Quantitative studies of mRNA recruitment to the eukaryotic ribosome

Biochimie

Volumn 114, Issue , 2015, Pages 58-71

  Fraser, Christopher S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

43S PIC; eIF4F; mRNA recruitment

Indexed keywords

INITIATION FACTOR 1; INITIATION FACTOR 1A; INITIATION FACTOR 3; INITIATION FACTOR 4F; INITIATION FACTOR 4G; MESSENGER RNA; INITIATION FACTOR; START CODON;

5' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CODON; EUKARYOTE; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE STUDY; RIBOSOME; RIBOSOME SUBUNIT; RNA TRANSLATION; TRANSLATION INITIATION; ANIMAL; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN MOTIF; RNA TRANSPORT; START CODON;

EUKARYOTA;

AMINO ACID MOTIFS; ANIMALS; CODON, INITIATOR; EUKARYOTIC INITIATION FACTORS; GENE EXPRESSION REGULATION; HUMANS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RIBOSOMES; RNA TRANSPORT; RNA, MESSENGER;

EID: 84930383499     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.02.017     Document Type: Review

References (181)

1. D. Chu, E. Kazana, N. Bellanger, T. Singh, M.F. Tuite, and T. von der Haar Translation elongation can control translation initiation on eukaryotic mRNAs EMBO J. 33 2014 21 34
2. J.B. Plotkin, and G. Kudla Synonymous but not the same: the causes and consequences of codon bias Nat. Rev. Genet. 12 2011 32 42
3. L. Ciandrini, I. Stansfield, and M.C. Romano Ribosome traffic on mRNAs maps to gene ontology: genome-wide quantification of translation initiation rates and polysome size regulation PLoS Comput. Biol. 9 2013 e1002866
4. A.J. Kemp, R. Betney, L. Ciandrini, A.C. Schwenger, M.C. Romano, and I. Stansfield A yeast tRNA mutant that causes pseudohyphal growth exhibits reduced rates of CAG codon translation Mol. Microbiol. 87 2013 284 300
5. M. Zhou, J. Guo, J. Cha, M. Chae, S. Chen, J.M. Barral, M.S. Sachs, and Y. Liu Non-optimal codon usage affects expression, structure and function of clock protein FRQ Nature 495 2013 111 115
6. T. Tuller, A. Carmi, K. Vestsigian, S. Navon, Y. Dorfan, J. Zaborske, T. Pan, O. Dahan, I. Furman, and Y. Pilpel An evolutionarily conserved mechanism for controlling the efficiency of protein translation Cell 141 2010 344 354
7. C. Pop, S. Rouskin, N.T. Ingolia, L. Han, E.M. Phizicky, J.S. Weissman, and D. Koller Causal signals between codon bias, mRNA structure, and the efficiency of translation and elongation Mol. Syst. Biol. 10 2014 770
8. E. Marshall, I. Stansfield, and M.C. Romano Ribosome recycling induces optimal translation rate at low ribosomal availability J. R. Soc. Interface/R. Soc. 11 2014 20140589
9. P. Shah, Y. Ding, M. Niemczyk, G. Kudla, and J.B. Plotkin Rate-limiting steps in yeast protein translation Cell 153 2013 1589 1601
10. A.G. Hinnebusch The scanning mechanism of eukaryotic translation initiation Annu. Rev. Biochem. 83 2014 779 812
11. C.E. Aitken, and J.R. Lorsch A mechanistic overview of translation initiation in eukaryotes Nat. Struct. Mol. Biol. 19 2012 568 576
12. A.G. Hinnebusch, and J.R. Lorsch The mechanism of eukaryotic translation initiation: new insights and challenges Cold Spring Harbor. Perspect. Biol. 4 2012
13. R.J. Jackson, C.U. Hellen, and T.V. Pestova The mechanism of eukaryotic translation initiation and principles of its regulation Nat. Rev. Mol. Cell Biol. 11 2010 113 127
14. J.R. Lorsch, and T.E. Dever Molecular view of 43 S complex formation and start site selection in eukaryotic translation initiation J. Biol. Chem. 285 2010 21203 21207
15. A.G. Hinnebusch Molecular mechanism of scanning and start codon selection in eukaryotes Microbiol. Mol. Biol. Rev.: MMBR 75 2011 434 467
16. M.A. Algire, and J.R. Lorsch Where to begin? The mechanism of translation initiation codon selection in eukaryotes Curr. Opin. Chem. Biol. 10 2006 480 486
17. R.J. Jackson, C.U. Hellen, and T.V. Pestova Termination and post-termination events in eukaryotic translation Adv. Protein Chem. Struct. Biol. 86 2012 45 93
18. T.E. Dever, and R. Green The elongation, termination, and recycling phases of translation in eukaryotes Cold Spring Harbor. Perspect. Biol. 4 2012 a013706
19. E. Nurenberg, and R. Tampe Tying up loose ends: ribosome recycling in eukaryotes and archaea Trends Biochem. Sci. 38 2013 64 74
20. S. Franckenberg, T. Becker, and R. Beckmann Structural view on recycling of archaeal and eukaryotic ribosomes after canonical termination and ribosome rescue Curr. Opin. Struct. Biol. 22 2012 786 796
