The many roles of the highly interactive HSV protein ICP27, a key regulator of infection

Future Microbiology

Volumn 6, Issue 11, 2011, Pages 1261-1277

  Sandri Goldin, Rozanne M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gene regulation; Herpes virus; ICP27; mRNA export; Multifunctional regulator; Pre mRNA splicing; Protein interactions; RNA binding; Translation

Indexed keywords

MESSENGER RNA PRECURSOR; PROTEIN ICP27; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; CELL GROWTH; HERPES SIMPLEX; HERPES SIMPLEX VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REVIEW; RNA SPLICING; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

HUMANS; IMMEDIATE-EARLY PROTEINS; PROTEIN BINDING; RNA-BINDING PROTEINS; SIMPLEXVIRUS; VIRULENCE FACTORS;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; SIMPLEXVIRUS;

EID: 81255208061     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.11.119     Document Type: Review

References (173)

1. Sandri-Goldin RM. The many roles of the regulatory protein ICP27 during herpes simplex virus infection. Front. Biosci. 13, 5241-5256 (2008).
2. Zhi Y, Sandri-Goldin RM. Analysis of the phosphorylation sites of the herpes simplex virus type 1 regulatory protein ICP27. J. Virol. 73, 3246-3257 (1999). (Pubitemid 29135717)
3. Mears WE, Rice SA. 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 (1996). (Pubitemid 26339048)
4. Souki SK, Gershon PD, Sandri-Goldin RM. Arginine methylation of the ICP27 RGG box regulates ICP27 export and is required for efficient herpes simplex virus 1 replication. J. Virol. 83, 5309-5320 (2009).
5. Yu J, Shin B, Park ES et al. Protein arginine methyltransferase 1 regulates herpes simplex virus replication through ICP27 RGG-box methylation. Biochem. Biophys. Res. Comm. 391, 322-328 (2010).
6. Corbin-Lickfett K, Rojas S, Li L, Cocco MJ, Sandri-Goldin RM. ICP27 phosphorylation site mutants display altered functional interactions with cellular export factors Aly/REF and TAP/NXF1 but are able to bind herpes simplex virus 1 RNA. J. Virol. 84, 2212-2222 (2010).
7. Rojas S, Corbin-Lickfett K, Escudero-Paunetto L, Sandri-Goldin RM. ICP27 phosphorylation site mutants are defective in herpes simplex virus 1 replication and gene expression. J. Virol. 84, 2200-2211 (2010).
8. Corbin-Lickfett K, Souki SK, Cocco MJ, Sandri-Goldin RM. Three arginine residues within the RGG box are crucial for ICP27 binding to herpes simplex virus 1 GC-rich sequences and for efficient viral RNA export. J. Virol. 84, 6367-6376 (2010).
9. Souki SK , Sandri-Goldin RM. Arginine methylation of the ICP27 RGG box regulates the functional interactions of ICP27 with SRPK1 and Aly/REF during herpes simplex virus 1 infection. J. Virol. 83, 8970-8975 (2009).
10. Linberg A, Kreivi JP. Splicing inhibition at the level of spliceosome assembly in the presence of herpes simplex virus protein ICP27. Virology 294, 189-198 (2002).
11. Hardwicke MA, Sandri-Goldin RM. The herpes simplex virus regulatory protein ICP27 can cause a decrease in cellular mRNA levels during infection. J. Virol. 68, 4797-4810 (1994). (Pubitemid 24226544)
12. Hardy WR, Sandri-Goldin RM. Herpes simplex virus inhibits host cell splicing, and regulatory protein ICP27 is required for this effect. J. Virol. 68, 7790-7799 (1994). (Pubitemid 24362665)
13. Sciabica KS, Dai QJ, Sandri-Goldin RM. ICP27 interacts with SRPK1 to mediate HSV-1 inhibition of pre-mRNA splicing by altering SR protein phosphorylation. EMBO J. 22, 1608-1619 (2003). (Pubitemid 36417409)
14. Bryant HE, Wadd S, Lamond AI, Silverstein SJ, Clements JB. 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 (2001). (Pubitemid 32410149)
15. Dai-Ju JQ, Li L, Johnson LA, Sandri-Goldin RM. ICP27 interacts with the C-terminal domain of RNA polymerase II and facilitates its recruitment to herpes simplex virus-1 transcription sites, where it undergoes proteasomal degradation during infection. J. Virol. 80, 3567-3581 (2006).
16. Zhou C, Knipe DM. Association of herpes simplex virus 1 ICP8 and ICP27 with cellular RNA polymerase II holoenzyme. J. Virol. 76, 5893-5904 (2001).
17. Escudero-Paunetto L, Li L, Hernandez FP, Sandri-Goldin RM. SR proteins SRp20 and 9G8 contribute to efficient export of herpes simplex virus 1 mRNAs. Virology 401, 155-164 (2010).
