalling. Nat. Cell Biol. 2021;23:330–340. doi: 10.1038/s41556-021-00659-0. PubMed DOI
Agelidis A.M., Shukla D. Cell Entry Mechanisms of HSV: What We Have Learned in Recent Years. Future Virol. 2015;10:1145–1154. doi: 10.2217/fvl.15.85. PubMed DOI PMC
Oh J., Fraser N.W. Temporal Association of the Herpes Simplex Virus Genome with Histone Proteins during a Lytic Infection. J. Virol. 2008;82:3530–3537. doi: 10.1128/JVI.00586-07. PubMed DOI PMC
Thorley-Lawson D.A., Duca K.A., Shapiro M. Epstein-Barr Virus: A Paradigm for Persistent Infection—For Real and in Virtual Reality. Trends Immunol. 2008;29:195–201. doi: 10.1016/j.it.2008.01.006. PubMed DOI
Weidner-Glunde M., Kruminis-Kaszkiel E., Savanagouder M. Herpesviral Latency—Common Themes. Pathogens. 2020;9:125. doi: 10.3390/pathogens9020125. PubMed DOI PMC
Varani S., Cederarv M., Feld S., Tammik C., Frascaroli G., Landini M.P., Söderberg-Nauclér C. Human Cytomegalovirus Differentially Controls B Cell and T Cell Responses through Effects on Plasmacytoid Dendritic Cells. J. Immunol. 2007;179:7767–7776. doi: 10.4049/jimmunol.179.11.7767. PubMed DOI
Krug A., Luker G.D., Barchet W., Leib D.A., Akira S., Colonna M. Herpes Simplex Virus Type 1 Activates Murine Natural Interferon-Producing Cells through Toll-like Receptor 9. Blood. 2004;103:1433–1437. doi: 10.1182/blood-2003-08-2674. PubMed DOI
Zyzak J., Mitkiewicz M., Leszczyńska E., Reniewicz P., Moynagh P.N., Siednienko J. HSV-1/TLR9-Mediated IFNβ and TNFα Induction Is Mal-Dependent in Macrophages. J. Innate Immun. 2020;12:387–398. doi: 10.1159/000504542. PubMed DOI PMC
Hochrein H., Schlatter B., O’Keeffe M., Wagner C., Schmitz F., Schiemann M., Bauer S., Suter M., Wagner H. Herpes Simplex Virus Type-1 Induces IFN- Production via Toll-like Receptor 9-Dependent and -Independent Pathways. Proc. Natl. Acad. Sci. USA. 2004;101:11416–11421. doi: 10.1073/pnas.0403555101. PubMed DOI PMC
Lund J., Sato A., Akira S., Medzhitov R., Iwasaki A. Toll-like Receptor 9–Mediated Recognition of Herpes Simplex Virus-2 by Plasmacytoid Dendritic Cells. J. Exp. Med. 2003;198:513–520. doi: 10.1084/jem.20030162. PubMed DOI PMC
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. doi: 10.1073/pnas.1211302109. PubMed DOI PMC
Duan Y., Zeng J., Fan S., Liao Y., Feng M., Wang L., Zhang Y., Li Q. Herpes Simplex Virus Type 1-Encoded MiR-H2-3p Manipulates Cytosolic DNA-Stimulated Antiviral Innate Immune Response by Targeting DDX41. Viruses. 2019;11:756. doi: 10.3390/v11080756. PubMed DOI PMC
Justice J.L., Kennedy M.A., Hutton J.E., Liu D., Song B., Phelan B., Cristea I.M. Systematic Profiling of Protein Complex Dynamics Reveals DNA-PK Phosphorylation of IFI16 En Route to Herpesvirus Immunity. Sci. Adv. 2021;7:eabg6680. doi: 10.1126/sciadv.abg6680. PubMed DOI PMC
Yamashiro L.H., Wilson S.C., Morrison H.M., Karalis V., Chung J.-Y.J., Chen K.J., Bateup H.S., Szpara M.L., Lee A.Y., Cox J.S., et al. Interferon-Independent STING Signaling Promotes Resistance to HSV-1 in Vivo. Nat. Commun. 2020;11:3382. doi: 10.1038/s41467-020-17156-x. PubMed DOI PMC
Wu J., Dobbs N., Yang K., Yan N. Interferon-Independent Activities of Mammalian STING Mediate Antiviral Response and Tumor Immune Evasion. Immunity. 2020;53:115–126.e5. doi: 10.1016/j.immuni.2020.06.009. PubMed DOI PMC
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. doi: 10.1016/j.chom.2011.04.008. PubMed DOI PMC
