Pub1p C-terminal RRM domain interacts with Tif4631p through a conserved region neighbouring the Pab1p binding site

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Santiveri, Clara M ^a,b   Mirassou, Yasmina ^a   Rico Lastres, Palma ^a   Martínez Lumbreras, Santiago ^a   Pérez Cañadillas, José Manuel ^a  

^a INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; POLY(U) BINDING PROTEIN 1; POLYADENYLIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG; FUNGAL PROTEIN; INITIATION FACTOR 4G; LIGASE; PUB1 PROTEIN, S POMBE; SACCHAROMYCES CEREVISIAE PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; TIF4631 PROTEIN, S CEREVISIAE;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GENETIC STABILITY; IN VITRO STUDY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA RECOGNITION MOTIF; STRUCTURE ANALYSIS; YEAST CELL; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SOLUBILITY;

METAZOA; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; BINDING SITES; CARBON-NITROGEN LIGASES; EUKARYOTIC INITIATION FACTOR-4G; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBILITY;

EID: 80052531130     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024481     Document Type: Article

References (89)

1. Sachs AB, Bond MW, Kornberg RD, (1986) A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45: 827-835.
2. Adam SA, Nakagawa T, Swanson MS, Woodruff TK, Dreyfuss G, (1986) mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol Cell Biol 6: 2932-2943.
3. Anderson JT, Paddy MR, Swanson MS, (1993) PUB1 is a major nuclear and cytoplasmic polyadenylated RNA-binding protein in Saccharomyces cerevisiae. Mol Cell Biol 13: 6102-6113.
4. Matunis MJ, Matunis EL, Dreyfuss G, (1993) PUB1: a major yeast poly(A)+ RNA-binding protein. Mol Cell Biol 13: 6114-6123.
5. Perez-Canadillas JM, Varani G, (2001) Recent advances in RNA-protein recognition. Curr Opin Struct Biol 11: 53-58.
6. Maris C, Dominguez C, Allain FH, (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. Febs J 272: 2118-2131.
7. Clery A, Blatter M, Allain FH, (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18: 290-298.
8. Kessler SH, Sachs AB, (1998) RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol Cell Biol 18: 51-57.
9. Otero LJ, Ashe MP, Sachs AB, (1999) The yeast poly(A)-binding protein Pab1p stimulates in vitro poly(A)-dependent and cap-dependent translation by distinct mechanisms. EMBO J 18: 3153-3163.
10. Sachs AB, Sarnow P, Hentze MW, (1997) Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89: 831-838.
11. Wickens M, Anderson P, Jackson RJ, (1997) Life and death in the cytoplasm: messages from the 3′ end. Curr Opin Genet Dev 7: 220-232.
12. Preiss T, Hentze MW, (1999) From factors to mechanisms: translation and translational control in eukaryotes. Curr Opin Genet Dev 9: 515-521.
13. Sonenberg N, Hinnebusch AG, (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
14. Hernandez G, Altmann M, Lasko P, (2010) Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci 35: 63-73.
15. Duttagupta R, Tian B, Wilusz CJ, Khounh DT, Soteropoulos P, et al. (2005) Global analysis of Pub1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol Cell Biol 25: 5499-5513.
16. Ruiz-Echevarria MJ, Peltz SW, (2000) The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101: 741-751.
17. Vasudevan S, Peltz SW, (2001) Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol Cell 7: 1191-1200.
18. Lopez de Silanes I, Galban S, Martindale JL, Yang X, Mazan-Mamczarz K, et al. (2005) Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol Cell Biol 25: 9520-9531.
19. Vasudevan S, Garneau N, Tu Khounh D, Peltz SW, (2005) p38 mitogen-activated protein kinase/Hog1p regulates translation of the AU-rich-element-bearing MFA2 transcript. Mol Cell Biol 25: 9753-9763.
20. Spriggs KA, Bushell M, Willis AE, (2010) Translational regulation of gene expression during conditions of cell stress. Mol Cell 40: 228-237.
21. Buchan JR, Parker R, (2009) Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36: 932-941.
22. Anderson P, Kedersha N, (2009) RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 10: 430-436.
23. Anderson P, Kedersha N, (2009) Stress granules. Curr Biol 19: R397-398.
24. Moser JJ, Fritzler MJ, (2010) Cytoplasmic ribonucleoprotein (RNP) bodies and their relationship to GW/P bodies. Int J Biochem Cell Biol 42: 828-843.
25. Lui J, Campbell SG, Ashe MP, (2010) Inhibition of translation initiation following glucose depletion in yeast facilitates a rationalization of mRNA content. Biochem Soc Trans 38: 1131-1136.
