Skip to main content
SpringerLink
Log in

Muscle Stem Cells: A Model System for Adult Stem Cell Biology

  • Protocol
  • First Online:
Muscle Stem Cells

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1556))

Abstract

Skeletal muscle stem cells, originally termed satellite cells for their position adjacent to differentiated muscle fibers, are absolutely required for the process of skeletal muscle repair and regeneration. In the last decade, satellite cells have become one of the most studied adult stem cell systems and have emerged as a standard model not only in the field of stem cell-driven tissue regeneration but also in stem cell dysfunction and aging. Here, we provide background in the field and discuss recent advances in our understanding of muscle stem cell function and dysfunction, particularly in the case of aging, and the potential involvement of muscle stem cells in genetic diseases such as the muscular dystrophies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  1. Till JE, McCulloch CE (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14:213–222

    Article  CAS  PubMed  Google Scholar 

  2. Till JE, Mak TW, Price GB, Senn JS, McCulloch EA (1976) Cellular subclasses in human leukemic hemopoiesis. Hamatol Bluttransfus 19:33–45

    CAS  PubMed  Google Scholar 

  3. Sabin FR, Doan CA, Forkner CE (1932) The production of osteogenic sarcomata and the effects on lymph nodes and bone marrow of intravenous injections of radium chloride and mesothorium in rabbits. J Exp Med 56(2):267–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ramalho-Santos M, Willenbring H (2007) On the origin of the term “stem cell”. Cell Stem Cell 1(1):35–38. doi:10.1016/j.stem.2007.05.013

    Article  CAS  PubMed  Google Scholar 

  5. Becker AJ, McCulloch CE, Till JE (1963) Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197:452–454

    Article  CAS  PubMed  Google Scholar 

  6. Hsu YC, Fuchs E (2012) A family business: stem cell progeny join the niche to regulate homeostasis. Nat Rev Mol Cell Biol 13(2):103–114. doi:10.1038/nrm3272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bond AM, Ming GL, Song H (2015) Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell 17(4):385–395. doi:10.1016/j.stem.2015.09.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93(1):23–67. doi:10.1152/physrev.00043.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chang NC, Rudnicki MA (2014) Satellite cells: the architects of skeletal muscle. Curr Top Dev Biol 107:161–181. doi:10.1016/B978-0-12-416022-4.00006-8

    Article  CAS  PubMed  Google Scholar 

  10. Scharner J, Zammit PS (2011) The muscle satellite cell at 50: the formative years. Skelet Muscle 1(1):28. doi:10.1186/2044-5040-1-28

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sambasivan R, Tajbakhsh S (2015) Adult skeletal muscle stem cells. Results Probl Cell Differ 56:191–213. doi:10.1007/978-3-662-44608-9_9

    Article  CAS  PubMed  Google Scholar 

  12. Frontera WR, Ochala J (2015) Skeletal muscle: a brief review of structure and function. Calcif Tissue Int 96(3):183–195. doi:10.1007/s00223-014-9915-y

    Article  CAS  PubMed  Google Scholar 

  13. Tello JF (1917) Genesis de las terminaciones nerviosas motrices y sensitivas. Trab Lab Invest biol Univ Madr 15:99

    Google Scholar 

  14. Mauro A (1961) Satellite cells of skeletal fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Sartorelli V, Caretti G (2005) Mechanisms underlying the transcriptional regulation of skeletal myogenesis. Curr Opin Genet Dev 15(5):528–535. doi:10.1016/j.gde.2005.04.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435(7044):954–958. doi:10.1038/nature03572

    Article  CAS  PubMed  Google Scholar 

  17. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S (2005) Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19(12):1426–1431. doi:10.1101/gad.345505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M (2006) Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172(1):91–102. doi:10.1083/jcb.200508044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102(6):777–786

    Article  CAS  PubMed  Google Scholar 

  20. Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, Goodyear LJ, Wagers AJ (2008) Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134(1):37–47. doi:10.1016/j.cell.2008.05.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122(2):289–301. doi:10.1016/j.cell.2005.05.010

    Article  CAS  PubMed  Google Scholar 

  22. Gunther S, Kim J, Kostin S, Lepper C, Fan CM, Braun T (2013) Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells. Cell Stem Cell 13(5):590–601. doi:10.1016/j.stem.2013.07.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129(5):999–1010. doi:10.1016/j.cell.2007.03.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lepper C, Conway SJ, Fan CM (2009) Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460(7255):627–631. doi:10.1038/nature08209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309(5743):2064–2067. doi:10.1126/science.1114758

    Article  CAS  PubMed  Google Scholar 

  26. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456(7221):502–506. doi:10.1038/nature07384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138(17):3639–3646. doi:10.1242/dev.067595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G (2011) Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138(17):3625–3637. doi:10.1242/dev.064162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B, Guenou H, Malissen B, Tajbakhsh S, Galy A (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138(17):3647–3656. doi:10.1242/dev.067587

