1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biochemistry
  4. Volume 88, 2019
  5. Article

Annual Review of Biochemistry

Volume 88, 2019

The Organizing Principles of Eukaryotic Ribosome Recruitment

Abstract

The stage at which ribosomes are recruited to messenger RNAs (mRNAs) is an elaborate and highly regulated phase of protein synthesis. Upon completion of this step, a ribosome is positioned at an appropriate initiation codon and primed to synthesize the encoded polypeptide product. In most circumstances, this step commits the ribosome to translate the mRNA. We summarize the knowledge regarding the initiation factors implicated in this activity as well as review different mechanisms by which this process is conducted.

Keyword(s): eIF4A, eIF4B, eIF4E, eIF4F, eIF4G, eIF4H, eukaryotic initiation factors, ribosome recruitment, translation
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-013118-111042
2019-06-20
2025-04-26
Loading full text...

Full text loading...

/deliver/fulltext/biochem/88/1/annurev-biochem-013118-111042.html?itemId=/content/journals/10.1146/annurev-biochem-013118-111042&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Sonenberg N, Morgan MA, Merrick WC, Shatkin AJ 1978. A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA. PNAS 75:4843–47
     [Google Scholar]
  2. 2. 
    Altmann M, Handschin C, Trachsel H 1987. mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae. Mol. Cell. Biol 7:998–1003
     [Google Scholar]
  3. 3. 
    Truitt ML, Conn CS, Shi Z, Pang X, Tokuyasu T et al. 2015. Differential requirements for eIF4E dose in normal development and cancer. Cell 162:59–71
     [Google Scholar]
  4. 4. 
    Altmann M, Muller PP, Pelletier J, Sonenberg N, Trachsel H 1989. A mammalian translation initiation factor can substitute for its yeast homologue in vivo. J. Biol. Chem. 264:12145–47
     [Google Scholar]
  5. 5. 
    Kulak NA, Pichler G, Paron I, Nagaraj N, Mann M 2014. Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat. Methods 11:319–24
     [Google Scholar]
  6. 6. 
    Lazaris-Karatzas A, Montine KS, Sonenberg N 1990. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature 345:544–47
     [Google Scholar]
  7. 7. 
    Wendel HG, de Stanchina E, Fridman JS, Malina A, Ray S et al. 2004. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428:332–37
     [Google Scholar]
  8. 8. 
    Rousseau D, Kaspar R, Rosenwald I, Gehrke L, Sonenberg N 1996. Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. PNAS 93:1065–70
     [Google Scholar]
  9. 9. 
    Ilic N, Utermark T, Widlund HR, Roberts TM 2011. PI3K-targeted therapy can be evaded by gene amplification along the MYC-eukaryotic translation initiation factor 4E (eIF4E) axis. PNAS 108:E699–708
     [Google Scholar]
  10. 10. 
    Bhat M, Robichaud N, Hulea L, Sonenberg N, Pelletier J, Topisirovic I 2015. Targeting the translation machinery in cancer. Nat. Rev. Drug Discov. 14:261–78
     [Google Scholar]
  11. 11. 
    Lin CJ, Cencic R, Mills JR, Robert F, Pelletier J 2008. c-Myc and eIF4F are components of a feedforward loop that links transcription and translation. Cancer Res 68:5326–34
     [Google Scholar]
  12. 12. 
    Schmidt EV. 2004. The role of c-myc in regulation of translation initiation. Oncogene 23:3217–21
     [Google Scholar]
  13. 13. 
    Lin CJ, Nasr Z, Premsrirut PK, Porco JA Jr, Hippo Y et al. 2012. Targeting synthetic lethal interactions between Myc and the eIF4F complex impedes tumorigenesis. Cell Rep 1:325–33
     [Google Scholar]
  14. 14. 
    Gkogkas CG, Khoutorsky A, Ran I, Rampakakis E, Nevarko T et al. 2013. Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 493:371–77
     [Google Scholar]
  15. 15. 
    Neves-Pereira M, Muller B, Massie D, Williams JH, O'Brien PC et al. 2009. Deregulation of EIF4E: a novel mechanism for autism. J. Med. Genet. 46:759–65
     [Google Scholar]
  16. 16. 
    Aguilar-Valles A, Haji N, De Gregorio D, Matta-Camacho E, Eslamizade MJ et al. 2018. Translational control of depression-like behavior via phosphorylation of eukaryotic translation initiation factor 4E. Nat. Commun. 9:2459
     [Google Scholar]
  17. 17. 
    Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK 1997. Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89:951–61
     [Google Scholar]
  18. 18. 
    Matsuo H, Li H, McGuire AM, Fletcher CM, Gingras AC et al. 1997. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat. Struct. Biol. 4:717–24
     [Google Scholar]
  19. 19. 
    Darzynkiewicz E, Ekiel I, Lassota P, Tahara SM 1987. Inhibition of eukaryotic translation by analogues of messenger RNA 5′-cap: chemical and biological consequences of 5′-phosphate modifications of 7-methylguanosine 5′-monophosphate. Biochemistry 26:4372–80
     [Google Scholar]
  20. 20. 
    Chen X, Kopecky DJ, Mihalic J, Jeffries S, Min X et al. 2012. Structure-guided design, synthesis, and evaluation of guanine-derived inhibitors of the eIF4E mRNA-cap interaction. J. Med. Chem. 55:3837–51
     [Google Scholar]
  21. 21. 
    Brown CJ, McNae I, Fischer PM, Walkinshaw MD 2007. Crystallographic and mass spectrometric characterisation of eIF4E with N7-alkylated cap derivatives. J. Mol. Biol. 372:7–15
     [Google Scholar]
  22. 22. 
    Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA et al. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371:762–67
     [Google Scholar]
  23. 23. 
    Peter D, Igreja C, Weber R, Wohlbold L, Weiler C et al. 2015. Molecular architecture of 4E-BP translational inhibitors bound to eIF4E. Mol. Cell 57:1074–87
     [Google Scholar]
  24. 24. 
    Igreja C, Peter D, Weiler C, Izaurralde E 2014. 4E-BPs require non-canonical 4E-binding motifs and a lateral surface of eIF4E to repress translation. Nat. Commun. 5:4790
     [Google Scholar]
  25. 25. 
    Lukhele S, Bah A, Lin H, Sonenberg N, Forman-Kay JD 2013. Interaction of the eukaryotic initiation factor 4E with 4E-BP2 at a dynamic bipartite interface. Structure 21:2186–96
     [Google Scholar]
  26. 26. 
    Merrick WC, Pavitt GD. 2018. Protein synthesis initiation in eukaryotic cells. Translation Mechanisms and Control MB Mathews, N Sonenberg, JW Hershey Cold Spring Harbor, NY: Cold Spring Harb. Lab.
