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Genes2022; 13(10); doi: 10.3390/genes13101836

MSTN Regulatory Network in Mongolian Horse Muscle Satellite Cells Revealed with miRNA Interference Technologies.

Abstract: Myostatin (MSTN), a member of the transforming growth factor-β superfamily, inhibits the activation of muscle satellite cells. However, the role and regulatory network of MSTN in equine muscle cells are not well understood yet. We discovered that MSTN knockdown significantly reduces the proliferation rate of equine muscle satellite cells. In addition, after the RNA sequencing of equine satellite cells transfected with MSTN-interference plasmid and control plasmid, an analysis of the differentially expressed genes was carried out. It was revealed that MSTN regulatory networks mainly involve genes related to muscle function and cell-cycle regulation, and signaling pathways, such as Notch, MAPK, and WNT. Subsequent real-time PCR in equine satellite cells and immunohistochemistry on newborn and adult muscle also verified the MSTN regulatory network found in RNA sequencing analysis. The results of this study provide new insight into the regulatory mechanism of equine MSTN.
Publication Date: 2022-10-11 PubMed ID: 36292721PubMed Central: PMC9601437DOI: 10.3390/genes13101836Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

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The study focuses on understanding the role of Myostatin (MSTN), a protein that inhibits muscle satellite cell activation, in Mongolian horse muscle cells. Researchers found that reducing MSTN levels slows down the proliferation of these muscle cells, and discovered pathways and genes that MSTN might control, offering new insight into its regulatory mechanisms in horses.

Research Background and Purpose

  • Myostatin (MSTN) is a protein belonging to the transforming growth factor-beta (TGF-β) family, known to inhibit the activation of muscle satellite cells, which are important for muscle development and repair.
  • The role and regulatory function of MSTN in equine muscle cells, particularly in Mongolian horses, is not completely understood.
  • The researchers sought to investigate the effects of MSTN depletion on equine muscle cell proliferation and uncover the underlying regulatory network.

Research Methods and Findings

  • The researchers used RNA interference technologies to silence the MSTN gene in equine muscle satellite cells.
  • They observed a significant reduction in the proliferation rate of these cells following MSTN knockdown (gene silencing), indicating its importance for cell growth and division.
  • RNA sequencing of MSTN-interfered and control satellite cells allowed researchers to identify differentially expressed genes due to MSTN manipulation.
  • The data revealed that MSTN regulatory networks are mostly associated with genes involved in muscle function and cell-cycle regulation, as well as signaling pathways such as the Notch, MAPK, and WNT pathways.
  • These results were further validated with real-time PCR on equine satellite cells and immunohistochemistry studies on newborn and adult muscle tissues.

Significance of the Study

  • This study offers fresh insights into the complex function of MSTN in equine muscle satellite cells by portraying its potential regulatory network.
  • The findings could prove beneficial for understanding and potentially manipulating muscle growth and repair in horses, with possible implications for other species as well.

Cite This Article

APA
Budsuren U, Ulaangerel T, Shen Y, Liu G, Davshilt T, Yi M, Bold D, Zhang X, Bai D, Dorjgotov D, Davaakhuu G, Jambal T, Li B, Du M, Dugarjav M, Bou G. (2022). MSTN Regulatory Network in Mongolian Horse Muscle Satellite Cells Revealed with miRNA Interference Technologies. Genes (Basel), 13(10). https://doi.org/10.3390/genes13101836

Publication

ISSN: 2073-4425
NlmUniqueID: 101551097
Country: Switzerland
Language: English
Volume: 13
Issue: 10

Researcher Affiliations

Budsuren, Undarmaa
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
  • School of Animal Science and Biotechnology, Mongolian University of Life Sciences, Ulaanbaatar 17024, Mongolia.
Ulaangerel, Tseweendolmaa
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Shen, Yingchao
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Liu, Guiqin
  • College of Agronomy and Agricultural Engineering, Liaocheng University, Liaocheng 252000, China.
Davshilt, Toli
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Yi, Minna
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Bold, Demuul
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Zhang, Xinzhuang
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Bai, Dongyi
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Dorjgotov, Dulguun
  • School of Industrial Technology, Mongolian University of Science and Technology, Ulaanbaatar 14191, Mongolia.
Davaakhuu, Gantulga
  • Institute of Biology, Mongolian Academy of Science, Ulaanbaatar 13330, Mongolia.
Jambal, Tuyatsetseg
  • School of Industrial Technology, Mongolian University of Science and Technology, Ulaanbaatar 14191, Mongolia.
Li, Bei
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Du, Ming
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Dugarjav, Manglai
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
Bou, Gerelchimeg
  • Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.

