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eIF4Es and Their Interactors from Yeast Species

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Evolution of the Protein Synthesis Machinery and Its Regulation

Abstract

Beside a general eIF4E gene version which allows for regular cap-dependent translation, yeast species show a remarkable variety of eIF4E genes which might exert specialized functions such as to downregulate eIF4E-activity or even repress specific mRNAs. Additionally, 4E-BPs (eIF4E binding proteins) modulate mRNA activity and might help certain yeast species to adapt to a large variation of possible stress conditions. In that sense, lower eukaryotes reflect the variety of regulatory mechanism for cap-dependent translation encountered among other eukaryotes.

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References

  1. Margulis L, Chapman MJ. Kingdoms and domains. An illustrated guide to the phyla of life on Earth. Amsterdam: Academic Press; 2010.

    Google Scholar 

  2. Ross D, Saxena M, Altmann M. eIF4E is an important determinant of adhesion and pseudohyphal growth of the yeast S. cerevisiae. PLoS One. 2012;7:e50773. doi:10.1371/journal.pone.0050773.

    Google Scholar 

  3. Cullen PJ, Sprague GF Jr. The regulation of filamentous growth in yeast. Genetics. 2012;190:23–49. doi:10.1534/genetics.111.127456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Youk H, Lim WA. Secreting and sensing the same molecule allows cells to achieve versatile social behaviors. Science. 2014;343:1242782. doi:10.1126/science.1242782.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Matsuo H, Li H, McGuire AM, Fletcher CM, Gingras AC, Sonenberg N, Wagner G. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol. 1997;4:717–24.

    Article  CAS  PubMed  Google Scholar 

  6. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. Cocrystal structure of the messenger RNA 5’ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell. 1997;89:951–61.

    Article  CAS  PubMed  Google Scholar 

  7. Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, McCarthy JE, Wagner G. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell. 2003;115:739–50.

    Article  CAS  PubMed  Google Scholar 

  8. Jones GD, Williams EP, Place AR, Jagus R, Bachvaroff TR. The alveolate translation initiation factor 4E family reveals a custom toolkit for translational control in core dinoflagellates. BMC Evol Biol. 2015;15:14. doi:10.1186/s12862-015-0301-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Joshi B, Lee K, Maeder DL, Jagus R. Phylogenetic analysis of eIF4E-family members. BMC Evol Biol. 2005;5:48. doi:10.1186/1471-2148-5-48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Tettweiler G, Kowanda M, Lasko P, Sonenberg N, Hernandez G. The distribution of eIF4E-family members across Insecta. Comp Funct Genomics. 2012;2012:960420. doi:10.1155/2012/960420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hernandez G, Altmann M, Sierra JM, Urlaub H, Diez del Corral R, Schwartz P, Rivera-Pomar R. Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila. Mech Dev. 2005;122:529–43. doi:10.1016/j.mod.2004.11.011.

    Google Scholar 

  12. Cho PF, Poulin F, Cho-Park YA, Cho-Park IB, Chicoine JD, Lasko P, Sonenberg N. A new paradigm for translational control: inhibition via 5’-3’ mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell. 2005;121:411–23. doi:10.1016/j.cell.2005.02.024.

    Article  CAS  PubMed  Google Scholar 

  13. 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;7:998–1003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Altmann M, Muller PP, Pelletier J, Sonenberg N, Trachsel H. A mammalian translation initiation factor can substitute for its yeast homologue in vivo. J Biol Chem. 1989;264:12145–7.

    CAS  PubMed  Google Scholar 

  15. Altmann M, Sonenberg N, Trachsel H. Translation in Saccharomyces cerevisiae: initiation factor 4E-dependent cell-free system. Mol Cell Biol. 1989;9:4467–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Altmann M, Trachsel H. Altered mRNA cap recognition activity of initiation factor 4E in the yeast cell cycle division mutant cdc33. Nucleic Acids Res. 1989;17:5923–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Altmann M, Linder P. Power of yeast for analysis of eukaryotic translation initiation. J Biol Chem. 2010;285:31907–12. doi:10.1074/jbc.R110.144196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Yoffe Y, Zuberek J, Lerer A, Lewdorowicz M, Stepinski J, Altmann M, Darzynkiewicz E, Shapira M. Binding specificities and potential roles of isoforms of eukaryotic initiation factor 4E in Leishmania. Eukaryot Cell. 2006;5:1969–79. doi:10.1128/EC.00230-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hernandez G, Vazquez-Pianzola P. Functional diversity of the eukaryotic translation initiation factors belonging to eIF4 families. Mech Dev. 2005;122:865–76. doi:10.1016/j.mod.2005.04.002.