21. S. Klinge, F. Voigts-Hoffmann, M. Leibundgut, and N. Ban Atomic structures of the eukaryotic ribosome Trends Biochem. Sci. 37 2012 189 198
22. F. Voigts-Hoffmann, S. Klinge, and N. Ban Structural insights into eukaryotic ribosomes and the initiation of translation Curr. Opin. Struct. Biol. 22 2012 768 777
23. L. Jenner, S. Melnikov, N. Garreau de Loubresse, A. Ben-Shem, M. Iskakova, A. Urzhumtsev, A. Meskauskas, J. Dinman, G. Yusupova, and M. Yusupov Crystal structure of the 80S yeast ribosome Curr. Opin. Struct. Biol. 22 2012 759 767
24. D.N. Wilson, and J.H. Doudna Cate The structure and function of the eukaryotic ribosome Cold Spring Harbor. Perspect. Biol. 4 2012
25. M.H. Schreier, B. Erni, and T. Staehelin Initiation of mammalian protein synthesis. I. Purification and characterization of seven initiation factors J. Mol. Biol. 116 1977 727 753
26. M.H. Schreier, and T. Staehelin Translation of rabbit hemoglobin meessenger RNA in vitro with purified and partially purified components from brain or liver of different species Proc. Natl. Acad. Sci. U. S. A. 70 1973 462 465
27. B. Safer, S.L. Adams, W.M. Kemper, K.W. Berry, M. Lloyd, and W.C. Merrick Purification and characterization of two initiation factors required for maximal activity of a highly fractionated globin mRNA translation system Proc. Natl. Acad. Sci. U. S. A. 73 1976 2584 2588
28. R. Benne, and J.W. Hershey The mechanism of action of protein synthesis initiation factors from rabbit reticulocytes J. Biol. Chem. 253 1978 3078 3087
29. S.L. Adams, B. Safer, W.F. Anderson, and W.C. Merrick Eukaryotic initiation complex formation. Evidence for two distinct pathways J. Biol. Chem. 250 1975 9083 9089
30. D. Etchison, S.C. Milburn, I. Edery, N. Sonenberg, and J.W. Hershey Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex J. Biol. Chem. 257 1982 14806 14810
31. C.S. Fraser, and J.A. Doudna Quantitative studies of ribosome conformational dynamics Q. Rev. Biophys. 40 2007 163 189
32. I.B. Lomakin, V.G. Kolupaeva, A. Marintchev, G. Wagner, and T.V. Pestova Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing Genes Dev. 17 2003 2786 2797
33. Y. Yu, A. Marintchev, V.G. Kolupaeva, A. Unbehaun, T. Veryasova, S.C. Lai, P. Hong, G. Wagner, C.U. Hellen, and T.V. Pestova Position of eukaryotic translation initiation factor eIF1A on the 40S ribosomal subunit mapped by directed hydroxyl radical probing Nucleic Acids Res. 37 15 2009 5167 5182
34. I.B. Lomakin, and T.A. Steitz The initiation of mammalian protein synthesis and mRNA scanning mechanism Nature 500 2013 307 311
35. J.P. Erzberger, F. Stengel, R. Pellarin, S. Zhang, T. Schaefer, C.H. Aylett, P. Cimermancic, D. Boehringer, A. Sali, R. Aebersold, and N. Ban Molecular architecture of the 40SeIF1eIF3 translation initiation complex Cell 158 2014 1123 1135
36. T. Hussain, Jose L. Llácer, Israel S. Fernández, A. Munoz, P. Martin-Marcos, Christos G. Savva, Jon R. Lorsch, Alan G. Hinnebusch, and V. Ramakrishnan Structural changes enable start codon recognition by the eukaryotic translation initiation complex Cell 159 2014 597 607
37. M. Weisser, F. Voigts-Hoffmann, J. Rabl, M. Leibundgut, and N. Ban The crystal structure of the eukaryotic 40S ribosomal subunit in complex with eIF1 and eIF1A Nat. Struct. Mol. Biol. 20 2013 1015 1017
38. Y. Hashem, A. des Georges, V. Dhote, R. Langlois, H.Y. Liao, R.A. Grassucci, C.U. Hellen, T.V. Pestova, and J. Frank Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29 Cell 153 2013 1108 1119
39. C.S. Fraser, K.E. Berry, J.W. Hershey, and J.A. Doudna eIF3j is located in the decoding center of the human 40S ribosomal subunit Mol. Cell 26 2007 811 819
40. J.S. Nanda, A.K. Saini, A.M. Munoz, A.G. Hinnebusch, and J.R. Lorsch Coordinated movements of eukaryotic translation initiation factors eIF1, eIF1A, and eIF5 trigger phosphate release from eIF2 in response to start codon recognition by the ribosomal preinitiation complex J. Biol. Chem. 288 2013 5316 5329
41. L.A. Passmore, T.M. Schmeing, D. Maag, D.J. Applefield, M.G. Acker, M.A. Algire, J.R. Lorsch, and V. Ramakrishnan The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome Mol. Cell 26 2007 41 50
42. T.V. Pestova, S.I. Borukhov, and C.U. Hellen Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons Nature 394 1998 854 859
43. C.S. Fraser, J.W. Hershey, and J.A. Doudna The pathway of hepatitis C virus mRNA recruitment to the human ribosome Nat. Struct. Mol. Biol. 16 2009 397 404
