An intact sequence-specific DNA-binding domain is required for human cytomegalovirus-mediated sequestration of p53 and may promote in vivo binding to the viral genome during infection

Virology

Volumn 348, Issue 1, 2006, Pages 19-34

  Rosenke, Kyle ^a   Samuel, Melanie A ^a   McDowell, Eric T ^a   Toerne, Melissa A ^a   Fortunato, Elizabeth A ^a  

^a UNIVERSITY OF IDAHO   (United States)

Author keywords

DNA binding domain; Human cytomegalovirus; In vivo binding assays; p53; Sequestration

Indexed keywords

GENOMIC DNA; GREEN FLUORESCENT PROTEIN; PROTEIN P53; STRUCTURAL PROTEIN; VIRUS DNA; VIRUS PROTEIN;

ACETYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA BINDING; DNA REPLICATION; DNA SEQUENCE; DNA TRANSFECTION; FIBROBLAST; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IN VIVO STUDY; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; TRANSACTIVATION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION; WILD TYPE;

ARTIFICIAL GENE FUSION; BINDING SITES; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CYTOMEGALOVIRUS; DNA, VIRAL; FIBROBLASTS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

DNA VIRUSES; HUMAN HERPESVIRUS 5;

EID: 33646062855     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2005.12.013     Document Type: Article

References (72)

