Specific domains in yeast translation initiation factor eIF4G strongly bias RNA unwinding activity of the eIF4F complex toward duplexes with 5′-overhangs

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20301-20312

  Rajagopal, Vaishnavi ^a   Park, Eun Hee ^b   Hinnebusch, Alan G ^b   Lorsch, Jon R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAP-BINDING; CAP-BINDING COMPLEXES; ESSENTIAL COMPONENT; EUKARYOTIC TRANSLATION; INITIATION FACTORS; PREINITIATION COMPLEX; RNA BINDING DOMAINS; RNA DUPLEXES; RNA SUBSTRATE; RNA UNWINDING; S.CEREVISIAE; SCAFFOLDING PROTEINS; SECONDARY STRUCTURES; STRUCTURAL ELEMENTS; UNTRANSLATED REGIONS;

MACHINERY; SUBSTRATES; YEAST;

RNA;

ADENOSINE TRIPHOSPHATASE; CAP BINDING PROTEIN; INITIATION FACTOR 4F; MESSENGER RNA; SINGLE STRANDED RNA;

ARTICLE; BINDING SITE; CODON; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; TRANSLATION INITIATION;

5' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; EUKARYOTIC INITIATION FACTOR-4F; EUKARYOTIC INITIATION FACTOR-4G; PROTEIN STRUCTURE, TERTIARY; RNA CAPS; RNA FOLDING; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84862000545     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.347278     Document Type: Article

References (43)