44. C.M. Spahn, J.S. Kieft, R.A. Grassucci, P.A. Penczek, K. Zhou, J.A. Doudna, and J. Frank Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit Science 291 2001 1959 1962
45. I.S. Fernandez, X.C. Bai, T. Hussain, A.C. Kelley, J.R. Lorsch, V. Ramakrishnan, and S.H. Scheres Molecular architecture of a eukaryotic translational initiation complex Science 342 2013 1240585
46. X.C. Bai, I.S. Fernandez, G. McMullan, and S.H. Scheres Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles eLife 2 2013 e00461
47. C.A. Fekete, S.F. Mitchell, V.A. Cherkasova, D. Applefield, M.A. Algire, D. Maag, A.K. Saini, J.R. Lorsch, and A.G. Hinnebusch N- and C-terminal residues of eIF1A have opposing effects on the fidelity of start codon selection EMBO J. 26 2007 1602 1614
48. D. Maag, M.A. Algire, and J.R. Lorsch Communication between eukaryotic translation initiation factors 5 and 1A within the ribosomal pre-initiation complex plays a role in start site selection J. Mol. Biol. 356 2006 724 737
49. D. Maag, C.A. Fekete, Z. Gryczynski, and J.R. Lorsch A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon Mol. Cell 17 2005 265 275
50. D. Maag, and J.R. Lorsch Communication between eukaryotic translation initiation factors 1 and 1A on the yeast small ribosomal subunit J. Mol. Biol. 330 2003 917 924
51. J.S. Nanda, Y.N. Cheung, J.E. Takacs, P. Martin-Marcos, A.K. Saini, A.G. Hinnebusch, and J.R. Lorsch eIF1 controls multiple steps in start codon recognition during eukaryotic translation initiation J. Mol. Biol. 394 2009 268 285
52. M. Sokabe, and C.S. Fraser Human eukaryotic initiation factor 2 (eIF2)-GTP-Met-tRNAi ternary complex and eIF3 stabilize the 43S preinitiation complex J. Biol. Chem. 289 2014 31827 31836
53. R. Duncan, and J.W. Hershey Identification and quantitation of levels of protein synthesis initiation factors in crude HeLa cell lysates by two-dimensional polyacrylamide gel electrophoresis J. Biol. Chem. 258 1983 7228 7235
54. C.R. Singh, T. Udagawa, B. Lee, S. Wassink, H. He, Y. Yamamoto, J.T. Anderson, G.D. Pavitt, and K. Asano Change in nutritional status modulates the abundance of critical pre-initiation intermediate complexes during translation initiation in vivo J. Mol. Biol. 370 2007 315 330
55. S. Ghaemmaghami, W.K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O'Shea, and J.S. Weissman Global analysis of protein expression in yeast Nature 425 2003 737 741
56. T. von der Haar, and J.E. McCarthy Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function Mol. Microbiol. 46 2002 531 544
57. H. Firczuk, S. Kannambath, J. Pahle, A. Claydon, R. Beynon, J. Duncan, H. Westerhoff, P. Mendes, and J.E. McCarthy An in vivo control map for the eukaryotic mRNA translation machinery Mol. Syst. Biol. 9 2013 635
58. P. Milon, C. Maracci, L. Filonava, C.O. Gualerzi, and M.V. Rodnina Real-time assembly landscape of bacterial 30S translation initiation complex Nat. Struct. Mol. Biol. 19 2012 609 615
59. A. Tsai, A. Petrov, R.A. Marshall, J. Korlach, S. Uemura, and J.D. Puglisi Heterogeneous pathways and timing of factor departure during translation initiation Nature 487 2012 390 393
60. K. Asano, J. Clayton, A. Shalev, and A.G. Hinnebusch A multifactor complex of eukaryotic initiation factors, eIF1, eIF2, eIF3, eIF5, and initiator tRNA(Met) is an important translation initiation intermediate in vivo Genes Dev. 14 2000 2534 2546
61. M. Sokabe, C.S. Fraser, and J.W. Hershey The human translation initiation multi-factor complex promotes methionyl-tRNAi binding to the 40S ribosomal subunit Nucleic Acids Res. 40 2012 905 913
62. D. Barthelme, S. Dinkelaker, S.V. Albers, P. Londei, U. Ermler, and R. Tampe Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1 Proc. Natl. Acad. Sci. U. S. A. 108 2011 3228 3233
63. A.V. Pisarev, M.A. Skabkin, V.P. Pisareva, O.V. Skabkina, A.M. Rakotondrafara, M.W. Hentze, C.U. Hellen, and T.V. Pestova The role of ABCE1 in eukaryotic posttermination ribosomal recycling Mol. Cell 37 2010 196 210
64. C.J. Shoemaker, and R. Green Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast Proc. Natl. Acad. Sci. U. S. A. 108 2011 E1392 E1398
65. F. Peske, M.V. Rodnina, and W. Wintermeyer Sequence of steps in ribosome recycling as defined by kinetic analysis Mol. Cell 18 2005 403 412
66. R. Karimi, M.Y. Pavlov, R.H. Buckingham, and M. Ehrenberg Novel roles for classical factors at the interface between translation termination and initiation Mol. Cell 3 1999 601 609
