Nuclear translocation and regulation of intranuclear distribution of cytoplasmic poly(A)-binding protein are distinct processes mediated by two Epstein Barr virus proteins

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Park, Richard ^a   El Guindy, Ayman ^a   Heston, Lee ^a   Lin, Su Fang ^b   Yu, Kuan Ping ^a   Nagy, Mate ^c   Borah, Sumit ^d   Delecluse, Henri Jacques ^e   Steitz, Joan ^a   Miller, George ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c YALE UNIVERSITY   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; BGLF5 PROTEIN; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; IMMEDIATE EARLY PROTEIN BZLF1; UNCLASSIFIED DRUG; VIRUS PROTEIN; BZLF1 PROTEIN, HERPESVIRUS 4, HUMAN; DEOXYRIBONUCLEASE; DEOXYRIBONUCLEASE, EPSTEIN-BARR VIRUS; POLYADENYLIC ACID BINDING PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; BGLF5 GENE; BZLF1 GENE; CELL NUCLEUS; CLICK CHEMISTRY; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EMBRYO; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS REPLICATION; ZEBRA GENE; ACTIVE TRANSPORT; CELL CULTURE; EPSTEIN BARR VIRUS INFECTION; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; TISSUE DISTRIBUTION; VIROLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; CELLS, CULTURED; DEOXYRIBONUCLEASES; EPSTEIN-BARR VIRUS INFECTIONS; HEK293 CELLS; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; POLY(A)-BINDING PROTEIN I; TISSUE DISTRIBUTION; TRANS-ACTIVATORS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84899427928     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092593     Document Type: Article

References (53)

1. Aranda M, Maule A (1998) Virus-induced host gene shutoff in animals and plants. Virology 243: 261-267. (Pubitemid 28384142)
2. Joachims M, Van Breugel PC, Lloyd RE (1999) Cleavage of poly(A)-binding protein by enterovirus proteases concurrent with inhibition of translation in vitro. J Virol 73: 718-727. (Pubitemid 28565417)
3. Kuyumcu-Martinez NM, Joachims M, Lloyd RE (2002) Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease. J Virol 76: 2062-2074. (Pubitemid 34150674)
4. Kuyumcu-Martinez NM, Van Eden ME, Younan P, Lloyd RE (2004) Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol Cell Biol 24: 1779-1790. (Pubitemid 38167098)
5. Alvarez E, Castello A, Menendez-Arias L, Carrasco L (2006) HIV protease cleaves poly(A)-binding protein. Biochem J 396: 219-226. (Pubitemid 43837237)
6. Piron M, Vende P, Cohen J, Poncet D (1998) Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J 17: 5811-5821. (Pubitemid 28445992)
7. Piron M, Delaunay T, Grosclaude J, Poncet D (1999) Identification of the RNA-binding, dimerization, and eIF4GI-binding domains of rotavirus nonstructural protein NSP3. J Virol 73: 5411-5421. (Pubitemid 29274823)
8. Vitour D, Lindenbaum P, Vende P, Becker MM, Poncet D (2004) RoXaN, a novel cellular protein containing TPR, LD, and zinc finger motifs, forms a ternary complex with eukaryotic initiation factor 4G and rotavirus NSP3. J Virol 78: 3851-3862. (Pubitemid 38437191)
9. Harb M, Becker MM, Vitour D, Baron CH, Vende P, et al. (2008) Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J Virol 82: 11283-11293.
10. Zhu H, Cong JP, Mamtora G, Gingeras T, Shenk T (1998) Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 14470-14475. (Pubitemid 28549391)
11. Kwong AD, Frenkel N (1987) Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc Natl Acad Sci U S A 84: 1926-1930. (Pubitemid 17054122)
12. Kumar GR, Glaunsinger BA (2010) Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Mol Cell Biol 30: 4996-5008.
13. Dobrikova E, Shveygert M, Walters R, Gromeier M (2010) Herpes simplex virus proteins ICP27 and UL47 associate with polyadenylate-binding protein and control its subcellular distribution. J Virol 84: 270-279.
14. Salaun C, MacDonald AI, Larralde O, Howard L, Lochtie K, et al. (2010) Poly(A)-binding protein 1 partially relocalizes to the nucleus during herpes simplex virus type 1 infection in an ICP27-independent manner and does not inhibit virus replication. J Virol 84: 8539-8548.
15. Glaunsinger B, Ganem D (2004) Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol Cell 13: 713-723. (Pubitemid 38368128)
16. Covarrubias S, Richner JM, Clyde K, Lee YJ, Glaunsinger BA (2009) Host Shutoff is a Conserved Phenotype of Gammaherpesvirus Infection and is Orchestrated Exclusively from the Cytoplasm. J Virol 83: 9554-9566.
