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Journal of Integrative Agriculture  2020, Vol. 19 Issue (9): 2137-2149    DOI: 10.1016/S2095-3119(20)63235-X
Special Issue: 动物科学合辑Animal Science
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The untold story between enhancers and skeletal muscle development
ZHANG Yong-sheng1, 3, LU Dan2, LIU Yu-wen1, 3, YI Guo-qiang1, 3, TANG Zhong-lin1, 3, 4 
1 Shenzhen Branch Guangdong Laboratory for Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, P.R.China
2 College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, P.R.China
3 Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, P.R.China
4 State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
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Currently, enhancers have key transcriptional regulatory roles in muscle development.  Skeletal muscle formation involves various molecules, and in animals, enhancers are one of the main types of transcriptional regulatory regions that are of great importance to regulate myogenic gene expression.  In muscle development, enhancers can generate enhancer RNAs (eRNAs) that are involved in the regulation of gene transcription.  The regulation of gene expression by eRNAs offers great potential in improving animal production traits.  Herein we comprehensively review the roles of enhancers in muscle formation and its potential function in skeletal muscle development.  This review will describe the future application of enhancers in skeletal muscle development and discuss the prospects that enhancer studies offer for agriculture, biotechnology, and animal breeding.
Keywords:  animal        enhancer        eRNA        skeletal muscle        growth and development  
Received: 30 March 2019   Accepted:
Fund: This work was supported by the Key R&D Programmes of Guangdong Province, China (2018B020203003), the National Natural Science Foundation of China (31830090), the Shenzhen Science Technology and Innovation Commission, China (JCYJ20170307160516413), and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ZDRW202006). We appreciate Postdoctoral Fellow Adeyinka Abiola Adetula, for grammar checking and suggestions.
Corresponding Authors:  Correspondence TANG Zhong-lin, E-mail:   
About author:  ZHANG Yong-sheng, Tel: +86-755-23251432, E-mail:;

Cite this article: 

ZHANG Yong-sheng, LU Dan, LIU Yu-wen, YI Guo-qiang, TANG Zhong-lin . 2020. The untold story between enhancers and skeletal muscle development. Journal of Integrative Agriculture, 19(9): 2137-2149.

Aljubran S A, Ruan C, Prasanna T P, Gurukumar K R, Venugopal R, Huynh B, Mohapatra S M, Richard L, Narasaiah K. 2012. Enhancer of zeste homolog 2 induces pulmonary artery smooth muscle cell proliferation. PLoS ONE, 7, e37712.
Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Makeev V J. 2014. An atlas of active enhancers across human cell types and tissues. Nature, 507, 455–461.
Arnold C D, Gerlach D, Stelzer C, Boryń ? M, Rath M, Stark A.
     2013. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science, 339, 1074–1077.
Babbitt C C, Markstein M, Gray J M. 2015. Recent advances in functional assays of transcriptional enhancers. Genomics, 106, 137–139.
Bai L, Liang R, Yang Y, Hou X, Wang Z, Zhu S, Wang C, Tang Z, Li K. 2015. MicroRNA-21 regulates PI3K/Akt/mTOR signaling by targeting TGFβI during skeletal muscle development in pigs. PLoS ONE, 10, e0119396.
Baribault C, Ehrlich K C, Ponnaluri V K C, Pradhan S, Lacey M, Ehrlich M. 2018. Developmentally linked human DNA hypermethylation is associated with down-modulation, repression, and upregulation of transcription. Epigenetics, 13, 275–289.
Benabdallah N S, Williamson I, Illingworth R S, Kane L, Boyle S, Sengupta D, Grimes G R, Therizols P, Bickmore W A. 2019. Decreased enhancer-promoter proximity accompanying enhancer activation. Molecular Cell, 76, 473-484.
Benoist C, Chambon P. 1981. In vivo, sequence requirements of the SV40 early promoter region. Nature, 290, 304–310.
Bentzinger C F, Wang Y X, Rudnicki M A. 2012. Building muscle: Molecular regulation of myogenesis. Cold Spring Harbor Perspectives in Biology, 4, 441–441.