26. Thomas MG, Loschi M, Desbats MA, Boccaccio GL, (2011) RNA granules: the good, the bad and the ugly. Cell Signal 23: 324-334.
27. Hoyle NP, Castelli LM, Campbell SG, Holmes LE, Ashe MP, (2007) Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J Cell Biol 179: 65-74.
28. Brengues M, Parker R, (2007) Accumulation of polyadenylated mRNA, Pab1p, eIF4E, and eIF4G with P-bodies in Saccharomyces cerevisiae. Mol Biol Cell 18: 2592-2602.
29. Buchan JR, Muhlrad D, Parker R, (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183: 441-455.
30. Swisher KD, Parker R, (2010) Localization to, and effects of Pbp1, Pbp4, Lsm12, Dhh1, and Pab1 on stress granules in Saccharomyces cerevisiae. PLoS One 5: e10006.
31. Grousl T, Ivanov P, Frydlova I, Vasicova P, Janda F, et al. (2009) Robust heat shock induces eIF2alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J Cell Sci 122: 2078-2088.
32. Buchan JR, Yoon JH, Parker R, (2011) Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J Cell Sci 124: 228-239.
33. Kato K, Yamamoto Y, Izawa S, (2011) Severe ethanol stress induces assembly of stress granules in Saccharomyces cerevisiae. Yeast 28: 339-347.
34. Kedersha NL, Gupta M, Li W, Miller I, Anderson P, (1999) RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147: 1431-1442.
35. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, et al. (2000) Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151: 1257-1268.
36. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, et al. (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15: 5383-5398.
37. Gal-Mark N, Schwartz S, Ram O, Eyras E, Ast G, (2009) The pivotal roles of TIA proteins in 5′ splice-site selection of alu exons and across evolution. PLoS Genet 5: e1000717.
38. Puig O, Gottschalk A, Fabrizio P, Seraphin B, (1999) Interaction of the U1 snRNP with nonconserved intronic sequences affects 5′ splice site selection. Genes Dev 13: 569-580.
39. Black DL, (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72: 291-336.
40. Forch P, Puig O, Kedersha N, Martinez C, Granneman S, et al. (2000) The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol Cell 6: 1089-1098.
41. Forch P, Puig O, Martinez C, Seraphin B, Valcarcel J, (2002) The splicing regulator TIA-1 interacts with U1-C to promote U1 snRNP recruitment to 5′ splice sites. EMBO J 21: 6882-6892.
42. Izquierdo JM, Majos N, Bonnal S, Martinez C, Castelo R, et al. (2005) Regulation of Fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition. Mol Cell 19: 475-484.
43. Li H, Shi H, Wang H, Zhu Z, Li X, et al. (2010) Crystal structure of the two N-terminal RRM domains of Pub1 and the poly(U)-binding properties of Pub1. J Struct Biol 171: 291-297.
44. Wishart DS, Sykes BD, (1994) Chemical shifts as a tool for structure determination. Methods Enzymol 239: 363-392.
45. Nagai K, Oubridge C, Ito N, Avis J, Evans P, (1995) The RNP domain: a sequence-specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem Sci 20: 235-240.
46. Dominguez C, Schubert M, Duss O, Ravindranathan S, Allain FH, (2010) Structure determination and dynamics of protein-RNA complexes by NMR spectroscopy. Prog Nucl Magn Reson Spectrosc in press.
47. Wang X, Tanaka Hall TM, (2001) Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat Struct Biol 8: 141-145.
48. Perez-Canadillas JM, (2006) Grabbing the message: structural basis of mRNA 3′UTR recognition by Hrp1. EMBO J 25: 3167-3178.
49. Handa N, Nureki O, Kurimoto K, Kim I, Sakamoto H, et al. (1999) Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398: 579-585.
50. Deo RC, Bonanno JB, Sonenberg N, Burley SK, (1999) Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98: 835-845.
51. Auweter SD, Oberstrass FC, Allain FH, (2007) Solving the structure of PTB in complex with pyrimidine tracts: an NMR study of protein-RNA complexes of weak affinities. J Mol Biol 367: 174-186.
52. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, et al. (2005) Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 309: 2054-2057.
53. Sudmeir JL, Evelhoch JL, Jonsson NB-H, (1980) Dependence of NMR lineshape analysis upon chemical rates and mechanisms: Implications for enzyme histidine titrations. J Magn Reson 40: 377-390.
54. Auweter SD, Fasan R, Reymond L, Underwood JG, Black DL, et al. (2006) Molecular basis of RNA recognition by the human alternative splicing factor Fox-1. EMBO J 25: 163-173.
55. Tsuda K, Kuwasako K, Takahashi M, Someya T, Inoue M, et al. (2009) Structural basis for the sequence-specific RNA-recognition mechanism of human CUG-BP1 RRM3. Nucleic Acids Res 37: 5151-5166.
56. Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141-147.
