Competitive and Cooperative Interactions Mediate RNA Transfer from Herpesvirus Saimiri ORF57 to the Mammalian Export Adaptor ALYREF

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Tunnicliffe, Richard B ^a   Hautbergue, Guillaume M ^b   Wilson, Stuart A ^c   Kalra, Priti ^a   Golovanov, Alexander P ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ORF57 PROTEIN; PROTEIN ALYREF; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GENE MUTATION; GENE TRANSFER; HERPES VIRUS SAIMIRI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RNA BINDING; SIMULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 2, SAIMIRIINE; HOST-PARASITE INTERACTIONS; HUMANS; NUCLEAR PROTEINS; PROTEIN STRUCTURE, QUATERNARY; REPRESSOR PROTEINS; RNA TRANSPORT; RNA, VIRAL; RNA-BINDING PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR VIRUS INFECTIONS;

EID: 84895733747     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003907     Document Type: Article

References (67)

1. Glisovic T, Bachorik JL, Yong J, Dreyfuss G, (2008) RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 582: 1977-1986.
2. Strasser K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, et al. (2002) TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417: 304-308.
3. Masuda S, Das R, Cheng H, Hurt E, Dorman N, et al. (2005) Recruitment of the human TREX complex to mRNA during splicing. Genes Dev 19: 1512-1517.
4. Hautbergue GM, Hung ML, Walsh MJ, Snijders AP, Chang CT, et al. (2009) UIF, a New mRNA Export Adaptor that Works Together with REF/ALY, Requires FACT for Recruitment to mRNA. Curr Biol 19: 1918-1924.
5. Hautbergue GM, Hung ML, Golovanov AP, Lian LY, Wilson SA, (2008) Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc Natl Acad Sci USA 105: 5154-5159.
6. Viphakone N, Hautbergue GM, Walsh M, Chang CT, Holland A, et al. (2012) TREX exposes the RNA-binding domain of Nxf1 to enable mRNA export. Nat Commun 3: 1006.
7. Stutz F, Bachi A, Doerks T, Braun IC, Seraphin B, et al. (2000) REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 6: 638-650.
8. Rodrigues JP, Rode M, Gatfield D, Blencowe BJ, Carmo-Fonseca M, et al. (2001) REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proc Natl Acad Sci USA 98: 1030-1035.
9. Perez-Alvarado GC, Martinez-Yamout M, Allen MM, Grosschedl R, Dyson HJ, et al. (2003) Structure of the nuclear factor ALY: insights into post-transcriptional regulatory and mRNA nuclear export processes. Biochemistry 42: 7348-7357.
10. Golovanov AP, Hautbergue GM, Tintaru AM, Lian LY, Wilson SA, (2006) The solution structure of REF2-I reveals interdomain interactions and regions involved in binding mRNA export factors and RNA. RNA 12: 1933-1948.
11. Hung ML, Hautbergue GM, Snijders AP, Dickman MJ, Wilson SA, (2010) Arginine methylation of REF/ALY promotes efficient handover of mRNA to TAP/NXF1. Nucleic Acids Research 38: 3351-3361.
12. Bachi A, Braun IC, Rodrigues JP, Pante N, Ribbeck K, et al. (2000) 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.
13. Fribourg S, Braun IC, Izaurralde E, Conti E, (2001) 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.
14. Grant RP, Hurt E, Neuhaus D, Stewart M, (2002) Structure of the C-terminal FG-nucleoporin binding domain of Tap/NXF1. Nature Struct Biol 9: 247-251.
15. Koffa MD, Clements JB, Izaurralde E, Wadd S, Wilson SA, et al. (2001) Herpes simplex virus ICP27 protein provides viral mRNAs with access to the cellular mRNA export pathway. EMBO J 20: 5769-5778.
16. Chen IH, Sciabica KS, Sandri-Goldin RM, (2002) ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J Virol 76: 12877-12889.
17. Malik P, Blackbourn DJ, Clements JB, (2004) The evolutionarily conserved Kaposi's sarcoma-associated herpesvirus ORF57 protein interacts with REF protein and acts as an RNA export factor. J Biol Chem 279: 33001-33011.
18. Hiriart E, Farjot G, Gruffat H, Nguyen MV, Sergeant A, et al. (2003) 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.
