Cryo-EM visualization of the ribosome in termination complex with apo-RF3 and RF1

eLife

Volumn 2013, Issue 2, 2013, Pages

  Pallesen, Jesper ^a   Hashem, Yaser ^a   Korkmaz, Gürkan ^b   Koripella, Ravi Kiran ^b   Huang, Chenhui ^b   Ehrenberg, Måns ^b   Sanyal, Suparna ^b   Frank, Joachim ^a  

^a Columbia University ^*  (United States)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; GUANINE NUCLEOTIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; RELEASE FACTOR 1; RELEASE FACTOR 2; RELEASE FACTOR 3; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; BACTERIAL RNA; ESCHERICHIA COLI PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MESSENGER RNA; PRFA PROTEIN, E COLI; PRFC PROTEIN, E COLI; PROTEIN BINDING; RPLL PROTEIN, E COLI; TRANSLATION TERMINATION FACTOR;

ARCHAEON; ARTICLE; BACTERIUM; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ELECTROSTATIC IMAGING SYSTEM; IMAGE PROCESSING; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN CONFORMATION; PROTEIN PURIFICATION; RIBOSOME; RNA TRANSLATION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION TERMINATION; BINDING SITE; BIOSYNTHESIS; CRYOELECTRON MICROSCOPY; GENETICS; METABOLISM; MUTATION; TIME; ULTRASTRUCTURE;

BINDING SITES; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI PROTEINS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MOLECULAR DYNAMICS SIMULATION; MUTATION; PEPTIDE TERMINATION FACTORS; PROTEIN BINDING; PROTEIN CONFORMATION; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, BACTERIAL; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84879049657     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00411     Document Type: Article

References (54)