Johnson K.E., Chikoti L., Chandran B. Herpes Simplex Virus 1 Infection Induces Activation and Subsequent Inhibition of the IFI16 and NLRP3 Inflammasomes. J. Virol. 2013;87:5005–5018. doi: 10.1128/JVI.00082-13. PubMed DOI PMC
Ansari M.A., Singh V.V., Dutta S., Veettil M.V., Dutta D., Chikoti L., Lu J., Everly D., Chandran B. Constitutive Interferon-Inducible Protein 16-Inflammasome Activation during Epstein-Barr Virus Latency I, II, and III in B and Epithelial Cells. J. Virol. 2013;87:8606–8623. doi: 10.1128/JVI.00805-13. PubMed DOI PMC
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-β Responses. PLoS Pathog. 2016;12:e1005967. doi: 10.1371/journal.ppat.1005967. PubMed DOI PMC
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-β Responses. PLoS Pathog. 2015;11:e1005030. doi: 10.1371/journal.ppat.1005030. PubMed DOI PMC
Su C., Zheng C. Herpes Simplex Virus 1 Abrogates the CGAS/STING-Mediated Cytosolic DNA-Sensing Pathway via Its Virion Host Shutoff Protein, UL41. J. Virol. 2017;91:e02414-16. doi: 10.1128/JVI.02414-16. PubMed DOI PMC
Huang J., You H., Su C., Li Y., Chen S., Zheng C. Herpes Simplex Virus 1 Tegument Protein VP22 Abrogates CGAS/STING-Mediated Antiviral Innate Immunity. J. Virol. 2018;92:e00841-18. doi: 10.1128/JVI.00841-18. PubMed DOI PMC
Teigler J.E., Kagan J.C., Barouch D.H. Late Endosomal Trafficking of Alternative Serotype Adenovirus Vaccine Vectors Augments Antiviral Innate Immunity. J. Virol. 2014;88:10354–10363. doi: 10.1128/JVI.00936-14. PubMed DOI PMC
Basner-Tschakarjan E., Gaffal E., O’Keeffe M., Tormo D., Limmer A., Wagner H., Hochrein H., Tüting T. Adenovirus Efficiently Transduces Plasmacytoid Dendritic Cells Resulting in TLR9-Dependent Maturation and IFN-α Production. J. Gene Med. 2006;8:1300–1306. doi: 10.1002/jgm.964. PubMed DOI
Hensley S.E., Giles-Davis W., McCoy K.C., Weninger W., Ertl H.C.J. Dendritic Cell Maturation, but Not CD8 + T Cell Induction, Is Dependent on Type I IFN Signaling during Vaccination with Adenovirus Vectors. J. Immunol. 2005;175:6032–6041. doi: 10.4049/jimmunol.175.9.6032. PubMed DOI
Huarte E., Larrea E., Hernández-Alcoceba R., Alfaro C., Murillo O., Arina A., Tirapu I., Azpilicueta A., Hervás-Stubbs S., Bortolanza S., et al. Recombinant Adenoviral Vectors Turn on the Type I Interferon System without Inhibition of Transgene Expression and Viral Replication. Mol. Ther. 2006;14:129–138. doi: 10.1016/j.ymthe.2006.02.015. PubMed DOI
Zhu J., Huang X., Yang Y. Innate Immune Response to Adenoviral Vectors Is Mediated by Both Toll-Like Receptor-Dependent and -Independent Pathways. J. Virol. 2007;81:3170–3180. doi: 10.1128/JVI.02192-06. PubMed DOI PMC
Iacobelli-Martinez M., Nemerow G.R. Preferential Activation of Toll-Like Receptor Nine by CD46-Utilizing Adenoviruses. J. Virol. 2007;81:1305–1312. doi: 10.1128/JVI.01926-06. PubMed DOI PMC
McGuire K.A., Barlan A.U., Griffin T.M., Wiethoff C.M. Adenovirus Type 5 Rupture of Lysosomes Leads to Cathepsin B-Dependent Mitochondrial Stress and Production of Reactive Oxygen Species. J. Virol. 2011;85:10806–10813. doi: 10.1128/JVI.00675-11. PubMed DOI PMC
Barlan A.U., Griffin T.M., Mcguire K.A., Wiethoff C.M. Adenovirus Membrane Penetration Activates the NLRP3 Inflammasome. J. Virol. 2011;85:146–155. doi: 10.1128/JVI.01265-10. PubMed DOI PMC
Lam E., Stein S., Falck-Pedersen E. Adenovirus Detection by the CGAS/STING/TBK1 DNA Sensing Cascade. J. Virol. 2014;88:974–981. doi: 10.1128/JVI.02702-13. PubMed DOI PMC
