Temporal viral genome-protein interactions define distinct stages of productive herpesviral infection

mBio

Volumn 9, Issue 4, 2018, Pages

  Dembowski, Jill A ^a   Deluca, Neal A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Affinity purification; DNA damage; DNA repair; Herpes simplex virus; ICP4; iPOND; Mediator; Transcription

Indexed keywords

ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA DAMAGE RESPONSE; DNA REPLICATION; GENE INTERACTION; GENE PRODUCT; HUMAN ALPHAHERPESVIRUS 1; ISOTOPE LABELING; LIFE CYCLE; LIMIT OF DETECTION; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEOMICS; STABLE ISOTOPE LABELING OF AMINO ACIDS IN CELL CULTURE; VIRUS REPLICATION; VIRUS TRANSCRIPTION; BIOSYNTHESIS; CELL LINE; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; GENETIC TRANSCRIPTION; GENETICS; HERPES SIMPLEX; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS ASSEMBLY; VIRUS ENTRY; VIRUS GENOME;

HERPES SIMPLEX VIRUS, TYPE 1 PROTEIN ICP4; IMMEDIATE EARLY PROTEIN; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR; VIRAL PROTEIN; VIRUS DNA;

CELL LINE; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA, VIRAL; GENOME, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIRAL PROTEINS; VIRUS ASSEMBLY; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 85055149335     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01182-18     Document Type: Article

References (61)

