Abstract
Circular RNAs (circRNAs) are a class of non-coding RNA that play crucial roles in the growth and development of skeletal muscle. However, little is known about the role of circRNAs in caprine skeletal muscle. In this study, the size of muscle fiber and the expression profiles of circRNAs were compared in Longissimus dorsi muscle of Liaoning cashmere (LC) goats and Ziwuling black (ZB) goats with significant phenotypic differences in meat production performance, using hematoxylin and eosin staining and RNA-Seq, respectively. The size of muscle fiber in LC goats was larger than those in ZB goats (P < 0.05). A total of 10,875 circRNAs were identified and 214 of these were differentially expressed between the two caprine breeds. The parent genes of differentially expressed circRNAs were mainly enriched in connective tissue development, Rap1, cGMP-PKG, cAMP and Ras signaling pathway. In conclusion, circRNAs may play important roles in skeletal mass, meat production performance and meat quality traits in goats. The results provide an improved understanding of the functions of circRNAs in skeletal muscle development of goats.
Similar content being viewed by others
Abbreviations
- circRNAs:
-
Circular RNAs
- miRNA:
-
MicroRNA
- LC:
-
Liaoning cashmere
- ZB:
-
Ziwuling black
- RT-PCR:
-
Reverse transcriptase-polymerase chain reaction
- STAT1:
-
Signal transducerand activator of transcription 1
- MYH4:
-
Myosin-4
- LMO7:
-
LIM domain 7
- GO:
-
Gene Ontology
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
References
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S (2014) CircRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56:55–66. https://doi.org/10.1016/j.molcel.2014.08.019
Bar DZ, Charar C, Gruenbaum Y (2018) Small GTPases in C. elegans metabolism. Small GTPases 9:415–419. https://doi.org/10.1080/21541248.2016.1247940
Begue G, Douillard A, Galbes O, Rossano B, Vernus B, Candau R, Py G (2013) Early activation of rat skeletal muscle IL-6/STAT1/STAT3 dependent gene expression in resistance exercise linked to hypertrophy. PLoS ONE 8:e57141. https://doi.org/10.1371/journal.pone.0057141
Bélanger G, Stocksley MA, Vromme M, Schaeffer L, Furic L, Desgroseillers L, Jasmin BJ (2003) Localization of the RNA-binding proteins Staufen1 and Staufen2 at the mammalian neuromuscular junction. J Neurochem 86:669–677. https://doi.org/10.1046/j.1471-4159.2003.01883.x
Berdeaux R, Stewart R (2012) CAMP signaling in skeletal muscle adaptation: hypertrophy, metabolism, and regeneration. Am J Physiol Endocrinol Metab 303:1–17. https://doi.org/10.1152/ajpendo.00555.2011
Bu D, Luo H, Huo P, Wang Z, Zhang S, He Z, Wu Y, Zhao L, Liu J, Guo J, Fang S, Cao W, Yi L, Zhao Y, Kong L (2021) KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res 49:W317–W325. https://doi.org/10.1093/nar/gkab447
Cai R, Zhang Q, Wang Y, Yong W, Pang W (2021) Lnc-ORA interacts with microRNA-532-3p and IGF2BP2 to inhibit skeletal muscle myogenesis. J Biol Chem 296:100376. https://doi.org/10.1016/j.jbc.2021.100376
Cao T, Shi L, Zhang L, Zhou H, Xun W, Hou G (2014) Comparative study on fetal muscle fiber of Wuzhishan pig and Changbai pig during 65d gestation. J Anim Ecol 35:37–40
Cao H, Liu J, Du T, Liu Y, Zhang X, Guo Y, Wang J, Zhou X, Li X, Yang G, Shi X (2022) Circular RNA screening identifies circMYLK4 as a regulator of fast/slow myofibers in porcine skeletal muscles. Mol Genet Genom 297:87–99. https://doi.org/10.1007/s00438-021-01835-5