Stein S.C., Falck-Pedersen E. Sensing Adenovirus Infection: Activation of Interferon Regulatory Factor 3 in RAW 264.7 Cells. J. Virol. 2012;86:4527–4537. doi: 10.1128/JVI.07071-11. PubMed DOI PMC
Yamaguchi T., Kawabata K., Kouyama E., Ishii K.J., Katayama K., Suzuki T., Kurachi S., Sakurai F., Akira S., Mizuguchi H. Induction of Type I Interferon by Adenovirus-Encoded Small RNAs. Proc. Natl. Acad. Sci. USA. 2010;107:17286–17291. doi: 10.1073/pnas.1009823107. PubMed DOI PMC
Sohn S.-Y., Hearing P. Mechanism of Adenovirus E4-ORF3-Mediated SUMO Modifications. mBio. 2019;10:e00022-19. doi: 10.1128/mBio.00022-19. PubMed DOI PMC
Lau L., Gray E.E., Brunette R.L., Stetson D.B. DNA Tumor Virus Oncogenes Antagonize the CGAS-STING DNA-Sensing Pathway. Science. 2015;350:568–571. doi: 10.1126/science.aab3291. PubMed DOI
Look D.C., Roswit W.T., Frick A.G., Gris-Alevy Y., Dickhaus D.M., Walter M.J., Holtzman M.J. Direct Suppression of Stat1 Function during Adenoviral Infection. Immunity. 1998;9:871–880. doi: 10.1016/S1074-7613(00)80652-4. PubMed DOI
McBride A.A. Human Papillomaviruses: Diversity, Infection and Host Interactions. Nat. Rev. Microbiol. 2022;20:95–108. doi: 10.1038/s41579-021-00617-5. PubMed DOI
Doorbar J., Quint W., Banks L., Bravo I.G., Stoler M., Broker T.R., Stanley M.A. The Biology and Life-Cycle of Human Papillomaviruses. Vaccine. 2012;30:F55–F70. doi: 10.1016/j.vaccine.2012.06.083. PubMed DOI
Day P.M., Thompson C.D., Schowalter R.M., Lowy D.R., Schiller J.T. Identification of a Role for the Trans-Golgi Network in Human Papillomavirus 16 Pseudovirus Infection. J. Virol. 2013;87:3862–3870. doi: 10.1128/JVI.03222-12. PubMed DOI PMC
Aydin I., Weber S., Snijder B., Samperio Ventayol P., Kühbacher A., Becker M., Day P.M., Schiller J.T., Kann M., Pelkmans L., et al. Large Scale RNAi Reveals the Requirement of Nuclear Envelope Breakdown for Nuclear Import of Human Papillomaviruses. PLoS Pathog. 2014;10:e1004162. doi: 10.1371/journal.ppat.1004162. PubMed DOI PMC
Cannella F., Pierangeli A., Scagnolari C., Cacciotti G., Tranquilli G., Stentella P., Recine N., Antonelli G. TLR9 Is Expressed in Human Papillomavirus-Positive Cervical Cells and Is Overexpressed in Persistent Infections. Immunobiology. 2015;220:363–368. doi: 10.1016/j.imbio.2014.10.012. PubMed DOI
Hasan U.A., Bates E., Takeshita F., Biliato A., Accardi R., Bouvard V., Mansour M., Vincent I., Gissmann L., Iftner T., et al. TLR9 Expression and Function Is Abolished by the Cervical Cancer-Associated Human Papillomavirus Type 16. J. Immunol. 2007;178:3186–3197. doi: 10.4049/jimmunol.178.5.3186. PubMed DOI
Reinholz M., Kawakami Y., Salzer S., Kreuter A., Dombrowski Y., Koglin S., Kresse S., Ruzicka T., Schauber J. HPV16 Activates the AIM2 Inflammasome in Keratinocytes. Arch. Dermatol. Res. 2013;305:723–732. doi: 10.1007/s00403-013-1375-0. PubMed DOI
Ainouze M., Rochefort P., Parroche P., Roblot G., Tout I., Briat F., Zannetti C., Marotel M., Goutagny N., Auron P., et al. Human Papillomavirus Type 16 Antagonizes IRF6 Regulation of IL-1β. PLoS Pathog. 2018;14:e1007158. doi: 10.1371/journal.ppat.1007158. PubMed DOI PMC
Uhlorn B.L., Jackson R., Li S., Bratton S.M., Van Doorslaer K., Campos S.K. Vesicular Trafficking Permits Evasion of CGAS/STING Surveillance during Initial Human Papillomavirus Infection. PLoS Pathog. 2020;16:e1009028. doi: 10.1371/journal.ppat.1009028. PubMed DOI PMC