Biben C, Kirschbaum B J, Garner I, Buckingham M. 1994. Novel muscle-specific enhancer sequences upstream of the cardiac actin gene. Molecular and Cellular Biology, 14, 3504.
Blum R. 2014. Activation of muscle enhancers by myod and epigenetic modifiers. Journal of Cellular Biochemistry, 115, 1855–1867.
Bonàs-Guarch S, Guindo-Martínez M, Miguel-Escalada I, Grarup N, Sebastian D, Rodriguez-Fos E, Sánchez F, Planas-Fèlix M, Cortes-Sánchez P, González S, Timshel P, Pers T H, Morgan C C, Moran I, Atla G, González J R, Puiggros M, Martí J, Andersson E A, Díaz C, et al. 2018. Re-analysis of public genetic data reveals a rare X-chromosomal variant associated with type 2 diabetes. Nature Communication, 9, 321.
Bose D A, Berger S L. 2017. eRNA binding produces tailored CBP activity profiles to regulate gene expression. RNA Biology, 14, 1655–1659.
Bose D A , Donahue G, Reinberg D, Shiekhattar R, Bonasio R, Berger S L. 2017. RNA binding to cbp stimulates histone acetylation and transcription. Cell, 168, 135–149.
Boyle A P, Davis S, Shulha H P, Meltzer P, Margulies E H, Weng Z P, Furey T S, Crawford G E. 2008. High-resolution mapping and characterization of open chromatin across the genome. Cell, 132, 311–322.
Braghetta P, Ferrari A, Fabbro C, Bizzotto D, Volpin D, Bonaldo P, Bressan G M. 2008. An enhancer required for transcription of the Col6a1 gene in muscle connective tissue is induced by signals released from muscle cells. Experimental Cell Research, 314, 3508–3518.
Brand-saberi B. 2005. Genetic and epigenetic control of skeletal muscle development. Annals of Anatomy-Anatomischer Anzeiger, 187, 199–207.
Brand-saberi B, Christ B. 1999. Genetic and epigenetic control of muscle development in vertebrates. Cell and Tissue Research, 296, 199–212.
Braun T, Gautel M. 2011. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nature Reviews Molecular Cell Biology, 12, 349–361.
Bryson-Richardson R J, Currie P D. 2008. The genetics of vertebrate myogenesis. Nature Reviews Genetics, 9, 632–646.
Bulger M, Groudine M. 1999. Looping versus linking: Toward a model for long-distance gene activation. Genes & Development, 13, 2465–2477.
Cai M, Kim S, Wang K, Farnham P J, Coetzee G A, Lu W. 2016. 4C-seq revealed long-range interactions of a functional enhancer at the 8q24 prostate cancer risk locus. Scientific Reports, 6, 22462.
Cao H Y, Dong X Y, Mao H G, Yang P C, Zhang Z X, Yu S L, Xu N Y, Yin Z Z. 2018. Polymorphisms of CEBPA and six1 genes and its association with carcass and body size traits in chickens (Gallus gallus). Journal of Agricultural Biotechnology, 26, 457–468. (in Chinese)
Casadaban M J, Cohen S N. 1979. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: In vivo probe for transcriptional control sequences. Proceedings of the National Academy of Sciences of the United States of America, 76, 4530–4533.
Catala F, Wanner R, Barton P, CohenA, Wright W, Buckingham M. 1995. A skeletal muscle-specific enhancer regulated by factors binding to E and CArG boxes is present in the promoter of the mouse myosin light-chain 1A gene. Molecular and Cellular Biology, 15, 4585–4596.
Davie K, Jacobs J, Atkins M, Potier D, Christiaens V, Halder G, Aerts S. 2015. Discovery of transcription factors and regulatory regions driving in vivo tumor development by ATAC-seq and FAIRE-seq open chromatin profiling. PLoS Genetics, 11, e1004994.
