The adenovirus E4 11k protein binds and relocalizes the cytoplasmic P-body component Ddx6 to aggresomes

Virology

Volumn 417, Issue 1, 2011, Pages 161-168

  Greer, Amy E ^a   Hearing, Patrick ^b   Ketner, Gary ^c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Adenovirus E4 11k; Adenovirus E4 ORF3; Aggresome; Ddx6; Host virus interaction; Late gene expression; MRNA degradation; P body; RCK; Relocalization; Reorganization

Indexed keywords

ADENOVIRUS E4 11 K PROTEIN; CYTOPLASM PROTEIN; DDX6 PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; DDX6 PROTEIN, HUMAN; DEAD BOX PROTEIN; ONCOPROTEIN;

ADENOVIRUS; AGGRESOME; ARTICLE; CELL SPECIFICITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; NONHUMAN; P BODY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RNA DEGRADATION; GENE EXPRESSION REGULATION; GENETICS; HELA CELL; METABOLISM; MUTATION; OPEN READING FRAME; PHYSIOLOGY; PROTEIN TRANSPORT; VIRUS REPLICATION;

ADENOVIRIDAE;

ADENOVIRUS E4 PROTEINS; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HUMANS; MUTATION; OPEN READING FRAMES; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; VIRUS REPLICATION;

EID: 79960958089     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.05.017     Document Type: Article

References (45)

