A role for E1B-AP5 in ATR signaling pathways during adenovirus infection

Journal of Virology

Volumn 82, Issue 15, 2008, Pages 7640-7652

  Blackford, Andrew N ^a   Bruton, Rachel K ^a   Dirlik, Orkide ^b   Stewart, Grant S ^a   Taylor, A Malcolm R ^a   Dobner, Thomas ^b   Grand, Roger J A ^a   Turnell, Andrew S ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF HAMBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATR INTERACTING PROTEIN; ATR PROTEIN; E1B 55K ASSOCIATED PROTEIN 5; HISTONE H2AX; NUCLEAR PROTEIN; PROTEIN RAD9; REPLICATION FACTOR A; REPLICATION PROTEIN A 32; REPLICATION PROTEIN A 70; RIBONUCLEOPROTEIN; SMC1 PROTEIN;

ADENOVIRUS; ADENOVIRUS 12; ADENOVIRUS 5; ARTICLE; DNA DAMAGE; DNA REPLICATION; EMBRYO; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRUS INFECTION; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOVIRIDAE; ADENOVIRUS E1B PROTEINS; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HISTONES; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ADENOVIRIDAE;

EID: 47749150000     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00170-08     Document Type: Article

References (39)

1. Araujo, F. D., T. H. Stracker, C. T. Carson, D. V. Lee, and M. D. Weitzman. 2005. Adenovirus type 5 E4orf3 protein targets the Mre11 complex to cytoplasmic aggresomes. J. Virol. 79:11382-11391.
2. Baker, A., K. J. Rohleder, L. A. Hanakahi, and G. Ketner. 2007. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 81:7034-7040.
3. Barral, P. M., A. Rusch, A. S. Turnell, P. H. Gallimore, P. J. Byrd, T. Dobner, and R. J. A. Grand. 2005. The interaction of the hnRNP family member E1B-AP5 with p53. FEBS Lett. 579:2752-2758.
4. Berk, A. J. 2005. Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 24:7673-7685.
5. Binz, S. K., A. M. Sheehan, and M. S. Wold. 2004. Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair 3:1015-1024.
6. Blanchette, P., C. Y. Cheng, Q. Yan, G. Ketner, D. A. Ornelles, T. Dobner, R. C. Conaway, J. W. Conaway, and P. E. Branton. 2004. Both BC-box motifs of adenovirus protein E4orf6 are required to efficiently assemble an E3 ligase complex that degrades p53. Mol. Cell. Biol. 24:9619-9629.
7. Blank, M., Y. Lerenthal, L. Mittelman, and Y. Shiloh. 2006. Condensin I recruitment and uneven chromatin condensation precede mitotic cell death in response to DNA damage. J. Cell Biol. 174:195-206.
8. Brush, G. S., C. W. Anderson, and T. J. Kelly. 1994. The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication. Proc. Natl. Acad. Sci. USA 91:12520-12524.
9. Carson, C. T., R. A. Schwartz, T. H. Stracker, C. E. Lilley, D. V. Lee, and M. D. Weitzman. 2003. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22:6610-6620.
10. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
11. de Jong, R. N., P. C. van der Vliet, and A. B. Brenkman. 2003. Adenovirus DNA replication: protein priming, jumping back and the role of the DNA binding protein DBP. Curr. Top. Microbiol. Immunol. 272:187-211.
12. Evans, J. D., and P. Hearing. 2005. Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol. 79:6207-6215.
13. Fairman, M. P., and B. Stillman. 1988. Cellular factors required for multiple stages of SV40 replication in vitro. EMBO J. 7:1211-1218.
14. Fanning, E., V. Klimovich, and A. R. Nager. 2006. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34:4126-4137.
15. Gabler, S., H. Schütt, P. Groitl, H. Wolf, T. Shenk, and T. Dobner. 1998. E1B 55-kilodalton-associated protein: a cellular protein with RNA-binding activity implicated in nucleocytoplasmic transport of adenovirus and cellular mRNAs. J. Virol. 72:7960-7971.
16. Harada, J. N., A. Shevchenko, A. Shevchenko, D. C. Pallas, and A. J. Berk. 2002. Analysis of the adenovirus E1B-55K-anchored proteome reveals its link to ubiquitination machinery. J. Virol. 76:9194-9206.
