Wnt antagonist, secreted frizzled-related protein 1, is involved in prenatal skeletal muscle development and is a target of miRNA-1/206 in pigs

BMC Molecular Biology

Kui Li¹  Zhonglin Tang¹  Rong Zhou²  Chuzhao Lei³  Ruiqi Wang²  Wei Sun³  Yalan Yang¹ 

[1] Agricultural Genome Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, P.R. China;Key Laboratory of Farm Animal Genetic Resources and Germplasm Innovation of Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China;College of Animal Science and Technology, Northwest A & F University, No. 22 Xinong Road, Yangling, 712100, Shanxi, P.R. China

关键词: Pig;    Development;    Skeletal muscle;    miRNA-1;    miRNA-206;    SFRP1;   

Others  :  1137772
DOI  :  10.1186/s12867-015-0035-7

 received in 2014-10-29, accepted in 2015-02-19,  发布年份 2015

【 摘 要 】

Background

The Wnt signaling pathway is involved in the control of cell proliferation and differentiation during skeletal muscle development. Secreted frizzled-related proteins (SFRPs), such as SFRP1, function as inhibitors of Wnt signaling. MicroRNA-1/206(miRNA-1/206) is specifically expressed in skeletal muscle and play a critical role in myogenesis. The miRNA-mRNA profiles and bioinformatics study suggested that the SFRP1 gene was potentially regulated by miRNA-1/206 during porcine skeletal muscle development.

Methods

To understand the function of SFRP1 and miRNA-1/206 in swine myogenesis, we first predicted the targets of miRNA-1/206 with the TargetScan and PicTar programs, and analyzed the molecular characterization of the porcine SFRP1 gene. We performed a temporal-spatial expression analysis of SFRP1 mRNA and miRNA-206 in Tongcheng pigs (a Chinese indigenous breed) by quantitative real-time polymerase chain reaction, and conducted the co-expression analyses of SFRP1 and miRNA-1/206. Subsequently, the interaction between SFRP1 and miRNA-1/206 was validated via dual luciferase and Western blot assays.

Results

The bioinformatics analysis predicted SFRP1 to be a target of miRNA-1/206. The expression level of the SFRP1 was highly varied across numerous pig tissues and it was down-regulated during porcine skeletal muscle development. The expression level of the SFRP1 was significantly higher in the embryonic skeletal compared with postnatal skeletal muscle, whereas miR-206 showed the inverse pattern of expression. A significant negative correlation was observed between the expression of miR-1/206 and SFRP1 during porcine skeletal muscle development (p <0.05). Dual luciferase assay and Western-blot results demonstrated that SFRP1 was a target of miR-1/206 in porcine iliac endothelial cells.

Conclusions

Our results indicate that the SFRP1 gene is regulated by miR-1/206 and potentially affects skeletal muscle development. These findings increase understanding of the biological functions and the regulation of the SFRP1 gene in mammals.

