Structural basis for nematode eIF4E binding an m 2,2,7G-Cap and its implications for translation initiation

Nucleic Acids Research

Volumn 39, Issue 20, 2011, Pages 8820-8832

  Liu, Weizhi ^a   Jankowska Anyszka, Marzena ^b   Piecyk, Karolina ^a,b   Dickson, Laura ^a   Wallace, Adam ^a   Niedzwiecka, Anna ^b,c   Stepinski, Janusz ^b   Stolarski, Ryszard ^b   Darzynkiewicz, Edward ^b   Kieft, Jeffrey ^a   Zhao, Rui ^a   Jones, David N M ^a   Davis, Richard E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WARSAW   (Poland)

^c INSTITUTE OF PHYSICS   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E;

5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; ASCARIS SUUM; BINDING AFFINITY; CONTROLLED STUDY; CRYSTALLIZATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; TRANSLATION INITIATION;

ANIMALS; ASCARIS SUUM; DINUCLEOSIDE PHOSPHATES; EUKARYOTIC INITIATION FACTOR-4E; HELMINTH PROTEINS; MODELS, MOLECULAR; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN BINDING; PROTEIN CONFORMATION; RNA CAP ANALOGS; RNA, SPLICED LEADER;

ASCARIS; ASCARIS SUUM; MAMMALIA; METAZOA;

EID: 80455168244     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr650     Document Type: Article

References (55)