Deng W, Blobel G A. 2017. Detecting long-range enhancer-promoter interactions by quantitative chromosome conformation capture. Methods in Molecular Biology, 1468, 51–62.
Dickel D E, Zhu Y W, Nord A S, Wylie J N, Akiyama J A, Afzal V, Plajzer-Frick I, Kirkpatrick A, Göttgens B, Bruneau B G, Visel A, Pennacchio L A. 2014. Function-based identification of mammalian enhancers using site-specific integration. Nature Methods, 11, 566–571.
Ehrlich K C, Paterson H L, Lacey M, Ehrlich M. 2016. DNA hypomethylation in intragenic and intergenic enhancer chromatin of muscle-specific genes usually correlates with their expression. Yale Journal of Biology & Medicine, 89, 441–455.
Eun B, Sampley M L, Van-Winkle M T, Good A L, Kachman M M, Pfeifer K. 2013. The Igf2/H19 muscle enhancer is an active transcriptional complex. Nucleic Acids Research, 41, 8126–8134.
Fu S, Wang Q, Moore J E, Purcaro M J, Pratt H E, Fan K, Gu C, Jiang C, Zhu R, Kundaje A, Lu A, Weng Z. 2018. Differential analysis of chromatin accessibility and histone modifications for predicting mouse developmental enhancers. Nucleic Acids Research, 46, 11184–11201.
Fullwood M J, Liu M H, Pan Y F, Liu J, Xu H, Mohamed Y B, Orlov Y L, Velkov S, Ho A, Mei P H, Chew E G, Huang P Y, Welboren W J, Han Y, Ooi H S, Ariyaratne P N, Vega V B, Luo Y, Tan P Y, Choy P Y, et al. 2009. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature, 462, 58–64.
Garstang M G, Pradeepa M M M. 2018. An enhancer-derived RNA muscles in to regulate myogenin in trans. Molecular Cell, 71, 3–5.
Gaulton K J, Nammo T, Pasquali L, Simon J M, Giresi P G, Fogarty M P, Panhuis T M, Mieczkowski P, Secchi A, Bosco D, Berney T, Montanya E, Mohlke K L, Lieb J D, Ferrer J. 2010. A map of open chromatin in human pancreatic islets.Nature Genetics, 42, 255–259.
Gavrilov A A, Razin S V. 2008. Study of spatial organization of chicken alpha-globin gene domain by 3C technique. Biochemistry (Mosc), 73, 1192–1199.
Goh K Y, Inoue T. 2018. A large transcribed enhancer region regulates C. elegans bed-3 and the development of egg laying muscles. Biochimica et Biophysica Acta Gene Regulatory Mechanisms, 1861, 519–533.
Gong Y, Lazaris C, Sakellaropoulos T, Lozano A, Kambadur P, Ntziachristos P, Aifantis I, Tsirigos A. 2018. Stratification of TAD boundaries reveals preferential insulation of super-enhancers by strong boundaries. Nature Communication, 9, 542.
Groenen M A, Archibald A L, Uenishi H, Tuggle C K, Takeuchi Y, Rothschild M F, Rogel-Gaillard C, Park C, Milan D, Megens H J, Li S, Larkin D M, Kim H, Frantz L A, Caccamo M, Ahn H, Aken B L, Anselmo A, Anthon C, Auvil L, Badaoui B, et al. 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491, 393–398.
Guerrero L, Marco-Ferreres R, Serrano A L, Arredondo J J, Cervera M. 2010. Secondary enhancers synergise with primary enhancers to guarantee fine-tuned muscle gene expression. Developmental Biology, 337, 16–28.
Hanssen L L P, Kassouf M T, Oudelaar A M, Biggs D, Preece C, Downes D J, Gosden M, Sharpe J A, Sloane-Stanley J A, Hughes J R, Davies B, Higgs D R. 2017. Tissue-specific CTCF-cohesin-mediated chromatin architecture delimits enhancer interactions and function in vivo. Nature Cell Biology, 19, 952–961.
