Herpes simplex virus type 1 immediate-early protein ICP22 is required for VICE domain formation during productive viral infection

Journal of Virology

Volumn 84, Issue 5, 2010, Pages 2384-2394

  Bastian, Thomas W ^a   Livingston, Christine M ^b   Weller, Sandra K ^b   Rice, Stephen A ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK COGNATE PROTEIN 70; PROTEIN ICP22; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; HELA CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HSC70 HEAT-SHOCK PROTEINS; HUMANS; IMMEDIATE-EARLY PROTEINS; INTRANUCLEAR INCLUSION BODIES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; VERO CELLS;

HUMAN HERPESVIRUS 1;

EID: 77649217752     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01686-09     Document Type: Article

References (58)

1. Bastian, T. W., and S. A. Rice. 2009. Identification of sequences in herpes simplex virus type 1 ICP22 that influence RNA polymerase II modification and viral late gene expression. J. Virol. 83:128-139.
2. Besse, S., and F. Puvion-Dutilleul. 1996. Intranuclear retention of ribosomal RNAs in response to herpes simplex virus type 1 infection. J. Cell Sci. 109:119-129.
3. Brandt, C. R., A. W. Kolb, D. D. Shah, A. M. Pumfery, R. L. Kintner, E. Jaehnig, and J. J. Van Gompel. 2003. Multiple determinants contribute to the virulence of HSV ocular and CNS infection and identification of serine 34 of the US1 gene as an ocular disease determinant. Invest. Ophthalmol. Vis. Sci. 44:2657-2668.
4. Bukau, B., J. Weissman, and A. Horwich. 2006. Molecular chaperones and protein quality control. Cell 125:443-451.
5. Burch, A. D., and S. K. Weller. 2005. Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J. Virol. 79:10740-10749.
6. Burch, A. D., and S. K. Weller. 2004. Nuclear sequestration of cellular chaperone and proteasomal machinery during herpes simplex virus type 1 infection. J. Virol. 78:7175-7185.
7. Cai, W., T. L. Astor, L. M. Liptak, C. Cho, D. M. Coen, and P. A. Schaffer. 1993. The herpes simplex virus type 1 regulatory protein ICP0 enhances virus replication during acute infection and reactivation from latency. J. Virol. 67:7501-7512.
8. Cun, W., M. Hong, L. D. Liu, C. H. Dong, J. Luo, and Q. H. Li. 2006. Structural and functional characterization of herpes simplex virus 1 immediate-early protein infected-cell protein 22. J. Biochem. 140:67-73.
9. Daugaard, M., M. Rohde, and M. Jaattela. 2007. The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett. 581:3702-3710.
10. DeLuca, N. A., A. M. McCarthy, and P. A. Schaffer. 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.
11. Everett, R. D., and G. G. Maul. 1994. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 13:5062-5069.
12. Everett, R. D., and J. Murray. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79:5078-5089.
13. Everett, R. D., G. Sourvinos, and A. Orr. 2003. Recruitment of herpes simplex virus type 1 transcriptional regulatory protein ICP4 into foci juxtaposed to ND10 in live, infected cells. J. Virol. 77:3680-3689.
14. Feierbach, B., S. Piccinotti, M. Bisher, W. Denk, and L. W. Enquist. 2006. Alpha-herpesvirus infection induces the formation of nuclear actin filaments. PLoS Pathog. 2:e85.
15. Florin, L., K. A. Becker, C. Sapp, C. Lambert, H. Sirma, M. Muller, R. E. Streeck, and M. Sapp. 2004. Nuclear translocation of papillomavirus minor capsid protein L2 requires Hsc70. J. Virol. 78:5546-5553.
16. Forest, T., S. Barnard, and J. D. Baines. 2005. Active intranuclear movement of herpesvirus capsids. Nat. Cell Biol. 7:429-431.
17. Fraser, K. A., and S. A. Rice. 2007. Herpes simplex virus immediate-early protein ICP22 triggers loss of serine 2-phosphorylated RNA polymerase II. J. Virol. 81:5091-5101.
18. Fraser, K. A., and S. A. Rice. 2005. Herpes simplex virus type 1 infection leads to loss of serine-2 phosphorylation on the carboxyl-terminal domain of RNA polymerase II. J. Virol. 79:11323-11334.
