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| SFRP2 affects prenatal muscle development and is regulated by microRNA-1/206 in pigs |
| MA Yan-jiao, YANG Ya-lan, SUN Wei, ZHOU Rong, LI Kui, TANG Zhong-lin |
1、Jilin Provincial Key Laboratory, College of Animal Science, Jilin University, Changchun 130012, P.R.China
2、Key Laboratory of Farm Animal Genetic Resources and Germplasm Innovation, Ministry of Agriculture/Institute of Animal Science,
Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
3、College of Animal Science and Technology, Northwest A&F University, Yangling 712100, P.R.China |
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摘要 Secreted frizzled-related protein 2 (SFRP2), a member of the SFRPs family, is associated with cell growth and differentiation in myogenesis. Our previous study suggested that SFRP2 was a potential target of microRNA (miRNA)-1/206, which was considered as myomiRs. To further explore the biological function and regulation mechanisms of the SFRP2 gene in porcine skeletal muscle development, we first analyzed the sequence structure of the porcine SFRP2 gene. Subsequently, we detected its tissue distribution in adult Tongcheng pigs (a Chinese indigenous breed) and investigated its dynamic expression in developmental skeletal muscle (13 prenatal and 7 postnatal time points) in Tongcheng pigs. An interaction analysis between SFRP2 and myomiRs was also performed. The results showed that the expression pattern of the SFRP2 varied greatly across diverse tissues. It exhibited abundant expression in prenatal skeletal muscle and peaked at 55 days post coitus (E55), and had a lower expression in postnatal skeletal muscle, indicating that the SFRP2 gene might affect porcine embryonic skeletal muscle development. Co-expression analysis revealed that the expression levels of SFRP2 correlated negatively with miRNA-1 (r=–0.570, P-value=0.009) and miRNA-206 (r=–0.546, P-value=0.013), but positively with SFRP1 (r=0.613, P-value=0.004). The bioinformatics analysis and dual luciferase assay verified that the SFRP2 was a putative target of miRNA-1/206 in pigs. Therefore, this study is helpful for understanding the biological function and molecular regulation of the SFRP2 gene during porcine skeletal muscle development.
Abstract Secreted frizzled-related protein 2 (SFRP2), a member of the SFRPs family, is associated with cell growth and differentiation in myogenesis. Our previous study suggested that SFRP2 was a potential target of microRNA (miRNA)-1/206, which was considered as myomiRs. To further explore the biological function and regulation mechanisms of the SFRP2 gene in porcine skeletal muscle development, we first analyzed the sequence structure of the porcine SFRP2 gene. Subsequently, we detected its tissue distribution in adult Tongcheng pigs (a Chinese indigenous breed) and investigated its dynamic expression in developmental skeletal muscle (13 prenatal and 7 postnatal time points) in Tongcheng pigs. An interaction analysis between SFRP2 and myomiRs was also performed. The results showed that the expression pattern of the SFRP2 varied greatly across diverse tissues. It exhibited abundant expression in prenatal skeletal muscle and peaked at 55 days post coitus (E55), and had a lower expression in postnatal skeletal muscle, indicating that the SFRP2 gene might affect porcine embryonic skeletal muscle development. Co-expression analysis revealed that the expression levels of SFRP2 correlated negatively with miRNA-1 (r=–0.570, P-value=0.009) and miRNA-206 (r=–0.546, P-value=0.013), but positively with SFRP1 (r=0.613, P-value=0.004). The bioinformatics analysis and dual luciferase assay verified that the SFRP2 was a putative target of miRNA-1/206 in pigs. Therefore, this study is helpful for understanding the biological function and molecular regulation of the SFRP2 gene during porcine skeletal muscle development.
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Received: 15 October 2014
Accepted:
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| Fund: This study was supported by the National Key Project (2015ZX08009-001), the National Basic Research Program of China (2012CB124706-6), the National Natural Science Foundation of China (31330074, 31171192) and the Agricultural Science and Technology Innovation Program, China (ASTIP-IAS05). |
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Corresponding Authors:
ZHOU Rong, Tel/Fax: +86-10-62813339,E-mail: zhourong03@caas.cn
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| About author: MA Yan-jiao, E-mail: 252076890@qq.com;* These authors contributed equally to this study. |
Cite this article:
MA Yan-jiao, YANG Ya-lan, SUN Wei, ZHOU Rong, LI Kui, TANG Zhong-lin.
