A new paradigm for translational control: Inhibition via 5′-3′ mRNA tethering by Bicoid and the eIF4E cognate 4EHP

Cell

Volumn 121, Issue 3, 2005, Pages 411-423

  Cho, Park F ^a   Poulin, Francis ^a,c   Cho Park, Yoon Andrew ^a   Cho Park, Ian B ^a   Chicoine, Jarred D ^b   Lasko, Paul ^b   Sonenberg, Nahum ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAP BINDING PROTEIN; INITIATION FACTOR 4E BINDING PROTEIN; INITIATION FACTOR 4E HOMOLOGOUS PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; DROSOPHILA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION; SEQUENCE HOMOLOGY; TRANSLATION REGULATION;

EID: 18844397041     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.02.024     Document Type: Article

References (48)

1. H.J. Bellen, R.W. Levis, G. Liao, Y. He, J.W. Carlson, G. Tsang, M. Evans-Holm, P.R. Hiesinger, K.L. Schulze, and G.M. Rubin The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes Genetics 167 2004 761 781
2. A. Brasey, M. Lopez-Lastra, T. Ohlmann, N. Beerens, B. Berkhout, J.L. Darlix, and N. Sonenberg The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G2/M phase of the cell cycle J. Virol. 77 2003 3939 3949
3. G. Calero, K.F. Wilson, T. Ly, J.L. Rios-Steiner, J.C. Clardy, and R.A. Cerione Structural basis of m7GpppG binding to the nuclear cap-binding protein complex Nat. Struct. Biol. 9 2002 912 917
4. S.K. Chan, and G. Struhl Sequence-specific RNA binding by bicoid Nature 388 1997 634
5. T.D. Dinkova, B.D. Keiper, N.L. Korneeva, E.J. Aamodt, and R.E. Rhoads Translation of a small subset of Caenorhabditis elegans mRNAs is dependent on a specific eukaryotic translation initiation factor 4E isoform Mol. Cell. Biol. 25 2005 100 113
6. W. Driever, and C. Nusslein-Volhard The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner Cell 54 1988 95 104
7. W. Driever, and C. Nusslein-Volhard A gradient of bicoid protein in Drosophila embryos Cell 54 1988 83 93
8. J. Dubnau, and G. Struhl RNA recognition and translational regulation by a homeodomain protein Nature 379 1996 694 699
9. F. Gebauer, and M.W. Hentze Molecular mechanisms of translational control Nat. Rev. Mol. Cell Biol. 5 2004 827 835
10. A.C. Gingras, B. Raught, and N. Sonenberg eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation Annu. Rev. Biochem. 68 1999 913 963
11. J.D. Gross, N.J. Moerke, T. von der Haar, A.A. Lugovskoy, A.B. Sachs, J.E. McCarthy, and G. Wagner Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E Cell 115 2003 739 750
12. N. Hay, and N. Sonenberg Upstream and downstream of mTOR Genes Dev. 18 2004 1926 1945
13. G. Hernandez, M. Altmann, J.M. Sierra, H. Urlaub, R. Diez Del Corral, P. Schwartz, and R. Rivera-Pomar Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila Mech. Dev. 122 2005 529 542
14. J.W.B. Hershey, and W.C. Merrick Pathway and mechanism of initiation of protein synthesis N. Sonenberg J.W.B. Hershey M.B. Mathews Translational Control of Gene Expression 2000 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 33 88
15. A.E. Hodel, P.D. Gershon, X. Shi, S.M. Wang, and F.A. Quiocho Specific protein recognition of an mRNA cap through its alkylated base Nat. Struct. Biol. 4 1997 350 354
16. O. Johnstone, and P. Lasko Translational regulation and RNA localization in Drosophila oocytes and embryos Annu. Rev. Genet. 35 2001 365 406
17. A. Kahvejian, Y.V. Svitkin, R. Sukarieh, M.N. M'Boutchou, and N. Sonenberg Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms Genes Dev. 19 2005 104 113
18. K. Khaleghpour, Y.V. Svitkin, A.W. Craig, C.T. DeMaria, R.C. Deo, S.K. Burley, and N. Sonenberg Translational repression by a novel partner of human poly(A) binding protein, Paip2 Mol. Cell 7 2001 205 216
19. S. Kobayashi, R. Amikura, A. Nakamura, and P.F. Lasko Techniques for analyzing protein and RNA distribution in Drosophila ovaries and embryos at structural and ultrastructural resolution J. Richter Advances in Molecular Biology: A Comparative Methods Approach to the Study of Oocytes and Embryos 1999 Oxford University Press New York 426 445
20. S. Kuersten, and E.B. Goodwin The power of the 3′ UTR: translational control and development Nat. Rev. Genet. 4 2003 626 637
21. J. Lynch, and C. Desplan Evolution of development: beyond bicoid Curr. Biol. 13 2003 R557 R559
