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Sequential eviction of crowded nucleoprotein complexes by the RecBCD molecular motor

Tsuyoshi Terakawa, Sy Redding, Timothy D. Silverstein, Eric C. Greene
doi: https://doi.org/10.1101/142224
Tsuyoshi Terakawa
1Department of Biochemistry & Molecular Biophysics, Columbia University, New York, NY 10032, USA
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Sy Redding
1Department of Biochemistry & Molecular Biophysics, Columbia University, New York, NY 10032, USA
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Timothy D. Silverstein
1Department of Biochemistry & Molecular Biophysics, Columbia University, New York, NY 10032, USA
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Eric C. Greene
1Department of Biochemistry & Molecular Biophysics, Columbia University, New York, NY 10032, USA
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  • For correspondence: ecg2108@cumc.columbia.edu
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Abstract

In physiological settings, all nucleic acids motor proteins must travel along substrates that are crowded with other proteins. However, the physical basis for how motor proteins behave in these highly crowded environments remains unknown. Here we use real–time single molecule imaging, kinetic Monte Carlo simulations, and Molecular dynamics simulations to determine how the ATP-dependent translocase RecBCD travels along DNA occupied by tandem arrays of high affinity DNA–binding proteins. We demonstrate that RecBCD forces each protein into its nearest adjacent neighbor, causing rapid disruption of the underlying protein–nucleic acid interface. This mechanism is not simply the same way that RecBCD disrupts isolated nucleoprotein complexes on otherwise naked DNA. Instead, molecular crowding itself completely alters the mechanism by which RecBCD removes tightly bound protein obstacles from DNA.

Significance statement Chromosomes are crowded places, and any nucleic acid motor proteins that act upon DNA must function within these crowded environments. How crowded environments affect motor protein behaviors remains largely unexplored. Here, we use single molecule fluorescence microscopy visualize the ATP-dependent motor protein RecBCD as it travels along crowded DNA molecules bearing long tandem arrays of DNA-binding proteins. Our findings show that RecBCD can push through highly crowded protein arrays while evicting the proteins from DNA. Molecular dynamics simulations suggest that RecBCD forces the proteins into once another, causing rapid disruption of the protein-DNA interface. These findings may provide insights into how other types of motor proteins travel along crowded nucleic acids.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 25, 2017.
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Sequential eviction of crowded nucleoprotein complexes by the RecBCD molecular motor
Tsuyoshi Terakawa, Sy Redding, Timothy D. Silverstein, Eric C. Greene
bioRxiv 142224; doi: https://doi.org/10.1101/142224
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Sequential eviction of crowded nucleoprotein complexes by the RecBCD molecular motor
Tsuyoshi Terakawa, Sy Redding, Timothy D. Silverstein, Eric C. Greene
bioRxiv 142224; doi: https://doi.org/10.1101/142224

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