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Temporal correlation between differentiation factor expression and microRNAs in Holstein bovine skeletal muscle

Published online by Cambridge University Press:  13 July 2016

S. Miretti ,
M. G. Volpe ,
E. Martignani ,
P. Accornero  and
M. Baratta
S. Miretti*
Affiliation:
Department of Veterinary Science, University of Torino, Largo P. Braccini 2, 10095 Grugliasco, Italy
M. G. Volpe
Affiliation:
Department of Veterinary Science, University of Torino, Largo P. Braccini 2, 10095 Grugliasco, Italy
E. Martignani
Affiliation:
Department of Veterinary Science, University of Torino, Largo P. Braccini 2, 10095 Grugliasco, Italy
P. Accornero
Affiliation:
Department of Veterinary Science, University of Torino, Largo P. Braccini 2, 10095 Grugliasco, Italy
M. Baratta
Affiliation:
Department of Veterinary Science, University of Torino, Largo P. Braccini 2, 10095 Grugliasco, Italy
*
†E-mail: [email protected]
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Abstract

Satellite cells are adult stem cells located between the basal lamina and sarcolemma of muscle fibers. Under physiological conditions, satellite cells are quiescent, but they maintain a strong proliferative potential and propensity to differentiate, which underlies their critical role in muscle preservation and growth. MicroRNAs (miRNAs) play essential roles during animal development as well as in stem cell self-renewal and differentiation regulation. MiRNA-1, miRNA-133a and miRNA-206 are closely related muscle-specific miRNAs, and are thus defined myomiRNAs. MyomiRNAs are integrated into myogenic regulatory networks. Their expression is under the transcriptional and post-transcriptional control of myogenic factors and, in turn, they exhibit widespread control of muscle gene expression. Very little information is available about the regulation and behavior of satellite cells in large farm animals, in particular during satellite cell differentiation. Here, we study bovine satellite cells (BoSCs) undergoing a differentiation process and report the expression pattern of selected genes and miRNAs involved. Muscle samples of longissimus thoracis from Holstein adult male animals were selected for the collection of satellite cells. All satellite cell preparations demonstrated myotube differentiation. To characterize the dynamics of several transcription factors expressed in BoSCs, we performed real-time PCR on complementary DNA generated from the total RNA extracted from BoSCs cultivated in growth medium (GM) or in differentiation medium (DM) for 4 days. In the GM condition, BoSCs expressed the satellite cell lineage markers as well as transcripts for the myogenic regulatory factors. At the time of isolation from muscle, PAX7 was expressed in nearly 100% of BoSCs; however, its messenger RNA (mRNA) levels dramatically decreased between 3 and 6 days post isolation (P<0.01). MyoD mRNA levels increased during the 1st day of cultivation in DM (day 7; P<0.02), showing a gradual activation of the myogenic gene program. During the subsequent 4 days of culture in DM, several tested genes, including MRF4, MYOG, MEF2C, TMEM8C, DES and MYH1, showed increased expression (P<0.05), and these levels remained high throughout the culture period investigated. Meanwhile, the expression of genes involved in the differentiation process also miRNA-1, miRNA-133a and miRNA-206 were strongly up-regulated on the 1st day in DM (day 7; P<0.05). Analysis revealed highly significant correlations between myomiRNAs expression and MEF2C, MRF4, TMEM8C, DES and MYH1 gene expression (P<0.001). Knowledge about the transcriptional changes correlating with the growth and differentiation of skeletal muscle fibers could be helpful for developing strategies to improve production performance in livestock.

