Solute probes of conformational changes in open complex (RPo) formation by Escherichia coli RNA polymerase at the λPR promoter: Evidence for unmasking of the active site in the isomerization step and for large-scale coupled folding in the subsequent conversion to RP o

Biochemistry

Volumn 45, Issue 7, 2006, Pages 2161-2177

  Kontur, Wayne S ^a   Saecker, Ruth M ^a,b   Davis, Caroline A ^a   Capp, Michael W ^a   Record Jr , M Thomas ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; DISSOCIATION; DNA; ESCHERICHIA COLI; ISOMERIZATION; NITROGEN COMPOUNDS; PROTEINS; RATE CONSTANTS; REACTION KINETICS; RNA; UREA;

COUPLED PROTEIN FOLDING; GLYCINE BETAINE (GB); RPO; SURFACE AREA;

ENZYMES;

BETAINE; DNA; RNA POLYMERASE; UREA;

AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL REACTION KINETICS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DISSOCIATION; DNA STRUCTURE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; TRANSCRIPTION INITIATION;

BACTERIOPHAGE LAMBDA; BETAINE; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, MOLECULAR; PROMOTER REGIONS (GENETICS); PROTEIN CONFORMATION; SIGMA FACTOR; UREA;

ESCHERICHIA COLI;

EID: 33144477944     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051835v     Document Type: Article

References (82)