19. Jackson BR, Boyne JR, Noerenberg M, Taylor A, Hautbergue GM, et al. (2011) An Interaction between KSHV ORF57 and UIF Provides mRNA-Adaptor Redundancy in Herpesvirus Intronless mRNA Export. PLoS Pathog 7: e1002138.
20. Goodwin DJ, Hall KT, Stevenson AJ, Markham AF, Whitehouse A, (1999) The open reading frame 57 gene product of herpesvirus saimiri shuttles between the nucleus and cytoplasm and is involved in viral RNA nuclear export. J Virol 73: 10519-10524.
21. Williams BJ, Boyne JR, Goodwin DJ, Roaden L, Hautbergue GM, et al. (2005) The prototype gamma-2 herpesvirus nucleocytoplasmic shuttling protein, ORF 57, transports viral RNA through the cellular mRNA export pathway. Biochem J 387: 295-308.
22. Boyne JR, Colgan KJ, Whitehouse A, (2008) Recruitment of the complete hTREX complex is required for Kaposi's sarcoma-associated herpesvirus intronless mRNA nuclear export and virus replication. PLoS Pathog 4: e1000194.
23. Boyne JR, Colgan KJ, Whitehouse A, (2008) Herpesvirus saimiri ORF57: a post-transcriptional regulatory protein. Front Biosci 13: 2928-2938.
24. Stubbs SH, Hunter OV, Hoover A, Conrad NK, (2012) Viral Factors Reveal a Role for REF/Aly in Nuclear RNA Stability. Mol Cell Biol 32: 1260-1270.
25. Sandri-Goldin RM, (2011) The many roles of the highly interactive HSV protein ICP27, a key regulator of infection. Future Microbiol 6: 1261-1277.
26. Taylor A, Jackson BR, Noerenberg M, Hughes DJ, Boyne JR, et al. (2011) Mutation of a C-Terminal Motif Affects Kaposi's Sarcoma-Associated Herpesvirus ORF57 RNA Binding, Nuclear Trafficking, and Multimerization. J Virol 85: 7881-7891.
27. Schumann S, Jackson BR, Baquero-Perez B, Whitehouse A, (2013) Kaposi's Sarcoma-Associated Herpesvirus ORF57 Protein: Exploiting All Stages of Viral mRNA Processing. Viruses 5: 1901-1923.
28. Hiriart E, Bardouillet L, Manet E, Gruffat H, Penin F, et al. (2003) A region of the Epstein-Barr virus (EBV) mRNA export factor EB2 containing an arginine-rich motif mediates direct binding to RNA. J Biol Chem 278: 37790-37798.
29. Toth Z, Stamminger T, (2008) The human cytomegalovirus regulatory protein UL69 and its effect on mRNA export. Front Biosci 13: 2939-2949.
30. Tunnicliffe RB, Hautbergue GM, Kalra P, Jackson BR, Whitehouse A, et al. (2011) 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.
31. Gray KA, Daugherty LC, Gordon SM, Seal RL, Wright MW, et al. (2013) Genenames.org: the HGNC resources in 2013. Nucleic Acids Res 41: D545-D552.
32. Colgan KJ, Boyne JR, Whitehouse A, (2009) Identification of a response element in a herpesvirus saimiri mRNA recognized by the ORF57 protein. J Gen Virol 90: 596-601.
33. 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.
34. 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.
35. Mackereth CD, Sattler M, (2012) Dynamics in multi-domain protein recognition of RNA. Curr Opin Struct Biol 22: 287-296.
36. Valkov E, Dean JC, Jani D, Kuhlmann SI, Stewart M, (2012) Structural basis for the assembly and disassembly of mRNA nuclear export complexes. Biochim Biophys Acta 1819: 578-592.
37. Takahashi H, Nakanishi T, Kami K, Arata Y, Shimada I, (2000) A novel NMR method for determining the interfaces of large protein-protein complexes. Nat Struct Biol 7: 220-223.
38. Golovanov AP, Blankley RT, Avis JM, Bermel W, (2007) Isotopically discriminated NMR spectroscopy: a tool for investigating complex protein interactions in vitro. J Am Chem Soc 129: 6528-6535.
39. Lane AN, Kelly G, Ramos A, Frenkiel TA, (2001) Determining binding sites in protein-nucleic acid complexes by cross-saturation. J Biomol NMR 21: 127-139.
