Allosteric vs. spontaneous exit-site (E-site) tRNA dissociation early in protein synthesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 41, 2011, Pages 16980-16985

  Chen, Chunlai ^a   Stevens, Benjamin ^a,b   Kaur, Jaskiran ^b,c   Smilansky, Zeev ^b   Cooperman, Barry S ^c   Goldman, Yale E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Anima Cell Metrology Inc   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alternating wavelength laser excitation (ALEX); Classical state; FRET; Hybrid state; Multi translation cycles

Indexed keywords

AMINOACYL TRANSFER RNA; ARGININE TRANSFER RNA; PHENYLALANINE TRANSFER RNA; TRANSFER RNA;

ALLOSTERISM; ALTERNATING WAVELENGTH LASER EXCITATION; ARTICLE; CODON; DISSOCIATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; RIBOSOME; RNA BINDING; RNA CONFORMATION; RNA SYNTHESIS; RNA TRANSLATION; TRANSFER RNA EXIT SITE;

ALLOSTERIC SITE; AMINO ACID SEQUENCE; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; BIOPHYSICAL PHENOMENA; FLUORESCENCE RESONANCE ENERGY TRANSFER; KINETICS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER;

EID: 80054769463     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1106999108     Document Type: Article

References (58)

1. Schmeing TM, Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature 461:1234-1242.
2. Ramakrishnan V (2002) Ribosome structure and the mechanism of translation. Cell 108:557-572.
3. Simonetti A, et al. (2009) A structural view of translation initiation in bacteria. Cell Mol Life Sci 66:423-436.
4. Mitra K, Frank J (2006) Ribosome dynamics: Insights from atomic structure modeling into cryo-electron microscopy maps. Annu Rev Biophys Biomol Struct 35:299-317. (Pubitemid 43877380)
5. Moazed D, Noller HF (1989) Intermediate states in the movement of transfer-RNA in the ribosome. Nature 342:142-148. (Pubitemid 19277015)
6. Antoun A, Pavlov MY, Lovmar M, EhrenbergM(2006) How initiation factors maximize the accuracy of tRNA selection in initiation of bacterial protein synthesis. Mol Cell 23:183-193. (Pubitemid 44062367)
7. Daviter T, Gromadski KB, Rodnina MV (2006) The ribosome's response to codon-anticodon mismatches. Biochimie 88:1001-1011.
8. Dorner S, Brunelle JL, Sharma D, Green R (2006) The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nat Struct Mol Biol 13:234-241. (Pubitemid 43348509)
9. Grigoriadou C, Marzi S, Kirillov S, Gualerzi CO, Cooperman BS (2007) A quantitative kinetic scheme for 70S translation initiation complex formation. J Mol Biol 373:562-572. (Pubitemid 47488388)
10. Pan DL, Kirillov SV, Cooperman BS (2007) Kinetically competent intermediates in the translocation step of protein synthesis. Mol Cell 25:519-529. (Pubitemid 46274443)
11. Savelsbergh A, et al. (2003) An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol Cell 11:1517-1523. (Pubitemid 36776538)
12. WintermeyerW, et al. (2004) Mechanisms of elongation on the ribosome: Dynamics of a macromolecular machine. Biochem Soc Trans 32:733-737. (Pubitemid 39524366)
13. Zavialov AV, Ehrenberg M (2003) Peptidyl-tRNA regulates the GTPase activity of translation factors. Cell 114:113-122. (Pubitemid 36859845)
14. Blanchard SC (2009) Single-molecule observations of ribosome function. Curr Opin Struct Biol 19:103-109.
15. Frank J, Gonzalez RL (2010) Structure and dynamics of a processive Brownian motor: The translating ribosome. Annu Rev Biochem 79:381-412.
16. Uemura S, et al. (2010) Real-time tRNA transit on single translating ribosomes at codon resolution. Nature 464:1012-1017.
17. Chen C, et al. (2011) Single molecule fluorescence measurements of ribosomal translocation dynamics. Mol Cell 42:367-377.
18. Semenkov YP, Rodnina MV,WintermeyerW(1996) The "allosteric three-site model" of elongation cannot be confirmed in a well-defined ribosome system from Escherichia coli. Proc Natl Acad Sci USA 93:12183-12188.
19. Nierhaus KH (1990) The allosteric 3-Site model for the ribosomal elongation cycle - features and future. Biochemistry 29:4997-5008.
20. Nierhaus KH, et al. (1995) The elongating ribosome: Structural and functional aspects. Biochem Cell Biol 73:1011-1021.
21. Nierhaus KH (2006) Decoding errors and the involvement of the E-site. Biochimie 88:1013-1019.
22. Zaher HS, Green R (2009) Fidelity at the molecular level: Lessons from protein synthesis. Cell 136:746-762.
23. Leger M, Dulude D, Steinberg SV, Brakier-Gingras L (2007) The three transfer RNAs occupying the A, P, and E sites on the ribosome are involved in viral programmed- 1 ribosomal frameshift. Nucleic Acids Res 35:5581-5592. (Pubitemid 47423929)
24. Liao PY, Gupta P, Petrov AN, Dinman JD, Lee KH (2008) A new kinetic model reveals the synergistic effect of E-, P- and A-sites on +1 ribosomal frameshifting. Nucleic Acids Res 36:2619-2629. (Pubitemid 351659576)