    Article  CAS  PubMed  Google Scholar 

  30. Kopan R, Nye JS, Weintraub H (1994) The intracellular domain of mouse Notch: A constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 120:2385–2396

    Article  CAS  PubMed  Google Scholar 

  31. Mourikis P, Sambasivan R, Castel D, Rocheteau P, Bizzarro V, Tajbakhsh S (2012) A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30(2):243–252. doi:10.1002/stem.775

    Article  CAS  PubMed  Google Scholar 

  32. Bjornson CR, Cheung TH, Liu L, Tripathi PV, Steeper KM, Rando TA (2012) Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30(2):232–242. doi:10.1002/stem.773

    Article  CAS  PubMed  Google Scholar 

  33. Vasyutina E, Lenhard DC, Wende H, Erdmann B, Epstein JA, Birchmeier C (2007) RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc Natl Acad Sci U S A 104(11):4443–4448. doi:10.1073/pnas.0610647104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Gopinath SD, Webb AE, Brunet A, Rando TA (2014) FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Reports 2(4):414–426. doi:10.1016/j.stemcr.2014.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Buas MF, Kabak S, Kadesch T (2010) The Notch effector Hey1 associates with myogenic target genes to repress myogenesis. J Biol Chem 285(2):1249–1258. doi:10.1074/jbc.M109.046441

    Article  CAS  PubMed  Google Scholar 

  36. Wen Y, Bi P, Liu W, Asakura A, Keller C, Kuang S (2012) Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cell Biol 32(12):2300–2311. doi:10.1128/MCB.06753-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kuroda K, Tani S, Tamura K, Minoguchi S, Kurooka H, Honjo T (1999) Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J Biol Chem 274(11):7238–7244

    Article  CAS  PubMed  Google Scholar 

  38. Pisconti A, Cornelison DD, Olguin HC, Antwine TL, Olwin BB (2010) Syndecan-3 and Notch cooperate in regulating adult myogenesis. J Cell Biol 190(3):427–441. doi:10.1083/jcb.201003081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25(10):2448–2459. doi:10.1634/stemcells.2007-0019

    Article  CAS  PubMed  Google Scholar 

  40. Chakkalakal JV, Christensen J, Xiang W, Tierney MT, Boscolo FS, Sacco A, Brack AS (2014) Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state. Development 141(8):1649–1659. doi:10.1242/dev.100842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Allen RE, Boxhorn LK (1989) Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138(2):311–315. doi:10.1002/jcp.1041380213

    Article  CAS  PubMed  Google Scholar 

  42. Chen SE, Gerken E, Zhang Y, Zhan M, Mohan RK, Li AS, Reid MB, Li YP (2005) Role of TNF-{alpha} signaling in regeneration of cardiotoxin-injured muscle. Am J Physiol Cell Physiol 289(5):C1179–C1187. doi:10.1152/ajpcell.00062.2005

    Article  CAS  PubMed  Google Scholar 

  43. Chen SE, Jin B, Li YP (2007) TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am J Physiol Cell Physiol 292(5):C1660–C1671. doi:10.1152/ajpcell.00486.2006

    Article  CAS  PubMed  Google Scholar 

  44. Mourkioti F, Rosenthal N (2005) IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol 26(10):535–542. doi:10.1016/j.it.2005.08.002

    Article  CAS  PubMed  Google Scholar 

  45. Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1(1):4. doi:10.1186/2044-5040-1-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sheehan SM, Allen RE (1999) Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J Cell Physiol 181(3):499–506. doi:10.1002/(SICI)1097-4652(199912)181:3<499::AID-JCP14>3.0.CO;2-1

    Article  CAS  PubMed  Google Scholar 

  47. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194:114–128

    Article  CAS  PubMed  Google Scholar 

  48. Lluis F, Perdiguero E, Nebreda AR, Munoz-Canoves P (2006) Regulation of skeletal muscle gene expression by p38 MAP kinases. Trends Cell Biol 16(1):36–44. doi:10.1016/j.tcb.2005.11.002

    Article  CAS  PubMed  Google Scholar 

  49. Wu Z, Woodring PJ, Bhakta KS, Tamura K, Wen F, Feramisco JR, Karin M, Wang JY, Puri PL (2000) p38 and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol Cell Biol 20(11):3951–3964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Takaesu G, Kang JS, Bae GU, Yi MJ, Lee CM, Reddy EP, Krauss RS (2006) Activation of p38alpha/beta MAPK in myogenesis via binding of the scaffold protein JLP to the cell surface protein Cdo. J Cell Biol 175(3):383–388. doi:10.1083/jcb.200608031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Perdiguero E, Ruiz-Bonilla V, Gresh L, Hui L, Ballestar E, Sousa-Victor P, Baeza-Raja B, Jardi M, Bosch-Comas A, Esteller M, Caelles C, Serrano AL, Wagner EF, Munoz-Canoves P (2007) Genetic analysis of p38 MAP kinases in myogenesis: fundamental role of p38alpha in abrogating myoblast proliferation. EMBO J 26(5):1245–1256. doi:10.1038/sj.emboj.7601587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ruiz-Bonilla V, Perdiguero E, Gresh L, Serrano AL, Zamora M, Sousa-Victor P, Jardi M, Wagner EF, Munoz-Canoves P (2008) Efficient adult skeletal muscle regeneration in mice deficient in p38beta, p38gamma and p38delta MAP kinases. Cell Cycle 7(14):2208–2214

