MRNA Expression Profiles in Muscle-derived Extracellular Vesicles of Large White and Wild Boar Piglets Reveal Their Potential Roles in Immunity and Muscle Phenotype

Overview

Journal Front Vet Sci

Specialty Veterinary Medicine

Date 2024 Oct 18

PMID 39421829

Authors

Naixiang Yu

Xiaolong Chang

Jianchao Hu

Jianjun Li

Junwu Ma

Lusheng Huang

Affiliations

Soon will be listed here.

Abstract

Introduction: Extracellular vesicles (EVs) known for their pivotal role in intercellular communication through RNA delivery, hold paramount implications for understanding muscle phenotypic variations in diverse pig breeds.

Methods: In this study, we compared the mRNA expression profiles of muscles and muscle-derived extracellular vesicles (M-EVs), and also examined the diversity of enriched genes in M-EVs between weaned wild boars and commercial Large White pigs with respect to their numbers and biological functions.

Results: The results of the study showed that the variation in the expression profiles of mRNAs between muscles and M-EVs was much greater than the variability between the respective breeds. Meanwhile, the enrichment trend of low-expressed genes (ranked <1,000) was significantly (-value ≤ 0.05) powerful in M-EVs compared to highly expressed genes in muscles. In addition, M-EVs carried a smaller proportion of coding sequences and a larger proportion of untranslated region sequences compared to muscles. There were 2,110 genes enriched in M-EVs (MEGs) in Large White pigs and 2,322 MEGs in wild boars, with 1,490 MEGs shared interbreeds including (), which inhibits myogenic differentiation. Of the 89 KEGG pathways that were significantly enriched (-value ≤ 0.05) for these MEGs, 13 unique to Large White pigs were mainly related to immunity, 27 unique to wild boars were functionally diverse but included cell fate regulation such as the Notch signaling pathway and the TGF-beta signaling pathway, and 49 were common to both breeds were also functionally complex but partially related to innate immunity, such as the Complement and coagulation cascades and the Fc gamma R-mediated phagocytosis.

Discussion: These findings suggest that mRNAs in M-EVs have the potential to serve as indicators of muscle phenotype differences between the two pig breeds, highlighting the need for further exploration into the role of EV-RNAs in pig phenotype formation.

References

Perez-Boza J, Lion M, Struman I . Exploring the RNA landscape of endothelial exosomes. RNA. 2017; 24(3):423-435. PMC: 5824360. DOI: 10.1261/rna.064352.117. View

Wang L, Wang S, Li W . RSeQC: quality control of RNA-seq experiments. Bioinformatics. 2012; 28(16):2184-5. DOI: 10.1093/bioinformatics/bts356. View

Ozdemir S . Identification and comparison of exosomal microRNAs in the milk and colostrum of two different cow breeds. Gene. 2020; 743:144609. DOI: 10.1016/j.gene.2020.144609. View

Becker K, Ghule P, Lian J, Stein J, van Wijnen A, Stein G . Cyclin D2 and the CDK substrate p220(NPAT) are required for self-renewal of human embryonic stem cells. J Cell Physiol. 2009; 222(2):456-64. PMC: 3059841. DOI: 10.1002/jcp.21967. View

Love M, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. PMC: 4302049. DOI: 10.1186/s13059-014-0550-8. View

Rome S, Forterre A, Mizgier M, Bouzakri K . Skeletal Muscle-Released Extracellular Vesicles: State of the Art. Front Physiol. 2019; 10:929. PMC: 6695556. DOI: 10.3389/fphys.2019.00929. View

Qin B, Hu X, Su Z, Zeng X, Ma H, Xiong K . Tissue-derived extracellular vesicles: Research progress from isolation to application. Pathol Res Pract. 2021; 226:153604. DOI: 10.1016/j.prp.2021.153604. View

Chen Y, Chen Y, Shi C, Huang Z, Zhang Y, Li S . SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. Gigascience. 2017; 7(1):1-6. PMC: 5788068. DOI: 10.1093/gigascience/gix120. View

Argiles J, Campos N, Lopez-Pedrosa J, Rueda R, Rodriguez-Manas L . Skeletal Muscle Regulates Metabolism via Interorgan Crosstalk: Roles in Health and Disease. J Am Med Dir Assoc. 2016; 17(9):789-96. DOI: 10.1016/j.jamda.2016.04.019. View

10.

Vechetti Jr I, Peck B, Wen Y, Walton R, Valentino T, Alimov A . Mechanical overload-induced muscle-derived extracellular vesicles promote adipose tissue lipolysis. FASEB J. 2021; 35(6):e21644. PMC: 8607211. DOI: 10.1096/fj.202100242R. View

11.

Wu Z, Gong H, Zhang M, Tong X, Ai H, Xiao S . A worldwide map of swine short tandem repeats and their associations with evolutionary and environmental adaptations. Genet Sel Evol. 2021; 53(1):39. PMC: 8063339. DOI: 10.1186/s12711-021-00631-4. View

12.

Uhlen M, Fagerberg L, Hallstrom B, Lindskog C, Oksvold P, Mardinoglu A . Proteomics. Tissue-based map of the human proteome. Science. 2015; 347(6220):1260419. DOI: 10.1126/science.1260419. View

13.

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

14.

Xiong J, Zhang H, Zeng B, Liu J, Luo J, Chen T . An Exploration of Non-Coding RNAs in Extracellular Vesicles Delivered by Swine Anterior Pituitary. Front Genet. 2021; 12:772753. PMC: 8667663. DOI: 10.3389/fgene.2021.772753. View

15.

Jalabert A, Vial G, Guay C, Wiklander O, Nordin J, Aswad H . Exosome-like vesicles released from lipid-induced insulin-resistant muscles modulate gene expression and proliferation of beta recipient cells in mice. Diabetologia. 2016; 59(5):1049-58. DOI: 10.1007/s00125-016-3882-y. View

16.

Sun J, Wang L, Matthews R, Walcott G, Lu Y, Wei Y . CCND2 Modified mRNA Activates Cell Cycle of Cardiomyocytes in Hearts With Myocardial Infarction in Mice and Pigs. Circ Res. 2023; 133(6):484-504. PMC: 10529295. DOI: 10.1161/CIRCRESAHA.123.322929. View

17.

Batagov A, Kurochkin I . Exosomes secreted by human cells transport largely mRNA fragments that are enriched in the 3'-untranslated regions. Biol Direct. 2013; 8:12. PMC: 3732077. DOI: 10.1186/1745-6150-8-12. View

18.

Zhou B, Lin W, Long Y, Yang Y, Zhang H, Wu K . Notch signaling pathway: architecture, disease, and therapeutics. Signal Transduct Target Ther. 2022; 7(1):95. PMC: 8948217. DOI: 10.1038/s41392-022-00934-y. View

19.

Conway E . Complement-coagulation connections. Blood Coagul Fibrinolysis. 2018; 29(3):243-251. DOI: 10.1097/MBC.0000000000000720. View

20.

Wolf P . The nature and significance of platelet products in human plasma. Br J Haematol. 1967; 13(3):269-88. DOI: 10.1111/j.1365-2141.1967.tb08741.x. View