18. Chen IB, Sciabica KS, Sandri-Goldin RM. ICP27 interacts with the export factor Aly/ REF to direct herpes simplex virus 1 intronless RNAs to the TAP export pathway. J. Virol. 76, 12877-12889 (2002). (Pubitemid 35386971)
19. Chen IB, Li L, Silva L, Sandri-Goldin RM. ICP27 recruits Aly/REF but not TAP/NXF1 to herpes simplex virus type 1 transcription sites although TAP/NXF1 is required for ICP27 export. J. Virol. 79, 3949-3961 (2005). (Pubitemid 40388335)
20. Koffa MD, Clements JB, Izaurralde E et al. Herpes simplex virus ICP27 protein provides viral mRNAs with access to the cellular mRNA export pathway. EMBO J. 20, 5769-5778 (2001). (Pubitemid 33010052)
21. Corbin-Lickfett K, Chen IB, Cocco MJ, Sandri-Goldin RM. The HSV-1 ICP27 RGG box specifically binds flexible, GC-rich sequences but not G-Quartet structures. Nucleic Acids Res. 37, 7290-7301 (2009).
22. Sandri-Goldin RM. ICP27 mediates herpes simplex virus 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 (1998). (Pubitemid 28150887)
23. Sokolowski M, Scott JE, Heaney RP, Patel AH, Clements JB. Identification of herpes simplex virus RNAs that interact specifically with regulatory protein ICP27 in vivo. J. Biol. Chem. 278, 33540-33549 (2003). (Pubitemid 37055808)
24. Hernandez FP, Sandri-Goldin RM. Head-to-tail intramolecular interaction of herpes simplex virus 1 regulatory protein ICP27 is important for its interaction with cellular mRNA export receptor TAP/NXF1. MBio 1(5), e00268-10 (2010).
25. Johnson LA, Sandri-Goldin RM. Efficient nuclear export of herpes simplex virus 1 transcripts requires both RNA binding by ICP27 and ICP27 interaction with TAP/ NXF1. J. Virol. 83, 1184-1192 (2009).
26. Johnson LA, Li L, Sandri-Goldin RM. The cellular RNA export receptor TAP/NXF1 is required for ICP27-mediated export of herpes simplex virus 1 RNA, whereas, the TREXcomplex adaptor protein Aly/REF appears to be dispensable. J. Virol. 83, 6335-6346 (2009).
27. Ellison KS, Maranchuk RA, Mottet KL, Smiley JR. Control of VP16 translation by the herpes simplex virus type 1 immediate-early protein ICP27. J. Virol. 79, 4120-4131 (2005). (Pubitemid 40388350)
28. Fontaine-Rodriquez EC, Taylor TJ, Olesky M, Knipe DM. Proteomics of herpes simplex virus infected cell protein 27: association with translation initiation factors. Virology 330, 487-492 (2004). (Pubitemid 39572854)
29. Fontaine-Rodriquez EC, Knipe DM. Herpes simplex virus ICP27 increases translation of a subset of viral late mRNAs. J. Virol. 82(7), 3538-3545 (2008). (Pubitemid 351429929)
30. Larralde O, Smith RW, Wilkie GS, Gray NK, Clements JB. Direct stimulation of translation by the multifunctional herpesvirus ICP27 protein. J. Virol. 80, 1588-1591 (2006). (Pubitemid 43134114)
31. Li L, Johnson LA, Dai-Ju JQ, Sandri-Goldin RM. Hsc70 focus formation at the periphery of HSV-1 transcription sites requires ICP27. PLoS ONE 3(1), e1491 (2008).
32. Burch AD, Weller SK. Nuclear sequestration of cellular chaperone and proteasomal machinery during herpes simplex virus type 1 infection. J. Virol. 78, 7175-7185 (2004). (Pubitemid 38781556)
33. Livingston CM, Ifrim MF, Cowan AE, Weller SK. Virus-induced chaperone-enriched (VICE) domains function as nuclear protein quality controlk centers during HSV-1 infection. PLoS Pathog. 5, e1000619 (2009).
34. Hargett D, Rice SA, Bachenheimer SL. Herpes simplex virus type 1 ICP27 dependent activation of NF-kB. J. Virol. 80, 10565-10578 (2006). (Pubitemid 44628903)
35. Kim JC, Lee SY, Kim SY et al. HSV-1 ICP27 suppresses NF-kB activity by stabilizing IkBa. FEBS Lett. 582, 2371-2376 (2008).
36. Johnson KE , Knipe DM. Herpes simplex virus-1 infection causes the secretion of a Type I interferon-antagonizing protein and inhibits signaling at or before Jak-1 activation. Virology 396, 21-29 (2010).
37. Johnson KE, Song B, Knipe DM. Role for herpes simplex virus 1 ICP27 in the inhibition of type I interferon signaling. Virology 374, 487-494 (2008).
