Crystal structure of a minimal eIF4E-Cup complex reveals a general mechanism of eIF4E regulation in translational repression

RNA

Volumn 18, Issue 9, 2012, Pages 1624-1634

  Kinkelin, Kerstin ^a,b   Veith, Katharina ^a   Grünwald, Marlene ^a   Bono, Fulvia ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

4E BP; Cup; eIF4E; mRNA localization; Translation

Indexed keywords

INITIATION FACTOR 4E; INITIATION FACTOR 4G; MESSENGER RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING KINETICS; BINDING SITE; CONSENSUS; CRYSTAL STRUCTURE; CRYSTALLIZATION; GEL PERMEATION CHROMATOGRAPHY; HYDROPHOBICITY; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; REGULATORY MECHANISM; STEREOCHEMISTRY; STRUCTURE ACTIVITY RELATION; TRANSLATION REGULATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DROSOPHILA PROTEINS; EUKARYOTIC INITIATION FACTOR-4E; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

EID: 84865118901     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.033639.112     Document Type: Article

References (67)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Ashby JA, Stevenson CEM, Jarvis GE, Lawson DM, Maule AJ. 2011. Structure-based mutational analysis of eIF4E in relation to sbm1 resistance to pea seed-borne mosaic virus in pea. PLoS ONE 6: e15873. doi: 10.1371/journal.pone.0015873.
3. Besse F, Ephrussi A. 2008. Translational control of localized mRNAs: Restricting protein synthesis in space and time. Nat Rev Mol Cell Biol 9: 971-980.
4. 7-alkylated cap derivatives. J Mol Biol 372: 7-15.
5. Brown CJ, Verma CS, Walkinshaw MD, Lane DP. 2009. Crystallization of eIF4E complexed with eIF4GI peptide and glycerol reveals distinct structural differences around the cap-binding site. Cell Cycle 8: 1905-1911.
6. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
7. Clouse KN, Ferguson SB, Schüpbach T. 2008. Squid, Cup, and PABP55B function together to regulate gurken translation in Drosophila. Dev Biol 313: 713-724.
8. Cohen N, Sharma M, Kentsis A, Perez JM, Strudwick S, Borden KL. 2001. PML RING suppresses oncogenic transformation by reducing the affinity of eIF4E for mRNA. EMBO J 20: 4547-4559. (Pubitemid 32772048)
9. Curry S, Kotik-Kogan O, Conte MR, Brick P. 2009. Getting to the end of RNA: Structural analysis of protein recognition of 5′ and 3′ termini. Biochim Biophys Acta 1789: 653-666.
10. Dostie J, Lejbkowicz F, Sonenberg N. 2000. Nuclear eukaryotic initiation factor 4E (eIF4E) colocalizes with splicing factors in speckles. J Cell Biol 148: 239-247.
11. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. (Pubitemid 41742764)
12. Filardo P, Ephrussi A. 2003. Bruno regulates gurken during Drosophila oogenesis. Mech Dev 120: 289-297. (Pubitemid 36184624)
13. Gebauer F, Hentze MW. 2004. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5: 827-835. (Pubitemid 39336276)
14. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, Aebersold R, Sonenberg N. 1999. Regulation of 4E-BP1 phosphorylation: A novel two-step mechanism. Genes Dev 13: 1422-1437. (Pubitemid 29270247)
15. Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, McCarthy JEG, Wagner G. 2003. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115: 739-750. (Pubitemid 38030302)
16. Haghighat A, Sonenberg N. 1997. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J Biol Chem 272: 21677-21680. (Pubitemid 27382778)
17. Haghighat A, Mader S, Pause A, Sonenberg N. 1995. Repression of cap-dependent translation by 4E-binding protein 1: Competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J 14: 5701-5709.
18. Hershey PE, McWhirter SM, Gross JD, Wagner G, Alber T, Sachs AB. 1999. The Cap-binding protein eIF4E promotes folding of a functional domain of yeast translation initiation factor eIF4G1. J Biol Chem 274: 21297-21304.
19. Igreja C, Izaurralde E. 2011. CUP promotes deadenylation and inhibits decapping of mRNA targets. Genes Dev 25: 1955-1967.