    Article  CAS  PubMed  Google Scholar 

  53. Brien P, Pugazhendhi D, Woodhouse S, Oxley D, Pell JM (2013) p38alpha MAPK regulates adult muscle stem cell fate by restricting progenitor proliferation during postnatal growth and repair. Stem Cells 31(8):1597–1610. doi:10.1002/stem.1399

    Article  CAS  PubMed  Google Scholar 

  54. Troy A, Cadwallader AB, Fedorov Y, Tyner K, Tanaka KK, Olwin BB (2012) Coordination of satellite cell activation and self-renewal by par-complex-dependent asymmetric activation of p38alpha/beta MAPK. Cell Stem Cell 11(4):541–553. doi:10.1016/j.stem.2012.05.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hausburg MA, Doles JD, Clement SL, Cadwallader AB, Hall MN, Blackshear PJ, Lykke-Andersen J, Olwin BB (2015) Post-transcriptional regulation of satellite cell quiescence by TTP-mediated mRNA decay. Elife 4:e03390. doi:10.7554/eLife.03390

    Article  PubMed  PubMed Central  Google Scholar 

  56. Sachidanandan C, Sambasivan R, Dhawan J (2002) Tristetraprolin and LPS-inducible CXC chemokine are rapidly induced in presumptive satellite cells in response to skeletal muscle injury. J Cell Sci 115(Pt 13):2701–2712

    Article  CAS  PubMed  Google Scholar 

  57. Crist CG, Montarras D, 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(1):118–126. doi:10.1016/j.stem.2012.03.011

    Article  CAS  PubMed  Google Scholar 

  58. Diao Y, Guo X, Li Y, Sun K, Lu L, Jiang L, Fu X, Zhu H, Sun H, Wang H, Wu Z (2012) Pax3/7BP is a Pax7- and Pax3-binding protein that regulates the proliferation of muscle precursor cells by an epigenetic mechanism. Cell Stem Cell 11(2):231–241. doi:10.1016/j.stem.2012.05.022

    Article  CAS  PubMed  Google Scholar 

  59. Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, Butler-Browne GS (1999) In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 112(Pt 17):2895–2901

    Article  CAS  PubMed  Google Scholar 

  60. Blum R, Vethantham V, Bowman C, Rudnicki M, Dynlacht BD (2012) Genome-wide identification of enhancers in skeletal muscle: the role of MyoD1. Genes Dev 26(24):2763–2779. doi:10.1101/gad.200113.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL, Gentleman RC, Tapscott SJ (2010) Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 18(4):662–674. doi:10.1016/j.devcel.2010.02.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Pallafacchina G, Francois S, Regnault B, Czarny B, Dive V, Cumano A, Montarras D, Buckingham M (2010) An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res 4(2):77–91. doi:10.1016/j.scr.2009.10.003

    Article  CAS  PubMed  Google Scholar 

  63. Liu L, Cheung TH, Charville GW, Hurgo BM, Leavitt T, Shih J, Brunet A, Rando TA (2013) Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep 4(1):189–204. doi:10.1016/j.celrep.2013.05.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Boonsanay V, Zhang T, Georgieva A, Kostin S, Qi H, Yuan X, Zhou Y, Braun T (2016) Regulation of skeletal muscle stem cell quiescence by Suv4-20h1-dependent facultative heterochromatin formation. Cell Stem Cell 18(2):229–242. doi:10.1016/j.stem.2015.11.002

    Article  CAS  PubMed  Google Scholar 

  65. Juan AH, Derfoul A, Feng X, Ryall JG, Dell’Orso S, Pasut A, Zare H, Simone JM, Rudnicki MA, Sartorelli V (2011) Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev 25(8):789–794. doi:10.1101/gad.2027911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Palacios D, Mozzetta C, Consalvi S, Caretti G, Saccone V, Proserpio V, Marquez VE, Valente S, Mai A, Forcales SV, Sartorelli V, Puri PL (2010) TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7(4):455–469. doi:10.1016/j.stem.2010.08.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Tierney MT, Sacco A (2016) Satellite cell heterogeneity in skeletal muscle homeostasis. Trends Cell Biol 26(6):434–444. doi:10.1016/j.tcb.2016.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151(6):1221–1234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Conboy MJ, Karasov AO, Rando TA (2007) High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol 5(5):e102. doi:10.1371/journal.pbio.0050102

    Article  PubMed  PubMed Central  Google Scholar 

  70. Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8(7):677–687. doi:10.1038/ncb1425

