IFI16 Restricts HSV-1 Replication by Accumulating on the HSV-1 Genome, Repressing HSV-1 Gene Expression, and Directly or Indirectly Modulating Histone Modifications

1. Knipe DM, Howley PM, editors (2006) Fields' Virology. Philadelphia: Lippincott Williams & Wilkins. 3177 p.

2. StreileinJW, DanaMR, KsanderBR (1997) Immunity causing blindness: five different paths to herpes stromal keratitis. Immunol Today 18: 443–449.

3. WhitleyRJ, GnannJW (2002) Viral encephalitis: familiar infections and emerging pathogens. Lancet 359: 507–513.

4. WhitleyRJ, SoongSJ, LinnemanCJr, LiuC, PazinG, et al. (1982) Herpes simplex encephalitis. Clinical Assessment. JAMA 247: 317–320.

5. HonessRW, RoizmanB (1974) Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol 14: 8–19.

6. HonessRW, RoizmanB (1975) Proteins specified by herpes simplex virus. XIII. Glycosylation of viral polypeptides. J Virol 16: 1308–1326.

7. KwongAD, FrenkelN (1987) Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc Natl Acad Sci U S A 84: 1926–1930.

8. OroskarAA, ReadGS (1989) Control of mRNA stability by the virion host shutoff function of herpes simplex virus. J Virol 63: 1897–1906.

9. DauberB, PelletierJ, SmileyJR (2011) The herpes simplex virus 1 vhs protein enhances translation of viral true late mRNAs and virus production in a cell type-dependent manner. J Virol 85: 5363–5373.

10. HeB, ChouJ, BrandimartiR, MohrI, GluzmanY, et al. (1997) Suppression of the phenotype of gamma(1)34.5- herpes simplex virus 1: failure of activated RNA-dependent protein kinase to shut off protein synthesis is associated with a deletion in the domain of the alpha47 gene. J Virol 71: 6049–6054.

11. KentJR, ZengPY, AtanasiuD, GardnerJ, FraserNW, et al. (2004) During lytic infection herpes simplex virus type 1 is associated with histones bearing modifications that correlate with active transcription. J Virol 78: 10178–10186.

12. HerreraFJ, TriezenbergSJ (2004) VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J Virol 78: 9689–9696.

13. CliffeAR, KnipeDM (2008) Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J Virol 82: 12030–12038.

14. HancockMH, CliffeAR, KnipeDM, SmileyJR (2010) Herpes simplex virus VP16, but not ICP0, is required to reduce histone occupancy and enhance histone acetylation on viral genomes in U2OS osteosarcoma cells. J Virol 84: 1366–1375.

15. DeshmaneSL, FraserNW (1989) During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure. J Virol 63: 943–947.

16. WangQY, ZhouC, JohnsonKE, ColgroveRC, CoenDM, et al. (2005) Herpesviral latency-associated transcript gene promotes assembly of heterochromatin on viral lytic-gene promoters in latent infection. Proc Natl Acad Sci U S A 102: 16055–16059.

17. SwygertSG, PetersonCL (2014) Chromatin dynamics: Interplay between remodeling enzymes and histone modifications. Biochim Biophys Acta 1839: 728–736.

18. GuH, RoizmanB (2007) Herpes simplex virus-infected cell protein 0 blocks the silencing of viral DNA by dissociating histone deacetylases from the CoREST-REST complex. Proc Natl Acad Sci U S A 104: 17134–17139.

19. JohnsonKE, ChikotiL, ChandranB (2013) HSV-1 Infection Induces Activation and Subsequent Inhibition of the IFI16 and NLRP3 Inflammasomes. J Virol 87: 5005–5018.

20. OrzalliMH, DelucaNA, KnipeDM (2012) Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci U S A 109: E3008–3017.

21. MaulGG, EverettRD (1994) The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J Gen Virol 75: 1223–1233.

22. MelroeGT, DeLucaNA, KnipeDM (2004) Herpes simplex virus 1 has multiple mechanisms for blocking virus-induced interferon production. J Virol 78: 8411–8420.