     [Google Scholar]
  27. 27. 
    Rhoads RE. 2009. eIF4E: new family members, new binding partners, new roles. J. Biol. Chem. 284:16711–15
     [Google Scholar]
  28. 28. 
    Kinkelin K, Veith K, Grunwald M, Bono F 2012. Crystal structure of a minimal eIF4E−Cup complex reveals a general mechanism of eIF4E regulation in translational repression. RNA 18:1624–34
     [Google Scholar]
  29. 29. 
    Napoli I, Mercaldo V, Boyl PP, Eleuteri B, Zalfa F et al. 2008. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134:1042–54
     [Google Scholar]
  30. 30. 
    Pacheco A, Lopez de Quinto S, Ramajo J, Fernandez N, Martinez-Salas E 2009. A novel role for Gemin5 in mRNA translation. Nucleic Acids Res 37:582–90
     [Google Scholar]
  31. 31. 
    Dostie J, Ferraiuolo M, Pause A, Adam SA, Sonenberg N 2000. A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5′ cap-binding protein, eIF4E. EMBO J 19:3142–56
     [Google Scholar]
  32. 32. 
    Nishimura T, Padamsi Z, Fakim H, Milette S, Dunham WH et al. 2015. The eIF4E-binding protein 4E-T is a component of the mRNA decay machinery that bridges the 5′ and 3′ termini of target mRNAs. Cell Rep 11:1425–36
     [Google Scholar]
  33. 33. 
    Gosselin P, Martineau Y, Morales J, Czjzek M, Glippa V et al. 2013. Tracking a refined eIF4E-binding motif reveals Angel1 as a new partner of eIF4E. Nucleic Acids Res 41:7783–92
     [Google Scholar]
  34. 34. 
    Joshi B, Cameron A, Jagus R 2004. Characterization of mammalian eIF4E-family members. Eur. J. Biochem. 271:2189–203
     [Google Scholar]
  35. 35. 
    Rosettani P, Knapp S, Vismara MG, Rusconi L, Cameron AD 2007. Structures of the human eIF4E homologous protein, h4EHP, in its m7GTP-bound and unliganded forms. J. Mol. Biol. 368:691–705
     [Google Scholar]
  36. 36. 
    Zuberek J, Kubacka D, Jablonowska A, Jemielity J, Stepinski J et al. 2007. Weak binding affinity of human 4EHP for mRNA cap analogs. RNA 13:691–97
     [Google Scholar]
  37. 37. 
    Cho PF, Poulin F, Cho-Park YA, Cho-Park IB, Chicoine JD et al. 2005. A new paradigm for translational control: inhibition via 5′-3′ mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121:411–23
     [Google Scholar]
  38. 38. 
    Morita M, Ler LW, Fabian MR, Siddiqui N, Mullin M et al. 2012. A novel 4EHP-GIGYF2 translational repressor complex is essential for mammalian development. Mol. Cell. Biol. 32:3585–93
     [Google Scholar]
  39. 39. 
    Chapat C, Jafarnejad SM, Matta-Camacho E, Hesketh GG, Gelbart IA et al. 2017. Cap-binding protein 4EHP effects translation silencing by microRNAs. PNAS 114:5425–30
     [Google Scholar]
  40. 40. 
    Osborne MJ, Volpon L, Kornblatt JA, Culjkovic-Kraljacic B, Baguet A, Borden KLB 2013. eIF4E3 acts as a tumor suppressor by utilizing an atypical mode of methyl-7-guanosine cap recognition. PNAS 110:3877–82
     [Google Scholar]
  41. 41. 
    Byrd MP, Zamora M, Lloyd RE 2005. Translation of eukaryotic translation initiation factor 4GI (eIF4GI) proceeds from multiple mRNAs containing a novel cap-dependent internal ribosome entry site (IRES) that is active during poliovirus infection. J. Biol. Chem. 280:18610–22
     [Google Scholar]
  42. 42. 
    Byrd MP, Zamora M, Lloyd RE 2002. Generation of multiple isoforms of eukaryotic translation initiation factor 4GI by use of alternate translation initiation codons. Mol. Cell. Biol. 22:4499–511
     [Google Scholar]
  43. 43. 
    Coldwell MJ, Sack U, Cowan JL, Barrett RM, Vlasak M et al. 2012. Multiple isoforms of the translation initiation factor eIF4GII are generated via use of alternative promoters, splice sites and a non-canonical initiation codon. Biochem. J. 448:1–11
     [Google Scholar]
  44. 44. 
    Sun F, Palmer K, Handel MA 2010. Mutation of Eif4g3, encoding a eukaryotic translation initiation factor, causes male infertility and meiotic arrest of mouse spermatocytes. Development 137:1699–707
     [Google Scholar]
  45. 45. 
    Gray NK, Hrabalkova L, Scanlon JP, Smith RW 2015. Poly(A)-binding proteins and mRNA localization: Who rules the roost. ? Biochem. Soc. Trans. 43:1277–84
     [Google Scholar]
  46. 46. 
    Gallie DR. 1991. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev 5:2108–16
     [Google Scholar]
  47. 47. 
    Adivarahan S, Livingston N, Nicholson B, Rahman S, Wu B et al. 2018. Spatial organization of single mRNPs at different stages of the gene expression pathway. Mol. Cell 72:727–38.e5
     [Google Scholar]
  48. 48. 
    Khong A, Parker R. 2018. mRNP architecture in translating and stress conditions reveals an ordered pathway of mRNP compaction. J. Cell Biol. 217:412440
     [Google Scholar]
  49. 49. 
    Khaleghpour K, Kahvejian A, De Crescenzo G, Roy G, Svitkin YV et al. 2001. Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol. Cell. Biol. 21:5200–13
     [Google Scholar]
  50. 50. 
    Svitkin YV, Imataka H, Khaleghpour K, Kahvejian A, Liebig HD, Sonenberg N 2001. Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation. RNA 7:1743–52
     [Google Scholar]
  51. 51. 
    Michel YM, Borman AM, Paulous S, Kean KM 2001. Eukaryotic initiation factor 4G-poly(A) binding protein interaction is required for poly(A) tail-mediated stimulation of picornavirus internal ribosome entry segment-driven translation but not for X-mediated stimulation of hepatitis C virus translation. Mol. Cell. Biol. 21:4097–109
     [Google Scholar]
  52. 52. 