    Article  CAS  PubMed  Google Scholar 

  71. Comai G, Sambasivan R, Gopalakrishnan S, Tajbakhsh S (2014) Variations in the efficiency of lineage marking and ablation confound distinctions between myogenic cell populations. Dev Cell 31(5):654–667. doi:10.1016/j.devcel.2014.11.005

    Article  CAS  PubMed  Google Scholar 

  72. Gayraud-Morel B, Chretien F, Jory A, Sambasivan R, Negroni E, Flamant P, Soubigou G, Coppee JY, Di Santo J, Cumano A, Mouly V, Tajbakhsh S (2012) Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells. J Cell Sci 125(Pt 7):1738–1749. doi:10.1242/jcs.097006

    Article  CAS  PubMed  Google Scholar 

  73. Ono Y, Masuda S, Nam HS, Benezra R, Miyagoe-Suzuki Y, Takeda S (2012) Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. J Cell Sci 125(Pt 5):1309–1317. doi:10.1242/jcs.096198

    Article  CAS  PubMed  Google Scholar 

  74. Schultz E (1996) Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol 175(1):84–94. doi:10.1006/dbio.1996.0097

    Article  CAS  PubMed  Google Scholar 

  75. Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, Blasco MA, Tajbakhsh S (2012) A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148(1–2):112–125. doi:10.1016/j.cell.2011.11.049

    Article  CAS  PubMed  Google Scholar 

  76. Tedesco FS, Moyle L, Perdiguero E (2017) Muscle interstitial cells: a brief field guide to non-satellite cell populations in skeletal muscle. Methods Mol Biol 1556:129–148

    Google Scholar 

  77. Mitchell KJ, Pannerec A, Cadot B, Parlakian A, Besson V, Gomes ER, Marazzi G, Sassoon DA (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12(3):257–266. doi:10.1038/ncb2025

    Article  CAS  PubMed  Google Scholar 

  78. Pannerec A, Formicola L, Besson V, Marazzi G, Sassoon DA (2013) Defining skeletal muscle resident progenitors and their cell fate potentials. Development 140(14):2879–2891. doi:10.1242/dev.089326

    Article  CAS  PubMed  Google Scholar 

  79. Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenzi A, Perani L, Antonini S, Sambasivan R, Brunelli S, Tajbakhsh S, Cossu G (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2:499. doi:10.1038/ncomms1508

    Article  CAS  PubMed  Google Scholar 

  80. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9(3):255–267. doi:10.1038/ncb1542

    Article  CAS  PubMed  Google Scholar 

  81. Sampaolesi M, Blot S, D’Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444(7119):574–579. doi:10.1038/nature05282

    Article  CAS  PubMed  Google Scholar 

  82. Kirkwood TB (2005) Understanding the odd science of aging. Cell 120(4):437–447. doi:10.1016/j.cell.2005.01.027

    Article  CAS  PubMed  Google Scholar 

  83. Alway SE, Myers MJ, Mohamed JS (2014) Regulation of satellite cell function in sarcopenia. Front Aging Neurosci 6:246. doi:10.3389/fnagi.2014.00246

    Article  PubMed  PubMed Central  Google Scholar 

  84. Glass D, Roubenoff R (2010) Recent advances in the biology and therapy of muscle wasting. Ann N Y Acad Sci 1211:25–36. doi:10.1111/j.1749-6632.2010.05809.x

    Article  PubMed  Google Scholar 

  85. Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M (2012) Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 3:260. doi:10.3389/fphys.2012.00260

    Article  PubMed  PubMed Central  Google Scholar 

  86. Faulkner JA, Brooks SV, Zerba E (1995) Muscle atrophy and weakness with aging: contraction-induced injury as an underlying mechanism. J Gerontol A Biol Sci Med Sci 50 Spec No:124–129

    CAS  PubMed  Google Scholar 

  87. Brack AS, Bildsoe H, Hughes SM (2005) Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy. J Cell Sci 118(Pt 20):4813–4821. doi:10.1242/jcs.02602

    Article  CAS  PubMed  Google Scholar 

  88. Chakkalakal JV, Jones KM, Basson MA, Brack AS (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490(7420):355–360. doi:10.1038/nature11438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sousa-Victor P, Gutarra S, Garcia-Prat L, Rodriguez-Ubreva J, Ortet L, Ruiz-Bonilla V, Jardi M, Ballestar E, Gonzalez S, Serrano AL, Perdiguero E, Munoz-Canoves P (2014) Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506(7488):316–321. doi:10.1038/nature13013

    Article  CAS  PubMed  Google Scholar 

  90. Verdijk LB, Dirks ML, Snijders T, Prompers JJ, Beelen M, Jonkers RA, Thijssen DH, Hopman MT, Van Loon LJ (2012) Reduced satellite cell numbers with spinal cord injury and aging in humans. Med Sci Sports Exerc 44(12):2322–2330. doi:10.1249/MSS.0b013e3182667c2e

