Distance-restrained docking of rifampicin and rifamycin SV to RNA polymerase using systematic FRET measurements: developing benchmarks of model quality and reliability.

We are developing distance-restrained docking strategies for modeling macromolecular complexes that combine available high-resolution structures of the components and intercomponent distance restraints derived from systematic fluorescence resonance energy transfer (FRET) measurements. In this article, we consider the problem of docking small-molecule ligands within macromolecular complexes. Using simulated FRET data, we have generated a series of benchmarks that permit estimation of model accuracy based on the quantity and quality of FRET-derived distance restraints, including the number, random error, systematic error, distance distribution, and radial distribution of FRET-derived distance restraints. We find that expected model accuracy is 10 A or better for models based on: i), > or =20 restraints with up to 15% random error and no systematic error, or ii), > or =20 restraints with up to 15% random error, up to 10% systematic error, and a symmetric radial distribution of restraints. Model accuracies can be improved to 5 A or better by increasing the number of restraints to > or =40 and/or by optimizing the distance distribution of restraints. Using experimental FRET data, we have defined the positions of the binding sites within bacterial RNA polymerase of the small-molecule inhibitors rifampicin (Rif) and rifamycin SV (Rif SV). The inferred binding sites for Rif and Rif SV were located with accuracies of, respectively, 7 and 10 A relative to the crystallographically defined binding site for Rif. These accuracies agree with expectations from the benchmark simulations and suffice to indicate that the binding sites for Rif and Rif SV are located within the RNA polymerase active-center cleft, overlapping the binding site for the RNA-DNA hybrid.

[1]  C. Wu,et al.  Spatial relationship of the sigma subunit and the rifampicin binding site in RNA polymerase of Escherichia coli. , 1976, Biochemistry.

[2]  J. Frank Single-particle imaging of macromolecules by cryo-electron microscopy. , 2002, Annual review of biophysics and biomolecular structure.

[3]  G. Chirikjian,et al.  An elastic network model of HK97 capsid maturation. , 2003, Journal of structural biology.

[4]  P. Cramer,et al.  Structural Basis of Transcription: RNA Polymerase II at 2.8 Ångstrom Resolution , 2001, Science.

[5]  Paul R. Selvin,et al.  The renaissance of fluorescence resonance energy transfer , 2000, Nature Structural Biology.

[6]  V. Unger,et al.  Electron cryomicroscopy methods. , 2001, Current opinion in structural biology.

[7]  R. Ebright,et al.  Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  N Maggi,et al.  Rifampicin: a new orally active rifamycin. , 1966, Chemotherapy.

[9]  I Chopra,et al.  Exploiting current understanding of antibiotic action for discovery of new drugs , 2002, Symposium series.

[10]  Jianpeng Ma,et al.  A dynamic analysis of the rotation mechanism for conformational change in F(1)-ATPase. , 2002, Structure.

[11]  W. Baumeister,et al.  Macromolecular electron microscopy in the era of structural genomics. , 2000, Trends in biochemical sciences.

[12]  W. Wriggers,et al.  Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory. , 2002, Journal of molecular biology.

[13]  B. Alberts The Cell as a Collection of Protein Machines: Preparing the Next Generation of Molecular Biologists , 1998, Cell.

[14]  A. Brünger Assessment of phase accuracy by cross validation: the free R value. Methods and applications. , 1993, Acta crystallographica. Section D, Biological crystallography.

[15]  John E. Johnson,et al.  Structural biology of viruses by the combination of electron cryomicroscopy and X-ray crystallography. , 2002, Biochemistry.

[16]  A. Lesk,et al.  Structural mechanisms for domain movements in proteins. , 1994, Biochemistry.

[17]  W. K. Hastings,et al.  Monte Carlo Sampling Methods Using Markov Chains and Their Applications , 1970 .

[18]  K. Murakami,et al.  Structural Basis of Transcription Initiation: RNA Polymerase Holoenzyme at 4 Å Resolution , 2002, Science.

