Toward the mechanism of eIF4F-mediated ribosomal attachment to mammalian capped mRNAs

Genes and Development

Volumn 30, Issue 13, 2016, Pages 1573-1588

  Kumar, Parimal ^a   Hellen, Christopher U T ^a   Pestova, Tatyana V ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

40S ribosomal subunit; eIF3l; eIF4E; eIF4F; Eukaryotic translation initiation; m7G

Indexed keywords

CAPPED RNA; INITIATION FACTOR 3; INITIATION FACTOR 4A; INITIATION FACTOR 4E; INITIATION FACTOR 4F; INITIATION FACTOR 4G; TRANSFER RNA; MESSENGER RNA; RECOMBINANT PROTEIN;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; IN VITRO STUDY; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; RIBOSOMAL ATTACHMENT; RIBOSOME; STEREOSPECIFICITY; TRANSLATION INITIATION; ANIMAL; GENETICS; MAMMAL; METABOLISM; MUTATION; SMALL RIBOSOMAL SUBUNIT;

ANIMALS; EUKARYOTIC INITIATION FACTOR-4F; MAMMALS; MUTATION; RECOMBINANT PROTEINS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RIBOSOMES; RNA CAPS; RNA, MESSENGER; RNA, TRANSFER;

EID: 84978032319     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.282418.116     Document Type: Article

References (61)