2016.
SFRP2 affects prenatal muscle development and is regulated by microRNA-1/206 in pigs. Journal of Integrative Agriculture, 15(1): 153-161.
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| Aubert J, Dunstan H, Chambers I, Smith A. 2002. Functionalgene screening in embryonic stem cells implicates Wntantagonism in neural differentiation. Nature Biotechnology,20, 1240-1245Bafico A, Gazit A, Pramila T, Finch P W, Yaniv A, Aaronson SA. 1999. Interaction of frizzled related protein (FRP) withWnt ligands and the frizzled receptor suggests alternativemechanisms for FRP inhibition of Wnt signaling. Journal ofBiological Chemistry, 274, 16180-16187Bartel D P. 2004. MicroRNAs: Genomics, biogenesis,mechanism, and function. Cell, 116, 281-297Betel D, Koppal A, Agius P, Sander C, Leslie C. 2010.Comprehensive modeling of microRNA targets predictsfunctional non-conserved and non-canonical sites. GenomeBiology, 11, R90.Brophy P D, Lang K M, Dressler G R. 2003. The secretedfrizzled related protein 2 (SFRP2) gene is a target of thePax2 transcription factor. Journal of Biological Chemistry,278, 52401-52405Chen J F, Tao Y, Li J, Deng Z, Yan Z, Xiao X, Wang D Z. 2010.microRNA-1 and microRNA-206 regulate skeletal musclesatellite cell proliferation and differentiation by repressingPax7. Journal of Cell Biology, 190, 867-879Deb A, Davis B H, Guo J, Ni A, Huang J, Zhang Z, Mu H, DzauV J. 2008. SFRP2 regulates cardiomyogenic differentiationby inhibiting a positive transcriptional autofeedback loop ofWnt3a. Stem Cells, 26, 35-44Descamps S, Arzouk H, Bacou F, Bernardi H, Fedon Y,Gay S, Reyne Y, Rossano B, Levin J. 2008. Inhibition ofmyoblast differentiation by Sfrp1 and Sfrp2. Cell and TissueResearch, 332, 299-306George S J. 2008. Wnt pathway: A new role in regulation ofinflammation. Arteriosclerosis, Thrombosis, and VascularBiology, 28, 400-402He W, Zhang L, Ni A, Zhang Z, Mirotsou M, Mao L, Pratt R E,Dzau V J. 2010. Exogenously administered secreted frizzledrelated protein 2 (Sfrp2) reduces fibrosis and improvescardiac function in a rat model of myocardial infarction.Proceedings of the National Academy of Sciences of theUnited States of America, 107, 21110-21115He L, Hannon G J. 2004. MicroRNAs: small RNAs with a big rolein gene regulation. Nature Reviews Genetics, 5, 522-531Heintzman N D, Hon G C, Hawkins R D, Kheradpour P, StarkA, Harp L F, Ye Z, Lee L K, Stuart R K, Ching C W. 2009.Histone modifications at human enhancers reflect globalcell-type-specific gene expression. Nature, 459, 108-112Hou X, Tang Z, Liu H, Wang N, Ju H, Li K. 2012. Discoveryof microRNAs associated with myogenesis by deepsequencing of serial developmental skeletal muscles inpigs. PLOS ONE, 7, e52123.Jaenisch R, Bird A. 2003. Epigenetic regulation of geneexpression: How the genome integrates intrinsic andenvironmental signals. Nature Genetics, 33, 245-254Jones S E, Jomary C. 2002. Secreted Frizzled-related proteins:Searching for relationships and patterns. Bioessays, 24,811-820Katoh M, Katoh M. 2007. WNT signaling pathway and stemcell signaling network. Clinical Cancer Research, 13,4042-4045Kawano Y, Kypta R. 2003. Secreted antagonists of theWnt signalling pathway. Journal of Cell Science, 116,2627-2634Kloosterman W P, Plasterk R H. 2006. The diverse functionsof microRNAs in animal development and disease.Developmental Cell, 11, 441-450Ladher R K, Church V L, Allen S, Robson L, Abdelfattah A,Brown N A, Hattersley G, Rosen V, Luyten F P, Dale L,Francis-West P H. 2000. Cloning and expression of theWnt antagonists Sfrp-2 and Frzb during chick development. Developmental Biology, 218, 183-198Levin J M, El Andalousi R A B, Dainat J, Reyne Y, Bacou F.2001. SFRP2 expression in rabbit myogenic progenitor cellsand in adult skeletal muscles. Journal of Muscle Research& Cell Motility, 22, 361-369Lewis B P, Burge C B, Bartel D P. 2005. Conserved seedpairing, often flanked by adenosines, indicates thatthousands of human genes are microRNA targets. Cell,120, 15-20Lin C T, Lin Y T, Kuo T F. 2007. Investigation of mRNAexpression for secreted frizzled-related protein 2 (sFRP2) inchick embryos. Journal of Reproduction and Development,53, 801-810Mccarthy J J. 2008. MicroRNA-206: The skeletal musclespecificmyomiR. Biochimica et Biophysica Acta, 1779,682-691Mccarthy J J, Esser K A. 2007. MicroRNA-1 and microRNA-133a expression are decreased during skeletal musclehypertrophy. Journal of Applied Physiology, 102, 306-313Melkonyan H S, Chang W C, Shapiro J P, Mahadevappa M,Fitzpatrick P A, Kiefer M C, Tomei L D, Umansky S R. 1997.SARPs: A family of secreted apoptosis-related proteins.Proceedings of the National Academy of Sciences of theUnited States of America, 94, 13636-13641Mukherji S, Ebert M S, Zheng G X, Tsang J S, Sharp P A, VanOudenaarden A. 2011. MicroRNAs can generate thresholdsin target gene expression. Nature Genetics, 43, 854-859Rattner A, Hsieh J C, Smallwood P M, Gilbert D J, CopelandN G, Jenkins N A, Nathans J. 1997. A family of secretedproteins contains homology to the cysteine-rich ligandbindingdomain of frizzled receptors. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 94, 2859-2863Reya T, Clevers H. 2005. Wnt signalling in stem cells andcancer. Nature, 434, 843-850Ritchie W, Rajasekhar M, Flamant S, Rasko J E. 2009.Conserved expression patterns predict microRNA targets.PLoS Computational Biology, 5, e1000513.Suzuki H, Toyota M, Caraway H, Gabrielson E, Ohmura T,Fujikane T, Nishikawa N, Sogabe Y, Nojima M, Sonoda T.2008. Frequent epigenetic inactivation of Wnt antagonistgenes in breast cancer. British Journal of Cancer, 98,1147-1156Tamura K, Peterson D, Peterson N, Stecher G, Nei M, KumarS. 2011. MEGA5: Molecular evolutionary genetics analysisusing maximum likelihood, evolutionary distance, andmaximum parsimony methods. Molecular Biology andEvolution, 28, 2731-2739Tang Z, Liang R, Zhao S, Wang R, Huang R, Li K. 2014. CNN3is regulated by microRNA-1 during muscle developmentin pigs. International Journal of Biological Sciences, 10,377-385Vinson C R, Conover S, Adler P N. 1989. A Drosophila tissuepolarity locus encodes a protein containing seven potentialtransmembrane domains. Nature, 338, 263-264Wigmore P M, Stickland N C. 1983. Muscle development inlarge and small pig fetuses. Journal of Anatomy, 137,235-245Xu Q, D’amore P A, Sokol S Y. 1998. Functional andbiochemical interactions of Wnts with FrzA, a secreted Wntantagonist. Development, 125, 4767-4776Yang Y, Li Y, Liang R, Zhou R, Ao H, Mou Y, Yang S, Tang Z,Li K. 2014. Dynamic expression of microRNA-127 duringporcine prenatal and postnatal skeletal muscle development.Journal of Integrative Agriculture, 13, 1331-1339Yang Y , Sun W, Wang R, Lei C , Zhou R, Tang Z , Li K. 2015.Wnt antagonist, secreted frizzled-related protein 1, isinvolved in prenatal skeletal muscle development and isa target of miRNA-1/206 in pigs. BMC Molecular Biology,16, 4.Zhang J, Ying Z Z, Tang Z L, Long L Q, Li K. 2012. MicroRNA-148a promotes myogenic differentiation by targeting theROCK1 gene. The Journal of Biological Chemistry, 287,21093-21101Zhao S, Zhang J, Hou X, Zan L, Wang N, Tang Z, Li K. 2012.OLFML3 expression is decreased during prenatal muscledevelopment and regulated by microRNA-155 in pigs.International Journal of Biological Sciences, 8, 459-469 |
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