Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency

Onkar Joshi; Shuang Yin Wang; Tatyana Kuznetsova; Yaser Atlasi; Tianran Peng; Pierre J. Fabre; Ehsan Habibi; Jani Shaik; Sadia Saeed; Lusy Handoko; Todd Richmond; Mikhail Spivakov; Daniel Burgess; Hendrik G. Stunnenberg

doi:10.1016/j.stem.2015.11.010

Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency

Onkar Joshi, Shuang Yin Wang, Tatyana Kuznetsova, Yaser Atlasi, Tianran Peng, Pierre J. Fabre, Ehsan Habibi, Jani Shaik, Sadia Saeed, Lusy Handoko, Todd Richmond, Mikhail Spivakov, Daniel Burgess, Hendrik G. Stunnenberg

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Abstract

Summary Serum-to-2i interconversion of mouse embryonic stem cells (mESCs) is a valuable in vitro model for early embryonic development. To assess whether 3D chromatin organization changes during this transition, we established Capture Hi-C with target-sequence enrichment of DNase I hypersensitive sites. We detected extremely long-range intra- and inter-chromosomal interactions between a small subset of H3K27me3 marked bivalent promoters involving the Hox clusters in serum-grown cells. Notably, these promoter-mediated interactions are not present in 2i ground-state pluripotent mESCs but appear upon their further development into primed-like serum mESCs. Reverting serum mESCs to ground-state 2i mESCs removes these promoter-promoter interactions in a spatiotemporal manner. H3K27me3, which is largely absent at bivalent promoters in ground-state 2i mESCs, is necessary, but not sufficient, to establish these interactions, as confirmed by Capture Hi-C on Eed^-/- serum mESCs. Our results implicate H3K27me3 and PRC2 as critical players in chromatin alteration during priming of ESCs for differentiation.

Original language	English
Pages (from-to)	748-757
Number of pages	10
Journal	Cell Stem Cell
Volume	17
Issue number	6
DOIs	https://doi.org/10.1016/j.stem.2015.11.010
Publication status	Published - 3 Dec 2015
Externally published	Yes

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Joshi, O., Wang, S. Y., Kuznetsova, T., Atlasi, Y., Peng, T., Fabre, P. J., Habibi, E., Shaik, J., Saeed, S., Handoko, L., Richmond, T., Spivakov, M., Burgess, D., & Stunnenberg, H. G. (2015). Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency. Cell Stem Cell, 17(6), 748-757. https://doi.org/10.1016/j.stem.2015.11.010

@article{98042c44182e459db9d745be94ffc912,

title = "Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency",

abstract = "Summary Serum-to-2i interconversion of mouse embryonic stem cells (mESCs) is a valuable in vitro model for early embryonic development. To assess whether 3D chromatin organization changes during this transition, we established Capture Hi-C with target-sequence enrichment of DNase I hypersensitive sites. We detected extremely long-range intra- and inter-chromosomal interactions between a small subset of H3K27me3 marked bivalent promoters involving the Hox clusters in serum-grown cells. Notably, these promoter-mediated interactions are not present in 2i ground-state pluripotent mESCs but appear upon their further development into primed-like serum mESCs. Reverting serum mESCs to ground-state 2i mESCs removes these promoter-promoter interactions in a spatiotemporal manner. H3K27me3, which is largely absent at bivalent promoters in ground-state 2i mESCs, is necessary, but not sufficient, to establish these interactions, as confirmed by Capture Hi-C on Eed-/- serum mESCs. Our results implicate H3K27me3 and PRC2 as critical players in chromatin alteration during priming of ESCs for differentiation.",

author = "Onkar Joshi and Wang, {Shuang Yin} and Tatyana Kuznetsova and Yaser Atlasi and Tianran Peng and Fabre, {Pierre J.} and Ehsan Habibi and Jani Shaik and Sadia Saeed and Lusy Handoko and Todd Richmond and Mikhail Spivakov and Daniel Burgess and Stunnenberg, {Hendrik G.}",

note = "Publisher Copyright: {\textcopyright} 2015 Elsevier Inc.",

year = "2015",

month = dec,

day = "3",

doi = "10.1016/j.stem.2015.11.010",

language = "English",

volume = "17",

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Joshi, O, Wang, SY, Kuznetsova, T, Atlasi, Y, Peng, T, Fabre, PJ, Habibi, E, Shaik, J, Saeed, S, Handoko, L, Richmond, T, Spivakov, M, Burgess, D & Stunnenberg, HG 2015, 'Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency', Cell Stem Cell, vol. 17, no. 6, pp. 748-757. https://doi.org/10.1016/j.stem.2015.11.010

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T1 - Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency

AU - Joshi, Onkar

AU - Wang, Shuang Yin

AU - Kuznetsova, Tatyana

AU - Atlasi, Yaser

AU - Peng, Tianran

AU - Fabre, Pierre J.

AU - Habibi, Ehsan

AU - Shaik, Jani

AU - Saeed, Sadia

AU - Handoko, Lusy

AU - Richmond, Todd

AU - Spivakov, Mikhail

AU - Burgess, Daniel

AU - Stunnenberg, Hendrik G.

PY - 2015/12/3

Y1 - 2015/12/3

N2 - Summary Serum-to-2i interconversion of mouse embryonic stem cells (mESCs) is a valuable in vitro model for early embryonic development. To assess whether 3D chromatin organization changes during this transition, we established Capture Hi-C with target-sequence enrichment of DNase I hypersensitive sites. We detected extremely long-range intra- and inter-chromosomal interactions between a small subset of H3K27me3 marked bivalent promoters involving the Hox clusters in serum-grown cells. Notably, these promoter-mediated interactions are not present in 2i ground-state pluripotent mESCs but appear upon their further development into primed-like serum mESCs. Reverting serum mESCs to ground-state 2i mESCs removes these promoter-promoter interactions in a spatiotemporal manner. H3K27me3, which is largely absent at bivalent promoters in ground-state 2i mESCs, is necessary, but not sufficient, to establish these interactions, as confirmed by Capture Hi-C on Eed-/- serum mESCs. Our results implicate H3K27me3 and PRC2 as critical players in chromatin alteration during priming of ESCs for differentiation.

AB - Summary Serum-to-2i interconversion of mouse embryonic stem cells (mESCs) is a valuable in vitro model for early embryonic development. To assess whether 3D chromatin organization changes during this transition, we established Capture Hi-C with target-sequence enrichment of DNase I hypersensitive sites. We detected extremely long-range intra- and inter-chromosomal interactions between a small subset of H3K27me3 marked bivalent promoters involving the Hox clusters in serum-grown cells. Notably, these promoter-mediated interactions are not present in 2i ground-state pluripotent mESCs but appear upon their further development into primed-like serum mESCs. Reverting serum mESCs to ground-state 2i mESCs removes these promoter-promoter interactions in a spatiotemporal manner. H3K27me3, which is largely absent at bivalent promoters in ground-state 2i mESCs, is necessary, but not sufficient, to establish these interactions, as confirmed by Capture Hi-C on Eed-/- serum mESCs. Our results implicate H3K27me3 and PRC2 as critical players in chromatin alteration during priming of ESCs for differentiation.

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DO - 10.1016/j.stem.2015.11.010

M3 - Article

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AN - SCOPUS:84952022547

SN - 1934-5909

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EP - 757

JO - Cell Stem Cell

JF - Cell Stem Cell

IS - 6

ER -

Dynamic Reorganization of Extremely Long-Range Promoter-Promoter Interactions between Two States of Pluripotency

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