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Research Article

Nucleosomal arrangement affects single-molecule transcription dynamics

Veronika Fitz, Jaeoh Shin, Christoph Ehrlich, Lucas Farnung, Patrick Cramer, Vasily Zaburdaev, and Stephan W. Grill
PNAS November 8, 2016 113 (45) 12733-12738; first published October 24, 2016; https://doi.org/10.1073/pnas.1602764113
Veronika Fitz
aBiotechnology Center, Technical University Dresden, 01307 Dresden, Germany;
bMax Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
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Jaeoh Shin
cMax Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany;
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Christoph Ehrlich
aBiotechnology Center, Technical University Dresden, 01307 Dresden, Germany;
bMax Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
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Lucas Farnung
dDepartment of Molecular Biology, Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany
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Patrick Cramer
dDepartment of Molecular Biology, Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany
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Vasily Zaburdaev
cMax Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany;
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Stephan W. Grill
aBiotechnology Center, Technical University Dresden, 01307 Dresden, Germany;
bMax Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
cMax Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany;
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  • For correspondence: stephan.grill@biotec.tu-dresden.de
  1. Edited by Steven M. Block, Stanford University, Stanford, CA, and approved September 27, 2016 (received for review March 16, 2016)

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Significance

Transcription is the first step toward protein production. During transcription, a polymerase enzyme moves along DNA and copies it to RNA. In the cell, DNA is highly compacted: roughly 150 bp of DNA is wrapped around histone proteins to form a nucleosome. However, little is known about how closely spaced nucleosomes impact polymerase transcription. We performed single-molecule optical tweezers transcription experiments on dinucleosomal DNA templates. We show that the effect of the second nucleosome on polymerase transcription efficiency through the first one depends on the internucleosomal spacing and the rotational arrangement of the nucleosomes on the helical DNA template. Our findings provide insights into how DNA compaction affects transcription in vitro.

Abstract

In eukaryotes, gene expression depends on chromatin organization. However, how chromatin affects the transcription dynamics of individual RNA polymerases has remained elusive. Here, we use dual trap optical tweezers to study single yeast RNA polymerase II (Pol II) molecules transcribing along a DNA template with two nucleosomes. The slowdown and the changes in pausing behavior within the nucleosomal region allow us to determine a drift coefficient, χ, which characterizes the ability of the enzyme to recover from a nucleosomal backtrack. Notably, χ can be used to predict the probability to pass the first nucleosome. Importantly, the presence of a second nucleosome changes χ in a manner that depends on the spacing between the two nucleosomes, as well as on their rotational arrangement on the helical DNA molecule. Our results indicate that the ability of Pol II to pass the first nucleosome is increased when the next nucleosome is turned away from the first one to face the opposite side of the DNA template. These findings help to rationalize how chromatin arrangement affects Pol II transcription dynamics.

  • Pol II
  • transcription
  • single-molecule
  • optical tweezers
  • internucleosomal distance

Footnotes

  • ↵1To whom correspondence should be addressed. Email: stephan.grill{at}biotec.tu-dresden.de.
  • Author contributions: V.F., P.C., V.Z., and S.W.G. designed research; V.F., J.S., and L.F. performed research; V.F., C.E., and L.F. contributed new reagents/analytic tools; V.F. and J.S. analyzed data; and V.F., J.S., P.C., V.Z., and S.W.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1602764113/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Nucleosomal arrangement affects RNA transcription
Veronika Fitz, Jaeoh Shin, Christoph Ehrlich, Lucas Farnung, Patrick Cramer, Vasily Zaburdaev, Stephan W. Grill
Proceedings of the National Academy of Sciences Nov 2016, 113 (45) 12733-12738; DOI: 10.1073/pnas.1602764113

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Nucleosomal arrangement affects RNA transcription
Veronika Fitz, Jaeoh Shin, Christoph Ehrlich, Lucas Farnung, Patrick Cramer, Vasily Zaburdaev, Stephan W. Grill
Proceedings of the National Academy of Sciences Nov 2016, 113 (45) 12733-12738; DOI: 10.1073/pnas.1602764113
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