Analysis of the functional interchange between the IE1 and pp71 proteins of human cytomegalovirus and ICP0 of herpes simplex virus 1

Journal of Virology

Volumn 89, Issue 6, 2015, Pages 3062-3075

  Lu, Yongxu ^a   Everett, Roger D ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN; IMMEDIATE EARLY PROTEIN ICP 0; PROTEIN IE1; PROTEIN IE2; PROTEIN PP71; UNCLASSIFIED DRUG; VIRUS PROTEIN; CYTOMEGALOVIRUS PHOSPHOPROTEIN 71KDA; IE1 PROTEIN, CYTOMEGALOVIRUS; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE; VIRAL PROTEIN; VMW110 PROTEIN, HUMAN HERPESVIRUS 1;

ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS GENE; VIRUS MORPHOLOGY; VIRUS PLAQUE; VIRUS REPLICATION; WILD TYPE; CELL LINE; CYTOMEGALOVIRUS; ENZYMOLOGY; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HERPES SIMPLEX; METABOLISM; VIROLOGY;

HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 5; PRIMATES;

CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FIBROBLASTS; GENE EXPRESSION REGULATION, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; PROTEIN BINDING; UBIQUITIN-PROTEIN LIGASES; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84923210248     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03480-14     Document Type: Article

References (72)

1. Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Strauss SE (ed). 2007. Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Reddehase MJ. 2013. Cytomegaloviruses: from molecular pathogenesis to intervention. Caister Academic Press, Norfolk, United Kingdom.
3. Weller SK. 2011. Alphaherpesviruses: molecular virology. Caister Academic Press, Norfolk, United Kingdom.
4. DeLuca NA. 2011. Functions and mechanism of action of the herpes simplex virus regulatory protein, ICP4, p 17-38. In Weller SK (ed), Alphaherpesviruses: molecular virology. Caister Academic Press, Norfolk, United Kingdom.
5. Wysocka J, Herr W. 2003. The herpes simplex virus VP16-induced complex: the makings of a regulatory switch. Trends Biochem Sci 28:294-304. http://dx.doi.org/10.1016/S0968-0004(03)00088-4.
6. Yan N, Chen ZJ. 2012. Intrinsic antiviral immunity. Nat Immunol 13: 214-222. http://dx.doi.org/10.1038/ni.2229.
7. Boutell C, Everett RD. 2013. Regulation of alphaherpesvirus infections by the ICP0 family of proteins. J Gen Virol 94:465-481. http://dx.doi.org/10 .1099/vir.0.048900-0.
8. Everett RD, Boutell C, Hale BG. 2013. Interplay between viruses and host sumoylation pathways. Nat Rev Microbiol 11:400-411. http://dx.doi.org/10.1038/nrmicro3015.
9. Everett RD, Chelbi-Alix MK. 2007. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89:819-830. http://dx.doi.org/10.1016/j.biochi.2007.01.004.
10. Schreiner S, Wodrich H. 2013. Virion factors that target Daxx to overcome intrinsic immunity. J Virol 87:10412-10422. http://dx.doi.org/10 .1128/JVI.00425-13.
11. Tavalai N, Stamminger T. 2008. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim Biophys Acta 1783: 2207-2221. http://dx.doi.org/10.1016/j.bbamcr.2008.08.004.
12. Bernardi R, Pandolfi PP. 2007. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8:1006-1016. http://dx.doi.org/10.1038/nrm2277.
13. Geoffroy MC, Chelbi-Alix MK. 2011. Role of promyelocytic leukemia protein in host antiviral defense. J Interferon Cytokine Res 31:145-158. http://dx.doi.org/10.1089/jir.2010.0111.
14. Everett RD, Murray J. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J Virol 79:5078-5089. http://dx.doi.org/10.1128/JVI.79.8 .5078-5089.2005.
15. Hagglund R, Roizman B. 2004. Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J Virol 78:2169-2178. http://dx.doi .org/10.1128/JVI.78.5.2169-2178.2004.
16. Smith MC, Boutell C, Davido DJ. 2011. HSV-1 ICP0: paving the way for viral replication. Future Virol 6:421-429. http://dx.doi.org/10 .2217/fvl.11.24.
17. Boutell C, Cuchet-Lourenco D, Vanni E, Orr A, Glass M, McFarlane S, Everett RD. 2011. A viral ubiquitin ligase has substrate preferential SUMOtargeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathog 7:e1002245. http://dx.doi.org/10.1371/journal.ppat .1002245.
18. Cuchet-Lourenco D, Boutell C, Lukashchuk V, Grant K, Sykes A, Murray J, Orr A, Everett RD. 2011. SUMO pathway dependent recruitment of cellular repressors to herpes simplex virus type 1 genomes. PLoS Pathog 7:e1002123. http://dx.doi.org/10.1371/journal.ppat.1002123.
19. Cuchet-Lourenco D, Vanni E, Glass M, Orr A, Everett RD. 2012. Herpes simplex virus 1 ubiquitin ligase ICP0 interacts with PML isoform I and induces its SUMO-independent degradation. J Virol 86:11209-11222. http://dx.doi.org/10.1128/JVI.01145-12.
20. 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.
21. Lukashchuk V, Orr A, Everett RD. 2010. Regulation of ICP0 null mutant HSV-1 infection by ND10 components ATRX and hDaxx. J Virol 84: 4026-4040. http://dx.doi.org/10.1128/JVI.02597-09.
22. Everett RD. 2011. The role of ICP0 in counteracting intrinsic cellular resistance to virus infection, p 39-50. In Weller SK (ed), Alphaherpesviruses: molecular virology. Caister Academic Press, Norfolk, United Kingdom.
23. Cantrell SR, Bresnahan WA. 2006. Human cytomegalovirus (HCMV) UL82 gene product (pp71) relieves hDaxx-mediated repression of HCMV replication. J Virol 80:6188-6191. http://dx.doi.org/10.1128/JVI.02676-05.
24. Lukashchuk V, McFarlane S, Everett RD, Preston CM. 2008. Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection. J Virol 82: 12543-12554. http://dx.doi.org/10.1128/JVI.01215-08.
25. Preston CM, Nicholl MJ. 2006. Role of the cellular protein hDaxx in human cytomegalovirus immediate-early gene expression. J Gen Virol 87:1113-1121. http://dx.doi.org/10.1099/vir.0.81566-0.
26. Saffert RT, Kalejta RF. 2006. 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 80:3863-3871. http://dx.doi.org/10.1128/JVI.80.8.3863-3871.2006.
27. Woodhall DL, Groves IJ, Reeves MB, Wilkinson G, Sinclair JH. 2006. Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J Biol Chem 281:37652-37660. http://dx .doi.org/10.1074/jbc.M604273200.
28. Hofmann H, Sindre H, Stamminger T. 2002. Functional interaction between the pp71 protein of human cytomegalovirus and the PMLinteracting protein human Daxx. J Virol 76:5769-5783. http://dx.doi.org/10.1128/JVI.76.11.5769-5783.2002.