17. Covarrubias S, Gaglia MM, Kumar GR, Wong W, Jackson AO, et al. (2011) Coordinated destruction of cellular messages in translation complexes by the gammaherpesvirus host shutoff factor and the mammalian exonuclease Xrn1. PLoS Pathog 7: e1002339.
18. Rowe M, Glaunsinger B, van Leeuwen D, Zuo J, Sweetman D, et al. (2007) Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc Natl Acad Sci U S A 104: 3366-3371. (Pubitemid 46364165)
19. Gaglia MM, Covarrubias S, Wong W, Glaunsinger BA (2012) A common strategy for host RNA degradation by divergent viruses. J Virol.
20. Horst D, Burmeister WP, Boer IG, van Leeuwen D, Buisson M, et al. (2012) The "Bridge" in the Epstein-Barr virus alkaline exonuclease protein BGLF5 contributes to shutoff activity during productive infection. J Virol 86: 9175-9187.
21. Delecluse HJ, Hilsendegen T, Pich D, Zeidler R, Hammerschmidt W (1998) Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc Natl Acad Sci U S A 95: 8245-8250. (Pubitemid 28326098)
22. Feederle R, Kost M, Baumann M, Janz A, Drouet E, et al. (2000) The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. Embo J 19: 3080-3089. (Pubitemid 30386778)
23. Feederle R, Bannert H, Lips H, Muller-Lantzsch N, Delecluse HJ (2009) The Epstein-Barr virus alkaline exonuclease BGLF5 serves pleiotropic functions in virus replication. J Virol 83: 4952-4962.
24. Park R, Heston L, Shedd D, Delecluse HJ, Miller G (2008) Mutations of amino acids in the DNA-recognition domain of Epstein-Barr virus ZEBRA protein alter its sub-nuclear localization and affect formation of replication compartments. Virology 382: 145-162.
25. Daikoku T, Kudoh A, Fujita M, Sugaya Y, Isomura H, et al. (2005) Architecture of replication compartments formed during Epstein-Barr virus lytic replication. J Virol 79: 3409-3418. (Pubitemid 40327929)
26. Fu XD, Maniatis T (1990) Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343: 437-441.
27. Ruvolo V, Gupta AK, Swaminathan S (2001) Epstein-Barr virus SM protein interacts with mRNA in vivo and mediates a gene-specific increase in cytoplasmic mRNA. J Virol 75: 6033-6041. (Pubitemid 32553134)
28. Gruffat H, Batisse J, Pich D, Neuhierl B, Manet E, et al. (2002) Epstein-Barr virus mRNA export factor EB2 is essential for production of infectious virus. J Virol 76: 9635-9644. (Pubitemid 35006504)
29. Francis A, Ragoczy T, Gradoville L, Heston L, El-Guindy A, et al. (1999) Amino acid substitutions reveal distinct functions of serine 186 of the ZEBRA protein in activation of early lytic cycle genes and synergy with the Epstein-Barr virus R transactivator. J Virol 73: 4543-4551. (Pubitemid 29246711)
30. Heston L, El-Guindy A, Countryman J, Dela Cruz C, Delecluse HJ, et al. (2006) Amino acids in the basic domain of Epstein-Barr virus ZEBRA protein play distinct roles in DNA binding, activation of early lytic gene expression, and promotion of viral DNA replication. J Virol 80: 9115-9133. (Pubitemid 44359985)
31. Francis AL, Gradoville L, Miller G (1997) Alteration of a single serine in the basic domain of the Epstein-Barr virus ZEBRA protein separates its functions of transcriptional activation and disruption of latency. J Virol 71: 3054-3061. (Pubitemid 27119950)
32. Bhende PM, Seaman WT, Delecluse HJ, Kenney SC (2005) BZLF1 activation of the methylated form of the BRLF1 immediate-early promoter is regulated by BZLF1 residue 186. J Virol 79: 7338-7348. (Pubitemid 40756769)
33. Park R, Wang'ondu R, Heston L, Shedd D, Miller G (2011) Efficient induction of nuclear aggresomes by specific single missense mutations in the DNA-binding domain of a viral AP-1 homolog. J Biol Chem 286: 9748-9762.