Shaikh M.H., Bortnik V., McMillan N.A.J., Idris A. CGAS-STING Responses Are Dampened in High-Risk HPV Type 16 Positive Head and Neck Squamous Cell Carcinoma Cells. Microb. Pathog. 2019;132:162–165. doi: 10.1016/j.micpath.2019.05.004. PubMed DOI
Cook L. Polyomaviruses. Microbiol. Spectr. 2016;4 doi: 10.1128/microbiolspec.DMIH2-0010-2015. PubMed DOI
Prado J., Monezi T., Amorim A., Lino V., Paladino A., Boccardo E. Human Polyomaviruses and Cancer: An Overview. Clinics. 2018;73 doi: 10.6061/clinics/2018/e558s. PubMed DOI PMC
Ehlers B., Moens U. Genome Analysis of Non-Human Primate Polyomaviruses. Infect. Genet. Evol. 2014;26:283–294. doi: 10.1016/j.meegid.2014.05.030. PubMed DOI
Soldatova I., Prilepskaja T., Abrahamyan L., Forstová J., Huérfano S. Interaction of the Mouse Polyomavirus Capsid Proteins with Importins Is Required for Efficient Import of Viral DNA into the Cell Nucleus. Viruses. 2018;10:165. doi: 10.3390/v10040165. PubMed DOI PMC
Liebl D., Difato F., Horníková L., Mannová P., Štokrová J., Forstová J. Mouse Polyomavirus Enters Early Endosomes, Requires Their Acidic PH for Productive Infection, and Meets Transferrin Cargo in Rab11-Positive Endosomes. J. Virol. 2006;80:4610–4622. doi: 10.1128/JVI.80.9.4610-4622.2006. PubMed DOI PMC
Horníková L., Bruštíková K., Forstová J. Microtubules in Polyomavirus Infection. Viruses. 2020;12:121. doi: 10.3390/v12010121. PubMed DOI PMC
Huérfano S., Ryabchenko B., Španielová H., Forstová J. Hydrophobic Domains of Mouse Polyomavirus Minor Capsid Proteins Promote Membrane Association and Virus Exit from the ER. FEBS J. 2017;284:883–902. doi: 10.1111/febs.14033. PubMed DOI
Padgett B.L., Zurhein G.M., Walker D.L., Eckroade R., Dessel B. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet. 1971;297:1257–1260. doi: 10.1016/S0140-6736(71)91777-6. PubMed DOI
Gardner S.D., Field A.M., Coleman D.V., Hulme B. New human papovavirus (B.K.) Isolated from urine after renal transplantation. Lancet. 1971;297:1253–1257. doi: 10.1016/S0140-6736(71)91776-4. PubMed DOI
Feng H., Shuda M., Chang Y., Moore P.S. Clonal Integration of a Polyomavirus in Human Merkel Cell Carcinoma. Science. 2008;319:1096–1100. doi: 10.1126/science.1152586. PubMed DOI PMC
Knowles W.A., Pipkin P., Andrews N., Vyse A., Minor P., Brown D.W.G., Miller E. Population-Based Study of Antibody to the Human Polyomaviruses BKV and JCV and the Simian Polyomavirus SV40. J. Med. Virol. 2003;71:115–123. doi: 10.1002/jmv.10450. PubMed DOI
Egli A., Infanti L., Dumoulin A., Buser A., Samaridis J., Stebler C., Gosert R., Hirsch H.H. Prevalence of Polyomavirus BK and JC Infection and Replication in 400 Healthy Blood Donors. J. Infect. Dis. 2009;199:837–846. doi: 10.1086/597126. PubMed DOI
Šroller V., Hamšíková E., Ludvíková V., Vochozková P., Kojzarová M., Fraiberk M., Saláková M., Morávková A., Forstová J., Němečková Š. Seroprevalence Rates of BKV, JCV, and MCPyV Polyomaviruses in the General Czech Republic Population: Seroprevalence of BKV, JCV, and MCPyV. J. Med. Virol. 2014;86:1560–1568. doi: 10.1002/jmv.23841. PubMed DOI
Foulongne V., Sauvage V., Hebert C., Dereure O., Cheval J., Gouilh M.A., Pariente K., Segondy M., Burguière A., Manuguerra J.-C., et al. Human Skin Microbiota: High Diversity of DNA Viruses Identified on the Human Skin by High Throughput Sequencing. PLoS ONE. 2012;7:e38499. doi: 10.1371/journal.pone.0038499. PubMed DOI PMC
Jouhi L., Koljonen V., Böhling T., Haglund C., Hagström J. The Expression of Toll-like Receptors 2, 4, 5, 7 and 9 in Merkel Cell Carcinoma. Anticancer. Res. 2015;35:1843–1849. PubMed