38. Song B, Yeh K-C, Knipe DM. Herpes simplex virus gene products required for expression of G1-phase functions. Virology 290, 320-328 (2001). (Pubitemid 33141233)
39. Song B, Liu JJ, Yeh KC, Knipe DM. Herpes simplex virus infection blocks events in the G1 phase of the cell cycle. Virology 267, 326-334 (2000). (Pubitemid 30123615)
40. Hargett D, McLean T, Bachenheimer SL. Herpes simplex virus ICP27 activation of stress kinases JNK and p38. J. Virol. 79, 8348-8360 (2005). (Pubitemid 40853538)
41. Gillis PA, Okagaki LH, Rice SA. Herpes simplex virus type 1 ICP27 induces p38 mitogen-activated protein kinase signaling and apoptosis in HeLa cells. J. Virol. 83, 1767-1777 (2009).
42. Jean S, LeVan KM, Song B, Levine M, Knipe DM. Herpes simplex virus 1 ICP27 is required for transcription of two viral late (g2) genes in infected cells. Virology 283, 273-284 (2001). (Pubitemid 32881174)
43. Rice SA , Knipe DM. Genetic evidence for two distinct transactivation functions of the herpes simplex virus a protein ICP27. J. Virol. 64, 1704-1715 (1990). (Pubitemid 20104909)
44. Sandri-Goldin RM , Mendoza GE. A herpes virus regulatory protein appears to act posttranscriptionally by affecting mRNA processing. Genes Dev. 6, 848-863 (1992).
45. Perkins KD, Gregonis J, Borge S, Rice SA. Transactivation of a viral target gene by herpes simplex virus ICP27 is posttranscriptional and does not require the endogenous promoter or polyadenylation site. J. Virol. 77, 9872-9884 (2003). (Pubitemid 37122068)
46. Rice SA, Long MC, Lam V, Spencer CA. RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following herpes simplex virus infection. J. Virol. 68, 988-1001 (1994). (Pubitemid 24022203)
47. Kalamvoki M , Roizman B. The histone acetyl transferase CLOCK is an essential component of the herpes simplex virus 1 transcriptome that includes TFIID, ICP4, ICP27 and ICP22. J. Virol. 85(18), 9472-9477 (2011).
48. Malik P, Blackbourn DJ, Cheng MF, Hayward GS, Clements JB. Functional co-operation between Kaposi's sarcoma associated herpesvirus ORF57 and ORF50 regulatory proteins. J. Gen.Virol. 85, 2155-2166 (2004). (Pubitemid 39162586)
49. Palmeri D, Spadavecchia S, Carroll KD, Lukac DM. Promoter-and cell-specific transcriptional transactivation by the Kaposi's sarcoma associated herpesvirus ORF57/Mta protein. J. Virol. 81, 13299-13314 (2007). (Pubitemid 350247827)
50. Sahin BB, Patel D, Conrad NK. Kaposi's sarcoma associated herpesvirus ORF57 protein binds and protects a nuclear noncoding RNA from cellular RNA decay pathways. PLoS Pathog. 6, e1000799 (2010).
51. Luo MJ, Reed R. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl Acad. Sci. USA 96, 14937-14942 (1999). (Pubitemid 30019743)
52. Luo MJ, Zhou Z, Magni K et al. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413, 644-647 (2001). (Pubitemid 32964065)
53. Masuda S, Das R, Cheng H, Hurt E, Dorman N, Reed R. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev. 19, 1512-1517 (2005). (Pubitemid 41002995)
54. Chan CC, Dostie J, Diem MD et al. eIF4A3 is a novel component of the exon junction complex. RNA 10, 200-209 (2004). (Pubitemid 38129825)
55. LeHir H, Gatfield D, Izaurralde E, Moore MJ. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20, 4987-4997 (2001). (Pubitemid 32848650)
56. Nott A, LeHir H, Moore MJ. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev. 18, 210-222 (2004). (Pubitemid 38141788)
57. Wiegand HL, Lu S, Cullen BR. Exon junction complexes the enhancing effect of splicing on mRNA expression. Proc. Natl Acad. Sci. USA 100, 11327-11332 (2003). (Pubitemid 37205934)
58. Graveley BR. Sorting out the complexity of SR protein functions. RNA 6, 1197-1211 (2000).
59. Makarova OV. Makarov EM, Luhrmann R. The 65 and 110 kDa SR-rleated proteins of the U4/U6.U5 tri-snRNP are essentail for the assembly of mature spliceosomes. EMBO J.20, 2553-2563 (2001) (Pubitemid 32452874)
60. Misteli T, Spector DL. Serine/threonine phosphatase 1 modulates the subnuclear distribution of pre-mRNA splicing factors. Mol. Biol. Cell 7, 1559-1572 (1996). (Pubitemid 26339729)
61. Misteli T, Caceres JF, Clement JQ, Krainer AR, Wilkinson MF, Spector DL. Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J. Cell. Biol. 143, 297-307 (1998). (Pubitemid 28487851)
62. Misteli T, Spector DL. Protein phosphorylation and the nuclear organization of pre-mRNA splicing. Trends Cell. Biol. 7, 135-138 (1997). (Pubitemid 27135571)
63. Colwill K, Feng LL, Yeakley JM et al. SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol.Chem. 271, 24569-24575 (1996). (Pubitemid 26333196)
64. Sandri-Goldin RM, Hibbard MK, Hardwicke MA. The C-terminal repressor region of HSV-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 (1995).
