A conserved carboxy-terminal domain in the major tegument structural protein VP22 facilitates virion packaging of a chimeric protein during productive herpes simplex virus 1 infection

Virology

Volumn 387, Issue 2, 2009, Pages 449-458

  Schlegel, Elisabeth F M ^a   Blaho, John A ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

GCT VP22; Marginalized chromatin; Tegument protein VP22; Virion packaging

Indexed keywords

CHIMERIC PROTEIN; GFP ANTIBODY; PROTEIN GCT VP22; PROTEIN VP22; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; GENE; GFP GENE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; IMMUNOFLUORESCENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; VIRION; VIRUS RECOMBINANT;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; VERO CELLS; VIRAL STRUCTURAL PROTEINS; VIRUS ASSEMBLY;

HUMAN HERPESVIRUS 1;

EID: 64849098999     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.02.040     Document Type: Article

References (82)

1. Aints A., Guven H., Gahrton G., Smith C.I., and Dilber M.S. Mapping of herpes simplex virus-1 VP22 functional domains for inter- and subcellular protein targeting. Gene Ther. 8 14 (2001) 1051-1056
2. Besse S., and Puvion-Dutilleul F. Distribution of ribosomal genes in nucleoli of herpes simplex virus type 1 infected cells. Eur. J. Cell Biol. 71 1 (1996) 33-44
3. Blaho J.A., Mitchell C., and Roizman B. Guanylylation and adenylylation of the alpha regulatory proteins of herpes simplex virus require a viral beta or gamma function. J. Virol. 67 7 (1993) 3891-3900
4. Blaho J.A., Mitchell C., and Roizman B. An amino acid sequence shared by the herpes simplex virus 1 alpha regulatory proteins 0, 4, 22, and 27 predicts the nucleotidylylation of the UL21, UL31, UL47, and UL49 gene products. J. Biol. Chem. 269 26 (1994) 17401-17410
5. Blouin A., and Blaho J.A. Assessment of the subcellular localization of the herpes simplex virus structural protein VP22 in the absence of other viral gene products. Virus Res. 81 1-2 (2001) 57-68
6. Brignati M.J., Loomis J.S., Wills J.W., and Courtney R.J. Membrane association of VP22, a herpes simplex virus type 1 tegument protein. J. Virol. 77 8 (2003) 4888-4898
7. Calle A., Ugrinova I., Epstein A.L., Bouvet P., Diaz J.J., and Greco A. Nucleolin is required for an efficient herpes simplex virus type 1 infection. J. Virol. 82 10 (2008) 4762-4773
8. Chi J.H., Harley C.A., Mukhopadhyay A., and Wilson D.W. The cytoplasmic tail of herpes simplex virus envelope glycoprotein D binds to the tegument protein VP22 and to capsids. J. Gen. Virol. 86 Pt. 2 (2005) 253-261
9. Davis L.I. The nuclear pore complex. Annu. Rev. Biochem. 64 (1995) 865-896
10. Davison A.J. Evolution of the herpesviruses. Vet. Microbiol. 86 1-2 (2002) 69-88
11. Donnelly M., and Elliott G. Fluorescent tagging of herpes simplex virus tegument protein VP13/14 in virus infection. J. Virol. 75 6 (2001) 2575-2583
12. Donnelly M., and Elliott G. Nuclear localization and shuttling of herpes simplex virus tegument protein VP13/14. J. Virol. 75 6 (2001) 2566-2574
13. Duffy C., Lavail J.H., Tauscher A.N., Wills E.G., Blaho J.A., and Baines J.D. Characterization of a UL49-null mutant: VP22 of herpes simplex virus type 1 facilitates viral spread in cultured cells and the mouse cornea. J. Virol. 80 17 (2006) 8664-8675
14. Duffy C., Mbong E.F., and Baines J.D. VP22 of herpes simplex virus 1 promotes protein synthesis at late times in infection and accumulation of a subset of viral mRNAs at early times in infection. J. Virol. 83 2 (2009) 1009-1017
15. Elliott G., Mouzakitis G., and O'Hare P. VP16 interacts via its activation domain with VP22, a tegument protein of herpes simplex virus, and is relocated to a novel macromolecular assembly in coexpressing cells. J. Virol. 69 12 (1995) 7932-7941
16. Elliott G., and O'Hare P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88 2 (1997) 223-233
17. Elliott G., and O'Hare P. Live-cell analysis of a green fluorescent protein-tagged herpes simplex virus infection. J. Virol. 73 5 (1999) 4110-4119