1. Aizer A., Brody Y., Ler L.W., Sonenberg N., Singer R.H., Shav-Tal Y. The dynamics of mammalian P body transport, assembly, and disassembly in vivo. Mol. Biol. Cell 2008, 19:4154-4166.
2. Anderson P., Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 2009, 10:430-436.
3. Araujo F.D., Stracker T.H., Carson C.T., Lee D.V., Weitzman M.D. Adenovirus type 5 E4orf3 protein targets the Mre11 complex to cytoplasmic aggresomes. J. Virol. 2005, 79:11382-11391.
4. Baker A., Rohleder K.J., Hanakahi L.A., Ketner G. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 2007, 81:7034-7040.
5. Boyer J., Rohleder K., Ketner G. Adenovirus E4 34k and E4 11k inhibit double strand break repair and are physically associated with the cellular DNA-dependent protein kinase. Virology 1999, 263:307-312.
6. Bridge E., Ketner G. Redundant control of adenovirus late gene expression by early region 4. J. Virol. 1989, 63:631-638.
7. Carson C.T., Orazio N.I., Lee D.V., Suh J., Bekker-Jensen S., Araujo F.D., Lakdawala S.S., Lilley C.E., Bartek J., Lukas J., Weitzman M.D. Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 2009, 28:652-662.
8. Carvalho T., Seeler J.S., Ohman K., Jordan P., Pettersson U., Akusjarvi G., Carmo-Fonseca M., Dejean A. Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. J. Cell Biol. 1995, 131:45-56.
9. Challberg S.S., Ketner G. Deletion mutants of adenovirus 2: isolation and initial characterization of virus carrying mutations near the right end of the viral genome. Virology 1981, 114:196-209.
10. Chu C.Y., Rana T.M. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 2006, 4:e210.
11. Coller J., Parker R. General translational repression by activators of mRNA decapping. Cell 2005, 122:875-886.
12. Coller J.M., Tucker M., Sheth U., Valencia-Sanchez M.A., Parker R. The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 2001, 7:1717-1727.
13. Cordin O., Banroques J., Tanner N.K., Linder P. The DEAD-box protein family of RNA helicases. Gene 2006, 367:17-37.
14. Decker C.J., Teixeira D., Parker R. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol. 2007, 179:437-449.
15. Doucas V., Ishov A.M., Romo A., Juguilon H., Weitzman M.D., Evans R.M., Maul G.G. Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev. 1996, 10:196-207.
16. Eulalio A., Behm-Ansmant I., Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 2007, 8:9-22.
17. Evans J.D., Hearing P. Distinct roles of the Adenovirus E4 ORF3 protein in viral DNA replication and inhibition of genome concatenation. J. Virol. 2003, 77:5295-5304.
18. Evans J.D., Hearing P. Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol. 2005, 79:6207-6215.
19. Garcia-Mata R., Gao Y.S., Sztul E. Hassles with taking out the garbage: aggravating aggresomes. Traffic 2002, 3:388-396.
20. Halbert D.N., Cutt J.R., Shenk T. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J. Virol. 1985, 56:250-257.
21. Huang M.M., Hearing P. Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. J. Virol. 1989, 63:2605-2615.
22. Johnston J.A., Ward C.L., Kopito R.R. Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 1998, 143:1883-1898.
23. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000, 10:524-530.
24. Linder P. Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res. 2006, 34:4168-4180.
25. Liu Y., Shevchenko A., Berk A.J. Adenovirus exploits the cellular aggresome response to accelerate inactivation of the MRN complex. J. Virol. 2005, 79:14004-14016.
26. Medghalchi S., Padmanabhan R., Ketner G. Early region 4 modulates adenovirus DNA replication by two genetically separable mechanisms. Virology 1997, 236:8-17.
27. Minshall N., Kress M., Weil D., Standart N. Role of p54 RNA helicase activity and its C-terminal domain in translational repression, P-body localization and assembly. Mol. Biol. Cell 2009, 20:2464-2472.
28. Mittereder N., March K.L., Trapnell B.C. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J. Virol. 1996, 70:7498-7509.
29. Ohman K., Nordqvist K., Akusjarvi G. Two adenovirus proteins with redundant activities in virus growth facilitates tripartite leader mRNA accumulation. Virology 1993, 194:50-58.
30. Querido E., Blanchette P., Yan Q., Kamura T., Morrison M., Boivin D., Kaelin W.G., Conaway R.C., Conaway J.W., Branton P.E. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 2001, 15:3104-3117.
31. Rocak S., Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 2004, 5:232-241.
32. Sandler A.B., Ketner G. Adenovirus early region 4 is essential for normal stability of late nuclear RNAs. J. Virol. 1989, 63:624-630.
33. Song C., Xiao Z., Nagashima K., Li C.C., Lockett S.J., Dai R.M., Cho E.H., Conrads T.P., Veenstra T.D., Colburn N.H., Wang Q., Wang J.M. The heavy metal cadmium induces valosin-containing protein (VCP)-mediated aggresome formation. Toxicol. Appl. Pharmacol. 2008, 228:351-363.
34. Stoecklin G., Mayo T., Anderson P. ARE-mRNA degradation requires the 5'-3' decay pathway. EMBO Rep. 2006, 7:72-77.
35. Stracker T.H., Carson C.T., Weitzman M.D. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 2002, 418:348-352.
36. Stracker T.H., Lee D.V., Carson C.T., Araujo F.D., Ornelles D.A., Weitzman M.D. Serotype-specific reorganization of the Mre11 complex by adenoviral E4orf3 proteins. J. Virol. 2005, 79:6664-6673.
37. Tauber B., Dobner T. Molecular regulation and biological function of adenovirus early genes: the E4 ORFs. Gene 2001, 278:1-23.
38. Ullman A.J., Hearing P. Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. J. Virol. 2008, 82:7325-7335.
39. Ullman A.J., Reich N.C., Hearing P. Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. J. Virol. 2007, 81:4744-4752.
40. Weiden M.D., Ginsberg H.S. Deletion of the E4 region of the genome produces adenovirus DNA concatemers. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:153-157.
41. Weitzman M.D., Ornelles D.A. Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 2005, 24:7686-7696.
42. Weston A., Sommerville J. Xp54 and related (DDX6-like) RNA helicases: roles in messenger RNP assembly, translation regulation and RNA degradation. Nucleic Acids Res. 2006, 34:3082-3094.
43. Wileman T. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design?. Annu. Rev. Microbiol. 2007, 61:149-167.
44. Yondola M.A., Hearing P. The adenovirus E4 ORF3 protein binds and reorganizes the TRIM family member transcriptional intermediary factor 1 alpha. J. Virol. 2007, 81:4264-4271.
45. Zantema A., Fransen J.A., Davis-Olivier A., Ramaekers F.C., Vooijs G.P., DeLeys B., Van der Eb A.J. Localization of the E1B proteins of adenovirus 5 in transformed cells, as revealed by interaction with monoclonal antibodies. Virology 1985, 142:44-58.