1. Mathews, M.B., Sonenberg, N. and Hershey, J. (2007) Origins and principles of translational control. In Mathews, M.B., Sonenberg, N. and Hershey, J. (eds), Translational Control in Biology and Medicine. Cold Spring Harbor Press, Cold Spring Harbor, pp. 1-40.
2. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell, 136, 731-745.
3. Jackson, R.J., Hellen, C.U. and Pestova, T.V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell. Biol., 11, 113-127.
4. Gingras, A.-C., Raught, B. and Sonenberg, N. (1999) eIF4 initiation factors: effectors of mrna recruitment to ribosomes and regulators of translation. Ann. Rev. Biochem., 68, 913-963.
5. Von Der Haar, T., Gross, J.D., Wagner, G. and McCarthy, J.E. (2004) The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat. Struct. Mol. Biol., 11, 503-511.
6. Rhoads, R.E. (2009) eIF4E - new family members, new binding partners, new roles. J. Biol. Chem., 284, 16711-16715.
7. Darzynkiewicz, E., Stepinski, J., Ekiel, I., Goyer, C., Sonenberg, N., Temeriusz, A., Jin, Y., Sijuwade, T., Haber, D. and Tahara, S.M. (1989) Inhibition of eukaryotic translation by nucleoside 50- monophosphate analogues of mRNA 50-cap: changes in N7 substituent affect analogue activity. Biochemistry, 28, 4771-4778.
8. Cai, A., Jankowska-Anyszka, M., Centers, A., Chlebicka, L., Stepinski, J., Stolarski, R., Darzynkiewicz, E. and Rhoads, R.E. (1999) Quantitative assessment of mRNA cap analogues as inhibitors of in vitro translation. Biochemistry, 38, 8538-8547.
9. Allen, M.A., Hillier, L.W., Waterston, R.H. and Blumenthal, T. (2011) A global analysis of C. elegans trans-splicing. Genome Res., 21, 255-264.
10. Lall, S., Friedman, C.C., Jankowska-Anyszka, M., Stepinski, J., Darzynkiewicz, E. and Davis, R.E. (2004) Contribution of trans-splicing, 50 -leader length, cap-poly(A) synergism, and initiation factors to nematode translation in an Ascaris suum embryo cell-free system. J. Biol. Chem., 279, 45573-45585.
11. Liou, R.F. and Blumenthal, T. (1990) Trans-spliced Caenorhabditis elegans mRNAs retain trimethylguanosine caps. Mol. Cell. Biol., 10, 1764-1768.
12. Maroney, P.A., Denker, J.A., Darzynkiewicz, E., Laneve, R. and Nilsen, T.W. (1995) Most mRNAs in the nematode Ascaris lumbricoides are trans-spliced: a role for spliced leader addition in translational efficiency. RNA, 1, 714-723.
13. Jankowska-Anyszka, M., Lamphear, B.J., Aamodt, E.J., Harrington, T., Darzynkiewicz, E., Stolarski, R. and Rhoads, R.E. (1998) Multiple isoforms of eukaryotic protein synthesis initiation factor 4E in C.elegans can distinguish between mono- and trimethylated mRNA cap structures. J. Biol. Chem., 273, 10538-10542.
14. Miyoshi, H., Dwyer, D.S., Keiper, B.D., Jankowska-Anyszka, M., Darzynkiewicz, E. and Rhoads, R.E. (2002) Discrimination between mono- and trimethylated cap structures by two isoforms of Caenorhabditis elegans eIF4E. EMBO J., 21, 4680-4690.
15. Keiper, B.D., Lamphear, B.J., Deshpande, A.M., Jankowska-Anyszka, M., Aamodt, E.J., Blumenthal, T. and Rhoads, R.E. (2000) Functional characterization of five eIF4E isoforms in Caenorhabditis elegans. J. Biol. Chem., 275, 10590-10596.
16. 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. (2002) Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 50 cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J. Mol. Biol., 319, 615-635.
17. Wallace, A., Filbin, M.E., Veo, B., McFarland, C., Stepinski, J., Jankowska-Anyszka, M., Darzynkiewicz, E. and Davis, R.E. (2010) The nematode eukaryotic translation initiation factor 4E/G complex works with a trans-spliced leader stem-loop to enable efficient translation of trimethylguanosine-capped RNAs. Mol. Cell Biol., 30, 1958-1970.
18. Darzynkiewicz, E., Stepinski, J., Ekiel, I., Jin, Y., Haber, D., Sijuwade, T. and Tahara, S.M. (1988) Beta-globin mRNAs capped with m7G, m2.7(2)G or m2.2.7(3)G differ in intrinsic translation efficiency. Nucleic Acids Res., 16, 8953-8962.
19. Ferguson, K.C., Heid, P.J. and Rothman, J.H. (1996) The SL1 trans-spliced leader RNA performs an essential embryonic function in Caenorhabditis elegans that can also be supplied by SL2 RNA. Genes Dev., 10, 1543-1556.
20. Hotez, P.J. (2008) Neglected infections of poverty in the United States of america. PLoS Negl. Trop. Dis., 2, e256.
21. Matsuo, H., Li, H., McGuire, A.M., Fletcher, C.M., Gingras, A.C., Sonenberg, N. and Wagner, G. (1997) Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat. Struct. Biol., 4, 717-724.
22. Marcotrigiano, J., Gingras, A.C., Sonenberg, N. and Burley, S.K. (1997) Cocrystal structure of the messenger RNA 50 cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell, 89, 951-961.
23. Monzingo, A.F., Dhaliwal, S., Dutt-Chaudhuri, A., Lyon, A., Sadow, J.H., Hoffman, D.W., Robertus, J.D. and Browning, K.S. (2007) The structure of eukaryotic translation initiation factor-4E from wheat reveals a novel disulfide bond. Plant Physiol., 143, 1504-1518.
24. Volpon, L., Osborne, M.J. and Borden, K.L. (2006) NMR assignment of human eukaryotic translation initiation factor 4E (eIF4E) in its cap-free form. J. Biomol. NMR, 36(Suppl. 1), 65.
25. Brown, C.J., McNae, I., Fischer, P.M. and Walkinshaw, M.D. (2007) Crystallographic and mass spectrometric characterisation of eIF4E with N7-alkylated cap derivatives. J. Mol. Biol., 372, 7-15.
