The Integration of Genome-Wide DNA Methylation and Transcriptomics Identifies the Potential Genes That Regulate the Development of Skeletal Muscles in Ducks

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2023 Oct 28

PMID 37895154

Authors

Yinglin Lu

Jing Zhou

Fan Li

Heng Cao

Xingyu Zhang

Debing Yu

Zongliang He

Hongjie Ji

Kunpeng Lv

Guansuo Wu

Minli Yu

Affiliations

Soon will be listed here.

Abstract

DNA methylation is a pivotal epigenetic regulatory mechanism in the development of skeletal muscles. Nonetheless, the regulators responsible for DNA methylation in the development of embryonic duck skeletal muscles remain unknown. In the present study, whole genome bisulfite sequencing (WGBS) and transcriptome sequencing were conducted on the skeletal muscles of embryonic day 21 (E21) and day 28 (E28) ducks. The DNA methylation pattern was found to fall mainly within the cytosine-guanine (CG) context, with high methylation levels in the intron, exon, and promoter regions. Overall, 7902 differentially methylated regions (DMRs) were identified, which corresponded to 3174 differentially methylated genes (DMGs). By using integrative analysis of both WGBS with transcriptomics, we identified 1072 genes that are DMGs that are negatively associated with differentially expressed genes (DEGs). The gene ontology (GO) analysis revealed significant enrichment in phosphorylation, kinase activity, phosphotransferase activity, alcohol-based receptors, and binding to cytoskeletal proteins. The Kyoto Encyclopedia of Genes and Genomes (KEGGs) analysis showed significant enrichment in MAPK signaling, Wnt signaling, apelin signaling, insulin signaling, and FoxO signaling. The screening of enriched genes showed that hyper-methylation inhibited the expression of , , , , , , and , and hypo-methylation stimulated the expression of , , , , , and . Further predictions showed that the CpG islands in the promoters of , , , , and may play a crucial role in regulating the development of skeletal muscles. This study provides new insights into the epigenetic regulation of the development of duck skeletal muscles.

References

Li X, Liu L, Dong H, Yang J, Wang W, Zhang Q . Comparative genome-wide methylation analysis of longissimus dorsi muscles in Yorkshire and Wannanhua pigs. Anim Genet. 2020; 52(1):78-89. DOI: 10.1111/age.13029. View

Zhang X, Sun W, He L, Wang L, Qiu K, Yin J . Global DNA methylation pattern involved in the modulation of differentiation potential of adipogenic and myogenic precursors in skeletal muscle of pigs. Stem Cell Res Ther. 2020; 11(1):536. PMC: 7731745. DOI: 10.1186/s13287-020-02053-3. View

Liu Z, Han S, Shen X, Wang Y, Cui C, He H . The landscape of DNA methylation associated with the transcriptomic network in layers and broilers generates insight into embryonic muscle development in chicken. Int J Biol Sci. 2019; 15(7):1404-1418. PMC: 6643139. DOI: 10.7150/ijbs.35073. View

Zhang M, Li D, Zhai Y, Wang Z, Ma X, Zhang D . The Landscape of DNA Methylation Associated With the Transcriptomic Network of Intramuscular Adipocytes Generates Insight Into Intramuscular Fat Deposition in Chicken. Front Cell Dev Biol. 2020; 8:206. PMC: 7142253. DOI: 10.3389/fcell.2020.00206. View

Thomson D . The Role of AMPK in the Regulation of Skeletal Muscle Size, Hypertrophy, and Regeneration. Int J Mol Sci. 2018; 19(10). PMC: 6212977. DOI: 10.3390/ijms19103125. View

Davegardh C, Hall Wedin E, Broholm C, Henriksen T, Pedersen M, Pedersen B . Sex influences DNA methylation and gene expression in human skeletal muscle myoblasts and myotubes. Stem Cell Res Ther. 2019; 10(1):26. PMC: 6332625. DOI: 10.1186/s13287-018-1118-4. View

Kravic B, Huraskin D, Frick A, Jung J, Redai V, Palmisano R . LAP proteins are localized at the post-synaptic membrane of neuromuscular junctions and appear to modulate synaptic morphology and transmission. J Neurochem. 2016; 139(3):381-395. DOI: 10.1111/jnc.13710. View