23. MelroeGT, SilvaL, SchafferPA, KnipeDM (2007) Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: Potential role in blocking IFN-beta induction. Virology 360: 305–321.

24. YokotaS, YokosawaN, KubotaT, SuzutaniT, YoshidaI, et al. (2001) Herpes simplex virus type 1 suppresses the interferon signaling pathway by inhibiting phosphorylation of STATs and janus kinases during an early infection stage. Virology 286: 119–124.

25. JohnsonKE, KnipeDM (2010) Herpes simplex virus-1 infection causes the secretion of a type I interferon-antagonizing protein and inhibits signaling at or before Jak-1 activation. Virology 396: 21–29.

26. JohnsonKE, SongB, KnipeDM (2008) Role for herpes simplex virus 1 ICP27 in the inhibition of type I interferon signaling. Virology 374: 487–494.

27. CheeAV, RoizmanB (2004) Herpes simplex virus 1 gene products occlude the interferon signaling pathway at multiple sites. J Virol 78: 4185–4196.

28. UnterholznerL, KeatingSE, BaranM, HoranKA, JensenSB, et al. (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11: 997–1004.

29. BrazdaV, CoufalJ, LiaoJC, ArrowsmithCH (2012) Preferential binding of IFI16 protein to cruciform structure and superhelical DNA. Biochem Biophys Res Commun 422: 716–720.

30. TrapaniJA, BrowneKA, DawsonMJ, RamsayRG, EddyRL, et al. (1992) A novel gene constitutively expressed in human lymphoid cells is inducible with interferon-gamma in myeloid cells. Immunogenetics 36: 369–376.

31. TrapaniJA, DawsonM, ApostolidisVA, BrowneKA (1994) Genomic organization of IFI16, an interferon-inducible gene whose expression is associated with human myeloid cell differentiation: correlation of predicted protein domains with exon organization. Immunogenetics 40: 415–424.

32. JohnstoneRW, KerryJA, TrapaniJA (1998) The human interferon-inducible protein, IFI 16, is a repressor of transcription. J Biol Chem 273: 17172–17177.

33. JohnstoneRW, WeiW, GreenwayA, TrapaniJA (2000) Functional interaction between p53 and the interferon-inducible nucleoprotein IFI 16. Oncogene 19: 6033–6042.

34. KwakJC, OngusahaPP, OuchiT, LeeSW (2003) IFI16 as a negative regulator in the regulation of p53 and p21(Waf1). J Biol Chem 278: 40899–40904.

35. TawaraH, FujiuchiN, SironiJ, MartinS, AglipayJ, et al. (2008) Loss of p53-regulatory protein IFI16 induces NBS1 leading to activation of p53-mediated checkpoint by phosphorylation of p53 SER37. Front Biosci 13: 240–248.

36. OuchiM, OuchiT (2008) Role of IFI16 in DNA damage and checkpoint. Front Biosci 13: 236–239.

37. LiT, DinerBA, ChenJ, CristeaIM (2012) Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc Natl Acad Sci U S A 109: 10558–10563.

38. OrzalliMH, ConwellSE, BerriosC, DeCaprioJA, KnipeDM (2013) Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc Natl Acad Sci U S A 110: E4492–4501.

39. KerurN, VeettilMV, Sharma-WaliaN, BotteroV, SadagopanS, et al. (2011) IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9: 363–375.

40. AnsariMA, SinghVV, DuttaS, VeettilMV, DuttaD, et al. (2013) Constitutive interferon-inducible protein 16-inflammasome activation during Epstein-Barr virus latency I, II, and III in B and epithelial cells. J Virol 87: 8606–8623.

41. JakobsenMR, BakRO, AndersenA, BergRK, JensenSB, et al. (2013) IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci U S A 110: E4571–4580.

42. SinghVV, KerurN, BotteroV, DuttaS, ChakrabortyS, et al. (2013) Kaposi's Sarcoma-Associated Herpesvirus Latency in Endothelial and B cells Activates Interferon Gamma-Inducible Protein 16 (IFI16) Mediated Inflammasomes. J Virol 87: 4417–4431.

