Structure of the eukaryotic translation initiation factor eIF4E in complex with 4EGI-1 reveals an allosteric mechanism for dissociating eIF4G

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 31, 2014, Pages

  Papadopoulos, Evangelos ^a   Jenni, Simon ^a   Kabha, Eihab ^a   Takrouri, Khuloud J ^a,b   Yi, Tingfang ^a   Salvi, Nicola ^a   Luna, Rafael E ^a   Gavathiotis, Evripidis ^c,d   Mahalingam, Poornachandran ^a,e   Arthanari, Haribabu ^a   Rodriguez Mias, Ricard ^a   Yefidoff Freedman, Revital ^a,b   Aktas, Bertal H ^a   Chorev, Michael ^a   Halperin, Jose A ^a   Wagner, Gerhard ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

Allosteric inhibitor; Inhibitor of protein protein interaction; NMR spectroscopy

Indexed keywords

4EGI 1; INITIATION FACTOR 4A; INITIATION FACTOR 4E; INITIATION FACTOR 4G; MESSENGER RNA; PROTEIN INHIBITOR; RIBOSOME RNA; RNA 40S; RNA HELICASE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ALLOSTERISM; AMINO ACID SYNTHESIS; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CARBON NUCLEAR MAGNETIC RESONANCE; CHEMICAL STRUCTURE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION; DISSOCIATION CONSTANT; DRUG DESIGN; FLUORESCENCE POLARIZATION; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; LOW TEMPERATURE; NEUROBIOLOGY; NITROGEN NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RNA TRANSLATION; SITE DIRECTED MUTAGENESIS; SMALL RIBOSOMAL SUBUNIT; START CODON; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC INHIBITOR; INHIBITOR OF PROTEIN-PROTEIN INTERACTION; NMR SPECTROSCOPY;

ALLOSTERIC REGULATION; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; HUMANS; HYDRAZONES; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RNA CAPS; SOLUTIONS; THIAZOLES;

EID: 84905653296     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1410250111     Document Type: Article

References (46)