1. Adimoolam S., and Ford J.M. p53 and regulation of DNA damage recognition during nucleotide excision repair. DNA Rep. (Amst) 2 9 (2003) 947-954
2. Ashcroft M., Kubbutat M.H., and Vousden K.H. Regulation of p53 function and stability by phosphorylation. Mol. Cell. Biol. 19 3 (1999) 1751-1758
3. Blander G., Kipnis J., Leal J.F., Yu C.E., Schellenberg G.D., and Oren M. Physical and functional interaction between p53 and the Werner's syndrome protein. J. Biol. Chem. 274 41 (1999) 29463-29469
4. Bogler O., Huang H.J., Kleihues P., and Cavenee W.K. The p53 gene and its role in human brain tumors. Glia 15 3 (1995) 308-327
5. Bonin L.R., and McDougall J.K. Human cytomegalovirus IE2 86-kilodalton protein binds p53 but does not abrogate G1 checkpoint function. J. Virol. 71 8 (1997) 5861-5870
6. Bresnahan W.A., Boldogh I., Thompson E.A., and Albrecht T. Human cytomegalovirus inhibits cellular DNA synthesis and arrests productively infected cells in late G1. Virology 224 (1996) 150-160
7. Bunz F., Dutriaux A., Lengauer C., Waldman T., Zhou S., Brown J.P., Sedivy J.M., Kinzler K.W., and Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282 5393 (1998) 1497-1501
8. Castillo J.P., Yurochko A.D., and Kowalik T.F. Role of human cytomegalovirus immediate-early proteins in cell growth control. J. Virol. 74 17 (2000) 8028-8037
9. Chene P. In vitro analysis of the dominant negative effect of p53 mutants. J. Mol. Biol. 281 2 (1998) 205-209
10. Chene P. The role of tetramerization in p53 function. Oncogene 20 21 (2001) 2611-2617
11. Chung T.W., Lee Y.C., Ko J.H., and Kim C.H. Hepatitis B Virus X protein modulates the expression of PTEN by inhibiting the function of p53, a transcriptional activator in liver cells. Cancer Res. 63 13 (2003) 3453-3458
12. Debbas M., and White E. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7 4 (1993) 546-554
13. Dridi W., Fetni R., Lavoie J., Poupon M.F., and Drouin R. The dominant-negative effect of p53 mutants and p21 induction in tetraploid G1 arrest depends on the type of p53 mutation and the nature of the stimulus. Cancer Genet. Cytogenet. 143 1 (2003) 39-49
14. Dumont P., Della Pietra A., and Murphy M.E. Methods to study p53-repressed promoters. Methods Mol. Biol. 234 (2003) 111-120
15. Dutta A., Ruppert J.M., Aster J.C., and Winchester E. Inhibition of DNA replication factor RPA by p53. Nature 365 6441 (1993) 79-82 (see comments)
16. el-Deiry W.S., Kern S.E., Pietenpol J.A., Kinzler K.W., and Vogelstein B. Definition of a consensus binding site for p53. Nat. Genet. 1 1 (1992) 45-49
17. Fortunato E.A., and Spector D.H. p53 and RPA are sequestered in viral replication centers in the nuclei of cells infected with human cytomegalovirus. J. Virol. 72 3 (1998) 2033-2039
18. Gostissa M., Hengstermann A., Fogal V., Sandy P., Schwarz S.E., Scheffner M., and Del Sal G. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 18 22 (1999) 6462-6471
19. Gu W., and Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90 4 (1997) 595-606
20. Hoffman W.H., Biade S., Zilfou J.T., Chen J., and Murphy M. Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J. Biol. Chem. 277 5 (2002) 3247-3257
21. Hsu C.H., Chang M.D., Tai K.Y., Yang Y.T., Wang P.S., Chen C.J., Wang Y.H., Lee S.C., Wu C.W., and Juan L.J. HCMV IE2-mediated inhibition of HAT activity downregulates p53 function. EMBO J. 23 11 (2004) 2269-2280
22. Hwang B.J., Ford J.M., Hanawalt P.C., and Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. U.S.A. 96 2 (1999) 424-428
23. Jault F.M., Jault J.-M., Ruchti F., Fortunato E.A., Clark C., Corbeil J., Richman D.D., and Spector D.H. Cytomegalovirus infection induces high levels of cyclins, phosphorylated RB, and p53, leading to cell cycle arrest. J. Virol. 69 (1995) 6697-6704
24. Jenkins J.R., Chumakov P., Addison C., Sturzbecher H.W., and Wade-Evans A. Two distinct regions of the murine p53 primary amino acid sequence are implicated in stable complex formation with simian virus 40 T antigen. J. Virol. 62 10 (1988) 3903-3906
25. Jeong S.J., Radonovich M., Brady J.N., and Pise Masison C.A. HTLV-I Tax induces a novel interaction between p65/RelA and p53 which results in inhibition of p53 transcriptional activity. Blood 104 5 (2004) 1490-1497