43. LiT, ChenJ, CristeaIM (2013) Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14: 591–599.

44. Cuchet-LourencoD, AndersonG, SloanE, OrrA, EverettRD (2013) 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 87: 13422–13432.

45. GarianoGR, Dell'OsteV, BronziniM, GattiD, LuganiniA, et al. (2012) The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog 8: e1002498.

46. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408.

47. KalamvokiM, RoizmanB (2014) HSV-1 degrades, stabilizes, requires, or is stung by STING depending on ICP0, the US3 protein kinase, and cell derivation. Proc Natl Acad Sci U S A 111: E611–617.

48. FujiuchiN, AglipayJA, OhtsukaT, MaeharaN, SahinF, et al. (2004) Requirement of IFI16 for the maximal activation of p53 induced by ionizing radiation. J Biol Chem 279: 20339–20344.

49. EverettRD, YoungDF, RandallRE, OrrA (2008) STAT-1- and IRF-3-dependent pathways are not essential for repression of ICP0-null mutant herpes simplex virus type 1 in human fibroblasts. J Virol 82: 8871–8881.

50. LiXL, BoyanapalliM, WeihuaX, KalvakolanuDV, HasselBA (1998) Induction of interferon synthesis and activation of interferon-stimulated genes by liposomal transfection reagents. J Interferon Cytokine Res 18: 947–952.

51. AltinkilicB, BrandnerG (1988) Interferon inhibits herpes simplex virus-specific translation: a reinvestigation. J Gen Virol 69: 3107–3112.

52. MittnachtS, StraubP, KirchnerH, JacobsenH (1988) Interferon treatment inhibits onset of herpes simplex virus immediate-early transcription. Virology 164: 201–210.

53. HornungV, AblasserA, Charrel-DennisM, BauernfeindF, HorvathG, et al. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458: 514–518.

54. MaliP, YangL, EsveltKM, AachJ, GuellM, et al. (2013) RNA-guided human genome engineering via Cas9. Science 339: 823–826.

55. VeresA, GosisBS, DingQ, CollinsR, RagavendranA, et al. (2014) Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 15: 27–30.

56. SmithC, GoreA, YanW, Abalde-AtristainL, LiZ, et al. (2014) Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 15: 12–13.

57. WuX, ScottDA, KrizAJ, ChiuAC, HsuPD, et al. (2014) Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat Biotechnol 32: 670–676.

58. FredrikssonS, GullbergM, JarviusJ, OlssonC, PietrasK, et al. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol 20: 473–477.

59. LesterJT, DeLucaNA (2011) Herpes simplex virus 1 ICP4 forms complexes with TFIID and mediator in virus-infected cells. J Virol 85: 5733–5744.

60. SpencerCA, KruhlakMJ, JenkinsHL, SunX, Bazett-JonesDP (2000) Mitotic transcription repression in vivo in the absence of nucleosomal chromatin condensation. J Cell Biol 150: 13–26.

61. JinT, PerryA, JiangJ, SmithP, CurryJA, et al. (2012) Structures of the HIN domain:DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36: 561–571.

62. SampathP, DelucaNA (2008) Binding of ICP4, TATA-binding protein, and RNA polymerase II to herpes simplex virus type 1 immediate-early, early, and late promoters in virus-infected cells. J Virol 82: 2339–2349.

63. MaruzuruY, FujiiH, OyamaM, Kozuka-HataH, KatoA, et al. (2013) Roles of p53 in herpes simplex virus 1 replication. J Virol 87: 9323–9332.

64. JonesKA, TjianR (1985) Sp1 binds to promoter sequences and activates herpes simplex virus ‘immediate-early’ gene transcription in vitro. Nature 317: 179–182.

65. HeS, WeintraubSJ (1998) Stepwise recruitment of components of the preinitiation complex by upstream activators in vivo. Mol Cell Biol 18: 2876–2883.

66. HallDB, StruhlK (2002) The VP16 activation domain interacts with multiple transcriptional components as determined by protein-protein cross-linking in vivo. J Biol Chem 277: 46043–46050.