Cassano M, Biressi S, Finan A, Benedetti L, Omes C, Boratto R, Martin F, Allegretti M, Broccoli V, Cusella De Angelis G, Comoglio PM, Basilico C, Torrente Y, Michieli P, Cossu G, Sampaolesi M (2008) Magic-factor 1, a partial agonist of Met, induces muscle hypertrophy by protecting myogenic progenitors from apoptosis. PLoS ONE 3(9):e3223. https://doi.org/10.1371/journal.pone.0003223
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chen B, Yu J, Guo L, Byers M, Wang Z, Chen X, Xu H, Nie Q (2019) Circular RNA circhipk3 promotes the proliferation and differentiation of chicken myoblast cells by sponging miR-30a-3p. Cells 8:177. https://doi.org/10.3390/cells8020177
Cheng X, Li L, Shi G, Chen L, Li C (2020) MEG3 promotes differentiation of porcine satellite cells by sponging miR-423-5p to relieve inhibiting effect on SRF. Cells 9:449. https://doi.org/10.3390/cells9020449
Choi YM, Oh HK (2016) Carcass performance, muscle fiber, meat quality, and sensory quality characteristics of crossbred pigs with different live weights. Korean J Food Sci An 36:389–396. https://doi.org/10.5851/kosfa.2016.36.3.389
Connolly M, Paul R, Farre-Garros R, Natanek SA, Bloch S, Lee J, Lorenzo JP, Patel H, Cooper C, Sayer AA, Wort SJ, Griffiths M, Polkey MI, Kemp PR (2018) miR-424-5p reduces ribosomal RNA and protein synthesis in muscle wasting. J Cachexia Sarcopeni 9:400–416. https://doi.org/10.1002/jcsm.12266
De Rubeis S, Pasciuto E, Li KW, Fernández E, Di Marino D, Buzzi A, Ostroff LE, Klann E, Zwartkruis FJ, Komiyama NH, Grant SG, Poujol C, Choquet D, Achsel T, Posthuma D, Smit AB, Bagni C (2013) CYFIP1 coordinates mRNA translation and cytoskeleton remodeling to ensure proper dendritic spine formation. Neuron 79:1169–1182. https://doi.org/10.1016/j.neuron.2013.06.039
Dedeic Z, Cetera M, Cohen TV, Holaska JM (2011) Emerin inhibits Lmo7 binding to the Pax3 and MyoD promoters and expression of myoblast proliferation genes. J Cell Sci 124:1691–1702. https://doi.org/10.1242/jcs.080259
Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 4:P3
Ding L, Zhang L, Biswas S, Schugar RC, Brown JM, Byzova T, Podrez E (2017) Akt3 inhibits adipogenesis and protects from diet-induced obesity via WNK1/SGK1 signaling. JCI Insight 2:e95687. https://doi.org/10.1172/jci.insight.95687
Fadia H, Adams GR (2004) Inhibition of MAP/ERK kinase prevents IGF-I-induced hypertrophy in rat muscles. J Appl Physiol 96:203. https://doi.org/10.1152/japplphysiol.00856
Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell B 37:1974–1984. https://doi.org/10.1016/j.biocel.2005.04.018
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388. https://doi.org/10.1038/nature11993
Hentze MW, Preiss T (2014) Circular RNAs: splicing’s enigma variations. EMBO J 32:923–925. https://doi.org/10.1038/emboj.2013.53
Hernández-Hernández JM, García-González EG, Brun CE, Rudnicki MA (2017) The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration. Semin Cell Dev Biol 72:10–18. https://doi.org/10.1016/j.semcdb.2017.11.010
Hirata Y, Nomura K, Senga Y, Okada Y, Kobayashi K, Okamoto S, Minokoshi Y, Imamura M, Takeda S, Hosooka T, Ogawa W (2019) Hyperglycemia induces skeletal muscle atrophy via a WWP1/KLF15 axis. JCI Insight 4:e124952. https://doi.org/10.1172/jci.insight.124952
Hong L, Gu T, He Y, Zhou C, Hu Q, Wang X, Zheng E, Huang S, Xu Z, Yang J, Yang H, Li Z, Liu D, Cai G, Wu Z (2019) Genome-Wide analysis of circular RNAs mediated ceRNA regulation in porcine embryonic muscle development. Front Cell Dev Biol 7:289. https://doi.org/10.3389/fcell.2019.00289