34. Rooney C, Taylor N, Countryman J, Jenson H, Kolman J, et al. (1988) Genome rearrangements activate the Epstein-Barr virus gene whose product disrupts latency. Proc Natl Acad Sci U S A 85: 9801-9805. (Pubitemid 19027213)
35. Schepers A, Pich D, Hammerschmidt W (1993) A transcription factor with homology to the AP-1 family links RNA transcription and DNA replication in the lytic cycle of Epstein-Barr virus. EMBO J 12: 3921-3929. (Pubitemid 23282768)
36. Oroskar AA, Read GS (1989) Control of mRNA stability by the virion host shutoff function of herpes simplex virus. J Virol 63: 1897-1906. (Pubitemid 19107783)
37. Sandri-Goldin RM (1998) ICP27 mediates HSV RNA export by shuttling through a leucine-rich nuclear export signal and binding viral intronless RNAs through an RGG motif. Genes Dev 12: 868-879.
38. Mears WE, Rice SA (1996) The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J Virol 70: 7445-7453. (Pubitemid 26339048)
39. Sokolowski M, Scott JE, Heaney RP, Patel AH, Clements JB (2003) Identification of herpes simplex virus RNAs that interact specifically with regulatory protein ICP27 in vivo. J Biol Chem 278: 33540-33549. (Pubitemid 37055808)
40. Bryant HE, Wadd SE, Lamond AI, Silverstein SJ, Clements JB (2001) Herpes simplex virus IE63 (ICP27) protein interacts with spliceosome-associated protein 145 and inhibits splicing prior to the first catalytic step. J Virol 75: 4376-4385. (Pubitemid 32410149)
41. Sciabica KS, Dai QJ, Sandri-Goldin RM (2003) ICP27 interacts with SRPK1 to mediate HSV splicing inhibition by altering SR protein phosphorylation. EMBO J 22: 1608-1619. (Pubitemid 36417409)
42. Sandri-Goldin RM, Hibbard MK, Hardwicke MA (1995) The C-terminal repressor region of herpes simplex virus type 1 ICP27 is required for the redistribution of small nuclear ribonucleoprotein particles and splicing factor SC35; however, these alterations are not sufficient to inhibit host cell splicing. J Virol 69: 6063-6076.
43. Phelan A, Carmo-Fonseca M, McLaughlan J, Lamond AI, Clements JB (1993) A herpes simplex virus type 1 immediate-early gene product, IE63, regulates small nuclear ribonucleoprotein distribution. Proc Natl Acad Sci U S A 90: 9056-9060. (Pubitemid 23306450)
44. Lin SF, Lin SW, Hsu TY, Liu MY, Chen JY, et al. (1994) Functional analysis of the amino terminus of Epstein-Barr virus deoxyribonuclease. Virology 199: 223-227.
45. Vende P, Piron M, Castagne N, Poncet D (2000) Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3' end. J Virol 74: 7064-7071. (Pubitemid 30470690)
46. Keryer-Bibens C, Legagneux V, Namanda-Vanderbeken A, Cosson B, Paillard L, et al. (2009) The rotaviral NSP3 protein stimulates translation of polyadenylated target mRNAs independently of its RNA-binding domain. Biochem Biophys Res Commun 390: 302-306.
47. Walsh D, Arias C, Perez C, Halladin D, Escandon M, et al. (2008) Eukaryotic translation initiation factor 4F architectural alterations accompany translation initiation factor redistribution in poxvirus-infected cells. Mol Cell Biol 28: 2648-2658. (Pubitemid 351542365)
48. Sugimoto A, Sato Y, Kanda T, Murata T, Narita Y, et al. (2013) Different distributions of Epstein-Barr virus early and late gene transcripts within viral replication compartments. J Virol 87: 6693-6699.
49. de-The G, Geser A, Day NE, Tukei PM, Williams EH, et al. (1978) Epidemiological evidence for causal relationship between Epstein-Barr virus and Burkitt's lymphoma from Ugandan prospective study. Nature 274: 756-761. (Pubitemid 8406152)
50. Zeng Y, Zhang LG, Wu YC, Huang YS, Huang NQ, et al. (1985) Prospective studies on nasopharyngeal carcinoma in Epstein-Barr virus IgA/VCA antibody-positive persons in Wuzhou City, China. Int J Cancer 36: 545-547. (Pubitemid 16233512)
51. Van der Eb AJ, Mulder C, Graham FL, Houweling A (1977) Transformation with specific fragments of adenovirus DNAs. I. Isolation of specific fragments with transforming activity of adenovirus 2 and 5 DNA. Gene 2: 115-132. (Pubitemid 9017110)
52. Old LJ, Boyse EA, Oettgen HF, Harven ED, Geering G, et al. (1966) Precipitating antibody in human serum to an antigen present in cultured burkitt's lymphoma cells. Proc Natl Acad Sci U S A 56: 1699-1704.
53. Pearson GR, Vroman B, Chase B, Sculley T, Hummel M, et al. (1983) Identification of polypeptide components of the Epstein-Barr virus early antigen complex with monoclonal antibodies. J Virol 47: 193-201. (Pubitemid 13107074)