22. S. Mader, H. Lee, A. Pause, and N. Sonenberg The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins Mol. Cell. Biol. 15 1995 4990 4997
23. J. Marcotrigiano, A.C. Gingras, N. Sonenberg, and S.K. Burley Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP Cell 89 1997 951 961
24. J. Marcotrigiano, A.C. Gingras, N. Sonenberg, and S.K. Burley Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G Mol. Cell 3 1999 707 716
25. H. Matsuo, H. Li, A.M. McGuire, C.M. Fletcher, A.C. Gingras, N. Sonenberg, and G. Wagner Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein Nat. Struct. Biol. 4 1997 717 724
26. C. Mazza, M. Ohno, A. Segref, I.W. Mattaj, and S. Cusack Crystal structure of the human nuclear cap binding complex Mol. Cell 8 2001 383 396
27. A. Nakamura, K. Sato, and K. Hanyu-Nakamura Drosophila Cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis Dev. Cell 6 2004 69 78
28. M.R. Nelson, A.M. Leidal, and C.A. Smibert Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression EMBO J. 23 2004 150 159
29. D. Niessing, N. Dostatni, H. Jackle, and R. Rivera-Pomar Sequence interval within the PEST motif of Bicoid is important for translational repression of caudal mRNA in the anterior region of the Drosophila embryo EMBO J. 18 1999 1966 1973
30. D. Niessing, S. Blanke, and H. Jackle Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation Genes Dev. 16 2002 2576 2582
31. F. Poulin, and N. Sonenberg Translation mechanisms in eukaryotes J. Lapointe L. Brakier-Gingras Translation Mechanisms 2003 Landes Bioscience Austin, TX 280 297
32. S. Pyronnet, H. Imataka, A.C. Gingras, R. Fukunaga, T. Hunter, and N. Sonenberg Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E EMBO J. 18 1999 270 279
33. B. Raught, A.C. Gingras, and N. Sonenberg Regulation of ribosomal recruitment in eukaryotes N. Sonenberg J.W.B. Hershey M.B. Mathews Translational Control of Gene Expression 2000 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 245 294
34. J.D. Richter, and N. Sonenberg Regulation of cap-dependent translation by eIF4E inhibitory proteins Nature 433 2005 477 480
35. R. Rivera-Pomar, D. Niessing, U. Schmidt-Ott, W.J. Gehring, and H. Jackle RNA binding and translational suppression by bicoid Nature 379 1996 746 749
36. E. Rom, H.C. Kim, A.C. Gingras, J. Marcotrigiano, D. Favre, H. Olsen, S.K. Burley, and N. Sonenberg Cloning and characterization of 4EHP, a novel mammalian eIF4E-related cap-binding protein J. Biol. Chem. 273 1998 13104 13109
37. G.M. Rubin, L. Hong, P. Brokstein, M. Evans-Holm, E. Frise, M. Stapleton, and D.A. Harvey A Drosophila complementary DNA resource Science 287 2000 2222 2224
38. A. Sachs Physical and functional interactions between the mRNA Cap structure and the poly(A) tail N. Sonenberg J.W.B. Hershey M.B. Mathews Translational Control of Gene Expression 2000 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 447 466
39. A.J. Shatkin Capping of eucaryotic mRNAs Cell 9 1976 645 653
40. S.J. Sigrist, P.R. Thiel, D.F. Reiff, P.E. Lachance, P. Lasko, and C.M. Schuster Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions Nature 405 2000 1062 1065
41. D. St Johnston, and C. Nusslein-Volhard The origin of pattern and polarity in the Drosophila embryo Cell 68 1992 201 219
42. B. Stebbins-Boaz, Q. Cao, C.H. de Moor, R. Mendez, and J.D. Richter Maskin is a CPEB-associated factor that transiently interacts with elF-4E Mol. Cell 4 1999 1017 1027
43. Y.V. Svitkin, H. Imataka, K. Khaleghpour, A. Kahvejian, H.D. Liebig, and N. Sonenberg Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation RNA 7 2001 1743 1752
44. D. Tautz Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres Nature 332 1988 281 284
45. A.R. Tee, J.A. Tee, and J. Blenis Characterizing the interaction of the mammalian eIF4E-related protein 4EHP with 4E-BP1 FEBS Lett. 564 2004 58 62
46. T. Thomson, and P. Lasko Drosophila tudor is essential for polar granule assembly and pole cell specification, but not for posterior patterning Genesis 40 2004 164 170
47. M. Wickens, E.B. Goodwin, J. Kimble, S. Strickland, and M. Hentze Translational control of developmental decisions N. Sonenberg J.W.B. Hershey M.B. Mathews Translational Control of Gene Expression 2000 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 295 370
48. J.E. Wilhelm, M. Hilton, Q. Amos, and W.J. Henzel Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz J. Cell Biol. 163 2003 1197 1204