Himeda C L, Debarnot C, Homma S, Beermann M L, Miller J B, Jones P L, Jones T I. 2014. Myogenic enhancers regulate expression of the facioscapulohumeral muscular dystrophy-associated DUX4 gene. Molecular & Cellular Biology, 34, 1942–1955.
Hossner K L. 2005. Hormonal Regulation of Farm Animal Growth. Common wealth Agricultural Bureaux International, Cambridge. pp. 13–33.
Jaynes J B, Johnson J E, Buskin J N, Gartside C L, Hauschka S D. 1988. The muscle creatine kinase gene is regulated by multiple upstream elements, including a muscle-specific enhancer. Molecular & Cellular Biology, 8, 62–70.
Jiang Y, Qian F, Bai X, Liu Y, Wang Q, Ai B, Han X, Shi S, Zhang J, Li X, Tang Z, Pan Q, Wang Y, Wang F, Li C. 2019. SEdb: A comprehensive human super-enhancer database. Nucleic Acids Research, 47, 235–243.
Khan A, Zhang X. 2016. dbSUPER: A database of super-enhancers in mouse and human genome. Nucleic Acids Research, 44, 164–171.
Kieffer-Kwon K R, Tang Z, Mathe E, Qian J, Sung M H, Li G, Resch W, Baek S, Pruett N, Grøntved L, Vian L, Nelson S, Zare H, Hakim O, Reyon D, Yamane A, Nakahashi H, Kovalchuk A L, Zou J, Joung J K, et al. 2013. Interactome maps of mouse gene regulatory domains reveal basic principles of transcriptional regulation. Cell, 155, 1507–1520.
Kim J R, Kee H J, Kim J Y, Joung H, Nam K I, Eom G H, Choe N, Kim H S, Kim J C, Kook H, Seo S B, Kook H. 2009. Enhancer of polycomb1 acts on serum response factor to regulate skeletal muscle differentiation. Journal of Biological Chemistry, 284, 16308–16316.
Kim T K, Hemberg M, Gray J M, Costa A M, Bear D M, Wu J, Harmin D A, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley P F, Kreiman G, Greenberg M E. 2010. Wide spread transcription at neuronal activity-regulated enhancers. Nature, 465, 182–187.
Kim T K, Shiekhattar R. 2015. Architectural and functional commonalities between enhancers and promoters. Cell, 162, 948–959.
Kwon A T, Chou A Y, Arenillas D J, Wasserman W W. 2011. Validation of skeletal muscle cis-regulatory module predictions reveals nucleotide composition bias in functional enhancers. PLoS Computational Biology, 7, 1–15.
Latinki? B V, Cooper B, Towers N, Sparrow D, Kotecha S, Mohun TJ. 2002. Distinct enhancers regulate skeletal and cardiac muscle-specific expression programs of the cardiac α-actin gene in xenopus embryos. Developmental Biology, 245, 57–70.
Lawrence T L J, Fowler V R. 2002. Growth of Farm Animals. Commonwealth Agricultural Bureaux International, New York. pp. 56–76.
Li R, Yi X, Wei X, Huo B, Guo X, Cheng C, Fang Z M, Wang J, Feng X, Zheng P, Su Y S, Masau J F, Zhu X H, Jiang D S. 2018. EZH2 inhibits autophagic cell death of aortic vascular smooth muscle cells to affect aortic dissection. Cell Death & Disease, 9, 180.
Li W, Notani D, Rosenfeld M G. 2016. Enhancers as non-coding RNA transcription units: Recent insights and future perspectives. Nature Reviews Genetics, 17, 207–223.
Liang G, Yang Y, Niu G, Tang Z, Li K. 2017. Genome-wide profiling of Sus scrofa circular RNAs across 9 organs and 3 developmental stages. DNA Research, 24, 523–535.
Lin D, Hong P, Zhang S, Xu W, Jamal M, Yan K, Lei Y, Liang Li, Ruan Y, Fu Z F, Li G, Cao G. 2018. Digestion-ligation-only Hi-c is an efficient and cost-effective method for chromosome conformation capture. Nature Genetics, 50, 754–763.