MeSH Terms

  • Horses / genetics
  • Animals
  • Myostatin / genetics
  • Myostatin / metabolism
  • MicroRNAs / genetics
  • Myoblasts / metabolism
  • Muscles / metabolism
  • Transforming Growth Factors

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 60 references
  1. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member.. Nature 1997;387:83–90.
    doi: 10.1038/387083a0pubmed: 9139826google scholar: lookup
  2. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle.. Nat. Genet. 1997;17:71–74.
    doi: 10.1038/ng0997-71pubmed: 9288100google scholar: lookup
  3. Kambadur R, Sharma M, Smith TP, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle.. Genome Res. 1997;7:910–916.
    doi: 10.1101/gr.7.9.910pubmed: 9314496google scholar: lookup
  4. Boman IA, Klemetsdal G, Blichfeldt T, Nafstad O, Vage DI. A frameshift mutation in the coding region of the myostatin gene (MSTN) affects carcass conformation and fatness in Norwegian White Sheep (Ovis aries). Anim. Genet. 2009;40:418–422.
  5. Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh CS, Parker HG, Ostrander EA. A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs.. PLoS Genet. 2007;3:e79.
  6. Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child.. N. Engl. J. Med. 2004;350:2682–2688.
    doi: 10.1056/NEJMoa040933pubmed: 15215484google scholar: lookup
  7. Rooney MF, Hill EW, Kelly VP, Porter RK. The “speed gene” effect of myostatin arises in Thoroughbred horses due to a promoter proximal SINE insertion.. PLoS ONE 2018;13:e0205664.
  8. Hill EW, McGivney BA, Rooney MF, Katz LM, Parnell A, MacHugh DE. The contribution of myostatin (MSTN) and additional modifying genetic loci to race distance aptitude in Thoroughbred horses racing in different geographic regions.. Equine Vet. J. 2019;51:625–633.
    doi: 10.1111/evj.13058pubmed: 30604488google scholar: lookup
  9. Miyata H, Itoh R, Sato F, Takebe N, Hada T, Tozaki T. Effect of Myostatin SNP on muscle fiber properties in male Thoroughbred horses during training period.. J. Physiol. Sci. 2018;68:639–646.
    doi: 10.1007/s12576-017-0575-3pmc: PMC10717627pubmed: 29058242google scholar: lookup
  10. Binns MM, Boehler DA, Lambert DH. Identification of the myostatin locus (MSTN) as having a major effect on optimum racing distance in the Thoroughbred horse in the USA.. Anim. Genet. 2010;41((Suppl. S2)):154–158.
  11. Hill EW, Gu J, Eivers SS, Fonseca RG, McGivney BA, Govindarajan P, Orr N, Katz LM, MacHugh DE. A sequence polymorphism in MSTN predicts sprinting ability and racing stamina in thoroughbred horses.. PLoS ONE 2010;5:e8645.
  12. Tozaki T, Miyake T, Kakoi H, Gawahara H, Sugita S, Hasegawa T, Ishida N, Hirota K, Nakano Y. A genome-wide association study for racing performances in Thoroughbreds clarifies a candidate region near the MSTN gene.. Anim. Genet. 2010;41((Suppl. S2)):28–35.
  13. Moro LN, Viale DL, Baston JI, Arnold V, Suva M, Wiedenmann E, Olguin M, Miriuka S, Vichera G. Generation of myostatin edited horse embryos using CRISPR/Cas9 technology and somatic cell nuclear transfer.. Sci. Rep. 2020;10:15587.
    doi: 10.1038/s41598-020-72040-4pmc: PMC7518276pubmed: 32973188google scholar: lookup
  14. O’Hara V, Cowan A, Riddell D, Massey C, Martin J, Piercy RJ. A highly prevalent SINE mutation in the myostatin (MSTN) gene promoter is associated with low circulating myostatin concentration in Thoroughbred racehorses.. Sci. Rep. 2021;11:7916.
    doi: 10.1038/s41598-021-86783-1pmc: PMC8041750pubmed: 33846367google scholar: lookup