    Article  PubMed  Google Scholar 

  91. Verdijk LB, Snijders T, Drost M, Delhaas T, Kadi F, van Loon LJ (2014) Satellite cells in human skeletal muscle; from birth to old age. Age 36(2):545–547. doi:10.1007/s11357-013-9583-2

    Article  CAS  PubMed  Google Scholar 

  92. Zwetsloot KA, Childs TE, Gilpin LT, Booth FW (2013) Non-passaged muscle precursor cells from 32-month old rat skeletal muscle have delayed proliferation and differentiation. Cell Prolif 46(1):45–57. doi:10.1111/cpr.12007

    Article  CAS  PubMed  Google Scholar 

  93. Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302(5650):1575–1577. doi:10.1126/science.1087573

    Article  CAS  PubMed  Google Scholar 

  94. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433(7027):760–764. doi:10.1038/nature03260

    Article  CAS  PubMed  Google Scholar 

  95. Garcia-Prat L, Martinez-Vicente M, Perdiguero E, Ortet L, Rodriguez-Ubreva J, Rebollo E, Ruiz-Bonilla V, Gutarra S, Ballestar E, Serrano AL, Sandri M, Munoz-Canoves P (2016) Autophagy maintains stemness by preventing senescence. Nature 529(7584):37–42. doi:10.1038/nature16187

    Article  CAS  PubMed  Google Scholar 

  96. Collins CA, Zammit PS, Ruiz AP, Morgan JE, Partridge TA (2007) A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25(4):885–894. doi:10.1634/stemcells.2006-0372

    Article  CAS  PubMed  Google Scholar 

  97. Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY, Llewellyn ME, Delp SL, Blau HM (2014) Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med 20(3):255–264. doi:10.1038/nm.3464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Shea KL, Xiang W, LaPorta VS, Licht JD, Keller C, Basson MA, Brack AS (2010) Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6(2):117–129. doi:10.1016/j.stem.2009.12.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Carlson ME, Hsu M, Conboy IM (2008) Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454(7203):528–532. doi:10.1038/nature07034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807–810. doi:10.1126/science.1144090

    Article  CAS  PubMed  Google Scholar 

  101. Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA (2008) A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2(1):50–59. doi:10.1016/j.stem.2007.10.006

    Article  CAS  PubMed  Google Scholar 

  102. Wagers AJ, Conboy IM (2005) Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122(5):659–667. doi:10.1016/j.cell.2005.08.021

    Article  CAS  PubMed  Google Scholar 

  103. Gutmann E, Carlson BM (1976) Regeneration and transplantation of muscles in old rats and between young and old rats. Life Sci 18(1):109–114

    Article  CAS  PubMed  Google Scholar 

  104. Carlson BM, Faulkner JA (1989) Muscle transplantation between young and old rats: age of host determines recovery. Am J Physiol 256(6 Pt 1):C1262–C1266

    Article  CAS  PubMed  Google Scholar 

  105. Roberts P, McGeachie JK, Grounds MD (1997) The host environment determines strain-specific differences in the timing of skeletal muscle regeneration: cross-transplantation studies between SJL/J and BALB/c mice. J Anat 191(Pt 4):585–594

    Article  PubMed  PubMed Central  Google Scholar 

  106. Harrison DE (1983) Long-term erythropoietic repopulating ability of old, young, and fetal stem cells. J Exp Med 157(5):1496–1504

    Article  CAS  PubMed  Google Scholar 

  107. Carlson BM, Faulkner JA (1983) The regeneration of skeletal muscle fibers following injury: a review. Med Sci Sports Exerc 15(3):187–198

    Article  CAS  PubMed  Google Scholar 

  108. Shavlakadze T, McGeachie J, Grounds MD (2010) Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology 11(3):363–376. doi:10.1007/s10522-009-9260-0

    Article  PubMed  Google Scholar 

  109. Smythe GM, Shavlakadze T, Roberts P, Davies MJ, McGeachie JK, Grounds MD (2008) Age influences the early events of skeletal muscle regeneration: studies of whole muscle grafts transplanted between young (8 weeks) and old (13-21 months) mice. Exp Gerontol 43(6):550–562. doi:10.1016/j.exger.2008.02.005

    Article  CAS  PubMed  Google Scholar 

  110. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park JS, Couillard-Despres S, Aigner L, Li G, Peskind ER, Kaye JA, Quinn JF, Galasko DR, Xie XS, Rando TA, Wyss-Coray T (2011) The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477(7362):90–94. doi:10.1038/nature10357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Naito AT, Sumida T, Nomura S, Liu ML, Higo T, Nakagawa A, Okada K, Sakai T, Hashimoto A, Hara Y, Shimizu I, Zhu W, Toko H, Katada A, Akazawa H, Oka T, Lee JK, Minamino T, Nagai T, Walsh K, Kikuchi A, Matsumoto M, Botto M, Shiojima I, Komuro I (2012) Complement C1q activates canonical Wnt signaling and promotes aging-related phenotypes. Cell 149(6):1298–1313. doi:10.1016/j.cell.2012.03.047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Elabd C, Cousin W, Upadhyayula P, Chen RY, Chooljian MS, Li J, Kung S, Jiang KP, Conboy IM (2014) Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat Commun 5:4082. doi:10.1038/ncomms5082