Liu N, Nelson B R, Bezprozvannaya S, Shelton J M, Olson E N. 2014. Requirement of MEF2A, C, and D for skeletal muscle regeneration. Proceedings of the National Academy of Sciences of the United States of America, 111, 4109–4114.
Liu X, Wang J, Li R, Yang X, Sun Q, Albrecht E, Zhao R. 2011. Maternal dietary protein affects transcriptional regulation of myostatin gene distinctively at weaning and finishing stages in skeletal muscle of Meishan pigs. Epigenetics, 6, 899–907.
Liu Y W, Yu S, Dhiman V K, Brunetti T, Eckart H, White K P. 2017. Functional assessment of human enhancer activities using whole-genome starr-sequencing. Genome Biology, 18, 219.
Mao R, Wu Y, Ming Y, Xu Y, Fan Y. 2018. Enhancer RNAs: A missing regulatory layer in gene transcription. Science China (Life Sciences), 61, 1–8.
Maston G A, Evans S K, Green M R. 2006. Transcriptional regulatory elements in the human genome. Annual Review of Genomics & Human Genetics, 7, 29–59.
Nagari A, Murakami S, Malladi V S, Kraus W L. 2017. Computational approaches for mining GRO-Seq data to identify and characterize active enhancers. Methods in Molecular Biology, 1468, 121–138.
Niu G, Yang Y, Zhang Y, Hua C, Wang Z, Tang Z, Li K. 2016.Identifying suitable reference genes for gene expression analysis in developing skeletal muscle in pigs. PeerJ - the Journal of Life and Environmental Sciences, 4, e2428.
Peng Y L, Zhang Y B. 2018. Enhancer and super-enhancer: Positive regulators in gene transcription. Animal Models and Experimental Medicine, 1, 169–179.
Pennacchio L A, Bickmore W, Dean A, Nobrega M A, Bejerano G. 2013. Enhancers: Five essential questions. Nature Reviews Genetics, 14, 288–295.
Pradeepa M M, Grimes G R, Kumar Y, Olley G, Taylor G C, Schneider R, Bickmore W A. 2016. Histone H3 globular domain acetylation identifies a new class of enhancers. Nature Genetics, 48, 681–686.
Qi L W, Li X M, Zhang S G, An D C. 2006. Genetic regulation by non-coding RNAs. Science in China (Series C: Life Sciences), 49, 201–217.
Rahnamoun H, Orozco P, Lauberth S M. 2020. The role of enhancer RNAs in epigenetic regulation of gene expression.Transcription, 11, 19–25.
Reményi A, Schöler H R, Wilmanns M. 2004. Combinatorial control of gene expression. Nature Structural & Molecular Biology, 11, 812–815.
Ren B. 2010. Transcription: Enhancers make non-coding RNA. Nature, 465, 173–174.
Repentigny D Y. 2004. The mouse dystrophin muscle enhancer-1 imparts skeletal muscle, but not cardiac muscle, expression onto the dystrophin Purkinje promoter in transgenic mice. Human Molecular Genetics, 13, 2853–2862.
Rhee H S, Pugh B F. 2011. Comprehensive genome-wide protein–DNA interactions detected at single-nucleotide resolution. Cell, 147, 1408–1409.
Rickels R, Shilatifard A. 2018. Enhancer logic and mechanics in development and disease. Trends in Cell Biology, 28, 608–630.
Rigby P W J, Teboul L, Hadchouel J, Daubas P, Summerbell D, Buckingham M. 2002. The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somiticmyogenesis. Development, 129, 4571–4580.
Rinaldi M, Signori E, Rosati P, Cannelli G, Parrella P, Iannace E, Monego G, Ciafrè S A, Farace M G, Iurescia S, Fioretti D, Rasi G, Fazio V M. 2006. Feasibility of in utero DNA vaccination following naked gene transfer into pig fetal muscle: Transgene expression, immunity and safety.Vaccine, 24, 4586–4591.
Ron G, Globerson Y, Moran D, Kaplan T. 2017. Promoter-enhancer interactions identified from Hi-C data using probabilistic models and hierarchical topological domains. Nature Communications, 8, 2237.
Rothschild G, Basu U. 2017. Lingering questions about enhancer RNA and enhancer transcription-coupled genomic instability. Trends in Genetics, 33, 143–154.
De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi B K, Muller H, Ragoussis J, Wei C L, Natoli G. 2010. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biology, 8, e1000384.
Schaffner W. 2015. Enhancers, enhancers - from their discovery to today’s universe of transcription enhancers. Biological Chemistry, 396, 311–27.
Schoenfelder S, Furlan-Magaril M, Mifsud B, Tavares-Cadete F, Sugar R, Javierre B M, Nagano T, Katsman Y, Sakthidevi M, Wingett S W, Dimitrova E, Dimond A, Edelman L B, Elderkin S, Tabbada K, Darbo E, Andrews S, Herman B, Higgs A, LeProust E, et al. 2015. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Research, 25, 582–597.
Summerbell D. 2000. The expression of myf-5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors. Development, 127, 3745–3757.
Sun C B, Zhang X. 2016. Advance in the research on super-enhancer. Hereditas, 38, 1056–1068.
Sur I, Taipale J. 2016. The role of enhancers in cancer. Nature Reviews Cancer, 16, 483–493.
Tang Z, Li Y, Wan P, Li X, Zhao S, Liu B, Fan B, Zhu M, Yu M, Li K. 2007. LongSAGE analysis of skeletal muscle at three prenatal stages in Tongcheng and Landrace pigs. Genome Biology, 8, R115.
Tang Z, Wu Y, Yang Y, Yang Y C T, Wang Z, Yuan J, Yang Y, Hua C, Fan X, Niu G, Zhang Y, Lu Z J, Li K. 2017. Comprehensive analysis of long non-coding RNAs highlights their spatio-temporal expression patterns and evolutional conservation in Sus scrofa. Scientific Reports, 7, 43166.
Thormann V, Rothkegel M C, Schöpflin R, Glaser L V, Djuric P, Li N, Chung H R, Schwahn K, Vingron M, Meijsing S H. 2018. Genomic dissection of enhancers uncovers principles of combinatorial regulation and cell type-specific wiring of enhancer–promoter contacts. Nucleic Acids Research, 46, 2868–2882.
Tjian R, Maniatis T. 1994. Transcriptional activation: A complex puzzle with few easy pieces. Cell, 77, 5–8.
Tsai P F, Dell’Orso S, Rodriguez J, Vivanco K O, Ko K D, Jiang K, Juan A H, Sarshad A A, Vian L, Tran M. 2018. A muscle-specific enhancer rna mediates cohesin recruitment and regulates transcription in trans. Molecular Cell, 71, 129–141.
Tse M C L, Herlea-Pana O, Brobst D, Yang X, Wood J, Hu X, Liu Z, Lee C W, Zaw A M, Chow B K C, Ye K, Chan C B. 2017. Tumor necrosis factor-α promotes phosphoinositide 3-kinase enhancer A and AMP-activated protein kinase interaction to suppress lipid oxidation in skeletal muscle. Diabetes, 66, 1858–1870.
Vastolo V, Nettore I C, Ciccarelli M, Albano L, Raciti G A, Longo M, Beguinot F, Ungaro P. 2018. High-fat diet unveils an enhancer element at the Ped/Pea-15 gene responsible for epigenetic memory in skeletal muscle. Metabolism, 87, 70–79.
Visel A, Blow M J, Li Z, Zhang T, Akiyama J A, Holt A. 2009. Chip-seq accurately predicts tissue-specific activity of enhancers. Nature, 457, 854–858.
Visel A, Minovitsky S, Dubchak I, Pennacchio L A. 2007. VISTA Enhancer Browser - a database of tissue-specific human enhancers. Nucleic Acids Research, 35, 88–92.
