1ipb Citations

Crystal structures of 7-methylguanosine 5'-triphosphate (m(7)GTP)- and P(1)-7-methylguanosine-P(3)-adenosine-5',5'-triphosphate (m(7)GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region.

Abstract

The crystal structures of the full-length human eukaryotic initiation factor (eIF) 4E complexed with two mRNA cap analogues [7-methylguanosine 5'-triphosphate (m(7)GTP) and P(1)-7-methylguanosine-P(3)-adenosine-5',5'-triphosphate (m(7)GpppA)] were determined at 2.0 A resolution (where 1 A=0.1 nm). The flexibility of the C-terminal loop region of eIF4E complexed with m(7)GTP was significantly reduced when complexed with m(7)GpppA, suggesting the importance of the second nucleotide in the mRNA cap structure for the biological function of eIF4E, especially the fixation and orientation of the C-terminal loop region, including the eIF4E phosphorylation residue. The present results provide the structural basis for the biological function of both N- and C-terminal mobile regions of eIF4E in translation initiation, especially the regulatory function through the switch-on/off of eIF4E-binding protein-eIF4E phosphorylation.

Articles - 1ipb mentioned but not cited (9)

  1. Reversing chemoresistance by small molecule inhibition of the translation initiation complex eIF4F. Cencic R, Hall DR, Robert F, Du Y, Min J, Li L, Qui M, Lewis I, Kurtkaya S, Dingledine R, Fu H, Kozakov D, Vajda S, Pelletier J. Proc Natl Acad Sci U S A 108 1046-1051 (2011)
  2. Structural insights into the allosteric effects of 4EBP1 on the eukaryotic translation initiation factor eIF4E. Siddiqui N, Tempel W, Nedyalkova L, Volpon L, Wernimont AK, Osborne MJ, Park HW, Borden KL. J Mol Biol 415 781-792 (2012)
  3. Systematic comparison of crystal and NMR protein structures deposited in the protein data bank. Sikic K, Tomic S, Carugo O. Open Biochem J 4 83-95 (2010)
  4. Crystal structure of the Trypanosoma cruzi EIF4E5 translation factor homologue in complex with mRNA cap-4. Reolon LW, Vichier-Guerre S, de Matos BM, Dugué L, Assunção TRDS, Zanchin NIT, Pochet S, Guimarães BG. Nucleic Acids Res 47 5973-5987 (2019)
  5. Distinct features of cap binding by eIF4E1b proteins. Kubacka D, Miguel RN, Minshall N, Darzynkiewicz E, Standart N, Zuberek J. J Mol Biol 427 387-405 (2015)
  6. Turnip mosaic virus genome-linked protein VPg binds C-terminal region of cap-bound initiation factor 4E orthologue without exhibiting host cellular specificity. Okade H, Fujita Y, Miyamoto S, Tomoo K, Muto S, Miyoshi H, Natsuaki T, Rhoads RE, Ishida T. J Biochem 145 299-307 (2009)
  7. Deciphering the mechanistic effects of eIF4E phosphorylation on mRNA-cap recognition. Lama D, Verma CS. Protein Sci 29 1373-1386 (2020)
  8. Computational study on the allosteric mechanism of Leishmania major IF4E-1 by 4E-interacting protein-1: Unravelling the determinants of m7GTP cap recognition. Hernández-Alvarez L, Oliveira AB, Hernández-González JE, Chahine J, Pascutti PG, de Araujo AS, de Souza FP. Comput Struct Biotechnol J 19 2027-2044 (2021)
  9. The structure at 2.5 A resolution of human basophilic leukemia-expressed protein BLES03. Bitto E, Bingman CA, Robinson H, Allard ST, Wesenberg GE, Phillips GN. Acta Crystallogr Sect F Struct Biol Cryst Commun 61 812-817 (2005)


Reviews citing this publication (19)

