Structure of the hypusinylated eukaryotic translation factor eIF-5A bound to the ribosome

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1944-1951

  Schmidt, Christian ^a   Becker, Thomas ^a   Heuer, André ^a   Braunger, Katharina ^a   Shanmuganathan, Vivekanandan ^a   Pech, Markus ^a   Berninghausen, Otto ^a   Wilson, Daniel N ^a   Beckmann, Roland ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYPUSINE; INITIATION FACTOR 5A; PEPTIDYLTRANSFERASE; PROLINE; TRANSFER RNA; ELONGATION FACTOR; FACTOR EF-P; INITIATION FACTOR; MESSENGER RNA; PEPTIDE; POLYPROLINE; RNA BINDING PROTEIN;

ARTICLE; BIOCATALYSIS; CRYOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RIBOSOME; RNA STABILITY; YEAST; CHEMISTRY; GENETICS; METABOLISM; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

CRYOELECTRON MICROSCOPY; PEPTIDE ELONGATION FACTORS; PEPTIDE INITIATION FACTORS; PEPTIDES; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RIBOSOMES; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE;

EID: 84960517154     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1517     Document Type: Article

References (58)

1. Glick, B.R. and Ganoza, M.C. (1975) Identification of a soluble protein that stimulates peptide bond synthesis. Proc. Natl Acad. Sci. U.S.A., 72, 4257-4260.
2. Dever, T.E., Gutierrez, E. and Shin, B.S. (2014) The hypusine-containing translation factor eIF5A. Crit. Rev. Biochem. Mol. Biol., 49, 413-425.
3. Ude, S., Lassak, J., Starosta, A.L., Kraxenberger, T., Wilson, D.N. and Jung, K. (2013) Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science, 339, 82-85.
4. Doerfel, L.K., Wohlgemuth, I., Kothe, C., Peske, F., Urlaub, H. and Rodnina, M.V. (2013) EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science, 339, 85-88.
5. Peil, L., Starosta, A.L., Lassak, J., Atkinson, G.C., Virumae, K., Spitzer, M., Tenson, T., Jung, K., Remme, J. and Wilson, D.N. (2013) Distinct XPPX sequence motifs induce ribosome stalling, which is rescued by the translation elongation factor EF-P. Proc. Natl. Acad. Sci. U.S.A., 110, 15265-15270.
6. Woolstenhulme, C.J., Parajuli, S., Healey, D.W., Valverde, D.P., Petersen, E.N., Starosta, A.L., Guydosh, N.R., Johnson, W.E., Wilson, D.N. and Buskirk, A.R. (2013) Nascent peptides that block protein synthesis in bacteria. Proc. Natl. Acad. Sci. U.S.A., 110, E878-E887.
7. Gutierrez, E., Shin, B.S., Woolstenhulme, C.J., Kim, J.R., Saini, P., Buskirk, A.R. and Dever, T.E. (2013) eIF5A promotes translation of polyproline motifs. Mol. Cell, 51, 35-45.
8. Park, M.H., Cooper, H.L. and Folk, J.E. (1981) Identification of hypusine, an unusual amino acid, in a protein from human lymphocytes and of spermidine as its biosynthetic precursor. Proc. Natl. Acad. Sci. U.S.A., 78, 2869-2873.
9. Park, M.H., Nishimura, K., Zanelli, C.F. and Valentini, S.R. (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids, 38, 491-500.
10. Wolff, E.C., Park, M.H. and Folk, J.E. (1990) Cleavage of spermidine as the first step in deoxyhypusine synthesis. The role of NAD. J. Biol. Chem., 265, 4793-4799.
11. Navarre, W.W., Zou, S.B., Roy, H., Xie, J.L., Savchenko, A., Singer, A., Edvokimova, E., Prost, L.R., Kumar, R., Ibba, M. et al. (2010) PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol. Cell, 39, 209-221.
12. Yanagisawa, T., Sumida, T., Ishii, R., Takemoto, C. and Yokoyama, S. (2010) A paralog of lysyl-tRNA synthetase aminoacylates a conserved lysine residue in translation elongation factor P. Nat. Struct. Mol. Biol., 17, 1136-1143.
13. Peil, L., Starosta, A.L., Virumae, K., Atkinson, G.C., Tenson, T., Remme, J. and Wilson, D.N. (2012) Lys34 of translation elongation factor EF-P is hydroxylated by YfcM. Nat. Chem. Biol., 8, 695-697.