    Article  CAS  PubMed  Google Scholar 

  20. Ptushkina M, Berthelot K, von der Haar T, Geffers L, Warwicker J, McCarthy JE. A second eIF4E protein in Schizosaccharomyces pombe has distinct eIF4G-binding properties. Nucleic Acids Res. 2001;29:4561–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ptushkina M, Malys N, McCarthy JE. eIF4E isoform 2 in Schizosaccharomyces pombe is a novel stress-response factor. EMBO Rep. 2004;5:311–6. doi:10.1038/sj.embor.7400088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ptushkina M, Fierro-Monti I, van den Heuvel J, Vasilescu S, Birkenhager R, Mita K, McCarthy JE. Schizosaccharomyces pombe has a novel eukaryotic initiation factor 4F complex containing a cap-binding protein with the human eIF4E C-terminal motif KSGST. J Biol Chem. 1996;271:32818–24.

    Article  CAS  PubMed  Google Scholar 

  23. Patrick RM, Mayberry LK, Choy G, Woodard LE, Liu JS, White A, Mullen RA, Tanavin TM, Latz CA, Browning KS. Two Arabidopsis loci encode novel eukaryotic initiation factor 4E isoforms that are functionally distinct from the conserved plant eukaryotic initiation factor 4E. Plant Physiol. 2014;164:1820–30. doi:10.1104/pp.113.227785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cawley A, Warwicker J. eIF4E-binding protein regulation of mRNAs with differential 5’-UTR secondary structure: a polyelectrostatic model for a component of protein-mRNA interactions. Nucleic Acids Res. 2012;40:7666–75. doi:10.1093/nar/gks511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Marcotrigiano J, Lomakin IB, Sonenberg N, Pestova TV, Hellen CU, Burley SK. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol Cell. 2001;7:193–203.

    Article  CAS  PubMed  Google Scholar 

  26. He H, von der Haar T, Singh CR, Ii M, Li B, Hinnebusch AG, McCarthy JE, Asano K. The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection. Mol Cell Biol. 2003;23:5431–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Jivotovskaya AV, Valasek L, Hinnebusch AG, Nielsen KH. Eukaryotic translation initiation factor 3 (eIF3) and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast. Mol Cell Biol. 2006;26:1355–72. doi:10.1128/mcb.26.4.1355-1372.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Berset C, Zurbriggen A, Djafarzadeh S, Altmann M, Trachsel H. RNA-binding activity of translation initiation factor eIF4G1 from Saccharomyces cerevisiae. RNA. 2003;9:871–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rajyaguru P, She M, Parker R. Scd6 targets eIF4G to repress translation: RGG motif proteins as a class of eIF4G-binding proteins. Mol Cell. 2012;45:244–54. doi:10.1016/j.molcel.2011.11.026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Goyer C, Altmann M, Lee HS, Blanc A, Deshmukh M, Woolford JL Jr, Trachsel H, Sonenberg N. TIF4631 and TIF4632: two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function. Mol Cell Biol. 1993;13:4860–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Clarkson BK, Gilbert WV, Doudna JA. Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae. PLoS ONE. 2010;5:e9114. doi:10.1371/journal.pone.0009114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Park EH, Zhang F, Warringer J, Sunnerhagen P, Hinnebusch AG. Depletion of eIF4G from yeast cells narrows the range of translational efficiencies genome-wide. BMC Genom. 2011;12:68. doi:10.1186/1471-2164-12-68.