Shahzad N., Shuda M., Gheit T., Kwun H.J., Cornet I., Saidj D., Zannetti C., Hasan U., Chang Y., Moore P.S., et al. The T Antigen Locus of Merkel Cell Polyomavirus Downregulates Human Toll-Like Receptor 9 Expression. J. Virol. 2013;87:13009–13019. doi: 10.1128/JVI.01786-13. PubMed DOI PMC
Ryabchenko B., Soldatova I., Šroller V., Forstová J., Huérfano S. Immune Sensing of Mouse Polyomavirus DNA by P204 and CGAS DNA Sensors. FEBS J. 2021;288:5964–5985. doi: 10.1111/febs.15962. PubMed DOI PMC
Krump N.A., Wang R., Liu W., Yang J.F., Ma T., You J. Merkel Cell Polyomavirus Infection Induces an Antiviral Innate Immune Response in Human Dermal Fibroblasts. J. Virol. 2021;95:e02211-20. doi: 10.1128/JVI.02211-20. PubMed DOI PMC
Liu W., Yang R., Payne A.S., Schowalter R.M., Spurgeon M.E., Lambert P.F., Xu X., Buck C.B., You J. Identifying the Target Cells and Mechanisms of Merkel Cell Polyomavirus Infection. Cell Host Microbe. 2016;19:775–787. doi: 10.1016/j.chom.2016.04.024. PubMed DOI PMC
Mannová P., Forstová J. Mouse Polyomavirus Utilizes Recycling Endosomes for a Traffic Pathway Independent of COPI Vesicle Transport. J. Virol. 2003;77:1672–1681. doi: 10.1128/JVI.77.3.1672-1681.2003. PubMed DOI PMC
de Kort H., Heutinck K.M., Ruben J.M., Ede V. Silva A., Wolthers K.C., Hamann J., ten Berge I.J.M. Primary Human Renal-Derived Tubular Epithelial Cells Fail to Recognize and Suppress BK Virus Infection. Transplantation. 2017;101:1820–1829. doi: 10.1097/TP.0000000000001521. PubMed DOI
An P., Sáenz Robles M.T., Duray A.M., Cantalupo P.G., Pipas J.M. Human Polyomavirus BKV Infection of Endothelial Cells Results in Interferon Pathway Induction and Persistence. PLoS Pathog. 2019;15:e1007505. doi: 10.1371/journal.ppat.1007505. PubMed DOI PMC
Manzetti J., Weissbach F.H., Graf F.E., Unterstab G., Wernli M., Hopfer H., Drachenberg C.B., Rinaldo C.H., Hirsch H.H. BK Polyomavirus Evades Innate Immune Sensing by Disrupting the Mitochondrial Network and Promotes Mitophagy. iScience. 2020;23:101257. doi: 10.1016/j.isci.2020.101257. PubMed DOI PMC
Yan H., Zhong G., Xu G., He W., Jing Z., Gao Z., Huang Y., Qi Y., Peng B., Wang H., et al. Sodium Taurocholate Cotransporting Polypeptide Is a Functional Receptor for Human Hepatitis B and D Virus. eLife. 2012;1:e00049. doi: 10.7554/eLife.00049. PubMed DOI PMC
Huang H.-C., Chen C.-C., Chang W.-C., Tao M.-H., Huang C. Entry of Hepatitis B Virus into Immortalized Human Primary Hepatocytes by Clathrin-Dependent Endocytosis. J. Virol. 2012;86:9443–9453. doi: 10.1128/JVI.00873-12. PubMed DOI PMC
Macovei A., Radulescu C., Lazar C., Petrescu S., Durantel D., Dwek R.A., Zitzmann N., Nichita N.B. Hepatitis B Virus Requires Intact Caveolin-1 Function for Productive Infection in HepaRG Cells. J. Virol. 2010;84:243–253. doi: 10.1128/JVI.01207-09. PubMed DOI PMC
Bock C.T., Schwinn S., Locarnini S., Fyfe J., Manns M.P., Trautwein C., Zentgraf H. Structural Organization of the Hepatitis B Virus Minichromosome. J. Mol. Biol. 2001;307:183–196. doi: 10.1006/jmbi.2000.4481. PubMed DOI
Mutz P., Metz P., Lempp F.A., Bender S., Qu B., Schöneweis K., Seitz S., Tu T., Restuccia A., Frankish J., et al. HBV Bypasses the Innate Immune Response and Does Not Protect HCV From Antiviral Activity of Interferon. Gastroenterology. 2018;154:1791–1804.e22. doi: 10.1053/j.gastro.2018.01.044. PubMed DOI