1. Abaeva IS, Marintchev A, Pisareva VP, Hellen CU, Pestova TV. 2011. Bypassing of stems versus linear base-by-base inspection of mammalian mRNAs during ribosomal scanning. EMBO J 30: 115-129.
2. Abaeva IS, Pestova TV, Hellen CU. 2016. Attachment of ribosomal complexes and retrograde scanning during initiation on the Halastavi árva virus IRES. Nucleic Acids Res 44: 2362-2377.
3. Abbas YM, Pichlmair A, Górna MW, Superti-Furga G, Nagar B. 2013. Structural basis for viral 5ʹ-PPP-RNA recognition by human IFIT proteins. Nature 494: 60-64.
4. 7GpppAm and ionic conditions. J Biol Chem 254: 459-468.
5. Berthelot K, Muldoon M, Rajkowitsch L, Hughes J, McCarthy JE. 2004. Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Mol Microbiol 51: 987-1001.
6. 7GpppX. FEBS Lett 64: 326-331.
7. De Gregorio E, Preiss T, Hentze MW. 1998. Translational activation of uncapped mRNAs by the central part of human eIF4G is 5ʹ end-dependent. RNA 4: 828-836.
8. des Georges A, Dhote V, Kuhn L, Hellen CU, Pestova TV, Frank J, Hashem Y. 2015. Structure of mammalian eIF3 in the context of the 43S preinitiation complex. Nature 525: 491-495.
9. 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: 7598-7609.
10. Ellisdon AM, Stewart M. 2012. Structural biology of the PCI-protein fold. Bioarchitecture 2: 118-123.
11. 7Gcap on β-globinmRNAand alfalfa mosaic virusRNA 4 increases the amounts of initiation factor 4F required for translation. J Biol Chem 265: 19582-19587.
12. García-García C, Frieda KL, Feoktistova K, Fraser CS, Block SM. 2015. Factor-dependent processivity in human eIF4A DEADbox helicase. Science 348: 1486-1488.
13. Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, McCarthy JE, Wagner G. 2003. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115: 739-750.
14. Hashem Y, des Georges A, Dhote V, Langlois R, Liao HY, Grassucci RA, Hellen CU, Pestova TV, Frank J. 2013. Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29. Cell 153: 1108-1119.
15. He H, von der Haar T, Singh CR, Ii M, Li B, Hinnebusch AG, Mc-Carthy JE, Asano K. 2003. The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection. Mol Cell Biol 23: 5431-5445.
16. Hinton TM, Coldwell MJ, Carpenter GA, Morley SJ, Pain VM. 2007. Functional analysis of individual binding activities of the scaffold protein eIF4G. J Biol Chem 282: 1695-1708.
17. Hussain T, Llácer JL, Fernández IS, Munoz A, Martin-Marcos P, Savva CG, Lorsch JR, Hinnebusch AG, Ramakrishnan V. 2014. Structural changes enable start codon recognition by the eukaryotic translation initiation complex. Cell 159: 597-607.
18. 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: 6940-6947.
19. Jackson RJ, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
20. 7G cap. J Biol Chem 284: 17742-17750.
21. Kolupaeva VG, Unbehaun A, Lomakin IB, Hellen CU, Pestova TV. 2005. Binding of eukaryotic initiation factor 3 to ribosomal 40S subunits and its role in ribosomal dissociation and antiassociation. RNA 11: 470-486.
22. Kumar P, Sweeney TR, Skabkin MA, Skabkina OV, Hellen CU, Pestova TV. 2014. Inhibition of translation by IFIT family members is determined by their ability to interact selectively with the 5ʹ-terminal regions of cap0-, cap1- and 5ʹpppmRNAs. Nucleic Acids Res 42: 3228-3245.
23. Lee AS, Kranzusch PJ, Cate JH. 2015. eIF3 targets cell-proliferation messenger RNAs for translational activation or repression. Nature 522: 111-114.
24. LeFebvre AK, Korneeva NL, Trutschl M, Cvek U, Duzan RD, Bradley CA, Hershey JW, Rhoads RE. 2006. Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J Biol Chem 281: 22917-22932.
25. Li L, Wang CC. 2004. Capped mRNA with a single nucleotide leader is optimally translated in a primitive eukaryote, Giardia lamblia. J Biol Chem 279: 14656-14664.
26. Lindqvist L, Imataka H, Pelletier J. 2008. Cap-dependent eukaryotic initiation factor-mRNA interactions probed by crosslinking. RNA 14: 960-969.
27. Llácer JL, Hussain T, Marler L, Aitken CE, Thakur A, Lorsch JR, Hinnebusch AG, Ramakrishnan V. 2015. Conformational differences between open and closed states of the eukaryotic translation initiation complex. Mol Cell 59: 399-412.
28. Lomakin IB, Hellen CU, Pestova TV. 2000. Physical association of eukaryotic initiation factor 4G (eIF4G) with eIF4A strongly enhances binding of eIF4G to the internal ribosomal entry site of encephalomyocarditis virus and is required for internal initiation of translation. Mol Cell Biol 20: 6019-6029.
29. Maag D, Fekete CA, Gryczynski Z, Lorsch JR. 2005. A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Mol Cell 17: 265-275.
30. Mader S, Lee H, Pause A, Sonenberg N. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4γ and the translational repressors 4Ebinding proteins. Mol Cell Biol 15: 4990-4997.