19. Fujimuro, M., H. Sawada, and H. Yokosawa. 1994. Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349:173-180.
20. Hughes, R. G., Jr., and W. H. Munyon. 1975. Temperature-sensitive mutants of herpes simplex virus type 1 defective in lysis but not in transformation. J. Virol. 16:275-283.
21. Jahedi, S., N. S. Markovitz, F. Filatov, and B. Roizman. 1999. Colocalization of the herpes simplex virus 1 UL4 protein with infected cell protein 22 in small, dense nuclear structures formed prior to onset of DNA synthesis. J. Virol. 73:5132-5138.
22. Knipe, D. M., D. Senechek, S. A. Rice, and J. L. Smith. 1987. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J. Virol. 61:276-284.
23. Kodiha, M., A. Chu, O. Lazrak, and U. Stochaj. 2005. Stress inhibits nucleocytoplasmic shuttling of heat shock protein hsc70. Am. J. Physiol. Cell Physiol. 289:C1034-C1041.
24. Kyratsous, C. A., and S. J. Silverstein. 2007. BAG3, a host cochaperone, facilitates varicella-zoster virus replication. J. Virol. 81:7491-7503.
25. Kyratsous, C. A., and S. J. Silverstein. 2008. The co-chaperone BAG3 regulates herpes simplex virus replication. Proc. Natl. Acad. Sci. U. S. A. 105:20912-20917.
26. Lamberti, C., and S. K. Weller. 1998. The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments. J. Virol. 72:2463-2473.
27. Leopardi, R., P. L. Ward, W. O. Ogle, and B. Roizman. 1997. Association of herpes simplex virus regulatory protein ICP22 with transcriptional complexes containing EAP, ICP4, RNA polymerase II, and viral DNA requires posttranslational modification by the U(L)13 proteinkinase. J. Virol. 71: 1133-1139.
28. Li, L., L. A. Johnson, J. Q. Dai-Ju, and R. M. Sandri-Goldin. 2008. Hsc70 focus formation at the periphery of HSV-1 transcription sites requires ICP27. PLoS One 3:e1491.
29. Liberek, K., A. Lewandowska, and S. Zietkiewicz. 2008. Chaperones in control of protein disaggregation. EMBO J. 27:328-335.
30. Liptak, L. M., S. L. Uprichard, and D. M. Knipe. 1996. Functional order of assembly of herpes simplex virus DNA replication proteins into prereplicative site structures. J. Virol. 70:1759-1767.
31. Livingston, C. M., N. A. DeLuca, D. E. Wilkinson, and S. K. Weller. 2008. Oligomerization of ICP4 and rearrangement of heat shock proteins may be important for herpes simplex virus type 1 prereplicative site formation. J. Virol. 82:6324-6336.
32. Livingston, C. M., M. F. Ifrim, A. E. Cowan, and S. K. Weller. 2009. Virusinduced chaperone-enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection. PLoS Pathog. 5:e1000619.
33. Long, M. C., V. Leong, P. A. Schaffer, C. A. Spencer, and S. A. Rice. 1999. ICP22 and the UL13 protein kinase are both required for herpes simplex virus-induced modification of the large subunit of RNA polymerase II. J. Virol. 73:5593-5604.
34. Lymberopoulos, M. H., and A. Pearson. 2007. Involvement of UL24 in herpes-simplex-virus-1-induced dispersal of nucleolin. Virology 363:397-409.
35. Markovitz, N. S., and B. Roizman. 2000. Small dense nuclear bodies are the site of localization of herpes simplex virus 1 U(L)3 and U(L)4 proteins and of ICP22 only when the latter protein is present. J. Virol. 74:523-528.
36. Martin, T. E., S. C. Barghusen, G. P. Leser, and P. G. Spear. 1987. Redistribution of nuclear ribonucleoprotein antigens during herpes simplex virus infection. J. Cell Biol. 105:2069-2082.
37. Monier, K., J. C. Armas, S. Etteldorf, P. Ghazal, and K. F. Sullivan. 2000. Annexation of the interchromosomal space during viral infection. Nat. Cell Biol. 2:661-665.
38. Orlando, J. S., T. L. Astor, S. A. Rundle, and P. A. Schaffer. 2006. The products of the herpes simplex virus type 1 immediate-early US1/US1.5 genes downregulate levels of S-phase-specific cyclins and facilitate virus replication in S-phase Vero cells. J. Virol. 80:4005-4016.
39. Orlando, J. S., J. W. Balliet, A. S. Kushnir, T. L. Astor, M. Kosz-Vnenchak, S. A. Rice, D. M. Knipe, and P. A. Schaffer. 2006. ICP22 is required for wild-type composition and infectivity of herpes simplex virus type 1 virions. J. Virol. 80:9381-9390.
