Phosphorylation of the VP16 transcriptional activator protein during herpes simplex virus infection and mutational analysis of putative phosphorylation sites

Virology

Volumn 345, Issue 2, 2006, Pages 468-481

  Ottosen, Søren ^a,c   Herrera, Francisco J ^a,d   Doroghazi, James R ^a   Hull, Angela ^a   Mittal, Sheenu ^a   Lane, William S ^b   Triezenberg, Steven J ^a  

^a Michigan State University   (United States)

^b HARVARD UNIVERSITY   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Trans inducing factor; Chromatin immunoprecipitation; Immediate early gene; Oct 1; Transcriptional activation; Vmw65

Indexed keywords

PROTEIN VP16; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL GROWTH; GENE EXPRESSION; GROWTH RATE; HERPES SIMPLEX; IMMEDIATE EARLY GENE; IN VITRO STUDY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; VIROGENESIS; VIRUS GENE; VIRUS MUTATION;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; CHROMATIN IMMUNOPRECIPITATION; HELA CELLS; HERPES SIMPLEX; HERPES SIMPLEX VIRUS PROTEIN VMW65; HUMANS; IMMEDIATE-EARLY PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; OCTAMER TRANSCRIPTION FACTOR-1; PHOSPHORYLATION; SIMPLEXVIRUS; TRANS-ACTIVATION (GENETICS); VERO CELLS;

ANIMALIA; HERPES; SIMPLEXVIRUS;

EID: 31944439843     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2005.10.011     Document Type: Article

References (68)