  15. Klein DJ, McKeever KH, Mirek ET, Anthony TG. Metabolomic Response of Equine Skeletal Muscle to Acute Fatiguing Exercise and Training.. Front. Physiol. 2020;11:110.
    doi: 10.3389/fphys.2020.00110pmc: PMC7040365pubmed: 32132934google scholar: lookup
  16. Bentzinger CF, Wang YX, Dumont NA, Rudnicki MA. Cellular dynamics in the muscle satellite cell niche.. EMBO Rep. 2013;14:1062–1072.
    doi: 10.1038/embor.2013.182pmc: PMC3849491pubmed: 24232182google scholar: lookup
  17. Byrne KM, Vierck J, Dodson MV. In vitro model of equine muscle regeneration.. Equine Vet. J. 2000;32:401–405.
    doi: 10.2746/042516400777591020pubmed: 11037261google scholar: lookup
  18. Giordani L, Parisi A, Le Grand F. Satellite Cell Self-Renewal.. Curr. Top. Dev. Biol. 2018;126:177–203.
    pubmed: 29304998
  19. Yin H, Price F, Rudnicki MA. Satellite cells and the muscle stem cell niche.. Physiol. Rev. 2013;93:23–67.
    doi: 10.1152/physrev.00043.2011pmc: PMC4073943pubmed: 23303905google scholar: lookup
  20. Kawai M, Aida H, Hiraga A, Miyata H. Muscle satellite cells are activated after exercise to exhaustion in Thoroughbred horses.. Equine Vet. J. 2013;45:512–517.
    doi: 10.1111/evj.12010pubmed: 23206314google scholar: lookup
  21. Younis A, Siddique MI, Kim CK, Lim KB. RNA Interference (RNAi) Induced Gene Silencing: A Promising Approach of Hi-Tech Plant Breeding.. Int. J. Biol. Sci. 2014;10:1150–1158.
    doi: 10.7150/ijbs.10452pmc: PMC4202031pubmed: 25332689google scholar: lookup
  22. Suravajhala P, Kogelman LJ, Kadarmideen HN. Multi-omic data integration and analysis using systems genomics approaches: Methods and applications in animal production, health and welfare.. Genet. Sel. Evol. 2016;48:38.
    doi: 10.1186/s12711-016-0217-xpmc: PMC4850674pubmed: 27130220google scholar: lookup
  23. Patel AK, Tripathi AK, Patel UA, Shah RK, Joshi CG. Myostatin knockdown and its effect on myogenic gene expression program in stably transfected goat myoblasts.. Vitr. Cell Dev. Biol. Anim. 2014;50:587–596.
    doi: 10.1007/s11626-014-9743-4pubmed: 24682647google scholar: lookup
  24. Magee TR, Artaza JN, Ferrini MG, Vernet D, Zuniga FI, Cantini L, Reisz-Porszasz S, Rajfer J, Gonzalez-Cadavid NF. Myostatin short interfering hairpin RNA gene transfer increases skeletal muscle mass.. J. Gene Med. 2006;8:1171–1181.
    doi: 10.1002/jgm.946pubmed: 16810717google scholar: lookup
  25. Asakura A, Komaki M, Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation.. Differentiation. 2001;68:245–253.
  26. Hernandez-Hernandez JM, Garcia-Gonzalez EG, Brun CE, Rudnicki MA. The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration.. Semin. Cell Dev. Biol. 2017;72:10–18.
  27. Verzola D, Milanesi S, Viazzi F, Ansaldo F, Saio M, Garibaldi S, Carta A, Costigliolo F, Salvidio G, Barisione C. Enhanced myostatin expression and signalling promote tubulointerstitial inflammation in diabetic nephropathy.. Sci. Rep. 2020;10:6343.
    doi: 10.1038/s41598-020-62875-2pmc: PMC7156449pubmed: 32286342google scholar: lookup
  28. Tang L, Gao X, Yang X, Zhang D, Zhang X, Du H, Han Y, Sun L. Combination of Weight-Bearing Training and Anti-MSTN Polyclonal Antibody Improve Bone Quality In Rats.. Int. J. Sport Nutr. Exerc. Metab. 2016;26:516–524.
    doi: 10.1123/ijsnem.2015-0337pubmed: 27098383google scholar: lookup
  29. Seyed Jafari SM, Hunger RE. IHC Optical Density Score: A New Practical Method for Quantitative Immunohistochemistry Image Analysis.. Appl. Immunohistochem. Mol. Morphol. 2017;25:e12–e13.
