Impact of adenovirus e4-orf3 oligomerization and protein localization on cellular gene expression

Viruses

Volumn 7, Issue 5, 2015, Pages 2428-2449

  Vink, Elizabeth I ^a,d   Zheng, Yueting ^a   Yeasmin, Rukhsana ^b   Stamminger, Thomas ^c   Krug, Laurie T ^a   Hearing, Patrick ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b Stony Brook University   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adenovirus; Cellular gene expression; E4 ORF3; Transcription

Indexed keywords

COMPLEMENTARY DNA; DAXX PROTEIN; DOXYCYCLINE; PROTEIN; TRIPARTITE MOTIF CONTAINING 33; UNCLASSIFIED DRUG; VIRUS PROTEIN; E4ORF3 PROTEIN, ADENOVIRUS; VIRAL PROTEIN;

ADENOVIRIDAE; ARTICLE; CONTROLLED STUDY; DAXX GENE; GENE; GENE EXPRESSION; GENE ONTOLOGY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NONHUMAN; OLIGOMERIZATION; PROTEIN LOCALIZATION; PROTEIN MICROARRAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TRIM33 GENE; WESTERN BLOTTING; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; IMMUNE EVASION; METABOLISM; MICROARRAY ANALYSIS; PHYSIOLOGY; PROTEIN MULTIMERIZATION;

ADENOVIRIDAE;

ADENOVIRIDAE; ADENOVIRUS E4 PROTEINS; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; MICROARRAY ANALYSIS; PROTEIN MULTIMERIZATION;

EID: 84929353513     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7052428     Document Type: Article

References (55)