14. Lassak, J., Keilhauer, E.C., Furst, M., Wuichet, K., Godeke, J., Starosta, A.L., Chen, J.M., Sogaard-Andersen, L., Rohr, J., Wilson, D.N. et al. (2015) Arginine-rhamnosylation as new strategy to activate translation elongation factor P. Nat. Chem. Biol., 11, 266-270.
15. Rajkovic, A., Erickson, S., Witzky, A., Branson, O.E., Seo, J., Gafken, P.R., Frietas, M.A., Whitelegge, J.P., Faull, K.F., Navarre, W. et al. (2015) Cyclic rhamnosylated elongation factor P establishes antibiotic resistance in pseudomonas aeruginosa. MBio, 6, e00823.
16. Blaha, G., Stanley, R.E. and Steitz, T.A. (2009) Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science, 325, 966-970.
17. Garneau, N.L., Wilusz, J. and Wilusz, C.J. (2007) The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol., 8, 113-126.
18. Frischmeyer, P.A., van Hoof, A., O'Donnell, K., Guerrerio, A.L., Parker, R. and Dietz, H.C. (2002) An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science, 295, 2258-2261.
19. van Hoof, A., Frischmeyer, P.A., Dietz, H.C. and Parker, R. (2002) Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science, 295, 2262-2264.
20. Defenouillere, Q., Yao, Y., Mouaikel, J., Namane, A., Galopier, A., Decourty, L., Doyen, A., Malabat, C., Saveanu, C., Jacquier, A. et al. (2013) Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products. Proc. Natl. Acad. Sci. U.S.A., 110, 5046-5051.
21. Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M. and Weissman, J.S. (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc., 7, 1534-1550.
22. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
23. Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., Agard, D.A. and Cheng, Y. (2013) Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods, 10, 584-590.
24. Chen, J.Z. and Grigorieff, N. (2007) SIGNATURE: a single-particle selection system for molecular electron microscopy. J. Struct. Biol., 157, 168-173.
25. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M. and Leith, A. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol., 116, 190-199.
26. Leidig, C., Thoms, M., Holdermann, I., Bradatsch, B., Berninghausen, O., Bange, G., Sinning, I., Hurt, E. and Beckmann, R. (2014) 60S ribosome biogenesis requires rotation of the 5S ribonucleoprotein particle. Nat. Commun., 5, 1-8.
27. Penczek, P.A., Frank, J. and Spahn, C.M. (2006) A method of focused classification, based on the bootstrap 3D variance analysis, and its application to EF-G-dependent translocation. J. Struct. Biol., 154, 184-194.
28. Scheres, S.H. (2012) RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol., 180, 519-530.
29. Mindell, J.A. and Grigorieff, N. (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol., 142, 334-347.
30. Kucukelbir, A., Sigworth, F.J. and Tagare, H.D. (2014) Quantifying the local resolution of cryo-EM density maps. Nat. Methods, 11, 63-65.
31. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
32. Ben-Shem, A., Garreau de Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G. and Yusupov, M. (2011) The structure of the eukaryotic ribosome at 3.0 A resolution. Science, 334, 1524-1529.
33. Polikanov, Y.S., Steitz, T.A. and Innis, C.A. (2014) A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat. Struct. Mol. Biol., 21, 787-793.
34. Soding, J., Biegert, A. and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res., 33, W244-W248.
35. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallographica Section. D Biol. Crystallogr., 60, 2126-2132.
36. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
37. Behrmann, E., Loerke, J., Budkevich, T.V., Yamamoto, K., Schmidt, A., Penczek, P.A., Vos, M.R., Burger, J., Mielke, T., Scheerer, P. et al. (2015) Structural snapshots of actively translating human ribosomes. Cell, 161, 845-857.
38. Shoemaker, C.J. and Green, R. (2012) Translation drives mRNA quality control. Nat. Struct. Mol. Biol., 19, 594-601.