67. H.F. Lodish Model for the regulation of mRNA translation applied to haemoglobin synthesis Nature 251 1974 385 388
68. T. Godefroy-Colburn, and R.E. Thach The role of mRNA competition in regulating translation. IV. Kinetic model J. Biol. Chem. 256 1981 11762 11773
69. T. Godefroy-Colburn, M. Ravelonandro, and L. Pinck Cap accessibility correlates with the initiation efficiency of alfalfa mosaic virus RNAs Eur. J. Biochem./FEBS 147 1985 549 552
70. T. Godefroy-Colburn, C. Thivent, and L. Pinck Translational discrimination between the four RNAs of alfalfa mosaic virus. A quantitative evaluation Eur. J. Biochem./FEBS 147 1985 541 548
71. M. Livingstone, E. Atas, A. Meller, and N. Sonenberg Mechanisms governing the control of mRNA translation Phys. Biol. 7 2010 021001
72. Y.V. Svitkin, A. Pause, A. Haghighat, S. Pyronnet, G. Witherell, G.J. Belsham, and N. Sonenberg The requirement for eukaryotic initiation factor 4A (elF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure RNA 7 2001 382 394
73. C.E. Hajdin, S. Bellaousov, W. Huggins, C.W. Leonard, D.H. Mathews, and K.M. Weeks Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots Proc. Natl. Acad. Sci. U. S. A. 110 2013 5498 5503
74. S. Aviran, C. Trapnell, J.B. Lucks, S.A. Mortimer, S. Luo, G.P. Schroth, J.A. Doudna, A.P. Arkin, and L. Pachter Modeling and automation of sequencing-based characterization of RNA structure Proc. Natl. Acad. Sci. U. S. A. 108 2011 11069 11074
75. J.B. Lucks, S.A. Mortimer, C. Trapnell, S. Luo, S. Aviran, G.P. Schroth, L. Pachter, J.A. Doudna, and A.P. Arkin Multiplexed RNA structure characterization with selective 2′-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq) Proc. Natl. Acad. Sci. U. S. A. 108 2011 11063 11068
76. M. Kertesz, Y. Wan, E. Mazor, J.L. Rinn, R.C. Nutter, H.Y. Chang, and E. Segal Genome-wide measurement of RNA secondary structure in yeast Nature 467 2010 103 107
77. J.M. Watts, K.K. Dang, R.J. Gorelick, C.W. Leonard, J.W. Bess Jr., R. Swanstrom, C.L. Burch, and K.M. Weeks Architecture and secondary structure of an entire HIV-1 RNA genome Nature 460 2009 711 716
78. D.R. Gallie The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency Genes Dev. 5 1991 2108 2116
79. A. Searfoss, T.E. Dever, and R. Wickner Linking the 3′ poly(A) tail to the subunit joining step of translation initiation: relations of Pab1p, eukaryotic translation initiation factor 5b (Fun12p), and Ski2p-Slh1p Mol. Cell. Biol. 21 2001 4900 4908
80. S.M. Tahara, M.A. Morgan, and A.J. Shatkin Two forms of purified m7G-cap binding protein with different effects on capped mRNA translation in extracts of uninfected and poliovirus-infected HeLa cells J. Biol. Chem. 256 1981 7691 7694
81. J.A. Grifo, S.M. Tahara, M.A. Morgan, A.J. Shatkin, and W.C. Merrick New initiation factor activity required for globin mRNA translation J. Biol. Chem. 258 1983 5804 5810
82. J.D. Richter, and N. Sonenberg Regulation of cap-dependent translation by eIF4E inhibitory proteins Nature 433 2005 477 480
83. M. Rau, T. Ohlmann, S.J. Morley, and V.M. Pain A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate J. Biol. Chem. 271 1996 8983 8990
84. S. Mader, H. Lee, A. Pause, and N. Sonenberg The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins Mol. Cell. Biol. 15 1995 4990 4997
85. J. Marcotrigiano, A.C. Gingras, N. Sonenberg, and S.K. Burley Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G Mol. Cell 3 1999 707 716
86. A. Bah, R.M. Vernon, Z. Siddiqui, M. Krzeminski, R. Muhandiram, C. Zhao, N. Sonenberg, L.E. Kay, and J.D. Forman-Kay Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch Nature 2014
87. A.C. Gingras, B. Raught, S.P. Gygi, A. Niedzwiecka, M. Miron, S.K. Burley, R.D. Polakiewicz, A. Wyslouch-Cieszynska, R. Aebersold, and N. Sonenberg Hierarchical phosphorylation of the translation inhibitor 4E-BP1 Genes Dev. 15 2001 2852 2864
88. C. Igreja, D. Peter, C. Weiler, and E. Izaurralde 4E-BPs require non-canonical 4E-binding motifs and a lateral surface of eIF4E to repress translation Nat. Commun. 5 2014 4790
89. S. Lukhele, A. Bah, H. Lin, N. Sonenberg, and J.D. Forman-Kay Interaction of the eukaryotic initiation factor 4E with 4E-BP2 at a dynamic bipartite interface Structure 21 2013 2186 2196