31. Marintchev A, Edmonds KA, Marintcheva B, Hendrickson E, Oberer M, Suzuki C, Herdy B, Sonenberg N, Wagner G. 2009. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136: 447- 460.
32. Masutani M, Sonenberg N, Yokoyama S, Imataka H. 2007. Reconstitution reveals the functional core of mammalian eIF3. EMBO J 26: 3373-3383.
33. 7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J 21: 5548-5557.
34. Morais AT, Meza AN, Araújo GC, Vidotto A, Souza FP, Fossey MA, Murakami MT, Nogueira ML. 2014. Biophysical and structural characterization of the recombinant human eIF3L. Protein Pept Lett 21: 56-62.
35. Morino S, Imataka H, Svitkin YV, Pestova TV, Sonenberg N. 2000. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol Cell Biol 20: 468-477.
36. Morris C, Wittmann J, Jäck HM, Jalinot P. 2007. Human INT6/ eIF3e is required for nonsense-mediated mRNA decay. EMBO Rep 8: 596-602.
37. Niedzwiecka A, Marcotrigiano J, Stepinski J, Jankowska-Anyszka M, Wyslouch-Cieszynska A, Dadlez M, Gingras AC, Mak P, Darzynkiewicz E, Sonenberg N, et al. 2002. Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5ʹ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J Mol Biol 319: 615-635.
38. Ohlmann T, Rau M, Pain VM, Morley SJ. 1996. The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J 15: 1371-1382.
39. Pestova TV, Kolupaeva VG. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16: 2906-2922.
40. Pestova TV, de Breyne S, Pisarev AV, Abaeva IS, Hellen CU. 2008. eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II. EMBO J 27: 1060-1072.
41. Pisarev AV, Kolupaeva VG, Pisareva VP, Merrick WC, Hellen CU, Pestova TV. 2006. Specific functional interactions of nucleotides at key −3 and +4 positions flanking the initiation codon with components of the mammalian 48S translation initiation complex. Genes Dev 20: 624-636.
42. Pisarev AV, Kolupaeva VG, Yusupov MM, Hellen CU, Pestova TV. 2008. Ribosomal position and contacts of mRNA in eukaryotic translation initiation complexes. EMBO J 27: 1609-1621.
43. Pisareva VP, Pisarev AV, Komar AA, Hellen CU, Pestova TV. 2008. Translation initiation on mammalian mRNAs with structured 5ʹUTRs requires DExH-box protein DHX29. Cell 135: 1237-1250.
44. Quiocho FA, Hu G, Gershon PD. 2000. Structural basis of mRNA cap recognition by proteins. Curr Opin Struct Biol 10: 78-86.
45. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485.
46. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E. 2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310: 1513-1515.
47. Skabkin MA, Skabkina OV, Hellen CU, Pestova TV. 2013. Reinitiation and other unconventional posttermination events during eukaryotic translation. Mol Cell 51: 249-264.
48. 7GpppG·eIF4E·eIF4G complex. J Biol Chem 283: 25227-25237.
49. Sonenberg N, Shatkin AJ. 1977. ReovirusmRNAcan be covalently crosslinked via the 5ʹ cap to proteins in initiation complexes. Proc Natl Acad Sci 74: 4288-4292.
50. 7GMP on protein-RNA interactions. J Biol Chem 253: 6630-6632.
51. Sonenberg N, Morgan MA, Testa D, Colonno RJ, Shatkin AJ. 1979a. Interaction of a limited set of proteins with different mRNAs and protection of 5ʹ-caps against pyrophosphatase digestion in initiation complexes. Nucleic Acids Res 7: 15-29.
52. 7GDP. Proc Natl Acad Sci 76: 4345-4349.
53. Tcherkezian J, Cargnello M, Romeo Y, Huttlin EL, Lavoie G, Gygi SP, Roux PP. 2014. Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5ʹTOP mRNA translation. Genes Dev 28: 357-371.
54. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM. 2012. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485: 109-113.
55. 7GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region. Biochem J 362: 539-544.
56. 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: 32932-32940.
57. von der Haar T, Gross JD, Wagner G, McCarthy JE. 2004. The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat Struct Mol Biol 11: 503-511.
58. Yanagiya A, Svitkin YV, Shibata S, Mikami S, Imataka H, Sonenberg N. 2009. Requirement ofRNAbinding of mammalian eukaryotic translation initiation factor 4GI (eIF4GI) for efficient interaction of eIF4E with the mRNA cap. Mol Cell Biol 29: 1661-1669.
59. Yu Y, Abaeva IS, Marintchev A, Pestova TV, Hellen CU. 2011. Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res 39: 4851-4865.
60. Zhou M, Sandercock AM, Fraser CS, Ridlova G, Stephens E, Schenauer MR, Yokoi-Fong T, Barsky D, Leary JA, Hershey JW, et al. 2008. Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc Natl Acad Sci 105: 18139-18144.
61. Zinoviev A, Hellen CU, Pestova TV. 2015. Multiple mechanisms of reinitiation on bicistronic calicivirus mRNAs. Mol Cell 57: 1059-1073.