Suslov A., Boldanova T., Wang X., Wieland S., Heim M.H. Hepatitis B Virus Does Not Interfere With Innate Immune Responses in the Human Liver. Gastroenterology. 2018;154:1778–1790. doi: 10.1053/j.gastro.2018.01.034. PubMed DOI
Chen Y., Tian Z. HBV-Induced Immune Imbalance in the Development of HCC. Front. Immunol. 2019;10:2048. doi: 10.3389/fimmu.2019.02048. PubMed DOI PMC
Hirsch I., Caux C., Hasan U., Bendriss-Vermare N., Olive D. Impaired Toll-like Receptor 7 and 9 Signaling: From Chronic Viral Infections to Cancer. Trends Immunol. 2010;31:391–397. doi: 10.1016/j.it.2010.07.004. PubMed DOI
Vincent I.E., Zannetti C., Lucifora J., Norder H., Protzer U., Hainaut P., Zoulim F., Tommasino M., Trépo C., Hasan U., et al. Hepatitis B Virus Impairs TLR9 Expression and Function in Plasmacytoid Dendritic Cells. PLoS ONE. 2011;6:e26315. doi: 10.1371/journal.pone.0026315. PubMed DOI PMC
Xu Y., Hu Y., Shi B., Zhang X., Wang J., Zhang Z., Shen F., Zhang Q., Sun S., Yuan Z. HBsAg Inhibits TLR9-Mediated Activation and IFN-α Production in Plasmacytoid Dendritic Cells. Mol. Immunol. 2009;46:2640–2646. doi: 10.1016/j.molimm.2009.04.031. PubMed DOI
Wu J., Lu M., Meng Z., Trippler M., Broering R., Szczeponek A., Krux F., Dittmer U., Roggendorf M., Gerken G., et al. Toll-like Receptor-Mediated Control of HBV Replication by Nonparenchymal Liver Cells in Mice. Hepatology. 2007;46:1769–1778. doi: 10.1002/hep.21897. PubMed DOI
Martinet J., Dufeu–Duchesne T., Bruder Costa J., Larrat S., Marlu A., Leroy V., Plumas J., Aspord C. Altered Functions of Plasmacytoid Dendritic Cells and Reduced Cytolytic Activity of Natural Killer Cells in Patients With Chronic HBV Infection. Gastroenterology. 2012;143:1586–1596.e8. doi: 10.1053/j.gastro.2012.08.046. PubMed DOI
Verrier E.R., Yim S., Heydmann L., El Saghire H., Bach C., Turon-Lagot V., Mailly L., Durand S.C., Lucifora J., Durantel D., et al. Hepatitis B Virus Evasion From Cyclic Guanosine Monophosphate–Adenosine Monophosphate Synthase Sensing in Human Hepatocytes. Hepatology. 2018;68:1695–1709. doi: 10.1002/hep.30054. PubMed DOI PMC
Chen H., He G., Chen Y., Zhang X. Hepatitis B Virus Might Be Sensed by STING-Dependent DNA Sensors and Attenuates the Response of STING-Dependent DNA Sensing Pathway in Humans with Acute and Chronic Hepatitis B Virus Infection. Viral Immunol. 2020;33:642–651. doi: 10.1089/vim.2020.0096. PubMed DOI
Thomsen M.K., Nandakumar R., Stadler D., Malo A., Valls R.M., Wang F., Reinert L.S., Dagnaes-Hansen F., Hollensen A.K., Mikkelsen J.G., et al. Lack of Immunological DNA Sensing in Hepatocytes Facilitates Hepatitis B Virus Infection. Hepatology. 2016;64:746–759. doi: 10.1002/hep.28685. PubMed DOI
Lauterbach-Rivière L., Bergez M., Mönch S., Qu B., Riess M., Vondran F.W.R., Liese J., Hornung V., Urban S., König R. Hepatitis B Virus DNA Is a Substrate for the CGAS/STING Pathway but Is Not Sensed in Infected Hepatocytes. Viruses. 2020;12:592. doi: 10.3390/v12060592. PubMed DOI PMC
Liu Y., Li J., Chen J., Li Y., Wang W., Du X., Song W., Zhang W., Lin L., Yuan Z. Hepatitis B Virus Polymerase Disrupts K63-Linked Ubiquitination of STING To Block Innate Cytosolic DNA-Sensing Pathways. J. Virol. 2015;89:2287–2300. doi: 10.1128/JVI.02760-14. PubMed DOI PMC
Hu J., Tang L., Cheng J., Zhou T., Li Y., Chang J., Zhao Q., Guo J.-T. Hepatitis B Virus Nucleocapsid Uncoating: Biological Consequences and Regulation by Cellular Nucleases. Emerg. Microbes Infect. 2021;10:852–864. doi: 10.1080/22221751.2021.1919034. PubMed DOI PMC