Keywords

cattlesatellite cellsdifferentiationmicroRNAtranscription factors
Type
Research Article
Information
animal , Volume 11 , Issue 2 , February 2017 , pp. 227 - 235
Copyright
© The Animal Consortium 2016 

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References

Beauchamp, JR, Heslop, L, Yu, DS, Tajbakhsh, S, Kelly, RG, Wernig, A, Buckingham, ME, Partridge, TA and Zammit, PS 2000. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. The Journal of Cell Biology 151, 1221–1234.Google Scholar
Biressi, S and Rando, TA 2010. Heterogeneity in the muscle satellite cell population. Seminars in Cell and Developmental Biology 21, 845–854.CrossRefGoogle ScholarPubMed
Boldrin, L, Muntoni, F and Morgan, JE 2010. Are human and mouse satellite cells really the same? The Journal of Histochemistry Cytochemistry 58, 941–955.CrossRefGoogle ScholarPubMed
Boutz, PL, Chawla, G, Stoilov, P and Black, DL 2007. MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Genes and Development 21, 71–84.CrossRefGoogle ScholarPubMed
Brack, AS and Rando, TA 2012. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 10, 504–514.Google Scholar
Braun, T and Gautel, M 2011. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nature Reviews Molecular Cell Biology 12, 349–361.Google Scholar
Chen, JF, Mandel, EM, Thomson, JM, Wu, Q, Callis, TE, Hammond, SM, Conlon, FL and Wang, DZ 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nature Genetics 38, 228–233.Google Scholar
Collins, CA, Olsen, I, Zammit, PS, Heslop, L, Petrie, A, Partridge, TA and Morgan, JE 2005. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289–301.Google Scholar
Crippa, S, Cassano, M and Sampaolesi, M 2012. Role of miRNAs in muscle stem cell biology: proliferation, differentiation and death. Current Pharmaceutical Design 18, 1718–1729.Google Scholar
Crist, CG, Montarras, D and Buckingham, M 2012. Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11, 118–126.CrossRefGoogle ScholarPubMed
Dai, Y, Wang, YM, Zhang, WR, Liu, XF, Li, X, Ding, XB and Guo, H 2016. The role of microRNA-1 and microRNA-206 in the proliferation and differentiation of bovine skeletal muscle satellite cells. In Vitro Cellular and Developmental Biology Animal 52, 27–34.Google Scholar
Gagan, J, Dey, BK, Layer, R, Yan, Z and Dutta, A 2012. Notch3 and Mef2c proteins are mutually antagonistic via Mkp1 protein and miR-1/206 microRNAs in differentiating myoblasts. The Journal of Biological Chemistry 287, 40360–40370.CrossRefGoogle ScholarPubMed
Günther, S, Kim, J, Kostin, S, Lepper, C, Fan, CM and Braun, T 2013. Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells. Cell Stem Cell 13, 590–601.Google Scholar
Hopwood, ND, Pluck, A and Gurdon, JB 1991. Xenopus Myf-5 marks early muscle cells and can activate muscle genes ectopically in early embryos. Development 111, 551–560.Google Scholar
Kim, HK, Lee, YS, Sivaprasad, U, Malhotra, A and Dutta, A 2006. Muscle-specific microRNA miR-206 promotes muscle differentiation. The Journal of Cell Biology 174, 677–687.Google Scholar
Kuang, S, Charge, SB, Seale, P, Huh, M and Rudnicki, MA 2006. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. The Journal of Cell Biology 172, 103–113.Google Scholar
Landemaine, A, Rescan, PY and Gabillard, JC 2014. Myomaker mediates fusion of fast myocytes in zebrafish embryos. Biochemical and Biophysical Research Communications 451, 480–484.Google Scholar
Lepper, C, Conway, SJ and Fan, CM 2009. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627–631.Google Scholar
Li, J, Gonzalez, JM, Walker, DK, Hersom, MJ, Ealy, AD and Johnson, SE 2011. Evidence of heterogeneity within bovine satellite cells isolated from young and adult animals. Journal of Animal Science 89, 1751–1757.Google Scholar
