Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1993 Oct;12(10):3997–4003. doi: 10.1002/j.1460-2075.1993.tb06077.x

A Saccharomyces cerevisiae homologue of mammalian translation initiation factor 4B contributes to RNA helicase activity.

M Altmann 1, P P Müller 1, B Wittmer 1, F Ruchti 1, S Lanker 1, H Trachsel 1
PMCID: PMC413682  PMID: 8404865

Abstract

The TIF3 gene of Saccharomyces cerevisiae was cloned and sequenced. The deduced amino acid sequence shows 26% identity with the sequence of mammalian translation initiation factor eIF-4B. The TIF3 gene is not essential for growth; however, its disruption results in a slow growth and cold-sensitive phenotype. In vitro translation of total yeast RNA in an extract from a TIF3 gene-disrupted strain is reduced compared with a wild-type extract. The translational defect is more pronounced at lower temperatures and can be corrected by the addition of wild-type extract or mammalian eIF-4B, but not by addition of mutant extract. In vivo translation of beta-galactosidase reporter mRNA with varying degree of RNA secondary structure in the 5' leader region in a TIF3 gene-disrupted strain shows preferential inhibition of translation of mRNA with more stable secondary structure. This indicates that Tif3 protein is an RNA helicase or contributes to RNA helicase activity in vivo.