Chen H., He G., Chen Y., Zhang X., Wu S. Differential Activation of NLRP3, AIM2, and IFI16 Inflammasomes in Humans with Acute and Chronic Hepatitis B. Viral Immunol. 2018;31:639–645. doi: 10.1089/vim.2018.0058. PubMed DOI
Lu Y.-Q., Wu J., Wu X.-J., Ma H., Ma Y.-X., Zhang R., Su M.-N., Wu N., Chen G.-Y., Chen H.-S., et al. Interferon Gamma-Inducible Protein 16 of Peripheral Blood Mononuclear Cells May Sense Hepatitis B Virus Infection and Regulate the Antiviral Immunity. Front. Cell. Infect. Microbiol. 2021;11:790036. doi: 10.3389/fcimb.2021.790036. PubMed DOI PMC
Yang Y., Zhao X., Wang Z., Shu W., Li L., Li Y., Guo Z., Gao B., Xiong S. Nuclear Sensor Interferon-Inducible Protein 16 Inhibits the Function of Hepatitis B Virus Covalently Closed Circular DNA by Integrating Innate Immune Activation and Epigenetic Suppression. Hepatology. 2020;71:1154–1169. doi: 10.1002/hep.30897. PubMed DOI
Wilen C.B., Tilton J.C., Doms R.W. HIV: Cell Binding and Entry. Cold Spring Harb. Perspect. Med. 2012;2:a006866. doi: 10.1101/cshperspect.a006866. PubMed DOI PMC
Zila V., Margiotta E., Turoňová B., Müller T.G., Zimmerli C.E., Mattei S., Allegretti M., Börner K., Rada J., Müller B., et al. Cone-Shaped HIV-1 Capsids Are Transported through Intact Nuclear Pores. Cell. 2021;184:1032–1046.e18. doi: 10.1016/j.cell.2021.01.025. PubMed DOI PMC
Shen Q., Wu C., Freniere C., Tripler T.N., Xiong Y. Nuclear Import of HIV-1. Viruses. 2021;13:2242. doi: 10.3390/v13112242. PubMed DOI PMC
Hatziioannou T., Perez-Caballero D., Cowan S., Bieniasz P.D. Cyclophilin Interactions with Incoming Human Immunodeficiency Virus Type 1 Capsids with Opposing Effects on Infectivity in Human Cells. J. Virol. 2005;79:176–183. doi: 10.1128/JVI.79.1.176-183.2005. PubMed DOI PMC
Nyamweya S., Hegedus A., Jaye A., Rowland-Jones S., Flanagan K.L., Macallan D.C. Comparing HIV-1 and HIV-2 Infection: Lessons for Viral Immunopathogenesis: Comparisons between HIV-1 and HIV-2 Infection. Rev. Med. Virol. 2013;23:221–240. doi: 10.1002/rmv.1739. PubMed DOI
Lahaye X., Manel N. Viral and Cellular Mechanisms of the Innate Immune Sensing of HIV. Curr. Opin. Virol. 2015;11:55–62. doi: 10.1016/j.coviro.2015.01.013. PubMed DOI
Gottlieb G.S., Raugi D.N., Smith R.A. 90-90-90 for HIV-2? Ending the HIV-2 Epidemic by Enhancing Care and Clinical Management of Patients Infected with HIV-2. Lancet HIV. 2018;5:e390–e399. doi: 10.1016/S2352-3018(18)30094-8. PubMed DOI
Gao D., Wu J., Wu Y.-T., Du F., Aroh C., Yan N., Sun L., Chen Z.J. Cyclic GMP-AMP Synthase Is an Innate Immune Sensor of HIV and Other Retroviruses. Science. 2013;341:903–906. doi: 10.1126/science.1240933. PubMed DOI PMC
Jakobsen M.R., Bak R.O., Andersen A., Berg R.K., Jensen S.B., Jin T., Laustsen A., Hansen K., Ostergaard L., Fitzgerald K.A., et al. PNAS Plus: From the Cover: IFI16 Senses DNA Forms of the Lentiviral Replication Cycle and Controls HIV-1 Replication. Proc. Natl. Acad. Sci. USA. 2013;110:E4571–E4580. doi: 10.1073/pnas.1311669110. PubMed DOI PMC
Goldstone D.C., Ennis-Adeniran V., Hedden J.J., Groom H.C.T., Rice G.I., Christodoulou E., Walker P.A., Kelly G., Haire L.F., Yap M.W., et al. HIV-1 Restriction Factor SAMHD1 Is a Deoxynucleoside Triphosphate Triphosphohydrolase. Nature. 2011;480:379–382. doi: 10.1038/nature10623. PubMed DOI
Goujon C., Rivière L., Jarrosson-Wuilleme L., Bernaud J., Rigal D., Darlix J.-L., Cimarelli A. SIVSM/HIV-2 Vpx Proteins Promote Retroviral Escape from a Proteasome-Dependent Restriction Pathway Present in Human Dendritic Cells. Retrovirology. 2007;4:2. doi: 10.1186/1742-4690-4-2. PubMed DOI PMC