    doi: 10.1097/PAI.0000000000000370pubmed: 27093452google scholar: lookup
  30. Huang J, Zhao Y, Shiraigol W, Li B, Bai D, Ye W, Daidiikhuu D, Yang L, Jin B, Zhao Q. Analysis of horse genomes provides insight into the diversification and adaptive evolution of karyotype.. Sci. Rep. 2014;4:4958.
    doi: 10.1038/srep04958pmc: PMC4021364pubmed: 24828444google scholar: lookup
  31. Han H, Wallner B, Rigler D, MacHugh DE, Manglai D, Hill EW. Chinese Mongolian horses may retain early domestic male genetic lineages yet to be discovered.. Anim. Genet. 2019;50:399–402.
    doi: 10.1111/age.12780pubmed: 31073991google scholar: lookup
  32. Bou T, Han H, Mongke T, Zhao R, La X, Ding W, Jia Z, Liu H, Tiemuqier A, An T. Fast and slow myofiber-specific expression profiles are affected by noncoding RNAs in Mongolian horses.. Comp. Biochem. Physiol. Part D Genom. Proteom. 2021;41:100942.
    doi: 10.1016/j.cbd.2021.100942pubmed: 34823143google scholar: lookup
  33. Greene EA, Raub RH. Procedures for Harvesting Satellite Cells from Equine Skeletal-Muscle.. J. Equine Vet. Sci. 1992;12:33–35.
  34. Greene EA, Balch SG, Raub RH, Gaughn E. The effect of moderate exercise on equine muscle satellite cells in vitro.. Equine Vet. J. 1995;18:218–222.
  35. Li EW, McKee-Muir OC, Gilbert PM. Cellular Biomechanics in Skeletal Muscle Regeneration.. Curr. Top. Dev. Biol. 2018;126:125–176.
    pubmed: 29304997
  36. Cornelison DD, Wold BJ. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells.. Dev. Biol. 1997;191:270–283.
    doi: 10.1006/dbio.1997.8721pubmed: 9398440google scholar: lookup
  37. Yablonka-Reuveni Z, Rudnicki MA, Rivera AJ, Primig M, Anderson JE, Natanson P. The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD.. Dev. Biol. 1999;210:440–455.
    doi: 10.1006/dbio.1999.9284pmc: PMC5027208pubmed: 10357902google scholar: lookup
  38. Olguin HC, Olwin BB. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: A potential mechanism for self-renewal.. Dev. Biol. 2004;275:375–388.
    doi: 10.1016/j.ydbio.2004.08.015pmc: PMC3322464pubmed: 15501225google scholar: lookup
  39. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells.. Cell. 2000;102:777–786.
    doi: 10.1016/S0092-8674(00)00066-0pubmed: 11030621google scholar: lookup
  40. Mauro A. Satellite cell of skeletal muscle fibers.. J. Biophys. Biochem. Cytol. 1961;9:493–495.
    doi: 10.1083/jcb.9.2.493pmc: PMC2225012pubmed: 13768451google scholar: lookup
  41. Schultz E, Gibson MC, Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: An EM and radioautographic study.. J. Exp. Zool. 1978;206:451–456.
    doi: 10.1002/jez.1402060314pubmed: 712350google scholar: lookup
  42. Matsuoka S, Edwards MC, Bai C, Parker S, Zhang P, Baldini A, Harper JW, Elledge SJ. p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene.. Genes Dev. 1995;9:650–662.
    doi: 10.1101/gad.9.6.650pubmed: 7729684google scholar: lookup
  43. Yu JS, Cui W. Proliferation, survival and metabolism: The role of PI3K/AKT/mTOR signalling in pluripotency and cell fate determination.. Development. 2016;143:3050–3060.
    doi: 10.1242/dev.137075pubmed: 27578176google scholar: lookup
  44. Rodriguez J, Vernus B, Chelh I, Cassar-Malek I, Gabillard JC, Hadj Sassi A, Seiliez I, Picard B, Bonnieu A. Myostatin and the skeletal muscle atrophy and hypertrophy signaling pathways.. Cell Mol. Life Sci. 2014;71:4361–4371.
    doi: 10.1007/s00018-014-1689-xpmc: PMC11113773pubmed: 25080109google scholar: lookup
