Eukaryotic Translation Initiation Factor 3 (eIF3) and eIF2 Can Promote mRNA Binding to 40S Subunits Independently of eIF4G in Yeast

REFERENCES

• Algire, M. A., D. Maag, P. Savio, M. G. Acker, S. Z. Tarun, Jr., A. B. Sachs, K. Asano, K. H. Nielsen, D. S. Olsen, L. Phan, A. G. Hinnebusch, and J. R. Lorsch. 2002. Development and characterization of a reconstituted yeast translation initiation system. RNA 8:382–397.
   PubMedGoogle Scholar
• Asano, K., J. Clayton, A. Shalev, and A. G. Hinnebusch. 2000. A multifactor complex of eukaryotic initiation factors eIF1, eIF2, eIF3, eIF5, and initiator tRNAMet is an important translation initiation intermediate in vivo. Genes Dev. 14:2534–2546.
   PubMed Web of Science ®Google Scholar
• Asano, K., T. G. Kinzy, W. C. Merrick, and J. W. B. Hershey. 1997. Conservation and diversity of eukaryotic translation initiation factor eIF3. J. Biol. Chem. 272:1101–1109.
   PubMedGoogle Scholar
• Asano, K., T. Krishnamoorthy, L. Phan, G. D. Pavitt, and A. G. Hinnebusch. 1999. Conserved bipartite motifs in yeast eIF5 and eIF2Bε, GTPase-activating and GDP-GTP exchange factors in translation initiation, mediate binding to their common substrate eIF2. EMBO J. 18:1673–1688.
   PubMed Web of Science ®Google Scholar
• Asano, K., L. Phan, L. Valasek, L. W. Schoenfeld, A. Shalev, J. Clayton, K. Nielsen, T. F. Donahue, and A. G. Hinnebusch. 2001. A multifactor complex of eIF1, eIF2, eIF3, eIF5, and tRNA(i)Met promotes initiation complex assembly and couples GTP hydrolysis to AUG recognition. Cold Spring Harbor Symp. Quant. Biol. 66:403–415.
   PubMedGoogle Scholar
• Asano, K., A. Shalev, L. Phan, K. Nielsen, J. Clayton, L. Valášek, T. F. Donahue, and A. G. Hinnebusch. 2001. Multiple roles for the carboxyl terminal domain of eIF5 in translation initiation complex assembly and GTPase activation. EMBO J. 20:2326–2337.
   PubMedGoogle Scholar
• Asano, K., H.-P. Vornlocher, N. J. Richter-Cook, W. C. Merrick, A. G. Hinnebusch, and J. W. B. Hershey. 1997. Structure of cDNAs encoding human eukaryotic initiation factor 3 subunits: possible roles in RNA binding and macromolecular assembly. J. Biol. Chem. 272:27042–27052.
   PubMedGoogle Scholar
• Benne, R., M. L. Brown-Luedi, and J. W. B. Hershey. 1978. Purification and characterization of protein synthesis initiation factors eIF-1, eIF-4C, eIF-4D, and eIF-5 from rabbit reticulocytes. J. Biol. Chem. 253:3070–3077.
   PubMedGoogle Scholar
• Benne, R., and J. W. B. Hershey. 1978. The mechanism of action of protein synthesis initiation factors from rabbit reticulocytes. J. Biol. Chem. 253:3078–3087.
   PubMed Web of Science ®Google Scholar
• Block, K. L., H. P. Vornlocher, and J. W. B. Hershey. 1998. Characterization of cDNAs encoding the p44 and p35 subunits of human translation initiation factor eIF3. J. Biol. Chem. 273:31901–31908.
   PubMedGoogle Scholar
• Boeke, J. D., J. Trueheart, G. Natsoulis, and G. R. Fink. 1987. 5-Fluoroorotic acid as a selective agent in yeast molecular genes. Methods Enzymol. 154:164–175.
   PubMed Web of Science ®Google Scholar
• Chaudhuri, J., D. Chowdhury, and U. Maitra. 1999. Distinct functions of eukaryotic translation initiation factors eIF1A and eIF3 in the formation of the 40S ribosomal preinitiation complex. J. Biol. Chem. 274:17975–17980.