1. R promoter, J. Mol. Biol. 176, 495-522.
2. R promoter: large scale conformational changes in forming the kinetically significant intermediates, J. Mol. Biol. 319, 649-671.
3. R promoter interaction. Assignment of the kinetic steps corresponding to protein conformational change and DNA opening, J. Mol. Biol. 184, 441-453.
4. R promoter by salt concentration, Biochemistry 24, 4721-4726.
5. 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.
6. Kadesch, T. R., Rosenberg, S., and Chamberlin, M. J. (1982) Binding of Escherichia coli RNA polymerase holoenzyme to bacteriophage T7 DNA. Measurements of binding at bacteriophage T7 promoter A1 using a template competition assay, J. Mol. Biol. 155, 1-29.
7. Rosenberg, S., Kadesch, T. R., and Chamberlin, M. J. (1982) Binding of Escherichia coli RNA polymerase holoenzyme to bacteriophage T7 DNA. Measurements of the rate of open complex formation at T7 promoter A, J. Mol. Biol. 155, 31-51.
8. Johnson, R. S., and Chester, R. E. (1998) Stopped-flow kinetic analysis of the interaction of Escherichia coli RNA polymerase with the bacteriophage T7 A1 promoter, J. Mol. Biol. 283, 353-370.
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. Li, X. Y., and McClure, W. R. (1998) Characterization of the closed complex intermediate formed during transcription initiation by Escherichia coli RNA polymerase, J. Biol. Chem. 273, 23549-23557.
11. Craig, M. L., Tsodikov, O. V., McQuade, K. L., Schlax, P. E., Jr., Capp, M. W., Saecker, R. M., and Record, M. T., Jr. (1998) DNA footprints of the two kinetically significant intermediates in formation of an RNA polymerase-promoter open complex: evidence that interactions with start site and downstream DNA induce sequential conformational changes in polymerase and DNA, J. Mol. Biol. 283, 741-756.
12. Davis, C. A., Capp, M. W., Record, M. T., Jr., and Saecker, R. M. (2005) The effects of upstream DNA on open complex formation by Escherichia coli RNA polymerase, Proc. Natl. Acad. Sci. U.S.A. 102, 285-290.
13. Schickor, P., Metzger, W., Werel, W., Lederer, H., and Heumann, H. (1990) Topography of intermediates in transcription initiation of E. coli, EMBO J. 9, 2215-2220.
14. Vassylyev, D. G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M. N., Borukhov, S., and Yokoyama, S. (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution, Nature 417, 712-719.
15. Murakami, K. S., Masuda, S., and Darst, S. A. (2002) Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Å resolution, Science 296, 1280-1284.
16. Murakami, K. S., and Darst, S. A. (2003) Bacterial RNA polymerases: the wholo story. Curr. Opin. Struct. Biol. 13, 31-39.
17. Mekler, V., Kortkhonjia, E., Mukhopadhyay, J., Knight, J., Revyakin, A., Kapanidis, A. N., Niu, W., Ebright, Y. W., Levy, R., and Ebright, R. H. (2002) Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell 108, 599-614.
18. Murakami, K. S., Masuda, S., Campbell, E. A., Muzzin, O., and Darst, S. A. (2002) Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex, Science 296, 1285-1290.
19. Callaci, S., Heyduk, E., and Heyduk, T. (1999) Core RNA polymerase from E. coli induces a major change in the domain arrangement of the sigma 70 subunit, Mol. Cell 3, 229-238.
20. Darst, S. A., Opalka, N., Chacon, P., Polyakov, A., Richter, C., Zhang, G., and Wriggers, W. (2002) Conformational flexibility of bacterial RNA polymerase, Proc. Natl. Acad. Sci. U.S.A. 99, 4296-4301.
21. Spassky, A., Kirkegaard, K., and Buc, H. (1985) Changes in the DNA structure of the lacUV5 promoter during formation of an open complex with Escherichia coli RNA polymerase, Biochemistry 24, 2723-2731.
22. Buckle, M., Pemberton, I. K., Jacquet, M. A., and Buc, H. (1999) The kinetics of sigma subunit directed promoter recognition by E. coli RNA polymerase, J. Mol. Biol. 285, 955-964.
23. McKane, M., and Gussin, G. N. (2000) Changes in the 17 bp spacer in the PR promoter of bacteriophage lambda affect steps in open complex formation that precede DNA strand separation, J. Mol. Biol. 299, 337-349.
24. Bartlett, M. S., Gaal, T., Ross, W., and Gourse, R. L. (1998) RNA polymerase mutants that destabilize RNA polymerase-promoter complexes alter NTP-sensing by rrn P1 promoters, J. Mol. Biol. 279, 331-345.
25. 32 at the groE promoter, J. Mol. Biol. 210, 521-530.
26. i), Biochemistry 40, 2023-2031.
27. Schroeder, L. A., and deHaseth, P. L. (2005) Mechanistic differences in promoter DNA melting by Thermus aquaticus and Escherichia coli RNA polymerases, J. Biol. Chem. 280, 17422-17429.
28. McQuade, K. L. (1996) Ph.D. Thesis, University of Wisconsin-Madison, Madison, WI.
29. Spolar, R. S., and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA, Science 263, 777-784.