    Cakmakci NG, Lerner RS, Wagner EJ, Zheng L, Marzluff WF 2008. SLIP1, a factor required for activation of histone mRNA translation by the stem-loop binding protein. Mol. Cell. Biol. 28:1182–94
     [Google Scholar]
  53. 53. 
    von Moeller H, Lerner R, Ricciardi A, Basquin C, Marzluff WF, Conti E 2013. Structural and biochemical studies of SLIP1-SLBP identify DBP5 and eIF3g as SLIP1-binding proteins. Nucleic Acids Res 41:7960–71
     [Google Scholar]
  54. 54. 
    Piron M, Vende P, Cohen J, Poncet D 1998. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J 17:5811–21
     [Google Scholar]
  55. 55. 
    Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK 1999. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol. Cell 3:707–16
     [Google Scholar]
  56. 56. 
    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 115:739–50
     [Google Scholar]
  57. 57. 
    Gruner S, Peter D, Weber R, Wohlbold L, Chung MY et al. 2016. The structures of eIF4E-eIF4G complexes reveal an extended interface to regulate translation initiation. Mol. Cell 64:467–79
     [Google Scholar]
  58. 58. 
    Miras M, Truniger V, Silva C, Verdaguer N, Aranda MA, Querol-Audi J 2017. Structure of eIF4E in complex with an eIF4G peptide supports a universal bipartite binding mode for protein translation. Plant Physiol 174:1476–91
     [Google Scholar]
  59. 59. 
    Schalm SS, Fingar DC, Sabatini DM, Blenis J 2003. TOS motif-mediated raptor binding regulates 4E-BP1 multisite phosphorylation and function. Curr. Biol. 13:797–806
     [Google Scholar]
  60. 60. 
    Brunn GJ, Fadden P, Haystead TA, Lawrence JC Jr 1997. The mammalian target of rapamycin phosphorylates sites having a (Ser/Thr)-Pro motif and is activated by antibodies to a region near its COOH terminus. J. Biol. Chem. 272:32547–50
     [Google Scholar]
  61. 61. 
    Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT et al. 1999. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13:1422–37
     [Google Scholar]
  62. 62. 
    Gingras AC, Raught B, Gygi SP, Niedzwiecka A, Miron M et al. 2001. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 15:2852–64
     [Google Scholar]
  63. 63. 
    Bah A, Vernon RM, Siddiqui Z, Krzeminski M, Muhandiram R et al. 2015. Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch. Nature 519:106–9
     [Google Scholar]
  64. 64. 
    Yanagiya A, Suyama E, Adachi H, Svitkin YV, Aza-Blanc P et al. 2012. Translational homeostasis via the mRNA cap-binding protein, eIF4E. Mol. Cell 46:847–58
     [Google Scholar]
  65. 65. 
    Imataka H, Sonenberg N. 1997. Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Mol. Cell. Biol. 17:6940–47
     [Google Scholar]
  66. 66. 
    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 136:447–60
     [Google Scholar]
  67. 67. 
    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. PNAS 105:9564–69
     [Google Scholar]
  68. 68. 
    Dominguez D, Altmann M, Benz J, Baumann U, Trachsel H 1999. Interaction of translation initiation factor eIF4G with eIF4A in the yeast Saccharomyces cerevisiae. J. Biol. Chem 274:26720–26
     [Google Scholar]
  69. 69. 
    Korneeva NL, First EA, Benoit CA, Rhoads RE 2005. Interaction between the NH2-terminal domain of eIF4A and the central domain of eIF4G modulates RNA-stimulated ATPase activity. J. Biol. Chem. 280:1872–81
     [Google Scholar]
  70. 70. 
    Hilbert M, Kebbel F, Gubaev A, Klostermeier D 2011. eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Res 39:2260–70
     [Google Scholar]
  71. 71. 
    Villa N, Do A, Hershey JW, Fraser CS 2013. Human eukaryotic initiation factor 4G (eIF4G) protein binds to eIF3c, -d, and -e to promote mRNA recruitment to the ribosome. J. Biol. Chem. 288:32932–40
     [Google Scholar]
  72. 72. 
    Harris TE, Chi A, Shabanowitz J, Hunt DF, Rhoads RE, Lawrence JC Jr 2006. mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin. EMBO J 25:1659–68
     [Google Scholar]
  73. 73. 
    LeFebvre AK, Korneeva NL, Trutschl M, Cvek U, Duzan RD et al. 2006. Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J. Biol. Chem. 281:22917–32
     [Google Scholar]
  74. 74. 
    Marcotrigiano J, Lomakin IB, Sonenberg N, Pestova TV, Hellen CU, Burley SK 2001. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol. Cell 7:193–203
     [Google Scholar]
  75. 75. 
    Yanagiya A, Svitkin YV, Shibata S, Mikami S, Imataka H, Sonenberg N 2009. Requirement of RNA binding of mammalian eukaryotic translation initiation factor 4GI (eIF4GI) for efficient interaction of eIF4E with the mRNA cap. Mol. Cell. Biol. 29:1661–69
     [Google Scholar]
  76. 76. 
    Park EH, Walker SE, Lee JM, Rothenburg S, Lorsch JR, Hinnebusch AG 2011. Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1ċPABP mRNPs in vivo. . EMBO J 30:302–16
     [Google Scholar]
  77. 77. 
    Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA 1999. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19:1871–80
     [Google Scholar]
  78. 78. 
    Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N 1999. Human eukaryotic translation initiation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E. EMBO J 18:270–79
     [Google Scholar]
  79. 79. 
    Furic L, Rong L, Larsson O, Koumakpayi IH, Yoshida K et al. 2010. eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. PNAS 107:14134–39
     [Google Scholar]
  80. 80. 
    Scheper GC, van Kollenburg B, Hu J, Luo Y, Goss DJ, Proud CG 2002. Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J. Biol. Chem. 277:3303–9
     [Google Scholar]
  81. 81. 
    Zuberek J, Jemielity J, Jablonowska A, Stepinski J, Dadlez M et al. 2004. Influence of electric charge variation at residues 209 and 159 on the interaction of eIF4E with the mRNA 5′ terminus. Biochemistry 43:5370–79
     [Google Scholar]
  82. 82. 
    Ueda T, Sasaki M, Elia AJ, Chio II, Hamada K et al. 2010. Combined deficiency for MAP kinase-interacting kinase 1 and 2 (Mnk1 and Mnk2) delays tumor development. PNAS 107:13984–90
     [Google Scholar]
  83. 83. 
    Topisirovic I, Ruiz-Gutierrez M, Borden KLB 2004. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res 64:8639–42
     [Google Scholar]
  84. 84. 
    Wendel HG, Silva RL, Malina A, Mills JR, Zhu H et al. 2007. Dissecting eIF4E action in tumorigenesis. Genes Dev 21:3232–37
     [Google Scholar]
  85. 85. 