Hou L, Xu J, Li H, Ou J, Jiao Y, Hu C, Wang C (2017) MiR-34c represses muscle development by forming a regulatory loop with Notch1. Sci Rep 7:9346. https://doi.org/10.1038/s41598-017-09688-y
Hunter RB, Kandarian SC (2004) Disruption of either the Nfkb1 or the Bcl3 gene inhibits skeletal muscle atrophy. J Clin Invest 114:1504–1511. https://doi.org/10.1172/JCI21696
Jeck WR, Sharpless NE (2014) Detecting and characterizing circular RNAs. Nat Biotechnol 32:453–461. https://doi.org/10.1038/nbt.2890
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Kimball SR, Jefferson LS (2006) Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136:227S-S231. https://doi.org/10.1093/jn/136.1.227S
Kuo IY, Ehrlich BE (2015) Signaling in muscle contraction. CSH Perspect Biol 7:a006023. https://doi.org/10.1101/cshperspect.a006023
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Larzul C, Lefaucheur L, Ecolan P, Gogué J, Talmant A, Sellier P, Le Roy P, Monin G (1997) Phenotypic and genetic parameters for longissimus muscle fiber characteristics in relation to growth, carcass, and meat quality traits in large white pigs. J Anim Sci 75:3126–3137. https://doi.org/10.2527/1997.75123126x
Lasda E, Parker R (2014) Circular RNAs: diversity of form and function. RNA 20:1829–1842. https://doi.org/10.1261/rna.047126.114
Lefebvre V, Li P, de Crombrugghe B (1998) A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 17:5718–5733. https://doi.org/10.1093/emboj/17.19.5718
Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20. https://doi.org/10.1016/j.cell.2004.12.035
Li J, Johnson SE (2006) ERK2 is required for efficient terminal differentiation of skeletal myoblasts. Biochem Bioph Res Co 345:1425–1433. https://doi.org/10.1016/j.bbrc.2006.05.051
Li JH, Liu S, Zhou H, Qu LH, Yang JH (2014) starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res 42:D92–D97. https://doi.org/10.1093/nar/gkt1248
Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, Zhu P, Chang Z, Wu Q, Zhao Y, Jia Y, Xu P, Liu H, Shan G (2015) Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 22:256–264. https://doi.org/10.1038/nsmb.2959
Li L, Chen Y, Nie L, Ding X, Zhang X, Zhao W, Xu X, Kyei B, Dai D, Zhan S, Guo J, Zhong T, Wang L, Zhang H (2019a) MyoD-induced circular RNA CDR1as promotes myogenic differentiation of skeletal muscle satellite cells. BBA-Gene Regul Mech 1862:807–821. https://doi.org/10.1016/j.bbagrm.2019.07.001
Li Z, Cai B, Abdalla BA, Zhu X, Zheng M, Han P, Nie Q, Zhang X (2019b) LncIRS1 controls muscle atrophy via sponging miR-15 family to activate IGF1-PI3K/AKT pathway. J Cachexia Sarcopeni 10:391–410. https://doi.org/10.1002/jcsm.12374
Li B, Yin D, Li P, Zhang Z, Zhang X, Li H, Li R, Hou L, Liu H, Wu W (2020) Profiling and functional analysis of circular RNAs in porcine fast and slow muscles. Front Cell Dev Biol 8:322. https://doi.org/10.3389/fcell.2020.00322
Liang G, Yang Y, Niu G, Tang Z, Li K (2017) Genome-wide profiling of Sus scrofa circular RNAs across nine organs and three developmental stages. DNA Res 24:523–535. https://doi.org/10.1093/dnares/dsx022
Ling YH, Sui MH, Zheng Q, Wang KY, Wu H, Li WY, Liu Y, Chu MX, Fang FG, Xu LN (2018) miR-27b regulates myogenic proliferation and differentiation by targeting Pax3 in goat. Sci Rep 8:3909. https://doi.org/10.1038/s41598-018-22262-4
Ling Y, Zheng Q, Zhu L, Xu L, Sui M, Zhang Y, Liu Y, Fang F, Chu M, Ma Y, Zhang X (2020) Trend analysis of the role of circular RNA in goat skeletal muscle development. BMC Genom 21:220. https://doi.org/10.1186/s12864-020-6649-2