   PubMedGoogle Scholar
• de la Cruz, J., I. Iost, D. Kressler, and P. Linder. 1997. The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94:5201–5206.
   PubMed Web of Science ®Google Scholar
• Dohmen, R. J., P. Wu, and A. Varshavsky. 1994. Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science 263:1273–1276.
   PubMed Web of Science ®Google Scholar
• Fekete, C. A., D. J. Applefield, S. A. Blakely, N. Shirokikh, T. Pestova, J. R. Lorsch, and A. G. Hinnebusch. 2005. The eIF1A C-terminal domain promotes initiation complex assembly, scanning and AUG selection in vivo. EMBO J. 24:3588–3601.
   PubMedGoogle Scholar
• Foiani, M., A. M. Cigan, C. J. Paddon, S. Harashima, and A. G. Hinnebusch. 1991. GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:3203–3216.
   PubMed Web of Science ®Google Scholar
• Gietz, R. D., A. R. Willems, and R. A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1 1: 355–360.
   Google Scholar
• Greenberg, J. R., L. Phan, Z. Gu, A. deSilva, C. Apolito, F. Sherman, A. G. Hinnebusch, and D. S. Goldfarb. 1998. Nip1p associates with 40S ribosomes and the Prt1p subunit of eIF3 and is required for efficient translation initiation. J. Biol. Chem. 273:23485–23494.
   PubMedGoogle Scholar
• Gross, J. D., N. J. Moerke, T. von der Haar, A. A. Lugovskoy, A. B. Sachs, J. E. McCarthy, and G. Wagner. 2003. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115:739–750.
   PubMed Web of Science ®Google Scholar
• Hanachi, P., J. W. B. Hershey, and H. P. Vornlocher. 1999. Characterization of the p33 subunit of eukaryotic translation initiation factor-3 from Saccharomyces cerevisiae. J. Biol. Chem. 274:8546–8553.
   PubMedGoogle Scholar
• He, H., T. von der Haar, C. R. Singh, M. Ii, B. Li, A. G. Hinnebusch, J. E. McCarthy, and K. Asano. 2003. The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection. Mol. Cell. Biol. 23:5431–5445.
   PubMedGoogle Scholar
• Hershey, J. W. B., and W. C. Merrick. 2000. Pathway and mechanism of initiation of protein synthesis, p. 33–88. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Herskowitz, I., and R. E. Jensen. 1991. Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol. 194:132–146.
   PubMedGoogle Scholar
• Hinnebusch, A. G. 2000. Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes, p. 185–243. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Hoffman, C. S., and F. Winston. 1987. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57:267–272.
   PubMed Web of Science ®Google Scholar
• Imataka, H., and N. Sonenberg. 1997. Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Mol. Cell. Biol. 17:6940–6947.
   PubMedGoogle Scholar
• Kolupaeva, V. G., A. Unbehaun, I. B. Lomakin, C. U. Hellen, and T. V. Pestova. 2005. Binding of eukaryotic initiation factor 3 to ribosomal 40S subunits and its role in ribosomal dissociation and anti-association. RNA 11:470–486.
   PubMed Web of Science ®Google Scholar
• Korneeva, N. L., B. J. Lamphear, F. L. Hennigan, and R. E. Rhoads. 2000. Mutually cooperative binding of eukaryotic translation initiation factor (eIF) 3 and eIF4A to human eIF4G-1. J. Biol. Chem. 275:41369–41376.
   PubMedGoogle Scholar
• Labib, K., J. A. Tercero, and J. F. Diffley. 2000. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288:1643–1647.
   PubMed Web of Science ®Google Scholar
• Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
   PubMed Web of Science ®Google Scholar
• Lamphear, B. J., R. Kirchweger, T. Skern, and R. E. Rhoads. 1995. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. J. Biol. Chem. 270:21975–21983.