1. C.I. Ace, T.A. McKee, J.M. Ryan, J.M. Cameron, and C.M. Preston Construction and characterization of a herpes simplex virus type 1 mutant unable to transinduce immediate-early gene expression J. Virol. 63 1989 2260 2269
2. R. Babb, C.C. Huang, D.J. Aufiero, and W. Herr DNA recognition by the herpes simplex virus transactivator VP16: a novel DNA-binding structure Mol. Cell. Biol. 21 2001 4700 4712
3. S.L. Berger, B. Pina, N. Silverman, G.A. Marcus, J. Agapite, J.L. Regier, S.J. Triezenberg, and L. Guarente Genetic isolation of ADA2-a potential transcriptional adaptor required for function of certain acidic activation domains Cell 70 1992 251 265
4. A. Cress, and S.J. Triezenberg Nucleotide and deduced amino acid sequences of the gene encoding virion protein 16 of herpes simplex virus type 2 Gene 103 1991 235 238
5. W.D. Cress, and S.J. Triezenberg Critical structural elements of the VP16 transcriptional activation domain Science 251 1991 87 90
6. G. Elliott, G. Mouzakitis, and P. O'Hare 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 1995 7932 7941
7. R.N. Freiman, and W. Herr Viral mimicry: common mode of association with HCF by VP16 and the cellular protein LZIP Genes Dev. 11 1997 3122 3127
8. T. Gerster, and R.G. Roeder A herpesvirus trans-activating protein interacts with transcription factor OTF-1 and other cellular proteins Proc. Natl. Acad. Sci. U.S.A. 85 1988 6347 6351
9. W. Gibson, and B. Roizman Proteins specified by herpes simplex virus: X. Staining and radiolabelling properties of B capsid and virion proteins in polyacrylamide gels J. Virol. 13 1974 155 165
10. R. Greaves, and P. O'Hare Separation of requirements for protein-DNA complex assembly from those for functional activity in the herpes simplex virus regulatory protein Vmw65 J. Virol. 63 1989 1641 1650
11. R.F. Greaves, and P. O'Hare Structural requirements in the herpes simplex virus type 1 transactivator Vmw65 for interaction with the cellular octamer-binding protein and target TAATGARAT sequences J. Virol. 64 1990 2716 2724
12. Greensides, D.R. 2000. VP16 localization during herpes simplex-1 infection. M.S. thesis, Michigan State University.
13. J.G. Grossmann, A.J. Sharff, P. O'Hare, and B. Luisi Molecular shapes of transcription factors TFIIB and VP16 in solution: implications for recognition Biochemistry 40 2001 6267 6274
14. W. Herr, and M.A. Cleary The POU domain: versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain Genes Dev. 9 1995 1679 1693
15. F.J. Herrera, and S.J. Triezenberg VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection J. Virol. 78 2004 9689 9696
16. P. Hippenmeyer, and M. Highkin High level, stable production of recombinant proteins in mammalian cell culture using the herpesvirus VP16 transactivator Biotechnology (NY) 11 1993 1037 1041
17. L.M. Iakoucheva, P. Radivojac, C.J. Brown, T.R. O'Connor, J.G. Sikes, Z. Obradovic, and A.K. Dunker The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 32 2004 1037 1049
18. R. Jordan, L. Schang, and P.A. Schaffer Transactivation of herpes simplex virus type 1 immediate-early gene expression by virion-associated factors is blocked by an inhibitor of cyclin-dependent protein kinases J. Virol. 73 1999 8843 8847
19. M. Katan, A. Haigh, C.P. Verrijzer, P.C. Vandervliet, and P. O'Hare Characterization of a cellular factor which interacts functionally with Oct-1 in the assembly of a multicomponent transcription complex Nucleic Acids Res. 18 1990 6871 6880
20. J. Knez, P.T. Bilan, and J.P. Capone A single amino acid substitution in herpes simplex virus type 1 VP16 inhibits binding to the virion host shutoff protein and is incompatible with virus growth J. Virol. 77 2003 2892 2902
21. T.M. Kristie, J.H. LeBowitz, and P.A. Sharp The octamer-binding proteins form multi-protein-DNA complexes with the HSV alpha TIF regulatory protein EMBO J. 8 1989 4229 4238
22. S. La Boissiere, A. Izeta, S. Malcomber, and P. O'Hare Compartmentalization of VP16 in cells infected with recombinant herpes simplex virus expressing VP16-green fluorescent protein fusion proteins J. Virol. 78 2004 8002 8014
23. J.S. Lai, and W. Herr Interdigitated residues within a small region of VP16 interact with Oct-1, HCF, and DNA Mol. Cell. Biol. 17 1997 3947 3954
24. Q. Lam, C.A. Smibert, K.E. Koop, C. Lavery, J.P. Capone, S.P. Weinheimer, and J.R. Smiley Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function EMBO J. 15 1996 2575 2581
25. K.L. LaMarco, and S.L. McKnight Purification of a set of cellular polypeptides that bind to the purine-rich cis-regulatory element of herpes simplex virus immediate early genes Genes Dev. 3 1989 1372 1383
26. I.A. Leighton, K.N. Dalby, F.B. Caudwell, P.T. Cohen, and P. Cohen Comparison of the specificities of p70 S6 kinase and MAPKAP kinase-1 identifies a relatively specific substrate for p70 S6 kinase: the N-terminal kinase domain of MAPKAP kinase-1 is essential for peptide phosphorylation FEBS Lett. 375 1995 289 293
27. S. Lemaster, and B. Roizman Herpes simplex virus phosphoproteins: II. Characterization of the virion protein kinase and of the polypeptides phosphorylated in the virion J. Virol. 35 1980 798 811
28. Y. Liu, W. Gong, C.C. Huang, W. Herr, and X. Cheng Crystal structure of the conserved core of the herpes simplex virus transcriptional regulatory protein VP16 Genes Dev. 13 1999 1692 1703
29. T method Methods 25 2001 402 408
30. R. Lu, and V. Misra Zhangfei: a second cellular protein interacts with herpes simplex virus accessory factor HCF in a manner similar to Luman and VP16 Nucleic Acids Res. 28 2000 2446 2454
31. R. Lu, P. Yang, S. Padmakumar, and V. Misra The herpesvirus transactivator VP16 mimics a human basic domain leucine zipper protein, Luman, in its interaction with HCF J. Virol. 72 1998 6291 6297
32. C. McLean, A. Buckmaster, D. Hancock, A. Buchanan, A. Fuller, and A.C. Minson Monoclonal antibodies to three nonglycosylated antigens of herpes simplex virus type 2 J. Gen. Virol. 63 1982 297 305
33. S. Memedula, and A.S. Belmont Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16 Curr. Biol. 13 2003 241 246
34. G. Mittler, T. Stuhler, L. Santolin, T. Uhlmann, E. Kremmer, F. Lottspeich, L. Berti, and M. Meisterernst A novel docking site on mediator is critical for activation by VP16 in mammalian cells EMBO J. 22 2003 6494 6504
35. H. Moriuchi, M. Moriuchi, R. Pichyangkura, S.J. Triezenberg, S.E. Straus, and J.I. Cohen Hydrophobic cluster analysis predicts an amino-terminal domain of varicella-zoster virus open reading frame 10 required for transcriptional activation Proc. Natl. Acad. Sci. U.S.A. 92 1995 9333 9337
36. E.E. Morrison, A.J. Stevenson, Y.F. Wang, and D.M. Meredith 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
37. E.E. Morrison, Y.F. Wang, and D.M. Meredith Phosphorylation of structural components promotes dissociation of the herpes simplex virus type 1 tegument J. Virol. 72 1998 7108 7114
38. H. Moss Properties of the herpes simplex virus type 2 trans-inducing factor Vmw65 in wild-type and mutant viruses J. Gen. Virol. 70 1989 1579 1585
39. K.E. Neely, A.H. Hassan, A.E. Wallberg, D.J. Steger, B.R. Cairns, A.P.H. Wright, and J.L. Workman Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays Mol. Cell 4 1999 649 655
40. M.L. Nogueira, V.E. Wang, D. Tantin, P.A. Sharp, and T.M. Kristie Herpes simplex virus infections are arrested in Oct-1-deficient cells Proc. Natl. Acad. Sci. U.S.A. 101 2004 1473 1478
41. P. O'Hare The virion transactivator of herpes simplex virus Semin. Virol. 4 1993 145 155
42. P. O'Hare, and C.R. Goding Herpes simplex virus regulatory elements and the immunoglobulin octamer bind a common factor and are both targets for virion transactivation Cell 52 1988 435 445
43. D. O'Reilly, O. Hanscombe, and P. O'Hare A single serine residue at position 375 of VP16 is critical for complex assembly with Oct-1 and HCF and is a target of phosphorylation by casein kinase II EMBO J. 16 1997 2420 2430
44. A.P.W. Poon, and B. Roizman The phenotype in vitro and in infected cells of herpes simplex virus 1 alpha-trans-inducing factor (VP16) carrying temperature-sensitive mutations introduced by substitution of cysteines J. Virol. 69 1995 7658 7667
45. J.L. Regier, F. Shen, and S.J. Triezenberg Pattern of aromatic and hydrophobic amino acids critical for one of two subdomains of the VP16 transcriptional activator Proc. Natl. Acad. Sci. U.S.A. 90 1993 883 887
46. P.P. Roux, and J. Blenis ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions Microbiol. Mol. Biol. Rev. 68 2004 320 344
47. L.M. Schang, A. Rosenberg, and P.A. Schaffer Transcription of herpes simplex virus immediate-early and early genes is inhibited by roscovitine, an inhibitor specific for cellular cyclin-dependent kinases J. Virol. 73 1999 2161 2172