18. Elliott G., and O'Hare P. Cytoplasm-to-nucleus translocation of a herpesvirus tegument protein during cell division. J. Virol. 74 5 (2000) 2131-2141
19. Elliott G., O'Reilly D., and O'Hare P. Phosphorylation of the herpes simplex virus type 1 tegument protein VP22. Virology 226 1 (1996) 140-145
20. Elliott G., O'Reilly D., and O'Hare P. Identification of phosphorylation sites within the herpes simplex virus tegument protein VP22. J. Virol. 73 7 (1999) 6203-6206
21. Elliott G.D., and Meredith D.M. The herpes simplex virus type 1 tegument protein VP22 is encoded by gene UL49. J. Gen. Virol. 73 Pt 3 (1992) 723-726
22. Enquist L.W., Husak P.J., Banfield B.W., and Smith G.A. Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 51 (1998) 237-347
23. Fang B., Xu B., Koch P., and Roth J.A. Intercellular trafficking of VP22-GFP fusion proteins is not observed in cultured mammalian cells. Gene Ther. 5 10 (1998) 1420-1424
24. Farnsworth A., Wisner T.W., and Johnson D.C. Cytoplasmic residues of herpes simplex virus glycoprotein gE required for secondary envelopment and binding of tegument proteins VP22 and UL11 to gE and gD. J. Virol. 81 1 (2007) 319-331
25. Fuchs W., Klupp B.G., Granzow H., Hengartner C., Brack A., Mundt A., Enquist L.W., and Mettenleiter T.C. Physical interaction between envelope glycoproteins E and M of pseudorabies virus and the major tegument protein UL49. J. Virol. 76 16 (2002) 8208-8217
26. Geiss B.J., Cano G.L., Tavis J.E., and Morrison L.A. Herpes simplex virus 2 VP22 phosphorylation induced by cellular and viral kinases does not influence intracellular localization. Virology 330 1 (2004) 74-81
27. Geiss B.J., Tavis J.E., Metzger L.M., Leib D.A., and Morrison L.A. Temporal regulation of herpes simplex virus type 2 VP22 expression and phosphorylation. J. Virol. 75 22 (2001) 10721-10729
28. Gibson W., and Roizman B. Proteins specified by herpes simplex virus. Staining and radiolabeling properties of B capsid and virion proteins in polyacrylamide gels. J. Virol. 13 1 (1974) 155-165
29. Gross S.T., Harley C.A., and Wilson D.W. The cytoplasmic tail of Herpes simplex virus glycoprotein H binds to the tegument protein VP16 in vitro and in vivo. Virology 317 1 (2003) 1-12
30. Hafezi W., Bernard E., Cook R., and Elliott G. Herpes simplex virus tegument protein VP22 contains an internal VP16 interaction domain and a C-terminal domain that are both required for VP22 assembly into the virus particle. J. Virol. 79 20 (2005) 13082-13093
31. Hampar B., and Ellison S.A. Chromosomal aberrations induced by an animal virus. Nature 192 (1961) 145-147
32. Harms J.S., Ren X., Oliveira S.C., and Splitter G.A. Distinctions between bovine herpesvirus 1 and herpes simplex virus type 1 VP22 tegument protein subcellular associations. J. Virol. 74 7 (2000) 3301-3312
33. Heine J.W., Honess R.W., Cassai E., and Roizman B. Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains. J. Virol. 14 3 (1974) 640-651
34. Hiscox J.A. The nucleolus-a gateway to viral infection?. Arch. Virol. 147 6 (2002) 1077-1089
35. Hubner S., Xiao C.Y., and Jans D.A. The protein kinase CK2 site (Ser111/112) enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin. J. Biol. Chem. 272 27 (1997) 17191-17195
36. Hutchinson I., Whiteley A., Browne H., and Elliott G. Sequential localization of two herpes simplex virus tegument proteins to punctate nuclear dots adjacent to ICP0 domains. J. Virol. 76 20 (2002) 10365-10373
37. Jans D.A., and Hubner S. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76 3 (1996) 651-685
38. Jans D.A., Xiao C.Y., and Lam M.H. Nuclear targeting signal recognition: a key control point in nuclear transport?. Bioessays 22 6 (2000) 532-544
39. Knopf K.W., and Kaerner H.C. Virus-specific basic phosphoproteins associated with herpes simplex virus type a (HSV-1) particles and the chromatin of HSV-1-infected cells. J. Gen. Virol. 46 2 (1980) 405-414