   PubMedGoogle Scholar
• Laurino, J. P., G. M. Thompson, E. Pacheco, and B. A. Castilho. 1999. The β subunit of eukaryotic translation initiation factor 2 binds mRNA through the lysine repeats and a region comprising the C2-C2 motif. Mol. Cell. Biol. 19:173–181.
   PubMed Web of Science ®Google Scholar
• Lee, J. H., T. V. Pestova, B. S. Shin, C. Cao, S. K. Choi, and T. E. Dever. 2002. Initiation factor eIF5B catalyzes second GTP-dependent step in eukaryotic translation initiation. Proc. Natl. Acad. Sci. USA 99:16689–16694.
   PubMed Web of Science ®Google Scholar
• Lomakin, I. B., V. G. Kolupaeva, A. Marintchev, G. Wagner, and T. V. Pestova. 2003. Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing. Genes Dev. 17:2786–2797.
   PubMed Web of Science ®Google Scholar
• Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additonal modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
   PubMed Web of Science ®Google Scholar
• Maag, D., C. A. Fekete, Z. Gryczynski, and J. R. Lorsch. 2005. A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Mol. Cell 17:265–275.
   PubMedGoogle Scholar
• Maiti, T., S. Das, and U. Maitra. 2000. Isolation and functional characterization of a temperature-sensitive mutant of the yeast Saccharomyces cerevisiae in translation initiation factor eIF5: an eIF5-dependent cell-free translation system. Gene 244:109–118.
   PubMedGoogle Scholar
• Maiti, T., and U. Maitra. 1997. Characterization of translation initiation factor 5 (eIF5) from Saccharomyces cerevisiae. J. Biol. Chem. 272:1833–18340.
   Google Scholar
• Majumdar, R., A. Bandyopadhyay, and U. Maitra. 2003. Mammalian translation initiation factor eIF1 functions with eIF1A and eIF3 in the formation of a stable 40S preinitiation complex. J. Biol. Chem. 278:6580–6587.
   PubMed Web of Science ®Google Scholar
• Morino, S., H. Imataka, Y. V. Svitkin, T. V. Pestova, and N. Sonenberg. 2000. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol. Cell. Biol. 20:468–477.
   PubMedGoogle Scholar
• Nielsen, K. H., B. Szamecz, L. Valasek, A. Jivotovskaya, B. S. Shin, and A. G. Hinnebusch. 2004. Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J. 23:1166–1177.
   PubMedGoogle Scholar
• Olsen, D. S., E. M. Savner, A. Mathew, F. Zhang, T. Krishnamoorthy, L. Phan, and A. G. Hinnebusch. 2003. Domains of eIF1A that mediate binding to eIF2, eIF3 and eIF5B and promote ternary complex recruitment in vivo. EMBO J. 22:193–204.
   PubMed Web of Science ®Google Scholar
• Pestova, T. V., and V. G. Kolupaeva. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 16:2906–2922.
   PubMed Web of Science ®Google Scholar
• Pestova, T. V., I. B. Lomakin, J. H. Lee, S. K. Choi, T. E. Dever, and C. U. T. Hellen. 2000. The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403:332–335.
   PubMed Web of Science ®Google Scholar
• Peterson, D. T., W. C. Merrick, and B. Safer. 1979. Binding and release of radiolabeled eukaryotic initiation factors 2 and 3 during 80S initiation complex formation. J. Biol. Chem. 254:2509–2519.
   PubMedGoogle Scholar
• Phan, L., X. Zhang, K. Asano, J. Anderson, H. P. Vornlocher, J. R. Greenberg, J. Qin, and A. G. Hinnebusch. 1998. Identification of a translation initiation factor 3 (eIF3) core complex, conserved in yeast and mammals, that interacts with eIF5. Mol. Cell. Biol. 18:4935–4946.
   PubMedGoogle Scholar
• Prevot, D., D. Decimo, C. H. Herbreteau, F. Roux, J. Garin, J. L. Darlix, and T. Ohlmann. 2003. Characterization of a novel RNA-binding region of eIF4GI critical for ribosomal scanning. EMBO J. 22:1909–1921.
   PubMedGoogle Scholar
• Rotenberg, M. O., M. Moritz, and J. L. Woolford, Jr. 1988. Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of half-mer polyribosomes. Genes Dev. 2:160–172.