    Robichaud N, Hsu BE, Istomine R, Alvarez F, Blagih J et al. 2018. Translational control in the tumor microenvironment promotes lung metastasis: phosphorylation of eIF4E in neutrophils. PNAS 115:E2202–9
     [Google Scholar]
  86. 86. 
    Cuesta R, Xi Q, Schneider RJ 2004. Structural basis for competitive inhibition of eIF4G-Mnk1 interaction by the adenovirus 100-kilodalton protein. J. Virol. 78:7707–16
     [Google Scholar]
  87. 87. 
    Juillard F, Bazot Q, Mure F, Tafforeau L, Macri C et al. 2012. Epstein-Barr virus protein EB2 stimulates cytoplasmic mRNA accumulation by counteracting the deleterious effects of SRp20 on viral mRNAs. Nucleic Acids Res 40:6834–49
     [Google Scholar]
  88. 88. 
    Burgui I, Aragon T, Ortin J, Nieto A 2003. PABP1 and eIF4GI associate with influenza virus NS1 protein in viral mRNA translation initiation complexes. J. Gen. Virol. 84:3263–74
     [Google Scholar]
  89. 89. 
    Castelló A, Álvarez E, Carrasco L 2011. The multifaceted poliovirus 2A protease: regulation of gene expression by picornavirus proteases. J. Biomed. Biotechnol. 2011:369648
     [Google Scholar]
  90. 90. 
    Levy-Strumpf N, Deiss LP, Berissi H, Kimchi A 1997. DAP-5, a novel homolog of eukaryotic translation initiation factor 4G isolated as a putative modulator of gamma interferon-induced programmed cell death. Mol. Cell. Biol. 17:1615–25
     [Google Scholar]
  91. 91. 
    Imataka H, Olsen HS, Sonenberg N 1997. A new translational regulator with homology to eukaryotic translation initiation factor 4G. EMBO J 16:817–25
     [Google Scholar]
  92. 92. 
    Yamanaka S, Poksay KS, Arnold KS, Innerarity TL 1997. A novel translational repressor mRNA is edited extensively in livers containing tumors caused by the transgene expression of the apoB mRNA-editing enzyme. Genes Dev 11:321–33
     [Google Scholar]
  93. 93. 
    Liberman N, Gandin V, Svitkin YV, David M, Virgili G et al. 2015. DAP5 associates with eIF2β and eIF4AI to promote Internal Ribosome Entry Site driven translation. Nucleic Acids Res 43:3764–75
     [Google Scholar]
  94. 94. 
    Liberman N, Marash L, Kimchi A 2009. The translation initiation factor DAP5 is a regulator of cell survival during mitosis. Cell Cycle 8:204–9
     [Google Scholar]
  95. 95. 
    Yamanaka S, Zhang XY, Maeda M, Miura K, Wang S et al. 2000. Essential role of NAT1/p97/DAP5 in embryonic differentiation and the retinoic acid pathway. EMBO J 19:5533–41
     [Google Scholar]
  96. 96. 
    Yoffe Y, David M, Kalaora R, Povodovski L, Friedlander G et al. 2016. Cap-independent translation by DAP5 controls cell fate decisions in human embryonic stem cells. Genes Dev 30:1991–2004
     [Google Scholar]
  97. 97. 
    Sugiyama H, Takahashi K, Yamamoto T, Iwasaki M, Narita M et al. 2017. Nat1 promotes translation of specific proteins that induce differentiation of mouse embryonic stem cells. PNAS 114:340–45
     [Google Scholar]
  98. 98. 
    Galicia-Vázquez G, Cencic R, Robert F, Agenor AQ, Pelletier J 2012. A cellular response linking eIF4AI activity to eIF4AII transcription. RNA 18:1373–84
     [Google Scholar]
  99. 99. 
    Nielsen PJ, McMaster GK, Trachsel H 1985. Cloning of eukaryotic protein synthesis initiation factor genes: isolation and characterization of cDNA clones encoding factor eIF-4A. Nucleic Acids Res 13:6867–80
     [Google Scholar]
  100. 100. 
    Conroy SC, Dever TE, Owens CL, Merrick WC 1990. Characterization of the 46,000-Dalton subunit of eIF-4F. Arch. Biochem. Biophys. 282:363–71
     [Google Scholar]
  101. 101. 
    Williams-Hill DM, Duncan RF, Nielsen PJ, Tahara SM 1997. Differential expression of the murine eukaryotic translation initiation factor isogenes eIF4AI and eIF4AII is dependent upon cellular growth status. Arch. Biochem. Biophys. 338:111–20
     [Google Scholar]
  102. 102. 
    Li W, Ross-Smith N, Proud CG, Belsham GJ 2001. Cleavage of translation initiation factor 4AI (eIF4AI) but not eIF4AII by foot-and-mouth disease virus 3C protease: identification of the eIF4AI cleavage site. FEBS Lett 507: https://doi.org/10.1016/S0014-5793(01)02885-X
    [Crossref] [Google Scholar]
  103. 103. 
    Galicia-Vázquez G, Chu J, Pelletier J 2015. eIF4AII is dispensable for miRNA-mediated gene silencing. RNA 21:1826–33
     [Google Scholar]
  104. 104. 
    Caruthers JM, Johnson ER, McKay DB 2000. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. PNAS 97:13080–85
     [Google Scholar]
  105. 105. 
    Chang JH, Cho YH, Sohn SY, Choi JM, Kim A et al. 2009. Crystal structure of the eIF4A-PDCD4 complex. PNAS 106:3148–53
     [Google Scholar]
  106. 106. 
    Loh PG, Yang HS, Walsh MA, Wang Q, Wang X et al. 2009. Structural basis for translational inhibition by the tumour suppressor Pdcd4. EMBO J 28:274–85
     [Google Scholar]
  107. 107. 
    Johnson ER, McKay DB. 1999. Crystallographic structure of the amino terminal domain of yeast initiation factor 4A, a representative DEAD-box RNA helicase. RNA 5:1526–34
     [Google Scholar]
  108. 108. 
    Oberer M, Marintchev A, Wagner G 2005. Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev 19:2212–23
     [Google Scholar]
  109. 109. 
    Rozen F, Edery I, Meerovitch K, Dever TE, Merrick WC, Sonenberg N 1990. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 10:1134–44
     [Google Scholar]
  110. 110. 
    Rajagopal V, Park EH, Hinnebusch AG, Lorsch JR 2012. 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. 287:20301–12
     [Google Scholar]
  111. 111. 
    García-García C, Frieda KL, Feoktistova K, Fraser CS, Block SM 2015. Factor-dependent processivity in human eIF4A DEAD-box helicase. Science 348:1486–88
     [Google Scholar]
  112. 112. 
