Mammalian SWI/SNF collaborates with a polycomb-associated protein to regulate male germ line transcription in the mouse

A deficiency in BRG1, the catalytic subunit of the SWI/SNF chromatin remodeling complex, results in a meiotic arrest during spermatogenesis. Here, we explore the causative mechanisms. BRG1 is preferentially enriched at active promoters of genes essential for spermatogonial pluripotency and meiosis....

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Published inbioRxiv
Main Authors Menon, Debashish U, Shibata, Yoichiro, Mu, Weipeng, Magnuson, Terry
Format Paper
LanguageEnglish
Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 26.11.2018
Cold Spring Harbor Laboratory
Edition1.2
Subjects
Acetylation
BRG1 protein
Chromatin remodeling
Developmental Biology
Gene silencing
Histone H2A
Localization
Lysine
Meiosis
Pluripotency
Polycomb group proteins
Promoters
Sex chromosomes
Spermatocytes
Spermatogenesis
Transcription
Ubiquitin
Ubiquitin-protein ligase
Ubiquitination
SCML2
BRG1
transcriptional regulation
SWI/SNF chromatin remodeling
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Abstract A deficiency in BRG1, the catalytic subunit of the SWI/SNF chromatin remodeling complex, results in a meiotic arrest during spermatogenesis. Here, we explore the causative mechanisms. BRG1 is preferentially enriched at active promoters of genes essential for spermatogonial pluripotency and meiosis. In contrast, BRG1 is also associated with the repression of somatic genes. Chromatin accessibility at these target promoters is dependent upon BRG1. These results favor a model where BRG1 coordinates spermatogenic transcription to ensure meiotic progression. In spermatocytes, BRG1 interacts with SCML2, a testes-specific PRC1 factor that is associated with the repression of somatic genes. We present evidence to suggest that BRG1 and SCML2 concordantly regulate genes during meiosis. Furthermore, BRG1 is required for the proper localization of SCML2 and its associated deubiquitinase, USP7, to the sex chromosomes during pachynema. SCML2 associated, mono ubiquitination of histone H2A lysine 119 (H2AK119ub1) and acetylation of histone lysine 27 (H3K27ac) are elevated in Brg1cKO testes. Coincidentally, the PRC1 ubiquitin ligase, RNF2 is activated while a histone H2A/H2B deubiquitinase, USP3 is repressed. Thus, BRG1 impacts the male epigenome by influencing the localization and expression of epigenetic modifiers. This mechanism highlights a novel paradigm of co-operativity between SWI/SNF and PRC1.
AbstractList A deficiency in BRG1, the catalytic subunit of the SWI/SNF chromatin remodeling complex, results in a meiotic arrest during spermatogenesis. Here, we explore the causative mechanisms. BRG1 is preferentially enriched at active promoters of genes essential for spermatogonial pluripotency and meiosis. In contrast, BRG1 is also associated with the repression of somatic genes. Chromatin accessibility at these target promoters is dependent upon BRG1. These results favor a model where BRG1 coordinates spermatogenic transcription to ensure meiotic progression. In spermatocytes, BRG1 interacts with SCML2, a testes-specific PRC1 factor that is associated with the repression of somatic genes. We present evidence to suggest that BRG1 and SCML2 concordantly regulate genes during meiosis. Furthermore, BRG1 is required for the proper localization of SCML2 and its associated deubiquitinase, USP7, to the sex chromosomes during pachynema. SCML2 associated, mono ubiquitination of histone H2A lysine 119 (H2AK119ub1) and acetylation of histone lysine 27 (H3K27ac) are elevated in Brg1cKO testes. Coincidentally, the PRC1 ubiquitin ligase, RNF2 is activated while a histone H2A/H2B deubiquitinase, USP3 is repressed. Thus, BRG1 impacts the male epigenome by influencing the localization and expression of epigenetic modifiers. This mechanism highlights a novel paradigm of co-operativity between SWI/SNF and PRC1.
A deficiency in BRG1, the catalytic subunit of the SWI/SNF chromatin remodeling complex, results in a meiotic arrest during spermatogenesis. Here, we explore the causative mechanisms. BRG1 is preferentially enriched at active promoters of genes essential for spermatogonial pluripotency and meiosis. In contrast, BRG1 is also associated with the repression of somatic genes. Chromatin accessibility at these target promoters is dependent upon BRG1. These results favor a model where BRG1 coordinates spermatogenic transcription to ensure meiotic progression. In spermatocytes, BRG1 interacts with SCML2, a testes specific PRC1 factor that is associated with the repression of somatic genes. We present evidence to suggest that BRG1 and SCML2 concordantly regulate genes during meiosis. Furthermore, BRG1 is required for the proper localization of SCML2 and its associated deubiquitinase, USP7, to the sex chromosomes during pachynema. SCML2 associated, mono ubiquitination of histone H2A lysine 119 (H2AK119ub1) and acetylation of histone lysine 27 (H3K27ac) are elevated in Brg1cKO testes. Coincidentally, the PRC1 ubiquitin ligase, RNF2 is activated while a histone H2A/H2B deubiquitinase, USP3 is repressed. Thus, BRG1 impacts the male epigenome by influencing the localization and expression of epigenetic modifiers. This mechanism highlights a novel paradigm of co-operativity between SWI/SNF and PRC1. BRG1, a catalytic subunit of SWI/SNF chromatin remodeling complex, interacts with SCML2 (Sex comb on midleg-like 2), a polycomb repressive 1 (PRC1) factor, to regulate transcription during spermatogenesis. This represents a novel paradigm of SWI/SNF-PRC1 co-operation during gametogenesis.
Author Menon, Debashish U
Shibata, Yoichiro
Mu, Weipeng
Magnuson, Terry
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Keywords SCML2
BRG1
transcriptional regulation
SWI/SNF chromatin remodeling
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SecondaryResourceType preprint
Snippet A deficiency in BRG1, the catalytic subunit of the SWI/SNF chromatin remodeling complex, results in a meiotic arrest during spermatogenesis. Here, we explore...
SourceID biorxiv
proquest
SourceType Open Access Repository
Aggregation Database
SubjectTerms Acetylation
BRG1 protein
Chromatin remodeling
Developmental Biology
Gene silencing
Histone H2A
Localization
Lysine
Meiosis
Pluripotency
Polycomb group proteins
Promoters
Sex chromosomes
Spermatocytes
Spermatogenesis
Transcription
Ubiquitin
Ubiquitin-protein ligase
Ubiquitination
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Title Mammalian SWI/SNF collaborates with a polycomb-associated protein to regulate male germ line transcription in the mouse
URI https://www.proquest.com/docview/2137638730
https://www.biorxiv.org/content/10.1101/476143
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