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DNA-segment-capture model for loop extrusion by structural maintenance of chromosome (SMC) protein complexes

John F. Marko, Paolo De Los Rios, Alessandro Barducci, Stephan Gruber
doi: https://doi.org/10.1101/325373
John F. Marko
1Department of Molecular Biosciences and Department of Physics & Astronomy, Northwestern University, Evanston IL 60208 USA
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  • For correspondence: john-marko@northwestern.edu
Paolo De Los Rios
2Laboratory of Statistical Biophysics, Institute of Physics, School of Basic Sciences and Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne - EPFL, 1015 Lausanne, Switzerland
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Alessandro Barducci
3Center de Biochimie Structurale, INSERM, CNRS, Université de Montpellier, 34090 Montpellier, France
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Stephan Gruber
4Department de microbiologie fondamentale, Université de Lausanne, 1015 Lausanne, Switzerland
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Abstract

Cells possess remarkable control of the folding and entanglement topology of long and flexible chromosomal DNA molecules. It is thought that structural maintenance of chromosome (SMC) protein complexes play a crucial role in this, by organizing long DNAs into series of loops. Experimental data suggest that SMC complexes are able to translocate on DNA, as well as pull out lengths of DNA via a “loop extrusion” process. We describe a Brownian loop-capture-ratchet model for translocation and loop extrusion based on known structural, catalytic, and DNA-binding properties of the Bacillus subtilis SMC complex. Our model provides an example of a new class of molecular motor where large conformational fluctuations of the motor ‘track’ - in this case DNA - are involved in the basic translocation process. Quantitative analysis of our model leads to a series of predictions for the motor properties of SMC complexes, most strikingly a strong dependence of SMC translocation velocity and step size on tension in the DNA track that it is moving along, with “stalling” occuring at subpiconewton tensions. We discuss how the same mechanism might be used by structurally related SMC complexes (E. coli MukBEF and eukaryote condensin, cohesin and SMC5/6) to organize genomic DNA.

Footnotes

  • Revision addresses referee concerns about presentation; no changes in results relative to original version. Essentially all the arithmetic has been moved to the Supplementary Data.

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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. It is made available under a CC-BY-NC 4.0 International license.
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Posted May 23, 2019.
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DNA-segment-capture model for loop extrusion by structural maintenance of chromosome (SMC) protein complexes
John F. Marko, Paolo De Los Rios, Alessandro Barducci, Stephan Gruber
bioRxiv 325373; doi: https://doi.org/10.1101/325373
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DNA-segment-capture model for loop extrusion by structural maintenance of chromosome (SMC) protein complexes
John F. Marko, Paolo De Los Rios, Alessandro Barducci, Stephan Gruber
bioRxiv 325373; doi: https://doi.org/10.1101/325373

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