67. SteinSC, Falck-PedersenE (2012) Sensing adenovirus infection: activation of interferon regulatory factor 3 in RAW 264.7 cells. J Virol 86: 4527–4537.

68. ShahA, FarooqAV, TiwariV, KimMJ, ShuklaD (2010) HSV-1 infection of human corneal epithelial cells: receptor-mediated entry and trends of re-infection. Mol Vis 16: 2476–2486.

69. MonroeKM, YangZ, JohnsonJR, GengX, DoitshG, et al. (2014) IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343: 428–432.

70. CristeaIM, MoormanNJ, TerhuneSS, CuevasCD, O'KeefeES, et al. (2010) Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J Virol 84: 7803–7814.

71. JohnstoneRW, TrapaniJA (1999) Transcription and growth regulatory functions of the HIN-200 family of proteins. Mol Cell Biol 19: 5833–5838.

72. AmraniY, TlibaO, ChoubeyD, HuangCD, KrymskayaVP, et al. (2003) IFN-gamma inhibits human airway smooth muscle cell proliferation by modulating the E2F-1/Rb pathway. Am J Physiol Lung Cell Mol Physiol 284: L1063–1071.

73. LiuCJ, ChangE, YuJ, CarlsonCS, PrazakL, et al. (2005) The interferon-inducible p204 protein acts as a transcriptional coactivator of Cbfa1 and enhances osteoblast differentiation. J Biol Chem 280: 2788–2796.

74. LuanY, YuXP, XuK, DingB, YuJ, et al. (2007) The retinoblastoma protein is an essential mediator of osteogenesis that links the p204 protein to the Cbfa1 transcription factor thereby increasing its activity. J Biol Chem 282: 16860–16870.

75. SongLL, PonomarevaL, ShenH, DuanX, AlimirahF, et al. (2010) Interferon-inducible IFI16, a negative regulator of cell growth, down-regulates expression of human telomerase reverse transcriptase (hTERT) gene. PLoS One 5: e8569.

76. KangHJ, LeeMH, KangHL, KimSH, AhnJR, et al. (2014) Differential regulation of estrogen receptor alpha expression in breast cancer cells by metastasis-associated protein 1. Cancer Res 74: 1484–1494.

77. Dell'osteV, GattiD, GugliesiF, De AndreaM, BawadekarM, et al. (2014) Innate nuclear sensor IFI16 translocates into the cytoplasm during early stage of in vitro HCMV infection and is entrapped in the egressing virions during late stage. J Virol 88: 6970–6982.

78. BarberGN (2011) STING-dependent signaling. Nat Immunol 12: 929–930.

79. AglipayJA, LeeSW, OkadaS, FujiuchiN, OhtsukaT, et al. (2003) A member of the Pyrin family, IFI16, is a novel BRCA1-associated protein involved in the p53-mediated apoptosis pathway. Oncogene 22: 8931–8938.

80. DuanX, PonomarevaL, VeerankiS, ChoubeyD (2011) IFI16 induction by glucose restriction in human fibroblasts contributes to autophagy through activation of the ATM/AMPK/p53 pathway. PLoS One 6: e19532.

81. PanD, FloresO, UmbachJL, PesolaJM, BentleyP, et al. (2014) A Neuron-Specific Host MicroRNA Targets Herpes Simplex Virus-1 ICP0 Expression and Promotes Latency. Cell Host Microbe 15: 446–456.

82. YaoF, SchafferPA (1995) An activity specified by the osteosarcoma line U2OS can substitute functionally for ICP0, a major regulatory protein of herpes simplex virus type 1. J Virol 69: 6249–6258.

83. CassadyKA, GrossM, RoizmanB (1998) The herpes simplex virus US11 protein effectively compensates for the gamma1(34.5) gene if present before activation of protein kinase R by precluding its phosphorylation and that of the alpha subunit of eukaryotic translation initiation factor 2. J Virol 72: 8620–8626.

84. Diaz-LatoudC, DiazJJ, Fabre-JoncaN, KindbeiterK, MadjarJJ, et al. (1997) Herpes simplex virus Us11 protein enhances recovery of protein synthesis and survival in heat shock treated HeLa cells. Cell Stress Chaperones 2: 119–131.

