Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment

O Alder; F Lavial; A Helness; E Brookes; S Pinho; A Chandrashekran; P Arnaud; A Pombo; Laura O'Neill; V Azuara

doi:10.1242/DEV.048363

Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment

O Alder, F Lavial, A Helness, E Brookes, S Pinho, A Chandrashekran, P Arnaud, A Pombo, Laura O'Neill, V Azuara

Immunology and Immunotherapy

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Abstract

Pluripotent cells develop within the inner cell mass of blastocysts, a mosaic of cells surrounded by an extra-embryonic layer, the trophectoderm. We show that a set of somatic lineage regulators (including Hox, Gata and Sox factors) that carry bivalent chromatin enriched in H3K27me3 and H3K4me2 are selectively targeted by Suv39h1-mediated H3K9me3 and de novo DNA methylation in extra-embryonic versus embryonic (pluripotent) lineages, as assessed both in blastocyst-derived stem cells and in vivo. This stably repressed state is linked with a loss of gene priming for transcription through the exclusion of PRC1 (Ring1B) and RNA polymerase II complexes at bivalent, lineage-inappropriate genes upon trophoblast lineage commitment. Collectively, our results suggest a mutually exclusive role for Ring1B and Suv39h1 in regulating distinct chromatin states at key developmental genes and propose a novel mechanism by which lineage specification can be reinforced during early development.

Original language	English
Pages (from-to)	2483-2492
Number of pages	10
Journal	Development (Cambridge)
Volume	137
Issue number	15
DOIs	https://doi.org/10.1242/DEV.048363
Publication status	Published - 1 Aug 2010

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title = "Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment",

abstract = "Pluripotent cells develop within the inner cell mass of blastocysts, a mosaic of cells surrounded by an extra-embryonic layer, the trophectoderm. We show that a set of somatic lineage regulators (including Hox, Gata and Sox factors) that carry bivalent chromatin enriched in H3K27me3 and H3K4me2 are selectively targeted by Suv39h1-mediated H3K9me3 and de novo DNA methylation in extra-embryonic versus embryonic (pluripotent) lineages, as assessed both in blastocyst-derived stem cells and in vivo. This stably repressed state is linked with a loss of gene priming for transcription through the exclusion of PRC1 (Ring1B) and RNA polymerase II complexes at bivalent, lineage-inappropriate genes upon trophoblast lineage commitment. Collectively, our results suggest a mutually exclusive role for Ring1B and Suv39h1 in regulating distinct chromatin states at key developmental genes and propose a novel mechanism by which lineage specification can be reinforced during early development.",

author = "O Alder and F Lavial and A Helness and E Brookes and S Pinho and A Chandrashekran and P Arnaud and A Pombo and Laura O'Neill and V Azuara",

year = "2010",

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doi = "10.1242/DEV.048363",

language = "English",

volume = "137",

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journal = "Development (Cambridge)",

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TY - JOUR

T1 - Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment

AU - Alder, O

AU - Lavial, F

AU - Helness, A

AU - Brookes, E

AU - Pinho, S

AU - Chandrashekran, A

AU - Arnaud, P

AU - Pombo, A

AU - O'Neill, Laura

AU - Azuara, V

PY - 2010/8/1

Y1 - 2010/8/1

N2 - Pluripotent cells develop within the inner cell mass of blastocysts, a mosaic of cells surrounded by an extra-embryonic layer, the trophectoderm. We show that a set of somatic lineage regulators (including Hox, Gata and Sox factors) that carry bivalent chromatin enriched in H3K27me3 and H3K4me2 are selectively targeted by Suv39h1-mediated H3K9me3 and de novo DNA methylation in extra-embryonic versus embryonic (pluripotent) lineages, as assessed both in blastocyst-derived stem cells and in vivo. This stably repressed state is linked with a loss of gene priming for transcription through the exclusion of PRC1 (Ring1B) and RNA polymerase II complexes at bivalent, lineage-inappropriate genes upon trophoblast lineage commitment. Collectively, our results suggest a mutually exclusive role for Ring1B and Suv39h1 in regulating distinct chromatin states at key developmental genes and propose a novel mechanism by which lineage specification can be reinforced during early development.

AB - Pluripotent cells develop within the inner cell mass of blastocysts, a mosaic of cells surrounded by an extra-embryonic layer, the trophectoderm. We show that a set of somatic lineage regulators (including Hox, Gata and Sox factors) that carry bivalent chromatin enriched in H3K27me3 and H3K4me2 are selectively targeted by Suv39h1-mediated H3K9me3 and de novo DNA methylation in extra-embryonic versus embryonic (pluripotent) lineages, as assessed both in blastocyst-derived stem cells and in vivo. This stably repressed state is linked with a loss of gene priming for transcription through the exclusion of PRC1 (Ring1B) and RNA polymerase II complexes at bivalent, lineage-inappropriate genes upon trophoblast lineage commitment. Collectively, our results suggest a mutually exclusive role for Ring1B and Suv39h1 in regulating distinct chromatin states at key developmental genes and propose a novel mechanism by which lineage specification can be reinforced during early development.

U2 - 10.1242/DEV.048363

DO - 10.1242/DEV.048363

M3 - Article

C2 - 20573702

SN - 1477-9129

VL - 137

SP - 2483

EP - 2492

JO - Development (Cambridge)

JF - Development (Cambridge)

IS - 15

ER -

Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment

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