1. Agrawal RK, Heagle AB, Penczek P, Grassucci RA, Frank J. 1999. EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome. Nat Struct Biol 6:643-7. doi: 10.1038/10695.
2. Agrawal RK, Penczek P, Grassucci RA, Frank J. 1998. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc Natl Acad Sci USA 95:6134-8. doi: 10.1073/pnas.95.11.6134.
3. Allen GS, Zavialov A, Gursky R, Ehrenberg M, Frank J. 2005. The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121:703-12. doi: 10.1016/j.cell.2005.03.023.
4. Antoun A, Pavlov MY, Tenson T, Ehrenberg MMA. 2004. Ribosome formation from subunits studied by stopped-flow and Rayleigh light scattering. Biol Proced Online 6:35-54. doi: 10.1251/bpo71.
5. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201. doi: 10.1093/bioinformatics/bti770.
6. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98:10037-41. doi: 10.1073/pnas.181342398.
7. Berk V, Zhang W, Pai RD, Cate JH. 2006. Structural basis for mRNA and tRNA positioning on the ribosome. Proc Natl Acad Sci USA 103:15830-4. doi: 10.1073/pnas.0607541103.
8. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, Schwede T. 2009. Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 4:1-13. doi: 10.1038/nprot.2008.197.
9. Bouakaz L, Bouakaz E, Murgola EJ, Ehrenberg M, Sanyal S. 2006. The role of ribosomal protein L11 in class I release factor-mediated translation termination and translational accuracy. J Biol Chem 281:4548-56. doi: 10.1074/jbc.M510433200.
10. Clementi N, Chirkova A, Puffer B, Micura R, Polacek N. 2010. Atomic mutagenesis reveals A2660 of 23S ribosomal RNA as key to EF-G GTPase activation. Nat Chem Biol 6:344-51. doi: 10.1038/nchembio.341.
11. Datta PP, Sharma MR, Qi L, Frank J, Agrawal RK. 2005. Interaction of the G' domain of elongation factor G and the C-terminal domain of ribosomal protein L7/L12 during translocation as revealed by cryo-EM. Mol Cell 20:723-31. doi: 10.1016/j.molcel.2005.10.028.
12. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. 2004. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32:W665-7. doi: 10.1093/nar/gkh381.
13. Frank J, Gao H, Sengupta J, Gao N, Taylor DJ. 2007. The process of mRNA-tRNA translocation. Proc Natl Acad Sci USA 104:19671-8. doi: 10.1073/pnas.0708517104.
14. Frank J, Radermacher M, Penczek P, Zhu J, Li Y, Ladjadj M, et al. 1996. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116:190-9. doi: 10.1006/jsbi.1996.0030.
15. Freistroffer DV, Pavlov MY, MacDougall J, Buckingham RH, Ehrenberg M. 1997. Release factor RF3 in E. coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner. EMBO J 16:4126-33. doi: 10.1093/emboj/16.13.4126.
16. Gao H, Zhou Z, Rawat U, Huang C, Bouakaz L, Wang C, et al. 2007. RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 129:929-41. doi: 10.1016/j.cell.2007.03.050.
17. Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V. 2009. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326:694-9. doi: 10.1126/science.1179709.
18. Graille M, Heurgue-Hamard V, Champ S, Mora L, Scrima N, Ulryck N, et al. 2005. Molecular basis for bacterial class I release factor methylation by PrmC. Mol Cell 20:917-27. doi: 10.1016/j.molcel.2005.10.025.
19. Grassucci RA, Taylor DJ, Frank J. 2007. Preparation of macromolecular complexes for cryo-electron microscopy. Nat Protoc 2:3239-46. doi: 10.1038/nprot.2007.452.
20. Guex N, Peitsch MC. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714-23. doi: 10.1002/elps.1150181505.
21. Harms JM, Wilson DN, Schluenzen F, Connell SR, Stachelhaus T, Zaborowska Z, et al. 2008. Translational regulation via L11: molecular switches on the ribosome turned on and off by thiostrepton and micrococcin. Mol Cell 30:26-38. doi: 10.1016/j.molcel.2008.01.009.
22. Hauryliuk V, Hansson S, Ehrenberg M. 2008. Cofactor dependent conformational switching of GTPases. Biophys J 95:1704-15. doi: 10.1529/biophysj.107.127290.
23. Helgstrand M, Mandava CS, Mulder FA, Liljas A, Sanyal S, Akke M. 2007. The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J Mol Biol 365:468-79. doi: 10.1016/j.jmb.2006.10.025.
24. Huang C, Mandava CS, Sanyal S. 2010. The ribosomal stalk plays a key role in IF2-mediated association of the ribosomal subunits. J Mol Biol 399:145-53. doi: 10.1016/j.jmb.2010.04.009.
25. Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. J Mol Graph 14:33-8, 27-8. doi: 10.1016/0263-7855(96)00018-5.
26. Jin H, Kelley AC, Ramakrishnan V. 2011. Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc Natl Acad Sci USA 108:15798-803. doi: 10.1073/pnas.1112185108.
27. Kihira K, Shimizu Y, Shomura Y, Shibata N, Kitamura M, Nakagawa A, et al. 2012. Crystal structure analysis of the translation factor RF3 (release factor 3). FEBS Lett 586:3705-9. doi: 10.1016/j.febslet.2012.08.029.
