Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development

ABSTRACT: The liver undergoes a slow process for lipid deposition during chick embryonic period. However, the underlying physiological and molecular mechanisms are still unclear. Therefore, the aim of the current study was to reveal the epigenetic mechanism of hepatic transcriptional reprogramming c...

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Main Authors: Xi Sun, Yumeng Wang, Chaohui Wang, Yibin Wang, Zhouzheng Ren, Xin Yang, Xiaojun Yang, Yanli Liu
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:Poultry Science
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S003257912300041X
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author Xi Sun
Yumeng Wang
Chaohui Wang
Yibin Wang
Zhouzheng Ren
Xin Yang
Xiaojun Yang
Yanli Liu
author_facet Xi Sun
Yumeng Wang
Chaohui Wang
Yibin Wang
Zhouzheng Ren
Xin Yang
Xiaojun Yang
Yanli Liu
author_sort Xi Sun
collection DOAJ
description ABSTRACT: The liver undergoes a slow process for lipid deposition during chick embryonic period. However, the underlying physiological and molecular mechanisms are still unclear. Therefore, the aim of the current study was to reveal the epigenetic mechanism of hepatic transcriptional reprogramming changes based on the integration analysis of RNA-seq and H3K27ac labeled CUT&Tag. Results showed that lipid contents increased gradually with the embryonic age (E) 11, E15, and E19 based on morphological analysis of Hematoxylin-eosin and Oil Red O staining as well as total triglyceride and cholesterol detection. The hepatic protein level of SREBP-1c was higher in E19 when compared with that in E11 and E15, while H3K27ac and H3K4me2 levels declined from E11 to E19. Differential expression genes (DEGs) among these 3 embryonic ages were determined by transcriptome analysis. A total of 107 and 46 genes were gradually upregulated and downregulated respectively with the embryonic age. Meanwhile, differential H3K27ac occupancy in chromatin was investigated. But the integration analysis of RNA-seq and CUT&Tag data showed that the overlap genes were less between DEGs and target genes of differential peaks in the promoter regions. Further, some KEGG pathways enriched from target genes of typical enhancer were overlapped with those from DEGs in transcriptome analysis such as insulin, FoxO, MAPK signaling pathways which were related to lipid metabolism. DNA motif analysis identify 8 and 10 transcription factors (TFs) based on up and down differential peaks individually among E11, E15, and E19 stages where 7 TFs were overlapped including COUP-TFII, FOXM1, FOXA1, HNF4A, RXR, ERRA, FOXA2. These results indicated that H3K27ac histone modification is involved in the transcriptional reprogramming regulation during embryonic development, which could recruit TFs binding to mediate differential enhancer activation. Differential activated enhancer impels dynamic transcriptional reprogramming towards lipid metabolism to promote the occurrence of special phenotype of hepatic lipid deposition.
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spelling doaj.art-7e2c18d674e3465aaa2aff94962065392023-04-02T06:10:51ZengElsevierPoultry Science0032-57912023-04-011024102516Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic developmentXi Sun0Yumeng Wang1Chaohui Wang2Yibin Wang3Zhouzheng Ren4Xin Yang5Xiaojun Yang6Yanli Liu7College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCorresponding author:; College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaABSTRACT: The liver undergoes a slow process for lipid deposition during chick embryonic period. However, the underlying physiological and molecular mechanisms are still unclear. Therefore, the aim of the current study was to reveal the epigenetic mechanism of hepatic transcriptional reprogramming changes based on the integration analysis of RNA-seq and H3K27ac labeled CUT&Tag. Results showed that lipid contents increased gradually with the embryonic age (E) 11, E15, and E19 based on morphological analysis of Hematoxylin-eosin and Oil Red O staining as well as total triglyceride and cholesterol detection. The hepatic protein level of SREBP-1c was higher in E19 when compared with that in E11 and E15, while H3K27ac and H3K4me2 levels declined from E11 to E19. Differential expression genes (DEGs) among these 3 embryonic ages were determined by transcriptome analysis. A total of 107 and 46 genes were gradually upregulated and downregulated respectively with the embryonic age. Meanwhile, differential H3K27ac occupancy in chromatin was investigated. But the integration analysis of RNA-seq and CUT&Tag data showed that the overlap genes were less between DEGs and target genes of differential peaks in the promoter regions. Further, some KEGG pathways enriched from target genes of typical enhancer were overlapped with those from DEGs in transcriptome analysis such as insulin, FoxO, MAPK signaling pathways which were related to lipid metabolism. DNA motif analysis identify 8 and 10 transcription factors (TFs) based on up and down differential peaks individually among E11, E15, and E19 stages where 7 TFs were overlapped including COUP-TFII, FOXM1, FOXA1, HNF4A, RXR, ERRA, FOXA2. These results indicated that H3K27ac histone modification is involved in the transcriptional reprogramming regulation during embryonic development, which could recruit TFs binding to mediate differential enhancer activation. Differential activated enhancer impels dynamic transcriptional reprogramming towards lipid metabolism to promote the occurrence of special phenotype of hepatic lipid deposition.http://www.sciencedirect.com/science/article/pii/S003257912300041Xchick embryohepatic transcriptometranscription factorsH3K27 acetylationenhancers
spellingShingle Xi Sun
Yumeng Wang
Chaohui Wang
Yibin Wang
Zhouzheng Ren
Xin Yang
Xiaojun Yang
Yanli Liu
Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
Poultry Science
chick embryo
hepatic transcriptome
transcription factors
H3K27 acetylation
enhancers
title Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
title_full Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
title_fullStr Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
title_full_unstemmed Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
title_short Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
title_sort genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development
topic chick embryo
hepatic transcriptome
transcription factors
H3K27 acetylation
enhancers
url http://www.sciencedirect.com/science/article/pii/S003257912300041X
work_keys_str_mv AT xisun genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT yumengwang genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT chaohuiwang genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT yibinwang genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT zhouzhengren genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT xinyang genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT xiaojunyang genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment
AT yanliliu genomeanalysisrevealshepatictranscriptionalreprogrammingchangesmediatedbyenhancersduringchickembryonicdevelopment