Liu W, Xu L, Wang Y, Shen H, Zhu X, Zhang K, Chen Y, Yu R, Limera C, Liu L (2015) Transcriptome-wide analysis of chromium-stress responsive microRNAs to explore miRNA-mediated regulatory networks in radish (Raphanus sativus L.). Sci Rep 5:14024. https://doi.org/10.1038/srep14024
Liu R, Liu X, Bai X, Xiao C, Dong Y (2020) Identification and characterization of circRNA in Longissimus dorsi of different breeds of cattle. Front Genet 11:565085. https://doi.org/10.3389/fgene.2020.56508511
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
Madsen L, Kristiansen K (2010) The importance of dietary modulation of cAMP and insulin signaling in adipose tissue and the development of obesity. Ann NY Acad Sci 1190:1–14. https://doi.org/10.1111/j.1749-6632.2009.05262.x
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–338. https://doi.org/10.1038/nature11928
Mitin N, Kudla AJ, Konieczny SF, Taparowsky EJ (2001) Differential effects of Ras signaling through NFkappaB on skeletal myogenesis. Oncogene 20:1276–1286. https://doi.org/10.1038/sj.onc.1204223
Murholm M, Dixen K, Hansen JB (2010) Ras signalling regulates differentiation and UCP1 expression in models of brown adipogenesis. Biochim Biophys Acta 1800:619–627. https://doi.org/10.1016/j.bbagen.2010.03.008
Nguyen MT, Min KH, Lee W (2020) MiR-96-5p induced by palmitic acid suppresses the myogenic differentiation of C2C12 myoblasts by targeting FHL1. Int J Mol Sci 21:9445. https://doi.org/10.3390/ijms21249445
Nishikimi T, Iemura-Inaba C, Akimoto K, Ishikawa K, Koshikawa S, Matsuoka H (2009) Stimulatory and Inhibitory regulation of lipolysis by the NPR-A/cGMP/PKG and NPR-C/G(i) pathways in rat cultured adipocytes. Regul Pept 153:56–63. https://doi.org/10.1016/j.regpep.2008.10.010
Olson EN, Spizz G, Tainsky MA (1987) The oncogenic forms of N-ras or H-ras prevent skeletal myoblast differentiation. Mol Cell Biol 7:2104–2111. https://doi.org/10.1128/mcb.7.6.2104
Ouyang H, Chen X, Wang Z, Yu J, Jia X, Li Z, Luo W, Abdalla BA, Jebessa E, Nie Q, Zhang X (2018) Circular RNAs are abundant and dynamically expressed during embryonic muscle development in chickens. DNA Res 25:71–86. https://doi.org/10.1093/dnares/dsx039
Possidonio AC, Soares CP, Fontenele M, Morris ER, Mouly V, Costa ML, Mermelstein C (2016) Knockdown of Lmo7 inhibits chick myogenesis. FEBS Lett 590:317–329. https://doi.org/10.1002/1873-3468.12067
Quan J, Kang Y, Luo Z, Zhao G, Li L, Liu Z (2021) Integrated analysis of the responses of a circRNA-miRNA-mRNA ceRNA network to heat stress in rainbow trout (Oncorhynchus mykiss) liver. BMC Genom 22:48. https://doi.org/10.1186/s12864-020-07335-x
Rehfeldt C, Fiedler I, Dietl G, Ender K (2000) Myogenesis and postnatal skeletal muscle cell growth as influenced by selection. Livest Prod Sci 66:177–188. https://doi.org/10.1016/S0301-6226(00)00225-6
Reyes NL, Banks GB, Tsang M, Margineantu D, Gu H, Djukovic D, Chan J, Torres M, Liggitt HD, Hirenallur-S DK, Hockenbery DM, Raftery D, Iritani BM (2015) Fnip1 regulates skeletal muscle fiber type specification, fatigue resistance, and susceptibility to muscular dystrophy. Proc Natl Aca Sci USA 112:424–429. https://doi.org/10.1073/pnas.1413021112
Ronzoni F, Ceccarelli G, Perini I, Benedetti L, Galli D, Mulas F, Balli M, Magenes G, Bellazzi R, De Angelis GC, Sampaolesi M (2017) Met-activating genetically improved chimeric factor-1 promotes angiogenesis and hypertrophy in adult myogenesis. Curr Pharm Biotechnol 18:309–317. https://doi.org/10.2174/1389201018666170201124602
Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280:4294–4314. https://doi.org/10.1111/febs.12253