1. McGeoch DJ, Rixon FJ, Davison AJ. 2006. Topics in herpesvirus genomics and evolution. Virus Res 117:90 –104. https://doi.org/10.1016/j.virusres.2006.01.002.
2. Roizman B, Whitley RJ. 2013. An inquiry into the molecular basis of HSV latency and reactivation. Annu Rev Microbiol 67:355–374. https://doi.org/10.1146/annurev-micro-092412-155654.
3. Tognon M, Furlong D, Conley AJ, Roizman B. 1981. Molecular genetics of herpes simplex virus. V. Characterization of a mutant defective in ability to form plaques at low temperatures and in a viral fraction which prevents accumulation of coreless capsids at nuclear pores late in infection. J Virol 40:870–880.
4. Maul GG, Guldner HH, Spivack JG. 1993. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J Gen Virol 74:2679 –2690. https://doi.org/10.1099/0022-1317-74-12-2679.
5. Everett RD, Rechter S, Papior P, Tavalai N, Stamminger T, Orr A. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J Virol 80:7995– 8005. https://doi.org/10.1128/JVI.00734-06.
6. Honess RW, Roizman B. 1974. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol 14:8 –19.
7. Honess RW, Roizman B. 1975. Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc Natl Acad Sci U S A 72:1276 –1280. https://doi.org/10.1073/pnas.72.4.1276.
8. Batterson W, Roizman B. 1983. Characterization of the herpes simplex virion-associated factor responsible for the induction of alpha genes. J Virol 46:371–377.
9. Campbell ME, Palfreyman JW, Preston CM. 1984. Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate early transcription. J Mol Biol 180:1–19. https://doi.org/10.1016/0022-2836(84)90427-3.
10. Watson RJ, Clements JB. 1980. A herpes simplex virus type 1 function continuously required for early and late virus RNA synthesis. Nature 285:329 –330. https://doi.org/10.1038/285329a0.
11. Dixon RA, Schaffer PA. 1980. Fine-structure mapping and functional analysis of temperature-sensitive mutants in the gene encoding the herpes simplex virus type 1 immediate early protein VP175. J Virol 36:189 –203.
12. DeLuca NA, McCarthy AM, Schaffer PA. 1985. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4. J Virol 56:558 –570.
13. Sirbu BM, Couch FB, Cortez D. 2012. Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat Protoc 7:594 – 605. https://doi.org/10.1038/nprot.2012.010.
14. Dembowski JA, DeLuca NA. 2015. Selective recruitment of nuclear factors to productively replicating herpes simplex virus genomes. PLoS Pathog 11:e1004939. https://doi.org/10.1371/journal.ppat.1004939.
15. Dembowski JA, Dremel SE, DeLuca NA. 2017. Replication-coupled recruitment of viral and cellular factors to herpes simplex virus type 1 replication forks for the maintenance and expression of viral genomes. PLoS Pathog 13:e1006166. https://doi.org/10.1371/journal.ppat.1006166.
16. Alandijany T, Roberts APE, Conn KL, Loney C, McFarlane S, Orr A, Boutell C. 2018. Distinct temporal roles for the promyelocytic leukaemia (PML) protein in the sequential regulation of intracellular host immunity to HSV-1 infection. PLoS Pathog 14:e1006769. https://doi.org/10.1371/journal.ppat.1006769.
17. Sekine E, Schmidt N, Gaboriau D, O’Hare P. 2017. Spatiotemporal dynamics of HSV genome nuclear entry and compaction state transitions using bioorthogonal chemistry and super-resolution microscopy. PLoS Pathog 13:e1006721. https://doi.org/10.1371/journal.ppat.1006721.
18. Wang IH, Suomalainen M, Andriasyan V, Kilcher S, Mercer J, Neef A, Luedtke NW, Greber UF. 2013. Tracking viral genomes in host cells at single-molecule resolution. Cell Host Microbe 14:468 – 480. https://doi.org/10.1016/j.chom.2013.09.004.
19. Dembowski JA, DeLuca NA. 2017. Purification of viral DNA for the identification of associated viral and cellular proteins. J Vis Exp 2017(126):e56374. https://doi.org/10.3791/56374.
20. Harkness JM, Kader M, DeLuca NA. 2014. Transcription of the herpes simplex virus 1 genome during productive and quiescent infection of neuronal and nonneuronal cells. J Virol 88:6847– 6861. https://doi.org/10.1128/JVI.00516-14.
21. Gibson W, Roizman B. 1972. Proteins specified by herpes simplex virus. VIII. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J Virol 10:1044 –1052.
22. Newcomb WW, Trus BL, Booy FP, Steven AC, Wall JS, Brown JC. 1993. Structure of the herpes simplex virus capsid. Molecular composition of the pentons and the triplexes. J Mol Biol 232:499 –511. https://doi.org/10.1006/jmbi.1993.1406.
23. Snel B, Lehmann G, Bork P, Huynen MA. 2000. STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 28:3442–3444. https://doi.org/10.1093/nar/28.18.3442.
24. Ishov AM, Maul GG. 1996. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J Cell Biol 134:815–826. https://doi.org/10.1083/jcb.134.4.815.
25. Lester JT, DeLuca NA. 2011. Herpes simplex virus 1 ICP4 forms complexes with TFIID and mediator in virus-infected cells. J Virol 85: 5733–5744. https://doi.org/10.1128/JVI.00385-11.
26. Fox HL, Dembowski JA, DeLuca NA. 2017. A herpesviral immediate early protein promotes transcription elongation of viral transcripts. mBio 8:e00745-17. https://doi.org/10.1128/mBio.00745-17.
27. Silva L, Cliffe A, Chang L, Knipe DM. 2008. Role for A-type lamins in herpesviral DNA targeting and heterochromatin modulation. PLoS Pathog 4:e1000071. https://doi.org/10.1371/journal.ppat.1000071.
28. DeLuca NA, Schaffer PA. 1988. Physical and functional domains of the herpes simplex virus transcriptional regulatory protein ICP4. J Virol 62:732–743.
29. Sanders I, Boyer M, Fraser NW. 2015. Early nucleosome deposition on, and replication of, HSV DNA requires cell factor PCNA. J Neurovirol 21:358 –369. https://doi.org/10.1007/s13365-015-0321-7.
30. Lilley CE, Carson CT, Muotri AR, Gage FH, Weitzman MD. 2005. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc Natl Acad Sci U S A 102:5844–5849. https://doi.org/10.1073/pnas.0501916102.
31. Quinlan MP, Chen LB, Knipe DM. 1984. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell 36:857– 868. https://doi.org/10.1016/0092-8674(84)90035-7.
