Conformational heterogeneity in RNA polymerase observed by single-pair FRET microscopy

Biophysical Journal

Volumn 90, Issue 12, 2006, Pages 4605-4617

  Coban, Oana ^a,d   Lamb, Don C ^a,b,e   Zaychikov, Evgeny ^c   Heumann, Hermann ^c   Nienhaus, G Ulrich ^a,b  

^a UNIVERSITY OF ULM   (Germany)

^b University of Illinois at Urbana Champaign   (United States)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; FLUORESCENT DYE; NUCLEOSIDE TRIPHOSPHATE; PRIMER RNA; RNA POLYMERASE; TRANSCRIPTION ELONGATION FACTOR;

ARTICLE; CONTROLLED STUDY; DNA RNA HYBRIDIZATION; DNA TRANSCRIPTION; ESCHERICHIA COLI; FEASIBILITY STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC HETEROGENEITY; GEOMETRY; MICROSCOPY; NONHUMAN; RNA CONFORMATION; RNA TRANSCRIPTION;

ESCHERICHIA COLI;

EID: 33744797914     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.078840     Document Type: Article

References (52)

1. Erie, D. A. 2002. The many conformational states of RNA polymerase elongation complexes and their roles in the regulation of transcription. Biochim. Biophys. Acta. 1577:224-239.
2. Foster, J. E., S. F. Holmes, and D. A. Erie. 2001. Allosteric binding of nucleoside triphosphates to RNA polymerase regulates transcription elongation. Cell. 106:243-252.
3. Cramer, P., D. A. Bushnell, and R. D. Kornberg. 2001. Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science. 292:1863-1876.
4. Darst, S. A., N. Opalka, P. Chacon, A. Polyakov, C. Richter, G. Y. Zhang, and W. Wriggers. 2002. Conformational flexibility of bacterial RNA polymerase. Proc. Natl. Acad. Sci. USA. 99:4296-4301.
5. Murakami, K. S., S. Masuda, E. A. Campbell, O. Muzzin, and S. A. Darst. 2002. Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science. 296:1285-1290.
6. Murakami, K. S., S. Masuda, and S. A. Darst. 2002. Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Ångstrom resolution. Science. 296:1280-1284.
7. Finn, R. D., E. V. Orlova, B. Gowen, M. Buck, and M. van Heel. 2000. Escherichia coli RNA polymerase core and holoenzyme structures. EMBO J. 19:6833-6844.
8. Adelman, K., A. La Porta, T. J. Santangelo, J. T. Lis, J. W. Roberts, and M. D. Wang. 2002. Single molecule analysis of RNA polymerase elongation reveals uniform kinetic behavior. Proc. Natl. Acad. Sci. USA. 99:13538-13543.
9. Davenport, R. J., G. J. L. Wuite, R. Landick, and C. Bustamante. 2000. Single-molecule study of transcriptional pausing and arrest by E. coli RNA polymerase. Science. 287:2497-2500.
10. Tolic-Nørrelykke, S. F., A. M. Engh, R. Landick, and J. Gelles. 2004. Diversity in the rates of transcript elongation by single RNA polymerase molecules. J. Biol. Chem. 279:3292-3299.
11. Clegg, R. 1996. Fluorescence Resonance Energy Transfer. In Fluorescence Imaging Spectroscopy and Microscopy. X. F. Wang and B. Herman, editors. John Wiley & Sons, New York. 170-252.
12. Selvin, P. R. 2000. The renaissance of fluorescence resonance energy transfer. Nat. Struct. Biol. 7:730-734.
13. Jares-Erijman, E. A., and T. M. Jovin. 2003. FRET imaging. Nat. Biotechnol. 21:1387-1395.
14. Selvin, P. R. 1995. Fluorescence resonance energy transfer. Methods Enzymol. 245:300-334.
15. Wu, P., and L. Brand. 1994. Resonance energy transfer: methods and applications. Anal. Biochem. 218:1-13.
16. Heyduk, T., and A. Niedziela-Majka. 2001. Fluorescence resonance energy transfer analysis of Escherichia coli RNA polymerase and polymerase-DNA complexes. Biopolymers. 61:201-213.
17. Heyduk, T. 2002. Measuring protein conformational changes by FRET/LRET. Curr. Opin. Biotechnol. 13:292-296.
