Whole-transcriptome analysis reveals the characteristics of intramuscular fat circRNA expression and its associated network in grazing yaks of different months of age under cold stress

Graphical abstract

Whole-transcriptome analysis reveals the characteristics of intramuscular fat circRNA expression and its associated network in grazing yaks of different months of age under cold stress
PDF
HTML

Keywords

bta-let-7i
ceRNA
circRNA
Cold stress
Gene expression
Intramuscular fat
Meat quality
miRNAs
Whole-transcriptome

How to Cite

1.
Liu Y, Sun Y, Han Y, Ding W, Jin S, Chen J, Gou F. Whole-transcriptome analysis reveals the characteristics of intramuscular fat circRNA expression and its associated network in grazing yaks of different months of age under cold stress. Electron. J. Biotechnol. [Internet]. 2025 Mar. 15 [cited 2026 Jan. 26];74:11-8. Available from: https://www.ejbiotechnology.info/index.php/ejbiotechnology/article/view/2425

Abstract

Background: The aim of this study was to screen circRNAs related to fat deposition in yaks, and to identify candidate circRNAs for yak meat quality improvement. Six male yaks with insignificant differences in body weights were selected as test subjects, and 3 yaks (G18_IMF) were randomly slaughtered at the beginning of the experiment, while the remaining 3 yaks were naturally grazed until 24 months of age (G24_IMF), and then slaughtered at the end of the experiment, and the intramuscular fat was collected from the dorsal muscle. At the end of the experiment, the yaks were slaughtered and the intramuscular fat from the back was collected for whole transcriptome sequencing.

Results: The results showed that 352 differential circRNAs, 86 differential miRNAs and 3981 differential mRNAs were found. miRNAs and mRNAs network regulation maps were successfully constructed through gene expression correlation analysis and target gene prediction.

Conclusions: Taking the intersection of the predicted circRNA target genes with the differential miRNAs for intramuscular fat in yaks of different months of age, we obtained two candidate ceRNA pairs that might be related to intramuscular fat deposition in yaks, and found that bta-let-7i might be related to fat deposition in yaks and might be regulated by X_85287959_85291068, and that X_85287959_85291068 could be a candidate circRNA to enhance the quality of yak meat. The results may provide a reference for further investigation of the regulatory network of intramuscular fat deposition in yak.

https://doi.org/10.1016/j.ejbt.2024.10.004
PDF
HTML

References

Wiener G, Han JL, Long RJ. The Yak 2nd edition. Regional Office for Asia and the Pacific Food and Agriculture Organization of the United Nations, Bangkok; 2003.

McCarthy SN, Henchion M, White A, et al. Evaluation of beef eating quality by Irish consumers. Meat Sci 2017;132:118-124. https://doi.org/10.1016/j.meatsci.2017.05.005 PMid: 28522169

Hunt MR, Legako JF, Dinh TT, et al. Assessment of volatile compounds, neutral and polar lipid fatty acids of four beef muscles from USDA Choice and Select graded carcasses and their relationships with consumer palatability scores and intramuscular fat content. Meat Sci 2016;116:91-101. https://doi.org/10.1016/j.meatsci.2016.02.010 PMid: 26874592

Piao MY, Baik M. Seasonal variation in carcass characteristics of Korean cattle steers. Asian-Australasian Journal of Animal Sciences 2015;28(3):442-50. https://doi.org/10.5713/ajas.14.0650 PMid: 25656196

Xiong L, Pei J, Chu M, et al. Fat deposition in the muscle of female and male yak and the correlation of yak meat quality with fat. Animals 2021;11(7):2142. https://doi.org/10.3390/ani11072142 PMid: 34359275

Luo J, Huang Z, Liu H, et al. Yak milk fat globules from the Qinghai-Tibetan Plateau: Membrane lipid composition and morphological properties. Food Chem 2018;245:731-737. https://doi.org/10.1016/j.foodchem.2017.12.001 PMid: 29287434

Khan R, Raza SHA, Junjvlieke Z, et al. RNA-seq reveal role of bovine TORC2 in the regulation of adipogenesis. Arch Biochem Biophys 2020;680:108236. https://doi.org/10.1016/j.abb.2019.108236 PMid: 31893525

Du J, Zhang P, Gan M, et al. MicroRNA-204-5p regulates 3T3-L1 preadipocyte proliferation, apoptosis and differentiation. Gene. 2018;668:1-7. https://doi.org/10.1016/j.gene.2018.05.036 PMid: 29775748

