breast muscle; chicken; co-expression; development; lncRNA; Physiology; Physiology (medical)
Abstract :
[en] The developmental complexity of muscle arises from elaborate gene regulation. Long non-coding RNAs (lncRNAs) play critical roles in muscle development through the regulation of transcription and post-transcriptional gene expression. In chickens, previous studies have focused on the lncRNA profile during the embryonic periods, but there are no studies that explore the profile from the embryonic to post-hatching period. Here, we reconstructed 14,793 lncRNA transcripts and identified 2,858 differentially expressed lncRNA transcripts and 4,282 mRNAs from 12-day embryos (E12), 17-day embryos (E17), 1-day post-hatch chicks (D1), 14-day post-hatch chicks (D14), 56-day post-hatch chicks (D56), and 98-day post-hatch chicks (D98), based on our published RNA-seq datasets. We performed co-expression analysis for the differentially expressed lncRNAs and mRNAs, using STEM, and identified two profiles with opposite expression trends: profile 4 with a downregulated pattern and profile 21 with an upregulated pattern. The cis- and trans-regulatory interactions between the lncRNAs and mRNAs were predicted within each profile. Functional analysis of the lncRNA targets showed that lncRNAs in profile 4 contributed to the cell proliferation process, while lncRNAs in profile 21 were mainly involved in metabolism. Our work highlights the lncRNA profiles involved in the development of chicken breast muscle and provides a foundation for further experiments on the role of lncRNAs in the regulation of muscle development.
Disciplines :
Animal production & animal husbandry Genetics & genetic processes
Author, co-author :
Liu, Jie; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China ; Poultry Breeding Engineering Technology Center of Shandong Province, Jinan, China
Zhou, Yan; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China
Hu, Xin ; Université de Liège - ULiège > TERRA Research Centre
Yang, Jingchao; Shandong Animal Husbandry General Station, Jinan, China
Lei, Qiuxia; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China ; Poultry Breeding Engineering Technology Center of Shandong Province, Jinan, China
Liu, Wei; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China ; Poultry Breeding Engineering Technology Center of Shandong Province, Jinan, China
Han, Haixia; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China
Li, Fuwei; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China
Cao, Dingguo; Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, China ; Poultry Breeding Engineering Technology Center of Shandong Province, Jinan, China
Language :
English
Title :
Transcriptome Analysis Reveals the Profile of Long Non-coding RNAs During Chicken Muscle Development.
We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript. Funding. This research was supported by the Natural Science Foundation of Shandong province (ZR2019BC077), the Thoroughbred Project of Shandong Province (2020LZGC013), the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-41), the Jinan Layer Experiment Station of China Agriculture Research System (CARA-40-S12), the Natural Science Foundation of Shandong province (ZR2020MC169), the Collection, Protection and Accurate Identification of Livestock Germplasm Resources (2019LZGC019), the Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2016A04), the Shandong Provincial Key Laboratory of Special Construction Project (SDKL201810), and the Construction of Subjects and Teams of Institute of Poultry Science (CXGC2018E11).This research was supported by the Natural Science Foundation of Shandong province (ZR2019BC077), the Thoroughbred Project of Shandong Province (2020LZGC013), the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-41), the Jinan Layer Experiment Station of China
Abu-Elmagd M., Robson L., Sweetman D., Hadley J., Francis-West P., Münsterberg A., (2010). Wnt/Lef1 signaling acts via Pitx2 to regulate somite myogenesis. Dev. Biol. 337 211–219. 10.1016/j.ydbio.2009.10.023 19850024
Alonso-Martin S., Rochat A., Mademtzoglou D., Morais J., De Reyniès A., Auradé F., et al. (2016). Gene expression profiling of muscle stem cells identifies novel regulators of postnatal myogenesis. Front. Cell Dev. Biol. 4:58. 10.3389/fcell.2016.00058 27446912
Beekman R., Chapaprieta V., Russiñol N., Vilarrasa-Blasi R., Verdaguer-Dot N., Martens J. H., et al. (2018). The reference epigenome and regulatory chromatin landscape of chronic lymphocytic leukemia. Nat. Med. 24 868–880.