1. Lorsch, J. R., and Dever, T. E. (2010) Molecular view of 43 S complex formation and start site selection in eukaryotic translation initiation. J. Biol. Chem. 285, 21203-21207
2. 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
3. Hinnebusch, A. G. (2011) Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75, 434-467
4. Parsyan, A., Svitkin, Y., Shahbazian, D., Gkogkas, C., Lasko, P., Merrick, W. C., and Sonenberg, N. (2011) mRNA helicases. The tacticians of translational control. Nat. Rev. Mol. Cell Biol. 12, 235-245
5. Gorbalenya, A. E., and Koonin, E. V. (1993) Helicases. Amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3, 419-429 (Pubitemid 23207576)
6. Schmid, S. R., and Linder, P. (1992) DEAD protein family of putative RNA helicases. Mol. Microbiol. 6, 283-291
7. Pause, A., Méthot, N., and Sonenberg, N. (1993) The HRIGRXXR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol. Cell. Biol. 13, 6789-6798
8. Blum, S., Schmid, S. R., Pause, A., Buser, P., Linder, P., Sonenberg, N., and Trachsel, H. (1992) ATP hydrolysis by initiation factor 4A is required for translation initiation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 89, 7664-7668
9. Nielsen, P. J., and Trachsel, H. (1988) The mouse protein synthesis initiation factor 4A gene family includes two related functional genes which are differentially expressed. EMBO J. 7, 2097-2105
10. Nielsen, P. J., McMaster, G. K., and Trachsel, H. (1985) Cloning of eukaryotic protein synthesis initiation factor genes. Isolation and characterization of cDNA clones encoding factor eIF-4A. Nucleic Acids Res. 13, 6867-6880
11. Caruthers, J. M., Johnson, E. R., and McKay, D. B. (2000) Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc. Natl. Acad. Sci. U.S.A. 97, 13080-13085
12. Oberer, M., Marintchev, A., and Wagner, G. (2005) Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev. 19, 2212-2223 (Pubitemid 41330322)
13. Schütz, P., Bumann, M., Oberholzer, A. E., Bieniossek, C., Trachsel, H., Altmann, M., and Baumann, U. (2008) Crystal structure of the yeast eIF4A-eIF4G complex. An RNA helicase controlled by protein-protein interactions. Proc. Natl. Acad. Sci. U.S.A. 105, 9564-9569 (Pubitemid 352031341)
14. Hinton, T. M., Coldwell, M. J., Carpenter, G. A., Morley, S. J., and Pain, V. M. (2007) Functional analysis of individual binding activities of the scaffold protein eIF4G. J. Biol. Chem. 282, 1695-1708 (Pubitemid 47076685)
15. Pause, A., Méthot, N., Svitkin, Y., Merrick, W. C., and Sonenberg, N. (1994) Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J. 13, 1205-1215 (Pubitemid 24074727)
16. Korneeva, N. L., First, E. A., Benoit, C. A., and Rhoads, R. E. (2005) Interaction between the NH2-terminal domain of eIF4A and the central domain of eIF4G modulates RNA-stimulated ATPase activity. J. Biol. Chem. 280, 1872-1881
17. Rogers, G. W., Jr., Richter, N. J., Lima, W. F., and Merrick, W. C. (2001) Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J. Biol. Chem. 276, 30914-30922
18. Rogers, G. W., Jr., Richter, N. J., and Merrick, W. C. (1999) Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J. Biol. Chem. 274, 12236-12244
19. Acker, M. G., Kolitz, S. E., Mitchell, S. F., Nanda, J. S., and Lorsch, J. R. (2007) Reconstitution of yeast translation initiation. Methods Enzymol. 430, 111-145
20. Mitchell, S. F., Walker, S. E., Algire, M. A., Park, E. H., Hinnebusch, A. G., and Lorsch, J. R. (2010) The 5′-7-methylguanosine cap on eukaryotic mRNAs serves both to stimulate canonical translation initiation and to block an alternative pathway. Mol. Cell 39, 950-962
21. Park, E. H., Walker, S. E., Lee, J. M., Rothenburg, S., Lorsch, J. R., and Hinnebusch, A. G. (2011) Multiple elements in the eIF4G1 N terminus promote assembly of eIF4G1·PABP mRNPs in vivo. EMBO J. 30, 302-316
22. Levin, M. K., Wang, Y. H., and Patel, S. S. (2004) The functional interaction of the hepatitis C virus helicase molecules is responsible for unwinding processivity. J. Biol. Chem. 279, 26005-26012 (Pubitemid 38798742)
23. Lorsch, J. R., and Herschlag, D. (1998) The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 37, 2180-2193 (Pubitemid 28119291)
24. Berset, C., Zurbriggen, A., Djafarzadeh, S., Altmann, M., and Trachsel, H. (2003) RNA-binding activity of translation initiation factor eIF4G1 from Saccharomyces cerevisiae. RNA 9, 871-880 (Pubitemid 36734784)
25. Lamphear, B. J., Kirchweger, R., Skern, T., and Rhoads, R. E. (1995) Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270, 21975-21983
26. Tarun, S. Z., Jr., and Sachs, A. B. (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15, 7168-7177
27. Rogers, G. W., Jr., Lima, W. F., and Merrick, W. C. (2001) Further characterization of the helicase activity of eIF4A. Substrate specificity. J. Biol. Chem. 276, 12598-12608
28. Rozen, F., Edery, I., Meerovitch, K., Dever, T. E., Merrick, W. C., and Sonenberg, N. (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 10, 1134-1144
29. Marintchev, A., Edmonds, K. A., Marintcheva, B., Hendrickson, E., Oberer, M., Suzuki, C., Herdy, B., Sonenberg, N., and Wagner, G. (2009) Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136, 447-460
30. Bi, X., and Goss, D. J. (2000) Wheat germ poly(A)-binding protein increases the ATPase and the RNA helicase activity of translation initiation factors eIF4A, eIF4B, and eIF-iso4F. J. Biol. Chem. 275, 17740-17746 (Pubitemid 30430823)
31. Bi, X., Ren, J., and Goss, D. J. (2000) Wheat germ translation initiation factor eIF4B affects eIF4A and eIFiso4F helicase activity by increasing the ATP binding affinity of eIF4A. Biochemistry 39, 5758-5765 (Pubitemid 30307964)
32. Altmann, M., Wittmer, B., Méthot, N., Sonenberg, N., and Trachsel, H. (1995) The Saccharomyces cerevisiae translation initiation factor Tif3 and its mammalian homologue, eIF-4B, have RNA annealing activity.EMBOJ. 14, 3820-3827
33. Kaye, N. M., Emmett, K. J., Merrick, W. C., and Jankowsky, E. (2009) Intrinsic RNA binding by the eukaryotic initiation factor 4F depends on a minimal RNA length but not on the m7G cap. J. Biol. Chem. 284, 17742-17750
34. Prévôt, D., Décimo, D., Herbreteau, C. H., Roux, F., Garin, J., Darlix, J. L., and Ohlmann, T. (2003) Characterization of a novel RNA-binding region of eIF4GI critical for ribosomal scanning. EMBO J. 22, 1909-1921 (Pubitemid 36460147)
35. Treder, K., Kneller, E. L., Allen, E. M., Wang, Z., Browning, K. S., and Miller, W. A. (2008) The 3′-cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 14, 134-147
36. Gallie, D. R. (2001) Cap-independent translation conferred by the 5′-leader of tobacco etch virus is eukaryotic initiation factor 4G-dependent. J. Virol. 75, 12141-12152
37. De Gregorio, E., Preiss, T., and Hentze, M. W. (1998) Translational activation of uncapped mRNAs by the central part of human eIF4G is 5′-enddependent. RNA 4, 828-836 (Pubitemid 28317830)
38. Tarun, S. Z., Jr., and Sachs, A. B. (1997) Binding of eukaryotic translation initiation factor 4E (eIF4E) to eIF4G represses translation of uncapped mRNA. Mol. Cell. Biol. 17, 6876-6886
39. Borman, A. M., Kirchweger, R., Ziegler, E., Rhoads, R. E., Skern, T., and Kean, K. M. (1997) eIF4G and its proteolytic cleavage products. Effect on initiation of protein synthesis from capped, uncapped, and IRES-containing mRNAs. RNA 3, 186-196
40. Ohlmann, T., Rau, M., Pain, V. M., and Morley, S. J. (1996) The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J. 15, 1371-1382 (Pubitemid 26093473)
41. Vassilenko, K. S., Alekhina, O. M., Dmitriev, S. E., Shatsky, I. N., and Spirin, A. S. (2011) Unidirectional constant rate motion of the ribosomal scanning particle during eukaryotic translation initiation. Nucleic Acids Res. 39, 5555-5567
42. Berthelot, K., Muldoon, M., Rajkowitsch, L., Hughes, J., and McCarthy, J. E. (2004) Dynamics and processivity of 40 S ribosome scanning on mRNA in yeast. Mol. Microbiol. 51, 987-1001 (Pubitemid 38270794)
43. Spirin, A. S. (2009) How does a scanning ribosomal particle move along the 5′-untranslated region of eukaryotic mRNA? Brownian Ratchet model. Biochemistry 48, 10688-10692