  45. Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis.. Cell Stem. Cell. 2008;2:50–59.
    doi: 10.1016/j.stem.2007.10.006pubmed: 18371421google scholar: lookup
  46. Fukada S, Higuchi S, Segawa M, Koda K, Yamamoto Y, Tsujikawa K, Kohama Y, Uezumi A, Imamura M, Miyagoe-Suzuki Y. Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody.. Exp. Cell Res. 2004;296:245–255.
    doi: 10.1016/j.yexcr.2004.02.018pubmed: 15149854google scholar: lookup
  47. Fu X, Wang H, Hu P. Stem cell activation in skeletal muscle regeneration.. Cell Mol. Life Sci. 2015;72:1663–1677.
    doi: 10.1007/s00018-014-1819-5pmc: PMC4412728pubmed: 25572293google scholar: lookup
  48. Cheung TH, Rando TA. Molecular regulation of stem cell quiescence.. Nat. Rev. Mol. Cell Biol. 2013;14:329–340.
    doi: 10.1038/nrm3591pmc: PMC3808888pubmed: 23698583google scholar: lookup
  49. Mcfarlane C, Sharma M, Kambadur R. Role of Myostatin in Skeletal Muscle Growth and Development: Implications for Sarcopenia.. 2010. pp. 419–447.
  50. Feng L, Wang X, Lu M, Ming L, Tong H, Li S, Yan Y. Effect of MSTN Propeptide and shRNA Co-expression Vector on Proliferation of Skeletal Muscle Satellite Cells.. J. Northeast. Agric. Univ. (Engl. Ed.) 2014;21:31–38.
  51. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation.. J. Biol. Chem. 2000;275:40235–40243.
    doi: 10.1074/jbc.M004356200pubmed: 10976104google scholar: lookup
  52. Beijersbergen RL, Bernards R. Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins.. Biochim. Biophys. Acta. 1996;1287:103–120.
    doi: 10.1016/0304-419X(96)00002-9pubmed: 8672526google scholar: lookup
  53. McFarlane C, Hui GZ, Amanda WZ, Lau HY, Lokireddy S, Xiaojia G, Mouly V, Butler-Browne G, Gluckman PD, Sharma M. Human myostatin negatively regulates human myoblast growth and differentiation.. Am. J. Physiol. Cell Physiol. 2011;301:C195–C203.
    doi: 10.1152/ajpcell.00012.2011pmc: PMC3129832pubmed: 21508334google scholar: lookup
  54. Spangenburg EE, Chakravarthy MV, Booth FW. p27Kip1: A key regulator of skeletal muscle satellite cell proliferation.. Clin. Orthop. Relat. Res. 2002;403:S221–S227.
  55. Hosoyama T, Nishijo K, Prajapati SI, Li G, Keller C. Rb1 gene inactivation expands satellite cell and postnatal myoblast pools.. J. Biol. Chem. 2011;286:19556–19564.
    doi: 10.1074/jbc.M111.229542pmc: PMC3103335pubmed: 21478154google scholar: lookup
  56. Shea KL, Xiang W, LaPorta VS, Licht JD, Keller C, Basson MA, Brack AS. Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration.. Cell Stem. Cell. 2010;6:117–129.
    doi: 10.1016/j.stem.2009.12.015pmc: PMC2846417pubmed: 20144785google scholar: lookup
  57. Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S. Molecular signature of quiescent satellite cells in adult skeletal muscle.. Stem. Cells. 2007;25:2448–2459.
    doi: 10.1634/stemcells.2007-0019pubmed: 17600112google scholar: lookup
  58. Liu L, Cheung TH, Charville GW, Hurgo BM, Leavitt T, Shih J, Brunet A, Rando TA. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging.. Cell Rep. 2013;4:189–204.
  59. von Maltzahn J, Bentzinger CF, Rudnicki A. Characteristics of Satellite Cells and Multipotent Adult Stem Cells in the Skeletal Muscle.. Stem. Cells Cancer Stem. Cells. 2013;12:63–73.
  60. Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: Molecular regulation of myogenesis.. Cold Spring Harb. Perspect. Biol. 2012;4:a008342.
    doi: 10.1101/cshperspect.a008342pmc: PMC3281568pubmed: 22300977google scholar: lookup