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Comprehensive Analysis of LncRNA Reveals the Temporal-Specific Module of Goat Skeletal Muscle Development

ABSTRACT: A series of complex processes regulate muscle development, and lncRNAs play essential roles in the regulation of skeletal myogenesis. Using RNA sequencing, we profiled the lncRNA expression during goat (Capra hircus) skeletal muscle development, which included seven stages across fetal 45 (F45), 65 (F65), 90 (F90), 120 (F120), 135 (F135) days, born for 24 h (B1) and 90 (B90) days. A total of 15,079 lncRNAs were identified in the seven stages, and they were less conservative with other species (human, cow, and mouse). Among them, 547 were differentially expressed, and they divided the seven stages into three functional transition periods. Following weighted gene co-expression network analysis (WGCNA), five lncRNA modules specific for developmental stages were defined as three types: 'Early modules', 'late modules', and 'individual-stage-specific modules'. The enrichment content showed that 'early modules' were related to muscle structure formation, 'late modules' participated in the 'p53 signaling pathway' and other pathways, the F90-highly related module was involved in the 'MAPK signaling pathway', and other pathways. Furthermore, we identified hub-lncRNA in three types of modules, and LNC_011371, LNC_ 007561, and LNC_001728 may play important roles in goat skeletal muscle. These data will facilitate further exploration of skeletal muscle lncRNA functions at different developmental stages in goats.

SUBMITTER: Ling Y

PROVIDER: S-EPMC6719106 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Comprehensive Analysis of LncRNA Reveals the Temporal-Specific Module of Goat Skeletal Muscle Development

Ling Yinghui Y Zheng Qi Q Sui Menghua M Zhu Lu L Xu Lina L Zhang Yunhai Y Liu Ya Y Fang Fugui F Chu Mingxing M Ma Yuehui Y Zhang Xiaorong X

International journal of molecular sciences 20190814 16

A series of complex processes regulate muscle development, and lncRNAs play essential roles in the regulation of skeletal myogenesis. Using RNA sequencing, we profiled the lncRNA expression during goat (<i>Capra hircus</i>) skeletal muscle development, which included seven stages across fetal 45 (F45), 65 (F65), 90 (F90), 120 (F120), 135 (F135) days, born for 24 h (B1) and 90 (B90) days. A total of 15,079 lncRNAs were identified in the seven stages, and they were less conservative with other spe ...[more]

PMID: 31416143

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Project description:BACKGROUND:Circular RNA (circRNA) is produced during the splicing of mRNA (in addition to linear splicing) and is part of the gene regulatory network. The temporal expression patterns the different developmental stages were inseparable from these molecules' function. RESULTS:Skeletal muscles of Anhui white goat (AWG) across seven fetal to postnatal development stages were sequenced and 21 RNA sequencing libraries were constructed. We thereby identified 9090 circRNAs and analyzed their molecular properties, temporal expression patterns, and potential functions at the different stages. CircRNAs showed complexities and diversity of formation as the same host gene produces multiple isoforms of these nucleic acids with different expression profiles. The differential expression of 2881 circRNAs (DECs, P < 0.05) was identified and four were randomly selected and validated by qPCR. Moreover, 1118 DECs under strict selected (SDECs, |log2FC| > 2 and P-adj value < 0.01) showed 4 expression trends (Clusters 0, 19, 16 and 18). Cluster 0 molecules had increasing expression at all stages with effects on muscle through metabolism, regulation of enzyme activity, and biosynthesis. Cluster 16 circRNAs had high expression in the early and late stages and are involved in "Wnt signaling pathway", "AMPK signaling pathway" and others. Cluster 18 molecules were mainly expressed at F120 and participate in "cytoskeletal protein binding", "Notch signaling pathway" and so on. Cluster 19 circRNAs were down-regulated at all stages and related to muscle structure and development. Lastly, the SDECs divided the period of skeletal muscle development into three transitional stages: stage 1 (F45 to F90), which related to muscle satellite cell proliferation and muscle fiber structure; stage 2 (F90 to B1), in which the attachment of the cytoplasmic surface to the actin cytoskeleton initiates; and stage 3, which involved the "cGMP-PKG signaling pathway". Moreover, the paraffin sections messages also validated that there are three transitional stages of skeletal muscle development. CONCLUSION:Our current study provides a catalog of goat muscle-related circRNAs that can stratify skeletal muscle development fetus 45 days to newborn 90 days into three developmental stages. These findings better our understanding of functional transitions during mammalian muscle development.

Project description:BackgroundSkeletal muscle development is pivotal for animal growth and health. Recently, long noncoding RNAs (lncRNAs) were found to interact with chromatin through diverse roles. However, little is known about how lncRNAs act as chromatin-associated RNAs to regulate skeletal muscle development. Here, we aim to investigate the regulation of chromatin-associated RNA (MYH1G-AS) during skeletal muscle development.MethodsWe provided comprehensive insight into the RNA profile and chromatin accessibility of different myofibers, combining RNA sequencing (RNA-seq) with an assay for transposase-accessible chromatin with high-throughput sequencing (ATAC-seq). The dual-luciferase reporter assay and chromatin immunoprecipitation (ChIP) assay were used to analyze the transcriptional regulation mechanism of MYH1G-AS. ALKBH5-mediated MYH1G-AS N6-methyladenosine (m6A) demethylation was assessed by a single-base elongation and ligation-based qPCR amplification method (SELECT) assay. Functions of MYH1G-AS were investigated through a primary myoblast and lentivirus/cholesterol-modified antisense oligonucleotide (ASO)-mediated animal model. To validate the interaction of MYH1G-AS with fibroblast growth factor 18 (FGF18) protein, RNA pull down and an RNA immunoprecipitation (RIP) assay were performed. Specifically, the interaction between FGF18 and SWI/SNF-related matrix-associated actin-dependent regulator of chromatin subfamily A member 5 (SMARCA5) protein was analyzed by coimmunoprecipitation (Co-IP) and a yeast two-hybrid assay.ResultsA total of 45 differentially expressed (DE) lncRNAs, with DE ATAC-seq peaks in their promoter region, were classified as open chromatin-associated lncRNAs. A skeletal muscle-specific lncRNA (MSTRG.15576.9; MYH1G-AS), which is one of the open chromatin-associated lncRNA, was identified. MYH1G-AS transcription is coordinately regulated by transcription factors (TF) SMAD3 and SP2. Moreover, SP2 represses ALKBH5 transcription to weaken ALKBH5-mediated m6A demethylation of MYH1G-AS, thus destroying MYH1G-AS RNA stability. MYH1G-AS accelerates myoblast proliferation but restrains myoblast differentiation. Moreover, MYH1G-AS drives a switch from slow-twitch to fast-twitch fibers and causes muscle atrophy. Mechanistically, MYH1G-AS inhibits FGF18 protein stabilization to reduce the interaction of FGF18 to SMARCA5, thus repressing chromatin accessibility of the SMAD4 promoter to activate the SMAD4-dependent pathway.ConclusionsOur results reveal a new pattern of the regulation of lncRNA expression at diverse levels and help expound the regulation of m6A methylation on chromatin status.

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Comprehensive Analysis of LncRNA Reveals the Temporal-Specific Module of Goat Skeletal Muscle Development

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Comprehensive Analysis of LncRNA Reveals the Temporal-Specific Module of Goat Skeletal Muscle Development

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