Li, J and Johnson, SE 2013. Ephrin-A5 promotes bovine muscle progenitor cell migration before mitotic activation. Journal Animal Science 91, 1086–1093.Google Scholar
Luo, W, Li, E, Nie, Q and Zhang, X 2015. Myomaker, regulated by MYOD, MYOG and miR-140-3p, promotes chicken myoblast fusion. International Journal of Molecular Sciences 16, 26186–26201.Google Scholar
Mauro, A 1961. Satellite cell of skeletal muscle fibers. The Journal of Biophysical and Biochemical Cytology 9, 493–495.Google Scholar
McCarthy, JJ 2008. MicroRNA-206: the skeletal muscle-specific myomiR. Biochimica et Biophysica Acta 1779, 682–691.Google Scholar
Millay, DP, O’Rourke, JR, Sutherland, LB, Bezprozvannaya, S, Shelton, JM, Bassel-Duby, R and Olson, EN 2013. Myomaker is a membrane activator of myoblast fusion and muscle formation. Nature 499, 301–305.Google Scholar
Miretti, S, Martignani, E, Accornero, P and Baratta, M 2013. Functional effect of mir-27b on myostatin expression: a relationship in Piedmontese cattle with double-muscled phenotype. BMC Genomics 14, 194.Google Scholar
Miretti, S, Martignani, E, Taulli, R, Bersani, F, Accornero, P and Baratta, M 2011. Differential expression of microRNA-206 in skeletal muscle of female Piedmontese and Friesian cattle. The Veterinary Journal 190, 412–413.Google Scholar
Motohashi, N and Asakura, A 2014. Muscle satellite cell heterogeneity and self-renewal. Frontiers in Cell and Developmental Biology 2, 1.Google Scholar
Muroya, S, Taniguchi, M, Shibata, M, Oe, M, Ojima, K, Nakajima, I and Chikuni, K 2013. Profiling of differentially expressed microRNA and the bioinformatic target gene analyses in bovine fast- and slow-type muscles by massively parallel sequencing. Journal of Animal Science 91, 90–103.Google Scholar
Pabinger, S, Thallinger, GG, Snajder, R, Eichhorn, H, Rader, R and Trajanoski, Z 2009. QPCR: application for real-time PCR data management and analysis. BMC Bioinformatics 10, 268.Google Scholar
Powell, DJ, McFarland, DC, Cowieson, AJ, Muir, WI and Velleman, SG 2014. The effect of nutritional status on myogenic gene expression of satellite cells derived from different muscle types. Poultry Science 93, 2278–2288.Google Scholar
Rao, PK, Kumar, RM, Farkhondeh, M, Baskerville, S and Lodish, HF 2006. Myogenic factors that regulate expression of muscle-specific microRNAs. Proceedings of the National Academy of Sciences of the United States of America 103, 8721–8726.Google Scholar
Tajbakhsh, S and Buckingham, M 2000. The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. Current Topics in Developmental Biology 48, 225–268.CrossRefGoogle ScholarPubMed
Theil, PK, Sørensen, IL, Nissen, PM and Oksbjerg, N 2006a. Temporal expression of growth factor genes of primary porcine satellite cells during myogenesis. Animal Science Journal 77, 330–337.Google Scholar
Theil, PK, Sørensen, IL, Therkildsen, M and Oksbjerg, N 2006b. Changes in proteolytic enzyme mRNAs relevant for meat quality during myogenesis of primary porcine satellite cells. Meat Science 73, 335–343.Google Scholar
Wang, X, Gu, Z and Jiang, H 2013. MicroRNAs in farm animals. Animal 7, 1567–1575.Google Scholar
Wang, YM, Ding, XB, Dai, Y, Liu, XF, Guo, H and Zhang, Y 2015. Identification and bioinformatics analysis of miRNAs involved in bovine skeletal muscle satellite cell myogenic differentiation. Molecular and Cellular Biochemistry 404, 113–122.Google Scholar
Zhang, WW, Tong, HL, Sun, XF, Hu, Q, Yang, Y, Li, SF, Yan, YQ and Li, GP 2015. Identification of miR-2400 gene as a novel regulator in skeletal muscle satellite cells proliferation by targeting MYOG gene. Biochemical and Biophysical Research Communications 463, 624–631.Google Scholar
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