57. Tarassov K, Messier V, Landry CR, Radinovic S, Serna Molina MM, et al. (2008) An in vivo map of the yeast protein interactome. Science 320: 1465-1470.
58. Anderson P, Kedersha N, (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci 33: 141-150.
59. Anderson P, Kedersha N, (2006) RNA granules. J Cell Biol 172: 803-808.
60. Schutz P, Bumann M, Oberholzer AE, Bieniossek C, Trachsel H, et al. (2008) Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc Natl Acad Sci U S A 105: 9564-9569.
61. Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, et al. (2003) Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115: 739-750.
62. Tarun SZ Jr, Wells SE, Deardorff JA, Sachs AB, (1997) Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc Natl Acad Sci U S A 94: 9046-9051.
63. Berset C, Zurbriggen A, Djafarzadeh S, Altmann M, Trachsel H, (2003) RNA-binding activity of translation initiation factor eIF4G1 from Saccharomyces cerevisiae. RNA 9: 871-880.
64. Marintchev A, Edmonds KA, Marintcheva B, Hendrickson E, Oberer M, et al. (2009) Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136: 447-460.
65. Pervushin K, Riek R, Wider G, Wuthrich K, (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A 94: 12366-12371.
66. Park EH, Walker SE, Lee JM, Rothenburg S, Lorsch JR, et al. (2011) Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1*PABP mRNPs in vivo. EMBO J 30: 302-316.
67. Fadouloglou VE, Kokkinidis M, Glykos NM, (2008) Determination of protein oligomerization state: two approaches based on glutaraldehyde crosslinking. Anal Biochem 373: 404-406.
68. Zhang D, Rosbash M, (1999) Identification of eight proteins that cross-link to pre-mRNA in the yeast commitment complex. Genes Dev 13: 581-592.
69. Liu-Yesucevitz L, Bilgutay A, Zhang YJ, Vanderwyde T, Citro A, et al. (2010) Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS One 5: e13250.
70. Freibaum BD, Chitta RK, High AA, Taylor JP, (2010) Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. J Proteome Res 9: 1104-1120.
71. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, et al. (2009) TDP-43 is recruited to stress granules in conditions of oxidative insult. J Neurochem 111: 1051-1061.
72. Kuo PH, Doudeva LG, Wang YT, Shen CK, Yuan HS, (2009) Structural insights into TDP-43 in nucleic-acid binding and domain interactions. Nucleic Acids Res 37: 1799-1808.
73. Kielkopf CL, Lucke S, Green MR, (2004) U2AF homology motifs: protein recognition in the RRM world. Genes Dev 18: 1513-1526.
74. Cukier CD, Hollingworth D, Martin SR, Kelly G, Diaz-Moreno I, et al. (2010) Molecular basis of FIR-mediated c-myc transcriptional control. Nat Struct Mol Biol.
75. Groft CM, Burley SK, (2002) Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol Cell 9: 1273-1283.
76. Maquat LE, Tarn WY, Isken O, (2010) The pioneer round of translation: features and functions. Cell 142: 368-374.
77. Warkocki Z, Odenwalder P, Schmitzova J, Platzmann F, Stark H, et al. (2009) Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat Struct Mol Biol 16: 1237-1243.
78. Neidhardt FC, Bloch PL, Smith DF, (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
79. Sattler M, Schleucher J, Griesinger C, (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog Nucl Magn Reson Spectrosc 34: 93-158.
80. Jung YS, Zweckstetter M, (2004) Mars - robust automatic backbone assignment of proteins. J Biomol NMR 30: 11-23.
81. Kay LE, Xu GY, Singer AU, Muhandiram DR, Forman-Kay JD, (1993) A Gradient-Enhanced HCCH-TOCSY Experiment for Recording Side-Chain 1H and 13C Correlations in H2O Samples of Proteins. Journal of Magnetic Resonance, Series B 101: 333-337.
82. 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.
83. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, et al. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59: 687-696.
84. Kumar A, Ernst RR, Wuthrich K, (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem Biophys Res Commun 95: 1-6.
85. Palmer AG, Cavanagh J, Byrd RA, Rance M, (1992) Sensitivity improvement in three-dimensional heteronuclear correlation NMR spectroscopy. Journal of Magnetic Resonance 96: 416-424.
86. Cornilescu G, Delaglio F, Bax A, (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302.
87. Guntert P, Mumenthaler C, Wuthrich K, (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273: 283-298.
88. Koradi R, Billeter M, Wuthrich K, (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55 29-32.
89. Fielding L, (2007) NMR methods for the determination of protein-ligand dissociation constants. Prog Nucl Magn Reson Spectrosc 51.