Sensing DNA opening in transcription using quenchable Förster resonance energy transfer

Biochemistry

Volumn 49, Issue 43, 2010, Pages 9171-9180

  Cordes, Thorben ^a   Santoso, Yusdi ^a   Tomescu, Alexandra I ^a   Gryte, Kristofer ^a   Hwang, Ling Chin ^a,c   Camará, Beatriz ^b   Wigneshweraraj, Sivaramesh ^b   Kapanidis, Achillefs N ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; BUBBLE EXPANSION; COMPLEMENTARY STRAND; DEQUENCHING; DNA FRAGMENT; DNA STRANDS; DOUBLE-STRANDED DNA (DS-DNA); ENCODED PROTEINS; FLUORESCENCE QUENCHING; GENE TRANSCRIPTIONS; MODE OF ACTION; POTENT INHIBITOR; REAL TIME; RESONANCE ENERGY TRANSFER; RNA POLYMERASE; SINGLE MOLECULE LEVEL; TRANSCRIPTION INITIATION;

DNA; ENERGY TRANSFER; ESCHERICHIA COLI; FLUOROPHORES; QUENCHING; RESONANCE; RNA; SULFUR COMPOUNDS;

TRANSCRIPTION;

BACTERIAL RNA; DNA; DNA FRAGMENT; DOUBLE STRANDED DNA; RIFAMPICIN; RNA POLYMERASE; SINGLE STRANDED DNA;

ARTICLE; DNA STRAND; DNA TRANSCRIPTION; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSCRIPTION; NONPHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DNA; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; LAC OPERON; MOLECULAR PROBE TECHNIQUES; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; RIFAMPIN; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 78049249486     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101184g     Document Type: Article

References (44)