17. Henricksen, L. A., C. B. Umbricht, and M. S. Wold. 1994. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269:11121-11132.
18. Kim, J. E., K. Minter-Dykhouse, and J. Chen. 2006. Signaling networks controlled by the MRN complex and MDC1 during early DNA damage responses. Mol. Carcinog. 45:403-408.
19. Kzhyshkowska, J., H. Schütt, M. Liss, E. Kremmer, R. Stauber, H. Wolf, and T. Dobner. 2001. Heterogeneous nuclear ribonucleoprotein E1B-AP5 is methylated in its Arg-Gly-Gly (RGG) box and interacts with human arginine methyltransferase HRMT1L1. Biochem. J. 358:305-314.
20. Kzhyshkowska, J., A. Rusch, H. Wolf, and T. Dobner. 2003. Regulation of transcription by the heterogeneous nuclear ribonucleoprotein E1B-AP5 is mediated by complex formation with the novel bromodomain-containing protein BRD7. Biochem. J. 371:385-393.
21. Lilley, C. E., R. A. Schwartz, and M. D. Weitzman. 2007. Using or abusing: viruses and the cellular DNA damage response. Trends Microbiol. 15:119-126.
22. Luo, M. H., K. Rosenke, K. Czornak, and E. A. Fortunato. 2007. Human cytomegalovirus disrupts both ataxia telangiectasia mutated protein (ATM)-and ATM-Rad3-related kinase-mediated DNA damage responses during lytic infection. J. Virol. 81:1934-1950.
23. Moumen, A., P. Masterson, M. J. O'Connor, and S. P. Jackson. 2005. hnRNP K: an HDM2 target and transcriptional coactivator of p53 in response to DNA damage. Cell 123:1065-1078.
24. Olson, E., C. J. Nievera, V. Klimovich, E. Fanning, and X. Wu. 2006. RPA2 is a direct downstream target for ATR to regulate the S-phase checkpoint. J. Biol. Chem. 281:39517-39533.
25. Paulsen, R. D., and K. A. Cimprich. 2007. The ATR pathway: fine-tuning the fork. DNA Repair (Amsterdam) 6:953-966.
26. Petermann, E., and K. W. Caldecott. 2006. Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 5:2203-2209.
27. Querido, E., P. Blanchette, Q. Yan, T. Kamura, M. Morrison, D. Boivin, W. G. Kaelin, R. C. Conaway, J. W. Conaway, and P. E. Branton. 2001. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15:3104-3117.
28. Roshal, M., B. Kim, Y. Zhu, P. Nghiem, and fsV. Planelles. 2003. Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J. Biol. Chem. 278:25879-25886.
29. Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155-168.
30. Stracker, T. H., C. T. Carson, and M. D. Weitzman. 2002. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418:348-352.
31. Stracker, T. H., D. V. Lee, C. T. Carson, F. D. Araujo, D. A. Ornelles, and M. D. Weitzman. 2005. Serotype-specific reorganization of the Mre11 complex by adenoviral E4orf3 proteins. J. Virol. 79:6664-6673.
32. Turnell, A. S., R. J. A. Grand, and P. H. Gallimore. 1999. The replicative capacities of large E1B-null group A and group C adenoviruses are independent of host cell p53 status. J. Virol. 73:2074-2083.
33. Weitzman, M. D., C. T. Carson, R. A. Schwartz, and C. E. Lilley. 2004. Interactions of viruses with the cellular DNA repair machinery. DNA Repair (Amsterdam) 3:1165-1173.
34. Wilkinson, D. E., and S. K. Weller. 2006. Herpes simplex virus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 119:2695-2703.
35. Wold, M. S., and T. J. Kelly. 1988. Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc. Natl. Acad. Sci. USA 85:2523-2527.
36. Woo, J. L., and A. J. Berk. 2007. Adenovirus ubiquitin-protein ligase stimulates viral late mRNA nuclear export. J. Virol. 81:575-587.
37. Yang, C., and F. Carrier. 2001. The UV-inducible RNA-binding protein A18 (A18 hnRNP) plays a protective role in the genotoxic stress response. J. Biol. Chem. 276:47277-47284.
38. Zou, L., D. Cortez, and S. J. Elledge. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16:198-208.
39. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.