    Article  CAS  PubMed  Google Scholar 

  113. Sinha M, Jang YC, Oh J, Khong D, Wu EY, Manohar R, Miller C, Regalado SG, Loffredo FS, Pancoast JR, Hirshman MF, Lebowitz J, Shadrach JL, Cerletti M, Kim MJ, Serwold T, Goodyear LJ, Rosner B, Lee RT, Wagers AJ (2014) Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344(6184):649–652. doi:10.1126/science.1251152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Egerman MA, Cadena SM, Gilbert JA, Meyer A, Nelson HN, Swalley SE, Mallozzi C, Jacobi C, Jennings LL, Clay I, Laurent G, Ma S, Brachat S, Lach-Trifilieff E, Shavlakadze T, Trendelenburg AU, Brack AS, Glass DJ (2015) GDF11 increases with age and inhibits skeletal muscle regeneration. Cell Metab 22(1):164–174. doi:10.1016/j.cmet.2015.05.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Brun CE, Rudnicki MA (2015) GDF11 and the mythical fountain of youth. Cell Metab 22(1):54–56. doi:10.1016/j.cmet.2015.05.009

    Article  CAS  PubMed  Google Scholar 

  116. Rodgers BD, Eldridge JA (2015) Reduced circulating GDF11 is unlikely responsible for age-dependent changes in mouse heart, muscle, and brain. Endocrinology 156(11):3885–3888. doi:10.1210/en.2015-1628

    Article  CAS  PubMed  Google Scholar 

  117. Smith SC, Zhang X, Zhang X, Gross P, Starosta T, Mohsin S, Franti M, Gupta P, Hayes D, Myzithras M, Kahn J, Tanner J, Weldon SM, Khalil A, Guo X, Sabri A, Chen X, MacDonnell S, Houser SR (2015) GDF11 does not rescue aging-related pathological hypertrophy. Circ Res 117(11):926–932. doi:10.1161/CIRCRESAHA.115.307527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Poggioli T, Vujic A, Yang P, Macias-Trevino C, Uygur A, Loffredo FS, Pancoast JR, Cho M, Goldstein J, Tandias RM, Gonzalez E, Walker RG, Thompson TB, Wagers AJ, Fong YW, Lee RT (2016) Circulating growth differentiation factor 11/8 levels decline with age. Circ Res 118(1):29–37. doi:10.1161/CIRCRESAHA.115.307521

    Article  CAS  PubMed  Google Scholar 

  119. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153(6):1194–1217. doi:10.1016/j.cell.2013.05.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Bortoli S, Renault V, Eveno E, Auffray C, Butler-Browne G, Piétu G. Gene expression profiling of human satellite cells during muscular aging using cDNA arrays. Gene. 2003 Dec 4;321:145–54. http://dx.doi.org/10.1016/j.gene.2003.08.025

    Google Scholar 

  121. Zhu CH, Mouly V, Cooper RN, Mamchaoui K, Bigot A, Shay JW, Di Santo JP, Butler-Browne GS, Wright WE (2007) Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: consequences in aging muscle and therapeutic strategies for muscular dystrophies. Aging Cell 6(4):515–523. doi:10.1111/j.1474-9726.2007.00306.x

    Article  CAS  PubMed  Google Scholar 

  122. Kadi F, Ponsot E (2010) The biology of satellite cells and telomeres in human skeletal muscle: effects of aging and physical activity. Scand J Med Sci Sports 20(1):39–48. doi:10.1111/j.1600-0838.2009.00966.x

    Article  CAS  PubMed  Google Scholar 

  123. Shadrach JL, Wagers AJ (2011) Stem cells for skeletal muscle repair. Philos Trans R Soc Lond B Biol Sci 366(1575):2297–2306. doi:10.1098/rstb.2011.0027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Kondo H, Kim HW, Wang L, Okada M, Paul C, Millard RW, Wang Y (2016) Blockade of senescence-associated microRNA-195 in aged skeletal muscle cells facilitates reprogramming to produce induced pluripotent stem cells. Aging Cell 15(1):56–66. doi:10.1111/acel.12411

    Article  CAS  PubMed  Google Scholar 

  125. Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V (2002) Regenerative potential of human skeletal muscle during aging. Aging Cell 1(2):132–139