18. Naryshkin, N., A. Revyakin, Y. G. Kim, V. Mekler, and R. H. Ebright. 2000. Structural organization of the RNA polymerase-promoter open complex. Cell. 101:601-611.
19. Mukhopadhyay, J., A. N. Kapanidis, V. Mekler, E. Kortkhonjia, Y. W. Ebright, and R. H. Ebright. 2001. Translocation of σ(70) with RNA polymerase during transcription: fluorescence resonance energy transfer assay for movement relative to DNA. Cell. 106:453-463.
20. Mukhopadhyay, J., V. Mekler, E. Kortkhonjia, A. N. Kapanidis, Y. W. Ebright, and R. H. Ebright. 2003. Fluorescence resonance energy transfer (FRET) in analysis of transcription-complex structure and function. Methods Enzymol. 371:144-159.
21. Mekler, V., E. Kortkhonjia, J. Mukhopadhyay, J. Knight, A. Revyakin, A. N. Kapanidis, W. Niu, Y. W. Ebright, R. Levy, and R. H. Ebright. 2002. Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell. 108:599-614.
22. Ha, T., T. Enderle, D. F. Ogletree, D. S. Chemla, P. R. Selvin, and S. Weiss. 1996. Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA. 93:6264-6268.
23. Zhuang, X., L. E. Bartley, H. P. Babcock, R. Russell, T. Ha, D. Herschlag, and S. Chu. 2000. A single-molecule study of RNA catalysis and folding. Science. 288:2048-2051.
24. Talaga, D. S., W. L. Lau, H. Roder, J. Tang, Y. Jia, W. F. DeGrado, and R. M. Hochstrasser. 2000. Dynamics and folding of single two-stranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy. Proc. Natl. Acad. Sci. USA. 97:13021-13026.
25. Schuler, B., E. A. Lipman, and W. A. Eaton. 2002. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature. 419:743-747.
26. Lipman, E. A., B. Schuler, O. Bakajin, and W. A. Eaton. 2003. Single-molecule measurement of protein folding kinetics. Science. 301:1233-1235.
27. Klostermeier, D., and D. P. Millar. 2001. RNA conformation and folding studied with fluorescence resonance energy transfer. Methods. 23:240-254.
28. Ishii, Y., T. Yoshida, T. Funatsu, T. Wazawa, and T. Yanagida. 1999. Fluorescence resonance energy transfer between single fluorophores attached to a coiled-coil protein in aqueous solution. Chem. Phys. 247:163-173.
29. Deniz, A. A., M. Dahan, J. R. Grunwell, T. J. Ha, A. E. Faulhaber, D. S. Chemla, S. Weiss, and P. G. Schultz. 1999. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: observation of Förster distance dependence and subpopulations. Proc. Natl. Acad. Sci. USA. 96:3670-3675.
30. Burgess, R. R., and J. J. Jendrisak. 1975. A procedure for the rapid, large-scale purification of Escherichia coli DNA-dependent RNA polymerase involving Polymin P precipitation and DNA-cellulose chromatography. Biochemistry. 14:4634-4638.
31. 2+-dependent conformational change of RNA studied by fluorescence correlation and FRET on immobilized single molecules. Proc. Natl. Acad. Sci. USA. 99:4284-4289.
32. Lakowicz, J. R. 1999. Principles of Fluorescence Spectroscopy, 2nd Ed. Plenum, New York.
33. Coban, O. 2004. A fluorescence resonance energy transfer study of protein-nucleic acid complexes: RNA polymerase and Lac repressor. (PhD Thesis.). University of Ulm, Germany.
34. Groll, J., E. V. Amirgoulova, T. Ameringer, C. D. Heyes, C. Rocker, G. U. Nienhaus, and M. Moller. 2004. Biofunctionalized, ultrathin coatings of cross-linked star-shaped poly(ethylene oxide) allow reversible folding of immobilized proteins. J. Am. Chem. Soc. 126:4234-4239.
35. Amirgoulova, E. V., J. Groll, C. D. Heyes, T. Ameringer, C. Rocker, M. Moller, and G. U. Nienhaus. 2004. Biofunctionalized polymer surfaces exhibiting minimal interaction towards immobilized proteins. ChemPhysChem. 5:552-555.
