Viral gene products actively promote latent infection by epigenetic silencing mechanisms

Current Opinion in Virology

Volumn 23, Issue , 2017, Pages 68-74

  Knipe, David M ^a   Raja, Priya ^a   Lee, Jennifer ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BNRF1 PROTEIN; ICP0 PROTEIN; K BZIP PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; LATENT MEMBRANE PROTEIN 1; LONG UNTRANSLATED RNA; MICRORNA; NUCLEAR RNA; POLYADENYLATED NUCLEAR RNA; UL138 PROTEIN; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS RNA;

CYTOMEGALOVIRUS INFECTION; EPIGENETICS; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE PRODUCT; GENE SILENCING; HERPES SIMPLEX; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS GENE; VIRUS GENOME; VIRUS INFECTION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HERPESVIRIDAE; HOST PATHOGEN INTERACTION; PHYSIOLOGY; VIRUS LATENCY;

EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; GENE SILENCING; HERPESVIRIDAE; HIV; HOST-PATHOGEN INTERACTIONS; VIRAL PROTEINS; VIRUS LATENCY;

EID: 85017480054     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2017.03.010     Document Type: Review

References (56)

1. 1 Roizman, B., Sears, A., An Inquiry into the mechanisms of herpes simplex virus latency. Annu. Rev. Microbiol. 41 (1987), 543–571.
2. 2 Stevens, J.G., Cook, M.L., Latent herpes simplex virus in spinal ganglia of mice. Science 173 (1971), 843–845.
3. 3 Mark, K.E., Wald, A., Magaret, A.S., Selke, S., Olin, L., Huang, M.L., Corey, L., Rapidly cleared episodes of herpes simplex virus reactivation in immunocompetent adults. J. Infect. Dis. 198 (2008), 1141–1149.
4. 4 Schiffer, J.T., Abu-Raddad, L., Mark, K.E., Zhu, J., Selke, S., Magaret, A., Wald, A., Corey, L., Frequent release of low amounts of herpes simplex virus from neurons: results of a mathematical model. Sci. Transl. Med., 1, 2009, 7ra16.
5. 5 Kramer, M.F., Coen, D.M., Quantification of transcripts from the ICP4 and thymidine kinase genes in mouse ganglia latently infected with herpes simplex virus. J. Virol. 69 (1995), 1389–1399.
6. 6 Kramer, M.F., Chen, S.H., Knipe, D.M., Coen, D.M., Accumulation of viral transcripts and DNA during establishment of latency by herpes simplex virus. J. Virol. 72 (1998), 1177–1185.
7. 7 Feldman, L.T., Ellison, A.R., Voytek, C.C., Yang, L., Krause, P., Margolis, T.P., Spontaneous molecular reactivation of herpes simplex virus type 1 latency in mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 978–983.
8. 8 Knipe, D.M., Lieberman, P.M., Jung, J.U., McBride, A.A., Morris, K.V., Ott, M., Margolis, D., Nieto, A., Nevels, M., Parks, R.J., et al. Snapshots: chromatin control of viral infection. Virology 435 (2013), 141–156.
9. 9 Lester, J.T., DeLuca, N.A., Herpes simplex virus 1 ICP4 forms complexes with TFIID and mediator in virus-infected cells. J. Virol. 85 (2011), 5733–5744.
10. 10 Cliffe, A.R., Knipe, D.M., Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J. Virol. 82 (2008), 12030–12038.
11. 11 Lee, J.S., Raja, P., Knipe, D.M., Herpesviral ICP0 protein promotes two waves of heterochromatin removal on an early viral promoter during lytic infection. MBio 7 (2016), e02007–02015.
12. 12 Roizman, B., Knipe, D.M., Whitley, R.J., Herpes simplex viruses. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th edn, 2013, Lippincott Williams & Wilkins, 1823–1897.
