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Chromosome organization by one-sided and two-sided loop extrusion

View ORCID ProfileEdward J. Banigan, View ORCID ProfileAafke A. van den Berg, View ORCID ProfileHugo B. Brandão, John F. Marko, View ORCID ProfileLeonid A. Mirny
doi: https://doi.org/10.1101/815340
Edward J. Banigan
1Institute for Medical Engineering & Science, Massachusetts Institute of Technology
2Department of Physics, Massachusetts Institute of Technology
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Aafke A. van den Berg
1Institute for Medical Engineering & Science, Massachusetts Institute of Technology
2Department of Physics, Massachusetts Institute of Technology
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Hugo B. Brandão
3Harvard Graduate Program in Biophysics, Harvard University
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John F. Marko
4Departments of Molecular Biosciences and Physics & Astronomy, Northwestern University
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Leonid A. Mirny
1Institute for Medical Engineering & Science, Massachusetts Institute of Technology
2Department of Physics, Massachusetts Institute of Technology
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  • ORCID record for Leonid A. Mirny
  • For correspondence: leonid@mit.edu
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Abstract

SMC complexes, such as condensin or cohesin, organize chromatin throughout the cell cycle by a process known as loop extrusion. SMC complexes reel in DNA, extruding and progressively growing DNA loops. Modeling assuming two-sided loop extrusion reproduces key features of chromatin organization across different organisms. In vitro single-molecule experiments confirmed that yeast condensins extrude loops, however, they remain anchored to their loading sites and extrude loops in a “one-sided” manner. We therefore simulate one-sided loop extrusion to investigate whether “one-sided” complexes can compact mitotic chromosomes, organize interphase domains, and juxtapose bacterial chromosomal arms, as can be done by “two-sided” loop extruders. While one-sided loop extrusion cannot reproduce these phenomena, variants can recapitulate in vivo observations. We predict that SMC complexes in vivo constitute effectively two-sided motors or exhibit biased loading and propose relevant experiments. Our work suggests that loop extrusion is a viable general mechanism of chromatin organization.

Impact statement We reconcile seemingly contradictory findings of single-molecule and in vivo experiments on a major mechanism of chromosome organization by computationally investigating mechanisms of loop extrusion that are consistent with both.

Footnotes

  • We have added a section to discuss the organization of the yeast chromosome, as well as a more thorough discussion of the effects of transcription and SMC diffusion on the chromosome organization. Furthermore, new figures were added or updated: Figure 2 supplements 6 and 7 and Figure supplement 8.

Copyright 
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-ND 4.0 International license.
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Posted April 02, 2020.
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Chromosome organization by one-sided and two-sided loop extrusion
Edward J. Banigan, Aafke A. van den Berg, Hugo B. Brandão, John F. Marko, Leonid A. Mirny
bioRxiv 815340; doi: https://doi.org/10.1101/815340
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Chromosome organization by one-sided and two-sided loop extrusion
Edward J. Banigan, Aafke A. van den Berg, Hugo B. Brandão, John F. Marko, Leonid A. Mirny
bioRxiv 815340; doi: https://doi.org/10.1101/815340

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