85. BenboudjemaL, MulveyM, GaoY, PimplikarSW, MohrI (2003) Association of the herpes simplex virus type 1 Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides. J Virol 77: 9192–9203.

86. Duc DodonM, MikaelianI, SergeantA, GazzoloL (2000) The herpes simplex virus 1 Us11 protein cooperates with suboptimal amounts of human immunodeficiency virus type 1 (HIV-1) Rev protein to rescue HIV-1 production. Virology 270: 43–53.

87. XingJ, WangS, LinR, MossmanKL, ZhengC (2012) Herpes simplex virus 1 tegument protein US11 downmodulates the RLR signaling pathway via direct interaction with RIG-I and MDA-5. J Virol 86: 3528–3540.

88. LussignolM, QuevalC, Bernet-CamardMF, Cotte-LaffitteJ, BeauI, et al. (2013) The herpes simplex virus 1 Us11 protein inhibits autophagy through its interaction with the protein kinase PKR. J Virol 87: 859–871.

89. Freed-PastorWA, PrivesC (2011) Dissimilar DNA binding by p53 in normal and tumor-derived cells. Cell Cycle 10: 4207.

90. Chaigne-DelalandeB, DeuveL, ReuzeauE, BasoniC, LafargeD, et al. (2006) RhoGTPases and p53 are involved in the morphological appearance and interferon-alpha response of hairy cells. Am J Pathol 168: 562–573.

91. Van MeirEG, RoemerK, DiserensAC, KikuchiT, RempelSA, et al. (1995) Single cell monitoring of growth arrest and morphological changes induced by transfer of wild-type p53 alleles to glioblastoma cells. Proc Natl Acad Sci U S A 92: 1008–1012.

92. ZambettiGP, OlsonD, LabowM, LevineAJ (1992) A mutant p53 protein is required for maintenance of the transformed phenotype in cells transformed with p53 plus ras cDNAs. Proc Natl Acad Sci U S A 89: 3952–3956.

93. SinghVV, DuttaD, AnsariMA, DuttaS, ChandranB (2014) Kaposi's sarcoma-associated herpesvirus induces the ATM and H2AX DNA damage response early during de novo infection of primary endothelial cells, which play roles in latency establishment. J Virol 88: 2821–2834.

94. SobyS, LaursenRR, OstergaardL, MelchjorsenJ (2012) HSV-1-induced chemokine expression via IFI16-dependent and IFI16-independent pathways in human monocyte-derived macrophages. Herpesviridae 3: 6.

95. KnipeDM, SpangAE (1982) Definition of a series of stages in the association of two herpesviral proteins with the cell nucleus. J Virol 43: 314–324.

96. RosenkeK, FortunatoEA (2004) Bromodeoxyuridine-labeled viral particles as a tool for visualization of the immediate-early events of human cytomegalovirus infection. J Virol 78: 7818–7822.

97. TiscorniaG, SingerO, VermaIM (2006) Production and purification of lentiviral vectors. Nat Protoc 1: 241–245.

98. BoydKE, FarnhamPJ (1999) Coexamination of site-specific transcription factor binding and promoter activity in living cells. Mol Cell Biol 19: 8393–8399.

99. ShangY, HuX, DiRenzoJ, LazarMA, BrownM (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103: 843–852.

100. KalamvokiM, RoizmanB (2010) Interwoven roles of cyclin D3 and cdk4 recruited by ICP0 and ICP4 in the expression of herpes simplex virus genes. J Virol 84: 9709–9717.

101. CookWJ, KramerMF, WalkerRM, BurwellTJ, HolmanHA, et al. (2004) Persistent expression of chemokine and chemokine receptor RNAs at primary and latent sites of herpes simplex virus 1 infection. Virol J 1: 5.

102. McNallyBA, TrgovcichJ, MaulGG, LiuY, ZhengP (2008) A role for cytoplasmic PML in cellular resistance to viral infection. PLoS One 3: e2277.