  1. The molecular mechanics of eukaryotic translation. Kapp LD, Lorsch JR. Annu Rev Biochem 73 657-704 (2004)
  2. Cap and cap-binding proteins in the control of gene expression. Topisirovic I, Svitkin YV, Sonenberg N, Shatkin AJ. Wiley Interdiscip Rev RNA 2 277-298 (2011)
  3. Eukaryotic translation initiation factors and regulators. Sonenberg N, Dever TE. Curr Opin Struct Biol 13 56-63 (2003)
  4. Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation? Scheper GC, Proud CG. Eur J Biochem 269 5350-5359 (2002)
  5. Targeting the eIF4F translation initiation complex: a critical nexus for cancer development. Pelletier J, Graff J, Ruggero D, Sonenberg N. Cancer Res 75 250-263 (2015)
  6. Starting the protein synthesis machine: eukaryotic translation initiation. Preiss T, W Hentze M. Bioessays 25 1201-1211 (2003)
  7. eIF4E: new family members, new binding partners, new roles. Rhoads RE. J Biol Chem 284 16711-16715 (2009)
  8. Cap-dependent translation initiation factor eIF4E: an emerging anticancer drug target. Jia Y, Polunovsky V, Bitterman PB, Wagner CR. Med Res Rev 32 786-814 (2012)
  9. Re-capping the message. Schoenberg DR, Maquat LE. Trends Biochem Sci 34 435-442 (2009)
  10. Crystallographic and mass spectrometric characterisation of eIF4E with N7-alkylated cap derivatives. Brown CJ, McNae I, Fischer PM, Walkinshaw MD. J Mol Biol 372 7-15 (2007)
  11. CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter. Maquat LE, Hwang J, Sato H, Tang Y. Cold Spring Harb Symp Quant Biol 75 127-134 (2010)
  12. Potential therapeutic applications of RNA cap analogs. Ziemniak M, Strenkowska M, Kowalska J, Jemielity J. Future Med Chem 5 1141-1172 (2013)
  13. The Role of Cytoplasmic mRNA Cap-Binding Protein Complexes in Trypanosoma brucei and Other Trypanosomatids. Freire ER, Sturm NR, Campbell DA, de Melo Neto OP. Pathogens 6 E55 (2017)
  14. The Eukaryotic Translation Initiation Factor 4E (eIF4E) as a Therapeutic Target for Cancer. Karaki S, Andrieu C, Ziouziou H, Rocchi P. Adv Protein Chem Struct Biol 101 1-26 (2015)
  15. Decapping Scavenger (DcpS) enzyme: advances in its structure, activity and roles in the cap-dependent mRNA metabolism. Milac AL, Bojarska E, Wypijewska del Nogal A. Biochim Biophys Acta 1839 452-462 (2014)
  16. Therapeutic Opportunities in Eukaryotic Translation. Chu J, Pelletier J. Cold Spring Harb Perspect Biol 10 (2018)
  17. Control of the eIF4E activity: structural insights and pharmacological implications. Romagnoli A, D'Agostino M, Ardiccioni C, Maracci C, Motta S, La Teana A, Di Marino D. Cell Mol Life Sci 78 6869-6885 (2021)
  18. Taking a re-look at cap-binding signatures of the mRNA cap-binding protein eIF4E orthologues in trypanosomatids. Das S. Mol Cell Biochem 476 1037-1049 (2021)
  19. Structural studies of specific intermolecular interactions and self-aggregation of biomolecules and their application to drug design. Ishida T. Chem Pharm Bull (Tokyo) 57 1309-1334 (2009)

Articles citing this publication (53)

  1. Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Ueda T, Watanabe-Fukunaga R, Fukuyama H, Nagata S, Fukunaga R. Mol Cell Biol 24 6539-6549 (2004)
  2. The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Nicaise V, German-Retana S, Sanjuán R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, LeGall O. Plant Physiol 132 1272-1282 (2003)
  3. Novel "anti-reverse" cap analogs with superior translational properties. Jemielity J, Fowler T, Zuberek J, Stepinski J, Lewdorowicz M, Niedzwiecka A, Stolarski R, Darzynkiewicz E, Rhoads RE. RNA 9 1108-1122 (2003)
  4. The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, Maule AJ. Plant J 40 376-385 (2004)
  5. An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomènech P, Pitrat M, Caboche M, Dogimont C, Garcia-Mas J, Aranda MA, Bendahmane A. Plant J 48 452-462 (2006)
  6. Characterization of mammalian eIF4E-family members. Joshi B, Cameron A, Jagus R. Eur J Biochem 271 2189-2203 (2004)
  7. Phosphorylation of eIF4E attenuates its interaction with mRNA 5' cap analogs by electrostatic repulsion: intein-mediated protein ligation strategy to obtain phosphorylated protein. Zuberek J, Wyslouch-Cieszynska A, Niedzwiecka A, Dadlez M, Stepinski J, Augustyniak W, Gingras AC, Zhang Z, Burley SK, Sonenberg N, Stolarski R, Darzynkiewicz E. RNA 9 52-61 (2003)
  8. Versatility of RNA-Binding Proteins in Cancer. Wurth L. Comp Funct Genomics 2012 178525 (2012)
  9. Cap-free structure of eIF4E suggests a basis for conformational regulation by its ligands. Volpon L, Osborne MJ, Topisirovic I, Siddiqui N, Borden KL. EMBO J 25 5138-5149 (2006)
  10. Phylogenetic analysis of eIF4E-family members. Joshi B, Lee K, Maeder DL, Jagus R. BMC Evol Biol 5 48 (2005)
  11. Remodeling of the pioneer translation initiation complex involves translation and the karyopherin importin beta. Sato H, Maquat LE. Genes Dev 23 2537-2550 (2009)
  12. Structure of a viral cap-independent translation element that functions via high affinity binding to the eIF4E subunit of eIF4F. Wang Z, Treder K, Miller WA. J Biol Chem 284 14189-14202 (2009)
  13. Translation of a small subset of Caenorhabditis elegans mRNAs is dependent on a specific eukaryotic translation initiation factor 4E isoform. Dinkova TD, Keiper BD, Korneeva NL, Aamodt EJ, Rhoads RE. Mol Cell Biol 25 100-113 (2005)
  14. Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila. Hernández G, Altmann M, Sierra JM, Urlaub H, Diez del Corral R, Schwartz P, Rivera-Pomar R. Mech Dev 122 529-543 (2005)
  15. Structural features of human initiation factor 4E, studied by X-ray crystal analyses and molecular dynamics simulations. Tomoo K, Shen X, Okabe K, Nozoe Y, Fukuhara S, Morino S, Sasaki M, Taniguchi T, Miyagawa H, Kitamura K, Miura K, Ishida T. J Mol Biol 328 365-383 (2003)
  16. EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. Nieto C, Piron F, Dalmais M, Marco CF, Moriones E, Gómez-Guillamón ML, Truniger V, Gómez P, Garcia-Mas J, Aranda MA, Bendahmane A. BMC Plant Biol 7 34 (2007)
  17. Toward the mechanism of eIF4F-mediated ribosomal attachment to mammalian capped mRNAs. Kumar P, Hellen CU, Pestova TV. Genes Dev 30 1573-1588 (2016)
  18. The structure of eukaryotic translation initiation factor-4E from wheat reveals a novel disulfide bond. Monzingo AF, Dhaliwal S, Dutt-Chaudhuri A, Lyon A, Sadow JH, Hoffman DW, Robertus JD, Browning KS. Plant Physiol 143 1504-1518 (2007)
  19. Yeast m6A Methylated mRNAs Are Enriched on Translating Ribosomes during Meiosis, and under Rapamycin Treatment. Bodi Z, Bottley A, Archer N, May ST, Fray RG. PLoS One 10 e0132090 (2015)
  20. Novel cap analogs for in vitro synthesis of mRNAs with high translational efficiency. Grudzien E, Stepinski J, Jankowska-Anyszka M, Stolarski R, Darzynkiewicz E, Rhoads RE. RNA 10 1479-1487 (2004)