90. S.F. Mitchell, S.E. Walker, M.A. Algire, E.H. Park, A.G. Hinnebusch, and J.R. Lorsch The 5′-7-methylguanosine cap on eukaryotic mRNAs serves both to stimulate canonical translation initiation and to block an alternative pathway Mol. Cell 39 2010 950 962
91. S. Lanker, P.P. Muller, M. Altmann, C. Goyer, N. Sonenberg, and H. Trachsel Interactions of the eIF-4F subunits in the yeast Saccharomyces cerevisiae J. Biol. Chem. 267 1992 21167 21171
92. S.F. Mitchell, and R. Parker Principles and properties of eukaryotic mRNPs Mol. Cell 54 2014 547 558
93. L.E. Maquat, J. Hwang, H. Sato, and Y. Tang CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter Cold Spring Harbor. Symposia Quantitative Biol. 75 2010 127 134
94. E.M. Nelson, and M.M. Winkler Regulation of mRNA entry into polysomes. Parameters affecting polysome size and the fraction of mRNA in polysomes J. Biol. Chem. 262 1987 11501 11506
95. N. Sonenberg, M.A. Morgan, W.C. Merrick, and A.J. Shatkin A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA Proc. Natl. Acad. Sci. U. S. A. 75 1978 4843 4847
96. J. Marcotrigiano, A.C. Gingras, N. Sonenberg, and S.K. Burley Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP Cell 89 1997 951 961
97. H. Matsuo, H. Li, A.M. McGuire, C.M. Fletcher, A.C. Gingras, N. Sonenberg, and G. Wagner Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein Nat. Struct. Biol. 4 1997 717 724
98. A. Niedzwiecka, J. Marcotrigiano, J. Stepinski, M. Jankowska-Anyszka, A. Wyslouch-Cieszynska, M. Dadlez, A.C. Gingras, P. Mak, E. Darzynkiewicz, N. Sonenberg, S.K. Burley, and R. Stolarski Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins J. Mol. Biol. 319 2002 615 635
99. S.V. Slepenkov, E. Darzynkiewicz, and R.E. Rhoads Stopped-flow kinetic analysis of eIF4E and phosphorylated eIF4E binding to cap analogs and capped oligoribonucleotides: evidence for a one-step binding mechanism J. Biol. Chem. 281 2006 14927 14938
100. S.V. Slepenkov, N.L. Korneeva, and R.E. Rhoads Kinetic mechanism for assembly of the m7GpppG.eIF4E.eIF4G complex J. Biol. Chem. 283 2008 25227 25237
101. S.E. O'Leary, A. Petrov, J. Chen, and J.D. Puglisi Dynamic recognition of the mRNA cap by Saccharomyces cerevisiae eIF4E Structure 21 2013 2197 2207
102. S.E. Carberry, E. Darzynkiewicz, and D.J. Goss A comparison of the binding of methylated cap analogues to wheat germ protein synthesis initiation factors 4F and (iso)4F Biochemistry 30 1991 1624 1627
103. D.E. Friedland, W.N. Wooten, J.E. LaVoy, C.H. Hagedorn, and D.J. Goss A mutant of eukaryotic protein synthesis initiation factor eIF4E(K119A) has an increased binding affinity for both m7G cap analogues and eIF4G peptides Biochemistry 44 2005 4546 4550
104. S.E. Carberry, D.E. Friedland, R.E. Rhoads, and D.J. Goss Binding of protein synthesis initiation factor 4E to oligoribonucleotides: effects of cap accessibility and secondary structure Biochemistry 31 1992 1427 1432
105. E.H. Park, S.E. Walker, J.M. Lee, S. Rothenburg, J.R. Lorsch, and A.G. Hinnebusch Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1∗PABP mRNPs in vivo EMBO J. 30 2011 302 316
106. A. Marintchev, K.A. Edmonds, B. Marintcheva, E. Hendrickson, M. Oberer, C. Suzuki, B. Herdy, N. Sonenberg, and G. Wagner Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation Cell 136 2009 447 460
107. S.Z. Tarun Jr., and A.B. Sachs Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G EMBO J. 15 1996 7168 7177
108. S.Z. Tarun Jr., S.E. Wells, J.A. Deardorff, and A.B. Sachs Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation Proc. Natl. Acad. Sci. U. S. A. 94 1997 9046 9051
109. H. Imataka, A. Gradi, and N. Sonenberg A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation EMBO J. 17 1998 7480 7489
110. H. Le, R.L. Tanguay, M.L. Balasta, C.C. Wei, K.S. Browning, A.M. Metz, D.J. Goss, and D.R. Gallie Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity J. Biol. Chem. 272 1997 16247 16255
111. C.M. Groft, and S.K. Burley Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization Mol. Cell 9 2002 1273 1283
112. S.E. Wells, P.E. Hillner, R.D. Vale, and A.B. Sachs Circularization of mRNA by eukaryotic translation initiation factors Mol. Cell 2 1998 135 140
113. Y.M. Michel, D. Poncet, M. Piron, K.M. Kean, and A.M. Borman Cap-Poly(A) synergy in mammalian cell-free extracts. Investigation of the requirements for poly(A)-mediated stimulation of translation initiation J. Biol. Chem. 275 2000 32268 32276
114. C.C. Wei, M.L. Balasta, J. Ren, and D.J. Goss Wheat germ poly(A) binding protein enhances the binding affinity of eukaryotic initiation factor 4F and (iso)4F for cap analogues Biochemistry 37 1998 1910 1916