65. Phelan A, Carmo-Fonseca M, McLauchlan J, Lamond AI, Clements JB. A herpes simplex virus Type 1 immediate-early gene product, IE63, regulates small nuclear ribonucleoprotein distribution. Proc. Natl Acad. Sci. USA 90, 9056-9060 (1993). (Pubitemid 23306450)
66. Ote I, Lebrun M, Vandevenne P et al. Varicella zoster virus IE4 protein interacts with SR proteins and exports mRNAs through the TAP/NXF1 pathway. PLoS ONE 4, e7882 (2009).
67. Cooper M, Goodwin DJ, Hall KT et al. The gene product encoded by ORF 57 of herpesvirus saimiri regulates the redistribution of the splicing factor SC-35. J. Gen. Virol. 80, 1311-1316 (1999). (Pubitemid 29213819)
68. Majerciak V, Yamanegi K, Allemand E, Kruhlak M, Krainer AR, Zheng ZM. Kaposi's sarcoma-associated herpesvirus ORF57 functions as a viral splicing factor and promotes expression of introncontaining viral lytic genes in spliceosomemediated RNA splicing. J. Virol. 82, 2792-2801 (2008). (Pubitemid 351329170)
69. Verma D, Swaminathan S. Epstein-Barr virus SM protein functions as an alternative splicing factor. J. Virol. 82, 7180-7188 (2008). (Pubitemid 351977735)
70. Verma D, Bais S, Gaillard M, Swaminathan S. Epstein-Barr virus SM protein utilizes cellular splicing factor SRp20 to mediate alternative splicing. J. Virol. 84, 11781-11789 (2010).
71. Jumaa H, Nielson PJ. The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation. EMBO J. 16, 5077-5085 (1997). (Pubitemid 27348416)
72. Nojima T, Oshiro-Ideue T, Nakanoya H et al. Herpesvirus protein ICP27 switches PML isoform by altering mRNA splicing. Nucleic Acids Res. 37, 6515-6527 (2009).
73. Sedlackova L, Perkins KD, Lengyel J, Strain AK, van Santen VL, Rice SA. Herpes simplex virus type 1 ICP27 regulates expression of a variant, secreted form of glycoprotein C by an intron retention mechanism. J. Virol. 82, 7443-7455 (2008). (Pubitemid 352031212)
74. Sedlackova L, Perkins KD, Meyer J, Strain AK, Goldman O, Rice SA. Identification of an ICP27 responsive element in the coding region of a herpes simplex virus type 1 late gene. J. Virol. 84, 2707-2718 (2010).
75. Chee AV, Lopez P, Pandolfi PP, Roizman B. Promyelocytic leukemai protein mediates intereron-based anti-herpes simplex virus 1 effects. J. Virol. 77, 7101-7105 (2003). (Pubitemid 36666903)
76. Everett RD, Chelbi-Alix MK. PML and PML nuclear bodies: implications in antiviral defence. Biochemie 89, 819-830 (2007). (Pubitemid 47008945)
77. Reed R, Hurt E. A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 108, 523-531 (2002). (Pubitemid 34260877)
78. Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R. Human mRNA export machinery recruited to the 5 end of mRNA. Cell 127, 1389-1400 (2006). (Pubitemid 44960410)
79. Zhou Z, Luo MJ, Straesser K, Katahira J, Hurt E, Reed R. The protein Aly links premessenger-RNA splicing to nuclear export in metazoans. Nature 407, 401-405 (2001).
80. Gatfield D, LeHir H, Schmitt C et al. The DexH/D box protein HEL/UAP56 is essential for mRNA export in Drosophila. Curr. Biol. 11, 1716-1721 (2001). (Pubitemid 33037786)
81. Kota KP, Wagner SR, Huerta E, Underwood JM, Nickerson JA. Binding of ATP to UAP56 is necessary for mRNA export. J. Cell. Sci. 121, 1526-1537 (2008). (Pubitemid 351936317)
82. Shen H. UAP56-a key player with surprisingly diverse roles in pre-mRNA splicing and nuclear export. BMB Rep. 42, 185-188 (2009).
83. Taniguchi I, Ohno M. ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. Mol. Cell. Biol. 28(601), 601-608 (2008).
84. Rondn AG, Jimeno S, Aguilera A. The interface between transcription and mRNP export: from THO to THSC/TREX-2. Biochim. Biophys. Acta 1799(8), 533-538 (2010).
