Single-molecule analysis of translational dynamics

Cold Spring Harbor Perspectives in Biology

Volumn 4, Issue 9, 2012, Pages

  Petrov, Alexey ^a   Chen, Jin ^a,b   O'Leary, Seán ^a   Tsai, Albert ^a,b   Puglisi, Joseph D ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2; TRANSFER RNA;

BIOLOGICAL MODEL; CHEMISTRY; CONFORMATION; METHODOLOGY; MOLECULAR BIOLOGY; PHYSIOLOGY; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA TRANSLATION; ULTRASTRUCTURE;

MODELS, GENETIC; MOLECULAR BIOLOGY; MOLECULAR CONFORMATION; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PROKARYOTIC INITIATION FACTOR-2; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, TRANSFER;

EID: 84866072282     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a011551     Document Type: Article

References (68)

1. Acker MG, Kolitz SE, Mitchell SF, Nanda JS, Lorsch JR. 2007. Reconstitution of yeast translation initiation. Methods Enzymol 430: 111-145.
2. Agirrezabala X, Lei J, Brunelle JL, Ortiz-Meoz RF, Green R, Frank J. 2008. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Molec Cell 32: 190-197.
3. Aitken CE, Puglisi JD. 2010. Following the intersubunit conformation of the ribosome during translation in real time. Nat Struct Mol Biol 17: 793-800.
4. Alatossava T, Jutte H, Kuhn A, Kellenberger E. 1985. Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187. J Bacteriol 162: 413-419.
5. Antoun A, Pavlov MY, Andersson K, Tenson T, Ehrenberg M. 2003. The roles of initiation factor 2 and guanosine triphosphate in initiation of protein synthesis. EMBO J 22: 5593-5601.
6. Antoun A, Pavlov MY, Lovmar M, Ehrenberg M. 2006. How initiation factors tune the rate of initiation of protein synthesis in bacteria. EMBO J 25: 2539-2550.
7. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-920.
8. Ben-Shem A, Jenner L, Yusupova G, Yusupov M. 2010. Crystal structure of the eukaryotic ribosome. Science 330: 1203-1209.
9. Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. 2011. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334: 1524-1529.
10. Blanchard SC, Gonzalez RL, Kim HD, Chu S, Puglisi JD. 2004a. tRNA selection and kinetic proofreading in translation. Nat Struct Mol Biol 11: 1008-1014.
11. Blanchard SC, Kim HD, Gonzalez RL Jr, Puglisi JD, Chu S. 2004b. tRNA dynamics on the ribosome during translation. Proc Natl Acad Sci 101: 12893-12898.
12. Caserta E, Tomsic J, Spurio R, La Teana A, Pon CL, Gualerzi CO. 2006. Translation initiation factor IF2 interacts with the 30S ribosomal subunit via two separate binding sites. J Mol Biol 362: 787-799.
13. Chen C, Stevens B, Kaur J, Smilansky Z, Cooperman BS, Goldman YE. 2011. Allosteric vs. spontaneous exit-site (E-site) tRNA dissociation early in protein synthesis. Proc Natl Acad Sci 108: 16980-16985.
14. Chen J, Tsai A, Petrov A, Puglisi JD. 2012. Non-fluorescent quenchers to correlate single-molecule conformational and compositional dynamics. J Am Chem Soc 134: 5734-5737.
15. Cornish PV, Ermolenko DN, Staple DW, Hoang L, Hickerson RP, Noller HF, Ha T. 2009. Following movement of the L1 stalk between three functional states in single ribosomes. Proc Natl Acad Sci 106: 2571-2576.
16. Dennis PP, Bremer H. 1974a. Differential rate of ribosomal protein synthesis in Escherichia coli B/r. J Mol Biol 84: 407-422.
17. Dennis PP, Bremer H. 1974b. Macromolecular composition during steady-state growth of Escherichia coli B-r. J Bacteriol 119: 270-281.
18. Dorywalska M, Blanchard SC, Gonzalez RL, Kim HD, Chu S, Puglisi JD. 2005. Site-specific labeling of the ribosome for single-molecule spectroscopy. Nucleic Acids Res 33: 182-189.
19. Dunkle JA, Wang L, Feldman MB, Pulk A, Chen VB, Kapral GJ, Noeske J, Richardson JS, Blanchard SC, Cate JH. 2011. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332: 981-984.