40. Perkins, K. D., J. Gregonis, S. Borge, and S. A. Rice. 2003. Transactivation of a viral target gene by herpes simplex virus ICP27 is posttranscriptional and does not require the endogenous promoter or polyadenylation site. J. Virol. 77:9872-9884.
41. Phelan, A., J. Dunlop, A. H. Patel, N. D. Stow, and J. B. Clements. 1997. Nuclear sites of herpes simplex virus type 1 DNA replication and transcription colocalize at early times postinfection and are largely distinct from RNA processing factors. J. Virol. 71:1124-1132.
42. Poffenberger, K. L., A. D. Idowu, E. B. Fraser-Smith, P. E. Raichlen, and R. C. Herman. 1994. A herpes simplex virus type 1 ICP22 deletion mutant is altered for virulence and latency in vivo. Arch. Virol. 139:111-119.
43. Poffenberger, K. L., P. E. Raichlen, and R. C. Herman. 1993. In vitro characterization of a herpes simplex virus type 1 ICP22 deletion mutant. Virus Genes 7:171-186.
44. Purves, F. C., W. O. Ogle, and B. Roizman. 1993. Processing of the herpes simplex virus regulatory protein alpha 22 mediated by the UL13 protein kinase determines the accumulation of a subset of alpha and gamma mRNAs and proteins in infected cells. Proc. Natl. Acad. Sci. U. S. A. 90:6701-6705.
45. Purves, F. C., and B. Roizman. 1992. The UL13 gene of herpes simplex virus 1 encodes the functions for posttranslational processing associated with phosphorylation of the regulatory protein alpha 22. Proc. Natl. Acad. Sci. U. S. A. 89:7310-7314.
46. Quinlan, M. P., L. B. Chen, and D. M. Knipe. 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.
47. Randall, R. E., and N. Dinwoodie. 1986. Intranuclear localization of herpes simplex virus immediate-early and delayed-early proteins: evidence that ICP 4 is associated with progeny virus DNA. J. Gen. Virol. 67:2163-2177.
48. Rice, S. A., and D. M. Knipe. 1990. Genetic evidence for two distinct transactivation functions of the herpes simplex virus alpha protein ICP27. J. Virol. 64:1704-1715.
49. Rice, S. A., M. C. Long, V. Lam, P. A. Schaffer, and C. A. Spencer. 1995. Herpes simplex virus immediate-early protein ICP22 is required for viral modification of host RNA polymerase II and establishment of the normal viral transcription program. J. Virol. 69:5550-5559.
50. Roizman, B., D. M. Knipe, and R. J. Whitley. 2007. Herpes simplex viruses, p. 2501-2601. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol. 2. Lippincott, Williams & Wilkins, Philadelphia, PA.
51. Salsman, J., N. Zimmerman, T. Chen, M. Domagala, and L. Frappier. 2008. Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog. 4:e1000100.
52. Schwartz, J., and B. Roizman. 1969. Concerning the egress of herpes simplex virus from infected cells: electron and light microscope observations. Virology 38:42-49.
53. Schwyzer, M., U. V. Wirth, B. Vogt, and C. Fraefel. 1994. BICP22 of bovine herpesvirus 1 is encoded by a spliced 1.7 kb RNA which exhibits immediate early and late transcription kinetics. J. Gen. Virol. 75:1703-1711.
54. Sears, A. E., I. W. Halliburton, B. Meignier, S. Silver, and B. Roizman. 1985. Herpes simplex virus 1 mutant deleted in the alpha 22 gene: growth and gene expression in permissive and restrictive cells and establishment of latency in mice. J. Virol. 55:338-346.
55. Simpson-Holley, M., R. C. Colgrove, G. Nalepa, J. W. Harper, and D. M. Knipe. 2005. Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J. Virol. 79:12840-12851.
56. Stelz, G., E. Rucker, O. Rosorius, G. Meyer, R. H. Stauber, M. Spatz, M. M. Eibl, and J. Hauber. 2002. Identification of two nuclear import signals in the alpha-gene product ICP22 of herpes simplex virus 1. Virology 295:360-370.
57. Weinheimer, S. P., B. A. Boyd, S. K. Durham, J. L. Resnick, and D. R. O'Boyle II. 1992. Deletion of the VP16 open reading frame of herpes simplex virus type 1. J. Virol. 66:258-269.
58. Yao, F., and P. A. Schaffer. 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.