32. Wilkie NM. 1973. The synthesis and substructure of herpesvirus DNA: the distribution of alkali-labile single strand interruptions in HSV-1 DNA. J Gen Virol 21:453– 467. https://doi.org/10.1099/0022-1317-21-3-453.
33. Everett RD, Freemont P, Saitoh H, Dasso M, Orr A, Kathoria M, Parkinson J. 1998. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110-and proteasome-dependent loss of several PML isoforms. J Virol 72:6581–6591.
34. Fortunato EA, Spector DH. 1998. p53 and RPA are sequestered in viral replication centers in the nuclei of cells infected with human cytomegalovirus. J Virol 72:2033–2039.
35. Wilcock D, Lane DP. 1991. Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349:429 – 431. https://doi.org/10.1038/349429a0.
36. Dellaire G, Bazett-Jones DP. 2004. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26:963–977. https://doi.org/10.1002/bies.20089.
37. Kim MY, Zhang T, Kraus WL. 2005. Poly(ADP-ribosyl)ation by PARP-1: “PAR-laying” NAD+ into a nuclear signal. Genes Dev 19:1951–1967. https://doi.org/10.1101/gad.1331805.
38. Everett RD. 2016. Dynamic response of IFI16 and promyelocytic leukemia nuclear body components to herpes simplex virus 1 infection. J Virol 90:167–179. https://doi.org/10.1128/JVI.02249-15.
39. Li T, Diner BA, Chen J, Cristea IM. 2012. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc Natl Acad Sci U S A 109:10558 –10563. https://doi.org/10.1073/pnas.1203447109.
40. Orzalli MH, DeLuca NA, Knipe DM. 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 –E3017. https://doi.org/10.1073/pnas.1211302109.
41. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, Bowie AG. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997–1004. https://doi.org/10.1038/ni.1932.
42. Cuchet-Lourenço D, Anderson G, Sloan E, Orr A, Everett RD. 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. https://doi.org/10.1128/JVI.02474-13.
43. Orzalli MH, Broekema NM, Diner BA, Hancks DC, Elde NC, Cristea IM, Knipe DM. 2015. cGAS-mediated stabilization of IFI16 promotes innate signaling during herpes simplex virus infection. Proc Natl Acad Sci U S A 112:E1773–E1781. https://doi.org/10.1073/pnas.1424637112.
44. Parkinson J, Lees-Miller SP, Everett RD. 1999. 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 73:650 – 657.
45. Lilley CE, Chaurushiya MS, Boutell C, Landry S, Suh J, Panier S, Everett RD, Stewart GS, Durocher D, Weitzman MD. 2010. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J 29:943–955. https://doi.org/10.1038/emboj.2009.400.
46. Mohni KN, Mastrocola AS, Bai P, Weller SK, Heinen CD. 2011. DNA mismatch repair proteins are required for efficient herpes simplex virus 1 replication. J Virol 85:12241–12253. https://doi.org/10.1128/JVI.05487-11.
47. Balasubramanian N, Bai P, Buchek G, Korza G, Weller SK. 2010. Physical interaction between the herpes simplex virus type 1 exonuclease, UL12, and the DNA double-strand break-sensing MRN complex. J Virol 84: 12504 –12514. https://doi.org/10.1128/JVI.01506-10.
48. Allen BL, Taatjes DJ. 2015. The Mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol 16:155–166. https://doi.org/10.1038/nrm3951.
49. Gardini A, Baillat D, Cesaroni M, Hu D, Marinis JM, Wagner EJ, Lazar MA, Shilatifard A, Shiekhattar R. 2014. Integrator regulates transcriptional initiation and pause release following activation. Mol Cell 56:128 –139. https://doi.org/10.1016/j.molcel.2014.08.004.
50. Stadelmayer B, Micas G, Gamot A, Martin P, Malirat N, Koval S, Raffel R, Sobhian B, Severac D, Rialle S, Parrinello H, Cuvier O, Benkirane M. 2014. Integrator complex regulates NELF-mediated RNA polymerase II pause/ release and processivity at coding genes. Nat Commun 5:5531. https://doi.org/10.1038/ncomms6531.
51. Lai F, Gardini A, Zhang A, Shiekhattar R. 2015. Integrator mediates the biogenesis of enhancer RNAs. Nature 525:399 – 403. https://doi.org/10.1038/nature14906.
52. Chen J, Wagner EJ. 2010. snRNA 3ʹ end formation: the dawn of the Integrator complex. Biochem Soc Trans 38:1082–1087. https://doi.org/10.1042/BST0381082.
53. Cazalla D, Xie M, Steitz JA. 2011. A primate herpesvirus uses the integrator complex to generate viral microRNAs. Mol Cell 43:982–992. https://doi.org/10.1016/j.molcel.2011.07.025.
54. Carrozza MJ, DeLuca NA. 1996. Interaction of the viral activator protein ICP4 with TFIID through TAF250. Mol Cell Biol 16:3085–3093. https://doi.org/10.1128/MCB.16.6.3085.
55. Wagner LM, DeLuca NA. 2013. Temporal association of herpes simplex virus ICP4 with cellular complexes functioning at multiple steps in PolII transcription. PLoS One 8:e78242. https://doi.org/10.1371/journal.pone.0078242.
56. Sampath P, DeLuca NA. 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. https://doi.org/10.1128/JVI.02459-07.
57. Grondin B, DeLuca N. 2000. Herpes simplex virus type 1 ICP4 promotes transcription preinitiation complex formation by enhancing the binding of TFIID to DNA. J Virol 74:11504 –11510. https://doi.org/10.1128/JVI.74.24.11504-11510.2000.
58. Lacasse JJ, Schang LM. 2012. Herpes simplex virus 1 DNA is in unstable nucleosomes throughout the lytic infection cycle, and the instability of the nucleosomes is independent of DNA replication. J Virol 86: 11287–11300. https://doi.org/10.1128/JVI.01468-12.
59. Showalter SD, Zweig M, Hampar B. 1981. Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4. Infect Immun 34:684 – 692.
60. Shepard AA, Tolentino P, DeLuca NA. 1990. trans-Dominant inhibition of herpes simplex virus transcriptional regulatory protein ICP4 by heterodimer formation. J Virol 64:3916 –3926.
61. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, Li T, Miteva YV, Hauri S, Sardiu ME, Low TY, Halim VA, Bagshaw RD, Hubner NC, Al-Hakim A, Bouchard A, Faubert D, Fermin D, Dunham WH, Goud-reault M, Lin ZY, Badillo BG, Pawson T, Durocher D, Coulombe B, Aebersold R, Superti-Furga G, Colinge J, Heck AJ, Choi H, Gstaiger M, Mohammed S, Cristea IM, Bennett KL, Washburn MP, Raught B, Ewing RM, Gingras AC, Nesvizhskii AI. 2013. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10:730 –736. https://doi.org/10.1038/nmeth.2557.