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Monitoring the compaction of single DNA molecules in Xenopus egg extract in real time

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [4];  [4];  [5];  [1]
  1. Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720
  2. Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, Institute for Quantitative Biosciences (QB3), University of California, Berkeley, CA 94720
  3. Institute for Quantitative Biosciences (QB3), University of California, Berkeley, CA 94720
  4. Chromosome Dynamics Laboratory, RIKEN, Wako 351-0198, Japan
  5. Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, Institute for Quantitative Biosciences (QB3), University of California, Berkeley, CA 94720, Department of Physics, University of California, Berkeley, CA 94720, Department of Chemistry, University of California, Berkeley, CA 94720, HHMI, University of California, Berkeley, CA 94720

DNA compaction is required for the condensation and resolution of chromosomes during mitosis, but the relative contribution of individual chromatin factors to this process is poorly understood. We developed a physiological, cell-free system using high-speed Xenopus egg extracts and optical tweezers to investigate real-time mitotic chromatin fiber formation and force-induced disassembly on single DNA molecules. Compared to interphase extract, which compacted DNA by ~60%, metaphase extract reduced DNA length by over 90%, reflecting differences in whole-chromosome morphology under these two conditions. Depletion of the core histone chaperone ASF1, which inhibits nucleosome assembly, decreased the final degree of metaphase fiber compaction by 29%, while depletion of linker histone H1 had a greater effect, reducing total compaction by 40%. Compared to controls, both depletions reduced the rate of compaction, led to more short periods of decompaction, and increased the speed of force-induced fiber disassembly. In contrast, depletion of condensin from metaphase extract strongly inhibited fiber assembly, resulting in transient compaction events that were rapidly reversed under high force. Altogether, these findings support a speculative model in which condensin plays the predominant role in mitotic DNA compaction, while core and linker histones act to reduce slippage during loop extrusion and modulate the degree of DNA compaction.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
Japan Society for the Promotion of Science (JSPS); National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1961479
Alternate ID(s):
OSTI ID: 2422587
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 12 Vol. 120; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

References (30)

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Chromatin Transitions during Early Xenopus Embryogenesis: Changes in Histone H4 Acetylation and in Linker Histone Type journal November 1993
Methods for Studying Spindle Assembly and Chromosome Condensation in Xenopus Egg Extracts book January 2006
Condensin action and compaction journal October 2018
Condensin: Architect of mitotic chromosomes journal February 2009
Effects of DNA supercoiling on chromatin architecture journal November 2016
[7] Optical-trap force transducer that operates by direct measurement of light momentum book January 2003
Differential Contributions of Condensin I and Condensin II to Mitotic Chromosome Architecture in Vertebrate Cells journal October 2003
Functional Comparison of H1 Histones in Xenopus Reveals Isoform-Specific Regulation by Cdk1 and RanGTP journal June 2010
Primary Role of the Nucleosome journal August 2020
Structural features of nucleosomes in interphase and metaphase chromosomes journal November 2021
Mitotic chromosomes journal September 2021
Mitotic Chromosome Mechanics: How Cells Segregate Their Genome journal September 2019
Nucleosomal regulation of chromatin composition and nuclear assembly revealed by histone depletion journal June 2014
Guiding functions of the C-terminal domain of topoisomerase IIα advance mitotic chromosome assembly journal May 2021
DNA-loop extruding condensin complexes can traverse one another journal March 2020
Histone H1 is essential for mitotic chromosome architecture and segregation in Xenopus laevis egg extracts journal June 2005
A quantitative map of human Condensins provides new insights into mitotic chromosome architecture journal April 2018
Micromanipulation Studies of Chromatin Fibers in Xenopus Egg Extracts Reveal ATP-dependent Chromatin Assembly Dynamics journal February 2007
Histone H1 compacts DNA under force and during chromatin assembly journal December 2012
Reconstituting Nuclear and Chromosome Dynamics Using Xenopus Extracts journal August 2018
Mitotic chromosome assembly despite nucleosome depletion in Xenopus egg extracts journal June 2017
A pathway for mitotic chromosome formation journal January 2018
Real-time imaging of DNA loop extrusion by condensin journal April 2018
Xenopus Egg Extracts Increase Dynamics of Histone H1 on Sperm Chromatin journal September 2010
Cohesin acetylation and Wapl‐Pds5 oppositely regulate translocation of cohesin along DNA journal November 2016
Single Chromatin Fiber Stretching Reveals Physically Distinct Populations of Disassembly Events journal May 2005
Probing the Mechanical Folding Kinetics of TAR RNA by Hopping, Force-Jump, and Force-Ramp Methods journal January 2006
Cohesin and condensin extrude DNA loops in a cell cycle-dependent manner journal May 2020
Linker histone H1.8 inhibits chromatin binding of condensins and DNA topoisomerase II to tune chromosome length and individualization journal August 2021

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