  21. Specificity of recognition of mRNA 5' cap by human nuclear cap-binding complex. Worch R, Niedzwiecka A, Stepinski J, Mazza C, Jankowska-Anyszka M, Darzynkiewicz E, Cusack S, Stolarski R. RNA 11 1355-1363 (2005)
  22. Structural basis for competitive inhibition of eIF4G-Mnk1 interaction by the adenovirus 100-kilodalton protein. Cuesta R, Xi Q, Schneider RJ. J Virol 78 7707-7716 (2004)
  23. Cap analogs modified with 1,2-dithiodiphosphate moiety protect mRNA from decapping and enhance its translational potential. Strenkowska M, Grzela R, Majewski M, Wnek K, Kowalska J, Lukaszewicz M, Zuberek J, Darzynkiewicz E, Kuhn AN, Sahin U, Jemielity J. Nucleic Acids Res 44 9578-9590 (2016)
  24. Structures of the human eIF4E homologous protein, h4EHP, in its m7GTP-bound and unliganded forms. Rosettani P, Knapp S, Vismara MG, Rusconi L, Cameron AD. J Mol Biol 368 691-705 (2007)
  25. Synthesis and properties of mRNA cap analogs containing imidodiphosphate moiety--fairly mimicking natural cap structure, yet resistant to enzymatic hydrolysis. Rydzik AM, Kulis M, Lukaszewicz M, Kowalska J, Zuberek J, Darzynkiewicz ZM, Darzynkiewicz E, Jemielity J. Bioorg Med Chem 20 1699-1710 (2012)
  26. Emetine suppresses SARS-CoV-2 replication by inhibiting interaction of viral mRNA with eIF4E. Kumar R, Afsar M, Khandelwal N, Chander Y, Riyesh T, Dedar RK, Gulati BR, Pal Y, Barua S, Tripathi BN, Hussain T, Kumar N. Antiviral Res 189 105056 (2021)
  27. Inhibition of mammalian target of rapamycin (mTOR) signalling in C2C12 myoblasts prevents myogenic differentiation without affecting the hyperphosphorylation of 4E-BP1. Willett M, Cowan JL, Vlasak M, Coldwell MJ, Morley SJ. Cell Signal 21 1504-1512 (2009)
  28. The proteasome inhibitor, MG132, promotes the reprogramming of translation in C2C12 myoblasts and facilitates the association of hsp25 with the eIF4F complex. Cowan JL, Morley SJ. Eur J Biochem 271 3596-3611 (2004)
  29. Discovery of Lysine-Targeted eIF4E Inhibitors through Covalent Docking. Wan X, Yang T, Cuesta A, Pang X, Balius TE, Irwin JJ, Shoichet BK, Taunton J. J Am Chem Soc 142 4960-4964 (2020)
  30. Intrinsic RNA binding by the eukaryotic initiation factor 4F depends on a minimal RNA length but not on the m7G cap. Kaye NM, Emmett KJ, Merrick WC, Jankowsky E. J Biol Chem 284 17742-17750 (2009)
  31. Structural basis for nematode eIF4E binding an m(2,2,7)G-Cap and its implications for translation initiation. Liu W, Jankowska-Anyszka M, Piecyk K, Dickson L, Wallace A, Niedzwiecka A, Stepinski J, Stolarski R, Darzynkiewicz E, Kieft J, Zhao R, Jones DN, Davis RE. Nucleic Acids Res 39 8820-8832 (2011)
  32. A multifunctional RNA recognition motif in poly(A)-specific ribonuclease with cap and poly(A) binding properties. Nilsson P, Henriksson N, Niedzwiecka A, Balatsos NA, Kokkoris K, Eriksson J, Virtanen A. J Biol Chem 282 32902-32911 (2007)
  33. Crystal structure of the RRM domain of poly(A)-specific ribonuclease reveals a novel m(7)G-cap-binding mode. Monecke T, Schell S, Dickmanns A, Ficner R. J Mol Biol 382 827-834 (2008)
  34. Structural insights into parasite eIF4E binding specificity for m7G and m2,2,7G mRNA caps. Liu W, Zhao R, McFarland C, Kieft J, Niedzwiecka A, Jankowska-Anyszka M, Stepinski J, Darzynkiewicz E, Jones DN, Davis RE. J Biol Chem 284 31336-31349 (2009)
  35. Recognition of cap structure by influenza B virus RNA polymerase is less dependent on the methyl residue than recognition by influenza A virus polymerase. Wakai C, Iwama M, Mizumoto K, Nagata K. J Virol 85 7504-7512 (2011)
  36. Identification in the ancient protist Giardia lamblia of two eukaryotic translation initiation factor 4E homologues with distinctive functions. Li L, Wang CC. Eukaryot Cell 4 948-959 (2005)