    Andersen CB, Ballut L, Johansen JS, Chamieh H, Nielsen KH et al. 2006. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313:1968–72
     [Google Scholar]
  113. 113. 
    Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S 2006. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125:287–300
     [Google Scholar]
  114. 114. 
    Bono F, Ebert J, Lorentzen E, Conti E 2006. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126:713–25
     [Google Scholar]
  115. 115. 
    Lorsch JR, Herschlag D. 1998. The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 37:2180–93
     [Google Scholar]
  116. 116. 
    Rogers GW Jr, Komar AA, Merrick WC. 2002. eIF4A: the godfather of the DEAD box helicases. Prog. Nucleic Acid Res. Mol. Biol. 72:307–31
     [Google Scholar]
  117. 117. 
    Peck ML, Herschlag D. 1999. Effects of oligonucleotide length and atomic composition on stimulation of the ATPase activity of translation initiation factor elF4A. RNA 5:1210–21
     [Google Scholar]
  118. 118. 
    Feoktistova K, Tuvshintogs E, Do A, Fraser CS 2013. Human eIF4E promotes mRNA restructuring by stimulating eIF4A helicase activity. PNAS 110:13339–44
     [Google Scholar]
  119. 119. 
    Svitkin YV, Pause A, Haghighat A, Pyronnet S, Witherell G et al. 2001. The requirement for eukaryotic initiation factor 4A (elF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure. RNA 7:382–94
     [Google Scholar]
  120. 120. 
    Waldron JA, Raza F, Le Quesne J 2018. eIF4A alleviates the translational repression mediated by classical secondary structures more than by G-quadruplexes. Nucleic Acids Res 46:3075–87
     [Google Scholar]
  121. 121. 
    Pestova TV, Kolupaeva VG. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16:2906–22
     [Google Scholar]
  122. 122. 
    Elfakess R, Sinvani H, Haimov O, Svitkin Y, Sonenberg N, Dikstein R 2011. Unique translation initiation of mRNAs-containing TISU element. Nucleic Acids Res 39:7598–609
     [Google Scholar]
  123. 123. 
    Gandin V, Masvidal L, Hulea L, Gravel SP, Cargnello M et al. 2016. nanoCAGE reveals 5′ UTR features that define specific modes of translation of functionally related MTOR-sensitive mRNAs. Genome Res 26:636–48
     [Google Scholar]
  124. 124. 
    Lawson TG, Cladaras MH, Ray BK, Lee KA, Abramson RD et al. 1988. Discriminatory interaction of purified eukaryotic initiation factors 4F plus 4A with the 5′ ends of reovirus messenger RNAs. J. Biol. Chem. 263:7266–76
     [Google Scholar]
  125. 125. 
    Svitkin YV, Ovchinnikov LP, Dreyfuss G, Sonenberg N 1996. General RNA binding proteins render translation cap dependent. EMBO J 15:7147–55
     [Google Scholar]
  126. 126. 
    Pelletier J, Sonenberg N. 1985. Photochemical cross-linking of cap binding proteins to eucaryotic mRNAs: effect of mRNA 5′ secondary structure. Mol. Cell. Biol. 5:3222–30
     [Google Scholar]
  127. 127. 
    Pelletier J, Sonenberg N. 1985. Insertion mutagenesis to increase secondary structure within the 5′ noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell 40:515–26
     [Google Scholar]
  128. 128. 
    Babendure JR, Babendure JL, Ding JH, Tsien RY 2006. Control of mammalian translation by mRNA structure near caps. RNA 12:851–61
     [Google Scholar]
  129. 129. 
    Yourik P, Aitken CE, Zhou F, Gupta N, Hinnebusch AG, Lorsch JR 2017. Yeast eIF4A enhances recruitment of mRNAs regardless of their structural complexity. eLife 6:e31476
     [Google Scholar]
  130. 130. 
    Sen ND, Zhou F, Ingolia NT, Hinnebusch AG 2015. Genome-wide analysis of translational efficiency reveals distinct but overlapping functions of yeast DEAD-box RNA helicases Ded1 and eIF4A. Genome Res 25:1196–205
     [Google Scholar]
  131. 131. 
    Guenther UP, Weinberg DE, Zubradt MM, Tedeschi FA, Stawicki BN et al. 2018. The helicase Ded1p controls use of near-cognate translation initiation codons in 5′ UTRs. Nature 559:130–34
     [Google Scholar]
  132. 132. 
    Soto-Rifo R, Rubilar PS, Limousin T, de Breyne S, Decimo D, Ohlmann T 2012. DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. EMBO J 31:3745–56
     [Google Scholar]
  133. 133. 
    Sharma D, Jankowsky E. 2014. The Ded1/DDX3 subfamily of DEAD-box RNA helicases. Crit. Rev. Biochem. Mol. Biol. 49:343–60
     [Google Scholar]
  134. 134. 
    Fraser CS, Hershey JW, Doudna JA 2009. The pathway of hepatitis C virus mRNA recruitment to the human ribosome. Nat. Struct. Mol. Biol. 16:397–404
     [Google Scholar]
  135. 135. 
    Sokabe M, Fraser CS. 2014. Human eukaryotic initiation factor 2 (eIF2)-GTP-Met-tRNAi ternary complex and eIF3 stabilize the 43S preinitiation complex. J. Biol. Chem. 289:31827–36
     [Google Scholar]
  136. 136. 
    Aylett CH, Boehringer D, Erzberger JP, Schaefer T, Ban N 2015. Structure of a yeast 40S-eIF1-eIF1A-eIF3-eIF3j initiation complex. Nat. Struct. Mol. Biol. 22:269–71
     [Google Scholar]
  137. 137. 
    Sokabe M, Fraser CS. 2017. A helicase-independent activity of eIF4A in promoting mRNA recruitment to the human ribosome. PNAS 114:6304–9
     [Google Scholar]
  138. 138. 
    Yang HS, Jansen AP, Komar AA, Zheng X, Merrick WC et al. 2003. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol. Cell. Biol. 23:26–37
     [Google Scholar]
  139. 139. 
    Yang HS, Knies JL, Stark C, Colburn NH 2003. Pdcd4 suppresses tumor phenotype in JB6 cells by inhibiting AP-1 transactivation. Oncogene 22:3712–20
     [Google Scholar]
  140. 140. 
    Zakowicz H, Yang HS, Stark C, Wlodawer A, Laronde-Leblanc N, Colburn NH 2005. Mutational analysis of the DEAD-box RNA helicase eIF4AII characterizes its interaction with transformation suppressor Pdcd4 and eIF4GI. RNA 11:261–74
     [Google Scholar]
  141. 141. 