Barrett SP, Salzman J. Circular RNAs: analysis, expression and potential functions. Development 2016;143(11):1838-1847. https://doi.org/10.1242/dev.128074 PMid: 27246710

Huang A, Zheng H, Wu Z, et al. Circular RNA-protein interactions: functions, mechanisms, and identification. Theranostics 2020;10(8):3503-3517. https://doi.org/10.7150/thno.42174 PMid: 32206104 [11] Abe N, Hiroshima M, Maruyama H, et al. Rolling circle amplification in a prokaryotic translation system using small circular RNA. Angew Chem Int Ed 2013;52(27):7004-7008. https://doi.org/10.1002/anie.201302044 PMid: 23716491

Xu X, Zhang J, Tian Y, et al: CircRNA inhibits DNA damage repair by interacting with host gene. Mol Cancer. 2020;19(1):128.https://doi.org/10.1186/s12943-020-01246-x PMid: 32838810

Zang J, Lu D, Xu A. The interaction of circRNAs and RNA binding proteins: An important part of circRNA maintenance and function. J Neurosci Res. 2020;98(1):87-97. https://doi.org/10.1002/jnr.24356 PMid: 30575990

Zhou WY, Cai ZR, Liu J, et al. Circular RNA: metabolism, functions and interactions with proteins. Mol Cancer. 2020;19(1):172. https://doi.org/10.1186/s12943-020-01286-3 PMid: 33317550

Thomas LF, Sætrom P: Circular RNAs are depleted of polymorphisms at microRNA binding sites. Bioinformatics 2014;30(16):2243-2246. https://doi.org/10.1093/bioinformatics/btu257 PMid: 24764460

Chen G, Wang Q, Li Z, et al. Circular RNA CDR1as promotes adipogenic and suppresses osteogenic differentiation of BMSCs in steroid-induced osteonecrosis of the femoral head. Bone 2020;133:115258. https://doi.org/10.1016/j.bone.2020.115258 PMid: 32018039

Feng X, Zhao J, Li F, et al. Weighted gene co-expression network analysis revealed that CircMARK3 is a potential CircRNA affects fat deposition in buffalo. Frontiers in Veterinary Science 2022;9 946447. https://doi.org/10.3389/fvets.2022.946447 PMid: 35873681

Zhu Y, Gui W, Lin X, et al. Knock-down of circular RNA H19 induces human adipose-derived stem cells adipogenic differentiation via a mechanism involving the polypyrimidine tract-binding protein 1. Exp Cell Res 2020;387(2):111753. https://doi.org/10.1016/j.yexcr.2019.111753 PMid: 31837293

Li H, Yang J, Wei X, et al. CircFUT10 reduces proliferation and facilitates differentiation of myoblasts by sponging miR-133a. J Cell Physiol 2018;233(6):4643-4651. https://doi.org/10.1002/jcp.26230 PMid: 29044517

Jiang R, Li H, Yang J, et al: circRNA profiling reveals an abundant circFUT10 that promotes adipocyte proliferation and inhibits adipocyte differentiation via sponging let-7. Mol Ther Nucleic Acids 2020;20:491-501. https://doi.org/10.1016/j.omtn.2020.03.011 PMid: 32305019

Wang L, Liang W, Wang S, et al: Circular RNA expression profiling reveals that circ-PLXNA1 functions in duck adipocyte differentiation. PLoS One 2020;15(7):e0236069. https://doi.org/10.1371/journal.pone.0236069 PMid: 32692763

Li B, He Y, Wu W, et al. Circular RNA profiling identifies novel circPPARA that promotes intramuscular fat deposition in pigs. J Agric Food Chem 2022;70(13):4123-4137. https://doi.org/10.1021/acs.jafc.1c07358 PMid: 35324170

Liu X, Bai Y, Cui R, et al. Sus_circPAPPA2 regulates fat deposition in castrated pigs through the miR-2366/GK pathway. Biomolecules 2022;12(6):753. https://doi.org/10.3390/biom12060753 PMid: 35740877

Lagos-Quintana M, Rauhut R, Meyer J, et al. New microRNAs from mouse and human. RNA 2003;9(2):175-179. https://doi.org/10.1261/rna.2146903 PMid: 12554859

Johnson CD, Esquela-Kerscher A, Stefani G, et al: The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res 2007;67(16):7713-7722. https://doi.org/10.1158/0008-5472.CAN-07-1083 PMid: 17699775

