Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization

Summary: Differentiated cardiomyocytes (CMs) must undergo diverse morphological and functional changes during postnatal development. However, the mechanisms underlying initiation and coordination of these changes remain unclear. Here, we delineate an integrated, time-ordered transcriptional network...

Full description

Bibliographic Details
Main Authors: Chia-Yeh Lin, Yao-Ming Chang, Hsin-Yi Tseng, Yen-Ling Shih, Hsiao-Hui Yeh, You-Rou Liao, Han-Hsuan Tang, Chia-Ling Hsu, Chien-Chang Chen, Yu-Ting Yan, Cheng-Fu Kao
Format: Article
Language:English
Published: Elsevier 2023-11-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723014286
_version_ 1797448085700345856
author Chia-Yeh Lin
Yao-Ming Chang
Hsin-Yi Tseng
Yen-Ling Shih
Hsiao-Hui Yeh
You-Rou Liao
Han-Hsuan Tang
Chia-Ling Hsu
Chien-Chang Chen
Yu-Ting Yan
Cheng-Fu Kao
author_facet Chia-Yeh Lin
Yao-Ming Chang
Hsin-Yi Tseng
Yen-Ling Shih
Hsiao-Hui Yeh
You-Rou Liao
Han-Hsuan Tang
Chia-Ling Hsu
Chien-Chang Chen
Yu-Ting Yan
Cheng-Fu Kao
author_sort Chia-Yeh Lin
collection DOAJ
description Summary: Differentiated cardiomyocytes (CMs) must undergo diverse morphological and functional changes during postnatal development. However, the mechanisms underlying initiation and coordination of these changes remain unclear. Here, we delineate an integrated, time-ordered transcriptional network that begins with expression of genes for cell-cell connections and leads to a sequence of structural, cell-cycle, functional, and metabolic transitions in mouse postnatal hearts. Depletion of histone H2B ubiquitin ligase RNF20 disrupts this gene network and impairs CM polarization. Subsequently, assay for transposase-accessible chromatin using sequencing (ATAC-seq) analysis confirmed that RNF20 contributes to chromatin accessibility in this context. As such, RNF20 is likely to facilitate binding of transcription factors at the promoters of genes involved in cell-cell connections and actin organization, which are crucial for CM polarization and functional integration. These results suggest that CM polarization is one of the earliest events during postnatal heart development and provide insights into how RNF20 regulates CM polarity and the postnatal gene program.
first_indexed 2024-03-09T14:05:16Z
format Article
id doaj.art-e159d2452509443bb54e6e0e7ef957b1
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-03-09T14:05:16Z
publishDate 2023-11-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-e159d2452509443bb54e6e0e7ef957b12023-11-30T05:07:09ZengElsevierCell Reports2211-12472023-11-014211113416Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarizationChia-Yeh Lin0Yao-Ming Chang1Hsin-Yi Tseng2Yen-Ling Shih3Hsiao-Hui Yeh4You-Rou Liao5Han-Hsuan Tang6Chia-Ling Hsu7Chien-Chang Chen8Yu-Ting Yan9Cheng-Fu Kao10Institute of Cellular and Organismic Biology, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Biomedical Sciences, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Cellular and Organismic Biology, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Biomedical Sciences, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Biomedical Sciences, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Cellular and Organismic Biology, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Cellular and Organismic Biology, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Cellular and Organismic Biology, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Biomedical Sciences, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, TaiwanInstitute of Biomedical Sciences, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, Taiwan; Corresponding authorInstitute of Cellular and Organismic Biology, Academia Sinica, 128, Academia Road, Section 2, Nankang, Taipei, Taiwan; Corresponding authorSummary: Differentiated cardiomyocytes (CMs) must undergo diverse morphological and functional changes during postnatal development. However, the mechanisms underlying initiation and coordination of these changes remain unclear. Here, we delineate an integrated, time-ordered transcriptional network that begins with expression of genes for cell-cell connections and leads to a sequence of structural, cell-cycle, functional, and metabolic transitions in mouse postnatal hearts. Depletion of histone H2B ubiquitin ligase RNF20 disrupts this gene network and impairs CM polarization. Subsequently, assay for transposase-accessible chromatin using sequencing (ATAC-seq) analysis confirmed that RNF20 contributes to chromatin accessibility in this context. As such, RNF20 is likely to facilitate binding of transcription factors at the promoters of genes involved in cell-cell connections and actin organization, which are crucial for CM polarization and functional integration. These results suggest that CM polarization is one of the earliest events during postnatal heart development and provide insights into how RNF20 regulates CM polarity and the postnatal gene program.http://www.sciencedirect.com/science/article/pii/S2211124723014286CP: Molecular biologyCP: Developmental biology
spellingShingle Chia-Yeh Lin
Yao-Ming Chang
Hsin-Yi Tseng
Yen-Ling Shih
Hsiao-Hui Yeh
You-Rou Liao
Han-Hsuan Tang
Chia-Ling Hsu
Chien-Chang Chen
Yu-Ting Yan
Cheng-Fu Kao
Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
Cell Reports
CP: Molecular biology
CP: Developmental biology
title Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
title_full Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
title_fullStr Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
title_full_unstemmed Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
title_short Epigenetic regulator RNF20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
title_sort epigenetic regulator rnf20 underlies temporal hierarchy of gene expression to regulate postnatal cardiomyocyte polarization
topic CP: Molecular biology
CP: Developmental biology
url http://www.sciencedirect.com/science/article/pii/S2211124723014286
work_keys_str_mv AT chiayehlin epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT yaomingchang epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT hsinyitseng epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT yenlingshih epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT hsiaohuiyeh epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT yourouliao epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT hanhsuantang epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT chialinghsu epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT chienchangchen epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT yutingyan epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization
AT chengfukao epigeneticregulatorrnf20underliestemporalhierarchyofgeneexpressiontoregulatepostnatalcardiomyocytepolarization