Wang C, Jia L, Wang Y, Du Z, Zhou L, Wen X, Li H, Zhang S, Chen H, Chen N, Chen J, Zhu Y, Nie Y, Celic I, Gao S, Zhang S, Hoffman A R, Li W, Hu J F, Cui J. 2020. Genome-wide interaction target profiling reveals a novel Peblr20-eRNA activation pathway to control stem cell pluripotency. Theranostics, 10, 353–370.
Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, Qiu J, Liu W, Kaikkonen M U, Ohgi K A, Glass C K, Rosenfeld M G, Fu X D. 2011. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature, 474, 390–394.
Wang J, Dai X, Berry L D, Cogan J D, Liu Q, Shyr Y. 2019. HACER: An atlas of human active enhancers to interpret regulatory variants. Nucleic Acids Research, 47, 106–112.
Wang Z, Zhang Q, Zhang W, Lin J R, Cai Y, Mitra J, Zhang Z D. 2018. HEDD: Human enhancer disease database. Nucleic Acids Research, 4, 113–120.
Wei Y, Zhang S, Shang S, Zhang B, Li S, Wang X, Wang F, Su J, Wu Q, Liu H, Zhang Y. 2016. SEA: A super-enhancer archive. Nucleic Acids Research, 44, 172–179.
Whyte W A, Orlando D A, Hnisz D, Abraham B J, Lin C Y, Kagey M H, Rahl P B, Lee T I, Young R A. 2013. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell, 153, 307–319.
Xiao S, Cao S, Huang Q, Xia L, Deng M, Yang M, Jia G, Liu X, Shi J, Wang W, Li Y, Liu S, Zhu H, Tan K, Luo Q, Zhong M, He C, Xia L. 2019. The RNA N6-methyladenosine modification landscape of human fetal tissues. Nature Cell Biology, 21, 651–661.
Xiong L, Kang R, Ding R, Kang W, Zhang Y, Liu W, Huang Q, Meng J, Guo Z. 2018. Genome-wide identification and characterization of enhancers across 10 human tissues. International Journal of Biological Science, 14, 1321–1332.
Xu Y, Yu W, Xiong Y, Xie H, Ren Z, Xu D, Lei M, Zuo B, Feng X. 2011. Molecular characterization and expression patterns of serine/arginine-rich specific kinase 3 (SPRK3) in porcine skeletal muscle. Molecular Biology Reports, 38, 2903–2909.
Yang Y, Liang G, Niu G, Zhang Y, Zhou R, Wang Y, Mu Y, Tang Z, Li K. 2017. Comparative analysis of DNA methylome and transcriptome of skeletal muscle in lean-, obese-, and mini-type pigs. Scientific Reports, 7, 39883.
Yang Y, Zhou R, Mu Y, Hou X, Tang Z, Li K. 2016. Genome-wide analysis of DNA methylation in obese, lean, and miniature pig breeds. Scientific Reports, 6, 30160.
Yang Y L, Zou R, Li K. 2017. Future livestock breeding: Precision breeding based on multiomics information and population personalization. Journal of Integrative Agriculture, 16, 2784–2791.
Yao J, Chen J, Li LY, Wu M. 2020. Epigenetic plasticity of enhancers in cancer. Transcription, 11, 26–36.
Yonamine C Y, Alves-Wagner A B, Esteves J V, Okamoto M M, Correa-Giannella M L, Giannella-Neto D, Machado U F. 2019. Diabetes induces tri-methylation at lysine 9 of histone 3?at Slc2a4 gene in skeletal muscle: A new target to improve glycemic control. Molecular & Cellular Endocrinology, 481, 26–34.
Zhang N, Cheng M, Bai L, Kang Y, Li H. 2016. eSNPdb, a database of SNPs in human enhancer regions. Genomics and Applied Biology, 35, 2867–2871.
Zhang X, Patel S P, McCarthy J J, Rabchevsky A G, Goldhamer D J, Esser K A. 2012. A non-canonical E-box within the MyoD core enhancer is necessary for circadian expression in skeletal muscle. Nucleic Acids Research, 40, 3419–3430.
