Biophysical and functional analyses suggest that adenovirus E4-ORF3 protein requires higher-order multimerization to function against promyelocytic leukemia protein nuclear bodies

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22573-22583

  Patsalo, Vadim ^b   Yondola, Mark A ^a,c   Luan, Bowu ^a   Shoshani, Ilana ^a   Kisker, Caroline ^a,d   Green, David F ^b   Raleigh, Daniel P ^a   Hearing, Patrick ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b Stony Brook University   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRAL ACTIVITIES; BIOPHYSICAL ANALYSIS; CO-IMMUNOPRECIPITATIONS; COEXPRESSED; GENE PRODUCTS; HIGHER ORDER; HUMAN ADENOVIRUS; IN-VITRO; MAMMALIAN CELLS; MULTIMERIZATION; MULTIMERS; MUTANT PROTEINS; NUCLEAR BODIES; OPEN READING FRAME; PROMYELOCYTIC LEUKEMIA PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SECONDARY STRUCTURES; UNIPROT;

AMINO ACIDS; BIOCHEMISTRY; ESCHERICHIA COLI; GENES;

PROTEINS;

EARLY REGION 4 OPEN READING FRAME 3 PROTEIN; MUTANT PROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CIRCULAR DICHROISM; CONTROLLED STUDY; DIMERIZATION; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; IMMUNOPRECIPITATION; IONIC STRENGTH; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ADENOVIRUS E4 PROTEINS; BIOPHYSICS; CELL NUCLEUS; DIMERIZATION; HELA CELLS; HOST-PARASITE INTERACTIONS; HUMANS; MULTIPROTEIN COMPLEXES; MUTAGENESIS; NUCLEAR PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

ADENOVIRIDAE; ESCHERICHIA COLI; HUMAN ADENOVIRUS; MAMMALIA;

EID: 84863308262     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.344234     Document Type: Article

References (47)

1. Geoffroy, M. C., and Chelbi-Alix, M. K. (2011) Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 31, 145-158
2. Everett, R. D., and Chelbi-Alix, M. K. (2007) PML and PML nuclear bodies: Implications in antiviral defense. Biochimie 89, 819-830 (Pubitemid 47008945)
3. Doucas, V., Ishov, A. M., Romo, A., Juguilon, H., Weitzman, M. D., Evans, R. M., and Maul, G. G. (1996) Adenovirus replication is coupled with the dynamic properties of thePMLnuclear structure. Genes Dev. 10, 196-207 (Pubitemid 26044607)
4. Ullman, A. J., and Hearing, P. (2008) Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. J. Virol. 82, 7325-7335 (Pubitemid 352031201)
5. Ullman, A. J., Reich, N. C., and Hearing, P. (2007) Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. J. Virol. 81, 4744-4752 (Pubitemid 46668671)
6. Forrester, N. A., Patel, R. N., Speiseder, T., Groitl, P., Sedgwick, G. G., Shimwell, N. J., Seed, R. I., Catnaigh, P. Ó., McCabe, C. J., Stewart, G. S., Dobner, T., Grand, R. J., Martin, A., and Turnell, A. S. (2012) Adenovirus E4orf3 targets transcriptional intermediary factor 1γ for proteasome-dependent degradation during infection. J. Virol. 86, 3167-3179
7. Vink, E. I., Yondola, M. A., Wu, K., and Hearing, P. (2012) Adenovirus E4-ORF3-dependent relocalization of TIF1α and TIF1γ relies on access to the coiled-coil motif. Virology 422, 317-325
8. Yondola, M. A., and Hearing, P. (2007) The adenovirus E4 ORF3 protein binds and reorganizes the TRIM family member transcriptional intermediary factor 1 β. J. Virol. 81, 4264-4271 (Pubitemid 46586920)
9. Carvalho, T., Seeler, J. S., Ohman, K., Jordan, P., Pettersson, U., Akusjärvi, G., Carmo-Fonseca, M., and Dejean, A. (1995) Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. J. Cell Biol. 131, 45-56
10. Leppard, K. N., and Everett, R. D. (1999) The adenovirus type 5 E1b 55K and E4 Orf3 proteins associate in infected cells and affect ND10 components. J. Gen. Virol. 80, 997-1008 (Pubitemid 29179061)
11. Lethbridge, K. J., Scott, G. E., and Leppard, K. N. (2003) Nuclear matrix localization and SUMO-1 modification of adenovirus type 5 E1b 55K protein are controlled by E4 Orf6 protein. J. Gen. Virol. 84, 259-268 (Pubitemid 36175698)
12. Weitzman, M. D., Lilley, C. E., and Chaurushiya, M. S. (2010) Genomes in conflict: Maintaining genome integrity during virus infection. Annu. Rev. Microbiol. 64, 61-81
13. Weitzman, M. D., and Ornelles, D. A. (2005) Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 24, 7686-7696 (Pubitemid 41670671)
14. Karen, K. A., Hoey, P. J., Young, C. S., and Hearing, P. (2009) Temporal regulation of the Mre11-Rad50-Nbs1 complex during adenovirus infection. J. Virol. 83, 4565-4573
15. Weiden, M. D., and Ginsberg, H. S. (1994) Deletion of the E4 region of the genome produces adenovirus DNA concatemers. Proc. Natl. Acad. Sci. U.S.A. 91, 153-157 (Pubitemid 24018661)
16. Barber, G. N. (2011) Innate immune DNA sensing pathways: STING, AIMII, and the regulation of interferon production and inflammatory responses. Curr. Opin. Immunol. 23, 10-20
17. Evans, J. D., and Hearing, P. (2005) Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol. 79, 6207-6215 (Pubitemid 40617225)
18. Stracker, T. H., Carson, C. T., and Weitzman, M. D. (2002) Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418, 348-352 (Pubitemid 34790688)
19. Lakdawala, S. S., Schwartz, R. A., Ferenchak, K., Carson, C. T., McSharry, B. P., Wilkinson, G. W., and Weitzman, M. D. (2008) Differential requirements of the C terminus of Nbs1 in suppressing adenovirus DNA replication and promoting concatemer formation. J. Virol. 82, 8362-8372
20. Mathew, S. S., and Bridge, E. (2007) The cellular Mre11 protein interferes with adenovirus E4 mutant DNA replication. Virology 365, 346-355 (Pubitemid 47223307)
21. Mathew, S. S., and Bridge, E. (2008) Nbs1-dependent binding of Mre11 to adenovirus E4 mutant viral DNA is important for inhibiting DNA replication. Virology 374, 11-22
22. Harada, J. N., Shevchenko, A., Shevchenko, A., Pallas, D. C., and Berk, A. J. (2002) Analysis of the adenovirus E1B-55K-anchored proteome reveals its link to ubiquitination machinery. J. Virol. 76, 9194-9206 (Pubitemid 34919878)
23. Querido, E., Blanchette, P., Yan, Q., Kamura, T., Morrison, M., Boivin, D., Kaelin, W. G., Conaway, R. C., Conaway, J. W., and Branton, P. E. (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 (Pubitemid 33115675)
24. Baker, A., Rohleder, K. J., Hanakahi, L. A., and Ketner, G. (2007) Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 81, 7034-7040 (Pubitemid 46986639)
25. Orazio, N. I., Naeger, C. M., Karlseder, J., and Weitzman, M. D. (2011) The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J. Virol. 85, 1887-1892
26. Araujo, F. D., Stracker, T. H., Carson, C. T., Lee, D. V., and Weitzman, M. D. (2005) Adenovirus type 5 E4orf3 protein targets the Mre11 complex to cytoplasmic aggresomes. J. Virol. 79, 11382-11391 (Pubitemid 41170679)
27. Liu, Y., Shevchenko, A., Shevchenko, A., and Berk, A. J. (2005) Adenovirus exploits the cellular aggresome response to accelerate inactivation of the MRN complex. J. Virol. 79, 14004-14016 (Pubitemid 41552699)
28. Soria, C., Estermann, F. E., Espantman, K. C., and O'Shea, C. C. (2010) Heterochromatin silencing of p53 target genes by a small viral protein. Nature 466, 1076-1081
29. Blanchette, P., Kindsmüller, K., Groitl, P., Dallaire, F., Speiseder, T., Branton, P. E., and Dobner, T. (2008) Control of mRNA export by adenovirus E4orf6 and E1B55K proteins during productive infection requires E4orf6 ubiquitin ligase activity. J. Virol. 82, 2642-2651 (Pubitemid 351329155)
30. Gonzalez, R., Huang, W., Finnen, R., Bragg, C., and Flint, S. J. (2006) Adenovirus E1B 55-kilodalton protein is required for both regulation of mRNAexport and efficient entry into the late phase of infection in normal human fibroblasts. J. Virol. 80, 964-974 (Pubitemid 43062908)
31. Goodrum, F. D., and Ornelles, D. A. (1999) Roles for the E4 orf6, orf3, and E1B 55-kilodalton proteins in cell cycle-independent adenovirus replication. J. Virol. 73, 7474-7488 (Pubitemid 29383231)
32. Nordqvist, K., Ohman, K., and Akusjärvi, G. (1994) Human adenovirus encodes two proteins, which have opposite effects on accumulation of alternatively spliced mRNAs. Mol. Cell. Biol. 14, 437-445
33. Ohman, K., Nordqvist, K., and Akusjärvi, G. (1993) Two adenovirus proteins with redundant activities in virus growth facilitates tripartite leader mRNA accumulation. Virology 194, 50-58
34. Sandler, A. B., and Ketner, G. (1989) Adenovirus early region 4 is essential for normal stability of late nuclear RNAs. J. Virol. 63, 624-630 (Pubitemid 19057227)
35. Shepard, R. N., and Ornelles, D. A. (2003) E4orf3 is necessary for enhanced S-phase replication of cell cycle-restricted subgroup C adenoviruses. J. Virol. 77, 8593-8595 (Pubitemid 36871490)
36. Shepard, R. N., and Ornelles, D. A. (2004) Diverse roles for E4orf3 at late times of infection revealed in an E1B 55-kilodalton protein mutant background. J. Virol. 78, 9924-9935 (Pubitemid 39187111)
37. Woo, J. L., and Berk, A. J. (2007) Adenovirus ubiquitin-protein ligase stimulates viral late mRNA nuclear export. J. Virol. 81, 575-587 (Pubitemid 46067885)
38. Schiedner, G., Hertel, S., and Kochanek, S. (2000) Efficient transformation of primary human amniocytes by E1 functions of Ad5: Generation of new cell lines for adenoviral vector production. Hum. Gene Ther. 11, 2105-2116
39. Liao, D., Yu, A., and Weiner, A. M. (1999) Coexpression of the adenovirus 12 E1B 55 kDa oncoprotein and cellular tumor suppressor p53 is sufficient to induce metaphase fragility of the human RNU2 locus. Virology 254, 11-23 (Pubitemid 29391710)
40. Nevels, M., Täuber, B., Kremmer, E., Spruss, T., Wolf, H., and Dobner, T. (1999) Transforming potential of the adenovirus type 5 E4orf3 protein. J. Virol. 73, 1591-1600 (Pubitemid 29036815)
41. Evans, J. D., and Hearing, P. (2003) Distinct roles of the adenovirus E4 ORF3 protein in viral DNA replication and inhibition of genome concatenation. J. Virol. 77, 5295-5304 (Pubitemid 36460943)
42. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS a Windows-PC based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
43. Guinier, A., and Fournet, G. (1955) Small-angle X-ray Scattering, John Wiley and Sons, Inc., New York
44. Gualfetti, P. J., Iwakura, M., Lee, J. C., Kihara, H., Bilsel, O., Zitzewitz, J. A., and Matthews, C. R. (1999) Apparent radii of the native, stable intermediates and unfolded conformers of the β-subunit of tryptophan synthase from Escherichia coli, a TIM barrel protein. Biochemistry 38, 13367-13378
45. Koide, S., Bu, Z., Risal, D., Pham, T. N., Nakagawa, T., Tamura, A., and Engelman, D. M. (1999) Multistep denaturation of Borrelia burgdorferi OspA, a protein containing a single-layer β-sheet. Biochemistry 38, 4757-4767
46. Kohn, J. E., Millett, I. S., Jacob, J., Zagrovic, B., Dillon, T. M., Cingel, N., Dothager, R. S., Seifert, S., Thiyagarajan, P., Sosnick, T. R., Hasan, M. Z., Pande, V. S., Ruczinski, I., Doniach, S., and Plaxco, K. W. (2004) Random coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 12491-12496 (Pubitemid 39122051)
47. Skolnick, J., Kolinski, A., and Ortiz, A. R. (1997) MONSSTER: A method for folding globular proteins with a small number of distance restraints. J. Mol. Biol. 265, 217-241 (Pubitemid 27110659)