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Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing

Proper chromosome alignment and segregation during mitosis depend on cohesion between sister chromatids. Cohesion is thought to occur through the entrapment of DNA within the tripartite ring (Smc1, Smc3 and Rad21) with enforcement from a fourth subunit (SA1/SA2). Surprisingly, cohesin rings do not p...

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Autores principales: Lin, Jiangguo, Countryman, Preston, Chen, Haijiang, Pan, Hai, Fan, Yanlin, Jiang, Yunyun, Kaur, Parminder, Miao, Wang, Gurgel, Gisele, You, Changjiang, Piehler, Jacob, Kad, Neil M., Riehn, Robert, Opresko, Patricia L., Smith, Susan, Tao, Yizhi Jane, Wang, Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5291270/
https://www.ncbi.nlm.nih.gov/pubmed/27298259
http://dx.doi.org/10.1093/nar/gkw518
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author Lin, Jiangguo
Countryman, Preston
Chen, Haijiang
Pan, Hai
Fan, Yanlin
Jiang, Yunyun
Kaur, Parminder
Miao, Wang
Gurgel, Gisele
You, Changjiang
Piehler, Jacob
Kad, Neil M.
Riehn, Robert
Opresko, Patricia L.
Smith, Susan
Tao, Yizhi Jane
Wang, Hong
author_facet Lin, Jiangguo
Countryman, Preston
Chen, Haijiang
Pan, Hai
Fan, Yanlin
Jiang, Yunyun
Kaur, Parminder
Miao, Wang
Gurgel, Gisele
You, Changjiang
Piehler, Jacob
Kad, Neil M.
Riehn, Robert
Opresko, Patricia L.
Smith, Susan
Tao, Yizhi Jane
Wang, Hong
author_sort Lin, Jiangguo
collection PubMed
description Proper chromosome alignment and segregation during mitosis depend on cohesion between sister chromatids. Cohesion is thought to occur through the entrapment of DNA within the tripartite ring (Smc1, Smc3 and Rad21) with enforcement from a fourth subunit (SA1/SA2). Surprisingly, cohesin rings do not play a major role in sister telomere cohesion. Instead, this role is replaced by SA1 and telomere binding proteins (TRF1 and TIN2). Neither the DNA binding property of SA1 nor this unique telomere cohesion mechanism is understood. Here, using single-molecule fluorescence imaging, we discover that SA1 displays two-state binding on DNA: searching by one-dimensional (1D) free diffusion versus recognition through subdiffusive sliding at telomeric regions. The AT-hook motif in SA1 plays dual roles in modulating non-specific DNA binding and subdiffusive dynamics over telomeric regions. TRF1 tethers SA1 within telomeric regions that SA1 transiently interacts with. SA1 and TRF1 together form longer DNA–DNA pairing tracts than with TRF1 alone, as revealed by atomic force microscopy imaging. These results suggest that at telomeres cohesion relies on the molecular interplay between TRF1 and SA1 to promote DNA–DNA pairing, while along chromosomal arms the core cohesin assembly might also depend on SA1 1D diffusion on DNA and sequence-specific DNA binding.
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spelling pubmed-52912702017-02-10 Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing Lin, Jiangguo Countryman, Preston Chen, Haijiang Pan, Hai Fan, Yanlin Jiang, Yunyun Kaur, Parminder Miao, Wang Gurgel, Gisele You, Changjiang Piehler, Jacob Kad, Neil M. Riehn, Robert Opresko, Patricia L. Smith, Susan Tao, Yizhi Jane Wang, Hong Nucleic Acids Res Nucleic Acid Enzymes Proper chromosome alignment and segregation during mitosis depend on cohesion between sister chromatids. Cohesion is thought to occur through the entrapment of DNA within the tripartite ring (Smc1, Smc3 and Rad21) with enforcement from a fourth subunit (SA1/SA2). Surprisingly, cohesin rings do not play a major role in sister telomere cohesion. Instead, this role is replaced by SA1 and telomere binding proteins (TRF1 and TIN2). Neither the DNA binding property of SA1 nor this unique telomere cohesion mechanism is understood. Here, using single-molecule fluorescence imaging, we discover that SA1 displays two-state binding on DNA: searching by one-dimensional (1D) free diffusion versus recognition through subdiffusive sliding at telomeric regions. The AT-hook motif in SA1 plays dual roles in modulating non-specific DNA binding and subdiffusive dynamics over telomeric regions. TRF1 tethers SA1 within telomeric regions that SA1 transiently interacts with. SA1 and TRF1 together form longer DNA–DNA pairing tracts than with TRF1 alone, as revealed by atomic force microscopy imaging. These results suggest that at telomeres cohesion relies on the molecular interplay between TRF1 and SA1 to promote DNA–DNA pairing, while along chromosomal arms the core cohesin assembly might also depend on SA1 1D diffusion on DNA and sequence-specific DNA binding. Oxford University Press 2016-07-27 2016-06-13 /pmc/articles/PMC5291270/ /pubmed/27298259 http://dx.doi.org/10.1093/nar/gkw518 Text en © The Author(s) 2016. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Nucleic Acid Enzymes
Lin, Jiangguo
Countryman, Preston
Chen, Haijiang
Pan, Hai
Fan, Yanlin
Jiang, Yunyun
Kaur, Parminder
Miao, Wang
Gurgel, Gisele
You, Changjiang
Piehler, Jacob
Kad, Neil M.
Riehn, Robert
Opresko, Patricia L.
Smith, Susan
Tao, Yizhi Jane
Wang, Hong
Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing
title Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing
title_full Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing
title_fullStr Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing
title_full_unstemmed Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing
title_short Functional interplay between SA1 and TRF1 in telomeric DNA binding and DNA–DNA pairing
title_sort functional interplay between sa1 and trf1 in telomeric dna binding and dna–dna pairing
topic Nucleic Acid Enzymes
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5291270/
https://www.ncbi.nlm.nih.gov/pubmed/27298259
http://dx.doi.org/10.1093/nar/gkw518
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