Hrecka K., Hao C., Gierszewska M., Swanson S.K., Kesik-Brodacka M., Srivastava S., Florens L., Washburn M.P., Skowronski J. Vpx Relieves Inhibition of HIV-1 Infection of Macrophages Mediated by the SAMHD1 Protein. Nature. 2011;474:658–661. doi: 10.1038/nature10195. PubMed DOI PMC
Laguette N., Sobhian B., Casartelli N., Ringeard M., Chable-Bessia C., Ségéral E., Yatim A., Emiliani S., Schwartz O., Benkirane M. SAMHD1 Is the Dendritic- and Myeloid-Cell-Specific HIV-1 Restriction Factor Counteracted by Vpx. Nature. 2011;474:654–657. doi: 10.1038/nature10117. PubMed DOI PMC
Lahaye X., Satoh T., Gentili M., Cerboni S., Conrad C., Hurbain I., El Marjou A., Lacabaratz C., Lelièvre J.-D., Manel N. The Capsids of HIV-1 and HIV-2 Determine Immune Detection of the Viral CDNA by the Innate Sensor CGAS in Dendritic Cells. Immunity. 2013;39:1132–1142. doi: 10.1016/j.immuni.2013.11.002. PubMed DOI
Lahaye X., Gentili M., Silvin A., Conrad C., Picard L., Jouve M., Zueva E., Maurin M., Nadalin F., Knott G.J., et al. NONO Detects the Nuclear HIV Capsid to Promote CGAS-Mediated Innate Immune Activation. Cell. 2018;175:488–501.e22. doi: 10.1016/j.cell.2018.08.062. PubMed DOI
Yan N., Regalado-Magdos A.D., Stiggelbout B., Lee-Kirsch M.A., Lieberman J. The Cytosolic Exonuclease TREX1 Inhibits the Innate Immune Response to Human Immunodeficiency Virus Type 1. Nat. Immunol. 2010;11:1005–1013. doi: 10.1038/ni.1941. PubMed DOI PMC
Kumar S., Morrison J.H., Dingli D., Poeschla E. HIV-1 Activation of Innate Immunity Depends Strongly on the Intracellular Level of TREX1 and Sensing of Incomplete Reverse Transcription Products. J. Virol. 2018;92 doi: 10.1128/JVI.00001-18. PubMed DOI PMC
Wheeler L.A., Trifonova R.T., Vrbanac V., Barteneva N.S., Liu X., Bollman B., Onofrey L., Mulik S., Ranjbar S., Luster A.D., et al. TREX1 Knockdown Induces an Interferon Response to HIV That Delays Viral Infection in Humanized Mice. Cell Rep. 2016;15:1715–1727. doi: 10.1016/j.celrep.2016.04.048. PubMed DOI PMC
Doitsh G., Cavrois M., Lassen K.G., Zepeda O., Yang Z., Santiago M.L., Hebbeler A.M., Greene W.C. Abortive HIV Infection Mediates CD4 T Cell Depletion and Inflammation in Human Lymphoid Tissue. Cell. 2010;143:789–801. doi: 10.1016/j.cell.2010.11.001. PubMed DOI PMC
Monroe K.M., Yang Z., Johnson J.R., Geng X., Doitsh G., Krogan N.J., Greene W.C. IFI16 DNA Sensor Is Required for Death of Lymphoid CD4 T Cells Abortively Infected with HIV. Science. 2014;343:428–432. doi: 10.1126/science.1243640. PubMed DOI PMC
Dunphy G., Flannery S.M., Almine J.F., Connolly D.J., Paulus C., Jønsson 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-ΚB Signaling after Nuclear DNA Damage. Mol. Cell. 2018;71:745–760.e5. doi: 10.1016/j.molcel.2018.07.034. PubMed DOI PMC
Heiser K., Nicholas C., Garcea R.L. Activation of DNA Damage Repair Pathways by Murine Polyomavirus. Virology. 2016;497:346–356. doi: 10.1016/j.virol.2016.07.028. PubMed DOI PMC
Jiang M., Zhao L., Gamez M., Imperiale M.J. Roles of ATM and ATR-Mediated DNA Damage Responses during Lytic BK Polyomavirus Infection. PLoS Pathog. 2012;8:e1002898. doi: 10.1371/journal.ppat.1002898. PubMed DOI PMC
Sowd G.A., Li N.Y., Fanning E. ATM and ATR Activities Maintain Replication Fork Integrity during SV40 Chromatin Replication. PLoS Pathog. 2013;9:e1003283. doi: 10.1371/journal.ppat.1003283. PubMed DOI PMC