    Article  CAS  PubMed  Google Scholar 

  126. Didier N, Hourde C, Amthor H, Marazzi G, Sassoon D (2012) Loss of a single allele for Ku80 leads to progenitor dysfunction and accelerated aging in skeletal muscle. EMBO Mol Med 4(9):910–923. doi:10.1002/emmm.201101075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Bernet JD, Doles JD, Hall JK, Kelly Tanaka K, Carter TA, Olwin BB (2014) p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med 20(3):265–271. doi:10.1038/nm.3465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Price FD, von Maltzahn J, Bentzinger CF, Dumont NA, Yin H, Chang NC, Wilson DH, Frenette J, Rudnicki MA (2014) Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nat Med 20(10):1174–1181. doi:10.1038/nm.3655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Tierney MT, Aydogdu T, Sala D, Malecova B, Gatto S, Puri PL, Latella L, Sacco A (2014) STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med 20(10):1182–1186. doi:10.1038/nm.3656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Lopez-Lluch G, Navas P (2015) Calorie restriction as an intervention in ageing. J Physiol 594(8):2043–2060. doi:10.1113/JP270543

  131. Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ (2012) Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10(5):515–519. doi:10.1016/j.stem.2012.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Wallace GQ, McNally EM (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71:37–57. doi:10.1146/annurev.physiol.010908.163216

    Article  CAS  PubMed  Google Scholar 

  133. Emery AE (2002) The muscular dystrophies. Lancet 359(9307):687–695

    Article  CAS  PubMed  Google Scholar 

  134. Heslop L, Morgan JE, Partridge TA (2000) Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 113(Pt 12):2299–2308

    Article  CAS  PubMed  Google Scholar 

  135. Webster C, Blau HM (1990) Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat Cell Mol Genet 16(6):557–565

    Article  CAS  PubMed  Google Scholar 

  136. Kottlors M, Kirschner J (2010) Elevated satellite cell number in Duchenne muscular dystrophy. Cell Tissue Res 340(3):541–548. doi:10.1007/s00441-010-0976-6

    Article  PubMed  Google Scholar 

  137. Mann CJ, Perdiguero E, Kharraz Y, Aguilar S, Pessina P, Serrano AL, Munoz-Canoves P (2011) Aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 1(1):21. doi:10.1186/2044-5040-1-21

    Article  PubMed  PubMed Central  Google Scholar 

  138. Delaporte C, Dehaupas M, Fardeau M (1984) Comparison between the growth pattern of cell cultures from normal and Duchenne dystrophy muscle. J Neurol Sci 64(2):149–160

    Article  CAS  PubMed  Google Scholar 

  139. Melone MA, Peluso G, Petillo O, Galderisi U, Cotrufo R (1999) Defective growth in vitro of Duchenne Muscular Dystrophy myoblasts: the molecular and biochemical basis. J Cell Biochem 76(1):118–132

    Article  CAS  PubMed  Google Scholar 

  140. Blau HM, Webster C, Pavlath GK (1983) Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 80(15):4856–4860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Boldrin L, Zammit PS, Morgan JE (2015) Satellite cells from dystrophic muscle retain regenerative capacity. Stem Cell Res 14(1):20–29. doi:10.1016/j.scr.2014.10.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Dumont NA, Wang YX, von Maltzahn J, Pasut A, Bentzinger CF, Brun CE, Rudnicki MA (2015) Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division. Nat Med 21(12):1455–1463. doi:10.1038/nm.3990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Decary S, Hamida CB, Mouly V, Barbet JP, Hentati F, Butler-Browne GS (2000) Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord 10(2):113–120

    Article  CAS  PubMed  Google Scholar 

  144. Lund TC, Grange RW, Lowe DA (2007) Telomere shortening in diaphragm and tibialis anterior muscles of aged mdx mice. Muscle Nerve 36(3):387–390. doi:10.1002/mus.20824

    Article  CAS  PubMed  Google Scholar 

  145. Sousa-Victor P, Perdiguero E, Munoz-Canoves P (2014) Geroconversion of aged muscle stem cells under regenerative pressure. Cell Cycle 13(20):3183–3190. doi:10.4161/15384101.2014.965072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M, Kraft P, Shkreli M, Delp S, Pomerantz JH, Artandi SE, Blau HM (2010) Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143(7):1059–1071. doi:10.1016/j.cell.2010.11.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Kudryashova E, Kramerova I, Spencer MJ (2012) Satellite cell senescence underlies myopathy in a mouse model of limb-girdle muscular dystrophy 2H. J Clin Invest 122(5):1764–1776. doi:10.1172/JCI59581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Goodell MA, Nguyen H, Shroyer N (2015) Somatic stem cell heterogeneity: diversity in the blood, skin and intestinal stem cell compartments. Nat Rev Mol Cell Biol 16(5):299–309. doi:10.1038/nrm3980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Gayraud-Morel B, Pala, F., Sakai, H., Tajbakhsh S. (2017) Isolation of muscle stem cells from mouse skeletal muscle. Methods Mol Biol 1556:23–40

    Google Scholar 

  150. Tonlorenzi R, Rossi G, Messina G (2017) Isolation and characterization of vessel-associated stem/progenitor cells from skeletal muscle. Methods Mol Biol 1556:149–170

    Google Scholar 

  151. Stuelsatz P, Keire P, Yablonka-Reuveni Z (2017) Isolation, culture, and immunostaining of skeletal muscle myofibers from wildtype and Nestin-GFP mice as a means to analyze satellite cells. Methods Mol Biol 1556:51–102