13. 13 Kristie, T.M., Vogel, J.L., Sears, A.E., Nuclear localization of the C1 factor (host cell factor) in sensory neurons correlates with reactivation of herpes simplex virus from latency. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 1229–1233.
14. 14•• Wang, Q.-Y., Zhou, C., Johnson, K.E., Colgrove, R.C., Coen, D.M., Knipe, D.M., 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 (2005), 16055–16059 This was the first paper showing that a viral gene product, the HSV LAT, promotes heterochromatin on the viral genome.
15. 15•• Garber, D.A., Schaffer, P.A., Knipe, D.M., A LAT-associated function reduces productive-cycle gene expression during acute infection of murine sensory neurons with herpes simplex virus type 1. J. Virol. 71 (1997), 5885–5893 This was the first paper showing that a viral gene product, the HSV LAT, inhibits lytic gene expression during establishment of latent infection.
16. 16•• Chen, S.H., Kramer, M.F., Schaffer, P.A., Coen, D.M., A viral function represses accumulation of transcripts from productive-cycle genes in mouse ganglia latently infected with herpes simplex virus. J. Virol. 71 (1997), 5878–5884 This was the first paper showing that a viral gene product, the HSV LAT, inhibits lytic gene expression during latent infection.
17. 17 Kwiatkowski, D.L., Thompson, H.W., Bloom, D.C., The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. J. Virol. 83 (2009), 8173–8181.
18. 18 Cliffe, A.R., Garber, D.A., Knipe, D.M., Transcription of the herpes simplex virus latency-associated transcript promotes the formation of facultative heterochromatin on lytic promoters. J. Virol. 83 (2009), 8182–8190.
19. 19 Nicoll, M.P., Proenca, J.T., Connor, V., Efstathiou, S., Influence of herpes simplex virus 1 latency-associated transcripts on the establishment and maintenance of latency in the ROSA26R reporter mouse model. J. Virol. 86 (2012), 8848–8858.
20. 20 Nicoll, M.P., Hann, W., Shivkumar, M., Harman, L.E., Connor, V., Coleman, H.M., Proenca, J.T., Efstathiou, S., The HSV-1 latency-associated transcript functions to repress latent phase lytic gene expression and suppress virus reactivation from latently infected neurons. PLoS Pathog., 12, 2016, e1005539.
21. 21 Davidovich, C., Cech, T.R., The recruitment of chromatin modifiers by long noncoding RNAs: lessons from PRC2. RNA 21 (2015), 2007–2022.
22. 22 Cliffe, A.R., Coen, D.M., Knipe, D.M., Kinetics of facultative heterochromatin and polycomb group protein association with the herpes simplex viral genome during establishment of latent infection. MBio 4 (2013), e00590–00512.
23. 23•• Raja, P., Lee, J.S., Pan, D., Pesola, J.M., Coen, D.M., Knipe, D.M., A herpesviral lytic protein regulates the structure of latent viral chromatin. MBio, 7, 2016 This was the first paper showing that a lytic viral gene product promotes heterochromatin during latent infection.
24. 24 Proenca, J.T., Coleman, H.M., Nicoll, M.P., Connor, V., Preston, C.M., Arthur, J., Efstathiou, S., An investigation of herpes simplex virus promoter activity compatible with latency establishment reveals VP16-independent activation of immediate-early promoters in sensory neurones. J. Gen. Virol. 92 (2011), 2575–2585.
25. 25 Wilcox, C.L., Smith, R.L., Everett, R.D., Mysofski, D., The herpes simplex virus type 1 immediate-early protein ICP0 is necessary for the efficient establishment of latent infection. J. Virol. 71 (1997), 6777–6785.
26. 26 Mocarski, E.S., Shenk, T., Griffiths, P.D., Pass, R.F., Cytomegaloviruses. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th edn, 2013, Lippincott Williams & Wilkins.