25. Wilson DN, Nierhaus KH (2006) The E-site story: The importance of maintaining two tRNAs on the ribosome during protein synthesis. Cell Mol Life Sci 63:2725-2737. (Pubitemid 44913314)
26. Aitken CE, Petrov A, Puglisi JD (2010) Single ribosome dynamics and the mechanism of translation. Annu Rev Biophys 39:491-513.
27. Kapanidis AN, et al. (2004) Fluorescence-aided molecule sorting: Analysis of structure and interactions by alternating-laser excitation of single molecules. Proc Natl Acad Sci USA 101:8936-8941. (Pubitemid 38781589)
28. Pape T, Wintermeyer W, Rodnina MV (1998) Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E-coli ribosome. EMBO J 17:7490-7497. (Pubitemid 29002715)
29. Johansson M, Bouakaz E, Lovmar M, Ehrenberg M (2008) The kinetics of ribosomal peptidyl transfer revisited. Mol Cell 30:589-598. (Pubitemid 351755061)
30. Blanchard SC, Kim HD, Gonzalez RL, Puglisi JD, Chu S (2004) tRNA dynamics on the ribosome during translation. Proc Natl Acad Sci USA 101:12893-12898. (Pubitemid 39167554)
31. Agirrezabala X, et al. (2008) Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol Cell 32:190-197.
32. Julian P, et al. (2008) Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc Natl Acad Sci USA 105:16924-16927.
33. Penner MH, Frieden C (1985) Substrate-induced hysteresis in the activity of Escherichia coli dihydrofolate reductase. J Biol Chem 260:5366-5369. (Pubitemid 15003278)
34. Yang H, et al. (2003) Protein conformational dynamics probed by single-molecule electron transfer. Science 302:262-266. (Pubitemid 37248752)
35. Valle M, et al. (2003) Locking and unlocking of ribosomal motions. Cell 114:123-134. (Pubitemid 36859846)
36. Cornish PV, Ermolenko DN, Noller HF, Ha T (2008) Spontaneous intersubunit rotation in single ribosomes. Mol Cell 30:578-588. (Pubitemid 351760964)
37. Cornish PV, et al. (2009) Following movement of the L1 stalk between three functional states in single ribosomes. Proc Natl Acad Sci USA 106:2571-2576.
38. Frank J, Agrawal RK (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406:318-322. (Pubitemid 30604411)
39. Horan LH, Noller HF (2007) Intersubunit movement is required for ribosomal translocation. Proc Natl Acad Sci USA 104:4881-4885. (Pubitemid 47186145)
40. Ermolenko DN, Noller HF (2011) mRNA translocation occurs during the second step of ribosomal intersubunit rotation. Nat Struct Mol Biol 18:457-462.
41. Ratje AH, et al. (2010) Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468:713-U143.
42. ZhangW, Dunkle JA, Cate JHD (2009) Structures of the ribosome in intermediate states of ratcheting. Science 325:1014-1017.
43. 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.
44. Mesters JR, Potapov AP, de Graaf JM, Kraal B (1994) Synergism between the GTPase activities of EF-Tu.GTP and EF-G.GTP on empty ribosomes: Elongation factors as stimulators of the ribosomal oscillation between two conformations. J Mol Biol 242:644-654.
45. SzaflarskiW, Nierhaus KH (2007) Optimized energy consumption for protein synthesis. Origins Life Evol B 37:423-428.
46. Tenson T, Hauryliuk V (2009) Does the ribosome have initiation and elongation modes of translation? Mol Microbiol 72:1310-1315.
47. Ramu H, Mankin A, Vazquez-Laslop N (2009) Programmed drug-dependent ribosome stalling. Mol Microbiol 71:811-824.
48. Devaraj A, Shoji S, Holbrook ED, Fredrick K (2009) A role for the 30S subunit E site in maintenance of the translational reading frame. RNA 15:255-265.
49. Sergiev PV, et al. (2005) Function of the ribosomal E-site: A mutagenesis study. Nucleic Acids Res 33:6048-6056. (Pubitemid 41742623)
50. Blaha G, Stanley RE, Steitz TA (2009) Formation of the first peptide bond: The structure of EF-P bound to the 70S ribosome. Science 325:966-970.
51. Xu J, et al. (2006) Molecular localization of a ribosome-dependent ATPase on Escherichia coli ribosomes. Nucleic Acids Res 34:1158-1165.
52. Qin Y, et al. (2006) The highly conserved LepA is a ribosomal elongation factor that back-translocates the ribosorne. Cell 127:721-733. (Pubitemid 44716253)
53. Connell SR, et al. (2008) A new tRNA intermediate revealed on the ribosome during EF4-mediated back-translocation. Nat Struct Mol Biol 15:910-915.
54. Liu HQ, Pan DL, Pech M, Cooperman BS (2010) Interrupted catalysis: The EF4 (LepA) effect on back-translocation. J Mol Biol 396:1043-1052.
55. Di Giacco V, et al. (2008) Shine-Dalgarno interaction prevents incorporation of noncognate amino acids at the codon following the AUG. Proc Natl Acad Sci USA 105:10715-10720.
56. Roy R, Hohng S, Ha T (2008) A practical guide to single-molecule FRET. Nat Methods 5:507-516. (Pubitemid 351761757)
57. Pan DL, Qin HO, Cooperman BS (2009) Synthesis and functional activity of tRNAs labeled with fluorescent hydrazides in the D-loop. RNA 15:346-354.
58. Kaur J, Raj M, Cooperman BS (2011) Fluorescent labeling of tRNA dihydrouridine residues: Mechanism and distribution. RNA 17:1393-400.