Polycomb complexes redundantly maintain epidermal stem cell identity during development

Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3. However, the functional contribution of each complex to...

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Published in	Genes & development Vol. 35; no. 5-6; pp. 354 - 366
Main Authors	Cohen, Idan, Bar, Carmit, Liu, Hequn, Valdes, Victor J., Zhao, Dejian, Galbo, Phillip M., Silva, Jose M., Koseki, Haruhiko, Zheng, Deyou, Ezhkova, Elena
Format	Journal Article
Language	English
Published	United States Cold Spring Harbor Laboratory Press 01.03.2021
Subjects	Animals Cell Differentiation - genetics Embryonic Stem Cells - cytology Embryonic Stem Cells - metabolism Epidermal Cells - cytology Epidermal Cells - metabolism Gene Expression Regulation, Developmental HEK293 Cells Humans Mice Polycomb Repressive Complex 1 - genetics Polycomb Repressive Complex 1 - metabolism Polycomb Repressive Complex 2 - genetics Polycomb Repressive Complex 2 - metabolism Polycomb-Group Proteins - genetics Polycomb-Group Proteins - metabolism Research Paper Transcription Factors - genetics Transcription Factors - metabolism PRC2 stem cell PRC1 H2AK119ub skin Polycomb epigenetics H3K27me3 epidermis
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Abstract	Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3. However, the functional contribution of each complex to gene repression has been a subject of debate, and understanding of its physiological significance requires further studies. Here, using the developing murine epidermis as a paradigm, we uncovered a previously unappreciated functional redundancy between Polycomb complexes. Coablation of PRC1 and PRC2 in embryonic epidermal progenitors resulted in severe defects in epidermal stratification, a phenotype not observed in the single PRC1-null or PRC2-null epidermis. Molecular dissection indicated a loss of epidermal identity that was coupled to a strong derepression of nonlineage transcription factors, otherwise repressed by either PRC1 or PRC2 in the absence of its counterpart. Ectopic expression of subsets of PRC1/2-repressed nonepidermal transcription factors in wild-type epidermal stem cells was sufficient to suppress epidermal identity genes, highlighting the importance of functional redundancy between PRC1 and PRC2. Altogether, our studies show how PRC1 and PRC2 function as two independent counterparts, thereby providing a repressive safety net that protects and preserves lineage identity.
AbstractList	Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3. However, the functional contribution of each complex to gene repression has been a subject of debate, and understanding of its physiological significance requires further studies. Here, using the developing murine epidermis as a paradigm, we uncovered a previously unappreciated functional redundancy between Polycomb complexes. Coablation of PRC1 and PRC2 in embryonic epidermal progenitors resulted in severe defects in epidermal stratification, a phenotype not observed in the single PRC1-null or PRC2-null epidermis. Molecular dissection indicated a loss of epidermal identity that was coupled to a strong derepression of nonlineage transcription factors, otherwise repressed by either PRC1 or PRC2 in the absence of its counterpart. Ectopic expression of subsets of PRC1/2-repressed nonepidermal transcription factors in wild-type epidermal stem cells was sufficient to suppress epidermal identity genes, highlighting the importance of functional redundancy between PRC1 and PRC2. Altogether, our studies show how PRC1 and PRC2 function as two independent counterparts, thereby providing a repressive safety net that protects and preserves lineage identity. In this study, Cohen et al. sought to understand the functional contribution of PRC1 and PRC2, which largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3, to gene repression. By using the developing murine epidermis as a paradigm, they uncovered a previously unappreciated functional redundancy between Polycomb complexes, and their findings show how PRC1 and PRC2 function as two independent counterparts, providing a repressive safety net that protects and preserves lineage identity. Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3. However, the functional contribution of each complex to gene repression has been a subject of debate, and understanding of its physiological significance requires further studies. Here, using the developing murine epidermis as a paradigm, we uncovered a previously unappreciated functional redundancy between Polycomb complexes. Coablation of PRC1 and PRC2 in embryonic epidermal progenitors resulted in severe defects in epidermal stratification, a phenotype not observed in the single PRC1-null or PRC2-null epidermis. Molecular dissection indicated a loss of epidermal identity that was coupled to a strong derepression of nonlineage transcription factors, otherwise repressed by either PRC1 or PRC2 in the absence of its counterpart. Ectopic expression of subsets of PRC1/2-repressed nonepidermal transcription factors in wild-type epidermal stem cells was sufficient to suppress epidermal identity genes, highlighting the importance of functional redundancy between PRC1 and PRC2. Altogether, our studies show how PRC1 and PRC2 function as two independent counterparts, thereby providing a repressive safety net that protects and preserves lineage identity. Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3. However, the functional contribution of each complex to gene repression has been a subject of debate, and understanding of its physiological significance requires further studies. Here, using the developing murine epidermis as a paradigm, we uncovered a previously unappreciated functional redundancy between Polycomb complexes. Coablation of PRC1 and PRC2 in embryonic epidermal progenitors resulted in severe defects in epidermal stratification, a phenotype not observed in the single PRC1-null or PRC2-null epidermis. Molecular dissection indicated a loss of epidermal identity that was coupled to a strong derepression of nonlineage transcription factors, otherwise repressed by either PRC1 or PRC2 in the absence of its counterpart. Ectopic expression of subsets of PRC1/2-repressed nonepidermal transcription factors in wild-type epidermal stem cells was sufficient to suppress epidermal identity genes, highlighting the importance of functional redundancy between PRC1 and PRC2. Altogether, our studies show how PRC1 and PRC2 function as two independent counterparts, thereby providing a repressive safety net that protects and preserves lineage identity.Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and cooperate to establish repressive chromatin domains demarcated by H2AK119ub and H3K27me3. However, the functional contribution of each complex to gene repression has been a subject of debate, and understanding of its physiological significance requires further studies. Here, using the developing murine epidermis as a paradigm, we uncovered a previously unappreciated functional redundancy between Polycomb complexes. Coablation of PRC1 and PRC2 in embryonic epidermal progenitors resulted in severe defects in epidermal stratification, a phenotype not observed in the single PRC1-null or PRC2-null epidermis. Molecular dissection indicated a loss of epidermal identity that was coupled to a strong derepression of nonlineage transcription factors, otherwise repressed by either PRC1 or PRC2 in the absence of its counterpart. Ectopic expression of subsets of PRC1/2-repressed nonepidermal transcription factors in wild-type epidermal stem cells was sufficient to suppress epidermal identity genes, highlighting the importance of functional redundancy between PRC1 and PRC2. Altogether, our studies show how PRC1 and PRC2 function as two independent counterparts, thereby providing a repressive safety net that protects and preserves lineage identity.
Author	Ezhkova, Elena Valdes, Victor J. Koseki, Haruhiko Bar, Carmit Galbo, Phillip M. Zheng, Deyou Liu, Hequn Silva, Jose M. Cohen, Idan Zhao, Dejian
AuthorAffiliation	1 The Shraga Segal Department of Microbiology, Immunology, and Genetics, Faculty of Health Science, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel 5 Yale Center for Genome Analysis, Yale University, New Haven, Connecticut 06510, USA 8 Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences (RIKEN-IMS), Tsurumi-ku, Yokohama 230-0045, Japan 3 Department of Genetics, Albert Einstein College of Medicine, Bronx, New York 10461, USA 2 Black Family Stem Cell Institute, Department of Cell, Developmental, and Regenerative Biology, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA 6 Department of Genetics, Yale School of Medicine, New Haven, Connecticut 06510, USA 11 Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461, USA 7 Department of Pathology, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA 10 Department of Neurology, Albert Einstein College of Medicine, Bronx, New York 10461,
AuthorAffiliation_xml	– name: 3 Department of Genetics, Albert Einstein College of Medicine, Bronx, New York 10461, USA – name: 7 Department of Pathology, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA – name: 8 Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences (RIKEN-IMS), Tsurumi-ku, Yokohama 230-0045, Japan – name: 10 Department of Neurology, Albert Einstein College of Medicine, Bronx, New York 10461, USA – name: 9 AMED-CREST, Tsurumi-ku, Yokohama 230-0045, Japan – name: 4 Department of Cell Biology and Development, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico – name: 5 Yale Center for Genome Analysis, Yale University, New Haven, Connecticut 06510, USA – name: 6 Department of Genetics, Yale School of Medicine, New Haven, Connecticut 06510, USA – name: 2 Black Family Stem Cell Institute, Department of Cell, Developmental, and Regenerative Biology, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA – name: 11 Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461, USA – name: 1 The Shraga Segal Department of Microbiology, Immunology, and Genetics, Faculty of Health Science, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
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Keywords	PRC2 stem cell PRC1 H2AK119ub skin Polycomb epigenetics H3K27me3 epidermis
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work. Present address: U1036, Institut National de la Santé et de la Recherche Médicale (INSERM), 38000 Grenoble, France.
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Snippet	Polycomb repressive complex 1 (PRC1) and PRC2 are critical epigenetic developmental regulators. PRC1 and PRC2 largely overlap in their genomic binding and... In this study, Cohen et al. sought to understand the functional contribution of PRC1 and PRC2, which largely overlap in their genomic binding and cooperate to...
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SubjectTerms	Animals Cell Differentiation - genetics Embryonic Stem Cells - cytology Embryonic Stem Cells - metabolism Epidermal Cells - cytology Epidermal Cells - metabolism Gene Expression Regulation, Developmental HEK293 Cells Humans Mice Polycomb Repressive Complex 1 - genetics Polycomb Repressive Complex 1 - metabolism Polycomb Repressive Complex 2 - genetics Polycomb Repressive Complex 2 - metabolism Polycomb-Group Proteins - genetics Polycomb-Group Proteins - metabolism Research Paper Transcription Factors - genetics Transcription Factors - metabolism
Title	Polycomb complexes redundantly maintain epidermal stem cell identity during development
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