39. Jackson, R.J., Hellen, C.U. and Pestova, T.V. (2012) Termination and post-termination events in eukaryotic translation. Adv. Protein Chem. Struct. Biol., 86, 45-93.
40. Franckenberg, S., Becker, T. and Beckmann, R. (2012) Structural view on recycling of archaeal and eukaryotic ribosomes after canonical termination and ribosome rescue. Curr. Opin. Struct. Biol., 22, 786-796.
41. Zuk, D. and Jacobson, A. (1998) A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. EMBO J., 17, 2914-2925.
42. Valentini, S.R., Casolari, J.M., Oliveira, C.C., Silver, P.A. and McBride, A.E. (2002) Genetic interactions of yeast eukaryotic translation initiation factor 5A (eIF5A) reveal connections to poly(A)-binding protein and protein kinase C signaling. Genetics, 160, 393-405.
43. Schrader, R., Young, C., Kozian, D., Hoffmann, R. and Lottspeich, F. (2006) Temperature-sensitive eIF5A mutant accumulates transcripts targeted to the nonsense-mediated decay pathway. J. Biol. Chem., 281, 35336-35346.
44. Klinge, S., Voigts-Hoffmann, F., Leibundgut, M., Arpagaus, S. and Ban, N. (2011) Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science, 334, 941-948.
45. Garreau de Loubresse, N., Prokhorova, I., Holtkamp, W., Rodnina, M.V., Yusupova, G. and Yusupov, M. (2014) Structural basis for the inhibition of the eukaryotic ribosome. Nature, 513, 517-522.
46. Pestova, T.V. and Hellen, C.U. (2003) Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev., 17, 181-186.
47. Schneider-Poetsch, T., Ju, J., Eyler, D.E., Dang, Y., Bhat, S., Merrick, W.C., Green, R., Shen, B. and Liu, J.O. (2010) Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol., 6, 209-217.
48. Selmer, M., Dunham, C.M., Murphy, F.V. 4th, Weixlbaumer, A., Petry, S., Kelley, A.C., Weir, J.R. and Ramakrishnan, V. (2006 ) Structure of the 70S ribosome complexed with mRNA and tRNA. Science, 313, 1935-1942.
49. Tong, Y., Park, I., Hong, B.S., Nedyalkova, L., Tempel, W. and Park, H.W. (2009) Crystal structure of human eIF5A1: insight into functional similarity of human eIF5A1 and eIF5A2. Proteins, 75, 1040-1045.
50. Spahn, C.M., Gomez-Lorenzo, M.G., Grassucci, R.A., Jorgensen, R., Andersen, G.R., Beckmann, R., Penczek, P.A., Ballesta, J.P. and Frank, J. (2004) Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J., 23, 1008-1019.
51. Voorhees, R.M., Weixlbaumer, A., Loakes, D., Kelley, A.C. and Ramakrishnan, V. (2009) Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol., 16, 528-533.
52. Jenner, L., Demeshkina, N., Yusupova, G. and Yusupov, M. (2011) Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol., 17, 1072-1078.
53. Hofer, A., Bussiere, C. and Johnson, A.W. (2007) Mutational analysis of the ribosomal protein Rpl10 from yeast. J. Biol. Chem., 282, 32630-32639.
54. Sulima, S.O., Gulay, S.P., Anjos, M., Patchett, S., Meskauskas, A., Johnson, A.W. and Dinman, J.D. (2014) Eukaryotic rpL10 drives ribosomal rotation. Nucleic Acids Res., 42, 2049-2063.
55. Wohlgemuth, I., Brenner, S., Beringer, M. and Rodnina, M.V. (2008) Modulation of the rate of peptidyl transfer on the ribosome by the nature of substrates. J. Biol. Chem., 283, 32229-32235.
56. Pavlov, M.Y., Watts, R.E., Tan, Z., Cornish, V.W., Ehrenberg, M. and Forster, A.C. (2009) Slow peptide bond formation by proline and other N-alkylamino acids in translation. Proc. Natl. Acad. Sci. U.S.A., 106, 50-54.
57. Muto, H. and Ito, K. (2008) Peptidyl-prolyl-tRNA at the ribosomal P-site reacts poorly with puromycin. Biochem. Biophys. Res. Commun., 366, 1043-1047.
58. Johansson, M., Ieong, K.W., Trobro, S., Strazewski, P., Aqvist, J., Pavlov, M.Y. and Ehrenberg, M. (2011) pH-sensitivity of the ribosomal peptidyl transfer reaction dependent on the identity of the A-site aminoacyl-tRNA. Proc. Natl Acad. Sci. U.S.A., 108, 79-84.