【 授权许可】

   
2015 Yang et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]von Maltzahn J, Chang NC, Bentzinger CF, Rudnicki MA: Wnt signaling in myogenesis. Trends Cell Biol 2012, 22(11):602-9.
• [2]Cisternas P, Henriquez JP, Brandan E, Inestrosa NC: Wnt signaling in skeletal muscle dynamics: myogenesis, neuromuscular synapse and fibrosis. Mol Neurobiol 2014, 49(1):574-89.
• [3]Ridgeway AG, Petropoulos H, Wilton S, Skerjanc IS: Wnt signaling regulates the function of MyoD and myogenin. J Biol Chem 2000, 275(42):32398-405.
• [4]Rudnicki MA, Le Grand F, McKinnell I, Kuang S: The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 2008, 73:323-31.
• [5]Vertino AM, Taylor-Jones JM, Longo KA, Bearden ED, Lane TF, McGehee RE Jr, et al.: Wnt10b deficiency promotes coexpression of myogenic and adipogenic programs in myoblasts. Mol Biol Cell 2005, 16(4):2039-48.
• [6]Otto A, Schmidt C, Luke G, Allen S, Valasek P, Muntoni F, et al.: Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J Cell Sci 2008, 121(Pt 17):2939-50.
• [7]Rattner A, Hsieh JC, Smallwood PM, Gilbert DJ, Copeland NG, Jenkins NA, et al.: A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci U S A 1997, 94(7):2859-63.
• [8]Xu Q, D'Amore PA, Sokol SY: Functional and biochemical interactions of Wnts with FrzA, a secreted Wnt antagonist. Development 1998, 125(23):4767-76.
• [9]Jones SE, Jomary C: Secreted Frizzled-related proteins: searching for relationships and patterns. Bioessays 2002, 24(9):811-20.
• [10]Chen Y, Stump RJ, Lovicu FJ, McAvoy JW: Expression of Frizzleds and secreted frizzled-related proteins (Sfrps) during mammalian lens development. Int J Dev Biol 2004, 48(8–9):867-77.
• [11]Lavergne E, Hendaoui I, Coulouarn C, Ribault C, Leseur J, Eliat PA, et al.: Blocking Wnt signaling by SFRP-like molecules inhibits in vivo cell proliferation and tumor growth in cells carrying active beta-catenin. Oncogene 2010, 30(4):423-33.
• [12]Descamps S, Arzouk H, Bacou F, Bernardi H, Fedon Y, Gay S, et al.: Inhibition of myoblast differentiation by Sfrp1 and Sfrp2. Cell Tissue Res 2008, 332(2):299-306.
• [13]Ezan J, Leroux L, Barandon L, Dufourcq P, Jaspard B, Moreau C, et al.: FrzA/sFRP-1, a secreted antagonist of the Wnt-Frizzled pathway, controls vascular cell proliferation in vitro and in vivo. Cardiovasc Res 2004, 63(4):731-8.
• [14]Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-97.
• [15]He L, Hannon GJ: MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004, 5(7):522-31.
• [16]Carrington JC, Ambros V: Role of microRNAs in plant and animal development. Science 2003, 301(5631):336-8.
• [17]Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al.: Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008, 18(10):997-1006.
• [18]Ren J, Huang HJ, Gong Y, Yue S, Tang LM, Cheng SY: MicroRNA-206 suppresses gastric cancer cell growth and metastasis. Cell Biosci 2014, 4:26. BioMed Central Full Text
• [19]Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I: MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008, 455(7216):1124-8.
• [20]Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, et al.: miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A 2005, 102(39):13944-9.
• [21]Krutzfeldt J, Stoffel M: MicroRNAs: a new class of regulatory genes affecting metabolism. Cell Metab 2006, 4(1):9-12.
• [22]Kloosterman WP, Plasterk RH: The diverse functions of microRNAs in animal development and disease. Dev Cell 2006, 11(4):441-50.
• [23]McCarthy JJ: MicroRNA-206: the skeletal muscle-specific myomiR. Biochim Biophys Acta 2008, 1779(11):682-91.
• [24]McCarthy JJ, Esser KA: MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J Appl Physiol 2007, 102(1):306-13.
• [25]Xu C, Lu Y, Pan Z, Chu W, Luo X, Lin H, et al.: The muscle-specific microRNAs miR-1 and miR-133 produce opposing effects on apoptosis by targeting HSP60, HSP70 and caspase-9 in cardiomyocytes. J Cell Sci 2007, 120(Pt 17):3045-52.
• [26]Baskerville S, Bartel DP: Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005, 11(3):241-7.
• [27]Chen JF, Tao Y, Li J, Deng Z, Yan Z, Xiao X, et al.: microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J Cell Biol 2010, 190(5):867-79.
• [28]Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A: Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol 2006, 174(5):677-87.
• [29]Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, et al.: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006, 38(2):228-33.
• [30]Hou X, Tang Z, Liu H, Wang N, Ju H, Li K: Discovery of MicroRNAs associated with myogenesis by deep sequencing of serial developmental skeletal muscles in pigs. PLoS One 2012, 7(12):e52123.
• [31]da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
• [32]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-9.
• [33]Kozomara A, Griffiths-Jones S: miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014, 42(Database issue):D68-73.
• [34]Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, et al.: Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 2010, 391(1):73-7.
• [35]Tang Z, Liang R, Zhao S, Wang R, Huang R, Li K: CNN3 Is Regulated by microRNA-1 during Muscle Development in Pigs. Int J Biol Sci 2014, 10(4):377-85.
• [36]Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, et al.: The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 2007, 13(4):486-91.
• [37]Taulli R, Bersani F, Foglizzo V, Linari A, Vigna E, Ladanyi M, et al.: The muscle-specific microRNA miR-206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation. J Clin Invest 2009, 119(8):2366-78.
• [38]Cadigan KM, Nusse R: Wnt signaling: a common theme in animal development. Genes Dev 1997, 11(24):3286-305.
• [39]van Amerongen R, Berns A: Knockout mouse models to study Wnt signal transduction. Trends Genet 2006, 22(12):678-89.
• [40]Tsivitse S: Notch and Wnt signaling, physiological stimuli and postnatal myogenesis. Int J Biol Sci 2010, 6(3):268-81.
• [41]Steelman CA, Recknor JC, Nettleton D, Reecy JM: Transcriptional profiling of myostatin-knockout mice implicates Wnt signaling in postnatal skeletal muscle growth and hypertrophy. FASEB J 2006, 20(3):580-2.
• [42]Zhao P, Hoffman EP: Embryonic myogenesis pathways in muscle regeneration. Dev Dyn 2004, 229(2):380-92.
• [43]Svensson A, Norrby M, Libelius R, Tagerud S: Secreted frizzled related protein 1 (Sfrp1) and Wnt signaling in innervated and denervated skeletal muscle. J Mol Histol 2008, 39(3):329-37.
• [44]Finch PW, He X, Kelley MJ, Uren A, Schaudies RP, Popescu NC, et al.: Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proc Natl Acad Sci U S A 1997, 94(13):6770-5.
• [45]Melkonyan HS, Chang WC, Shapiro JP, Mahadevappa M, Fitzpatrick PA, Kiefer MC, et al.: SARPs: a family of secreted apoptosis-related proteins. Proc Natl Acad Sci U S A 1997, 94(25):13636-41.
• [46]Picard B, Lefaucheur L, Berri C, Duclos MJ: Muscle fibre ontogenesis in farm animal species. Reprod Nutr Dev 2002, 42(5):415-31.
• [47]Lefaucheur L, Edom F, Ecolan P, Butler-Browne GS: Pattern of muscle fiber type formation in the pig. Dev Dyn 1995, 203(1):27-41.
• [48]Wigmore PM, Stickland NC: Muscle development in large and small pig fetuses. J Anat 1983, 137(Pt 2):235-45.
• [49]Cossu G, Borello U: Wnt signaling and the activation of myogenesis in mammals. EMBO J 1999, 18(24):6867-72.
• [50]Nagalla S, Shaw C, Kong X, Kondkar AA, Edelstein LC, Ma L, et al.: Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 2011, 117(19):5189-97.
• [51]Ponsuksili S, Du Y, Hadlich F, Siengdee P, Murani E, Schwerin M, et al.: Correlated mRNAs and miRNAs from co-expression and regulatory networks affect porcine muscle and finally meat properties. BMC Genomics 2013, 14:533. BioMed Central Full Text
• [52]Zhao S, Zhang J, Hou X, Zan L, Wang N, Tang Z, et al.: OLFML3 expression is decreased during prenatal muscle development and regulated by microRNA-155 in pigs. Int J Biol Sci 2012, 8(4):459-69.