29. Korioth F, Maul GG, Plachter B, Stamminger T, Frey J. 1996. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp Cell Res 229:155-158. http://dx.doi.org/10.1006/excr.1996.0353.
30. Muller S, Dejean A. 1999. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J Virol 73:5137-5143.
31. Wilkinson GW, Kelly C, Sinclair JH, Rickards C. 1998. Disruption of PML-associated nuclear bodies mediated by the human cytomegalovirus major immediate early gene product. J Gen Virol 79:1233-1245.
32. Xu Y, Ahn JH, Cheng M, apRhys CM, Chiou CJ, Zong J, Matunis MJ, Hayward GS. 2001. Proteasome-independent disruption of PML oncogenic domains (PODs), but not covalent modification by SUMO-1, is required for human cytomegalovirus immediate-early protein IE1 to inhibit PML-mediated transcriptional repression. J Virol 75:10683-10695. http://dx.doi.org/10.1128/JVI.75.22.10683-10695.2001.
33. Kang H, Kim ET, Lee HR, Park JJ, Go YY, Choi CY, Ahn JH. 2006. Inhibition of SUMO-independent PML oligomerization by the human cytomegalovirus IE1 protein. J Gen Virol 87:2181-2190. http://dx.doi.org/10.1099/vir.0.81787-0.
34. Kim YE, Lee JH, Kim ET, Shin HJ, Gu SY, Seol HS, Ling P, Lee CH, Ahn JH. 2011. Human cytomegalovirus infection causes degradation of Sp100 proteins that suppress viral gene expression. J Virol 85:11928-11937. http://dx.doi.org/10.1128/JVI.00758-11.
35. Lee HR, Huh YH, Kim YE, Lee K, Kim S, Ahn JH. 2007. N-terminal determinants of human cytomegalovirus IE1 protein in nuclear targeting and disrupting PML-associated subnuclear structures. Biochem Biophys Res Commun 356:499-504. http://dx.doi.org/10.1016/j.bbrc .2007.03.007.
36. Everett RD, Parada C, Gripon P, Sirma H, Orr A. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J Virol 82:2661-2672. http://dx.doi.org/10.1128/JVI .02308-07.
37. 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. http://dx.doi.org/10.1128/JVI.00734-06.
38. Glass M, Everett RD. 2013. Components of promyelocytic leukemia nuclear bodies (ND10) act cooperatively to repress herpesvirus infection. J Virol 87:2174-2185. http://dx.doi.org/10.1128/JVI.02950-12.
39. Tavalai N, Adler M, Scherer M, Riedl Y, Stamminger T. 2011. Evidence for a dual antiviral role of the major nuclear domain 10 component Sp100 during the immediate-early and late phases of the human cytomegalovirus replication cycle. J Virol 85:9447-9458. http://dx.doi.org/10.1128/JVI.00870-11.
40. Tavalai N, Papior P, Rechter S, Leis M, Stamminger T. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J Virol 80:8006-8018. http://dx.doi.org/10.1128/JVI.00743-06.
41. Tavalai N, Papior P, Rechter S, Stamminger T. 2008. Nuclear domain 10 components promyelocytic leukemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J Virol 82:126-137. http://dx.doi.org/10.1128/JVI.01685-07.
42. Everett RD, Boutell C, McNair C, Grant L, Orr A. 2010. Comparison of the biological and biochemical activities of several members of the alphaherpesvirus ICP0 family of proteins. J Virol 84:3476-3487. http://dx.doi .org/10.1128/JVI.02544-09.
43. Kyratsous CA, Silverstein SJ. 2009. Components of nuclear domain 10 bodies regulate varicella-zoster virus replication. J Virol 83:4262-4274. http://dx.doi.org/10.1128/JVI.00021-09.
44. Everett RD, Bell AJ, Lu Y, Orr A. 2013. The replication defect of ICP0-null mutant herpes simplex virus 1 can be largely complemented by the combined activities of human cytomegalovirus proteins IE1 and pp71. J Virol 87:978-990. http://dx.doi.org/10.1128/JVI.01103-12.
45. Stow EC, Stow ND. 1989. Complementation of a herpes simplex virus type 1 Vmw110 deletion mutant by human cytomegalovirus. J Gen Virol 70:695-704. http://dx.doi.org/10.1099/0022-1317-70-3-695.
46. Stow ND, Stow EC. 1986. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J Gen Virol 67:2571-2585. http://dx.doi.org/10.1099/0022-1317-67-12-2571.
47. Marchini A, Liu H, Zhu H. 2001. Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J Virol 75:1870-1878. http://dx.doi.org/10.1128/JVI.75.4.1870-1878.2001.
48. Knoblach T, Grandel B, Seiler J, Nevels M, Paulus C. 2011. Human cytomegalovirus IE1 protein elicits a type II interferon-like host cell response that depends on activated STAT1 but not interferon-gamma. PLoS Pathog 7:e1002016. http://dx.doi.org/10.1371/journal.ppat.1002016.
49. Zalckvar E, Paulus C, Tillo D, Asbach-Nitzsche A, Lubling Y, Winterling C, Strieder N, Mucke K, Goodrum F, Segal E, Nevels M. 2013. Nucleosome maps of the human cytomegalovirus genome reveal a temporal switch in chromatin organization linked to a major IE protein. Proc Natl Acad Sci U S A 110:13126-13131. http://dx.doi.org/10.1073/pnas .1305548110.
50. Bresnahan WA, Hultman GE, Shenk T. 2000. Replication of wild-type and mutant human cytomegalovirus in life-extended human diploid fibroblasts. J Virol 74:10816-10818. http://dx.doi.org/10.1128/JVI.74.22 .10816-10818.2000.
51. Smith MC, Goddard ET, Perusina Lanfranca M, Davido DJ. 2013. hTERT extends the life of human fibroblasts without compromising type I interferon signaling. PLoS One 8:e58233. http://dx.doi.org/10.1371/journal.pone.0058233.