1. Orphanides, G. and Reinberg, D. (2002) A unified theory of gene expression Cell 108, 439-451
2. Murakami, K. S. and Darst, S. A. (2003) Bacterial RNA polymerases: The wholo story Curr. Opin. Struct. Biol. 13, 31-39
3. Young, B. A., Gruber, T. M., and Gross, C. A. (2002) Views of transcription initiation Cell 109, 417-420
4. Buc, H. and McClure, W. R. (1985) Kinetics of open complex formation between Escherichia coli RNA polymerase and the lac UV5 promoter. Evidence for a sequential mechanism involving three steps Biochemistry 24, 2712-2723
5. Revyakin, A., Ebright, R. H., and Strick, T. R. (2004) Promoter unwinding and promoter clearance by RNA polymerase: Detection by single-molecule DNA nanomanipulation Proc. Natl. Acad. Sci. U.S.A. 101, 4776-4780
6. Borowiec, J. A., Zhang, L., Sasse-Dwight, S., and Gralla, J. D. (1987) DNA supercoiling promotes formation of a bent repression loop in lac DNA J. Mol. Biol. 196, 101-111
7. Kirkegaard, K., Buc, H., Spassky, A., and Wang, J. C. (1983) Mapping of single-stranded regions in duplex DNA at the sequence level: Single-strand-specific cytosine methylation in RNA polymerase-promoter complexes Proc. Natl. Acad. Sci. U.S.A. 80, 2544-2548
8. Sclavi, B., Woodson, S., Sullivan, M., Chance, M. R., and Brenowitz, M. (1997) Time-resolved synchrotron X-ray "footprinting", a new approach to the study of nucleic acid structure and function: Application to protein-DNA interactions and RNA folding J. Mol. Biol. 266, 144-159
9. Sclavi, B., Zaychikov, E., Rogozina, A., Walther, F., Buckle, M., and Heumann, H. (2005) Real-time characterization of intermediates in the pathway to open complex formation by Escherichia coli RNA polymerase at the T7A1 promoter Proc. Natl. Acad. Sci. U.S.A. 102, 4706-4711
10. Sylvester, J. E. and Cashel, M. (1980) Stable RNA-DNA-RNA Polymerase Complexes Can Accompany Formation of a Single Phosphodiester Bond Biochemistry 19, 1069-1074
11. Callaci, S. and Heyduk, T. (1998) Conformation and DNA binding properties of a single-stranded DNA binding region of σ70 subunit from Escherichia coli RNA polymerase are modulated by an interaction with the core enzyme Biochemistry 37, 3312-3320
12. Matlock, D. L. and Heyduk, T. (1999) A real-time fluorescence method to monitor the melting of duplex DNA during transcription initiation by RNA polymerase Anal. Biochem. 270, 140-147
13. Jia, Y., Kumar, A., and Patel, S. S. (1996) Equilibrium and stopped-flow kinetic studies of interaction between T7 RNA polymerase and its promoters measured by protein and 2-aminopurine fluorescence changes J. Biol. Chem. 271, 30451-30458
14. Sastry, S. S. and Ross, B. M. (1996) A direct real-time spectroscopic investigation of the mechanism of open complex formation by T7 RNA polymerase Biochemistry 35, 15715-15725
15. Sullivan, J. J., Bjornson, K. P., Sowers, L. C., and deHaseth, P. L. (1997) Spectroscopic determination of open complex formation at promoters for Escherichia coli RNA polymerase Biochemistry 36, 8005-8012
16. Kapanidis, A. N. and Strick, T. (2009) Biology, one molecule at a time Trends Biochem. Sci. 34, 234-243
17. Myong, S., Bruno, M. M., Pyle, A. M., and Ha, T. (2007) Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase Science 317, 513-516
18. Revyakin, A., Liu, C., Ebright, R. H., and Strick, T. R. (2006) Abortive initiation and productive initiation by RNA polymerase involve DNA scrunching Science 314, 1139-1143
19. Hohlbein, J., Gryte, K., Heilemann, M., and Kapanidis, A. N. (2010) Surfing on a new wave of single-molecule fluorescence methods Phys. Biol. 7, 031001
20. Merrick, M. J. (1993) In a class of its own: The RNA polymerase sigma factor sigma 54 (sigma N) Mol. Microbiol. 10, 903-909
21. Tjian, R. (1996) The biochemistry of transcription in eukaryotes: A paradigm for multisubunit regulatory complexes Philos. Trans. R. Soc. London, Ser. B 351, 491-499
22. Holden, S. J., Uphoff, S., Hohlbein, J., Yadin, D., Le Reste, L., Britton, O. J., and Kapanidis, A. N. (2010) Defining the limits of single-molecule FRET resolution in TIRF microscopy Biophysical J. 99, 9 (in press)
