Structure of a human translation termination complex

Nucleic Acids Research

Volumn 43, Issue 18, 2015, Pages 8615-8626

  Matheisl, Sarah ^a   Berninghausen, Otto ^a   Becker, Thomas ^a   Beckmann, Roland ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ERF1; TRANSLATION TERMINATION COMPLEX; TRANSLATION TERMINATION FACTOR; UNCLASSIFIED DRUG; ETF1 PROTEIN, HUMAN; PEPTIDE; STOP CODON;

ARTICLE; CONFORMATION; CRYOELECTRON MICROSCOPY; HUMAN; HUMAN CYTOMEGALOVIRUS; HYDROXYLATION; IN VITRO STUDY; MOLECULAR MODEL; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RIBOSOME; STOP CODON; CHEMISTRY; CYTOMEGALOVIRUS; METABOLISM; RNA TRANSLATION;

CODON, TERMINATOR; CRYOELECTRON MICROSCOPY; CYTOMEGALOVIRUS; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE TERMINATION FACTORS; PEPTIDES; RIBOSOMES;

EID: 84957605728     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv909     Document Type: Article

References (58)

1. Ogle, J.M., Carter, A.P. and Ramakrishnan, V. (2003) Insights into the decoding mechanism from recent ribosome structures. Trends Biochem. Sci., 28, 259-266.
2. Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. and Yusupova, G. (2012) A new understanding of the decoding principle on the ribosome. Nature, 484, 256-259.
3. Zhou, J., Korostelev, A., Lancaster, L. and Noller, H.F. (2012) Crystal structures of 70S ribosomes bound to release factors RF1, RF2 and RF3. Curr. Opin. Struct. Biol., 22, 733-742.
4. Korostelev, A.A. (2011) Structural aspects of translation termination on the ribosome. RNA, 17, 1409-1421.
5. Rodnina, M.V. (2013) The ribosome as a versatile catalyst: reactions at the peptidyl transferase center. Curr. Opin. Struct. Biol., 23, 595-602.
6. Korostelev, A., Asahara, H., Lancaster, L., Laurberg, M., Hirschi, A., Zhu, J., Trakhanov, S., Scott, W.G. and Noller, H.F. (2008) Crystal structure of a translation termination complex formed with release factor RF2. Proc. Natl. Acad. Sci. U.S.A., 105, 19684-19689.
7. Laurberg, M., Asahara, H., Korostelev, A., Zhu, J., Trakhanov, S. and Noller, H.F. (2008) Structural basis for translation termination on the 70S ribosome. Nature, 454, 852-857.
8. Weixlbaumer, A., Jin, H., Neubauer, C., Voorhees, R.M., Petry, S., Kelley, A.C. and Ramakrishnan, V. (2008) Insights into Translational Termination from the Structure of RF2 Bound to the Ribosome. Science (80)., 322, 953-956.
9. Jin, H., Kelley, A.C., Loakes, D. and Ramakrishnan, V. (2010) Structure of the 70S ribosome bound to release factor 2 and a substrate analog provides insights into catalysis of peptide release. Proc. Natl. Acad. Sci. U.S.A., 107, 8593-8598.
10. Bertram, G., Bell, H.A., Ritchie, D.W., Fullerton, G. and Stansfield, I. (2000) Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA, 6, 1236-1247.
11. Song, H., Mugnier, P., Das, A.K., Webb, H.M., Evans, D.R., Tuite, M.F., Hemmings, B.A. and Barford, D. (2000) The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell, 100, 311-321.
12. Cheng, Z., Saito, K., Pisarev, A. V, Wada, M., Pisareva, V.P., Pestova, T. V, Gajda, M., Round, A., Kong, C., Lim, M. et al. (2009) Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev., 23, 1106-1118.
13. Preis, A., Heuer, A., Barrio-Garcia, C., Hauser, A., Eyler, D.E., Berninghausen, O., Green, R., Becker, T. and Beckmann, R. (2014) Cryoelectron microscopic structures of eukaryotic translation termination complexes containing eRF1-eRF3 or eRF1-ABCE1. Cell Rep., 8, 59-65.
14. Pisarev, A. V, Skabkin, M.A., Pisareva, V.P., Skabkina, O. V, Rakotondrafara, A.M., Hentze, M.W., Hellen, C.U.T. and Pestova, T. V (2010) The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell, 37, 196-210.
15. Shoemaker, C.J. and Green, R. (2011) Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proc. Natl. Acad. Sci. U.S.A., 108, E1392-E1398.