Bhattacharya T., Shukla R., Chatterjee R., Bhanja S., (2019). Comparative analysis of silencing expression of myostatin (MSTN) and its two receptors (ACVR2A and ACVR2B) genes affecting growth traits in knock down chicken. Sci. Rep. 9:7789.
Cai B., Li Z., Ma M., Wang Z., Han P., Abdalla B. A., et al. (2017). LncRNA-Six1 encodes a micropeptide to activate Six1 in Cis and is involved in cell proliferation and muscle growth. Front. Physiol. 8:230. 10.3389/fphys.2017.00230 28473774
Cassano M., Quattrocelli M., Crippa S., Perini I., Ronzoni F., Sampaolesi M., (2009). Cellular mechanisms and local progenitor activation to regulate skeletal muscle mass. J. Muscle Res. Cell Motil. 30 243–253. 10.1007/s10974-010-9204-y 20195710
Cusella-De Angelis M., Molinari S., Le Donne A., Coletta M., Vivarelli E., Bouche M., et al. (1994). Differential response of embryonic and fetal myoblasts to TGF beta: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120 925–933.
Darrah R., Mckone E., O’connor C., Rodgers C., Genatossio A., Mcnamara S., et al. (2010). EDNRA variants associate with smooth muscle mRNA levels, cell proliferation rates, and cystic fibrosis pulmonary disease severity. Physiol. Genomics 41 71–77. 10.1152/physiolgenomics.00185.2009 20028935
Dervishi E., Serrano C., Joy M., Serrano M., Rodellar C., Calvo J., (2011). The effect of feeding system in the expression of genes related with fat metabolism in semitendinous muscle in sheep. Meat Sci. 89 91–97. 10.1016/j.meatsci.2011.04.003 21543161
Djebali S., Davis C. A., Merkel A., Dobin A., Lassmann T., Mortazavi A., et al. (2012). Landscape of transcription in human cells. Nature 489:101.
Ernst J., Bar-Joseph Z., (2006). STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7:191. 10.1186/1471-2105-7-191 16597342
Feng X.-H., Derynck R., (2005). Specificity and versatility in TGF-β signaling through Smads. Annu. Rev. Cell Dev. Biol. 21 659–693. 10.1146/annurev.cellbio.21.022404.142018 16212511
Frazee A. C., Pertea G., Jaffe A. E., Langmead B., Salzberg S. L., Leek J. T., (2015). Ballgown bridges the gap between transcriptome assembly and expression analysis. Nat. Biotechnol. 33:243. 10.1038/nbt.3172 25748911
Fridolfsson A.-K., Ellegren H., (1999). A simple and universal method for molecular sexing of non-ratite birds. J. Avian Biol. 30 116–121. 10.2307/3677252
Gao P., Guo X., Du M., Cao G., Yang Q., Pu Z., et al. (2017). LncRNA profiling of skeletal muscles in Large White pigs and Mashen pigs during development. J. Anim. Sci. 95 4239–4250. 10.2527/jas2016.1297 29108073
Girardi F., Le Grand F., (2018). Wnt signaling in skeletal muscle development and regeneration. Prog. Mol. Biol. Transl. Sci. 153 157–179. 10.1016/bs.pmbts.2017.11.026 29389515
Huang Y., Wen H., Zhang M., Hu N., Si Y., Li S., et al. (2018). The DNA methylation status of MyoD and IGF-I genes are correlated with muscle growth during different developmental stages of Japanese flounder (Paralichthys olivaceus). Comp. Biochem. Physiol. Part B 219 33–43. 10.1016/j.cbpb.2018.02.005 29486246
Keren A., Tamir Y., Bengal E., (2006). The p38 MAPK signaling pathway: a major regulator of skeletal muscle development. Mol. Cell. Endocrinol. 252 224–230. 10.1016/j.mce.2006.03.017 16644098
Kern C., Wang Y., Chitwood J., Korf I., Delany M., Cheng H., et al. (2018). Genome-wide identification of tissue-specific long non-coding RNA in three farm animal species. BMC Genomics 19:684. 10.1186/s12864-018-5037-7 30227846
Kim D., Langmead B., Salzberg S. L., (2015). HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12 357–360. 10.1038/nmeth.3317 25751142
Kiss T., (2004). Biogenesis of small nuclear RNPs. J. Cell Sci. 117 5949–5951. 10.1242/jcs.01487 15564372
Kollias H. D., McDermott J. C., (2008). Transforming growth factor-β and myostatin signaling in skeletal muscle. J. Appl. Physiol. 104 579–587. 10.1152/japplphysiol.01091.2007 18032576
Kong L., Zhang Y., Ye Z.-Q., Liu X.-Q., Zhao S.-Q., Wei L., et al. (2007). CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 35 W345–W349.