23. Kapanidis, A. N., Margeat, E., Ho, S. O., Kortkhonjia, E., Weiss, S., and Ebright, R. H. (2006) Initial transcription by RNA polymerase proceeds through a DNA-scrunching mechanism Science 314, 1144-1147
24. 70 in Transcription Elongation: Single-Molecule Analysis Mol. Cell 20, 347-356
25. Vogelsang, J., Cordes, T., and Tinnefeld, P. (2009) Single-molecule photophysics of oxazines on DNA and its application in a FRET switch Photochem. Photobiol. Sci. 8, 486-496
26. Santoso, Y., Joyce, C. M., Potapova, O., Le Reste, L., Hohlbein, J., Torella, J. P., Grindley, N. D. F., and Kapanidis, A. N. (2010) Conformational transitions in DNA polymerase I revealed by single-molecule FRET Proc. Natl. Acad. Sci. U.S.A. 107, 715-720
27. Santoso, Y. and Kapanidis, A. N. (2009) Probing Biomolecular Structures and Dynamics of Single Molecules Using In-gel Alternating-Laser Excitation Anal. Chem. 81, 9561-9570
28. Kapanidis, A. N., Laurence, T. A., Lee, N. K., Margeat, E., Kong, X., and Weiss, S. (2005) Alternating-laser excitation of single molecules Acc. Chem. Res. 38, 523-533
29. Kapanidis, A. N., Lee, N. K., Laurence, T. A., Doose, S., Margeat, E., and Weiss, S. (2004) Fluorescence-aided molecule sorting: Analysis of structure and interactions by alternating-laser excitation of single molecules Proc. Natl. Acad. Sci. U.S.A. 101, 8936-8941
30. Eggeling, C., Berger, S., Brand, L., Fries, J. R., Schaffer, J., Volkmer, A., and Seidel, C. A. (2001) Data registration and selective single-molecule analysis using multi-parameter fluorescence detection J. Biotechnol. 86, 163-180
31. Kong, X. X., Nir, E., Hamadani, K., and Weiss, S. (2007) Photobleaching pathways in single-molecule FRET experiments J. Am. Chem. Soc. 129, 4643-4654
32. Brune, R., Doose, S., and Sauer, M. (2007) Analyzing the influence of contact-mediated quenching processes on Förster resonance energy transfer. In Progress in Biomedical Optics and Imaging, pp 6633 - 6657, Optical Society of America, Baltimore.
33. Di Fiori, N. and Meller, A. (2010) The effect of dye-dye interactions on the spatial resolution of single-molecule FRET measurements in nucleic acids Biophys. J. 98, 2265-2272
34. Kumbhakar, M., Kiel, A., Pal, H., and Herten, D. P. (2009) Single-molecule fluorescence studies reveal long-range electron-transfer dynamics through double-stranded DNA ChemPhysChem 10, 629-633
35. Doose, S., Neuweiler, H., and Sauer, M. (2009) Fluorescence quenching by photoinduced electron transfer: A reporter for conformational dynamics of macromolecules ChemPhysChem 10, 1389-1398
36. Gralla, J. D., Carpousis, A. J., and Stefano, J. E. (1980) Productive and abortive initiation of transcription in vitro at the lac UV5 promoter Biochemistry 19, 5864-5869
37. Margeat, E., Kapanidis, A. N., Tinnefeld, P., Wang, Y., Mukhopadhyay, J., Ebright, R. H., and Weiss, S. (2006) Direct observation of abortive initiation and promoter escape within single immobilized transcription complexes Biophys. J. 90, 1419-1431
38. Roberts, J. W. (2006) Biochemistry. RNA polymerase, a scrunching machine Science 314, 1097-1098
39. Cheetham, G. M. and Steitz, T. A. (1999) Structure of a transcribing T7 RNA polymerase initiation complex Science 286, 2305-2309
40. Tang, G. Q., Roy, R., Ha, T., and Patel, S. S. (2008) Transcription initiation in a single-subunit RNA polymerase proceeds through DNA scrunching and rotation of the N-terminal subdornains Mol. Cell 30, 567-577
41. 70 with RNA polymerase during transcription: Fluorescence resonance energy transfer assay for movement relative to DNA Cell 106, 453-463
42. Kubori, T. and Shimamoto, N. (1996) A branched pathway in the early stage of transcription by Escherichia coli RNA polymerase J. Mol. Biol. 256, 449-457
43. Campbell, E. A., Korzheva, N., Mustaev, A., Murakami, K., Nair, S., Goldfarb, A., and Darst, S. A. (2001) Structural mechanism for rifampicin inhibition of bacterial RNA polymerase Cell 104, 901-912
44. Camara, B., Liu, M., Reynolds, J., Shadrin, A., Liu, B., Kwok, K., Simpson, P., Weinzierl, R., Severinov, K., Cota, E., Matthews, S., and Wigneshweraraj, S. R. (2010) T7 phage protein Gp2 inhibits the Escherichia coli RNA polymerase by antagonizing stable DNA strand separation near the transcription start site Proc. Natl. Acad. Sci. U.S.A. 107, 2247-2252