Regulation of the Mammalian SWI/SNF Family of Chromatin Remodeling Enzymes by Phosphorylation during Myogenesis

Padilla‐Benavides, Teresita; Reyes-Gutierrez, Pablo

doi:10.3390/biology9070152

Cited by 6 publications

(11 citation statements)

References 192 publications

(279 reference statements)

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“…The myoblast dataset was obtained using the OMNI-ATAC method on four biological replicates of myoblasts in growth phase (referred to as "Grow", in figures) and three biological replicates of cells after 24 hours in differentiation medium (called "Diff" in figures). At this stage, the myoblasts have exited the cell cycle and initiated the expression of muscle differentiation and function genes like Myogenin, various myosin and troponin isoforms (27)(28)(29) and this is known to coincide with chromatin remodeling and changes in DNA accessibility (30)(31)(32). The OMNI-ATAC method was selected for its ability to reduce mitochondrial DNA reads.…”

Section: Resultsmentioning

confidence: 99%

Improved sensitivity and resolution of ATAC-seq differential DNA accessibility analysis

Sheikh

Blais

2022

Preprint

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Eukaryotic genomes are packaged into chromatin, and the extent of its compaction must be modulated to allow several biological processes such as gene transcription. The regulatory elements of expressed genes are typically in relatively accessible chromatin, and several studies have revealed a reliable correlation between the abundance of mRNA transcripts and the degree of DNA accessibility at the regulatory elements of their coding genes. In consequence, the genome-wide profiling of DNA accessibility by methods such as ATAC-seq can help in the study of gene regulatory networks by serving as a proxy for gene expression and by helping identify important gene cis-regulatory elements and the trans-acting factors that bind them. The predominant approach used to identify differentially accessible genomic loci from ATAC-seq data obtained in two conditions of interest is comparable to that employed in RNA-seq gene expression profiling studies: accessible regions are identified through peak calling and treated like "genes", then sequenced DNA fragments (originating from two neighboring transposase integration events) that overlap them are counted and subjected to abundance modeling, which then allows to identify those that have a significant difference between the two conditions. We reasoned that this approach could be improved in terms of sensitivity and resolution by introducing two changes: bypassing peak calling, using instead a genome-wide sliding window quantification approach, and counting transposase integration sites, instead of fragments originating from two neighboring integration sites. We present the development of this approach, which we term "widaR", for Window- and Insertion-based Differential Accessibility in R, using a murine skeletal myoblast differentiation dataset. Reproducible R code is provided.

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Section: Resultsmentioning

confidence: 99%

Improved sensitivity and resolution of ATAC-seq differential DNA accessibility analysis

Sheikh

Blais

2022

Preprint

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“…The mSWI/SNF subunits are phosphoproteins (79)(80)(81)(82). To date, p38, AKT, CK2, and PKCb have been identified as kinases involved in mSWI/SNF subunit phosphorylation and function in myoblast proliferation or differentiation, and calcineurin has been identified as a critical phosphatase that counteracts PKCb and facilitates the activation of the Brg1 ATPase for chromatin remodeling and myogenic gene induction (15,(24)(25)(26)(27)(28)83). We add Pkm1 and Pkm2 to the list of signaling molecules that can regulate the mSWI/SNF chromatin remodeling enzymes, further increasing the complexity of mSWI/SNF protein modifications.…”

Section: Discussionmentioning

confidence: 99%

“…Integration of the mechanisms by which this multitude of factors cooperates to regulate myoblast proliferation and the onset and the execution of the myoblast differentiation program is complicated by the impact of developmentally relevant signaling molecules and their effector molecules. These effector molecules, including protein kinases and phosphatases, usually have multiple substrates, making a comprehensive understanding of the myoblast to myotube transition difficult (14)(15)(16).…”

Section: Introductionmentioning

confidence: 99%

“…These enzymes alter local myogenic gene chromatin structure to facilitate the assembly of active transcription complexes that initiate or up-regulate the expression of differentiation-specific genes (11,23,24). In addition to working within the context of activities by multiple histone modifying enzymes, the mSWI/SNF enzymes themselves are regulated by signaling pathways that involve modification by p38, PKC and calcineurin, and CK2, amongst others (15,(24)(25)(26)(27)(28).…”

Section: Introductionmentioning

confidence: 99%

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Muscle-Specific Pyruvate Kinase Isoforms, Pkm1 and Pkm2, Regulate Mammalian SWI/SNF Proteins and Histone 3 Phosphorylation During Myoblast Differentiation