Kosinska-Selbi B., Mielczarek M., Szyda J., (2020). Review: long non-coding RNA in livestock. Animal 14 2003–2013. 10.1017/s1751731120000841 32381139
Li T., Wang S., Wu R., Zhou X., Zhu D., Zhang Y., (2012). Identification of long non-protein coding RNAs in chicken skeletal muscle using next generation sequencing. Genomics 99 292–298. 10.1016/j.ygeno.2012.02.003 22374175
Li Z., Li B., Zhang L., Chen L., Sun G., Zhang Q., et al. (2016). The proliferation impairment induced by AQP3 deficiency is the result of glycerol uptake and metabolism inhibition in gastric cancer cells. Tumor Biol. 37 9169–9179. 10.1007/s13277-015-4753-8 26768614
Li Z., Ouyang H., Zheng M., Cai B., Han P., Abdalla B. A., et al. (2017). Integrated analysis of long non-coding RNAs (LncRNAs) and mRNA expression profiles reveals the potential role of LncRNAs in skeletal muscle development of the chicken. Front. Physiol. 7:687. 10.3389/fphys.2016.00687 28119630
Lin L., Flisikowski K., Schwarzenbacher H., Scharfe M., Severitt S., Blöcker H., et al. (2010). Characterization of the porcine AMPK alpha 2 catalytic subunitgene (PRKAA2): genomic structure, polymorphism detection and association study. Anim. Genet. 41 203–207. 10.1111/j.1365-2052.2009.01971.x 19793316
Liu J., Lei Q., Li F., Zhou Y., Gao J., Liu W., et al. (2019). Dynamic transcriptomic analysis of breast muscle development from the embryonic to post-hatching periods in chickens. Front. Genet. 10:1308. 10.3389/fgene.2019.01308 31998367
Liu R., Wang H., Liu J., Wang J., Zheng M., Tan X., et al. (2017). Uncovering the embryonic development-related proteome and metabolome signatures in breast muscle and intramuscular fat of fast-and slow-growing chickens. BMC Genomics 18:816. 10.1186/s12864-017-4150-3 29061108
Livak K. J., Schmittgen T. D., (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. Methods 25 402–408. 10.1006/meth.2001.1262 11846609
Marotta M., Ruiz-Roig C., Sarria Y., Peiro J. L., Nunez F., Ceron J., et al. (2009). Muscle genome-wide expression profiling during disease evolution in mdx mice. Physiol. Genomics 37 119–132. 10.1152/physiolgenomics.90370.2008 19223608
Martin M., (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17 10–12. 10.14806/ej.17.1.200
Moncaut N., Rigby P. W., Carvajal J. J., (2013). Dial M (RF) for myogenesis. FEBS J. 280 3980–3990. 10.1111/febs.12379 23751110
Montén C., Gudjonsdottir A. H., Browaldh L., Arnell H., Nilsson S., Agardh D., et al. (2015). Genes involved in muscle contractility and nutrient signaling pathways within celiac disease risk loci show differential mRNA expression. BMC Med. Genet. 16:44. 10.1186/s12881-015-0190-1 26123480
Moss T., Langlois F., Gagnon-Kugler T., Stefanovsky V., (2007). A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 64 29–49. 10.1007/s00018-006-6278-1 17171232
Muendlein A., Saely C. H., Geller-Rhomberg S., Sonderegger G., Rein P., Winder T., et al. (2011). Single nucleotide polymorphisms of TCF7L2 are linked to diabetic coronary atherosclerosis. PLoS One 6:e17978. 10.1371/journal.pone.0017978 21423583
Muers M., (2011). RNA: genome-wide views of long non-coding RNAs. Nat. Rev. Genet. 12:742. 10.1038/nrg3088 21989130