    Article  CAS  Google Scholar 

  33. Altmann M, Schmitz N, Berset C, Trachsel H. A novel inhibitor of cap-dependent translation initiation in yeast: p20 competes with eIF4G for binding to eIF4E. EMBO J. 1997;16:1114–21. doi:10.1093/emboj/16.5.1114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. de la Cruz J, Iost I, Kressler D, Linder P. The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 1997;94:5201–6.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Cridge AG, Castelli LM, Smirnova JB, Selley JN, Rowe W, Hubbard SJ, McCarthy JE, Ashe MP, Grant CM, Pavitt GD. Identifying eIF4E-binding protein translationally-controlled transcripts reveals links to mRNAs bound by specific PUF proteins. Nucleic Acids Res. 2010;38:8039–50. doi:10.1093/nar/gkq686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Castelli LM, Talavera D, Kershaw CJ, Mohammad-Qureshi SS, Costello JL, Rowe W, Sims PF, Grant CM, Hubbard SJ, Ashe MP, Pavitt GD. The 4E-BP Caf20p mediates both eIF4E-dependent and independent repression of translation. PLoS Genet. 2015;11:e1005233. doi:10.1371/journal.pgen.1005233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hernandez G, Altmann M, Lasko P. Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci. 2010;35:63–73. doi:10.1016/j.tibs.2009.10.009.

    Article  CAS  PubMed  Google Scholar 

  38. Hughes JM, Ptushkina M, Karim MM, Koloteva N, von der Haar T, McCarthy JE. Translational repression by human 4E-BP1 in yeast specifically requires human eIF4E as target. J Biol Chem. 1999;274:3261–4.

    Article  CAS  PubMed  Google Scholar 

  39. Cosentino GP, Schmelzle T, Haghighat A, Helliwell SB, Hall MN, Sonenberg N. Eap1p, a novel eukaryotic translation initiation factor 4E-associated protein in Saccharomyces cerevisiae. Mol Cell Biol. 2000;20:4604–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sezen B, Seedorf M, Schiebel E. The SESA network links duplication of the yeast centrosome with the protein translation machinery. Genes Dev. 2009;23:1559–70. doi:10.1101/gad.524209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Chial HJ, Stemm-Wolf AJ, McBratney S, Winey M. Yeast Eap1p, an eIF4E-associated protein, has a separate function involving genetic stability. Curr Biol. 2000;10:1519–22.

    Article  CAS  PubMed  Google Scholar 

  42. Deloche O, de la Cruz J, Kressler D, Doere M, Linder P. A membrane transport defect leads to a rapid attenuation of translation initiation in Saccharomyces cerevisiae. Mol Cell. 2004;13:357–66.

    Article  CAS  PubMed  Google Scholar 

  43. Meier KD, Deloche O, Kajiwara K, Funato K, Riezman H. Sphingoid base is required for translation initiation during heat stress in Saccharomyces cerevisiae. Mol Biol Cell. 2006;17:1164–75. doi:10.1091/mbc.E05-11-1039.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Blewett NH, Goldstrohm AC. A eukaryotic translation initiation factor 4E-binding protein promotes mRNA decapping and is required for PUF repression. Mol Cell Biol. 2012;32:4181–94. doi:10.1128/MCB.00483-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Rendl LM, Bieman MA, Vari HK, Smibert CA. The eIF4E-binding protein Eap1p functions in Vts1p-mediated transcript decay. PLoS ONE. 2012;7:e47121. doi:10.1371/journal.pone.0047121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by Swiss National Foundation grant 31003A_146722/1.

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Authors and Affiliations

  1. Institut für Biochemie und Molekulare Medizin (IBMM), University of Bern, Bühlstr. 28, 3012, Bern, Switzerland

    Daniela Ross & Michael Altmann

Authors
  1. Daniela Ross
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  2. Michael Altmann
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Correspondence to Michael Altmann .

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Editors and Affiliations

  1. Division of Basic Research, National Institute for Cancer, Mexico City, Distrito Federal, Mexico

    Greco Hernández

  2. Institute of Marine and Environmental Te, Univ. of Maryland Center for Environment, Baltimore, Maryland, USA

    Rosemary Jagus

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Ross, D., Altmann, M. (2016). eIF4Es and Their Interactors from Yeast Species. In: Hernández, G., Jagus, R. (eds) Evolution of the Protein Synthesis Machinery and Its Regulation. Springer, Cham. https://doi.org/10.1007/978-3-319-39468-8_7

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