Olea-Flores,

Sharma,

Verdejo-Torres

et al. 2024

Preprint

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Pyruvate kinase is a glycolytic enzyme that converts phosphoenolpyruvate and ADP into pyruvate and ATP. There are two genes that encode pyruvate kinase in vertebrates; Pkm and Pkl encode muscle- and liver/erythrocyte-specific forms, respectively. Each gene encodes two isoenzymes due to alternative splicing. Both muscle-specific enzymes, Pkm1 and Pkm2, function in glycolysis, but Pkm2 also has been implicated in gene regulation due to its ability to phosphorylate histone 3 threonine 11 (H3T11) in cancer cells. Here, we examined the roles of Pkm1 and Pkm2 during myoblast differentiation. RNA-seq analysis revealed that Pkm2 promotes the expression of Dpf2/Baf45d and Baf250a/Arid1A. Dpf2 and Baf250a are subunits that identify a specific sub-family of the mammalian SWI/SNF (mSWI/SNF) of chromatin remodeling enzymes that is required for activation of myogenic gene expression during differentiation. Pkm2 also mediated the incorporation of Dpf2 and Baf250a into the regulatory sequences controlling myogenic gene expression. Pkm1 did not affect expression but was required for nuclear localization of Dpf2. Additionally, Pkm2 was required not only for the incorporation of phosphorylated H3T11 in myogenic promoters, but also for the incorporation of phosphorylated H3T6 and H3T45 at myogenic promoters via regulation of AKT and protein kinase C isoforms that phosphorylate those amino acids. Our results identify multiple unique roles for Pkm2 and a novel function for Pkm1 in gene expression and chromatin regulation during myoblast differentiation.

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“…The SWI/SNF is a complex that shares in chromatin remodeling, playing a role in controlling DNA availability for different cellular processes, such as DNA transcription and repair. Moreover, it is involved in the regulation of different pathways including the sucrose fermentation pathway (8) . Such roles take place by the actions of different protein subunits of this complex, including SMARCB1 (SWI/SNF-related matrix-associated actin dependent regulator of chromatin subfamily B member 1).…”

Section: Introductionmentioning

confidence: 99%

SMARCB1 as a potential indicator of the prognosis of oral squamous cell carcinoma

Fathi

Shebl

2023

Egyptian Dental Journal

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Background: Being the most common intraoral malignancy, studying of possible prognostic markers for squamous cell carcinoma (SCC) is of great benefit that can alter treatment and followup protocols proposed for different grades of the lesion. As a newly identified tumor suppressor gene, SMARCB1 protein level in different histological grades of SCC can be used as a predictor of prognosis. Similarly, levels of CD3 positive tumor infiltrating lymphocytes (TILs) in SCC can be used to distinguish tumor grades. Aim:To assess the levels of SMARCB1 gene expression by immunohistochemical analysis of the gene protein and to evaluate the level of CD3 in different grades of SCC, and to correlate between their expression and tumor prognosis based on the histological grade.Material & methods: Thirty three formalin fixed paraffin-embedded archival blocks of oral squamous cell carcinoma (OSCC) were used in this study; eleven cases from each group were tested (group 1 well-differentiated, group 2 moderately-differentiated and group 3 poorly-differentiated). Immunohistochemical study was performed on the specimens to evaluate the expression of the protein of SMARCB1 gene and CD3 positive tumor infiltrating lymphocytes (TILs). The area fraction of both genes' expression was calculated. The data was analyzed and expressed statistically.Results: Group1 showed high CD3 gene expression and low SMARCB1 gene expression. Group2 to showed almost similar gene expression results as group 1. Group3 showed marked decrease in CD3 gene expression and high SMARCB1 gene expression. Conclusion:Our findings revealed that high expression values of the protein of SMARCB1 gene may be used as an evidence for poor prognosis while presence of high numbers of CD3+ T cells is associated with good prognosis and increased survival in oral squamous cell carcinoma.

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Regulation of the Mammalian SWI/SNF Family of Chromatin Remodeling Enzymes by Phosphorylation during Myogenesis

Cited by 6 publications

References 192 publications

Improved sensitivity and resolution of ATAC-seq differential DNA accessibility analysis

Improved sensitivity and resolution of ATAC-seq differential DNA accessibility analysis

Muscle-Specific Pyruvate Kinase Isoforms, Pkm1 and Pkm2, Regulate Mammalian SWI/SNF Proteins and Histone 3 Phosphorylation During Myoblast Differentiation

SMARCB1 as a potential indicator of the prognosis of oral squamous cell carcinoma

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