40. Kotsakis A., Pomeranz L.E., Blouin A., and Blaho J.A. Microtubule reorganization during herpes simplex virus type 1 infection facilitates the nuclear localization of VP22, a major virion tegument protein. J. Virol. 75 18 (2001) 8697-8711
41. Lee J.H., Vittone V., Diefenbach E., Cunningham A.L., and Diefenbach R.J. Identification of structural protein-protein interactions of herpes simplex virus type 1. Virology 378 2 (2008) 347-354
42. Leopardi R., and Roizman B. Functional interaction and colocalization of the herpes simplex virus 1 major regulatory protein ICP4 with EAP, a nucleolar-ribosomal protein. Proc. Natl. Acad. Sci. U. S. A. 93 10 (1996) 4572-4576
43. Leuzinger H., Ziegler U., Schraner E.M., Fraefel C., Glauser D.L., Heid I., Ackermann M., Mueller M., and Wild P. Herpes simplex virus 1 envelopment follows two diverse pathways. J. Virol. 79 20 (2005) 13047-13059
44. Lopez M.R., Schlegel E.F., Wintersteller S., and Blaho J.A. The major tegument structural protein VP22 targets areas of dispersed nucleolin and marginalized chromatin during productive herpes simplex virus 1 infection. Virus Res. 136 1-2 (2008) 175-188
45. Lymberopoulos M.H., and Pearson A. Involvement of UL24 in herpes-simplex-virus-1-induced dispersal of nucleolin. Virology 363 2 (2007) 397-409
46. MacLean C.A., Rixon F.J., and Marsden H.S. The products of gene US11 of herpes simplex virus type 1 are DNA-binding and localize to the nucleoli of infected cells. J. Gen. Virol. 68 Pt 7 (1987) 1921-1937
47. Martin A., O'Hare P., McLauchlan J., and Elliott G. Herpes simplex virus tegument protein VP22 contains overlapping domains for cytoplasmic localization, microtubule interaction, and chromatin binding. J. Virol. 76 10 (2002) 4961-4970
48. Mayer C., and Grummt I. Cellular stress and nucleolar function. Cell Cycle 4 8 (2005) 1036-1038
49. McGeoch D.J., Dalrymple M.A., Davison A.J., Dolan A., Frame M.C., McNab D., Perry L.J., Scott J.E., and Taylor P. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 69 Pt 7 (1988) 1531-1574
50. Mears W.E., Lam V., and Rice S.A. Identification of nuclear and nucleolar localization signals in the herpes simplex virus regulatory protein ICP27. J. Virol. 69 2 (1995) 935-947
51. Mettenleiter T.C. Herpesvirus assembly and egress. J. Virol. 76 4 (2002) 1537-1547
52. Mettenleiter T.C. Budding events in herpesvirus morphogenesis. Virus Res. 106 2 (2004) 167-180
53. Morency E., Coute Y., Thomas J., Texier P., and Lomonte P. The protein ICP0 of herpes simplex virus type 1 is targeted to nucleoli of infected cells. Brief report. Arch. Virol. 150 11 (2005) 2387-2395
54. Morrison E.E., Stevenson A.J., Wang Y.F., and Meredith D.M. Differences in the intracellular localization and fate of herpes simplex virus tegument proteins early in the infection of Vero cells. J. Gen. Virol. 79 Pt 10 (1998) 2517-2528
55. Morrison E.E., Wang Y.F., and Meredith D.M. Phosphorylation of structural components promotes dissociation of the herpes simplex virus type 1 tegument. J. Virol. 72 9 (1998) 7108-7114
56. Mouzakitis G., McLauchlan J., Barreca C., Kueltzo L., and O'Hare P. Characterization of VP22 in herpes simplex virus-infected cells. J. Virol. 79 19 (2005) 12185-12198
57. Murphy M.A., Bucks M.A., O'Regan K.J., and Courtney R.J. The HSV-1 tegument protein pUL46 associates with cellular membranes and viral capsids. Virology 376 2 (2008) 279-289
58. O'Regan K.J., Murphy M.A., Bucks M.A., Wills J.W., and Courtney R.J. Incorporation of the herpes simplex virus type 1 tegument protein VP22 into the virus particle is independent of interaction with VP16. Virology 369 2 (2007) 263-280
59. Ojala P.M., Sodeik B., Ebersold M.W., Kutay U., and Helenius A. Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol. Cell. Biol. 20 13 (2000) 4922-4931
60. Olson M.O. Sensing cellular stress: another new function for the nucleolus?. Sci. STKE 2004 224 (2004) 10
61. Pederson T. The plurifunctional nucleolus. Nucleic Acids Res. 26 17 (1998) 3871-3876
