Codon-dependent tRNA fluctuations monitored with fluorescence polarization

Biophysical Journal

Volumn 99, Issue 11, 2010, Pages 3849-3858

  Mishra, Padmaja P ^a   Qureshi, Mohd Tanvir ^a   Ren, Wenhui ^a   Lee, Tae Hee ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78649774217     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.10.026     Document Type: Article

References (61)

1. Green, R., and H. F. Noller. 1997. Ribosomes and translation. Annu. Rev. Biochem. 66:679-716.
2. Rodnina, M. V., and W. Wintermeyer. 2001. Ribosome fidelity: tRNA discrimination, proofreading and induced fit. Trends Biochem. Sci. 26:124-130.
3. Ban, N., P. Nissen, T. A. Steitz. 2000. The complete atomic structure of the large ribosomal subunit at 2.4. A resolution. Science. 289:902-921.
4. Yonath, A., C. Glotz, H. G. Wittmann. 1988. Characterization of crystals of small ribosomal subunits. J. Mol. Biol. 203:831-834.
5. Cate, J. H., M. M. Yusupov, H. F. Noller. 1999. X-ray crystal structures of 70S ribosome functional complexes. Science. 285:2095-2104.
6. Kurland, C. G., D. Hughes, and M. Ehrenberg. 1996. In Limitations of Translational Accuracy. ASM Press, Washington, DC.
7. Rodnina, M. V., R. Fricke, W. Wintermeyer. 1995. Codon-dependent conformational change of elongation factor Tu preceding GTP hydrolysis on the ribosome. EMBO J. 14:2613-2619.
8. Hunter, S. E., and L. L. Spremulli. 2004. Mutagenesis of glutamine 290 in Escherichia coli and mitochondrial elongation factor Tu affects interactions with mitochondrial aminoacyl-tRNAs and GTPase activity. Biochemistry. 43:6917-6927.
9. Moazed, D., J. M. Robertson, and H. F. Noller. 1988. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature. 334:362-364.
10. Kjeldgaard, M., P. Nissen, J. Nyborg. 1993. The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure. 1:35-50.
11. Abel, K., M. D. Yoder, F. Jurnak. 1996. An α to β conformational switch in EF-Tu. Structure. 4:1153-1159.
12. Stark, H., M. V. Rodnina, M. van Heel. 1997. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature. 389:403-406.
13. Stark, H., M. V. Rodnina, M. van Heel. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat. Struct. Biol. 9:849-854.
14. Rodnina, M. V., and W. Wintermeyer. 2001. Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annu. Rev. Biochem. 70:415-435.
15. Blanchard, S. C., R. L. Gonzalez, J. D. Puglisi. 2004. tRNA selection and kinetic proofreading in translation. Nat. Struct. Mol. Biol. 11:1008-1014.
16. Lee, T.-H., S. C. Blanchard, S. Chu. 2007. The role of fluctuations in tRNA selection by the ribosome. Proc. Natl. Acad. Sci. USA. 104:13661-13665.
17. Ogle, J. M., F. V. Murphy, V. Ramakrishnan. 2002. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell. 111:721-732.
18. Adilakshmi, T., D. L. Bellur, and S. A. Woodson. 2008. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature. 455:1268-1272.
19. Lakowicz, J. R. 2006. Principles of Fluorescence Spectroscopy. Springer, Berlin, Heidelberg.
20. Piepenburg, O., T. Pape, M. V. Rodnina. 2000. Intact aminoacyl-tRNA is required to trigger GTP hydrolysis by elongation factor Tu on the ribosome. Biochemistry. 39:1734-1738.
21. Cochella, L., and R. Green. 2005. An active role for tRNA in decoding beyond codon:anticodon pairing. Science. 308:1178-1180.
22. Schultz, D. W., and M. Yarus. 1994. tRNA structure and ribosomal function. II. Interaction between anticodon helix and other tRNA mutations. J. Mol. Biol. 235:1395-1405.
23. Schuette, J.-C., F. V. Murphy, 4th, C. M. Spahn. 2009. GTPase activation of elongation factor EF-Tu by the ribosome during decoding. EMBO J. 28:755-765.
24. Frank, J., J. Sengupta, M. Ehrenberg. 2005. The role of tRNA as a molecular spring in decoding, accommodation, and peptidyl transfer. FEBS Lett. 579:959-962.
25. Valle, M., A. Zavialov, J. Frank. 2003. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nat. Struct. Biol. 10:899-906.
26. Schmeing, T. M., R. M. Voorhees, V. Ramakrishnan. 2009. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science. 326:688-694.
27. Forster, T. 1959. Transfer mechanisms of electronic excitation. Discuss. Faraday Soc. 27:7-17.
28. Deniz, A. A., M. Dahan, P. G. Schultz. 1999. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: observation of Forster distance dependence and subpopulations. Proc. Natl. Acad. Sci. USA. 96:3670-3675.
29. Ha, T., A. Y. Ting, S. Weiss. 1999. Temporal fluctuations of fluorescence resonance energy transfer between two dyes conjugated to a single protein. Chem. Phys. 247:107-118.
30. Zhuang, X., T. Ha, S. Chu. 2000. Fluorescence quenching: a tool for single-molecule protein-folding study. Proc. Natl. Acad. Sci. USA. 97:14241-14244.
31. Ha, T., I. Rasnik, S. Chu. 2002. Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature. 419:638-641.