16. Alkalaeva, E.Z., Pisarev, A.V., Frolova, L.Y., Kisselev, L.L. and Pestova, T.V. (2006) In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell, 125, 1125-1136.
17. Frolova, L., Le Goff, X., Zhouravleva, G., Davydova, E., Philippe, M. and Kisselev, L. (1996) Eukaryotic polypeptide chain release factor eRF3 is an eRF1-and ribosome-dependent guanosine triphosphatase. RNA, 2, 334-341.
18. Muhs, M., Hilal, T., Mielke, T., Skabkin, M.A., Sanbonmatsu, K.Y., Pestova, T.V. and Spahn, C.M.T. (2015) Cryo-EM of ribosomal 80S complexes with termination factors reveals the translocated cricket paralysis virus IRES. Mol. Cell, 57, 422-432.
19. Behrmann, E., Loerke, J., Budkevich, T.V., Yamamoto, K., Schmidt, A., Penczek, P.A., Vos, M.R., Bürger, J., Mielke, T., Scheerer, P. et al. (2015) Structural Snapshots of Actively Translating Human Ribosomes. Cell, 161, 845-857.
20. Barthelme, D., Dinkelaker, S., Albers, S.-V., Londei, P., Ermler, U. and Tampé, R. (2011) Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. Proc. Natl. Acad. Sci. U.S.A., 108, 3228-3233.
21. Becker, T., Franckenberg, S., Wickles, S., Shoemaker, C.J., Anger, A.M., Armache, J.-P., Sieber, H., Ungewickell, C., Berninghausen, O., Daberkow, I. et al. (2012) Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature, 482, 501-506.
22. Des Georges, A., Hashem, Y., Unbehaun, A., Grassucci, R.A., Taylor, D., Hellen, C.U.T., Pestova, T.V. and Frank, J. (2014) Structure of the mammalian ribosomal pre-termination complex associated with eRF1.eRF3.GDPNP. Nucleic Acids Res., 42, 3409-3418.
23. Frolova, L., Seit-Nebi, A. and Kisselev, L. (2002) Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA, 8, 129-136.
24. Wong, L.E., Li, Y., Pillay, S., Frolova, L. and Pervushin, K. (2012) Selectivity of stop codon recognition in translation termination is modulated by multiple conformations of GTS loop in eRF1. Nucleic Acids Res., 40, 5751-5765.
25. Conard, S.E., Buckley, J., Dang, M., Bedwell, G.J., Carter, R.L., Khass, M. and Bedwell, D.M. (2012) Identification of eRF1 residues that play critical and complementary roles in stop codon recognition. RNA, 18, 1210-1221.
26. Seit-Nebi, A. (2002) Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Rep., 3, 881-886.
27. Miyazaki, K. (2011) MEGAWHOP cloning: a method of creating random mutagenesis libraries via megaprimer PCR of whole plasmids. Methods Enzymol, 498, 399-406.
28. Feng, T., Yamamoto, A., Wilkins, S.E., Sokolova, E., Yates, L.A., Münzel, M., Singh, P., Hopkinson, R.J., Fischer, R., Cockman, M.E. et al., (2014) Optimal Translational Termination Requires C4 Lysyl Hydroxylation of eRF1. Mol. Cell, 53, 645-654.
29. Mikami, S., Kobayashi, T. and Imataka, H. (2010) Cell-free protein synthesis systems with extracts from cultured human cells. Methods Mol. Biol., 607, 43-52.
30. Beckmann, R., Spahn, C.M., Eswar, N., Helmers, J., Penczek, P.A., Sali, A., Frank, J. and Blobel, G. (2001) Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell, 107, 361-372.
31. Halic, M., Becker, T., Pool, M.R., Spahn, C.M., Grassucci, R.A., Frank, J. and Beckmann, R. (2004) Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature, 427, 808-814.
32. 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.
33. Chen, J.Z. and Grigorieff, N. (2007) SIGNATURE: a single-particle selection system for molecular electron microscopy. J. Struct. Biol., 157, 168-173.
34. 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.
35. Loerke, J., Giesebrecht, J. and Spahn, C.M.T. (2010) Multiparticle cryo-EM of ribosomes. Methods Enzymol, 483, 161-177.
36. Kucukelbir, A., Sigworth, F.J. and Tagare, H.D. (2014) Quantifying the local resolution of cryo-EM density maps. Nat. Methods, 11, 63-65.