30. Spolar, R. S., Livingstone, J. R., and Record, M. T., Jr. (1992) Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water, Biochemistry 31, 3947-3955.
31. Murphy, K. P., and Freire, E. (1992) Thermodynamics of structural stability and cooperative folding behavior in proteins, Adv. Protein Chem. 43, 313-361.
32. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m-values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
33. Ferrari, M. E., and Lohman, T. M. (1994) Apparent heat capacity change accompanying a nonspecific protein-DNA interaction. Escherichia coli SSB tetramer binding to oligodeoxyadenylates, Biochemistry 33, 12896-12910.
34. Kozlov, A. G., and Lohman, T. M. (1999) Adenine base unstacking dominates the observed enthalpy and heat capacity changes for the Escherichia coli SSB tetramer binding to single-stranded oligoadenylates, Biochemistry, 38, 7388-7397.
35. Kozlov, A. G., and Lohman, T. M. (2000) Large contributions of coupled protonation equilibria to the observed enthalpy and heat capacity changes for ssDNA binding to Escherichia coli SSB protein, Proteins (Suppl. 4), 8-22.
36. Holbrook, J. A., Tsodikov, O. V., Saecker, R. M., and Record, M. T., Jr. (2001) Specific and non-specific interactions of integration host factor with DNA: thermodynamic evidence for disruption of multiple IHF surface salt-bridges coupled to DNA binding, J. Mol. Biol. 310, 379-401.
37. Scholtz, J. M., Barrick, D., York, E. J., Stewart, J. M., and Baldwin, R. L. (1995) Urea unfolding of peptide helices as a model for interpreting protein unfolding, Proc. Natl. Acad. Sci. U.S.A. 92, 185-189.
38. Hong, J., Capp, M. W., Anderson, C. F., Saecker, R. M., Felitsky, D. J., Anderson, M. W., and Record, M. T., Jr. (2004) Preferential interactions of glycine betaine and of urea with DNA: implications for DNA hydration and for effects of these solutes on DNA stability. Biochemistry 43, 14744-58.
39. Hong, J., Capp, M. W., Saecker, R. M., and Record, M. T., Jr. (2005) Use of urea and glycine betaine to quantify coupled folding and probe the burial of DNA phosphates in lac repressor-lac operator binding, Biochemistry 44, 16896-16911.
40. Bell, C. E., and Lewis, M. (2000) A closer view of the conformation of the lac repressor bound to operator, Nat. Struct. Biol. 7, 209-214.
41. Spronk, C. A., Slijper, M., van Boom, J. H., Kaptein, R., and Boelens, R. (1996) Formation of the hinge helix in the lac repressor is induced upon binding to the lac operator, Nat. Struct. Biol. 3, 916-919.
42. Schiefner, A., Breed, J., Bosser, L., Kneip, S., Gade, J., Holtmann, G., Diederichs, K., Weite, W., and Bremer, E. (2004) Cation-pi interactions as determinants for binding of the compatible solutes glycine betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli, J. Biol. Chem. 279, 5588-5596.
43. Felitsky, D. J., Cannon, J. G., Capp, M. W., Hong, J., Van Wynsberghe, A. W., Anderson, C. F., and Record, M. T., Jr. (2004) The exclusion of glycine betaine from anionic biopolymer surface: why glycine betaine is an effective osmoprotectant but also a compatible solute, Biochemistry 43, 14732-14743.
44. Artsimovitch, I., Svetlov, V., Murakami, K. S., and Landick, R. (2003) Co-overexpression of Escherichia coli RNA polymerase subunits allows isolation and analysis of mutant enzymes lacking lineage-specific sequence insertions, J. Biol. Chem. 278, 12344-12355.
45. Studier, F. W. (2005) Protein production by auto-induction in high-density shaking cultures, Protein Expression Purif. 41, 207-234.
46. Borukhov, S., and Goldfarb, A. (1993) Recombinant Escherichia coli RNA polymerase: purification of individually overexpressed subunits and in vitro assembly, Protein Expression Purif. 4, 503-511.
47. 2+ binding and its structural consequences at the transcription start site, Biochemistry 34, 15624-15632.
48. Saecker, R. M., Tsodikov, O. V., Capp, M. W., and Record, M. T., Jr. (2003) Rapid quench mixing to quantify kinetics of steps in association of Escherichia coli RNA polymerase with promoter DNA, Methods Enzymol. 370, 535-546.
49. R promoter DNA, Biophys. J. 76, 1320-1329.
50. Hong, J., Capp, M. W., Anderson, C. F., and Record, M. T. (2003) Preferential interactions in aqueous solutions of urea and KCl, Biophys. Chem. 105, 517-532.
51. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., and Dunker, A. K. (2001) Sequence complexity of disordered protein, Proteins 42, 38-48.
52. Li, X., Romero, P., Rani, M., Dunker, A. K., and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions, Genome Inf. Ser. 10, 30-40.
53. Kamali-Moghaddam, M., and Geiduschek, E. P. (2003) Thermoirreversible and thermoreversible promoter opening by two Escherichia coli RNA polymerase holoenzymes, J. Biol. Chem. 278, 29701-29709.