1. Pickering BM, Willis AE (2005) The implications of structured 5′ untranslated regions on translation and disease. Semin Cell Dev Biol 16(1):39-47. (Pubitemid 40126875)
2. Koromilas AE, Lazaris-Karatzas A, Sonenberg N (1992) mRNAs containing extensive secondary structure in their 5′ non-coding region translate efficiently in cells over-expressing initiation factor eIF-4E. EMBO J 11(11):4153-4158.
3. Tcherkezian J, et al. (2014) Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5'TOP mRNA translation. Genes Dev 28(4):357-371.
4. Casadio A, et al. (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99(2):221-237. (Pubitemid 29491788)
5. Sutton MA, Schuman EM (2005) Local translational control in dendrites and its role in long-term synaptic plasticity. J Neurobiol 64(1):116-131. (Pubitemid 40847435)
6. Silvera D, Formenti SC, Schneider RJ (2010) Translational control in cancer. Nat Rev Cancer 10(4):254-266.
7. Moerke NJ, et al. (2007) Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128(2):257-267. (Pubitemid 46137991)
8. Chen L, et al. (2012) Tumor suppression by small molecule inhibitors of translation initiation. Oncotarget 3(8):869-881.
9. Tamburini J, et al. (2009) Protein synthesis is resistant to rapamycin and constitutes a promising therapeutic target in acute myeloid leukemia. Blood 114(8):1618-1627.
10. Descamps G, et al. (2012) The cap-translation inhibitor 4EGI-1 induces apoptosis in multiple myeloma through Noxa induction. Br J Cancer 106(10):1660-1667.
11. Yi T, Papadopoulos E, Hagner PR, Wagner G (2013) Hypoxia-inducible factor-1α (HIF-1α) promotes cap-dependent translation of selective mRNAs through up-regulating initiation factor eIF4E1 in breast cancer cells under hypoxia conditions. J Biol Chem 288(26):18732-18742.
12. Fan S, Li Y, Yue P, Khuri FR, Sun SY (2010) The eIF4E/eIF4G interaction inhibitor 4EGI-1 augments TRAIL-mediated apoptosis through c-FLIP Down-regulation and DR5 induction independent of inhibition of cap-dependent protein translation. Neoplasia 12(4):346-356.
13. Hagner PR, Schneider A, Gartenhaus RB (2010) Targeting the translational machinery as a novel treatment strategy for hematologic malignancies. Blood 115(11):2127-2135.
14. Willimott S, Beck D, Ahearne MJ, Adams VC, Wagner SD (2013) Cap-translation inhibitor, 4EGI-1, restores sensitivity to ABT-737 apoptosis through cap-dependent and -independent mechanisms in chronic lymphocytic leukemia. Clin Cancer Res 19(12):3212-3223.
15. Takrouri K, et al. (2014) Structure-activity relationship study of 4EGI-1, small molecule eIF4E/eIF4G protein-protein interaction inhibitors. Eur J Med Chem 77:361-377.
16. Hoeffer CA, et al. (2011) Inhibition of the interactions between eukaryotic initiation factors 4E and 4G impairs long-term associative memory consolidation but not reconsolidation. Proc Natl Acad Sci USA 108(8):3383-3388.
17. Hoeffer CA, et al. (2013) Multiple components of eIF4F are required for protein synthesis-dependent hippocampal long-term potentiation. J Neurophysiol 109(1):68-76.
18. Gkogkas CG, et al. (2013) Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 493(7432):371-377.
19. Gingras AC, et al. (2001) Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 15(21):2852-2864.
20. Pause A, et al. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371(6500):762-767.
21. Teleman AA, Chen YW, Cohen SM (2005) 4E-BP functions as a metabolic brake used under stress conditions but not during normal growth. Genes Dev 19(16):1844-1848. (Pubitemid 41186984)
22. Avdulov S, et al. (2004) Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells. Cancer Cell 5(6):553-563. (Pubitemid 38748917)
23. 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(6):707-716. (Pubitemid 29323049)
24. Allard EK, Grujic M, Fisone G, Kristensson K (2013) Prion formation correlates with activation of translation-regulating protein 4E-BP and neuronal transcription factor Elk1. Neurobiol Dis 58:116-122.
25. Santini E, et al. (2013) Exaggerated translation causes synaptic and behavioural aberrations associated with autism. Nature 493(7432):411-415.
26. Cencic R, et al. (2011) Blocking eIF4E-eIF4G interaction as a strategy to impair coronavirus replication. J Virol 85(13):6381-6389.
27. Volpon L, Osborne MJ, Capul AA, de la Torre JC, Borden KL (2010) Structural characterization of the Z RING-eIF4E complex reveals a distinct mode of control for eIF4E. Proc Natl Acad Sci USA 107(12):5441-5446.
28. Buxade M, Parra-Palau JL, Proud CG (2008) The Mnks: MAP kinase-interacting kinases (MAP kinase signal-integrating kinases). Front Biosci 13:5359-5373.
29. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774-797. (Pubitemid 47321791)
30. Wang C, Rance M, Palmer AG, 3rd (2003) Mapping chemical exchange in proteins with MW > 50 kD. J Am Chem Soc 125(30):8968-8969. (Pubitemid 36903790)
31. Zhou P, Lugovskoy AA, Wagner G (2001) A solubility-enhancement tag (SET) for NMR studies of poorly behaving proteins. J Biomol NMR 20(1):11-14. (Pubitemid 32519649)
32. Cencic R, et al. (2011) Reversing chemoresistance by small molecule inhibition of the translation initiation complex eIF4F. Proc Natl Acad Sci USA 108(3):1046-1051.
33. Matsuo H, et al. (1997) Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol 4(9):717-724. (Pubitemid 27382431)
34. Fletcher CM, et al. (1998) 4E binding proteins inhibit the translation factor eIF4E without folded structure. Biochemistry 37(1):9-15. (Pubitemid 28049102)
35. Gross JD, Matsuo H, Fletcher M, Sachs AB, Wagner G (2001) Interactions of the eukaryotic translation initiation factor eIF4E. Cold Spring Harb Symp Quant Biol 66:397-402. (Pubitemid 36097947)
36. Edery I, Altmann M, Sonenberg N (1988) High-level synthesis in Escherichia coli of functional cap-binding eukaryotic initiation factor eIF-4E and affinity purification using a simplified cap-analog resin. Gene 74(2):517-525. (Pubitemid 19060665)
37. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66(Pt 2):125-132.
38. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674. (Pubitemid 47080256)
39. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47(Pt 2):110-119.
40. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
41. Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62(Pt 4):439-450.
42. Davis IW, et al. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35(Web Server issue):W375-W383.
43. Lee D, Hilty C, Wider G, Wüthrich K (2006) Effective rotational correlation times of proteins from NMR relaxation interference. J Magn Reson 178(1):72-76. (Pubitemid 41774013)
44. McCubbin WD, Edery I, Altmann M, Sonenberg N, Kay CM (1988) Circular dichroism and fluorescence studies on protein synthesis initiation factor eIF-4E and two mutant forms from the yeast Saccharomyces cerevisiae. J Biol Chem 263(33):17663-17671.
45. Shen X, Tomoo K, Uchiyama S, Kobayashi Y, Ishida T (2001) Structural and thermodynamic behavior of eukaryotic initiation factor 4E in supramolecular formation with 4E-binding protein 1 and mRNA cap analogue, studied by spectroscopic methods. Chem Pharm Bull (Tokyo) 49(10):1299-1303. (Pubitemid 33035640)
46. Niedzwiecka A, et al. (2002) 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(3):615-635. (Pubitemid 34729439)