  37. Identification and Verification of m7G Modification Patterns and Characterization of Tumor Microenvironment Infiltration via Multi-Omics Analysis in Clear Cell Renal Cell Carcinoma. Dong K, Gu D, Shi J, Bao Y, Fu Z, Fang Y, Qu L, Zhu W, Jiang A, Wang L. Front Immunol 13 874792 (2022)
  38. Identification and bioinformatics characterization of translation initiation complex eIF4F components and poly(A)-binding protein from Plasmodium falciparum. Tuteja R. Commun Integr Biol 2 245-260 (2009)
  39. Charge distribution in 7-methylguanine regarding cation-pi interaction with protein factor eIF4E. Ruszczynska K, Kamienska-Trela K, Wojcik J, Stepinski J, Darzynkiewicz E, Stolarski R. Biophys J 85 1450-1456 (2003)
  40. Diverse role of three tyrosines in binding of the RNA 5' cap to the human nuclear cap binding complex. Worch R, Jankowska-Anyszka M, Niedzwiecka A, Stepinski J, Mazza C, Darzynkiewicz E, Cusack S, Stolarski R. J Mol Biol 385 618-627 (2009)
  41. Synthesis of biotin labelled cap analogue--incorporable into mRNA transcripts and promoting cap-dependent translation. Jemielity J, Lukaszewicz M, Kowalska J, Czarnecki J, Zuberek J, Darzynkiewicz E. Org Biomol Chem 10 8570-8574 (2012)
  42. Stacking efficiency and flexibility analysis of aromatic amino acids in cap-binding proteins. Worch R, Stolarski R. Proteins 71 2026-2037 (2008)
  43. Expression, purification and characterization of recombinant mouse translation initiation factor eIF4E as a dihydrofolate reductase (DHFR) fusion protein. Ghosh P, Cheng J, Chou TF, Jia Y, Avdulov S, Bitterman PB, Polunovsky VA, Wagner CR. Protein Expr Purif 60 132-139 (2008)
  44. Phosphorylation of initiation factor 4E is resistant to SB203580 in cells expressing a drug-resistant mutant of stress-activated protein kinase 2a/p38. Morley SJ, Naegele S. Cell Signal 15 741-749 (2003)
  45. The Distribution of eIF4E-Family Members across Insecta. Tettweiler G, Kowanda M, Lasko P, Sonenberg N, Hernández G. Comp Funct Genomics 2012 960420 (2012)
  46. Upregulation of eIF4E, but not other translation initiation factors, in dendritic spines during memory formation. Gindina S, Botsford B, Cowansage K, LeDoux J, Klann E, Hoeffer C, Ostroff L. J Comp Neurol 529 3112-3126 (2021)
  47. Variations of five eIF4E genes across cassava accessions exhibiting tolerant and susceptible responses to cassava brown streak disease. Shi S, Zhang X, Mandel MA, Zhang P, Zhang Y, Ferguson M, Amuge T, Rounsley S, Liu Z, Xiong Z. PLoS One 12 e0181998 (2017)
  48. Dynamical insight into Caenorhabditis elegans eIF4E recognition specificity for mono-and trimethylated structures of mRNA 5' cap. Ruszczyńska-Bartnik K, Maciejczyk M, Stolarski R. J Mol Model 17 727-737 (2011)
  49. High-throughput translational profiling with riboPLATE-seq. Metz JB, Hornstein NJ, Sharma SD, Worley J, Gonzalez C, Sims PA. Sci Rep 12 5718 (2022)
  50. Interpretation of intramolecular stacking effect on the fluorescence intensity decay of 3-methylbenzimidazolyl(5'-5')guanosine dinucleotides using a model of lifetime distribution. Kierdaszuk B, Włodarczyk J. Eur Biophys J 35 424-430 (2006)
  51. Thermodynamics of 7-methylguanosine cation stacking with tryptophan upon mRNA 5' cap binding to translation factor eIF4E. Niedzwiecka A, Stepinski J, Balaspiri L, Darzynkiewicz E, Stolarski R. Nucleosides Nucleotides Nucleic Acids 22 1557-1561 (2003)
  52. Interpretation of fluorescence decay kinetics in 3-methylbenzimidazolyl(5'-5')guanosine dinucleotides: exponential dependence on the number of phosphates in the polyphosphate bridge. Kierdaszuk B, Włodarczyk J. Eur Biophys J 36 253-259 (2007)
  53. The translation initiation factor EIF4E5 from Leishmania: crystal structure and interacting partners. de Lima GB, de Lima Cavalcanti TYV, de Brito ANALM, de Assis LA, Andrade-Vieira RP, Freire ER, da Silva Assunção TR, de Souza Reis CR, Zanchin NIT, Guimarães BG, de-Melo-Neto OP. RNA Biol 18 2433-2449 (2021)