CENP-C directs a structural transition of CENP-A nucleosomes mainly through sliding of DNA gyres

Samantha J. Falk; Jaehyoun Lee; Nikolina Sekulic; Michael A. Sennett; Tae Hee Lee; Ben E. Black

doi:10.1038/nsmb.3175

CENP-C directs a structural transition of CENP-A nucleosomes mainly through sliding of DNA gyres

Samantha J. Falk, Jaehyoun Lee, Nikolina Sekulic, Michael A. Sennett, Tae Hee Lee, Ben E. Black

Research output: Contribution to journal › Article › peer-review

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Abstract

The histone H3 variant CENP-A is incorporated into nucleosomes that mark centromere location. We have recently reported that CENP-A nucleosomes, compared with their H3 counterparts, confer an altered nucleosome shape. Here, using a single-molecule fluorescence resonance energy transfer (FRET) approach with recombinant human histones and centromere DNA, we found that the nucleosome shape change directed by CENP-A is dominated by lateral passing of two DNA gyres (gyre sliding). A nonhistone centromere protein, CENP-C, binds and reshapes the nucleosome, sliding the DNA gyres back to positions similar to those in canonical nucleosomes containing conventional histone H3. The model that we generated to explain the CENP-A-nucleosome transition provides an example of a shape change imposed by external binding proteins and has notable implications for understanding of the epigenetic basis of the faithful inheritance of centromere location on chromosomes.

Original language	English (US)
Pages (from-to)	204-208
Number of pages	5
Journal	Nature Structural and Molecular Biology
Volume	23
Issue number	3
DOIs	https://doi.org/10.1038/nsmb.3175
State	Published - Mar 1 2016

All Science Journal Classification (ASJC) codes

Structural Biology
Molecular Biology

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10.1038/nsmb.3175

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title = "CENP-C directs a structural transition of CENP-A nucleosomes mainly through sliding of DNA gyres",

abstract = "The histone H3 variant CENP-A is incorporated into nucleosomes that mark centromere location. We have recently reported that CENP-A nucleosomes, compared with their H3 counterparts, confer an altered nucleosome shape. Here, using a single-molecule fluorescence resonance energy transfer (FRET) approach with recombinant human histones and centromere DNA, we found that the nucleosome shape change directed by CENP-A is dominated by lateral passing of two DNA gyres (gyre sliding). A nonhistone centromere protein, CENP-C, binds and reshapes the nucleosome, sliding the DNA gyres back to positions similar to those in canonical nucleosomes containing conventional histone H3. The model that we generated to explain the CENP-A-nucleosome transition provides an example of a shape change imposed by external binding proteins and has notable implications for understanding of the epigenetic basis of the faithful inheritance of centromere location on chromosomes.",

author = "Falk, {Samantha J.} and Jaehyoun Lee and Nikolina Sekulic and Sennett, {Michael A.} and Lee, {Tae Hee} and Black, {Ben E.}",

note = "Funding Information: We thank K. Gupta (University of Pennsylvania) for advice on modeling, C. Davey (Nanyang Technical University) and U. Surana (Agency for Science, Technology and Research, Singapore) for advice on ENA experiments and D. Cleveland (University of California, San Diego), K. Luger (University of Colorado) and A. Straight (Stanford University) for plasmids. This work was supported by US National Institutes of Health grants GM082989 (B.E.B.) and GM097286 (T.-H.L.), and a postdoctoral fellowship from the American Cancer Society (N.S.). We acknowledge support from a University of Pennsylvania Genetics Training Grant (US National Institutes of Health grant GM008216 supporting S.J.F.). Publisher Copyright: {\textcopyright} 2016 Nature America, Inc.",

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CENP-C directs a structural transition of CENP-A nucleosomes mainly through sliding of DNA gyres

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