Zhang Y B. 2018. 3D genomics and precision biology. Chinese Journal of Biochemistry & Molecular Biology, 34, 351–363.(in Chinese)
Zhao Y, Zhou J, He L, Li Y, Yuan J, Sun K, Chen X, Bao X, Esteban M A, Sun H, Wang H. 2019. MyoD induced enhancer RNA interacts with hnRNPL to activate target gene transcription during myogenic differentiation. Nature Communications, 10, 5787.
Zou Y, Dong Y, Meng Q, Zhao Y, Li N. 2018. Incorporation of a skeletal muscle-specific enhancer in the regulatory region of Igf1 upregulates IGF1 expression and induces skeletal muscle hypertrophy. Scientific Reports, 8, 2781.
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[6] Hong Quyen Dang, XU Gu-li, HOU Lian-jie, XU Jian, HONG Guang-liang, Chingyuan Hu, WANG Chong. MicroRNA-22 inhibits proliferation and promotes differentiation of satellite cells in porcine skeletal muscle[J]. >Journal of Integrative Agriculture, 2020, 19(1): 225-233.
[7] LU Lin, LIAO Xiu-dong, LUO Xu-gang. Nutritional strategies for reducing nitrogen, phosphorus and trace mineral excretions of livestock and poultry[J]. >Journal of Integrative Agriculture, 2017, 16(12): 2815-2833.
[8] XIONG Yan, MENG Qing-shi, GAO Jie, TANG Xiang-fang, ZHANG Hong-fu. Effects of relative humidity on animal health and welfare[J]. >Journal of Integrative Agriculture, 2017, 16(08): 1653-1658.
[9] DONG Li-feng, XU Xian-cha, ZHANG Nai-feng, TU Yan, DIAO Qi-yu. Effects of different feeding methods and space allowance on the growth performance, individual and social behaviors of Holstein calves[J]. >Journal of Integrative Agriculture, 2017, 16(06): 1375-1382.
[10] LIAO Yan, WU Wen-liang, MENG Fan-qiao, LI Hu. Impact of agricultural intensification on soil organic carbon: A study using DNDC in Huantai County, Shandong Province, China[J]. >Journal of Integrative Agriculture, 2016, 15(06): 1364-1375.
[11] SHAN Yan-ju, XU Wen-juan, SHU Jing-ting, ZHANG Ming, SONG Wei-tao, TAO Zhi-yun, ZHU Chunhong, LI Hui-fang. Differentiation of expression profiles of two calcineurin subunit genes in chicken skeletal muscles during early postnatal growth depending on anatomical location of muscles and breed[J]. >Journal of Integrative Agriculture, 2016, 15(05): 1085-1094.
[12] D J Connor, H van Rees, P S Carberry. Impact of systems modelling on agronomic research and adoption of new practices in smallholder agriculture[J]. >Journal of Integrative Agriculture, 2015, 14(8): 1478-1489.
[13] ZHANG Yong-qiang, LIU Hai-sheng, WU Xiao-dong, WANG Xiao-zhen, LI Jin-ming, ZHAO Yonggang, Lü Yan, REN Wei-jie, GE Sheng-qiang, WANG Zhi-liang. A novel real-time RT-PCR with TaqMan-MGB probes and its application in detecting BVDV infections in dairy farms[J]. >Journal of Integrative Agriculture, 2015, 14(8): 1637-1643.
[14] ZHAO Fu-ping, GUO Gang, WANG Ya-chun, GUO Xiang-yu, ZHANG Yuan, DU Li-xin. Genetic parameters for somatic cell score and production traits in the first three lactations of Chinese Holstein cows[J]. >Journal of Integrative Agriculture, 2015, 14(1): 125-130.
[15] ZHANG Wen-guang. Development of Genome-Wide Scan for Selection Signature in Farm Animals[J]. >Journal of Integrative Agriculture, 2013, 12(8): 1461-1470.
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