52. Everett RD, Parsy ML, Orr A. 2009. Analysis of the functions of herpes simplex virus type 1 regulatory protein ICP0 that are critical for lytic infection and derepression of quiescent viral genomes. J Virol 83:4963-4977. http://dx.doi.org/10.1128/JVI.02593-08.
53. Jamieson DRS, Robinson LH, Daksis JI, Nicholl MJ, Preston CM. 1995. Quiescent viral genomes in human fibroblasts after infection with herpes simplex virus Vmw65 mutants. J Gen Virol 76:1417-1431. http://dx.doi .org/10.1099/0022-1317-76-6-1417.
54. Stuurman N, de Graaf A, Floore A, Josso A, Humbel B, de Jong L, van Driel R. 1992. A monoclonal antibody recognizing nuclear matrixassociated nuclear bodies. J Cell Sci 101:773-784.
55. Gawn JM, Greaves RF. 2002. Absence of IE1 p72 protein function during low-multiplicity infection by human cytomegalovirus results in a broad block to viral delayed-early gene expression. J Virol 76:4441-4455. http://dx.doi.org/10.1128/JVI.76.9.4441-4455.2002.
56. Greaves RF, Mocarski ES. 1998. Defective growth correlates with reduced accumulation of a viral DNA replication protein after low-multiplicity infection by a human cytomegalovirus IE1 mutant. J Virol 72:366-379.
57. 1491aa is replication defective due to a failure in autoregulation. Proc Natl Acad Sci U S A 93:11321-11326. http://dx.doi.org/10.1073/pnas.93.21.11321.
58. Spengler ML, Kurapatwinski K, Black AR, Azizkhan-Clifford J. 2002. SUMO-1 modification of human cytomegalovirus IE1/IE72. J Virol 76: 2990-2996. http://dx.doi.org/10.1128/JVI.76.6.2990-2996.2002.
59. Nevels M, Brune W, Shenk T. 2004. SUMOylation of the human cytomegalovirus 72-kilodalton IE1 protein facilitates expression of the 86-kilodalton IE2 protein and promotes viral replication. J Virol 78:7803-7812. http://dx.doi.org/10.1128/JVI.78.14.7803-7812.2004.
60. Mucke K, Paulus C, Bernhardt K, Gerrer K, Schon K, Fink A, Sauer EM, Asbach-Nitzsche A, Harwardt T, Kieninger B, Kremer W, Kalbitzer HR, Nevels M. 2014. Human cytomegalovirus major immediate early 1 protein targets host chromosomes by docking to the acidic pocket on the nucleosome surface. J Virol 88:1228-1248. http://dx.doi.org/10.1128/JVI .02606-13.
61. Shin HJ, Kim YE, Kim ET, Ahn JH. 2012. The chromatin-tethering domain of human cytomegalovirus immediate-early (IE) 1 mediates associations of IE1, PML and STAT2 with mitotic chromosomes, but is not essential for viral replication. J Gen Virol 93:716-721. http://dx.doi.org/10.1099/vir.0.037986-0.
62. Scherer M, Klingl S, Sevvana M, Otto V, Schilling EM, Stump JD, Muller R, Reuter N, Sticht H, Muller YA, Stamminger T. 2014. Crystal structure of cytomegalovirus IE1 protein reveals targeting of TRIM family memberPMLvia coiled-coil interactions. PLoS Pathog 10:e1004512. http://dx.doi.org/10.1371/journal.ppat.1004512.
63. Preston CM, Nicholl MJ. 1997. Repression of gene expression upon infection of cells with herpes simplex virus type 1 mutants impaired for immediate-early protein synthesis. J Virol 71:7807-7813.
64. Samaniego LA, Neiderhiser L, DeLuca NA. 1998. Persistence and expression of the herpes simplex virus genome in the absence of immediateearly proteins. J Virol 72:3307-3320.
65. Burgdorf SW, Clark CL, Burgdorf JR, Spector DH. 2011. Mutation of glutamine to arginine at position 548 of IE2 86 in human cytomegalovirus leads to decreased expression of IE2 40, IE2 60, UL83, and UL84 and increased transcription of US8-9 and US29-32. J Virol 85:11098-11110. http://dx.doi.org/10.1128/JVI.05315-11.
66. Everett RD, Boutell C, Orr A. 2004. Phenotype of a herpes simplex virus type 1 mutant that fails to express immediate-early regulatory protein ICP0. J Virol 78:1763-1774. http://dx.doi.org/10.1128/JVI.78 .4.1763-1774.2004.
67. Malone CL, Vesole DH, Stinski MF. 1990. Transactivation of a human cytomegalovirus early promoter by gene products from the immediateearly gene IE2 and augmentation by IE1: mutational analysis of the viral proteins. J Virol 64:1498-1506.
68. Stenberg RM, Fortney J, Barlow SW, Magrane BP, Nelson JA, Ghazal P. 1990. Promoter-specific trans activation and repression by human cytomegalovirus immediate-early proteins involves common and unique protein domains. J Virol 64:1556-1565.
69. Depto AS, Stenberg RM. 1989. Regulated expression of the human cytomegalovirus pp65 gene: octamer sequence in the promoter is required for activation by viral gene products. J Virol 63:1232-1238.
70. Yao F, Schaffer PA. 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.
71. Sommer MH, Scully AL, Spector DH. 1994. Transactivation by the human cytomegalovirus IE2 86-kilodalton protein requires a domain that binds to both the TATA box-binding protein and the retinoblastoma protein. J Virol 68:6223-6231.
72. White EA, Spector DH. 2005. Exon 3 of the human cytomegalovirus major immediate-early region is required for efficient viral gene expression and for cellular cyclin modulation. J Virol 79:7438-7452. http://dx .doi.org/10.1128/JVI.79.12.7438-7452.2005.