    Google Scholar 

  152. Sincennes MC, Wang YX, Rudnicki MA (2017) Primary mouse myoblast purification using magnetic cell separation. Methods Mol Biol 1556:41–50

    Google Scholar 

  153. Low M, Eisner C, Rossi FM (2017) Fibro/adipogenic progenitors (FAPs): isolation by FACS and culture. Methods Mol Biol 1556:179–190

    Google Scholar 

  154. Saclier M, Theret M, Mounier R, Chazaud B (2017) Effects of macrophage conditioned-medium on murine and human muscle cells: analysis of proliferation, differentiation and fusion. Methods Mol Biol 1556:317–328

    Google Scholar 

  155. Arora R, Rumman M, Venugopal N, Gala H, Dhawan J (2017) Mimicking muscle stem cell quiescence in culture: methods for synchronization in reversible arrest. Methods Mol Biol 1556:283–302

    Google Scholar 

  156. Davoudi S, Gilbert PM (2017) Optimization of satellite cell culture through biomaterials. Methods Mol Biol 1556:329–342

    Google Scholar 

  157. Gatto S, Puri PL, Malecova B (2017) Single cell gene expression profiling of skeletal muscle-derived cells. Methods Mol Biol 1556:191–221

    Google Scholar 

  158. Sreenivasan K, Braun T, Kim J (2017) Systematic identification of genes regulating muscle stem cell self-renewal and differentiation. Methods Mol Biol 1556:343–354

    Google Scholar 

  159. Peng X, Sun K, Zhou J, Sun H, Wang H (2017) Bioinformatics for novel large intergenic non-coding RNA (lincRNA) identification in skeletal muscle cells. Methods Mol Biol 1556:355–362

    Google Scholar 

  160. Ryall JG (2017) Simultaneous measurement of mitochondrial and glycolytic activity in quiescent muscle stem cells. Methods Mol Biol 1556:245–254

    Google Scholar 

  161. Garcia-Prat L, Munoz-Canoves P, Martinez-Vicente M (2017) Monitoring autophagy in muscle stem cells. Methods Mol Biol 1556:255–281

    Google Scholar 

  162. Lund DK, McAnulty P, Siegel AL, Cornelison DD (2016) Methods for observing and quantifying muscle satellite cell motility and invasion in vitro. Methods Mol Biol 1556:303–316

    Google Scholar 

  163. Tierney D, Sacco A (2017) Engraftment of FACS isolated muscle stem cells into injured skeletal muscle. Methods Mol Biol 1556:223–236

    Google Scholar 

  164. Hall MN, Hall JK, Cadwallader AB, Pawlikowski BT, Doles JD, Elston TC, Olwin BB (2017) Transplantation of Skeletal Muscle Stem cells. Methods Mol Biol 1556:237–244

    Google Scholar 

  165. Nguyen PD, Currie PD (2017) Using transgenic zebrafish to study muscle stem/progenitor cells. Methods Mol Biol 1556:117–127

    Google Scholar 

  166. Lavergne G, Soler C, Zmojdzian M, Jagla K (2016) Characterization of Drosophila muscle stem cell-like adult muscle precursors. Methods Mol Biol 1556:103–116

    Google Scholar 

Download references

Acknowledgments

We thank Drs. Pura Muñoz-Cánoves and Antonio Serrano (UPF, Barcelona) and Elena Rebollo (MIP, IBMB, Barcelona) for their insightful discussions. E.P. acknowledges the funding from MINECO, Spain (SAF2015-67369-R and “María de Maeztu” Programme for Units of Excellence in R&D MDM-2014-0370), AFM, CIBERNED (IntraCIBER 2015-2/06, InterCIBER PIE14/00061). DDWC was funded by National Institutes of Health grant #AR067450.

Author information

Authors and Affiliations

  1. Division of Biological Sciences and Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

    DDW Cornelison

  2. Cell Biology Group, Department of Experimental and Health Sciences (DCEXS), Pompeu Fabra University (UPF), CIBER on Neurodegenerative Diseases (CIBERNED), 08003, Barcelona, Spain

    Eusebio Perdiguero

Authors
  1. DDW Cornelison
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eusebio Perdiguero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to DDW Cornelison or Eusebio Perdiguero .

Editor information

Editors and Affiliations

  1. Cell Biology Group, Department of Experimental and Health Sciences, University Pompeu Fabra (UPF), Barcelona, Spain

    Eusebio Perdiguero

  2. Division of Biological Sciences and Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

    DDW Cornelison

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Science+Business Media LLC

About this protocol

Cite this protocol

Cornelison, D., Perdiguero, E. (2017). Muscle Stem Cells: A Model System for Adult Stem Cell Biology. In: Perdiguero, E., Cornelison, D. (eds) Muscle Stem Cells. Methods in Molecular Biology, vol 1556. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-6771-1_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-6771-1_1

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-4939-6769-8

  • Online ISBN: 978-1-4939-6771-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation