[en] BACKGROUND: miRNAs play critical roles in growth and development. Various studies of chicken muscle development have focused on identifying miRNAs that are important for embryo or adult muscle development. However, little is known about the role of miRNAs in the whole muscle development process from embryonic to post-hatching periods. Here, we present a comprehensive investigation of miRNA transcriptomes at 12-day embryo (E12), E17, and day 1 (D1), D14, D56 and D98 post-hatching stages.
RESULTS: We identified 337 differentially expressed miRNAs (DE-miRNAs) during muscle development. A Short Time-Series Expression Miner analysis identified two significantly different expression profiles. Profile 4 with downregulated pattern contained 106 DE-miRNAs, while profile 21 with upregulated pattern contained 44 DE-miRNAs. The DE-miRNAs with the upregulated pattern mainly played regulatory roles in cellular turnover, such as pyrimidine metabolism, DNA replication, and cell cycle, whereas DE-miRNAs with the downregulated pattern directly or indirectly contributed to protein turnover metabolism such as glycolysis/gluconeogenesis, pyruvate metabolism and biosynthesis of amino acids.
CONCLUSIONS: The main functional miRNAs during chicken muscle development differ between embryonic and post-hatching stages. miRNAs with an upregulated pattern were mainly involved in cellular turnover, while miRNAs with a downregulated pattern mainly played a regulatory role in protein turnover metabolism. These findings enrich information about the regulatory mechanisms involved in muscle development at the miRNA expression level, and provide several candidates for future studies concerning miRNA-target function in regulation of chicken muscle development.
Disciplines :
Animal production & animal husbandry Genetics & genetic processes
Author, co-author :
Liu, Jie; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China ; Poultry Breeding Engineering Technology Center of Shandong Province, Ji'nan, 250023, China
Li, Fuwei; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China ; Shandong Provincial Key Laboratory of Poultry Diseases Diagnosis and Immunology, Ji'nan, 250023, China
Hu, Xin ; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Beijing, 100193, China
Cao, Dingguo; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China ; Poultry Breeding Engineering Technology Center of Shandong Province, Ji'nan, 250023, China
Liu, Wei; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China
Han, Haixia; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China
Zhou, Yan; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China. sally7919@163.com ; Shandong Provincial Key Laboratory of Poultry Diseases Diagnosis and Immunology, Ji'nan, 250023, China. sally7919@163.com
Lei, Qiuxia; Shandong Academy of Agricultural Sciences, Poultry Institute, Ji'nan, 250023, China. lei_qiuxia@163.com ; Poultry Breeding Engineering Technology Center of Shandong Province, Ji'nan, 250023, China. lei_qiuxia@163.com
Language :
English
Title :
Deciphering the miRNA transcriptome of breast muscle from the embryonic to post-hatching periods in chickens.
Natural Science Foundation of Shandong Province Key Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs Earmarked Fund for Modern Agro-industry Technology Research System Jinan Layer Experiment Station of China Agriculture Research System Collection, Protection and Accurate Identification of Livestock Germplasm Resources Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences Research and Demonstration on Key Technologies of Precision Breeding and Management of Laying Hens in Key R & D Projects in Shandong Province Shandong Provincial Key Laboratory of Special Construction Project
Funding text :
We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.This research was funded by Natural Science Foundation of Shandong province (ZR2019BC077); Key Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs (poultrylab2019–3); Earmarked Fund for Modern Agro-industry Technology Research System (CARS-41); Jinan Layer Experiment Station of China Agriculture Research System (CARA-40-S12); Collection, Protection and Accurate Identification of Livestock Germplasm Resources (2019LZGC019); Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2016A04); Research and Demonstration on Key Technologies of Precision Breeding and Management of Laying Hens in Key R & D Projects in Shandong Province (2019JZZY020611); Shandong Provincial Key Laboratory of Special Construction Project (SDKL201810); and Construction of Subjects and Teams of Institute of Poultry Science (CXGC2018E11).
Saccone V, Puri PL. Epigenetic regulation of skeletal myogenesis. Organogenesis. 2010;6(1):48–53. DOI: 10.4161/org.6.1.11293
Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibe B, Bouix J, Caiment F, Elsen J, Eychenne F. A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet. 2006;38(7):813–8. DOI: 10.1038/ng1810
Callis TE, Chen J, Wang D. MicroRNAs in skeletal and cardiac muscle development. DNA Cell Biol. 2007;26(4):219–25. DOI: 10.1089/dna.2006.0556
Luo W, Abdalla BA, Nie Q, Zhang X. The genetic regulation of skeletal muscle development: insights from chicken studies. Front Agric Sci Eng. 2017;4(3):295–304. DOI: 10.15302/J-FASE-2017159
Horak M, Novak J, Bienertovavasku J. Muscle-specific microRNAs in skeletal muscle development. Dev Biol. 2016;410(1):1–13. DOI: 10.1016/j.ydbio.2015.12.013
Orourke JR, Georges SA, Seay HR, Tapscott SJ, Mcmanus MT, Goldhamer DJ, Swanson MS, Harfe BD. Essential role for Dicer during skeletal muscle development. Dev Biol. 2007;311(2):359–68. DOI: 10.1016/j.ydbio.2007.08.032
Chen J, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang D. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006;38(2):228–33. DOI: 10.1038/ng1725
Anderson C, Catoe H, Werner R. MIR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids Res. 2006;34(20):5863–71. DOI: 10.1093/nar/gkl743
Dey BK, Gagan J, Dutta A. miR-206 and -486 induce myoblast differentiation by Downregulating Pax7. Mol Cell Biol. 2011;31(1):203–14. DOI: 10.1128/MCB.01009-10
Sartorelli V, Fulco M. Molecular and Cellular Determinants of Skeletal Muscle Atrophy and Hypertrophy. Sci Signal. 2004;2004(244):re11.
Luo W, Nie Q, Zhang X. MicroRNAs involved in skeletal muscle differentiation. J Genet Genomics. 2013;40(3):107–16. DOI: 10.1016/j.jgg.2013.02.002
Oksbjerg N, Gondret F, Vestergaard M. Basic principles of muscle development and growth in meat-producing mammals as affected by the insulin-like growth factor (IGF) system. Domest Anim Endocrinol. 2004;27(3):219–40. DOI: 10.1016/j.domaniend.2004.06.007
Rehfeldt C, Fiedler I, Dietl G, Ender K. Myogenesis and postnatal skeletal muscle cell growth as influenced by selection. Livest Prod Sci. 2000;66(2):177–88. DOI: 10.1016/S0301-6226(00)00225-6
Liu J, Lei Q, Li F, Zhou Y, Gao J, Liu W, Han H, Cao D: Dynamic Transcriptomic Analysis of Breast Muscle Development From the Embryonic to Post-hatching Periods in Chickens. Front Genet. 2020;10:1038.
Jebessa E, Ouyang H, Abdalla BA, Li Z, Abdullahi AY, Liu Q, Nie Q, Zhang X. Characterization of miRNA and their target gene during chicken embryo skeletal muscle development. Oncotarget. 2017;9(25):17309–24. DOI: 10.18632/oncotarget.22457
Li Y, Chen Y, Jin W, Fu S, Li D, Zhang Y, Sun G, Jiang R, Han R, Li Z. Analyses of MicroRNA and mRNA expression profiles reveal the crucial interaction networks and pathways for regulation of chicken breast muscle development. Front Genet. 2019;10:197. DOI: 10.3389/fgene.2019.00197
Huang B, Qi ZT, Xu Z, Nie P. Global characterization of interferon regulatory factor (IRF) genes in vertebrates: glimpse of the diversification in evolution. BMC Immunol. 2010;11(1):22. DOI: 10.1186/1471-2172-11-22
Xie B, Zhang C, Kang K, Jiang S. miR-599 Inhibits Vascular Smooth Muscle Cells Proliferation and Migration by Targeting TGFB2. PLoS One. 2015;10(11):e0141512.
Moraes LN, Fernandez GJ, Vechetti-Júnior IJ, Freire PP, Souza RWA, Villacis RAR, Rogatto SR, Reis PP, Dal-Pai-Silva M, Carvalho RF. Integration of miRNA and mRNA expression profiles reveals microRNA-regulated networks during muscle wasting in cardiac cachexia. Sci Rep. 2017;7(1):6998. DOI: 10.1038/s41598-017-07236-2
Ernst J, Barjoseph Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics. 2006;7(1):191. DOI: 10.1186/1471-2105-7-191
Diao Y, Guo X, Li Y, Sun K, Lu L, Jiang L, Fu X, Zhu H, Sun H, Wang H. Pax3/7BP is a Pax7- and Pax3-binding protein that regulates the proliferation of muscle precursor cells by an epigenetic mechanism. Cell Stem Cell. 2012;11(2):231–41. DOI: 10.1016/j.stem.2012.05.022
Chaudhry HW, Dashoush NH, Tang H, Zhang L, Wang X, Wu EX, Wolgemuth DJ. Cyclin A2 mediates Cardiomyocyte mitosis in the Postmitotic myocardium. J Biol Chem. 2004;279(34):35858–66. DOI: 10.1074/jbc.M404975200
Snow AJ, Puri P, Ackerpalmer A, Bouwmeester T, Vijayaraghavan S, Kline D. Phosphorylation-dependent interaction of tyrosine 3-Monooxygenase/tryptophan 5-Monooxygenase activation protein (YWHA) with PADI6 following oocyte maturation in mice. Biol Reprod. 2008;79(2):337–47. DOI: 10.1095/biolreprod.108.069328
Bilek K, Knoll A, Stratil A, Svobodova K, Horak P, Bechyňova R, Van Poucke M. Analysis of mRNA expression of CNN3, DCN, FBN2, POSTN, SPARC and YWHAQ genes in porcine foetal and adult skeletal muscles. Czech J Anim Sci. 2018;53(5):181–6. DOI: 10.17221/313-CJAS
Xu TS, Zhang X, Gu LH, Zhou HL, Rong G, Sun WP. Identification and characterization of genes related to the development of skeletal muscle in the Hainan black goat. Biosci Biotechnol Biochem. 2012;76(2):238–44. DOI: 10.1271/bbb.110461
Li T, Wu R, Zhang Y, Zhu D. A systematic analysis of the skeletal muscle miRNA transcriptome of chicken varieties with divergent skeletal muscle growth identifies novel miRNAs and differentially expressed miRNAs. BMC Genomics. 2011;12(1):186. DOI: 10.1186/1471-2164-12-186
Hu R, Pan W, Fedulov AV, Jester W, Jones MR, Weiss ST, Panettieri RA, Tantisira KG, Lu Q. MicroRNA-10a controls airway smooth muscle cell proliferation via direct targeting of the PI3 kinase pathway. FASEB J. 2014;28(5):2347–57. DOI: 10.1096/fj.13-247247
Huang H, Xie C, Sun X, Ritchie RP, Zhang J, Chen YE. miR-10a contributes to retinoid acid-induced smooth muscle cell differentiation. J Biol Chem. 2010;285(13):9383–9. DOI: 10.1074/jbc.M109.095612
Orom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell. 2008;30(4):460–71. DOI: 10.1016/j.molcel.2008.05.001
Mccarthy JJ, Esser KA. MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J Appl Physiol. 2007;102(1):306–13. DOI: 10.1152/japplphysiol.00932.2006
Zhang D, Li X, Chen C, Li Y, Zhao L, Jing Y, Liu W, Wang X, Zhang Y, Xia H. Attenuation of p38-Mediated miR-1/133 Expression Facilitates Myoblast Proliferation during the Early Stage of Muscle Regeneration. PLoS One. 2012;7(7):e41478.
Guess MG, Barthel KKB, Harrison BC, Leinwand LA. miR-30 family microRNAs regulate myogenic differentiation and provide negative feedback on the microRNA pathway. PLoS One. 2015;10(2):0118229. DOI: 10.1371/journal.pone.0118229
Huang W, Guo L, Zhao M, Zhang D, Xu H, Nie Q. The inhibition on MDFIC and PI3K/AKT pathway caused by miR-146b-3p triggers suppression of myoblast proliferation and differentiation and promotion of apoptosis. Cells. 2019;8(7):656. DOI: 10.3390/cells8070656
Teltathum T, Mekchay S. Proteome changes in Thai indigenous chicken muscle during growth period. Int J Biol Sci. 2009;5(7):679–85. DOI: 10.7150/ijbs.5.679
Doherty MK, Mclean L, Hayter JR, Pratt JM, Robertson DHL, Elshafei A, Gaskell SJ, Beynon RJ. The proteome of chicken skeletal muscle: changes in soluble protein expression during growth in a layer strain. Proteomics. 2004;4(7):2082–93. DOI: 10.1002/pmic.200300716
Mosleth EF. Comparison of muscle proteome profile in Norwegian landrace, Duroc and Hampshire at three different ages. Meat Sci. 2008;81(3):487–92.
Damon M, Wyszynskakoko J, Vincent A, Herault F, Lebret B. Comparison of Muscle Transcriptome between Pigs with Divergent Meat Quality Phenotypes Identifies Genes Related to Muscle Metabolism and Structure. PLoS One. 2012;7(3):e33763.
Kamli MR, Kim J, Pokharel S, Jan AT, Lee EJ, Choi I. Expressional studies of the aldehyde oxidase (AOX1) gene during myogenic differentiation in C2C12 cells. Biochem Biophys Res Commun. 2014;450(4):1291–6. DOI: 10.1016/j.bbrc.2014.06.126
Zheng Q, Zhang Y, Chen Y, Yang N, Wang X, Zhu D. Systematic identification of genes involved in divergent skeletal muscle growth rates of broiler and layer chickens. BMC Genomics. 2009;10(1):87. DOI: 10.1186/1471-2164-10-87
Krzysikwalker SM, Hadley JA, Pesall JE, McFarland DC, Vasilatosyounken R, Ramachandran R. Nampt/visfatin/PBEF affects expression of myogenic regulatory factors and is regulated by interleukin-6 in chicken skeletal muscle cells. Comp Biochem Physiol A Mol Integr Physiol. 2011;159(4):413–21. DOI: 10.1016/j.cbpa.2011.04.007
Xue J, Xue J, Zhang J, Li D, Jiang L. miR-130b-3p/301b-3p negatively regulated Rb1cc1 expression on myogenic differentiation of chicken primary myoblasts. Biotechnol Lett. 2017;39(11):1611–9. DOI: 10.1007/s10529-017-2400-8
Cai B, Ma M, Chen B, Li Z, Abdalla BA, Nie Q, Zhang X. MiR-16-5p targets SESN1 to regulate the p53 signaling pathway, affecting myoblast proliferation and apoptosis, and is involved in myoblast differentiation. Cell Death Dis. 2018;9(3):367. DOI: 10.1038/s41419-018-0403-6
Jia L, Li Y, Wu G, Song Z, Lu H, Song C, Zhang Q, Zhu J, Yang G, Shi X. MiRNA-199a-3p regulates C2C12 myoblast differentiation through IGF-1/AKT/mTOR signal pathway. Int J Mol Sci. 2013;15(1):296–308. DOI: 10.3390/ijms15010296
Zhu Y, Long H, Zeng L, Tang Y, Zhao R, Lin Z, Zhao S, Cheng L. MiR-19b-3p regulates osteogenic differentiation of PDGFRα+ muscle cells by specifically targeting PTEN. Cell Biol Int. 2019;43(5):565–73. DOI: 10.1002/cbin.11133
Yin H, He H, Shen X, Zhao J, Cao X, Han S, Cui C, Chen Y, Wei Y, Xia L. miR-9-5p inhibits skeletal muscle satellite cell proliferation and differentiation by targeting IGF2BP3 through the IGF2-PI3K/Akt signaling pathway. Int J Mol Sci. 2020;21(5):1655. DOI: 10.3390/ijms21051655
Li Z, Cai B, Abdalla BA, Zhu X, Zheng M, Han P, Nie Q, Zhang X. LncIRS1 controls muscle atrophy via sponging miR-15 family to activate IGF1-PI3K/AKT pathway. J Cachexia Sarcopenia Muscle. 2019;10(2):391–410. DOI: 10.1002/jcsm.12374
Kovanda A, Režen T, Rogelj B. MicroRNA in skeletal muscle development, growth, atrophy, and disease. Wiley Interdiscip Rev - Rna. 2014;5(4):509–25. DOI: 10.1002/wrna.1227
Yu M, Wang J, Wang G, You X, Zhao X, Jing Q, Qin Y. Vascular smooth muscle cell proliferation is influenced by let-7d MicroRNA and its interaction with KRAS. Circulation. 2011;75(3):703–9. DOI: 10.1253/circj.CJ-10-0393
Liu R, Wang H, Liu J, Wang J, Zheng M, Tan X, Xing S, Cui H, Li Q, Zhao G. Uncovering the embryonic development-related proteome and metabolome signatures in breast muscle and intramuscular fat of fast-and slow-growing chickens. BMC Genomics. 2017;18(1):816. DOI: 10.1186/s12864-017-4150-3
Sun Y, Zhao G, Liu R, Zheng M, Hu Y, Wu D, Zhang L, Li P, Wen J. The identification of 14 new genes for meat quality traits in chicken using a genome-wide association study. BMC Genomics. 2013;14(1):458. DOI: 10.1186/1471-2164-14-458
Fridolfsson A, Ellegren H. A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol. 1999;30(1):116–21. DOI: 10.2307/3677252
Rio DC, Ares M, Hannon GJ, Nilsen TW. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc. 2010;2010(6):pdb.prot5439. DOI: 10.1101/pdb.prot5439
Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2013;42(D1):D68–73. DOI: 10.1093/nar/gkt1181
Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003;4(9):R60. DOI: 10.1186/gb-2003-4-9-r60
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011;39(suppl_2):W316–22. DOI: 10.1093/nar/gkr483
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 2001;25(4):402–8. DOI: 10.1006/meth.2001.1262