26. Juven T., Barak Y., Zauberman A., George D.L., and Oren M. Wild type p53 can mediate sequence-specific transactivation of an internal promoter within the mdm2 gene. Oncogene 8 12 (1993) 3411-3416
27. Kaeser M.D., and Iggo R.D. Chromatin immunoprecipitation analysis fails to support the latency model for regulation of p53 DNA binding activity in vivo. Proc. Natl. Acad. Sci. U.S.A. 99 1 (2002) 95-100
28. Kerry J.A., Priddy M.A., Jervey T.Y., Kohler C.P., Staley T.L., Vanson C.D., Jones T.R., Iskenderian A.C., Anders D.G., and Stenberg R.M. Multiple regulatory events influence human cytomegalovirus DNA polymerase (UL54) expression during viral infection. J. Virol. 70 1 (1996) 373-382
29. Ko L.J., and Prives C. p53: puzzle and paradigm. Genes Dev. 10 9 (1996) 1054-1072
30. Kovacs A., Weber M.L., Burns L.J., Jacob H.S., and Vercellotti G.M. Cytoplasmic sequestration of p53 in cytomegalovirus-infected human endothelial cells. Am. J. Pathol. 149 5 (1996) 1531-1539
31. Liu Y., and Kulesz-Martin M. p53 protein at the hub of cellular DNA damage response pathways through sequence-specific and non-sequence-specific DNA binding. Carcinogenesis 22 6 (2001) 851-860
32. Liu L., Scolnick D.M., Trievel R.C., Zhang H.B., Marmorstein R., Halazonetis T.D., and Berger S.L. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol. Cell. Biol. 19 2 (1999) 1202-1209
33. Lokensgard J.R., Cheeran M.C., Gekker G., Hu S., Chao C.C., and Peterson P.K. Human cytomegalovirus replication and modulation of apoptosis in astrocytes. J. Hum. Virol. 2 2 (1999) 91-101
34. MacLachlan T.K., and El-Deiry W.S. Identification of DNA-binding of tumor suppressor genes by chromatin immunoprecipitation. Methods Mol. Biol. 223 (2003) 129-133
35. MacLachlan T.K., Takimoto R., and El-Deiry W.S. BRCA1 directs a selective p53-dependent transcriptional response towards growth arrest and DNA repair targets. Mol. Cell. Biol. 22 12 (2002) 4280-4292
36. Meertens L., Pise-Masison C., Quere N., Brady J., Gessain A., and Mahieux R. Utilization of the CBP but not the p300 co-activator by human T-lymphotropic virus type-2 Tax for p53 inhibition. Oncogene 23 32 (2004) 5447-5458
37. Milner J., and Medcalf E.A. Cotranslation of activated mutant p53 with wild type drives the wild-type p53 protein into the mutant conformation. Cell 65 5 (1991) 765-774
38. Mirza A., Wu Q., Wang L., McClanahan T., Bishop W.R., Gheyas F., Ding W., Hutchins B., Hockenberry T., Kirschmeier P., Greene J.R., and Liu S. Global transcriptional program of p53 target genes during the process of apoptosis and cell cycle progression. Oncogene 22 23 (2003) 3645-3654
39. Miyashita T., Harigai M., Hanada M., and Reed J.C. Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res. 54 12 (1994) 3131-3135
40. Muganda P., Mendoza O., Hernandez J., and Qian Q. Human cytomegalovirus elevates levels of the cellular protein p53 in infected fibroblasts. J. Virol. 68 (1994) 8028-8034
41. Muganda P., Carrasco R., and Qian Q. The human cytomegalovirus IE2 86 kDa protein elevates p53 levels and transactivates the p53 promoter in human fibroblasts. Cell. Mol. Biol. (Noisy-le-grand) 44 2 (1998) 321-331
42. Murphy M., Hinman A., and Levine A.J. Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes Dev. 10 23 (1996) 2971-2980
43. Murphy E.A., Streblow D.N., Nelson J.A., and Stinski M.F. The human cytomegalovirus IE86 protein can block cell cycle progression after inducing transition into the S phase of permissive cells. J. Virol. 74 15 (2000) 7108-7118
44. Naviaux R.K., Costanzi E., Haas M., and Verma I.M. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70 8 (1996) 5701-5715
45. Prives C., and Manley J.L. Why is p53 acetylated?. Cell 107 7 (2001) 815-818
46. Qian H., Wang T., Naumovski L., Lopez C.D., and Brachmann R.K. Groups of p53 target genes involved in specific p53 downstream effects cluster into different classes of DNA binding sites. Oncogene 21 51 (2002) 7901-7911
47. Raycroft L., Wu H.Y., and Lozano G. Transcriptional activation by wild-type but not transforming mutants of the p53 anti-oncogene. Science 249 4972 (1990) 1049-1051
48. Rodriguez M.S., Desterro J.M., Lain S., Midgley C.A., Lane D.P., and Hay R.T. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 18 22 (1999) 6455-6461