20. Jackson RJ, Hellen CUT, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
21. Kabsch W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26: 795-800.
22. Keyes LN, Spradling AC. 1997. The Drosophila gene fs(2)cup interacts with otu to define a cytoplasmic pathway required for the structure and function of germ-line chromosomes. Development 124: 1419-1431. (Pubitemid 27190114)
23. Kim-Ha J, Kerr K, Macdonald PM. 1995. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 81: 403-412.
24. Lin TA, Kong X, Haystead TA, Pause A, Belsham G, Sonenberg N, Lawrence JC. 1994. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266: 653-656. (Pubitemid 24363524)
25. 2,2,7G-Cap and its implications for translation initiation. Nucleic Acids Res 39: 8820-8832.
26. 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 4E-binding proteins. Mol Cell Biol 15: 4990-4997.
27. 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: 951-961. (Pubitemid 27513521)
28. 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: 707-716. (Pubitemid 29323049)
29. Matsuo H, Li H, McGuire AM, Fletcher CM, Gingras AC, Sonenberg N, Wagner G. 1997. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol 4: 717-724. (Pubitemid 27382431)
30. McCoy A, Grosse-Kunstleve R, Adams P, Winn M, Storoni L, Read R. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674. (Pubitemid 47080256)
31. 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: 17663-17671.
32. McGuire AM, Matsuo H, Wagner G. 1998. Internal and overall motions of the translation factor eIF4E: Cap binding and insertion in a CHAPS detergent micelle. J Biomol NMR 12: 73-88. (Pubitemid 128512835)
33. Mizuno A, In Y, Fujita Y, Abiko F, Miyagawa H, Kitamura K, Tomoo K, Ishida T. 2008. Importance of C-terminal flexible region of 4E-binding protein in binding with eukaryotic initiation factor 4E. FEBS Lett 582: 3439-3444.
34. Monzingo AF, Dhaliwal S, Dutt-Chaudhuri A, Lyon A, Sadow JH, Hoffman DW, Robertus JD, Browning KS. 2007. The structure of eukaryotic translation initiation factor-4E from wheat reveals a novel disulfide bond. Plant Physiol 143: 1504-1518. (Pubitemid 46849464)
35. Nakamura A, Sato K, Hanyu-Nakamura K. 2004. Drosophila Cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev Cell 6: 69-78. (Pubitemid 38089206)
36. Nelson MR, Leidal AM, Smibert CA. 2004. Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. EMBO J 23: 150-159. (Pubitemid 38165755)
37. Niedzwiecka A, Marcotrigiano J, Stepinski J, Jankowska-Anyszka M, Wyslouch-Cieszynska A, Dadlez M, Gingras A-C, Mak P, Darzynkiewicz E, Sonenberg N, et al. 2002a. 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: 615-635. (Pubitemid 34729439)
38. Niedzwiecka A, Stepinski J, Darzynkiewicz E, Sonenberg N, Stolarski R. 2002b. Positive heat capacity change upon specific binding of translation initiation factor eIF4E to mRNA 5′ Cap. Biochemistry 41: 12140-12148.
39. Niesen FH, Berglund H, Vedadi M. 2007. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2: 2212-2221. (Pubitemid 351565860)
40. Niessing D, Blanke S, Jäckle H. 2002. Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation. Genes Dev 16: 2576-2582.
41. Norvell A, Kelley RL, Wehr K, Schüpbach T. 1999. Specific isoforms of squid, a Drosophila hnRNP, perform distinct roles in Gurken localization during oogenesis. Genes Dev 13: 864-876. (Pubitemid 29169845)
42. Paku KS, Umenaga Y, Usui T, Fukuyo A, Mizuno A, In Y, Ishida T, Tomoo K. 2011. A conserved motif within the flexible C-terminus of the translational regulator 4E-BP is required for tight binding to the mRNA cap-binding protein eIF4E. Biochem J 441: 237-245.
43. Pause A, Belsham GJ, Gingras AC, Donzé O, Lin TA, Lawrence JC, Sonenberg N. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371: 762-767.
44. Ptushkina M, von der Haar T, Vasilescu S, Frank R, Birkenhäger R, McCarthy JE. 1998. Cooperative modulation by eIF4G of eIF4Ebinding to the mRNA 5′ cap in yeast involves a site partially shared by p20. EMBO J 17: 4798-4808. (Pubitemid 28377180)