Münsterberg A., Kitajewski J., Bumcrot D. A., Mcmahon A. P., Lassar A. B., (1995). Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9 2911–2922. 10.1101/gad.9.23.2911 7498788
Muret K., Klopp C., Wucher V., Esquerré D., Legeai F., Lecerf F., et al. (2017). Long noncoding RNA repertoire in chicken liver and adipose tissue. Genet. Sel. Evol. 49 1–17. 10.1155/2019/3945475 31355260
Nakasa T., Ishikawa M., Shi M., Shibuya H., Adachi N., Ochi M., (2010). Acceleration of muscle regeneration by local injection of muscle−specific microRNAs in rat skeletal muscle injury model. J. Cell. Mol. Med. 14 2495–2505. 10.1111/j.1582-4934.2009.00898.x 19754672
Neguembor M. V., Jothi M., Gabellini D., (2014). Long noncoding RNAs, emerging players in muscle differentiation and disease. Skelet. Muscle 4:8. 10.1186/2044-5040-4-8 24685002
Ouyang H., Wang Z., Chen X., Yu J., Li Z., Nie Q., (2017). Proteomic analysis of chicken skeletal muscle during embryonic development. Front. Physiol. 8:281. 10.3389/fphys.2017.00281 28533755
Pertea M., Pertea G. M., Antonescu C. M., Chang T.-C., Mendell J. T., Salzberg S. L., (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33 290–295. 10.1038/nbt.3122 25690850
Ren T., Li Z., Zhou Y., Liu X., Han R., Wang Y., et al. (2018). Sequencing and characterization of lncRNAs in the breast muscle of Gushi and Arbor Acres chickens. Genome 61 337–347. 10.1139/gen-2017-0114 29447476
Ren T., Zhou Y., Zhou Y., Tian W., Gu Z., Zhao S., et al. (2017). Identification and association of novel lncRNA pouMU1 gene mutations with chicken performance traits. J. Genet. 96 941–950. 10.1007/s12041-017-0858-8 29321353
Sartori R., Schirwis E., Blaauw B., Bortolanza S., Zhao J., Enzo E., et al. (2013). BMP signaling controls muscle mass. Nat. Genet. 45 1309–1318. 10.1038/ng.2772 24076600
Serin E. A., Nijveen H., Hilhorst H. W., Ligterink W., (2016). Learning from co-expression networks: possibilities and challenges. Front. Plant Sci. 7:444. 10.3389/fpls.2016.00444 27092161
Sethi J. K., Vidal-Puig A., (2010). Wnt signalling and the control of cellular metabolism. Biochem. J. 427 1–17. 10.1042/bj20091866 20226003
Sherman B. T., Lempicki R. A., (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44. 10.1038/nprot.2008.211 19131956
Sporer K. R., Tempelman R. J., Ernst C. W., Reed K. M., Velleman S. G., Strasburg G. M., (2011). Transcriptional profiling identifies differentially expressed genes in developing turkey skeletal muscle. BMC Genomics 12:143. 10.1186/1471-2164-12-143 21385442
Srivastava R., Zhang J., Go G.-W., Narayanan A., Nottoli T. P., Mani A., (2015). Impaired LRP6-TCF7L2 activity enhances smooth muscle cell plasticity and causes coronary artery disease. Cell Rep. 13 746–759. 10.1016/j.celrep.2015.09.028 26489464
Sudre K., Cassar-Malek I., Listrat A., Ueda Y., Leroux C., Jurie C., et al. (2005). Biochemical and transcriptomic analyses of two bovine skeletal muscles in Charolais bulls divergently selected for muscle growth. Meat Sci. 70 267–277. 10.1016/j.meatsci.2005.01.012 22063483
Sulayman A., Tian K., Huang X., Tian Y., Xu X., Fu X., et al. (2019). Genome-wide identification and characterization of long non-coding RNAs expressed during sheep fetal and postnatal hair follicle development. Sci. Rep. 9:8501.