Thum T, Galuppo P, Wolf C, et al. MicroRNAs in the human heart: A clue to fetal gene reprogramming in heart failure. Circulation 2007;116(3):258-267. https://doi.org/10.1161/CIRCULATIONAHA.107.687947 PMid: 17606841

Harfe BD, McManus MT, Mansfield JH, et al. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci USA 2005;102(31):10898-10903. https://doi.org/10.1073/pnas.0504834102 PMid: 16040801

Satoh M, Tabuchi T, Minami Y, et al. Expression of let-7i is associated with Toll-like receptor 4 signal in coronary artery disease: Effect of statins on let-7i and Toll-like receptor 4 signal. Immunobiology 2012;217(5):533-539. https://doi.org/10.1016/j.imbio.2011.08.005 PMid: 21899916

Jiang S. A regulator of metabolic reprogramming: MicroRNA Let-7. Transl Oncol 2019;12(7):1005-1013. https://doi.org/10.1016/j.tranon.2019.04.013 PMid: 31128429

Dai LL, Li SD, Ma YC, et al. MicroRNA-30b regulates insulin sensitivity by targeting SERCA2b in non-alcoholic fatty liver disease. Liver Int 2019;39(8):1504-1513. https://doi.org/10.1111/liv.14067 PMid: 30721562

Xue Y, Marvin ME, Ivanova IG, et al. Rif1 and Exo1 regulate the genomic instability following telomere losses. Aging Cell 2016;15(3):553-562. https://doi.org/10.1111/acel.12466 PMid: 27004475

Keijzers G, Liu D, Rasmussen LJ. Exonuclease 1 and its versatile roles in DNA repair. Crit Rev Biochem Mol Biol 2016;51(6):440-451. https://doi.org/10.1080/10409238.2016.1215407 PMid: 27494243

Kim JT, Cho HJ, Park SY, et al. DNA replication and sister chromatid cohesion 1 (DSCC1) of the replication factor complex CTF18-RFC is critical for colon cancer cell growth. J Cancer. 2019;10(24):6142-6153. https://doi.org/10.7150/jca.32339 PMid: 31762824

Boehm EM, Gildenberg MS, Washington MT. The Many Roles of PCNA in Eukaryotic DNA Replication. In: Kaguni LS, Oliveira MT editors, The Enzymes, Academic Press.,. 2016;39:231-254. https://doi.org/10.1016/bs.enz.2016.03.003 PMid: 27241932

Bermudez VP, Maniwa Y, Tappin I, et al. The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc Natl Acad Sci USA 2003;100(18):10237-10242. https://doi.org/10.1073/pnas.1434308100 PMid: 12930902

Chang S, Zhu Y, Xi Y, et al. High DSCC1 level predicts poor prognosis of lung adenocarcinoma. Int J Gen Med 2021;14:6961-6974. https://doi.org/10.2147/IJGM.S329482 PMid: 34707388

Jin G, Wang W, Cheng P, et al. DNA replication and sister chromatid cohesion 1 promotes breast carcinoma progression by modulating the Wnt/?-catenin signaling and p53 protein. J Biosci 2020;45:127. https://doi.org/10.1007/s12038-020-00100-y PMid: 33184243

Bartrons R, Simon-Molas H, Rodríguez-García A, et al. Fructose 2,6-bisphosphate in cancer cell metabolism. Front Oncol 2018;8:331. https://doi.org/10.3389/fonc.2018.00331 PMid: 30234009

De Bock K, Georgiadou M, Carmeliet P. Role of endothelial cell metabolism in vessel sprouting. Cell Metab 2013;18(5):634-647. https://doi.org/10.1016/j.cmet.2013.08.001 PMid: 23973331

Li FL, Liu JP, Bao RX, et al. Acetylation accumulates PFKFB3 in cytoplasm to promote glycolysis and protects cells from cisplatin-induced apoptosis. Nat Commun 2018;9(1):508. https://doi.org/10.1038/s41467-018-02950-5 PMid: 29410405

Yalcin A, Clem BF, Imbert-Fernandez Y, et al. 6-Phosphofructo-2-kinase (PFKFB3) promotes cell cycle progression and suppresses apoptosis via Cdk1-mediated phosphorylation of p27. Cell Death Dis. 2014;5(7):e1337. Published 2014 Jul 1r7. https://doi.org/10.1038/cddis.2014.292 PMid: 2503286

Creative Commons License

This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

Copyright (c) 2025 Electronic Journal of Biotechnology