45. Ptushkina M, von der Haar T, Karim MM, Hughes JM, McCarthy JE. 1999. Repressor binding to a dorsal regulatory site traps human eIF4E in a high cap-affinity state. EMBO J 18: 4068-4075. (Pubitemid 29335859)
46. Reichmann D, CohenM, Abramovich R, Dym O, Lim D, Strynadka NCJ, Schreiber G. 2007. Binding hot spots in the TEM1-BLIP interface in light of its modular architecture. J Mol Biol 365: 663-679. (Pubitemid 44960349)
47. Rosettani P, Knapp S, Vismara M-G, 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. (Pubitemid 46527609)
48. 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: 3303-3309. (Pubitemid 34953196)
49. Schüpbach T,Wieschaus E. 1991. Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129: 1119-1136.
50. Siddiqui N, Tempel W, Nedyalkova L, Volpon L, Wernimont AK, Osborne MJ, Park H-W, Borden KLB. 2012. Structural insights into the allosteric effects of 4EBP1 on the eukaryotic translation initiation factor eIF4E. J Mol Biol 415: 781-792.
51. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745.
52. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
53. Tomoo K, Shen X, Okabe K, Nozoe Y, Fukuhara S, Morino S, Sasaki M, Taniguchi T, Miyagawa H, Kitamura K, et al. 2003. Structural features of human initiation factor 4E, studied by X-ray crystal analyses and molecular dynamics simulations. J Mol Biol 328: 365-383. (Pubitemid 36407580)
54. Tomoo K, Matsushita Y, Fujisaki H, Abiko F, Shen X, Taniguchi T, Miyagawa H, Kitamura K, Miura K-i, Ishida T. 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 1753: 191-208. (Pubitemid 41643152)
55. Topisirovic I, Svitkin YV, Sonenberg N, Shatkin AJ. 2011. Cap and cap-binding proteins in the control of gene expression. Wiley Interdiscip Rev RNA 2: 277-298.
56. Vardy L, Orr-Weaver TL. 2007. Regulating translation of maternal messages: Multiple repression mechanisms. Trends Cell Biol 17: 547-554. (Pubitemid 350087663)
57. Verrotti AC, Wharton RP. 2000. Nanos interacts with Cup in the female germline of Drosophila. Development 127: 5225-5232. (Pubitemid 32000678)
58. Volpon L, Osborne MJ, Topisirovic I, Siddiqui N, Borden KLB. 2006. Cap-free structure of eIF4E suggests a basis for conformational regulation by its ligands. EMBO J 25: 5138-5149. (Pubitemid 44658531)
59. Volpon L, Osborne MJ, Capul AA, de la Torre JC, Borden KLB. 2010. Structural characterization of the Z RING-eIF4E complex reveals a distinct mode of control for eIF4E. Proc Natl Acad Sci 107: 5441-5446.
60. von der Haar T, Ball PD, McCarthy JE. 2000. Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5′-Cap by domains of eIF4G. J Biol Chem 275: 30551-30555.
61. von der Haar T, Gross JD, Wagner G, McCarthy JEG. 2004. The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat Struct Mol Biol 11: 503-511. (Pubitemid 38691916)
62. von der Haar T, Oku Y, Ptushkina M, Moerke N, Wagner G, Gross JD, McCarthy JEG. 2006. Folding transitions during assembly of the eukaryotic mRNA cap-binding complex. J Mol Biol 356: 982-992. (Pubitemid 43145950)
63. Webster PJ, Liang L, Berg CA, Lasko P, Macdonald PM. 1997. Translational repressor bruno plays multiple roles in development and is widely conserved. Genes Dev 11: 2510-2521. (Pubitemid 27438832)
64. Wilhelm JE, Hilton M, Amos Q, Henzel WJ. 2003. Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz. J Cell Biol 163: 1197-1204. (Pubitemid 38032081)
65. 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: 1661-1669.
66. Zappavigna V, Piccioni F, Villaescusa JC, Verrotti AC. 2004. Cup is a nucleocytoplasmic shuttling protein that interacts with the eukaryotic translation initiation factor 4E to modulate Drosophila ovary development. Proc Natl Acad Sci 101: 14800-14805. (Pubitemid 39410755)
67. Zhai B, Villén J, Beausoleil SA, Mintseris J, Gygi SP. 2008. Phosphoproteome analysis of Drosophila melanogaster embryos. J Proteome Res 7: 1675-1682.