Manoharan P, Song T, Radzyukevich T, Sadayappan S, Lingrel J, Heiny J . KLF2 in Myeloid Lineage Cells Regulates the Innate Immune Response during Skeletal Muscle Injury and Regeneration. iScience. 2019; 17:334-346. PMC: 6652133. DOI: 10.1016/j.isci.2019.07.009. View

Ehrlich K, Baribault C, Ehrlich M . Epigenetics of Muscle- and Brain-Specific Expression of KLHL Family Genes. Int J Mol Sci. 2020; 21(21). PMC: 7672584. DOI: 10.3390/ijms21218394. View

10.

Kahn B, Alquier T, Carling D, Grahame Hardie D . AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005; 1(1):15-25. DOI: 10.1016/j.cmet.2004.12.003. View

11.

Valdes-Hernandez J, Ramayo-Caldas Y, Passols M, Sebastia C, Criado-Mesas L, Crespo-Piazuelo D . Global analysis of the association between pig muscle fatty acid composition and gene expression using RNA-Seq. Sci Rep. 2023; 13(1):535. PMC: 9834388. DOI: 10.1038/s41598-022-27016-x. View

12.

Carrio E, Diez-Villanueva A, Lois S, Mallona I, Cases I, Forn M . Deconstruction of DNA methylation patterns during myogenesis reveals specific epigenetic events in the establishment of the skeletal muscle lineage. Stem Cells. 2015; 33(6):2025-36. DOI: 10.1002/stem.1998. View

13.

Li H, Zhu C, Tao Z, Xu W, Song W, Hu Y . MyoD and Myf6 gene expression patterns in skeletal muscle during embryonic and posthatch development in the domestic duck (Anas platyrhynchos domestica). J Anim Breed Genet. 2013; 131(3):194-201. DOI: 10.1111/jbg.12057. View

14.

Sun L, Bai M, Xiang L, Zhang G, Ma W, Jiang H . Comparative transcriptome profiling of longissimus muscle tissues from Qianhua Mutton Merino and Small Tail Han sheep. Sci Rep. 2016; 6:33586. PMC: 5028831. DOI: 10.1038/srep33586. View

15.

Ran J, Li J, Yin L, Zhang D, Yu C, Du H . Comparative Analysis of Skeletal Muscle DNA Methylation and Transcriptome of the Chicken Embryo at Different Developmental Stages. Front Physiol. 2021; 12:697121. PMC: 8283280. DOI: 10.3389/fphys.2021.697121. View

16.

Fan Y, Liang Y, Deng K, Zhang Z, Zhang G, Zhang Y . Analysis of DNA methylation profiles during sheep skeletal muscle development using whole-genome bisulfite sequencing. BMC Genomics. 2020; 21(1):327. PMC: 7191724. DOI: 10.1186/s12864-020-6751-5. View

17.

Ji G, Shu J, Zhang M, Ju X, Shan Y, Liu Y . Transcriptional regulatory region and DNA methylation analysis of gene promoters in Gaoyou duck skeletal muscle (). Br Poult Sci. 2019; 60(3):202-208. DOI: 10.1080/00071668.2019.1602250. View

18.

Pan Y, Chen L, Cheng J, Zhu X, Wu P, Bao L . Genome-wide DNA methylation profiles provide insight into epigenetic regulation of red and white muscle development in Chinese perch Siniperca chuatsi. Comp Biochem Physiol B Biochem Mol Biol. 2021; 256:110647. DOI: 10.1016/j.cbpb.2021.110647. View

19.

Zhang X, Li Y, Zhu C, Li F, Liu Z, Li X . DNA Demethylation of Myogenic Genes May Contribute to Embryonic Leg Muscle Development Differences between Wuzong and Shitou Geese. Int J Mol Sci. 2023; 24(8). PMC: 10138404. DOI: 10.3390/ijms24087188. View

20.

Zhang M, Yan F, Li F, Jiang K, Li D, Han R . Genome-wide DNA methylation profiles reveal novel candidate genes associated with meat quality at different age stages in hens. Sci Rep. 2017; 7:45564. PMC: 5381223. DOI: 10.1038/srep45564. View