20. Fei J, Kosuri P, MacDougall DD, Gonzalez RL Jr. 2008. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol Cell 30: 348-359.
21. Fei J, Bronson JE, Hofman JM, Srinivas RL, Wiggins CH, Gonzalez RL Jr. 2009. Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc Natl Acad Sci 106: 15702-15707.
22. Fei J, Richard AC, Bronson JE, Gonzalez RL Jr. 2011. Transfer RNA-mediated regulation of ribosome dynamics during protein synthesis. Nat Struct Mol Biol 18: 1043-1051.
23. Feldman MB, Terry DS, Altman RB, Blanchard SC. 2010. Aminoglycoside activity observed on single pre-translocation ribosome complexes. Nat Chem Biol 6: 54-62.
24. Fischer N, Konevega AL, Wintermeyer W, Rodnina MV, Stark H. 2010. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 466: 329-333.
25. Frank J, Agrawal RK. 2000. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406: 318-322.
26. 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: 694-699.
27. Ha T. 2001. Single-molecule fluorescence resonance energy transfer. Methods 25: 78-86.
28. Klinge S, Voigts-Hoffmann F, Leibundgut M, Arpagaus S, Ban N. 2011. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 334: 941-948.
29. Korostelev A, Trakhanov S, Laurberg M, Noller HF. 2006. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126: 1065-1077.
30. Korostelev A, Trakhanov S, Asahara H, Laurberg M, Lancaster L, Noller HF. 2007. Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome. Proc Natl Acad Sci 104: 16840-16843.
31. Kurata S, Weixlbaumer A, Ohtsuki T, Shimazaki T, Wada T, Kirino Y, Takai K, Watanabe K, Ramakrishnan V, Suzuki T. 2008. Modified uridines with C5-methylene substituents at the first position of the tRNA anticodon stabilize U.G wobble pairing during decoding. J Biol Chem 283: 18801-18811.
32. Levene MJ, Korlach J, Turner SW, Foquet M, Craighead HG, Webb WW. 2003. Zero-mode waveguides for single-molecule analysis at high concentrations. Science 299: 682-686.
33. Lockwood AH, Chakraborty PR, Maitra U. 1971. A complex between initiation factor IF2, guanosine triphosphate, and fMet-tRNA: An intermediate in initiation complex formation. Proc Natl Acad Sci 68: 3122-3126.
34. Lockwood AH, Sarkar P, Maitra U. 1972. Release of polypeptide chain initiation factor IF-2 during initiation complex formation. Proc Natl Acad Sci 69: 3602-3605.
35. Lusk JE, Williams RJ, Kennedy EP. 1968. Magnesium and the growth of Escherichia coli. J Biol Chem 243: 2618-2624.
36. Majumdar A, Bose KK, Gupta NK. 1976. Specific binding of Excherichia coli chain initiation factor 2 to fMet-tRnaf-Met. J Biol Chem 251: 137-140.
37. Marshall RA, Dorywalska M, Puglisi JD. 2008. Irreversible chemical steps control intersubunit dynamics during translation. Proc Natl Acad Sci 105: 15364-15369.
38. Marshall RA, Aitken CE, Puglisi JD. 2009. GTP hydrolysis by IF2 guides progression of the ribosome into elongation. Mol Cell 35: 37-47.
39. Milon P, Carotti M, Konevega AL, Wintermeyer W, Rodnina MV, Gualerzi CO. 2010. The ribosome-bound initiation factor 2 recruits initiator tRNA to the 30S initiation complex. EMBO Rep 11: 312-316.
40. Mitchell SF, Walker SE, Algire MA, Park EH, Hinnebusch AG, Lorsch JR. 2010. The 50-7-methylguanosine cap on eukaryotic mRNAs serves both to stimulate canonical translation initiation and to block an alternative pathway. Mol Cell 39: 950-962.
41. Munro JB, Altman RB, O'Connor N, Blanchard SC. 2007. Identification of two distinct hybrid state intermediates on the ribosome. Mol Cell 25: 505-517.
42. Ogle JM, Brodersen DE, Clemons WM Jr, Tarry MJ, Carter AP, Ramakrishnan V. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292: 897-902.
43. Park EH, Walker SE, Lee JM, Rothenburg S, Lorsch JR, Hinnebusch AG. 2011. Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1.PABP mRNPs in vivo. EMBO J 30: 302-316.