85. Strasser K, Masuda S, Mason P et al. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417, 304-308 (2002). (Pubitemid 34534714)
86. Dufu K, Livingstone MJ, Seebacher J, Gygi SP, Wilson SA, Reed R. ATP is required for interactions between UAP56 and two conserved mRNA export proteins, Aly and CIP29, to assemble the TREX complex. Genes Dev. 24, 2043-2053 (2011).
87. Nojima T, Hirose T, Kimura H, Hagiwara M. The interaction between cap-binding complex and RNA export factor (REF) is required for intronless mRNA export. J. Biol. Chem. 282, 15645-15651 (2007). (Pubitemid 47093268)
88. Kang Y, Cullen BR. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 13, 1126-1139 (1999). (Pubitemid 29233144)
89. Hautbergue GM, Hung ML, Golovanov AP, Lian LY, Wilson SA. Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc. Natl Acad. Sci. USA 105, 5154-5159 (2008). (Pubitemid 351738526)
90. Hung ML, Hautbergue GM, Snijders APL, Dickman MJ, Wilson SA. Arginine methylation of REF/Aly promotes efficient handover of mRNA to TAP/NXF1. Nucleic Acids Res. 38(10), 3351-3361 (2010).
91. Bacchi A, Braun IC, Rodrigues JP et al. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6, 136-158 (2000). (Pubitemid 30069044)
92. Fribourg S, Braun IC, Izaurralde E, Conti E. Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor. Mol. Cell 8, 645-656 (2001). (Pubitemid 32946941)
93. Grant RP, Hurt E, Neuhaus D, Stewart M. Structure of the C-terminal FG-nuceoporin binding domain of TAP/NXF1. Nat. Struct. Biol. 9, 247-251 (2002). (Pubitemid 34289894)
94. Huang Y, Steitz JA. Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 7, 899-905 (2001). (Pubitemid 32436449)
95. Huang Y, Steitz JA. SRprises along a messenger's journey. Mol. Cell 17, 613-615 (2005). (Pubitemid 40320911)
96. Huang Y, Yario TA, Steitz JA. A molecular link between SR protein dephosphorylation and mRNA export. Proc. Natl Acad. Sci. USA 101, 9666-9670 (2004). (Pubitemid 38869293)
97. Hargous Y, Hautbergue GM, Tintaru AM et al. Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J. 25, 5126-5137 (2006). (Pubitemid 44658530)
98. Tunnicliffe RB, Hautbergue GM, Kalra P et al. Structural basis for the recognition of cellular mRNA export factor REF by herpes viral proteins HSV-1 ICP27 and HVS ORF57. PLoS Pathog. 7, e1001244 (2011).
99. Mears WE, Lam V, Rice SA. Identification of nuclear and nucleolar localization signals in the herpes simplex virus regulatory protein ICP27. J. Virol. 69, 935-947 (1995).
100. Hiriart E, Farjot G, Gruffat H, Nguyen MVC, Sergeant A, Manet E. A novel nuclear export signal and a REF interaction domain both promote mRNA export by the Epstein-Barr virus EB2 protein. J. Biol. Chem. 278, 335-342 (2003). (Pubitemid 36043581)
101. Boyne JR, Colgan KJ, Whitehouse A. Recruitment of the complete hTREX complex is required for Kaposi's sarcomaassociated herpesvirus intronless mRNA nuclear export and virus replication. PLoS Pathog. 4, e1000194 (2008).
102. Malik P, Blackbourn DJ, Clements JB. The evolutionarily conserved Kaposi's sarcomaassociated ORF57 protein interacts with REF protein and acts as an RNA export factor. J. Biol. Chem. 279, 33001-33011 (2004). (Pubitemid 39014760)
103. Nekorchuk M, Han Z, Hsieh TT, Swaminathan S. Kaposi's sarcoma associated herpesvirus ORF57 protein enhances mRNA accumulation independent of effects on nuclear RNA export. J. Virol. 81, 9990-9998 (2007). (Pubitemid 350067702)
104. Majerciak V, Uranishi H, Kruhlak M et al. Kaposi's sarcoma assicated herpesvirus ORF57 interacts with cellular RNA export cofactors RBM15 and OTT3 to promote expression of virual ORF59. J. Virol. 85, 1528-1540 (2011).
105. Jackson BR, Boyne JR, Norerenberg M et al. An interaction between KSHV ORF57 and UIF provides mRNA adaptor redundancy in herpesvirus intronless mRNA export. PLoS Pathog. 7, e1002138 (2011).
106. Zielke B, Thomas M, Giede-Jeppe A, Muller R, Stamminger T. Characterization of bherpesviral pUL69 protein family reveals binding of the cellular mRNA export factor UAP56 as a prerequisite for stimulation of nuclear mRNA export and for efficient viral replication. J. Virol. 85, 1804-1819 (2011).