115. H. Le, K.S. Browning, and D.R. Gallie The phosphorylation state of poly(A)-binding protein specifies its binding to poly(A) RNA and its interaction with eukaryotic initiation factor (eIF) 4F, eIFiso4F, and eIF4B J. Biol. Chem. 275 2000 17452 17462
116. M. Gorlach, C.G. Burd, and G. Dreyfuss The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins J. Biol. Chem. 269 1994 23074 23078
117. N. Amrani, S. Ghosh, D.A. Mangus, and A. Jacobson Translation factors promote the formation of two states of the closed-loop mRNP Nature 453 2008 1276 1280
118. V. Rajagopal, E.H. Park, A.G. Hinnebusch, and J.R. Lorsch Specific domains in yeast translation initiation factor eIF4G strongly bias RNA unwinding activity of the eIF4F complex toward duplexes with 5′-overhangs J. Biol. Chem. 287 2012 20301 20312
119. G.W. Rogers Jr., N.J. Richter, W.F. Lima, and W.C. Merrick Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F J. Biol. Chem. 276 2001 30914 30922
120. P. Linder, and E. Jankowsky From unwinding to clamping - the DEAD box RNA helicase family Nat. Rev. Mol. Cell Biol. 12 2011 505 516
121. A.R. Ozes, K. Feoktistova, B.C. Avanzino, and C.S. Fraser Duplex unwinding and ATPase activities of the DEAD-box helicase eIF4A are coupled by eIF4G and eIF4B J. Mol. Biol. 412 2011 674 687
122. K.H. Nielsen, M.A. Behrens, Y. He, C.L. Oliveira, L.S. Jensen, S.V. Hoffmann, J.S. Pedersen, and G.R. Andersen Synergistic activation of eIF4A by eIF4B and eIF4G Nucleic Acids Res. 39 2011 2678 2689
123. U. Harms, A.Z. Andreou, A. Gubaev, and D. Klostermeier eIF4B, eIF4G and RNA regulate eIF4A activity in translation initiation by modulating the eIF4A conformational cycle Nucleic Acids Res. 42 2014 7911 7922
124. Y. Sun, E. Atas, L.M. Lindqvist, N. Sonenberg, J. Pelletier, and A. Meller Single-molecule kinetics of the eukaryotic initiation factor 4AI upon RNA unwinding Structure 22 2014 941 948
125. M. Hilbert, F. Kebbel, A. Gubaev, and D. Klostermeier eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism Nucleic Acids Res. 39 2011 2260 2270
126. D. Shahbazian, A. Parsyan, E. Petroulakis, J. Hershey, and N. Sonenberg eIF4B controls survival and proliferation and is regulated by proto-oncogenic signaling pathways Cell. Cycle 9 2010 4106 4109
127. K. Feoktistova, E. Tuvshintogs, A. Do, and C.S. Fraser Human eIF4E promotes mRNA restructuring by stimulating eIF4A helicase activity Proc. Natl. Acad. Sci. U. S. A. 110 2013 13339 13344
128. M. Bushell, W. Wood, G. Carpenter, V.M. Pain, S.J. Morley, and M.J. Clemens Disruption of the interaction of mammalian protein synthesis eukaryotic initiation factor 4B with the poly(A)-binding protein by caspase- and viral protease-mediated cleavages J. Biol. Chem. 276 2001 23922 23928
129. M.E. Fairman, P.A. Maroney, W. Wang, H.A. Bowers, P. Gollnick, T.W. Nilsen, and E. Jankowsky Protein displacement by DExH/D "RNA helicases" without duplex unwinding Science 304 2004 730 734
130. J.R. Babendure, J.L. Babendure, J.H. Ding, and R.Y. Tsien Control of mammalian translation by mRNA structure near caps RNA 12 2006 851 861
131. N.M. Kaye, K.J. Emmett, W.C. Merrick, and E. Jankowsky Intrinsic RNA binding by the eukaryotic initiation factor 4F depends on a minimal RNA length but not on the m7G cap J. Biol. Chem. 284 2009 17742 17750
132. M. Kozak, and A.J. Shatkin Migration of 40 S ribosomal subunits on messenger RNA in the presence of edeine J. Biol. Chem. 253 1978 6568 6577
133. A.V. Pisarev, V.G. Kolupaeva, M.M. Yusupov, C.U. Hellen, and T.V. Pestova Ribosomal position and contacts of mRNA in eukaryotic translation initiation complexes EMBO J. 27 2008 1609 1621
134. G. Pesole, F. Mignone, C. Gissi, G. Grillo, F. Licciulli, and S. Liuni Structural and functional features of eukaryotic mRNA untranslated regions Gene 276 2001 73 81
135. M. Muckenthaler, N.K. Gray, and M.W. Hentze IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F Mol. Cell 2 1998 383 388
136. J. Ma, S. Haldar, M.A. Khan, S.D. Sharma, W.C. Merrick, E.C. Theil, and D.J. Goss Fe2+ binds iron responsive element-RNA, selectively changing protein-binding affinities and regulating mRNA repression and activation Proc. Natl. Acad. Sci. U. S. A. 109 2012 8417 8422
137. N. Villa, A. Do, J.W. Hershey, and C.S. Fraser Human eukaryotic initiation factor 4G (eIF4G) protein binds to eIF3c, -d, and -e to promote mRNA recruitment to the ribosome J. Biol. Chem. 288 2013 32932 32940