Sun L., Luo H., Bu D., Zhao G., Yu K., Zhang C., et al. (2013). Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res. 41:e166. 10.1093/nar/gkt646 23892401
Sun X., Li M., Sun Y., Cai H., Lan X., Huang Y., et al. (2016). The developmental transcriptome sequencing of bovine skeletal muscle reveals a long noncoding RNA, lncMD, promotes muscle differentiation by sponging miR-125b. Biochim. Biophys. Acta Mol. Cell Res. 1863 2835–2845. 10.1016/j.bbamcr.2016.08.014 27589905
Takata H., Terada K., Oka H., Sunada Y., Moriguchi T., Nohno T., (2007). Involvement of Wnt4 signaling during myogenic proliferation and differentiation of skeletal muscle. Dev. Dyn. 236 2800–2807. 10.1002/dvdy.21327 17879321
Trapnell C., Williams B. A., Pertea G., Mortazavi A., Kwan G., Van Baren M. J., et al. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28 511–515. 10.1038/nbt.1621 20436464
von Maltzahn J., Chang N. C., Bentzinger C. F., Rudnicki M. A., (2012). Wnt signaling in myogenesis. Trends Cell Biol. 22 602–609. 10.1016/j.tcb.2012.07.008 22944199
Wang W., Hart P., Piesco N., Lu X., Gorry M., Hart T., (2003). Aquaporin expression in developing human teeth and selected orofacial tissues. Calcif. Tissue Int. 72 222–227. 10.1007/s00223-002-1014-9 12522663
Wenzel A., Akbaşli E., Gorodkin J., (2012). RIsearch: fast RNA–RNA interaction search using a simplified nearest-neighbor energy model. Bioinformatics 28 2738–2746. 10.1093/bioinformatics/bts519 22923300
Xie C., Mao X., Huang J., Ding Y., Wu J., Dong S., et al. (2011). KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39 W316–W322.
Yao X., Yu T., Xi F., Xu Y., Ma L., Pan X., et al. (2019). BAMBI shuttling between cytosol and membrane is required for skeletal muscle development and regeneration. Biochem. Biophys. Res. Commun. 509 125–132. 10.1016/j.bbrc.2018.12.082 30580997
Ylihärsilä H., Kajantie E., Osmond C., Forsen T., Barker D. J., Eriksson J. G., (2007). Birth size, adult body composition and muscle strength in later life. Int. J. Obes. 31 1392–1399. 10.1038/sj.ijo.0803612 17356523
Zhan S., Dong Y., Zhao W., Guo J., Zhong T., Wang L., et al. (2016). Genome-wide identification and characterization of long non-coding RNAs in developmental skeletal muscle of fetal goat. BMC Genomics 17:666. 10.1186/s12864-016-3009-3 27550073
Zhan S., Zhao W., Song T., Dong Y., Guo J., Cao J., et al. (2018). Dynamic transcriptomic analysis in hircine longissimus dorsi muscle from fetal to neonatal development stages. Funct. Integr. Genomics 18 43–54. 10.1007/s10142-017-0573-9 28993898
Zhang J., Li Y., Qi J., Yu X., Ren H., Zhao X., et al. (2020). Circ-calm4 serves as an miR-337-3p sponge to regulate Myo10 (Myosin 10) and promote pulmonary artery smooth muscle proliferation. Hypertension 75 668–679. 10.1161/hypertensionaha.119.13715 32008463
Zhao S. J., Liu H., Chen J., Qian D. F., Kong F. Q., Jie J., et al. (2020). Macrophage GIT1 contributes to bone regeneration by regulating inflammatory responses in an ERK/NRF2−dependent way. J. Bone Mineral Res. 35 2015–2031. 10.1002/jbmr.4099 32460388
Zhao W., Mu Y., Ma L., Wang C., Tang Z., Yang S., et al. (2015). Systematic identification and characterization of long intergenic non-coding RNAs in fetal porcine skeletal muscle development. Sci. Rep. 5:8957.