107. Toth Z, Stamminger T. The human cytomegalovirus regulatory protein UL69 and its effect on mRNA export. Front. Biosci. 13, 2939-2949 (2008). (Pubitemid 351589210)
108. Lischka P, Toth Z, Thomas M, Mueller R, Stamminger T. The UL69 transactivator protein of human cytomegalovirus interacts with DEAD/H-box RNA helicase UAP56 to promote cytoplasmic accumulation of unspliced RNA. Mol. Cell. Biol. 26, 1631-1643 (2006).
109. Kronemann D, Hagemeier SR, Cygnar D, Phillips S, Breshnahan WA. Binding of the HCMV tegument protein UL69 to UAP56/ URH49 is not required for efficient human cytomegalovirus replication. J. Virol. 84, 84(18), 9649-9654 (2010).
110. Huang Y, Gattoni R, Stevenin J, Steitz JA. SR splicing factors serve as adaptor proteins for TAP-dependent mRNA export. Mol. Cell 11, 837-843 (2003). (Pubitemid 36385134)
111. Juillard F, Hiriart E, Sergeant N et al. Epstein-Barr virus protein EB2 contains an N-terminal transferable nuclear export signal that promotes nucleocytoplasmic export by directly binding TAP/NXF1. J. Virol. 83, 12759-12768 (2009).
112. Sergeant A, Gruffat H, Manet E. The Epstein-Barr virus (EBV) protein EB2 is an mRNA export factor essential for virus production. Front. Biosci. 13, 3798-3813 (2008). (Pubitemid 351606100)
113. Walsh MJ, Hautbergue GM, Wilson SA. Structure and function of mRNA export adaptors. Biochem. Soc. Trans. 38, 232-236 (2010).
114. Ingram A, Phelan A, Dunlop J, Clements JB. Immediate early protein IE63 of herpes simplex virus Type-1 binds RNA directly. J. Gen. Virol. 77, 1847-1851 (1996). (Pubitemid 26278767)
115. Toth Z, Lischka P, Stamminger T. RNA-binding of the human cytomegalovirus transactivator protein UL69, mediated by arginine-rich motifs, is not required for nuclear export of unspliced RNA. Nucleic Acids Res. 34, 1237-1249 (2006).
116. Ruvolo V, Gupta AK, Swaminathan S. Epstein-Barr virus SM protein interacts with mRNA in vivo and mediates a gene-specific increase in cytoplasmic mRNA. J. Virol. 75, 6033-6041 (2001). (Pubitemid 32553134)
117. Kang J, Pripuzova N, Majerciak V, Kruhlak M, Lee S, Zheng ZM. Kaposi's sarcoma associated herpesvirus ORF57 promotes escape of viral and human interleukin-6 from microRNA mediated suppression. J. Virol. 85, 2620-2630 (2011).
118. Majerciak V, Zheng ZM. Kaposi's sarcoma associated herpesvirus ORF57 in viral RNA processing. Front. Biosci. 14, 1516-1528 (2009).
119. Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 265, 615-620 (1994).
120. Ramos A, Hollingworth D, Pastore A. G-quartet-dependent recognition between the FMRP RGG box and RNA. RNA 9, 1198-1207 (2003). (Pubitemid 37151675)
121. Herrmann F, Pably P, Eckerich C, Bedford MT, Fackelmayer FO. Human protein arginine methyltransferases in vivo-distinct properties of eight canonical members of the PRMT family. J. Cell. Sci. 122, 667-677 (2009).
122. Norseen J, Johnson FB, Lieberman PM. Role for G-quadruplex RNA binding by Epstein-Barr virus nuclear antigen 1 in DNA replication and metaphase chromosome attachment. J. Virol. 83, 10336-10346 (2009).
123. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST, Darnell RB. Fragile X metal retardation protein targets G quartet mRNAs important for neuronal function. Cell 107, 489-499 (2001). (Pubitemid 33152784)
124. Cocco MJ, Hanakahi LA, Huber MD, Maizels N. Specific interactions of distamycin with G-quadruplex DNA. Nucleic Acids Res. 31, 2944-2951 (2003). (Pubitemid 37442137)
125. Boyne JR, Colgan KJ, Whitehouse A. Herpes virus saimiri ORF57: a post-transcriptional regulatory protein. Front. Biosci. 13, 2928-2938 (2008). (Pubitemid 351606108)
126. Han Z, Verma D, Hilscher C, Dittmer DP, Swaminathan S. General and target-specific RNA binding properties of Epstein-Barr virus SM posttranscriptional regulatory protein. J. Virol. 83, 11635-11644 (2009).
127. Aoyagi M, Gaspar M, Shenk T. Human cytomegalovirus UL69 protein facilitates translation by associating with the mRNA cap-binding complex and excluding 4EBP1. Proc. Natl Acad. Sci. USA 107, 2640-2645 (2010).