48. L.M. Schang, A. Bantly, M. Knockaert, F. Shaheen, L. Meijer, M.H. Malim, N.S. Gray, and P.A. Schaffer Pharmacological cyclin-dependent kinase inhibitors inhibit replication of wild-type and drug-resistant strains of herpes simplex virus and human immunodeficiency virus type 1 by targeting cellular, not viral, proteins J. Virol. 76 2002 7874 7882
49. P. Shaw, J. Knez, and J.P. Capone Amino acid substitutions in the herpes simplex virus transactivator VP16 uncouple direct protein-protein interaction and DNA binding from complex assembly and transactivation J. Biol. Chem. 270 1995 29030 29037
50. K.A. Simmen, A. Newell, M. Robinson, J.S. Mills, G. Canning, R. Handa, K. Parkes, N. Borkakoti, and R. Jupp Protein interactions in the herpes simplex virus type 1 VP16 induced complex: VP16 peptide inhibition and mutational analysis of the host cell factor requirements J. Virol. 71 1997 3886 3894
51. C.A. Smibert, B. Popova, P. Xiao, J.P. Capone, and J.R. Smiley Herpes simplex virus VP16 forms a complex with the virion host shutoff protein vhs J. Virol. 68 1994 2339 2346
52. J.R. Smiley, and J. Duncan Truncation on the C-terminal acidic transcriptional activation domain of herpes simplex virus VP16 produces a phenotype similar to that of the in1814 linker insertion mutation J. Virol. 71 1997 6191 6193
53. S.S. Strand, and D.A. Leib Role of the VP16-binding domain of vhs in viral growth, host shutoff activity, and pathogenesis J. Virol. 78 2004 13562 13572
54. S.S. Strand, T.K. Vanheyningen, and D.A. Leib The virion host shutoff protein of herpes simplex virus type 1 has RNA degradation activity in primary neurons J. Virol. 78 2004 8400 8403
55. S.M. Sullivan, P.J. Horn, V.A. Olson, A.H. Koop, W. Niu, R.H. Ebright, and S.J. Triezenberg Mutational analysis of a transcriptional activation region of the VP16 protein of herpes simplex virus Nucleic Acids Res. 26 1998 4487 4496
56. R. Tal-Singer, R. Pichyangkura, E. Chung, T.M. Lasner, B.P. Randazzo, J.Q. Trojanowski, N.W. Fraser, and S.J. Triezenberg The transcriptional activation domain of VP16 is required for efficient infection and establishment of latency by HSV-1 in the murine peripheral and central nervous systems Virology 259 1999 20 33
57. S.J. Triezenberg Structure and function of transcriptional activation domains Curr. Opin. Genet. Dev. 5 1995 190 196
58. S.J. Triezenberg, R.C. Kingsbury, and S.L. McKnight Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression Genes Dev. 2 1988 718 729
59. S.J. Triezenberg, K.L. LaMarco, and S.L. McKnight Evidence of DNA:protein interactions that mediate HSV-1 immediate early gene activation by VP16 Genes Dev. 2 1988 730 743
60. R.T. Utley, K. Ikeda, P.A. Grant, J. Cote, D.J. Steger, A. Eberharter, S. John, and J.L. Workman Transcriptional activators direct histone acetyltransferase complexes to nucleosomes Nature 394 1998 498 502
61. S. Walker, R. Greaves, and P. O'Hare Transcriptional activation by the acidic domain of Vmw65 requires the integrity of the domain and involves additional determinants distinct from those necessary for TFIIB binding Mol. Cell. Biol. 13 1993 5233 5244
62. S. Walker, S. Hayes, and P. O'Hare Site-specific conformational alteration of the Oct-1 POU domain-DNA complex as the basis for differential recognition by Vmw65 (VP16) Cell 79 1994 841 852
63. L. Wang, S.R. Grossman, and E. Kieff Epstein-Barr virus nuclear protein 2 interacts with p300, CBP, and PCAF histone acetyltransferases in activation of the LMP1 promoter Proc. Natl. Acad. Sci. U.S.A. 97 2000 430 435
64. S.P. Weinheimer, B.A. Boyd, S.K. Durham, J.L. Resnick, and D.R. O'Boyle Deletion of the VP16 open reading frame of herpes simplex virus type 1 J. Virol. 66 1992 258 269
65. G. Werstuck, and J.P. Capone Mutational analysis of the herpes simplex virus trans-inducing factor Vmw65 Gene 75 1989 213 224
66. T.-J. Wu, G. Monokian, D.F. Mark, and C.R. Wobbe Transcriptional activation by herpes simplex virus type 1 VP16 in vitro and its inhibition by oligopeptides Mol. Cell. Biol. 14 1994 3484 3493
67. P. Xiao, and J.P. Capone A cellular factor binds to the herpes simplex virus type-1 transactivator Vmw65 and is required for Vmw65-dependent protein-DNA complex assembly with Oct-1 Mol. Cell. Biol. 10 1990 4974 4977
68. F. Yang, R. DeBeaumont, S. Zhou, and A.M. Näär The activator-recruited cofactor/Mediator coactivator subunit ARC92 is a functionally important target of the VP16 transcriptional activator Proc. Natl. Acad. Sci. U.S.A. 101 2004 2339 2344