Schiaffino S, Dyar KA, Calabria E (2018) Skeletal muscle mass is controlled by the MRF4-MEF2 axis. Curr Opin Clin Nutr 21:164–167. https://doi.org/10.1097/MCO.0000000000000456
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Shen L, Gan M, Tang Q, Tang G, Jiang Y, Li M, Chen L, Bai L, Shuai S, Wang J, Li X, Liao K, Zhang S, Zhu L (2019a) Comprehensive analysis of lncRNAs and circRNAs reveals the metabolic specialization in oxidative and glycolytic skeletal muscles. Int J Mol Sci 20:2855. https://doi.org/10.3390/ijms20122855
Shen X, Liu Z, Cao X, He H, Han S, Chen Y, Cui C, Zhao J, Li D, Wang Y, Zhu Q, Yin H (2019b) Circular RNA profiling identified an abundant circular RNA circTMTC1 that inhibits chicken skeletal muscle satellite cell differentiation by sponging miR-128-3p. Int J Biol Sci 15:2265–2281. https://doi.org/10.7150/ijbs.36412
Shen J, Hao Z, Wang J, Hu J, Liu X, Li S, Ke N, Song Y, Lu Y, Hu L, Qiao L, Wu X, Luo Y (2021) Comparative transcriptome profile analysis of Longissimus dorsi muscle tissues from two goat breeds with different meat production performance using RNA-Seq. Front Genet 11:619399. https://doi.org/10.3389/fgene.2020.619399
Shi T, Yan X, Qiao L, Li B, Cheng L, Pan Y, Jing J, Cao N, Liu W (2018) MiR-330-5p negatively regulates ovine preadipocyte differentiation by targeting branched-chain aminotransferase 2. Anim Sci J 89:858–867. https://doi.org/10.1111/asj.12995
Sun L, Ma K, Wang H, Xiao F, Gao Y, Zhang W, Wang K, Gao X, Ip N, Wu Z (2007) JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J Cell Biol 179:129–138. https://doi.org/10.1083/jcb.200703184
Tao S, Yan X, Qiao L, Li B, Liu W (2018) MiR-330-5p negatively regulates ovine preadipocyte differentiation by targeting branched-chain aminotransferase 2. Anim Sci J 89:858–867. https://doi.org/10.1111/asj.12995
Taylor MV, Hughes SM (2017) Mef2 and the skeletal muscle differentiation program. Semin Cell Dev Biol 72:33–44. https://doi.org/10.1016/j.semcdb.2017.11.020
Tuma HJ, Venable JH, Wuthier PR, Henrickson RL (1962) Relationship of fiber diameter to tenderness and meatiness as influenced by bovine age. J Animalence. https://doi.org/10.2307/1235645
Turner DA (1985) Miranda: a non-strict functional language with polymorphic types. In: Conference on functional programming languages and computer architecture. Springer, Berlin, Heidelberg, p 1–16
Varendi K, Kumar A, Härma MA, Andressoo JO (2014) MiR-1, miR-10b, miR-155, and miR-191 are novel regulators of BDNF. Cell Mol Life Sci 71:4443–4456. https://doi.org/10.1007/s00018-014-1628-x
Wang Y, Wang Z (2015) Efficient backsplicing produces translatable circular mRNAs. RNA 21:172–179. https://doi.org/10.1261/rna.048272
Wang J, Ren Q, Hua L, Chen J, Zhang J, Bai H, Li H, Xu B, Shi Z, Cao H, Xing B, Bai X (2019a) Comprehensive analysis of differentially expressed mRNA, lncRNA and circRNA and their ceRNA networks in the Longissimus dorsi muscle of two different pig breeds. Int J Mol Sci 20:1107. https://doi.org/10.3390/ijms20051107
Wang Z, Zhang X, Li Z, Abdalla BA, Chen Y, Nie Q (2019b) MiR-34b-5p mediates the proliferation and differentiation of myoblasts by targeting IGFBP2. Cells 8:360. https://doi.org/10.3390/cells8040360
Wang J, Song C, Cao X, Li H, Cai H, Ma Y, Huang Y, Lan X, Lei C, Ma Y, Bai Y, Lin F, Chen H (2019c) MiR-208b regulates cell cycle and promotes skeletal muscle cell proliferation by targeting CDKN1A. J Cell Physiol 234:3720–3729. https://doi.org/10.1002/jcp.27146