32. Antonik, M., S. Felekyan, C. A. Seidel. 2006. Separating structural heterogeneities from stochastic variations in fluorescence resonance energy transfer distributions via photon distribution analysis. J. Phys. Chem. B. 110:6970-6978.
33. Kalinin, S., S. Felekyan, C. A. Seidel. 2007. Probabilitydistribution analysis of single-molecule fluorescence anisotropy and resonance energy transfer. J. Phys. Chem. B. 111:10253-10262.
34. Lee, T.-H., L. J. Lapidus, S. Chu. 2007. Measuring the folding transition time of single RNA molecules. Biophys. J. 92:3275-3283.
35. Brochon, J.-C., P. Wahl, and J.-C. Auchet. 1974. Fluorescence time-resolved spectroscopy and fluorescence anisotropy decay of the Staphylococcus aureus endonuclease. Eur. J. Biochem. 41:577-583.
36. Harms, G. S., M. Sonnleitner, T. Schmidt. 1999. Single-molecule anisotropy imaging. Biophys. J. 77:2864-2870.
37. Kungl, A. J., N. V. Visser, M. Auer. 1998. Time-resolved fluorescence anisotropy of HIV-1 protease inhibitor complexes correlates with inhibitory activity. Biochemistry. 37:2778-2786.
38. Rasnik, I., S. A. McKinney, and T. Ha. 2005. Surfaces and orientations: much to FRET about? Acc. Chem. Res. 38:542-548.
39. Gopich, I., and A. Szabo. 2005. Theory of photon statistics in single-molecule Forster resonance energy transfer. J. Chem. Phys. 122:14707.
40. Armitage, B. A. 2005. Topics in Current Chemistry: Cyanine Dye - DNA Interactions: Intercalation, Groove Binding, and Aggregation. Springer, Berlin/Heidelberg.
41. Iqbal, A., L. Wang, D. G. Norman. 2008. The structure of cyanine 5 terminally attached to double-stranded DNA: implications for FRET studies. Biochemistry. 47:7857-7862.
42. Blanchard, S. C., H. D. Kim, S. Chu. 2004. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA. 101:12893-12898.
43. Lee, T.-H. 2009. Extracting kinetics information from single-molecule fluorescence resonance energy transfer data using hidden Markov models. J. Phys. Chem. B. 113:11535-11542.
44. Harvey, B. J., C. Perez, and M. Levitus. 2009. DNAsequence-dependent enhancement of Cy3 fluorescence. Photochem. Photobiol. Sci. 8: 1105-1110.
45. Frank, Jr., J., and R. L. Gonzalez. 2010. Structure and dynamics of a processive Brownian motor: the translating ribosome. Annu. Rev. Biochem. 79:381-412.
46. Hirsh, D. 1971. Tryptophan transfer RNA as the UGA suppressor. J. Mol. Biol. 58:439-458.
47. Powers, T., and H. F. Noller. 1993. Evidence for functional interaction between elongation factor Tu and 16S ribosomal RNA. Proc. Natl. Acad. Sci. USA. 90:1364-1368.
48. Polekhina, G., S. Thirup, J. Nyborg. 1996. Helix unwinding in the effector region of elongation factor EF-Tu-GDP. Structure. 4:1141-1151.
49. Nissen, P., M. Kjeldgaard, J. Nyborg. 1995. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science. 270:1464-1472.
50. Berchtold, H., L. Reshetnikova, R. Hilgenfeld. 1993. Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature. 365:126-132.
51. Weinger, J. S., K. M. Parnell, S. A. Strobel. 2004. Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat. Struct. Mol. Biol. 11:1101-1106.
52. Hausner, T. P., J. Atmadja, and K. H. Nierhaus. 1987. Evidence that the G2661 region of 23S rRNA is located at the ribosomal binding sites of both elongation factors. Biochimie. 69:911-923.
53. Vorstenbosch, E., T. Pape, W. Wintermeyer. 1996. The G222D mutation in elongation factor Tu inhibits the codon-induced conformational changes leading to GTPase activation on the ribosome. EMBO J. 15:6766-6774.
54. Ogle, J. M., D. E. Brodersen, V. Ramakrishnan. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science. 292:897-902.
55. Dey, D., A. V. Oleinikov, and R. R. Traut. 1995. The hinge region of Escherichia coli ribosomal protein L7/L12 is required for factor binding and GTP hydrolysis. Biochimie. 77:925-930.
56. Kühberger, R., W. Piepersberg, .,A. Bock. 1979. Alteration of ribosomal protein L6 in gentamicin-resistant strains of Escherichia coli. Effects on fidelity of protein synthesis. Biochemistry. 18:187-193.
57. Powers, T., and H. F. Noller. 1994. Selective perturbation of G530 of 16 S rRNA by translational miscoding agents and a streptomycin-dependence mutation in protein S12. J. Mol. Biol. 235:156-172.
58. O'Connor, M. O., and A. E. Dahlberg. 1995. The involvement of two distinct regions of 23 S ribosomal RNA in tRNA selection. J. Mol. Biol. 254:838-847.
59. Ban, N., P. Nissen, T. A. Steitz. 1999. Placement of protein and RNA structures into a 5 A-resolution map of the 50S ribosomal subunit. Nature. 400:841-847.
60. Kim, H. D., J. D. Puglisi, and S. Chu. 2007. Fluctuations of transfer RNAs between classical and hybrid states. Biophys. J. 93:3575-3582.
61. Uemura, S., M. Dorywalska, S. Chu. 2007. Peptide bond formation destabilizes Shine-Dalgarno interaction on the ribosome. Nature. 446:454-457.