49. Sakaguchi K., Herrera J.E., Saito S., Miki T., Bustin M., Vassilev A., Anderson C.W., and Appella E. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 12 18 (1998) 2831-2841
50. Sax J.K., and El-Deiry W.S. p53 downstream targets and chemosensitivity. Cell Death Differ. 10 4 (2003) 413-417
51. Scheffner M., Werness B.A., Huibregtse J.M., Levine A.J., and Howley P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63 6 (1990) 1129-1136
52. Song Y.J., and Stinski M.F. Inhibition of cell division by the human cytomegalovirus IE86 protein: role of the p53 pathway or cyclin-dependent kinase 1/cyclin B1. J. Virol. 79 4 (2005) 2597-2603
53. Speir E., Modali R., Huang E.-S., Leon M.B., Sahwl F., Finkel T., and Epstein S.E. Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 265 (1994) 391-394
54. Sturzbecher H.W., Donzelmann B., Henning W., Knippschild U., and Buchhop S. p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO J. 15 8 (1996) 1992-2002
55. Szak S.T., Mays D., and Pietenpol J.A. Kinetics of p53 binding to promoter sites in vivo. Mol. Cell. Biol. 21 10 (2001) 3375-3386
56. Tamashiro J.C., Hock L.J., and Spector D.H. Construction of a cloned library of the EcoRI fragments from the human cytomegalovirus genome (strain AD169). J. Virol. 42 2 (1982) 547-557
57. Tsai H.L., Kou G.H., Chen S.C., Wu C.W., and Lin Y.S. Human cytomegalovirus immediate-early protein IE2 tethers a transcriptional repression domain to p53. J. Biol. Chem. 271 7 (1996) 3534-3540
58. Tuck S.P., and Crawford L. Characterization of the human p53 gene promoter. Mol. Cell. Biol. 9 5 (1989) 2163-2172
59. Unger T., Nau M.M., Segal S., and Minna J.D. p53: a transdominant regulator of transcription whose function is ablated by mutations occurring in human cancer. EMBO J. 11 4 (1992) 1383-1390
60. Wang X.W., Forrester K., Yeh H., Feitelson M.A., Gu J.R., and Harris C.C. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc. Natl. Acad. Sci. U.S.A. 91 6 (1994) 2230-2234
61. Wang X.W., Yeh H., Schaeffer L., Roy R., Moncollin V., Egly J.M., Wang Z., Freidberg E.C., Evans M.K., Taffe B.G., et al. p53 modulation of TFIIH-associated nucleotide excision repair activity. Nat. Genet. 10 2 (1995) 188-195
62. Wang J., Marker P.H., Belcher J.D., Wilcken D.E., Burns L.J., Vercellotti G.M., and Wang X.L. Human cytomegalovirus immediate early proteins upregulate endothelial p53 function. FEBS Lett. 474 2-3 (2000) 213-216
63. Wang X.W., Tseng A., Ellis N.A., Spillare E.A., Linke S.P., Robles A.I., Seker H., Yang Q., Hu P., Beresten S., Bemmels N.A., Garfield S., and Harris C.C. Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem. 276 35 (2001) 32948-32955
64. Wei W., Hemmer R.M., and Sedivy J.M. Role of p14 (ARF) in replicative and induced senescence of human fibroblasts. Mol. Cell. Biol. 21 20 (2001) 6748-6757
65. Werness B.A., Levine A.J., and Howley P.M. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248 4951 (1990) 76-79
66. Wing B.A., Johnson R.A., and Huang E.S. Identification of positive and negative regulatory regions involved in regulating expression of the human cytomegalovirus UL94 late promoter: role of IE2-86 and cellular p53 in mediating negative regulatory function. J. Virol. 72 3 (1998) 1814-1825
67. Xu Y. Regulation of p53 responses by post-translational modifications. Cell Death Differ. 10 4 (2003) 400-403
68. Zakut-Houri R., Bienz-Tadmor B., Givol D., and Oren M. Human p53 cellular tumor antigen: cDNA sequence and expression in COS cells. EMBO J. 4 5 (1985) 1251-1255
69. Zantema A., Fransen J.A., Davis-Olivier A., Ramaekers F.C., Vooijs G.P., DeLeys B., and Van der Eb A.J. Localization of the E1B proteins of adenovirus 5 in transformed cells, as revealed by interaction with monoclonal antibodies. Virology 142 1 (1985) 44-58
70. Zhu H., Shen Y., and Shenk T. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69 12 (1995) 7960-7970
71. Zink D., Mayr C., Janz C., and Wiesmuller L. Association of p53 and MSH2 with recombinative repair complexes during S phase. Oncogene 21 31 (2002) 4788-4800
72. Zotchev S.B., Protopopova M., and Selivanova G. p53 C-terminal interaction with DNA ends and gaps has opposing effect on specific DNA binding by the core. Nucleic Acids Res. 28 20 (2000) 4005-4012