28. Kisselev LL, Buckingham RH. 2000. Translational termination comes of age. Trends Biochem Sci 25:561-6. doi: 10.1016/S0968-0004(00)01669-8.
29. Klaholz BP. 2011. Molecular recognition and catalysis in translation termination complexes. Trends Biochem Sci 36:282-92. doi: 10.1016/j.tibs.2011.02.001.
30. Klaholz BP, Myasnikov AG, Van Heel M. 2004. Visualization of release factor 3 on the ribosome during termination of protein synthesis. Nature 427:862-5. doi: 10.1038/nature02332.
31. Kothe U, Wieden HJ, Mohr D, Rodnina MV. 2004. Interaction of helix D of elongation factor Tu with helices 4 and 5 of protein L7/12 on the ribosome. J Mol Biol 336:1011-21. doi: 10.1016/j.jmb.2003.12.080.
32. Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S, Noller HF. 2008. Structural basis for translation termination on the 70S ribosome. Nature 454:852-7. doi: 10.1038/nature07115.
33. Lei J, Frank J. 2005. Automated acquisition of cryo-electron micrographs for single particle reconstruction on an FEI Tecnai electron microscope. J Struct Biol 150:69-80. doi: 10.1016/j.jsb.2005.01.002.
34. Leijonmarck M, Liljas A. 1987. Structure of the C-terminal domain of the ribosomal protein L7/L12 from Escherichia coli at 1.7 A. J Mol Biol 195:555-79. doi: 10.1016/0022-2836(87)90183-5.
35. MacKerell AD Jr., Bashford D, Bellott M, Dunbrack RL, Evanseck JD Jr., Field MJ, et al. 1998. All-atom empirical potential for molecular modelling and dynamics studies of proteins. J. Phys. Chem. B 102:3586-616. doi: 10.1021/jp973084f.
36. Petry S, Brodersen DE, Murphy FV IV, Dunham CM, Selmer M, Tarry MJ, et al. 2005. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123:1255-66. doi: 10.1016/j.cell.2005.09.039.
37. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-12. doi: 10.1002/jcc.20084.
38. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, et al. 2005. Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-802. doi: 10.1002/jcc.20289.
39. Pintilie GD, Zhang J, Goddard TD, Chiu W, Gossard DC. 2010. Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J Struct Biol 170:427-38. doi: 10.1016/j.jsb.2010.03.007.
40. Rath BK, Frank J. 2004. Fast automatic particle picking from cryo-electron micrographs using a locally normalized cross-correlation function: a case study. J Struct Biol 145:84-90. doi: 10.1016/j.jsb.2003.11.015.
41. Rawat U, Gao H, Zavialov A, Gursky R, Ehrenberg M, Frank J. 2006. Interactions of the release factor RF1 with the ribosome as revealed by cryo-EM. J Mol Biol 357:1144-53. doi: 10.1016/j.jmb.2006.01.038.
42. Ruusala T, Ehrenberg M, Kurland CG. 1982. Catalytic effects of elongation factor Ts on polypeptide synthesis. EMBO J 1:75-8. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC552998/.
43. Schwede T, Kopp J, Guex N, Peitsch MC. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381-5. doi: 10.1093/nar/gkg520.
44. Sengupta J, Bussiere C, Pallesen J, West M, Johnson AW, Frank J. 2010. Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J Cell Biol 189:1079-86. doi: 10.1083/jcb.201001124.
45. Sethi A, O'Donoghue P, Luthey-Schulten Z. 2005. Evolutionary profiles from the QR factorization of multiple sequence alignments. Proc Natl Acad Sci USA 102:4045-50. doi: 10.1073/pnas.0409715102.
46. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, Leith A, et al. 2008. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3:1941-74. doi: 10.1038/nprot.2008.156.
47. Stark H, Rodnina MV, Rinke-Appel J, Brimacombe R, Wintermeyer W, van Heel M. 1997. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389:403-6. doi: 10.1038/38770.
48. Sternberg SH, Fei J, Prywes N, McGrath KA, Gonzalez RL Jnr, 2009. Translation factors direct intrinsic ribosome dynamics during translation termination and ribosome recycling. Nat Struct Mol Biol 16:861-8. doi: 10.1038/nsmb.1622.
49. Sund J, Ander M, Aqvist J. 2010. Principles of stop-codon reading on the ribosome. Nature 465:947-50. doi: 10.1038/nature09082.
50. Trabuco LG, Villa E, Schreiner E, Harrison CB, Schulten K. 2009. Molecular dynamics flexible fitting: a practical guide to combine cryo-electron microscopy and X-ray crystallography. Methods 49:174-80. doi: 10.1016/j.ymeth.2009.04.005.
51. Zavialov AV, Buckingham RH, Ehrenberg M. 2001. A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell 107:115-24. doi: 10.1016/S0092-8674(01)00508-6.
52. Zavialov AV, Ehrenberg M. 2003. Peptidyl-tRNA regulates the GTPase activity of translation factors. Cell 114:113-22. doi: 10.1016/S0092-8674(03)00478-1.
53. Zavialov AV, Mora L, Buckingham RH, Ehrenberg M. 2002. Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol Cell 10:789-98. doi: 10.1016/S1097-2765(02)00691-3.
54. Zhou J, Lancaster L, Trakhanov S, Noller HF. 2012. Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA 18:230-40. doi: 10.1261/rna.031187.111.