37. Scheres, S.H.W. and Chen, S. (2012) Prevention of overfitting in cryo-EM structure determination. Nat. Methods, 9, 853-854.
38. Fernández, J.J., Luque, D., Castón, J.R. and Carrascosa, J.L. (2008) Sharpening high resolution information in single particle electron cryomicroscopy. J. Struct. Biol., 164, 170-175.
39. 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.
40. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr., 60, 2126-2132.
41. Adams, P.D., Afonine, P.V., Bunkóczi, 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.
42. Bhushan, S., Meyer, H., Starosta, A.L., Becker, T., Mielke, T., Berninghausen, O., Sattler, M., Wilson, D.N. and Beckmann, R. (2010) Structural basis for translational stalling by human cytomegalovirus and fungal arginine attenuator peptide. Mol. Cell, 40, 138-146.
43. Degnin, C.R., Schleiss, M.R., Cao, J. and Geballe, A.P. (1993) Translational inhibition mediated by a short upstream open reading frame in the human cytomegalovirus gpUL4 (gp48) transcript. J. Virol., 67, 5514-5521.
44. Janzen, D.M., Frolova, L. and Geballe, A.P. (2002) Inhibition of translation termination mediated by an interaction of eukaryotic release factor 1 with a nascent peptidyl-tRNA. Mol. Cell. Biol., 22, 8562-8570.
45. Wilson, J.E., Pestova, T. V, Hellen, C.U. and Sarnow, P. (2000) Initiation of protein synthesis from the A site of the ribosome. Cell, 102, 511-520.
46. Anger, A.M., Armache, J.-P., Berninghausen, O., Habeck, M., Subklewe, M., Wilson, D.N. and Beckmann, R. (2013) Structures of the human and Drosophila 80S ribosome. Nature, 497, 80-85.
47. Khatter, H., Myasnikov, A.G., Natchiar, S.K. and Klaholz, B.P. (2015) Structure of the human 80S ribosome. Nature, 520, 640-645.
48. Alderete, J.P., Jarrahian, S. and Geballe, A.P. (1999) Translational Effects of Mutations and Polymorphisms in a Repressive Upstream Open Reading Frame of the Human Cytomegalovirus UL4 Gene. 73, 8330-8337.
49. Youngman, E.M., Brunelle, J.L., Kochaniak, A.B. and Green, R. (2004) The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell, 117, 589-599.
50. Arenz, S., Meydan, S., Starosta, A.L., Berninghausen, O., Beckmann, R., Vázquez-Laslop, N. and Wilson, D.N. (2014) Drug Sensing by the Ribosome Induces Translational Arrest via Active Site Perturbation. Mol. Cell, 56, 446-452.
51. Gutell, R.R., Cannone, J.J., Konings, D. and Gautheret, D. (2000) Predicting U-turns in ribosomal RNA with comparative sequence analysis. J. Mol. Biol., 300, 791-803.
52. Blanchet, S., Rowe, M., Haar, T., Fabret, C., Demais, S., Howard, M.J. and Namy, O. (2015) New insights into stop codon recognition by eRF1. Nucleic Acids Res., 43, 3298-3308.
53. Saito, K. and Ito, K. (2015) Genetic analysis of L123 of the tRNA-mimicking eukaryote release factor eRF1, an amino acid residue critical for discrimination of stop codons. Nucleic Acids Res., 43, 4591-4601.
54. Chavatte, L., Seit-Nebi, A., Dubovaya, V. and Favre, A. (2002) The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J., 21, 5302-5311.
55. Friedman, R.A. and Honig, B. (1995) A free energy analysis of nucleic acid base stacking in aqueous solution. Biophys. J., 69, 1528-1535.
56. Conard, S.E., Buckley, J., Dang, M., Bedwell, G.J., Carter, R.L., Khass, M. and Bedwell, D.M. (2012) Identification of eRF1 residues that play critical and complementary roles in stop codon recognition. RNA, 18, 1210-1221.
57. Kryuchkova, P., Grishin, A., Eliseev, B., Karyagina, A., Frolova, L. and Alkalaeva, E. (2013) Two-step model of stop codon recognition by eukaryotic release factor eRF1. Nucleic Acids Res., 41, 4573-4586.
58. Tate, W.P. and Mannering, S.A. (1996) Three, four or more: the translational stop signal at length. Mol. Microbiol., 21, 213-219.