Wang J, Shen J, Liu X, Li S, Luo Y, Zhao M, Hao Z, Ke N, Song Y, Qiao L (2021) Comparative analysis of meat production traits, meat quality, and muscle nutrient and fatty acid contents between Ziwuling black goats and Liaoning cashmere goats. Acta Pratacult Sin 30:166–177. https://doi.org/10.11686/cyxb2020199
Wei W, He HB, Zhang WY, Zhang HX, Bai JB, Liu HZ, Cao JH, Chang KC, Li XY, Zhao SH (2013) miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death Dis 4:e668. https://doi.org/10.1038/cddis.2013.184
Wei X, Li H, Yang J, Hao D, Dong D, Huang Y, Lan X, Plath M, Lei C, Lin F, Bai Y, Chen H (2017) Circular RNA profiling reveals an abundant circLMO7 that regulates myoblasts differentiation and survival by sponging miR-378a-3p. Cell Death Dis 8:e3153. https://doi.org/10.1038/cddis.2017.541
Wu W, Wang S, Xu Z, Wang X, Feng J, Shan T, Wang Y (2018) Betaine promotes lipid accumulation in adipogenic-differentiated skeletal muscle cells through ERK/PPARγ signalling pathway. Mol Cell Biochem 447:137–149. https://doi.org/10.1007/s11010-018-3299-7
Yan XM, Zhang Z, Meng Y, Li HB, Gao L, Luo D, Jiang H, Gao Y, Yuan B, Zhang JB (2020) Genome-wide identification and analysis of circular RNAs differentially expressed in the longissimus dorsi between Kazakh cattle and Xinjiang brown cattle. Peer J 8:e8646. https://doi.org/10.7717/peerj.8646
Yin H, He H, Cao X, Shen X, Han S, Cui C, Zhao J, Wei Y, Chen Y, Xia L, Wang Y, Li D, Zhu Q (2020) MiR-148a-3p regulates skeletal muscle satellite cell differentiation and apoptosis via the PI3K/AKT signaling pathway by targeting Meox2. Front Genet 11:512. https://doi.org/10.3389/fgene.2020.00512
Zammit PS (2017) Function of the myogenic regulatory factors Myf5, MyoD, myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Semin Cell Dev Biol 72:19–32. https://doi.org/10.1016/j.semcdb.2017.11.011
Zhang Q, Wang K, Yong Z, Meng J, Yu F, Yan C, Zhu D (2010) The myostatin-induced E3 ubiquitin ligase RNF13 negatively regulates the proliferation of chicken myoblasts. FEBS J 277:466–476. https://doi.org/10.1111/j.1742-4658.2009.07498.x
Zhao X, Mo D, Li A, Gong W, Xiao S, Zhang Y, Qin L, Niu Y, Guo Y, Liu X, Cong P, He Z, Wang C, Li J, Chen Y (2011) Comparative analyses by sequencing of transcriptomes during skeletal muscle development between pig breeds differing in muscle growth rate and fatness. PLoS ONE 6:e19774. https://doi.org/10.1371/journal.pone.0019774
Acknowledgements
This research was funded by the fund for Basic Research Creative Groups of Gansu Province (18JR3RA190), the Fuxi Young Talents Fund of Gansu Agricultural University (Gaufx-02Y02) and the Projects of Gansu Agricultural University (GSAU-ZL-2015-033).
Author information
Authors and Affiliations
Contributions
JS, JW, and YL conceived and designed the experiments. JS, HZ, LL, and YZ performed the experiments. JS analyzed the data. JW, YL, JH, XL, SL, ZH, ML, and ZZ contributed reagents, materials and tools and collected the samples. JS and JW wrote the manuscript and revised the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval
Ethical approval by the Ethics Committee of Gansu Agricultural University, was obtained (GAU-LC-2020-27).
Additional information
Communicated by Joan Cerda.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shen, J., Zhen, H., Li, L. et al. Identification and characterization of circular RNAs in Longissimus dorsi muscle tissue from two goat breeds using RNA-Seq. Mol Genet Genomics 297, 817–831 (2022). https://doi.org/10.1007/s00438-022-01887-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-022-01887-1