[19]  P. Cramer,et al.  Architecture of the RNA Polymerase II-TFIIS Complex and Implications for mRNA Cleavage , 2003, Cell.

[20]  P. Doruker,et al.  Collective Motions of RNA Polymerases. Analysis of Core Enzyme, Elongation Complex and Holoenzyme , 2004, Journal of biomolecular structure & dynamics.

[21]  Jennifer L. Knight,et al.  Structural Organization of Bacterial RNA Polymerase Holoenzyme and the RNA Polymerase-Promoter Open Complex , 2002, Cell.

[22]  Jianpeng Ma New advances in normal mode analysis of supermolecular complexes and applications to structural refinement. , 2004, Current protein & peptide science.

[23]  P. Chacón,et al.  Multi-resolution contour-based fitting of macromolecular structures. , 2002, Journal of molecular biology.

[24]  W. Delano The PyMOL Molecular Graphics System , 2002 .

[25]  D. Bushnell,et al.  Structural Basis of Transcription: Separation of RNA from DNA by RNA Polymerase II , 2004, Science.

[26]  X. Verykios,et al.  Reforming reactions of acetic acid on nickel catalysts over a wide temperature range , 2006 .

[27]  W. L. Jorgensen,et al.  Development and Testing of the OPLS All-Atom Force Field on Conformational Energetics and Properties of Organic Liquids , 1996 .

[28]  C. Wu,et al.  Molecular mechanism of the rifampicin -RNA polymerase interaction. , 1976, Biochemistry.

[29]  Willy Wriggers,et al.  Conformational flexibility of bacterial RNA polymerase , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P. Sensi History of the development of rifampin. , 1983, Reviews of infectious diseases.

[31]  Th. Förster Zwischenmolekulare Energiewanderung und Fluoreszenz , 1948 .

[32]  R. Ebright RNA polymerase: structural similarities between bacterial RNA polymerase and eukaryotic RNA polymerase II. , 2000, Journal of molecular biology.

[33]  A. Brunger Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. , 1992 .

[34]  C. Wu,et al.  Statistical interpretation of fluorescence energy transfer measurements in macromolecular systems. , 1976, Biochemistry.

[35]  C. Wu,et al.  Studies of nucleotide binding to the ribonucleic acid polymerase by a fluoresence technique. , 1969, Biochemistry.

[36]  G. Kleywegt,et al.  Checking your imagination: applications of the free R value. , 1996, Structure.

[37]  P. Cramer,et al.  Structural Basis of Transcription: An RNA Polymerase II Elongation Complex at 3.3 Å Resolution , 2001, Science.

[38]  Jianjun Cui,et al.  Equidistribution on the Sphere , 1997, SIAM J. Sci. Comput..

[39]  R. Ebright,et al.  Fluorescence resonance energy transfer (FRET) in analysis of transcription-complex structure and function. , 2003, Methods in enzymology.

[40]  S. Yokoyama,et al.  Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution , 2002, Nature.

[41]  M. Sande The use of rifampin in the treatment of nontuberculous infections: an overview. , 1983, Reviews of infectious diseases.

[42]  K. Severinov,et al.  Crystal Structure of Thermus aquaticus Core RNA Polymerase at 3.3 Å Resolution , 1999, Cell.

[43]  Roger D Kornberg,et al.  Structural Basis of Transcription: An RNA Polymerase II-TFIIB Cocrystal at 4.5 Angstroms , 2004, Science.

[44]  S. Lowen The Biophysical Journal , 1960, Nature.

[45]  K Schulten,et al.  Protein domain movements: detection of rigid domains and visualization of hinges in comparisons of atomic coordinates , 1997, Proteins.

[46]  M. Rossmann,et al.  Combining electron microscopic with x-ray crystallographic structures. , 2001, Journal of structural biology.

[47]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.

[48]  Florence Tama,et al.  Mega-Dalton biomolecular motion captured from electron microscopy reconstructions. , 2003, Journal of molecular biology.

[49]  Roger D Kornberg,et al.  Complete, 12-subunit RNA polymerase II at 4.1-Å resolution: Implications for the initiation of transcription , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  B. W. van der Meer Kappa-squared: from nuisance to new sense. , 2002, Journal of biotechnology.

[51]  E. Orlova,et al.  Structure determination of macromolecular assemblies by single-particle analysis of cryo-electron micrographs. , 2004, Current opinion in structural biology.

[52]  C. D. dos Remedios,et al.  Fluorescence resonance energy transfer spectroscopy is a reliable "ruler" for measuring structural changes in proteins. Dispelling the problem of the unknown orientation factor. , 1995, Journal of structural biology.

[53]  P. Cramer,et al.  Architecture of initiation-competent 12-subunit RNA polymerase II , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  J Frank,et al.  Domain motions of EF-G bound to the 70S ribosome: insights from a hand-shaking between multi-resolution structures. , 2000, Biophysical journal.

[55]  B. V. D. Meer Kappa-squared: from nuisance to new sense , 2002 .

[56]  E. Katchalski‐Katzir,et al.  Effect of the orientation of donor and acceptor on the probability of energy transfer involving electronic transitions of mixed polarization. , 1978, Biochemistry.

[57]  S Birmanns,et al.  Using situs for flexible and rigid-body fitting of multiresolution single-molecule data. , 2001, Journal of structural biology.

[58]  R. Crowther,et al.  Macromolecular assemblages - putting the pieces together. , 2004, Current opinion in structural biology.

[59]  Robert E. Dale,et al.  Intramolecular distances determined by energy transfer. Dependence on orientational freedom of donor and acceptor , 1974 .

[60]  W Wriggers,et al.  Modeling tricks and fitting techniques for multiresolution structures. , 2001, Structure.

[61]  J. Eisinger,et al.  The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. , 1979, Biophysical journal.

[62]  S. Diekmann,et al.  Recent advances in FRET: distance determination in protein-DNA complexes. , 2001, Current opinion in structural biology.

[63]  M. Gerstein,et al.  A database of macromolecular motions. , 1998, Nucleic acids research.

[64]  C. Cech,et al.  On the mechanism of rifampicin inhibition of RNA synthesis. , 1978, The Journal of biological chemistry.

[65]  B. Meer,et al.  Resonance Energy Transfer: Theory and Data , 1994 .

[66]  Jianpeng Ma,et al.  Motions and negative cooperativity between p97 domains revealed by cryo-electron microscopy and quantised elastic deformational model. , 2003, Journal of molecular biology.

[67]  Jennifer L. Knight,et al.  Antibacterial peptide microcin J25 inhibits transcription by binding within and obstructing the RNA polymerase secondary channel. , 2004, Molecular cell.

[68]  M. Uschold,et al.  Methods and applications , 1953 .

[69]  H. Berendsen,et al.  Systematic analysis of domain motions in proteins from conformational change: New results on citrate synthase and T4 lysozyme , 1998, Proteins.

[70]  D. Lilley,et al.  Fluorescence resonance energy transfer as a structural tool for nucleic acids. , 2000, Current opinion in chemical biology.

[71]  J. Frank,et al.  Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[72]  R. Clegg Fluorescence resonance energy transfer and nucleic acids. , 1992, Methods in enzymology.

[73]  Arkady Mustaev,et al.  Structural Mechanism for Rifampicin Inhibition of Bacterial RNA Polymerase , 2001, Cell.

[74]  T S Baker,et al.  Low resolution meets high: towards a resolution continuum from cells to atoms. , 1996, Current opinion in structural biology.

[75]  A. Brünger Free R value: a novel statistical quantity for assessing the accuracy of crystal structures , 1992, Nature.

[76]  S. Darst,et al.  Insights into Escherichia coli RNA polymerase structure from a combination of x-ray and electron crystallography. , 1998, Journal of structural biology.

[77]  A. Gronenborn,et al.  Assessing the quality of solution nuclear magnetic resonance structures by complete cross-validation. , 1993, Science.