Identification and characterization of functionally critical, conserved motifs in the internal repeats and n-terminal domain of yeast translation initiation factor 4B (yeIF4B)

Journal of Biological Chemistry

Volumn 289, Issue 3, 2014, Pages 1704-1722

  Zhou, Fujun ^a   Walker, Sarah E ^a   Mitchell, Sarah F ^a,b   Lorsch, Jon R ^a   Hinnebusch, Alan G ^a  

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

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRITICAL SEQUENCE; GENERAL TRANSLATION; INITIATION FACTORS; N-TERMINAL DOMAINS; PREINITIATION COMPLEX; RNA-RECOGNITION MOTIFS; START CODONS; WILD TYPES;

AMINO ACIDS; YEAST;

NUCLEIC ACIDS;

ARGININE; ASPARTIC ACID; INITIATION FACTOR 4B; MESSENGER RNA; TRYPTOPHAN; EIF-4B; FUNGAL RNA; INITIATION FACTOR; INITIATION FACTOR 4F; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOLOGICAL FUNCTIONS; CONTROLLED STUDY; FUNGAL STRAIN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION; YEAST; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; EUKARYOTIC INITIATION FACTOR-4F; EUKARYOTIC INITIATION FACTORS; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84892661037     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.529370     Document Type: Article

References (37)