Full text

PDF
3997

Images in this article

3999Image
on p.3999

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altmann M., Edery I., Sonenberg N., Trachsel H. Purification and characterization of protein synthesis initiation factor eIF-4E from the yeast Saccharomyces cerevisiae. Biochemistry. 1985 Oct 22;24(22):6085–6089. doi: 10.1021/bi00343a009. [DOI] [PubMed] [Google Scholar]
  2. Altmann M., Handschin C., Trachsel H. mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae. Mol Cell Biol. 1987 Mar;7(3):998–1003. doi: 10.1128/mcb.7.3.998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Altmann M., Krieger M., Trachsel H. Nucleotide sequence of the gene encoding a 20 kDa protein associated with the cap binding protein eIF-4E from Saccharomyces cerevisiae. Nucleic Acids Res. 1989 Sep 25;17(18):7520–7520. doi: 10.1093/nar/17.18.7520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baim S. B., Pietras D. F., Eustice D. C., Sherman F. A mutation allowing an mRNA secondary structure diminishes translation of Saccharomyces cerevisiae iso-1-cytochrome c. Mol Cell Biol. 1985 Aug;5(8):1839–1846. doi: 10.1128/mcb.5.8.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baim S. B., Sherman F. mRNA structures influencing translation in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1988 Apr;8(4):1591–1601. doi: 10.1128/mcb.8.4.1591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benne R., Hershey J. W. The mechanism of action of protein synthesis initiation factors from rabbit reticulocytes. J Biol Chem. 1978 May 10;253(9):3078–3087. [PubMed] [Google Scholar]
  7. Blum S., Mueller M., Schmid S. R., Linder P., Trachsel H. Translation in Saccharomyces cerevisiae: initiation factor 4A-dependent cell-free system. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6043–6046. doi: 10.1073/pnas.86.16.6043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cigan A. M., Feng L., Donahue T. F. tRNAi(met) functions in directing the scanning ribosome to the start site of translation. Science. 1988 Oct 7;242(4875):93–97. doi: 10.1126/science.3051379. [DOI] [PubMed] [Google Scholar]
  9. Coppolecchia R., Buser P., Stotz A., Linder P. A new yeast translation initiation factor suppresses a mutation in the eIF-4A RNA helicase. EMBO J. 1993 Oct;12(10):4005–4011. doi: 10.1002/j.1460-2075.1993.tb06078.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Darnbrough C., Legon S., Hunt T., Jackson R. J. Initiation of protein synthesis: evidence for messenger RNA-independent binding of methionyl-transfer RNA to the 40 S ribosomal subunit. J Mol Biol. 1973 May 25;76(3):379–403. doi: 10.1016/0022-2836(73)90511-1. [DOI] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fu L. N., Ye R. Q., Browder L. W., Johnston R. N. Translational potentiation of messenger RNA with secondary structure in Xenopus. Science. 1991 Feb 15;251(4995):807–810. doi: 10.1126/science.1990443. [DOI] [PubMed] [Google Scholar]
  13. Goyer C., Altmann M., Trachsel H., Sonenberg N. Identification and characterization of cap-binding proteins from yeast. J Biol Chem. 1989 May 5;264(13):7603–7610. [PubMed] [Google Scholar]
  14. Gulyas K. D., Donahue T. F. SSL2, a suppressor of a stem-loop mutation in the HIS4 leader encodes the yeast homolog of human ERCC-3. Cell. 1992 Jun 12;69(6):1031–1042. doi: 10.1016/0092-8674(92)90621-i. [DOI] [PubMed] [Google Scholar]
  15. Görlach M., Wittekind M., Beckman R. A., Mueller L., Dreyfuss G. Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J. 1992 Sep;11(9):3289–3295. doi: 10.1002/j.1460-2075.1992.tb05407.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hershey J. W. Translational control in mammalian cells. Annu Rev Biochem. 1991;60:717–755. doi: 10.1146/annurev.bi.60.070191.003441. [DOI] [PubMed] [Google Scholar]
  17. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kenan D. J., Query C. C., Keene J. D. RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci. 1991 Jun;16(6):214–220. doi: 10.1016/0968-0004(91)90088-d. [DOI] [PubMed] [Google Scholar]
  19. Kozak M. Role of ATP in binding and migration of 40S ribosomal subunits. Cell. 1980 Nov;22(2 Pt 2):459–467. doi: 10.1016/0092-8674(80)90356-6. [DOI] [PubMed] [Google Scholar]
  20. Kozak M., Shatkin A. J. Migration of 40 S ribosomal subunits on messenger RNA in the presence of edeine. J Biol Chem. 1978 Sep 25;253(18):6568–6577. [PubMed] [Google Scholar]
  21. Kozak M. The scanning model for translation: an update. J Cell Biol. 1989 Feb;108(2):229–241. doi: 10.1083/jcb.108.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levin D. H., Kyner D., Acs G. Protein synthesis initiation in eukaryotes. Characterization of ribosomal factors from mouse fibroblasts. J Biol Chem. 1973 Sep 25;248(18):6416–6425. [PubMed] [Google Scholar]
  23. Linder P. Molecular biology of translation in yeast. Antonie Van Leeuwenhoek. 1992 Aug;62(1-2):47–62. doi: 10.1007/BF00584462. [DOI] [PubMed] [Google Scholar]
  24. Linder P., Slonimski P. P. An essential yeast protein, encoded by duplicated genes TIF1 and TIF2 and homologous to the mammalian translation initiation factor eIF-4A, can suppress a mitochondrial missense mutation. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2286–2290. doi: 10.1073/pnas.86.7.2286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Linder P., Slonimski P. P. Sequence of the genes TIF1 and TIF2 from Saccharomyces cerevisiae coding for a translation initiation factor. Nucleic Acids Res. 1988 Nov 11;16(21):10359–10359. doi: 10.1093/nar/16.21.10359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mandel T., Trachsel H. Yeast, Saccharomyces cerevisiae, cell-free translation: the inhibition of translation by high temperature is reversible. Biochim Biophys Acta. 1989 Jan 23;1007(1):80–83. doi: 10.1016/0167-4781(89)90133-4. [DOI] [PubMed] [Google Scholar]
  27. Merrick W. C. Mechanism and regulation of eukaryotic protein synthesis. Microbiol Rev. 1992 Jun;56(2):291–315. doi: 10.1128/mr.56.2.291-315.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Milburn S. C., Hershey J. W., Davies M. V., Kelleher K., Kaufman R. J. Cloning and expression of eukaryotic initiation factor 4B cDNA: sequence determination identifies a common RNA recognition motif. EMBO J. 1990 Sep;9(9):2783–2790. doi: 10.1002/j.1460-2075.1990.tb07466.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Moldave K. Eukaryotic protein synthesis. Annu Rev Biochem. 1985;54:1109–1149. doi: 10.1146/annurev.bi.54.070185.005333. [DOI] [PubMed] [Google Scholar]
  30. Mueller P. P., Harashima S., Hinnebusch A. G. A segment of GCN4 mRNA containing the upstream AUG codons confers translational control upon a heterologous yeast transcript. Proc Natl Acad Sci U S A. 1987 May;84(9):2863–2867. doi: 10.1073/pnas.84.9.2863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Müller P. P., Trachsel H. Translation and regulation of translation in the yeast Saccharomyces cerevisiae. Eur J Biochem. 1990 Jul 31;191(2):257–261. doi: 10.1111/j.1432-1033.1990.tb19118.x. [DOI] [PubMed] [Google Scholar]
  32. Pain V. M. Initiation of protein synthesis in mammalian cells. Biochem J. 1986 May 1;235(3):625–637. doi: 10.1042/bj2350625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rhoads R. E. Cap recognition and the entry of mRNA into the protein synthesis initiation cycle. Trends Biochem Sci. 1988 Feb;13(2):52–56. doi: 10.1016/0968-0004(88)90028-x. [DOI] [PubMed] [Google Scholar]
  35. Rozen F., Edery I., Meerovitch K., Dever T. E., Merrick W. C., Sonenberg N. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol Cell Biol. 1990 Mar;10(3):1134–1144. doi: 10.1128/mcb.10.3.1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schnier J., Schwelberger H. G., Smit-McBride Z., Kang H. A., Hershey J. W. Translation initiation factor 5A and its hypusine modification are essential for cell viability in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jun;11(6):3105–3114. doi: 10.1128/mcb.11.6.3105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sonenberg N. Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation. Prog Nucleic Acid Res Mol Biol. 1988;35:173–207. doi: 10.1016/s0079-6603(08)60614-5. [DOI] [PubMed] [Google Scholar]
  40. Stanley K. K., Luzio J. P. Construction of a new family of high efficiency bacterial expression vectors: identification of cDNA clones coding for human liver proteins. EMBO J. 1984 Jun;3(6):1429–1434. doi: 10.1002/j.1460-2075.1984.tb01988.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Trachsel H., Erni B., Schreier M. H., Staehelin T. Initiation of mammalian protein synthesis. II. The assembly of the initiation complex with purified initiation factors. J Mol Biol. 1977 Nov;116(4):755–767. doi: 10.1016/0022-2836(77)90269-8. [DOI] [PubMed] [Google Scholar]
  42. Yoon H., Miller S. P., Pabich E. K., Donahue T. F. SSL1, a suppressor of a HIS4 5'-UTR stem-loop mutation, is essential for translation initiation and affects UV resistance in yeast. Genes Dev. 1992 Dec;6(12B):2463–2477. doi: 10.1101/gad.6.12b.2463. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES