The effect of macromolecular crowding on single-round transcription by Escherichia coli RNA polymerase

Previous works have reported significant effects of macromolecular crowding on the structure and behavior of biomolecules. The crowded intracellular environment, in contrast to in vitro buffer solutions, likely imparts similar effects on biomolecules. The enzyme serving as the gatekeeper for the genome, RNA polymerase (RNAP), is among the most regulated enzymes. Although it was previously demonstrated that macromolecular crowding affects association of RNAP to DNA, not much is known about how crowding acts on late initiation and promoter clearance steps, which are considered to be the rate-determining steps for many promoters. Here, we demonstrate that macromolecular crowding enhances the rate of late initiation and promoter clearance using in vitro quenching-based single-molecule kinetics assays. Moreover, the enhancement's dependence on crowder size notably deviates from predictions by the scaled-particle theory, commonly used for description of crowding effects. Our findings shed new light on how enzymatic reactions could be affected by crowded conditions in the cellular milieu.

[1]  Antonino Ingargiola,et al.  Different types of pausing modes during transcription initiation , 2017, Transcription.

[2]  S. Weiss,et al.  Backtracked and paused transcription initiation intermediate of Escherichia coli RNA polymerase , 2016, Proceedings of the National Academy of Sciences.

[3]  Nicole C. Robb,et al.  RNA Polymerase Pausing during Initial Transcription , 2016, Molecular cell.

[4]  Antonino Ingargiola,et al.  FRETBursts: An Open Source Toolkit for Analysis of Freely-Diffusing Single-Molecule FRET , 2016, bioRxiv.

[5]  B. Wielgus-Kutrowska,et al.  How can macromolecular crowding inhibit biological reactions? The enhanced formation of DNA nanoparticles , 2016, Scientific Reports.

[6]  Lenny H. H. Meijer,et al.  Macromolecular crowding develops heterogeneous environments of gene expression in picoliter droplets , 2015, Nature nanotechnology.

[7]  Thomas A Steitz,et al.  Crystal structures of the E. coli transcription initiation complexes with a complete bubble. , 2015, Molecular cell.

[8]  M. Raghunath,et al.  Macromolecular crowding gives rise to microviscosity, anomalous diffusion and accelerated actin polymerization , 2015, Physical biology.

[9]  Vladimir N. Uversky,et al.  Beyond the Excluded Volume Effects: Mechanistic Complexity of the Crowded Milieu , 2015, Molecules.

[10]  C. Bustamante,et al.  Trigger loop folding determines transcription rate of Escherichia coli’s RNA polymerase , 2014, Proceedings of the National Academy of Sciences.

[11]  V. Uversky,et al.  What Macromolecular Crowding Can Do to a Protein , 2014, International journal of molecular sciences.

[12]  M. Tabaka,et al.  The effect of macromolecular crowding on mobility of biomolecules, association kinetics, and gene expression in living cells , 2014, Front. Phys..

[13]  R. Best,et al.  Molecular Origins of Internal Friction Effects on Protein Folding Rates , 2014, Nature Communications.

[14]  K. Murakami,et al.  Structural Basis of Transcription Initiation by Bacterial RNA Polymerase Holoenzyme* , 2014, The Journal of Biological Chemistry.

[15]  D. Nesbitt,et al.  Molecular-crowding effects on single-molecule RNA folding/unfolding thermodynamics and kinetics , 2014, Proceedings of the National Academy of Sciences.

[16]  Vadim Backman,et al.  Macromolecular crowding as a regulator of gene transcription. , 2014, Biophysical journal.

[17]  B. Schuler,et al.  Single-molecule spectroscopy reveals polymer effects of disordered proteins in crowded environments , 2014, Proceedings of the National Academy of Sciences.

[18]  Carlos Bustamante,et al.  Molecular Mechanisms of Transcription through Single-Molecule Experiments , 2014, Chemical reviews.

[19]  Craig T Martin,et al.  Insights into the Mechanism of Initial Transcription in Escherichia coli RNA Polymerase* , 2013, The Journal of Biological Chemistry.

[20]  A. Piruska,et al.  Enhanced transcription rates in membrane-free protocells formed by coacervation of cell lysate , 2013, Proceedings of the National Academy of Sciences.

[21]  A. Cheng,et al.  Development of new photon-counting detectors for single-molecule fluorescence microscopy , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  Charles C. Richardson,et al.  Impact of macromolecular crowding on DNA replication , 2012, Nature Communications.

[23]  Dan Luo,et al.  Cell-Free Protein Expression under Macromolecular Crowding Conditions , 2011, PloS one.

[24]  K. O'Halloran,et al.  “Double-Trouble” for Respiratory Control in Pompe Disease , 2011, Front. Physio..

[25]  T. Powers,et al.  Effects of Viscogens on RNA Transcription inside Reovirus Particles* , 2011, The Journal of Biological Chemistry.

[26]  H. Butt,et al.  Comparative analysis of viscosity of complex liquids and cytoplasm of mammalian cells at the nanoscale. , 2011, Nano letters.

[27]  Ron R Lin,et al.  High-throughput single-molecule optofluidic analysis , 2011, Nature Methods.

[28]  A. Loman Molecular Sizing using Fluorescence Correlation Spectroscopy , 2010 .

[29]  S. Hagen,et al.  Solvent viscosity and friction in protein folding dynamics. , 2010, Current protein & peptide science.

[30]  Heidelinde R. C. Dietrich,et al.  The persistence length of double stranded DNA determined using dark field tethered particle motion. , 2009, The Journal of chemical physics.

[31]  Michelle D. Wang,et al.  Chapter 9:Kinetic Modeling of Transcription Elongation , 2009 .

[32]  H. Buc,et al.  Where it all Begins: An Overview of Promoter Recognition and Open Complex Formation , 2009 .

[33]  Huan‐Xiang Zhou,et al.  Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. , 2008, Annual review of biophysics.

[34]  Shimon Weiss,et al.  Initial Transcription by RNA Polymerase Proceeds Through a DNA-Scrunching Mechanism , 2006, Science.

[35]  Shimon Weiss,et al.  Shot-noise limited single-molecule FRET histograms: comparison between theory and experiments. , 2006, The journal of physical chemistry. B.

[36]  A. Minton,et al.  How can biochemical reactions within cells differ from those in test tubes? , 2006, Journal of Cell Science.

[37]  A. Minton,et al.  Macromolecular crowding , 2006, Current Biology.

[38]  Nam Ki Lee,et al.  Alternating-laser excitation of single molecules. , 2005, Accounts of chemical research.

[39]  Nam Ki Lee,et al.  Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. , 2005, Biophysical journal.

[40]  N H Dekker,et al.  Single-molecule measurements of the persistence length of double-stranded RNA. , 2005, Biophysical journal.

[41]  D. Thirumalai,et al.  Molecular crowding enhances native state stability and refolding rates of globular proteins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Minton,et al.  Models for excluded volume interaction between an unfolded protein and rigid macromolecular cosolutes: macromolecular crowding and protein stability revisited. , 2005, Biophysical journal.

[43]  Arkady Mustaev,et al.  A Ratchet Mechanism of Transcription Elongation and Its Control , 2005, Cell.

[44]  R. Landick,et al.  The Structure of Bacterial RNA Polymerase , 2005 .

[45]  S. Hagen,et al.  Internal friction controls the speed of protein folding from a compact configuration. , 2004, Biochemistry.

[46]  Nam Ki Lee,et al.  Fluorescence-aided molecule sorting: Analysis of structure and interactions by alternating-laser excitation of single molecules , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  T. Ha,et al.  Probing single-stranded DNA conformational flexibility using fluorescence spectroscopy. , 2004, Biophysical journal.

[48]  Joshua W. Shaevitz,et al.  Backtracking by single RNA polymerase molecules observed at near-base-pair resolution , 2003, Nature.

[49]  Elio A. Abbondanzieri,et al.  Ubiquitous Transcriptional Pausing Is Independent of RNA Polymerase Backtracking , 2003, Cell.

[50]  Allen P. Minton,et al.  Cell biology: Join the crowd , 2003, Nature.

[51]  K. Murakami,et al.  Bacterial RNA polymerases: the wholo story. , 2003, Current opinion in structural biology.

[52]  R. Ellis Macromolecular crowding : obvious but underappreciated , 2022 .

[53]  A Volkmer,et al.  Data registration and selective single-molecule analysis using multi-parameter fluorescence detection. , 2001, Journal of biotechnology.

[54]  J. Hofrichter,et al.  Effect of Viscosity on the Kinetics of α-Helix and β-Hairpin Formation , 2001 .

[55]  C. Dobson,et al.  Macromolecular crowding perturbs protein refolding kinetics: implications for folding inside the cell , 2000, The EMBO journal.

[56]  F. Rojo Repression of Transcription Initiation in Bacteria , 1999, Journal of bacteriology.

[57]  D Baker,et al.  Limited internal friction in the rate-limiting step of a two-state protein folding reaction. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[58]  M. Thomas Record,et al.  RNA Polymerase-Promoter Interactions: the Comings and Goings of RNA Polymerase , 1998, Journal of bacteriology.

[59]  D. Dasgupta,et al.  Enhancement of transcriptional activity of T7 RNA polymerase by guanidine hydrochloride , 1998, FEBS letters.

[60]  S. Zimmerman,et al.  Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. , 1991, Journal of molecular biology.

[61]  J. C. Selser,et al.  Asymptotic behavior and long-range interactions in aqueous solutions of poly(ethylene oxide) , 1991 .

[62]  M. Meireles,et al.  A contribution to the translation of retention curves into pore size distributions for sieving membranes , 1990 .

[63]  A. Fulton,et al.  How crowded is the cytoplasm? , 1982, Cell.

[64]  Shigenoki Kuga Pore size distribution analysis of gel substances by size exclusion chromatography , 1981 .

[65]  R. Losick In vitro transcription. , 1972, Annual review of biochemistry.

[66]  A. K. Solomon,et al.  Determination of the Effective Hydrodynamic Radii of Small Molecules by Viscometry , 1961, The Journal of general physiology.

[67]  H. Kramers Brownian motion in a field of force and the diffusion model of chemical reactions , 1940 .