138. T.M. Hinton, M.J. Coldwell, G.A. Carpenter, S.J. Morley, and V.M. Pain Functional analysis of individual binding activities of the scaffold protein eIF4G J. Biol. Chem. 282 2007 1695 1708
139. C.C. Thoreen, L. Chantranupong, H.R. Keys, T. Wang, N.S. Gray, and D.M. Sabatini A unifying model for mTORC1-mediated regulation of mRNA translation Nature 485 2012 109 113
140. T.E. Harris, A. Chi, J. Shabanowitz, D.F. Hunt, R.E. Rhoads, and J.C. Lawrence Jr. mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin EMBO J. 25 2006 1659 1668
141. K. Asano, A. Shalev, L. Phan, K. Nielsen, J. Clayton, L. Valasek, T.F. Donahue, and A.G. Hinnebusch Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation EMBO J. 20 2001 2326 2337
142. S.E. Walker, F. Zhou, S.F. Mitchell, V.S. Larson, L. Valasek, A.G. Hinnebusch, and J.R. Lorsch Yeast eIF4B binds to the head of the 40S ribosomal subunit and promotes mRNA recruitment through its N-terminal and internal repeat domains RNA 19 2013 191 207
143. R. Majumdar, A. Bandyopadhyay, and U. Maitra Mammalian translation initiation factor eIF1 functions with eIF1A and eIF3 in the formation of a stable 40 S preinitiation complex J. Biol. Chem. 278 2003 6580 6587
144. J. Chaudhuri, D. Chowdhury, and U. Maitra Distinct functions of eukaryotic translation initiation factors eIF1A and eIF3 in the formation of the 40 S ribosomal preinitiation complex J. Biol. Chem. 274 1999 17975 17980
145. H. Trachsel, B. Erni, M.H. Schreier, and T. Staehelin Initiation of mammalian protein synthesis. II. The assembly of the initiation complex with purified initiation factors J. Mol. Biol. 116 1977 755 767
146. V.G. Kolupaeva, A. Unbehaun, I.B. Lomakin, C.U. Hellen, and T.V. Pestova Binding of eukaryotic initiation factor 3 to ribosomal 40S subunits and its role in ribosomal dissociation and anti-association RNA 11 2005 470 486
147. W.L. Chiu, S. Wagner, A. Herrmannova, L. Burela, F. Zhang, A.K. Saini, L. Valasek, and A.G. Hinnebusch The C-terminal region of eukaryotic translation initiation factor 3a (eIF3a) promotes mRNA recruitment, scanning, and, together with eIF3j and the eIF3b RNA recognition motif, selection of AUG start codons Mol. Cell. Biol. 30 2010 4415 4434
148. A.V. Jivotovskaya, L. Valasek, A.G. Hinnebusch, and K.H. Nielsen Eukaryotic translation initiation factor 3 (eIF3) and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast Mol. Cell. Biol. 26 2006 1355 1372
149. M.A. Algire, D. Maag, P. Savio, M.G. Acker, S.Z. Tarun Jr., A.B. Sachs, K. Asano, K.H. Nielsen, D.S. Olsen, L. Phan, A.G. Hinnebusch, and J.R. Lorsch Development and characterization of a reconstituted yeast translation initiation system RNA 8 2002 382 397
150. A.G. Hinnebusch Translational regulation of GCN4 and the general amino acid control of yeast Annu. Rev. Microbiol. 59 2005 407 450
151. L.R. Palam, T.D. Baird, and R.C. Wek Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation J. Biol. Chem. 286 2011 10939 10949
152. M.C. Dasso, S.C. Milburn, J.W. Hershey, and R.J. Jackson Selection of the 5′-proximal translation initiation site is influenced by mRNA and eIF-2 concentrations Eur. J. Biochem./FEBS 187 1990 361 371
153. A.Z. Andreou, and D. Klostermeier eIF4B and eIF4G jointly stimulate eIF4A ATPase and unwinding activities by modulation of the eIF4A conformational cycle J. Mol. Biol. 426 2014 51 61
154. X. Bi, J. Ren, and D.J. Goss Wheat germ translation initiation factor eIF4B affects eIF4A and eIFiso4F helicase activity by increasing the ATP binding affinity of eIF4A Biochemistry 39 2000 5758 5765
155. E.H. Park, S.E. Walker, F. Zhou, J.M. Lee, V. Rajagopal, J.R. Lorsch, and A.G. Hinnebusch Yeast eukaryotic initiation factor 4B (eIF4B) enhances complex assembly between eIF4A and eIF4G in vivo J. Biol. Chem. 288 2013 2340 2354
156. A.S. Spirin How does a scanning ribosomal particle move along the 5′-untranslated region of eukaryotic mRNA? Brownian Ratchet model Biochemistry 48 2009 10688 10692
157. F. Zhou, S.E. Walker, S.F. Mitchell, J.R. Lorsch, and A.G. Hinnebusch Identification and characterization of functionally critical, conserved motifs in the internal repeats and N-terminal domain of yeast translation initiation factor 4B (yeIF4B) J. Biol. Chem. 289 2014 1704 1722
158. H.S. Park, K.S. Browning, T. Hohn, and L.A. Ryabova Eucaryotic initiation factor 4B controls eIF3-mediated ribosomal entry of viral reinitiation factor EMBO J. 23 2004 1381 1391