128. Russell RC, Fang C, Guan K. An emerging role for TOR signaling in mammalian tissue and stem cell physiology. Development 138, 3343-3356 (2011).
129. Ekim B, Magnuson B, Acosta-Jaquez HA, Keller JA, Freener EP, Finger DC. mTOR kniase domain phosphorylation promotes mTORC1 signaling, cell growth, and cell cycle progression. Mol. Cell. Biol. 31, 2787-2801 (2011).
130. Wang X , Proud CG. mTORC1 signaling: what we still don't know. J. Mol.Cell. Biol. 3, 206-270 (2011).
131. Boyne JR, Jackson BR, Taylor A, Macnab SA, Whitehouse A. Kaposi's sarcoma-associated herpesvirus ORF57 protein interacts with PYM to enhance translation of viral intronless mRNAs. EMBO J. 29, 1851-1864 (2010).
132. Ricci EP, Mure F, Gruffat H et al. Translation of intronless RNAs is strongly stimulated by the Epstein-Barr virus mRNA export factor EB2. Nucleic Acids Res. 37, 4932-4943 (2009).
133. Poppers J, Mulvey M, Perez C, Khoo D, Mohr I. Identification of a lytic-cycle Epstein-Barr virus gene product that can regulate PKR activity. J. Virol. 77, 228-236 (2003). (Pubitemid 36004963)
134. Dosztanyi Z, Chen J, Dunker AK, Simon I, Tompa P. Disorder and sequence repeats in hub proteins and their implications for network evolution. J. Proteome Res. 5, 2985-2995 (2006). (Pubitemid 44749217)
135. Haynes C, Oldfield CJ, Ji F et al. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol. 2, e100 (2006).
136. Uversky VN, Dunker AK. Controlled chaos. Science 322, 1340-1341 (2008).
137. Singh VP, Pacheco I, Uversky VN, Smith SP, MacLeod RJ, Jia Z. Intrinsically disordered human C/EBP homologous protein regulates biological activity of colon cancewr cells during calcium stress. J. Mol. Biol. 380, 313-326 (2008).
138. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN. Flexible nets: the roles of intrinsic disorder in protein interaction networks. FEBS J. 272, 5129-5148 (2005). (Pubitemid 41503146)
139. Karlin D, Ferron F, Canard B, Longhi S. Structural disorder and modular organization in Paramyxovirinae N and P. J. Gen. Virol. 84, 3239-3252 (2003). (Pubitemid 37540753)
140. Uversky VN, Roman A, Oldfield CJ, Dunker AK. Protein intrinsic disorder and human papillomavirures: increased amount of disorder in E6 and E7 oncoproteins from high risk HPVs. J. Proteome Res. 5, 1829-1842 (2006). (Pubitemid 44232696)
141. Xue B, Williams RW, Oldfield CJ, Goh GK, Dunker AK, Uversky VN. Viral disorder or disordered viruses: do viral proteins possess unique features?. Protein Peptide Lett. 17, 932-951 (2010).
142. Ferreon JC, Martinez-Yamout MA, Dyson HJ, Wright PE. Structural basis for subversion of cellular control mechanisms by the adenoviral E1A oncoprotein. Proc. Natl Acad. Sci. USA 106, 13260-13265 (2009).
143. Sieber T, Scholz R, Spoerner M, Schumann F, Kalbitzer HR, Dobner T. Intrinsic disorder in the common N-terminus of human adenovirus 5 E1B-55K and its related E1BN proteins indicated by studies on E1B-93R. Virology 418, 133-143 (2011).
144. Schlessinger A, Punta M, Yachdav G, Kajan L, Rost B. Improved disorder prediction by combination of orthogonal approaches. PLoS ONE 4, e4433 (2009).
145. Schlessinger A, Liu J, Rost B. Natively unstructured loops differ from other loops. PLoS Comput. Biol. 3, e140 (2007).
146. Wu S, Szilagy A, Zhang Y. Improving protein structure prediction using multiple sequencebased contact predictions. Structure 19, 1182-1191 (2011).
147. Dunker AK, Silman I, Uversky VN, Sussman JL. Function and structure of inherently disordered proteins. Curr. Opin. Struct. Biol. 18, 756-764 (2008).
148. Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell. Biol. 6, 197-208 (2005). (Pubitemid 40314921)
149. Mittag T, Kay LE, Forman-Kay JD. Protein dyamics and conformational disorder in molecular recognition. J. Mol. Recognit. 23, 105-116 (2010).
150. Sugase K, Dyson HJ, Wright PE. Mechanism of coupled folding and binding of an instrinsically disordered protein. Nature 447, 1021-1025 (2007). (Pubitemid 46975749)
151. Turoverov KK, Kuznetsova IM, Uversky VN. The protein kingdom exteneded: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation. Prog. Biophys. Mol. Biol. 102, 73-84 (2010).