27. 27 Hummel, M., Yan, S., Li, Z., Varghese, T.K., Abecassis, M., Transcriptional reactivation of murine cytomegalovirus ie gene expression by 5-aza-2′-deoxycytidine and trichostatin A in latently infected cells despite lack of methylation of the major immediate-early promoter. J. Gen. Virol. 88 (2007), 1097–1102.
28. 28 Reeves, M.B., Sinclair, J.H., Analysis of latent viral gene expression in natural and experimental latency models of human cytomegalovirus and its correlation with histone modifications at a latent promoter. J. Gen. Virol. 91 (2010), 599–604.
29. 28a Saffert, R.T., Kalejta, R.F., Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J. Virol. 80 (2006), 3863–3871.
30. 29 Kalejta, R.F., Bechtel, J.T., Shenk, T., Human cytomegalovirus pp71 stimulates cell cycle progression by inducing the proteasome-dependent degradation of the retinoblastoma family of tumor suppressors. Mol. Cell Biol. 23 (2003), 1885–1895.
31. 30 Lee, S.H., Albright, E.R., Lee, J.H., Jacobs, D., Kalejta, R.F., Cellular defense against latent colonization foiled by human cytomegalovirus UL138 protein. Sci. Adv., 1, 2015, e1501164.
32. 31 Poole, E., Sinclair, J., Sleepless latency of human cytomegalovirus. Med. Microbiol. Immunol. 204 (2015), 421–429.
33. 32 Rossetto, C.C., Tarrant-Elorza, M., Pari, G.S., Cis and trans acting factors involved in human cytomegalovirus experimental and natural latent infection of CD14 (+) monocytes and CD34 (+) cells. PLoS Pathog., 9, 2013, e1003366.
34. 33 Longnecker, R., Kieff, E., Cohen, J., Epstein–Barr virus. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th edn, 2013, Lippincott Williams & Wilkins, 1898–1959.
35. 34 Tsai, K., Chan, L., Gibeault, R., Conn, K., Dheekollu, J., Domsic, J., Marmorstein, R., Schang, L.M., Lieberman, P.M., Viral reprogramming of the Daxx histone H3.3 chaperone during early Epstein–Barr virus infection. J. Virol. 88 (2014), 14350–14363.
36. 35•• Huang, H., Deng, Z., Vladimirova, O., Wiedmer, A., Lu, F., Lieberman, P.M., Patel, D.J., Structural basis underlying viral hijacking of a histone chaperone complex. Nat. Commun., 7, 2016, 12707 This was the first paper showing that a viral lytic protein can promote expression of viral latent proteins during establishment of latent infection.
37. 36 Kim, H., Choi, H., Lee, S.K., Epstein–Barr virus microRNA miR-BART20-5p suppresses lytic induction by inhibiting BAD-mediated caspase-3-dependent apoptosis. J. Virol. 90 (2015), 1359–11368.
38. 37 Qiu, H., Huang, F., Gong, J., Xiao, H., Sun, B.L., Yang, R.G., TRIM22 can activate the noncanonical NF-kappaB pathway by affecting IKKalpha. J. Recept. Signal Transduct. Res., 2014, 1–6.
39. 38 Iizasa, H., Wulff, B.E., Alla, N.R., Maragkakis, M., Megraw, M., Hatzigeorgiou, A., Iwakiri, D., Takada, K., Wiedmer, A., Showe, L., et al. Editing of Epstein–Barr virus-encoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency. J. Biol. Chem. 285 (2010), 33358–33370.
40. 39 Bentz, G.L., Moss, C.R. 2nd, Whitehurst, C.B., Moody, C.A., Pagano, J.S., LMP1-induced sumoylation influences the maintenance of Epstein–Barr virus latency through KAP1. J. Virol. 89 (2015), 7465–7477.
41. 40 Damania, B., Cesarman, E., Kaposi's sarcoma-associated herpesvirus. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th edn, 2013, Lippincott-Raven Publishers, 2080–2128.
42. 41 Gunther, T., Schreiner, S., Dobner, T., Tessmer, U., Grundhoff, A., Influence of ND10 components on epigenetic determinants of early KSHV latency establishment. PLoS Pathog., 10, 2014, e1004274.