    LaRonde-LeBlanc N, Santhanam AN, Baker AR, Wlodawer A, Colburn NH 2007. Structural basis for inhibition of translation by the tumor suppressor Pdcd4. Mol. Cell. Biol. 27:147–56
     [Google Scholar]
  142. 142. 
    Waters LC, Veverka V, Böhm M, Schmedt T, Choong PT et al. 2007. Structure of the C-terminal MA-3 domain of the tumour suppressor protein Pdcd4 and characterization of its interaction with eIF4A. Oncogene 26:4941–50
     [Google Scholar]
  143. 143. 
    Yang HS, Cho MH, Zakowicz H, Hegamyer G, Sonenberg N, Colburn NH 2004. A novel function of the MA-3 domains in transformation and translation suppressor Pdcd4 is essential for its binding to eukaryotic translation initiation factor 4A. Mol. Cell. Biol. 24:3894–906
     [Google Scholar]
  144. 144. 
    Dorrello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M 2006. S6K1- and βTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 314:467–71
     [Google Scholar]
  145. 145. 
    Liwak U, Thakor N, Jordan LE, Roy R, Lewis SM et al. 2012. Tumor suppressor PCD4 repressed internal ribosome site-mediated translation of antiapoptotic proteins and is regulated by S6 kinase 2. Mol. Cell. Biol. 32:1818–29
     [Google Scholar]
  146. 146. 
    Altmann M, Muller PP, Wittmer B, Ruchti F, Lanker S, Trachsel H 1993. A Saccharomyces cerevisiae homologue of mammalian translation initiation factor 4B contributes to RNA helicase activity. EMBO J 12:3997–4003
     [Google Scholar]
  147. 147. 
    Coppolecchia R, Buser P, Stotz A, Linder P 1993. A new yeast translation initiation factor suppresses a mutation in the eIF-4A RNA helicase. EMBO J 12:4005–11
     [Google Scholar]
  148. 148. 
    Methot N, Pause A, Hershey JW, Sonenberg N 1994. The translation initiation factor eIF-4B contains an RNA-binding region that is distinct and independent from its ribonucleoprotein consensus sequence. Mol. Cell. Biol. 14:2307–16
     [Google Scholar]
  149. 149. 
    Naranda T, Strong WB, Menaya J, Fabbri BJ, Hershey JW 1994. Two structural domains of initiation factor eIF-4B are involved in binding to RNA. J. Biol. Chem. 269:14465–72
     [Google Scholar]
  150. 150. 
    Methot N, Pickett G, Keene JD, Sonenberg N 1996. In vitro RNA selection identifies RNA ligands that specifically bind to eukaryotic translation initiation factor 4B: the role of the RNA remotif. RNA 2:38–50
     [Google Scholar]
  151. 151. 
    Eliseev B, Yeramala L, Leitner A, Karuppasamy M, Raimondeau E et al. 2018. Structure of a human cap-dependent 48S translation pre-initiation complex. Nucleic Acids Res 46:2678–89
     [Google Scholar]
  152. 152. 
    Walker SE, Zhou F, Mitchell SF, Larson VS, Valasek L et al. 2013. Yeast eIF4B binds to the head of the 40S ribosomal subunit and promotes mRNA recruitment through its N-terminal and internal repeat domains. RNA 19:191–207
     [Google Scholar]
  153. 153. 
    Capossela S, Muzio L, Bertolo A, Bianchi V, Dati G et al. 2012. Growth defects and impaired cognitive-behavioral abilities in mice with knockout for Eif4h, a gene located in the mouse homolog of the Williams-Beuren syndrome critical region. Am. J. Pathol. 180:1121–35
     [Google Scholar]
  154. 154. 
    Rozovsky N, Butterworth AC, Moore MJ 2008. Interactions between eIF4AI and its accessory factors eIF4B and eIF4H. RNA 14:2136–48
     [Google Scholar]
  155. 155. 
    Parsyan A, Svitkin Y, Shahbazian D, Gkogkas C, Lasko P et al. 2011. mRNA helicases: the tacticians of translational control. Nat. Rev. Mol. Cell Biol. 12:235–45
     [Google Scholar]
  156. 156. 
    Richter-Cook NJ, Dever TE, Hensold JO, Merrick WC 1998. Purification and characterization of a new eukaryotic protein translation factor: eukaryotic initiation factor 4H. J. Biol. Chem. 273:7579–87
     [Google Scholar]
  157. 157. 
    Ozes AR, Feoktistova K, Avanzino BC, Fraser CS 2011. Duplex unwinding and ATPase activities of the DEAD-box helicase eIF4A are coupled by eIF4G and eIF4B. J. Mol. Biol. 412:674–87
     [Google Scholar]
  158. 158. 
    Rogers GW Jr, Richter NJ, Lima WF, Merrick WC. 2001. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J. Biol. Chem. 276:30914–22
     [Google Scholar]
  159. 159. 
    van Gorp AG, van der Vos KE, Brenkman AB, Bremer A, van den Broek N et al. 2009. AGC kinases regulate phosphorylation and activation of eukaryotic translation initiation factor 4B. Oncogene 28:95–106
     [Google Scholar]
  160. 160. 
    Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B et al. 2006. The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J 25:2781–91
     [Google Scholar]
  161. 161. 
    Csibi A, Lee G, Yoon SO, Tong H, Ilter D et al. 2014. The mTORC1/S6K1 pathway regulates glutamine metabolism through the eIF4B-dependent control of c-Myc translation. Curr. Biol. 24:2274–80
     [Google Scholar]
  162. 162. 
    Sonenberg N. 1981. ATP/Mg++-dependent cross-linking of cap binding proteins to the 5′ end of eukaryotic mRNA. Nucleic Acids Res 9:1643–56
     [Google Scholar]
  163. 163. 
    Lawson TG, Ray BK, Dodds JT, Grifo JA, Abramson RD et al. 1986. Influence of 5′ proximal secondary structure on the translational efficiency of eukaryotic mRNAs and on their interaction with initiation factors. J. Biol. Chem. 261:13979–89
     [Google Scholar]
  164. 164. 
    Tomoo K, Matsushita Y, Fujisaki H, Abiko F, Shen X et al. 2005. Structural basis for mRNA Cap-Binding regulation of eukaryotic initiation factor 4E by 4E-binding protein, studied by spectroscopic, X-ray crystal structural, and molecular dynamics simulation methods. Biochim. Biophys. Acta Proteins Proteom. 1753:191–208
     [Google Scholar]
  165. 165. 