1. Pestova, T. V., Lorsch, J. R., and Hellen, C. U. (2007) in Translational Control in Biology and Medicine (Mathews, M., Sonenberg, N., and Hershey, J. W., eds) pp. 87-128, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
2. Hinnebusch, A. G., and Lorsch, J. R. (2012) The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb. Perspect. Biol. 4, 1-25
3. 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
4. Méthot, N., Pause, A., Hershey, J. W., and Sonenberg, N. (1994) The translation initiation factor eIF-4B contains an RNA-binding region that is distinct and independent from its ribonucleoprotein consensus sequence. Mol. Cell. Biol. 14, 2307-2316 (Pubitemid 24108212)
5. Naranda, T., Strong, W. B., Menaya, J., Fabbri, B. J., and Hershey, J. W. (1994) Two structural domains of initiation factor eIF-4B are involved in binding to RNA. J. Biol. Chem. 269, 14465-14472 (Pubitemid 24193999)
6. Rozovsky, N., Butterworth, A. C., and Moore, M. J. (2008) Interactions between eIF4AI and its accessory factors eIF4B and eIF4H. RNA 14, 2136-2148
7. Özeš, A. R., Feoktistova, K., Avanzino, B. C., and Fraser, C. S. (2011) Duplex unwinding and ATPase activities of the DEAD-box helicase eIF4A are coupled by eIF4G and eIF4B. J. Mol. Biol. 412, 674-687
8. Methot, N., Pickett, G., Keene, J. D., and Sonenberg, N. (1996) In vitro RNA selection identifies RNA ligands that specifically bind to eukaryotic translation initiation factor 4B: the role of the RNA remotif. RNA 2, 38-50 (Pubitemid 26371310)
9. Méthot, N., Song, M. S., and Sonenberg, N. (1996) Aregion rich in aspartic acid, arginine, tyrosine, and glycine (DRYFG) mediates eukaryotic initiation factor 4B (eIF4B) self-association and interaction with eIF3. Mol. Cell. Biol. 16, 5328-5334 (Pubitemid 26315051)
10. Altmann, M., Müller, P. P., Wittmer, B., Ruchti, F., Lanker, S., and Trachsel, H. (1993) A Saccharomyces cerevisiae homologue of mammalian translation initiation factor 4B contributes to RNA helicase activity. EMBO J. 12, 3997-4003 (Pubitemid 23282775)
11. Coppolecchia, R., Buser, P., Stotz, A., and Linder, P. (1993) A new yeast translation initiation factor suppresses a mutation in the eIF-4A RNA helicase. EMBO J. 12, 4005-4011 (Pubitemid 23282776)
12. 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. EMBO J. 14, 3820-3827
13. Rajagopal, V., Park, E. H., Hinnebusch, A. G., and Lorsch, J. R. (2012) Specific domains in yeast eIF4G strongly bias the RNA unwinding activity of the eIF4F complex toward duplexes with 5'-overhangs. J. Biol. Chem. 287, 20301-20312
14. 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
15. de la Cruz, J., Iost, I., Kressler, D., and Linder, P. (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 94, 5201-5206 (Pubitemid 27214761)
16. Park, E. H., Walker, S. E., Zhou, F., Lee, J. M., Rajagopal, V., Lorsch, J. R., and Hinnebusch, A. G. (2013) Yeast eukaryotic initiation factor (eIF) 4B enhances complex assembly between eIF4A and eIF4G in vivo. J. Biol. Chem. 288, 2340-2354
17. Andreou, A. Z., and Klostermeier, D. (2013) eIF4B and eIF4G jointly stimulate eIF4A ATPase and unwinding activities by modulation of the eIF4A conformational cycle. J. Mol. Biol., 10.1016/j.jmb.2013.09.02718.
18. 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 block an alternative pathway. Mol. Cell 39, 950-962
19. Walker, S. E., Zhou, F., Mitchell, S. F., Larson, V. S., Valasek, L., Hinnebusch, A. G., and Lorsch, J. R. (2013) Yeast eIF4B binds to the head of the 40 S ribosomal subunit and promotes mRNA recruitment through its Nterminal and internal repeat domains. RNA 19, 191-207
20. Niederberger, N., Trachsel, H., and Altmann, M. (1998) The RNA recognition motif of yeast translation initiation factor Tif3/eIF4B is required but not sufficient for RNA strand-exchange and translational activity. RNA 4, 1259-1267 (Pubitemid 28457856)
21. Sikorski, R. S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
22. Reid, G. A., and Schatz, G. (1982) Import of proteins into mitochondria. J. Biol. Chem. 257, 13062-13067
23. Cigan, A. M., Bushman, J. L., Boal, T. R., and Hinnebusch, A. G. (1993) A protein complex of translational regulators of GCN4 is the guanine nucleotide exchange factor for eIF-2 in yeast. Proc. Natl. Acad. Sci. U.S.A. 90, 5350-5354 (Pubitemid 23183036)
24. 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
25. Walker, S. E., and Fredrick, K. (2008) Preparation and evaluation of acylated tRNAs. Methods 44, 81 86 (Pubitemid 351172807)
26. Nielsen, K. H., Szamecz, B., Valásek, L., Jivotovskaya, A., Shin, B. S., and Hinnebusch, A. G. (2004) Functions of eIF3 downstream of 48 S assembly impact AUG recognition and GCN4 translational control. EMBO J. 23, 1166-1177 (Pubitemid 38436880)
27. Hinnebusch, A. G. (2011) Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75, 434-467
28. von der Haar, T., and McCarthy, J. E. (2002) Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in capcomplex function. Mol. Microbiol. 46, 531-544 (Pubitemid 35340962)
29. Chiu, W. L., Wagner, S., Herrmannová, A., Burela, L., Zhang, F., Saini, A. K., Valásek, L., and Hinnebusch, A. G. (2010) The C-terminal region of eukaryotic translation initiation factor 3a (eIF3a) promotes mRNA recruitment, scanning, and, together with eIF3j and the eIF3b RNA recognition motif, selection of AUG start codons. Mol. Cell. Biol. 30, 4415-4434
30. 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)
31. Cheng, S., and Gallie, D. R. (2006) Wheat eukaryotic initiation factor 4B organizes assembly of RNA and eIFiso4G, eIF4A, and poly(A)-binding protein. J. Biol. Chem. 281, 24351-24364 (Pubitemid 44274207)
32. 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
33. Nielsen, K. H., Behrens, M. A., He, Y., Oliveira, C. L., Jensen, L. S., Hoffmann, S. V., Pedersen, J. S., and Andersen, G. R. (2011) Synergistic activation of eIF4A by eIF4B and eIF4G. Nucleic Acids Res. 39, 2678-2689
34. Gietz, R. D., and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534 (Pubitemid 19060666)
35. Schwer, B., Linder, P., and Shuman, S. (1998) Effects of deletion mutations in the yeast Ces1 protein on cell growth and morphology and on high copy suppression of mutations in mRNA capping enzyme and translation initiation factor 4A. Nucleic Acids Res. 26, 803-809 (Pubitemid 28291280)
36. Brenner, C., Nakayama, N., Goebl, M., Tanaka, K., Toh-e, A., and Matsumoto, K. (1988) CDC33 encodes mRNA cap-binding protein eIF-4E of Saccharomyces cerevisiae. Mol. Cell. Biol. 8, 3556-3559
37. Li, Z., Vizeacoumar, F. J., Bahr, S., Li, J., Warringer, J., Vizeacoumar, F. S., Min, R., Vandersluis, B., Bellay, J., Devit, M., Fleming, J. A., Stephens, A., Haase, J., Lin, Z. Y., Baryshnikova, A., Lu, H., Yan, Z., Jin, K., Barker, S., Datti, A., Giaever, G., Nislow, C., Bulawa, C., Myers, C. L., Costanzo, M., Gingras, A. C., Zhang, Z., Blomberg, A., Bloom, K., Andrews, B., and Boone, C. (2011) Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat. Biotechnol. 29, 361-367