44. Petersen HU, Roll T, Grunberg-Manago M, Clark BF. 1979. Specific interaction of initiation factor IF2 of E. coli with formylmethionyl-tRNA f Met. Biochem Biophys Res Commun 91: 1068-1074.
45. Petrov A, Puglisi JD. 2010. Site-specific labeling of Saccharomyces cerevisiae ribosomes for single-molecule manipulations. Nucleic Acids Res 38: e143.
46. Qu X, Wen JD, Lancaster L, Noller HF, Bustamante C, Ti-noco I Jr. 2011. The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature 475: 118-121.
47. Reibarkh M, Yamamoto Y, Singh CR, del Rio F, Fahmy A, Lee B, Luna RE, Ii M, Wagner G, Asano K. 2008. Eukaryotic initiation factor (eIF) 1 carries two distinct eIF5-binding faces important for multifactor assembly and AUG selection. J Biol Chem 283: 1094-1103.
48. Ruusala T, Ehrenberg M, Kurland CG. 1982. Is there proofreading during polypeptide synthesis? EMBO J 1: 741-745.
49. Schlunzen F, Zarivach R, Harms J, Bashan A, Tocilj A, Al-brecht R, Yonath A, Franceschi F. 2001. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413: 814-821.
50. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310: 827-834.
51. Spurio R, Brandi L, Caserta E, Pon CL, Gualerzi CO, Misselwitz R, Krafft C, Welfle K, Welfle H. 2000. The C-terminal subdomain (IF2 C-2) contains the entire fMet-tRNA binding site of initiation factor IF2. J Biol Chem 275: 2447-2454.
52. Sundari RM, Stringer EA, Schulman LH, Maitra U. 1976. Interaction of bacterial initiation factor 2 with initiator tRNA. J Biol Chem 251: 3338-3345.
53. Takyar S, Hickerson RP, Noller HF. 2005. mRNA helicase activity of the ribosome. Cell 120: 49-58.
54. Thompson RC, Stone PJ. 1977. Proofreading of the codonanticodon interaction on ribosomes. Proc Natl Acad Sci 74: 198-202.
55. Tomsic J, Vitali LA, Daviter T, Savelsbergh A, Spurio R, Striebeck P, Wintermeyer W, Rodnina MV, Gualerzi CO. 2000. Late events of translation initiation in bacteria: A kinetic analysis. EMBO J 19: 2127-2136.
56. Tsai A, Petrov R, Marshall A, Korlach J, Uemura S, Puglisi JD. 2012. Heterogeneous pathways and timing of factor departure during translation initiation. Nature (in press).
57. Uemura S, Dorywalska M, Lee TH, Kim HD, Puglisi JD, Chu S. 2007. Peptide bond formation destabilizes Shine-Dalgarno interaction on the ribosome. Nature 446: 454-457.
58. Uemura S, Aitken CE, Korlach J, Flusberg BA, Turner SW, Puglisi JD. 2010. Real-time tRNA transit on single translating ribosomes at codon resolution. Nature 464: 1012-1017.
59. Underwood KA, Swartz JR, Puglisi JD. 2005. Quantitative polysome analysis identifies limitations in bacterial cell-free protein synthesis. Biotechnol Bioeng 91: 425-435.
60. Valle M, Zavialov A, Sengupta J, Rawat U, Ehrenberg M, Frank J. 2003. Locking and unlocking of ribosomal motions. Cell 114: 123-134.
61. Wen JD, Lancaster L, Hodges C, Zeri AC, Yoshimura SH, Noller HF, Bustamante C, Tinoco I. 2008. Following translation by single ribosomes one codon at a time. Nature 452: 598-603.
62. Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
63. Wu XQ, RajBhandary UL. 1997. Effect of the amino acid attached to Escherichia coli initiator tRNA on its affinity for the initiation factor IF2 and on the IF2 dependence of its binding to the ribosome. J Biol Chem 272: 1891-1895.
64. Wu XQ, Iyengar P, RajBhandary UL. 1996. Ribosome-initiator tRNA complex as an intermediate in translation initiation in Escherichia coli revealed by use of mutant initiator tRNAs and specialized ribosomes. EMBO J 15: 4734-4739.
65. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.
66. Yusupova GZ, Yusupov MM, Cate JH, Noller HF. 2001. The path of messenger RNA through the ribosome. Cell 106: 233-241.
67. Yusupova G, Jenner L, Rees B, Moras D, Yusupov M. 2006. Structural basis for messenger RNA movement on the ribosome. Nature 444: 391-394.
68. Zhang W, Dunkle JA, Cate JH. 2009. Structures of the ribosome in intermediate states of ratcheting. Science 325: 1014-1017.