159. N. Methot, M.S. Song, and N. Sonenberg A region rich in aspartic acid, arginine, tyrosine, and glycine (DRYG) mediates eukaryotic initiation factor 4B (eIF4B) self-association and interaction with eIF3 Mol. Cell. Biol. 16 1996 5328 5334
160. B. Raught, F. Peiretti, A.C. Gingras, M. Livingstone, D. Shahbazian, G.L. Mayeur, R.D. Polakiewicz, N. Sonenberg, and J.W. Hershey Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases EMBO J. 23 2004 1761 1769
161. M.K. Holz, B.A. Ballif, S.P. Gygi, and J. Blenis mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events Cell 123 2005 569 580
162. D. Shahbazian, P.P. Roux, V. Mieulet, M.S. Cohen, B. Raught, J. Taunton, J.W. Hershey, J. Blenis, M. Pende, and N. Sonenberg The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity EMBO J. 25 2006 2781 2791
163. L.I. Shagam, I.M. Terenin, D.E. Andreev, J.E. Dunaevsky, and S.E. Dmitriev In vitro activity of human translation initiation factor eIF4B is not affected by phosphomimetic amino acid substitutions S422D and S422E Biochimie 94 2012 2484 2490
164. N.J. Richter-Cook, T.E. Dever, J.O. Hensold, and W.C. Merrick Purification and characterization of a new eukaryotic protein translation factor. Eukaryotic initiation factor 4H J. Biol. Chem. 273 1998 7579 7587
165. N.J. Richter, G.W. Rogers Jr., J.O. Hensold, and W.C. Merrick Further biochemical and kinetic characterization of human eukaryotic initiation factor 4H J. Biol. Chem. 274 1999 35415 35424
166. A. Parsyan, Y. Svitkin, D. Shahbazian, C. Gkogkas, P. Lasko, W.C. Merrick, and N. Sonenberg mRNA helicases: the tacticians of translational control Nat. Rev. Mol. Cell Biol. 12 2011 235 245
167. M. Kozak Evaluation of the "scanning model" for initiation of protein synthesis in eucaryotes Cell 22 1980 7 8
168. T.V. Pestova, and V.G. Kolupaeva The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection Genes Dev. 16 2002 2906 2922
169. R. Soto-Rifo, P.S. Rubilar, T. Limousin, S. de Breyne, D. Decimo, and T. Ohlmann DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs EMBO J. 31 2012 3745 3756
170. A. Hilliker, Z. Gao, E. Jankowsky, and R. Parker The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex Mol. Cell 43 2011 962 972
171. V.P. Pisareva, A.V. Pisarev, A.A. Komar, C.U. Hellen, and T.V. Pestova Translation initiation on mammalian mRNAs with structured 5′UTRs requires DExH-box protein DHX29 Cell 135 2008 1237 1250
172. A. Parsyan, D. Shahbazian, Y. Martineau, E. Petroulakis, T. Alain, O. Larsson, G. Mathonnet, G. Tettweiler, C.U. Hellen, T.V. Pestova, Y.V. Svitkin, and N. Sonenberg The helicase protein DHX29 promotes translation initiation, cell proliferation, and tumorigenesis Proc. Natl. Acad. Sci. U. S. A. 106 2009 22217 22222
173. N.T. Ingolia, L.F. Lareau, and J.S. Weissman Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes Cell 147 2011 789 802
174. M.A. Algire, D. Maag, and J.R. Lorsch Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation Mol. Cell 20 2005 251 262
175. P. Milon, and M.V. Rodnina Kinetic control of translation initiation in bacteria Crit. Rev. Biochem. Mol. Biol. 47 2012 334 348
176. L. Zhang, X. Pan, and J.W. Hershey Individual overexpression of five subunits of human translation initiation factor eIF3 promotes malignant transformation of immortal fibroblast cells J. Biol. Chem. 282 2007 5790 5800
177. P. Schutz, M. Bumann, A.E. Oberholzer, C. Bieniossek, H. Trachsel, M. Altmann, and U. Baumann Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions Proc. Natl. Acad. Sci. U. S. A. 105 2008 9564 9569
178. C.B. Andersen, L. Ballut, J.S. Johansen, H. Chamieh, K.H. Nielsen, C.L. Oliveira, J.S. Pedersen, B. Seraphin, H. Le Hir, and G.R. Andersen Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA Science 313 2006 1968 1972
179. J.D. Gross, N.J. Moerke, T. von der Haar, A.A. Lugovskoy, A.B. Sachs, J.E. McCarthy, and G. Wagner Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E Cell 115 2003 739 750
180. L. Bellsolell, P.F. Cho-Park, F. Poulin, N. Sonenberg, and S.K. Burley Two structurally atypical HEAT domains in the c-terminal portion of human eIF4G support binding to eIF4A and Mnk1 Structure 14 2006 913 923
181. N. Safaee, G. Kozlov, A.M. Noronha, J. Xie, C.J. Wilds, and K. Gehring Interdomain allostery promotes assembly of the poly(A) mRNA complex with PABP and eIF4G Mol. Cell 48 2012 375 386