   PubMed Web of Science ®Google Scholar
• Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202–211.
   PubMed Web of Science ®Google Scholar
• Sachs, A. 2000. Physical and functional interactions between the mRNA cap structure and the poly(A) tail, p. 447–465. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Sachs, A. B., and G. Varani. 2000. Eukaryotic translation initiation: there are (at least) two sides to every story. Nat. Struct. Biol. 7:356–361.
   PubMedGoogle Scholar
• Sherman, F., G. R. Fink, and C. W. Lawrence. 1974. Methods of yeast genetics, p. 61–64. Cold Spring Harbor Laboratory, Plainview, N.Y.
   Google Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Singh, C. R., H. He, M. Ii, Y. Yamamoto, and K. Asano. 2004. Efficient incorporation of eukaryotic initiation factor 1 into the multifactor complex is critical for formation of functional ribosomal preinitiation complexes in vivo. J. Biol. Chem. 279:31910–31920.
   PubMed Web of Science ®Google Scholar
• Singh, C. R., Y. Yamamoto, and K. Asano. 2004. Physical association of eukaryotic initiation factor (eIF) 5 carboxyl-terminal domain with the lysine-rich eIF2β segment strongly enhances its binding to eIF3. J. Biol. Chem. 279:49644–49655.
   PubMedGoogle Scholar
• Trachsel, H., B. Erni, M. H. Schreier, and T. Staehelin. 1977. Initiation of mammalian protein synthesis: the assembly of the initiation complex with purified initiation factors. J. Mol. Biol. 116:755–767.
   PubMed Web of Science ®Google Scholar
• Trachsel, H., and T. Staehelin. 1979. Initiation of mammalian protein synthesis: the multiple functions of the initiation factor eIF-3. Biochim. Biophys. Acta 565:305–314.
   PubMedGoogle Scholar
• Unbehaun, A., S. I. Borukhov, C. U. Hellen, and T. V. Pestova. 2004. Release of initiation factors from 48S complexes during ribosomal subunit joining and the link between establishment of codon-anticodon base-pairing and hydrolysis of eIF2-bound GTP. Genes Dev. 18:3078–3093.
   PubMedGoogle Scholar
• Valášek, L., A. Mathew, B. S. Shin, K. H. Nielsen, B. Szamecz, and A. G. Hinnebusch. 2003. The yeast eIF3 subunits TIF32/a and NIP1/c and eIF5 make critical connections with the 40S ribosome in vivo. Genes Dev. 17:786–799.
   PubMed Web of Science ®Google Scholar
• Valášek, L., K. H. Nielsen, and A. G. Hinnebusch. 2002. Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo. EMBO J. 21:5886–5898.
   PubMed Web of Science ®Google Scholar
• Valasek, L., K. H. Nielsen, F. Zhang, C. A. Fekete, and A. G. Hinnebusch. 2004. Interactions of eukaryotic translation initiation factor 3 (eIF3) subunit NIP1/c with eIF1 and eIF5 promote preinitiation complex assembly and regulate start codon selection. Mol. Cell. Biol. 24:9437–9455.
   PubMedGoogle Scholar
• von der Haar, T., and J. E. McCarthy. 2002. Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function. Mol. Microbiol. 46:531–544.
   PubMed Web of Science ®Google Scholar
• Vornlocher, H. P., P. Hanachi, S. Ribeiro, and J. W. B. Hershey. 1999. A 110-kilodalton subunit of translation initiation factor eIF3 and an associated 135-kilodalton protein are encoded by the Saccharomyces cerevisiae TIF32 and TIF31 genes. J. Biol. Chem. 274:16802–16812.
   PubMed Web of Science ®Google Scholar
• Westermann, P., and O. Nygard. 1984. Cross-linking of mRNA to initiation factor eIF-3, 24 kDa cap binding protein and ribosomal proteins S1, S3/3a, S6 and S11 within the 48S preinitiation complex. Nucleic Acids Res. 12:8887–8897.
   PubMedGoogle Scholar