    Parkin NT, Cohen EA, Darveau A, Rosen C, Haseltine W, Sonenberg N 1988. Mutational analysis of the 5′ non-coding region of human immunodeficiency virus type 1: effects of secondary structure on translation. EMBO J 7:2831–37
     [Google Scholar]
  166. 166. 
    Lindqvist L, Imataka H, Pelletier J 2008. Cap-dependent eukaryotic initiation factor-mRNA interactions probed by cross-linking. RNA 14:960–69
     [Google Scholar]
  167. 167. 
    Sun Y, Atas E, Lindqvist L, Sonenberg N, Pelletier J, Meller A 2012. The eukaryotic initiation factor eIF4H facilitates loop-binding, repetitive RNA unwinding by the eIF4A DEAD-box helicase. Nucleic Acids Res 40:6199–207
     [Google Scholar]
  168. 168. 
    Pisareva VP, Pisarev AV, Komar AA, Hellen CUT, Pestova TV 2008. Translation initiation on mammalian mRNAs with structured 5′UTRs requires DExH-box protein DHX29. Cell 135:1237–50
     [Google Scholar]
  169. 169. 
    Kumar P, Hellen CU, Pestova TV 2016. Toward the mechanism of eIF4F-mediated ribosomal attachment to mammalian capped mRNAs. Genes Dev 30:1573–88
     [Google Scholar]
  170. 170. 
    Archer SK, Shirokikh NE, Beilharz TH, Preiss T 2016. Dynamics of ribosome scanning and recycling revealed by translation complex profiling. Nature 535:570–74
     [Google Scholar]
  171. 171. 
    Slepenkov SV, Korneeva NL, Rhoads RE 2008. Kinetic mechanism for assembly of the m7GpppGċeIF4EċeIF4G complex. J. Biol. Chem. 283:25227–37
     [Google Scholar]
  172. 172. 
    Asselbergs FAM, Peters W, van Venrooij WJ, Bloemendal H 1978. Diminished sensitivity of re-initiation of translation to inhibition by cap analogues in reticulocyte lysates. Eur. J. Biochem. 88:483–88
     [Google Scholar]
  173. 173. 
    Pelletier J, Sonenberg N. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320–25
     [Google Scholar]
  174. 174. 
    Jang SK, Kräusslich HG, Nicklin MJ, Duke GM, Palmenberg AC, Wimmer E 1988. A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:2636–43
     [Google Scholar]
  175. 175. 
    Mailliot J, Martin F. 2018. Viral internal ribosomal entry sites: four classes for one goal. Wiley Interdiscip. Rev. RNA 9:e1458
     [Google Scholar]
  176. 176. 
    Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU 1998. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev 12:67–83
     [Google Scholar]
  177. 177. 
    Hashem Y, des Georges A, Dhote V, Langlois R, Liao HY et al. 2013. Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 503:539–43
     [Google Scholar]
  178. 178. 
    Wilson JE, Pestova TV, Hellen CU, Sarnow P 2000. Initiation of protein synthesis from the A site of the ribosome. Cell 102:511–20
     [Google Scholar]
  179. 179. 
    Fernández IS, Bai XC, Murshudov G, Scheres SH, Ramakrishnan V 2014. Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome. Cell 157:823–31
     [Google Scholar]
  180. 180. 
    Jackson RJ. 2013. The current status of vertebrate cellular mRNA IRESs. Cold Spring Harb. Perspect. Biol. 5:a011569
     [Google Scholar]
  181. 181. 
    Weingarten-Gabbay S, Elias-Kirma S, Nir R, Gritsenko AA, Stern-Ginossar N et al. 2016. Comparative genetics. Systematic discovery of cap-independent translation sequences in human and viral genomes. Science 351:aad4939
     [Google Scholar]
  182. 182. 
    Meyer KD, Patil DP, Zhou J, Zinoviev A, Skabkin MA et al. 2015. 5′ UTR m6A promotes cap-independent translation. Cell 163:999–1010
     [Google Scholar]
  183. 183. 
    Lin S, Choe J, Du P, Triboulet R, Gregory RI 2016. The m6A methyltransferase METTL3 promotes translation in human cancer cells. Mol. Cell 62:335–45
     [Google Scholar]
  184. 184. 
    Wang X, Zhao BS, Roundtree IA, Lu Z, Han D et al. 2015. N6-methyladenosine modulates messenger RNA translation efficiency. Cell 161:1388–99
     [Google Scholar]
  185. 185. 
    Krug RM, Morgan MA, Shatkin AJ 1976. Influenza viral mRNA contains internal N6-methyladenosine and 5′-terminal 7-methylguanosine in cap structures. J. Virol. 20:45–53
     [Google Scholar]
  186. 186. 
    Fu Y, Dominissini D, Rechavi G, He C 2014. Gene expression regulation mediated through reversible m6A RNA methylation. Nat. Rev. Genet. 15:293–306
     [Google Scholar]
  187. 187. 
    Salzman J. 2016. Circular RNA expression: its potential regulation and function. Trends Genet 32:309–16
     [Google Scholar]
  188. 188. 
    Chekulaeva M, Rajewsky N. 2018. Roles of long noncoding RNAs and circular RNAs in translation. Translation Mechanisms and Control MB Mathews, N Sonenberg, JW Hershey 213–27 Cold Spring Harbor, NY: Cold Spring Harb. Lab.
     [Google Scholar]
  189. 189. 
    Chen CY, Sarnow P. 1998. Internal ribosome entry sites tests with circular mRNAs. Methods Mol. Biol. 77:355–63
     [Google Scholar]
  190. 190. 
    Wang Y, Wang Z. 2015. Efficient backsplicing produces translatable circular mRNAs. RNA 21:172–79
     [Google Scholar]
  191. 191. 
    Mazza C, Ohno M, Segref A, Mattaj IW, Cusack S 2001. Crystal structure of the human nuclear cap binding complex. Mol. Cell 8:383–96
     [Google Scholar]
  192. 192. 
    Gao Q, Das B, Sherman F, Maquat LE 2005. Cap-binding protein 1-mediated and eukaryotic translation initiation factor 4E-mediated pioneer rounds of translation in yeast. PNAS 102:4258–63
     [Google Scholar]
  193. 193. 
    Lee AS, Kranzusch PJ, Doudna JA, Cate JH 2016. eIF3d is an mRNA cap-binding protein that is required for specialized translation initiation. Nature 536:96–99
     [Google Scholar]
  194. 194. 
    Leen EN, Sorgeloos F, Correia S, Chaudhry Y, Cannac F et al. 2016. A conserved interaction between a C-terminal motif in norovirus VPg and the HEAT-1 domain of eIF4G is essential for translation initiation. PLOS Pathog 12:e1005379
     [Google Scholar]
  195. 195. 