43. 42 Gupta, N., Thakker, S., Verma, S.C., KSHV encoded LANA recruits Nucleosome Assembly Protein NAP1L1 for regulating viral DNA replication and transcription. Sci. Rep., 6, 2016, 32633.
44. 43•• Toth, Z., Papp, B., Brulois, K., Choi, Y.J., Gao, S.J., Jung, J.U., LANA-mediated recruitment of host polycomb repressive complexes onto the KSHV genome during de novo infection. PLoS Pathog., 12, 2016, e1005878 This was the first paper showing that a viral protein, KSHV LANA, can play a direct role in promoting heterochromatin on the viral genome.
45. 44 Gjyshi, O., Roy, A., Dutta, S., Veettil, M.V., Dutta, D., Chandran, B., Activated Nrf2 Interacts with Kaposi's sarcoma-associated herpesvirus latency protein LANA-1 and host protein KAP1 to mediate global lytic gene repression. J. Virol. 89 (2015), 7874–7892.
46. 45 Rossetto, C.C., Tarrant-Elorza, M., Verma, S., Purushothaman, P., Pari, G.S., Regulation of viral and cellular gene expression by Kaposi's sarcoma-associated herpesvirus polyadenylated nuclear RNA. J. Virol. 87 (2013), 5540–5553.
47. 46 Full, F., Jungnickl, D., Reuter, N., Bogner, E., Brulois, K., Scholz, B., Sturzl, M., Myoung, J., Jung, J.U., Stamminger, T., et al. Kaposi's sarcoma associated herpesvirus tegument protein ORF75 is essential for viral lytic replication and plays a critical role in the antagonization of ND10-instituted intrinsic immunity. PLoS Pathog., 10, 2014, e1003863.
48. 47 Yang, W.S., Hsu, H.W., Campbell, M., Cheng, C.Y., Chang, P.C., K-bZIP mediated SUMO-2/3 specific modification on the KSHV genome negatively regulates lytic gene expression and viral reactivation. PLoS Pathog., 11, 2015, e1005051.
49. 48 Bellare, P., Ganem, D., Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation. Cell Host Microbe 6 (2009), 570–575.
50. 49 Lin, X., Liang, D., He, Z., Deng, Q., Robertson, E.S., Lan, K., miR-K12-7-5p encoded by Kaposi's sarcoma-associated herpesvirus stabilizes the latent state by targeting viral ORF50/RTA. PLoS One, 6, 2011, e16224.
51. 50 Freed, E.O., Martin, M.A., Human immunodeficiency viruses: replication. Knipe, D.M., Howley, P.M., (eds.) Fields Virology, 6th edn, 2013, Lippincott Williams & Wilkins, 1502–1561.
52. 51 Friedman, J., Cho, W.K., Chu, C.K., Keedy, K.S., Archin, N.M., Margolis, D.M., Karn, J., Epigenetic silencing of HIV-1 by the histone H3 lysine 27 methyltransferase enhancer of Zeste 2. J. Virol. 85 (2011), 9078–9089.
53. 52 du Chene, I., Basyuk, E., Lin, Y.L., Triboulet, R., Knezevich, A., Chable-Bessia, C., Mettling, C., Baillat, V., Reynes, J., Corbeau, P., et al. Suv39H1 and HP1gamma are responsible for 1 chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J. 26 (2007), 424–435.
54. 53 Saayman, S., Ackley, A., Turner, A.M., Famiglietti, M., Bosque, A., Clemson, M., Planelles, V., Morris, K.V., An HIV-encoded antisense long noncoding RNA epigenetically regulates viral transcription. Mol. Ther. 22 (2014), 1164–1175.
55. 54 Dahabieh, M.S., Battivelli, E., Verdin, E., Understanding HIV latency: the road to an HIV cure. Annu. Rev. Med. 66 (2015), 407–421.
56. 55 Hill, J.M., Quenelle, D.C., Cardin, R.D., Vogel, J.L., Clement, C., Bravo, F.J., Foster, T.P., Bosch-Marce, M., Raja, P., Lee, J.S., et al. Inhibition of LSD1 reduces herpesvirus infection, shedding, and recurrence by promoting epigenetic suppression of viral genomes. Sci. Transl. Med., 6, 2014, 265ra169.