26. Tomoo, K., Shen, X., Okabe, K., Nozoe, Y., Fukuhara, S., Morino, S., Ishida, T., Taniguchi, T., Hasegawa, H., Terashima, A. et al. (2002) Crystal structures of 7-methylguanosine (m7GTP)- and P1-7-methylguanosine-P3-adenosine- 50, 50-triphosphate (m7GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region. Biochem. J., 362, 539-544.
27. 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.
28. Rosettani, P., Knapp, S., Vismara, M.G., Rusconi, L. and Cameron, A.D. (2007) Structures of the human eIF4E homologous protein, h4EHP, in its m7GTP-bound and unliganded forms. J. Mol. Biol., 368, 691-705.
29. Rutkowska-Wlodarczyk, I., Stepinski, J., Dadlez, M., Darzynkiewicz, E., Stolarski, R. and Niedzwiecka, A. (2008) Structural changes of eIF4E upon binding to the mRNA 50 monomethylguanosine and trimethylguanosine cap. Biochemistry, 47, 2710-2720.
30. Liu, W., Zhao, R., McFarland, C., Kieft, J., Niedzwiecka, A., Jankowska-Anyszka, M., Stepinski, J., Darzynkiewicz, E., Jones, D.N. and Davis, R.E. (2009) Structural insights into parasite eIF4E binding specificity for m7G and m2, 2, 7G mRNA caps. J. Biol. Chem., 284, 31336-31349.
31. Darzynkiewicz, E., Ekiel, I., Tahara, S.M., Seliger, L.R. and Shatkin, A.J. (1985) Chemical synthesis and characterization of 7-methylguanosine cap analogs. Biochemistry, 24, 1701-1707.
32. Jankowska, M., Temeriusz, A., Stolarski, R. and Darzynkiewicz, E. (1993) Synthesis of m2, 7GTP- and m2, 2, 7GTP-sepharose 4B: new affinity resins for isolation of cap binding proteins. Collect. Czech. Chem. Commun., 58, 132-137.
33. Stepinski, J., Bretner, M., Jankowska, M., Felczak, K., Stolarski, R., Wieczorek, Z., Cai, A.-L., Rhoads, R.E., Temeriusz, A., Haber, D. et al. (1995) Synthesis and properties of P1, P2-, P1, P3- and P1, P4-dinucleoside di-, tri- and tetraphosphate mRNA 50-cap analogues. Nucleosides Nucleotides, 14, 717-721.
34. Avino, A.M., Espuny, R., Bach, M. and Eritja, R. (1995) A convenient method for the preparation of N2, N2-dimethylguanosine. Nucleosides Nucleotides, 7, 1613-1617.
35. Yoshikawa, M., Kato, T. and Takenishi, T. (1967) A novel method for phosphorylation of nucleosides to 50-nucleotides. Tetrahedron Lett., 8, 5065-5068.
36. CCP4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr., 50, 760-763.
37. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60(Pt 12 Pt 1), 2126-2132.
38. Delano, W.L. (2002) The Pymol Molecular Graphics System. Delano Scientific, San Carlos, CA.
39. Painter, J. and Merritt, E.A. (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.
40. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
41. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Ulrich, E.L., Markley, J.L., Ionides, J. and Laue, E.D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 59, 687-696.
42. Kowalska, J., Lukaszewicz, M., Zuberek, J., Ziemniak, M., Darzynkiewicz, E. and Jemielity, J. (2009) Phosphorothioate analogs of m7GTP are enzymatically stable inhibitors of cap-dependent translation. Bioorg. Med. Chem. Lett., 19, 1921-1925.
43. Marcotrigiano, J., Gingras, A.C., Sonenberg, N. and Burley, S.K. (1999) Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol. Cell, 3, 707-716.
44. Stachelska, A., Wieczorek, Z., Ruszczynska, K., Stolarski, R., Pietrzak, M., Lamphear, B.J., Rhoads, R.E., Darzynkiewicz, E. and Jankowska-Anyszka, M. (2002) Interaction of three Caenorhabditis elegans isoforms of translation initiation factor eIF4E with mono- and trimethylated mRNA 50 cap analogues. Acta Biochim. Pol., 49, 671-682.
45. Niedzwiecka, A., Darzynkiewicz, E. and Stolarski, R. (2004) Thermodynamics of mRNA 50 cap binding by eukaryotic translation initiation factor eIF4E. Biochemistry, 43, 13305-13317.
46. Strasser, A., Dickmanns, A., Luhrmann, R. and Ficner, R. (2005) Structural basis for m3G-cap-mediated nuclear import of spliceosomal UsnRNPs by snurportin1. EMBO J., 24, 2235-2243.
47. Zidek, L., Novotny, M.V. and Stone, M.J. (1999) Increased protein backbone conformational entropy upon hydrophobic ligand binding. Nat. Struct. Biol., 6, 1118-1121.
48. Ruszczynska-Bartnik, K., Maciejczyk, M. and Stolarski, R. (2011) Dynamical insight into Caenorhabditis elegans eIF4E recognition specificity for mono-and trimethylated structures of mRNA 50 cap. J. Mol. Mod., 17, 727-737.
49. Amiri, A., Keiper, B.D., Kawasaki, I., Fan, Y., Kohara, Y., Rhoads, R.E. and Strome, S. (2001) An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans. Development, 128, 3899-3912.
50. Ruszczynska, K., Kamienska-Trela, K., Wojcik, J., Stepinski, J., Darzynkiewicz, E. and Stolarski, R. (2003) Charge distribution in 7-methylguanine regarding cation-pi interaction with protein factor eIF4E. Biophys. J., 85, 1450-1456.
51. De Benedetti, A. and Graff, J.R. (2004) eIF-4E expression and its role in malignancies and metastases. Oncogene, 23, 3189-3199.
52. Koromilas, A.E., Lazaris-Karatzas, A. and Sonenberg, N. (1992) mRNAs containing extensive secondary structure in their 50 non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. EMBO J., 11, 4153-4158.
53. Mamane, Y., Petroulakis, E., Martineau, Y., Sato, T.A., Larsson, O., Rajasekhar, V.K. and Sonenberg, N. (2007) Epigenetic activation of a subset of mRNAs by eIF4E explains its effects on cell proliferation. PLoS ONE, 2, e242.
54. Grzesiek, S., Stahl, S.J., Wingfield, P.T. and Bax, A. (1996) The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry, 35, 10256-10261.
55. Gross, J.D., von Moerke, N.J., der Haar, T., Lugovsky, A.A., Sachs, A.B., McCarthy, J.E.G. and Wagner, G. (2003) Ribosome Loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell, 115, 739-750.