    Eskelin K, Hafrén A, Rantalainen KI, Makinen K 2011. Potyviral VPg enhances viral RNA translation and inhibits reporter mRNA translation in planta. J. Virol 85:9210–21
     [Google Scholar]
  196. 196. 
    Leonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, Laliberte JF 2000. Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J. Virol. 74:7730–37
     [Google Scholar]
  197. 197. 
    Kozak M. 1989. Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol. Cell. Biol. 9:5134–42
     [Google Scholar]
  198. 198. 
    Kozak M. 1986. Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. PNAS 83:2850–54
     [Google Scholar]
  199. 199. 
    Kozak M, Shatkin AJ. 1978. Migration of 40 S ribosomal subunits on messenger RNA in the presence of edeine. J. Biol. Chem. 253:6568–77
     [Google Scholar]
  200. 200. 
    Kozak M. 1991. Effects of long 5′ leader sequences on initiation by eukaryotic ribosomes in vitro. Gene Expr 1:117–25
     [Google Scholar]
  201. 201. 
    Calvo SE, Pagliarini DJ, Mootha VK 2009. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. PNAS 106:7507–12
     [Google Scholar]
  202. 202. 
    Ingolia NT, Lareau LF, Weissman JS 2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147:789–802
     [Google Scholar]
  203. 203. 
    Kozak M. 2001. Constraints on reinitiation of translation in mammals. Nucleic Acids Res 29:5226–32
     [Google Scholar]
  204. 204. 
    Poyry TA, Kaminski A, Jackson RJ 2004. What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame. ? Genes Dev 18:62–75
     [Google Scholar]
  205. 205. 
    Starck SR, Tsai JC, Chen K, Shodiya M, Wang L et al. 2016. Translation from the 5′ untranslated region shapes the integrated stress response. Science 351:aad3867
     [Google Scholar]
  206. 206. 
    Sendoel A, Dunn JG, Rodriguez EH, Naik S, Gomez NC et al. 2017. Translation from unconventional 5′ start sites drives tumour initiation. Nature 541:494–99
     [Google Scholar]
  207. 207. 
    Liang H, He S, Yang J, Jia X, Wang P et al. 2014. PTENα, a PTEN isoform translated through alternative initiation, regulates mitochondrial function and energy metabolism. Cell Metab 19:836–48
     [Google Scholar]
  208. 208. 
    Golovko A, Kojukhov A, Guan BJ, Morpurgo B, Merrick WC et al. 2016. The eIF2A knockout mouse. Cell Cycle 15:3115–20
     [Google Scholar]
  209. 209. 
    Chew GL, Pauli A, Rinn JL, Regev A, Schier AF, Valen E 2013. Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs. Development 140:2828–34
     [Google Scholar]
  210. 210. 
    Ruiz-Orera J, Messeguer X, Subirana JA, Alba MM 2014. Long non-coding RNAs as a source of new peptides. eLife 3:e03523
     [Google Scholar]
  211. 211. 
    Bazzini AA, Johnstone TG, Christiano R, Mackowiak SD, Obermayer B et al. 2014. Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation. EMBO J 33:981–93
     [Google Scholar]
  212. 212. 
    Mackowiak SD, Zauber H, Bielow C, Thiel D, Kutz K et al. 2015. Extensive identification and analysis of conserved small ORFs in animals. Genome Biol 16:179
     [Google Scholar]
  213. 213. 
    Wang H, Wang Y, Xie S, Liu Y, Xie Z 2017. Global and cell-type specific properties of lincRNAs with ribosome occupancy. Nucleic Acids Res 45:2786–96
     [Google Scholar]
  214. 214. 
    Kearse MG, Green KM, Krans A, Rodriguez CM, Linsalata AE et al. 2016. CGG repeat-associated non-AUG translation utilizes a cap-dependent scanning mechanism of initiation to produce toxic proteins. Mol. Cell 62:314–22
     [Google Scholar]
  215. 215. 
    Meyuhas O, Kahan T. 2015. The race to decipher the top secrets of TOP mRNAs. Biochim. Biophys. Acta Gene Regul. Mech. 1849:801–11
     [Google Scholar]
  216. 216. 
    Fonseca BD, Lahr RM, Damgaard CK, Alain T, Berman AJ 2018. LARP1 on TOP of ribosome production. Wiley Interdiscip. Rev. RNA 9:e1480
     [Google Scholar]
  217. 217. 
    Fonseca BD, Zakaria C, Jia JJ, Graber TE, Svitkin Y et al. 2015. La-related protein 1 (LARP1) represses terminal oligopyrimidine (TOP) mRNA translation downstream of mTOR complex 1 (mTORC1). J. Biol. Chem. 290:15996–6020
     [Google Scholar]
  218. 218. 
    Tcherkezian J, Cargnello M, Romeo Y, Huttlin EL, Lavoie G et al. 2014. Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5′TOP mRNA translation. Genes Dev 28:357–71
     [Google Scholar]
  219. 219. 
    Lahr RM, Fonseca BD, Ciotti GE, Al-Ashtal HA, Jia JJ et al. 2017. La-related protein 1 (LARP1) binds the mRNA cap, blocking eIF4F assembly on TOP mRNAs. eLife 6:e24146
     [Google Scholar]
  220. 220. 
    Philippe L, Vasseur J-J, Debart F, Thoreen CC 2017. La-related protein 1 (LARP1) repression of TOP mRNA translation is mediated through its cap-binding domain and controlled by an adjacent regulatory region. Nucl. Acids Res. 46:1457–69
     [Google Scholar]
  221. 221. 
    Shah P, Ding Y, Niemczyk M, Kudla G, Plotkin JB 2013. Rate-limiting steps in yeast protein translation. Cell 153:1589–601
     [Google Scholar]
  222. 222. 
    Yan X, Hoek TA, Vale RD, Tanenbaum ME 2016. Dynamics of translation of single mRNA molecules in vivo. Cell 165:976–89
     [Google Scholar]
  223. 223. 
    Peter D, Weber R, Sandmeir F, Wohlbold L, Helms S et al. 2017. GIGYF1/2 proteins use auxiliary sequences to selectively bind to 4EHP and repress target mRNA expression. Genes Dev 31:1147–61
     [Google Scholar]
/content/journals/10.1146/annurev-biochem-013118-111042
Loading
The Organizing Principles of Eukaryotic Ribosome Recruitment
Annual Review of Biochemistry 88, 307 (2019); https://doi.org/10.1146/annurev-biochem-013118-111042
/content/journals/10.1146/annurev-biochem-013118-111042
/content/journals/10.1146/annurev-biochem-013118-111042
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error