40. Jones DT, (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202.
41. Lacroix E, Viguera AR, Serrano L, (1998) Elucidating the folding problem of alpha-helices: local motifs, long-range electrostatics, ionic-strength dependence and prediction of NMR parameters. J Mol Biol 284: 173-191.
42. Shen Y, Delaglio F, Cornilescu G, Bax A, (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 44: 213-223.
43. Kuzmic P, (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase. Analytical Biochemistry 237: 260-273.
44. Williamson JR, (2008) Cooperativity in macromolecular assembly. Nature Chem Biol 4: 458-465.
45. Borg M, Mittag T, Pawson T, Tyers M, Forman-Kay JD, et al. (2007) Polyelectrostatic interactions of disordered ligands suggest a physical basis for ultrasensitivity. Proc Natl Acad Sci USA 104: 9650-9655.
46. Calnan BJ, Biancalana S, Hudson D, Frankel AD, (1991) Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features of RNA-protein recognition. Genes Dev 5: 201-210.
47. Wilkinson TA, Zhu LY, Hu WD, Chen Y, (2004) Retention of conformational flexibility in HIV-1 Rev-RNA complexes. Biochemistry 43: 16153-16160.
48. Bayer TS, Booth LN, Knudsen SM, Ellington AD, (2005) Arginine-rich motifs present multiple interfaces for specific binding by RNA. RNA 11: 1848-1857.
49. Lunde BM, Moore C, Varani G, (2007) RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol 8: 479-490.
50. Kielkopf CL, Rodionova NA, Green MR, Burley SK, (2001) A novel peptide recognition mode revealed by the X-ray structure of a core U2AF-(35)/U2AF(65) heterodimer. Cell 106: 595-605.
51. Kielkopf CL, Lucke S, Green AR, (2004) U2AF homology motifs: protein recognition in the RRM world. Genes & Dev 18: 1513-1526.
52. Clery A, Blatter M, Allain FH, (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18: 290-298.
53. Majerciak V, Yamanegi K, Nie SH, Zheng ZM, (2006) Structural and functional analyses of Kaposi sarcoma-associated herpesvirus ORF57 nuclear localization signals in living cells. J Biol Chem 281: 28365-28378.
54. Tian X, Devi-Rao G, Golovanov AP, Sandri-Goldin RM, (2013) The Interaction of the Cellular Export Adaptor Protein Aly/REF with ICP27 Contributes to the Efficiency of Herpes Simplex Virus 1 mRNA Export. J Virol 87: 7210-7217.
55. Tompa P, Fuxreiter M, (2008) Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 33: 2-8.
56. Tompa P, (2011) Unstructural biology coming of age. Curr Opin Struct Biol 21: 419-425.
57. Boehr DD, Nussinov R, Wright PE, (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5: 789-796.
58. Mittag T, Kay LE, Forman-Kay JD, (2010) Protein dynamics and conformational disorder in molecular recognition. J Mol Recogn 23: 105-116.
59. Davey NE, Trave G, Gibson TJ, (2011) How viruses hijack cell regulation. Trends Biochem Sci 36: 159-169.
60. Ellisdon AM, Dimitrova L, Hurt E, Stewart M, (2012) Structural basis for the assembly and nucleic acid binding of the TREX-2 transcription-export complex. Nature Struct Mol Biol 19: 328-U390.
61. Marsh JA, Teichmann SA, Forman-Kay JD, (2012) Probing the diverse landscape of protein flexibility and binding. Curr Opin Struct Biol 22: 643-650.
62. Golovanov AP, Hautbergue GM, Wilson SA, Lian LY, (2004) A simple method for improving protein solubility and long-term stability. J Am Chem Soc 126: 8933-8939.
63. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
64. Guntert P, (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378.
65. Stuart AC, Borzilleri KA, Withka JM, Palmer AG, (1999) Compensating for Variations in 1H-13C Scalar Coupling Constants in Isotope-Filtered NMR Experiments. J Am Chem Soc 121: 5346-5347.
66. Zwahlen C, Legault P, Vincent SbJF, Greenblatt J, Konrat R, et al. (1997) Methods for Measurement of Intermolecular NOEs by Multinuclear NMR Spectroscopy: Application to a bacteriophage λ N-peptide/boxB RNA complex. J Am Chem Soc 119: 6711-6721.
67. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, et al. (2006) COPASI- A COmplex PAthway SImulator. Bioinformatics 22: 3067-3074.