36. Heyes, C. D., A. Y. Kobitski, E. V. Amirgoulova, and G. U. Nienhaus. 2004. Biocompatible surfaces for specific tethering of individual protein molecules. J. Phys. Chem. B. 108:13387-13394.
37. Kuzmenkina, E. V., C. D. Heyes, and G. U. Nienhaus. 2005. Single-molecule Förster resonance energy transfer study of protein dynamics under denaturing conditions. Proc. Natl. Acad. Sci. USA. 102:15471-15476.
38. Ying, L. M., M. I. Wallace, S. Balasubramanian, and D. Klenerman. 2000. Ratiometric analysis of single-molecule fluorescence resonance energy transfer using logical combinations of threshold criteria: a study of 12-mer DNA. J. Phys. Chem. B. 104:5171-5178.
39. Widengren, J., E. Schweinberger, S. Berger, and C. A. M. Seidel. 2001. Two new concepts to measure fluorescence resonance energy transfer via fluorescence correlation spectroscopy: theory and experimental realizations. J. Phys. Chem. A. 105:6851-6866.
40. Hagerman, P. J. 1988. Flexibility of DNA. Annu. Rev. Biophys. Biophys. Chem. 17:265-286.
41. Clegg, R. M., A. I. H. Murchie, A. Zechel, and D. M. J. Lilley. 1993. Observing the helical geometry of double-stranded DNA in solution by fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA. 90:2994-2998.
42. Korzheva, N., A. Mustaev, M. Kozlov, A. Malhotra, V. Nikiforov, A. Goldfarb, and S. A. Darst. 2000. A structural model of transcription elongation. Science. 289:619-625.
43. Kuznedelov, K., N. Korzheva, A. Mustaev, and K. Severinov. 2002. Structure-based analysis of RNA polymerase function: the largest subunit's rudder contributes critically to elongation complex stability and is not involved in the maintenance of RNA-DNA hybrid length. EMBO J. 21:1369-1378.
44. Daube, S. S., and P. H. von Hippel. 1992. Functional transcription elongation complexes from synthetic RNA-DNA bubble duplexes. Science. 258:1320-1324.
45. Daube, S. S., C. R. Hart, and P. H. von Hippel. 1994. Coupling of RNA displacement and intrinsic termination in transcription from synthetic RNA-DNA bubble duplex constructs. Proc. Natl. Acad. Sci. USA. 91:9539-9543.
46. Daube, S. S., and P. H. von Hippel. 1994. RNA displacement pathways during transcription from synthetic RNA-DNA bubble duplexes. Biochemistry. 33:340-347.
47. Parkhurst, L. J., K. M. Parkhurst, R. Powell, J. Wu, and S. Williams. 2002. Time-resolved fluorescence resonance energy transfer studies of DNA bending in double-stranded oligonucleotides and in DNA-protein complexes. Biopolymers. 61:180-200.
48. Levin, J. R., B. Krummel, and M. J. Chamberlin. 1987. Isolation and properties of transcribing ternary complexes of Escherichia coli RNA polymerase positioned at a single template base. J. Mol. Biol. 196:85-100.
49. Krummel, B., and M. J. Chamberlin. 1989. RNA chain initiation by Escherichia coli RNA polymerase. Structural transitions of the enzyme in early ternary complexes. Biochemistry. 28:7829-7842.
50. Holstege, F. C. P., U. Fiedler, and H. T. M. Timmers. 1997. Three transitions in the RNA polymerase II transcription complex during initiation. EMBO J. 16:7468-7480.
51. Wilson, K. S., C. R. Conant, and P. H. von Hippel. 1999. Determinants of the stability of transcription elongation complexes: interactions of the nascent RNA with the DNA template and the RNA polymerase. J. Mol. Biol. 289:1179-1194.
52. Greive, S. J., and P. H. von Hippel. 2005. Thinking quantitatively about transcriptional regulation. Nat. Rev. Mol. Cell Biol. 6:221-232.