152. Wright PE, Dyson HJ. Linking folding and binding. Curr. Opin. Struct. Biol. 19, 31-38 (2009).
153. Golovanov AP, Hautbergue GM, Tintaru AM, Lian LY, Wilson SA. The solution structure of REF2-1 reveals interdomain interactions and regions involved in binding mRNA export factors and RNA. RNA 12, 1933-1948 (2006). (Pubitemid 44771753)
154. Hernandez FP, Sandri-Goldin RM. Herpes simplex virus 1 regulatory protein ICP27 undergoes a head-to-tail intramolecular interaction. J. Virol. 84, 4124-4135 (2010).
155. Chattopadhyay S, Weller SK. Direct interaction between the N-and C-terminal portions of the herpes simplex virus type 1 origin binding protein UL9 implies the formation of a head to tail dimer. J. Virol. 81, 13659-13667 (2007). (Pubitemid 350247859)
156. Peters C, Brejec K, Belmont L et al. Insight into the molecular mechanism of the multitasking kinesin-8 motor protein. EMBO J. 29, 3437-3447 (2010).
157. Chen Y, Dokholyan NV. Insights into allosteric control of vinculin function from its large scale conformational dynamics. J. Biol. Chem. 281, 29148-29154 (2006). (Pubitemid 44507058)
158. Dietrich KA, Sindelar CV, Brewer PD, Downing KH, Cremo CR, Rice SA. The kinesin-1 motor protein is regulated by a direct interaction of its head and tail. Proc. Natl Acad. Sci. USA 105, 8938-8943 (2008).
159. Wong YL, Dietrich KA, Naber N, Cooke R, Rice SA. The kinesin-1 tail conformationally restricts the nucleotide pocket. Biophys. J. 96, 2799-2807 (2009).
160. Morales FC, Takahashi Y, Momin S, Adams H, Chen X, Georgescu M. NHERF1/EBP50 head to tail intramolecular interaction masks association with PDZ domain ligands. Mol. Cell. Biol. 27, 2527-2537 (2007). (Pubitemid 46581344)
161. Chong H, Guan K. Regulation of Raf through phosphorylation and N terminus-C terminus interaction. J. Biol. Chem. 218, 36269-36276 (2003). (Pubitemid 37139951)
162. LaLonde DP, Bretscher A. The scaffold protein PDZK1 undergoes a head to tail intramolecular association that negatively regulates its interaction with EBP50. Biochemistry 48, 2261-2271 (2009).
163. Umeki N, Jung HS, Watanabe S et al. The tail binds to the head-neck domain, inhibiting ATPase activity of myosin VIIA. Proc. Natl Acad. Sci. USA 106, 8483-8488 (2009).
164. Moody JD, Grange J, Ascione MPA, Boothe D, Bushnell E, Hansen M.D.H. A zyxin head to tail interaction regulates zyxin-VASP complex formation. Biochem. Biophys. Res. Comm. 378, 625-628 (2009).
165. Roberts GCK, Critchley DR. Structural and biophysical properties of the integrinassociated cytoskeletal protein talin. Biophys. Rev. 1, 61-69 (2009).
166. Kerppola TK. Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Ann. Rev. Biophys. 37, 465-487 (2008).
167. Kerppola TK. Bimolecular fluorescence complementation: visualization of molecular interactions in living cells. Methods Cell. Biol. 85, 431-470 (2008).
168. Zachos G, Koffa MD, Preston CM, Clements JB, Conner J. Herpes simplex virus type 1 blocks the apoptotic host cell defense mechanisms that target Bcl-2 and manipulates activation of p38 mitogen activated protein kinase to improve viral replication. J. Virol. 75, 2710-2728 (2001). (Pubitemid 32185035)
169. Aubert M, Rice SA, Blaho JA. Accumulation of herpes simplex virus Type 1 early and leaky-late proteins correlates with apoptosis prevention in infected human HEp-2 cells. J. Virol. 75, 1013-1030 (2001). (Pubitemid 32037304)
170. Blaho JA, Mitchell C, Roizman B. The herpes simplex virus a proteins 0, 4, 22, and 27 predicted the nucleotidylylation of proteins encoded by the UL21, UL31, UL47 and UL49 genes. J. Biol. Chem. 269, 17401-17410 (1994).
171. McLean TI, Bachenheimer SL. Activation of cJUN N-terminal kinase by herpes simplex virus type 1 enhances viral replication. J. Virol. 73, 8415-8426 (1999). (Pubitemid 29441704)
172. Wadd S, Bryant H, Filhol O et al. The multifunctional herpes simplex virus IE63 protein interacts with heterogeneous ribonucleoprotein K and with casein kinase 2. J. Biol. Chem. 274, 28991-28998 (1999).
173. Koffa MD, Kean J, Zachos G, Rice SA, Clements JB. CK2 protein kinase is stimulated and redistributed by functional herpes simplex virus ICP27 protein. J. Virol. 77, 4315-4325 (2003). (Pubitemid 36350970)