54. Walter, G., Zillig, W., Palm, P., and Fuchs, E. (1967) Initiation of DNA-dependent RNA synthesis and the effect of heparin on RNA polymerase, Eur. J. Biochem. 3, 194-201.
55. Helmann, J. D., and deHaseth, P. L. (1999) Protein-nucleic acid interactions during open complex formation investigated by systematic alteration of the protein and DNA binding partners, Biochemistry 38, 5959-5967.
56. Korzheva, N., Mustaev, A., Kozlov, M., Malhotra, A., Nikiforov, V., Goldfarb, A., and Darst, S. A. (2000) A structural model of transcription elongation, Science 289, 619-625.
57. Opalka, N., Chlenov, M., Chacon, P., Rice, W. J., Wriggers, W., and Darst, S. A. (2003) Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase, Cell 114, 335-345.
58. Chlenov, M., Masuda, S., Murakami, K. S., Nikiforov, V., Darst, S. A., and Mustaev, A. (2005) Structure and function of lineage-specific sequence insertions in the bacterial RNA polymerase β′ subunit, J. Mol. Biol. 353, 138-154.
59. Karlin, D., Perron, F., Canard, B., and Longhi, S. (2003) Structural disorder and modular organization in Paramyxovirinae N and P, J. Gen. Virol. 84, 3239-3252.
60. Tozawa, K., Macdonald, C. J., Penfold, C. N., James, R., Kleanthous, C., Clayden, N. J., and Moore, G. R. (2005) Clusters in an intrinsically disordered protein create a protein-binding site: the TolB-binding region of colicin E, Biochemistry 44, 11496-11507.
61. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol. 6, 197-208.
62. Zhang, G., Campbell, E. A., Minakhin, L., Richter, C., Severinov, K., and Darst, S. A. (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution, Cell 98, 811-824.
63. Ederth, J., Artsimovitch, I., Isaksson, L. A., and Landick, R. (2002) The downstream DNA jaw of bacterial RNA polymerase facilitates both transcriptional initiation and pausing, J. Biol. Chem. 277, 37456-37463.
64. Paul, B. J., Barker, M. M., Ross, W., Schneider, D. A., Webb, C., Foster, J. W., and Course, R. L. (2004) DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP, Cell 118, 311-322.
65. Perederina, A., Svetlov, V., Vassylyeva, M. N., Tahirov, T. H., Yokoyama, S., Artsimovitch, I., and Vassylyev, D. G. (2004) Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription, Cell 118, 297-309.
66. Paul, B. J., Berkmen, M. B., and Gourse, R. L. (2005) DksA potentiates direct activation of amino acid promoters by ppGpp, Proc. Natl. Acad. Sci. U.S.A. 102, 7823-7828.
67. Stebbins, C. E., Borukhov, S., Orlova, M., Polyakov, A., Goldfarb, A., and Darst, S. A. (1995) Crystal structure of the GreA transcript cleavage factor from Escherichia coli, Nature 373, 636-640.
68. Koulich, D., Orlova, M., Malhotra, A., Sali, A., Darst, S. A., and Borukhov, S. (1997) Domain organization of Escherichia coli transcript cleavage factors GreA and GreB, J. Biol. Chem. 272, 7201-7210.
69. Lerner, R. A., Benkovic, S. J., and Schultz, P. G. (1991) At the crossroads of chemistry and immunology: catalytic antibodies, Science 252, 659-667.
70. 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.
71. Campbell, E. A., Muzzin, O., Chlenov, M., Sun, J. L., Olson, C. A., Weinman, O., Trester-Zedlitz, M. L., and Darst, S. A. (2002) Structure of the bacterial RNA polymerase promoter specificity sigma subunit, Mol. Cell 9, 527-539.
72. Benoff, B., Yang, H., Lawson, C. L., Parkinson, G., Liu, J., Blatter, E., Ebright, Y. W., Berman, H. M., and Ebright, R. H. (2002) Structural basis of transcription activation: the CAP-alpha CTD-DNA complex, Science 297, 1562-1566.
73. 70 that are involved in interaction with RNA polymerase core enzyme, Genes Cells 2, 725-734.
74. Saecker, R. M., and Record, M. T., Jr. (2002) Protein surface salt bridges and paths for DNA wrapping, Curr. Opin. Struct. Biol. 12, 311-319.
75. Holbrook, J. A., Capp, M. W., Saecker, R. M., and Record, M. T., Jr. (1999) Enthalpy and heat capacity changes for formation of an oligomeric DNA duplex: interpretation in terms of coupled processes of formation and association of single-stranded helices, Biochemistry 38, 8409-8422.
76. 2+, Biochemistry 31, 7815-7825.
77. 2O system, J. Phys. Chem. Ref. Data 28, 1-17.
78. Weast, R. C. Handbook of Chemistry and Physics; CRC Press, Cleveland, OH, 1975; p D-235.
79. Rice, P. A., Yang, S., Mizuuchi, K., and Nash, H. A. (1996) Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn, Cell 87, 1295-306.
80. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W., and Richmond, T. J. (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution, J. Mol. Biol. 319, 1097-1113.
81. Kraulis, P. J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
82. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: photorealistic molecular graphics, Methods Enzymol. 277, 505-524.