1. Bridge, E.; Ketner, G. Redundant control of adenovirus late gene expression by early region 4. J. Virol. 1989, 63, 631-638
2. 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
3. Sandler, A.B.; Ketner, G. Adenovirus early region 4 is essential for normal stability of late nuclear RNAs. J. Virol. 1989, 63, 624-630
4. Cheng, C.Y.; Blanchette, P.; Branton, P.E. The adenovirus E4orf6 E3 ubiquitin ligase complex assembles in a novel fashion. Virology 2007, 364, 36-44
5. Cheng, C.Y.; Gilson, T.; Dallaire, F.; Ketner, G.; Branton, P.E.; Blanchette, P. The E4orf6/E1B55K E3 ubiquitin ligase complexes of human adenoviruses exhibit heterogeneity in composition and substrate specificity. J. Virol. 2011, 55, 765-775
6. Harada, J.N.; Shevchenko, A.; Pallas, D.C.; Berk, A.J. Analysis of the adenovirus E1B-55K-anchored proteome reveals its link to ubiquitination machinery. J. Virol. 2002, 76, 9194-9206
7. 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, 75, 3104-3117
8. Stracker, T.H.; Carson, C.T.; Weitzman, M.D. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 2002, 475, 348-352
9. 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, 57, 7034-7040
10. Dallaire, F.; Blanchette, P.; Groitl, P.; Dobner, T.; Branton, P.E. Identification of integrin alpha3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex. J. Virol. 2009, 53, 5329-5338
11. Orazio, N.I.; Naeger, C.M.; Karlseder, J.; Weitzman, M.D. The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J. Virol. 2011, 55, 1887-1892
12. 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, 70, 196-207
13. Ou, H.D.; Kwiatkowski, W.; Deerinck, T.J.; Noske, A.; Blain, K.Y.; Land, H.S.; Soria, C.; Powers, C.J.; May, A.P.; Shu, X.; et al. A structural basis for the assembly and functions of a viral polymer that inactivates multiple tumor suppressors. Cell 2012, 757, 304-319
14. Patsalo, V.; Yondola, M.A.; Luan, B.; Shoshani, I.; Kisker, C.; Green, D.F.; Raleigh, D.P.; Hearing, P. Biophysical and functional analyses suggest that adenovirus E4-ORF3 protein requires higher-order multimerization to function against promyelocytic leukemia protein nuclear bodies. J. Biol. Chem. 2012, 257, 22573-22583
15. Weitzman, M.D.; Ornelles, D.A. Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 2005, 24, 7686-7696
16. Sohn, S.Y.; Hearing, P. Adenovirus regulates sumoylation of Mre11-Rad50-Nbs1 components through a paralog-specific mechanism. J. Virol. 2012, 56, 9656-9665
17. 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
18. Soria, C.; Estermann, F.E.; Espantman, K.C.; O'Shea, C.C. Heterochromatin silencing of p53 target genes by a small viral protein. Nature 2010, 466, 1076-1081
19. Vink, E.I.; Yondola, M.A.; Wu, K.; Hearing, P. Adenovirus E4-ORF3-dependent relocalization of TIF1alpha and TIF1gamma relies on access to the Coiled-Coil motif. Virology 2012, 422, 317-325
20. 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, 57, 4264-4271
21. 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, 52, 7325-7335
22. Ullman, A.J.; Reich, N.C.; Hearing, P. Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. J. Virol. 2007, 57, 4744-4752
23. Karen, K.A.; Hoey, P.J.; Young, C.S.; Hearing, P. Temporal regulation of the Mre11-Rad50-Nbs1 complex during adenovirus infection. J. Virol. 2009, 53, 4565-4573
24. Weiden, M.D.; Ginsberg, H.S. Deletion of the E4 region of the genome produces adenovirus DNA concatemers. Proc. Natl. Acad. Sci. USA 1994, 97, 153-157
25. Lakdawala, S.S.; Schwartz, R.A.; Ferenchak, K.; Carson, C.T.; McSharry, B.P.; Wilkinson, G.W.; Weitzman, M.D. Differential requirements of the C terminus of Nbs1 in suppressing adenovirus DNA replication and promoting concatemer formation. J. Virol. 2008, 52, 8362-8372
26. 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
27. Mathew, S.S.; Bridge, E. Nbs1-dependent binding of Mre11 to adenovirus E4 mutant viral DNA is important for inhibiting DNA replication. Virology 2008, 374, 11-22
28. Geoffroy, M.C.; Chelbi-Alix, M.K. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 2011, 37, 145-158
29. Van Damme, E.; Laukens, K.; Dang, T.H.; van Ostade, X. A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. Int. J. Biol. Sci. 2010, 6, 51-67