62. Perelygina L., Zhu L., Zurkuhlen H., Mills R., Borodovsky M., and Hilliard J.K. Complete sequence and comparative analysis of the genome of herpes B virus (Cercopithecine herpesvirus 1) from a rhesus monkey. J. Virol. 77 11 (2003) 6167-6177
63. Politz J.C., Polena I., Trask I., Bazett-Jones D.P., and Pederson T. A nonribosomal landscape in the nucleolus revealed by the stem cell protein nucleostemin. Mol. Biol. Cell 16 7 (2005) 3401-3410
64. Pomeranz, L. E. (2000). Mount Sinai School of Medicine, New York.
65. Pomeranz L.E., and Blaho J.A. Modified VP22 localizes to the cell nucleus during synchronized herpes simplex virus type 1 infection. J. Virol. 73 8 (1999) 6769-6781
66. Pomeranz L.E., and Blaho J.A. Assembly of infectious Herpes simplex virus type 1 virions in the absence of full-length VP22. J. Virol. 74 21 (2000) 10041-10054
67. Ren X., Harms J.S., and Splitter G.A. Tyrosine phosphorylation of bovine herpesvirus 1 tegument protein VP22 correlates with the incorporation of VP22 into virions. J. Virol. 75 19 (2001) 9010-9017
68. Roizman B., and Knipe D.M. Herpes simplex viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology Vol. 2 (2001), Lippincot, Williams, and Wlkins, Philadelphia 2399-2459
69. Roizman B.a.F.D. The replication of herpesviruses. In: Fraenkel-Conrat H., and Wagner R.R. (Eds). Comprehensive Virology vol. 3 (1974), Plenum Press, New York 229-403
70. Roller R.J., Monk L.L., Stuart D., and Roizman B. Structure and function in the herpes simplex virus 1 RNA-binding protein U(s)11: mapping of the domain required for ribosomal and nucleolar association and RNA binding in vitro. J. Virol. 70 5 (1996) 2842-2851
71. Roller R.J., and Roizman B. The herpes simplex virus Us11 open reading frame encodes a sequence-specific RNA-binding protein. J. Virol. 64 7 (1990) 3463-3470
72. Rowland R.R., and Yoo D. Nucleolar-cytoplasmic shuttling of PRRSV nucleocapsid protein: a simple case of molecular mimicry or the complex regulation by nuclear import, nucleolar localization and nuclear export signal sequences. Virus Res. 95 1-2 (2003) 23-33
73. Sciortino M.T., Taddeo B., Poon A.P., Mastino A., and Roizman B. Of the three tegument proteins that package mRNA in herpes simplex virions, one (VP22) transports the mRNA to uninfected cells for expression prior to viral infection. Proc. Natl. Acad. Sci. U. S. A. 99 12 (2002) 8318-8323
74. Simpson-Holley M., Colgrove R.C., Nalepa G., Harper J.W., and Knipe D.M. 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 20 (2005) 12840-12851
75. Smibert C.A., Popova B., Xiao P., Capone J.P., and Smiley J.R. Herpes simplex virus VP16 forms a complex with the virion host shutoff protein vhs. J. Virol. 68 4 (1994) 2339-2346
76. Spear P.G., and Roizman B. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion. J. Virol. 9 1 (1972) 143-159
77. Sugimoto K., Uema M., Sagara H., Tanaka M., Sata T., Hashimoto Y., and Kawaguchi Y. Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J. Virol. 82 11 (2008) 5198-5211
78. Taddeo B., Sciortino M.T., Zhang W., and Roizman B. Interaction of herpes simplex virus RNase with VP16 and VP22 is required for the accumulation of the protein but not for accumulation of mRNA. Proc. Natl. Acad. Sci. U. S. A. 104 29 (2007) 12163-12168
79. Vittone V., Diefenbach E., Triffett D., Douglas M.W., Cunningham A.L., and Diefenbach R.J. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 79 15 (2005) 9566-9571
80. Yamada H., Jiang Y.M., Zhu H.Y., Inagaki-Ohara K., and Nishiyama Y. Nucleolar localization of the UL3 protein of herpes simplex virus type 2. J. Gen. Virol. 80 Pt 8 (1999) 2157-2164
81. Yedowitz J.C., Kotsakis A., Schlegel E.F., and Blaho J.A. Nuclear localizations of the herpes simplex virus type 1 tegument proteins VP13/14, vhs, and VP16 precede VP22-dependent microtubule reorganization and VP22 nuclear import. J. Virol. 79 8 (2005) 4730-4743
82. Zheng C., Brownlie R., Babiuk L.A., and van Drunen Littel-van den Hurk S. Characterization of the nuclear localization and nuclear export signals of bovine herpesvirus 1 VP22. J. Virol. 79 18 (2005) 11864-11872