30. Cammas, F.; Khetchoumian, K.; Chambon, P.; Losson, R. TRIM involvement in transcriptional regulation. Adv. Exp. Med. Biol. 2012, 770, 59-76
31. Ikeda, K.; Inoue, S. TRIM proteins as RING finger E3 ubiquitin ligases. Adv. Exp. Med. Biol. 2012, 770, 27-37
32. Napolitano, L.M.; Meroni, G. TRIM family: Pleiotropy and diversification through homomultimer and heteromultimer formation. IUBMB Life 2012, 64, 64-71
33. Allton, K.; Jain, A.K.; Herz, H.M.; Tsai, W.W.; Jung, S.Y.; Qin, J.; Bergmann, A.; Johnson, R.L.; Barton, M.C. Trim24 targets endogenous p53 for degradation. Proc. Natl. Acad. Sci. USA 2009, 706, 11612-11616
34. Dupont, S.; Zacchigna, L.; Cordenonsi, M.; Soligo, S.; Adorno, M.; Rugge, M.; Piccolo, S. Germ-layer specification and control of cell growth by Ectodermin, a Smad4 ubiquitin ligase. Cell 2005, 727, 87-99
35. Ikeuchi, Y.; Dadakhujaev, S.; Chandhoke, A.S.; Huynh, M.A.; Oldenborg, A.; Ikeuchi, M.; Deng, L.; Bennett, E.J.; Harper, J.W.; Bonni, A.; Bonni, S. TIF1gamma protein regulates epithelial-mesenchymal transition by operating as a small ubiquitin-like modifier (SUMO) E3 ligase for the transcriptional regulator SnoN1. J. Biol. Chem. 2014, 259, 25067-25078
36. Khetchoumian, K.; Teletin, M.; Tisserand, J.; Mark, M.; Herquel, B.; Ignat, M.; Zucman-Rossi, J.; Cammas, F.; Lerouge, T.; Thibault, C.; Metzger, D.; Chambon, P.; Losson, R. Loss of Trim24 (Tif1alpha) gene function confers oncogenic activity to retinoic acid receptor alpha. Nat. Genet. 2007, 39, 1500-1506
37. Tsai, W.W.; Wang, Z.; Yiu, T.T.; Akdemir, K.C.; Xia, W.; Winter, S.; Tsai, C.Y.; Shi, X.; Schwarzer, D.; Plunkett, W.; et al. TRIM24 links a non-canonical histone signature to breast cancer. Nature 2010, 465, 927-932
38. Zhong, S.; Delva, L.; Rachez, C.; Cenciarelli, C.; Gandini, D.; Zhang, H.; Kalantry, S.; Freedman, L.P.; Pandolfi, P.P. A RA-dependent, tumour-growth suppressive transcription complex is the target of the PML-RARalpha and T18 oncoproteins. Nat. Genet. 1999, 23, 287-295
39. He, W.; Dorn, D.C.; Erdjument-Bromage, H.; Tempst, P.; Moore, M.A.; Massague, J. Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell 2006, 725, 929-941
40. Agricola, E.; Randall, R.A.; Gaarenstroom, T.; Dupont, S.; Hill, C.S. Recruitment of TIF1gamma to chromatin via its PHD finger-bromodomain activates its ubiquitin ligase and transcriptional repressor activities. Mol. Cell 2011, 43, 85-96
41. Xi, Q.; Wang, Z.; Zaromytidou, A.I.; Zhang, X.H.; Chow-Tsang, L.F.; Liu, J.X.; Kim, H.; Barlas, A.; Manova-Todorova, K.; Kaartinen, V.; et al. A poised chromatin platform for TGF-beta access to master regulators. Cell 2011, 747, 1511-1524
42. Nevels, M.; Tauber, B.; Kremmer, E.; Spruss, T.; Wolf, H.; Dobner, T. Transforming potential of the adenovirus type 5 E4orf3 protein. J. Virol. 1999, 73, 1591-1600
43. Smyth, G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3, 1-25
44. Smyth, G.K.; Speed, T. Normalization of cDNA microarray data. Methods 2003, 37, 265-273
45. de Hoon, M.J.; Imoto, S.; Nolan, J.; Miyano, S. Open source clustering software. Bioinformatics 2004, 20, 1453-1454
46. Saldanha, A.J. Java Treeview—Extensible visualization of microarray data. Bioinformatics 2004, 20, 3246-3248
47. Huang da, W.; Sherman, B.T.; Lempicki, R.A. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucl. Acids Res. 2009, 37, 1-13
48. Huang da, W.; Sherman, B.T.; Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4, 44-57
49. Cui, W.; Taub, D.D.; Gardner, K. qPrimerDepot: A primer database for quantitative real time PCR. Nucl. Acids Res. 2007, 35, D805-D809
50. Lefever, S.; Vandesompele, J.; Speleman, F.; Pattyn, F. RTPrimerDB: The portal for real-time PCR primers and probes. Nucl. Acids Res. 2009, 37 Suppl. 7, D942-D945
51. Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 2001, 29, e45
52. Tavalai, N.; Papior, P.; Rechter, S.; Leis, M.; Stamminger, T. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 2006, 50, 8006-8018
53. Salomoni, P. The PML-Interacting Protein DAXX: Histone Loading Gets into the Picture. Front. Oncol. 2013, 3, e152
54. Lowe, S.W.; Ruley, H.E. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 1993, 7, 535-545
55. Debbas, M.; White, E. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 1993, 7, 546-554