Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease

Nature Reviews Molecular Cell Biology

Volumn 17, Issue 5, 2016, Pages 267-279

  Almada, Albert E ^a   Wagers, Amy J ^a  

^a Harvard University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ACTIVATION; CELL AGING; CELL DIFFERENTIATION; CELL FATE; ECTOPIC EXPRESSION; EXTRACELLULAR MATRIX; HUMAN; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SATELLITE CELL ACTIVATION; SATELLITE CELL FATE; SATELLITE CELL SELF RENEWAL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE SATELLITE CELL; STEM CELL; STEM CELL SELF-RENEWAL; AGING; ANIMAL; CELL SELF-RENEWAL; METABOLISM; MUSCLE DISEASE; PATHOLOGY; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE;

MUSCLE PROTEIN;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL SELF RENEWAL; HUMANS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DISEASES; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION;

EID: 84960171956     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm.2016.7     Document Type: Review

References (148)

1. Mauro, A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493-495 (1961).
2. Bentzinger, C. F. et al. Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell 12, 75-87 (2013).
3. Yin, H., Price, F. & Rudnicki, M. A. Satellite cells and the muscle stem cell niche. Physiol. Rev. 93, 23-67 (2013).
4. Urciuolo, A. et al. Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat. Commun. 4, 1964 (2013).
5. Brohl, D. et al. Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals. Dev. Cell 23, 469-481 (2012).
6. + T cells recruited to sites of sterile skeletal muscle injury regulate the fate of satellite cells and guide effective tissue regeneration. PLoS ONE 10, e0128094 (2015).
7. Burzyn, D. et al. A special population of regulatory T cells potentiates muscle repair. Cell 155, 1282-1295 (2013).
8. Murphy, M. M., Lawson, J. A., Mathew, S. J., Hutcheson, D. A. & Kardon, G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138, 3625-3637 (2011).
9. Joe, A. W. et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12, 153-163 (2010).
10. + stem cells from injured muscle. PLoS Biol. 2, E130 (2004).
11. Seale, P. et al. Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777-786 (2000).
12. Yablonka-Reuveni, Z. et al. The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev. Biol. 210, 440-455 (1999).
13. White, J. D. et al. Myotube formation is delayed but not prevented in MyoD-deficient skeletal muscle: studies in regenerating whole muscle grafts of adult mice. J. Histochem. Cytochem. 48, 1531-1544 (2000).
14. Megeney, L. A., Kablar, B., Garrett, K., Anderson, J. E. & Rudnicki, M. A. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10, 1173-1183 (1996).
15. Gayraud-Morel, B. et al. A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev. Biol. 312, 13-28 (2007).
16. Cooper, R. N. et al. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell Sci. 112, 2895-2901 (1999).
17. Ustanina, S., Carvajal, J., Rigby, P. & Braun, T. The myogenic factor Myf5 supports efficient skeletal muscle regeneration by enabling transient myoblast amplification. Stem Cells 25, 2006-2016 (2007).
18. Faralli, H. & Dilworth, F. J. Turning on myogenin in muscle: a paradigm for understanding mechanisms of tissue-specific gene expression. Comp. Funct. Genomics 2012, 836374 (2012).
19. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S. & Blau, H. M. Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506 (2008).
20. Zammit, P. S. et al. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166, 347-357 (2004).
21. Collins, C. A. et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289-301 (2005).
22. Sambasivan, R. et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138, 3647-3656 (2011).
23. Lepper, C., Partridge, T. A. & Fan, C. M. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138, 3639-3646 (2011).
24. Lepper, C., Conway, S. J. & Fan, C. M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627-631 (2009).
25. Brack, A. S. Pax7 is back. Skelet. Muscle 4, 24 (2014).
26. von Maltzahn, J., Jones, A. E., Parks, R. J. & Rudnicki, M. A. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc. Natl Acad. Sci. USA 110, 16474-16479 (2013).
27. Gunther, S. et al. Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells. Cell Stem Cell 13, 590-601 (2013).
28. Blau, H. M., Cosgrove, B. D. & Ho, A. T. The central role of muscle stem cells in regenerative failure with aging. Nat. Med. 21, 854-862 (2015).
29. Sousa-Victor, P., Garcia-Prat, L., Serrano, A. L., Perdiguero, E. & Munoz-Canoves, P. Muscle stem cell aging: regulation and rejuvenation. Trends Endocrinol. Metab. 26, 287-96 (2015).
30. Liu, L., Cheung, T. H., Charville, G. W. & Rando, T. A. Isolation of skeletal muscle stem cells by fluorescence-activated cell sorting. Nat. Protoc. 10, 1612-1624 (2015).
31. Conboy, M. J., Cerletti, M., Wagers, A. J. & Conboy, I. M. Immuno-analysis and FACS sorting of adult muscle fiber-associated stem/precursor cells. Methods Mol. Biol. 621, 165-173 (2010).
32. Pasut, A., Oleynik, P. & Rudnicki, M. A. Isolation of muscle stem cells by fluorescence activated cell sorting cytometry. Methods Mol. Biol. 798, 53-64 (2012).
33. Liu, L. et al. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 4, 189-204 (2013).
34. Fukada, S. et al. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25, 2448-2459 (2007).
35. Fukada, S. et al. Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp. Cell Res. 296, 245-255 (2004).
36. Sherwood, R. I. et al. Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119, 543-554 (2004).
37. Cerletti, M. et al. Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134, 37-47 (2008).
38. Castiglioni, A. et al. Isolation of progenitors that exhibit myogenic/osteogenic bipotency in vitro by fluorescence-activated cell sorting from human fetal muscle. Stem Cell Rep. 2, 92-106 (2014).
39. Mackey, A. L. et al. Assessment of satellite cell number and activity status in human skeletal muscle biopsies. Muscle Nerve 40, 455-465 (2009).
40. Charville, G. W. et al. Ex vivo expansion and in vivo self-renewal of human muscle stem cells. Stem Cell Rep. 5, 621-632 (2015).
41. Cornelison, D. D., Filla, M. S., Stanley, H. M., Rapraeger, A. C. & Olwin, B. B. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 239, 79-94 (2001).
42. Montarras, D. et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science 309, 2064-2067 (2005).
43. Yoshida, N., Yoshida, S., Koishi, K., Masuda, K. & Nabeshima, Y. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates 'reserve cells'. J. Cell Sci. 111, 769-779 (1998).
44. Shea, K. L. et al. Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6, 117-129 (2010).
45. Chakkalakal, J. V., Jones, K. M., Basson, M. A. & Brack, A. S. The aged niche disrupts muscle stem cell quiescence. Nature 490, 355-360 (2012).
46. Chen, S., Lewallen, M. & Xie, T. Adhesion in the stem cell niche: biological roles and regulation. Development 140, 255-265 (2013).
47. Koopman, R., Ly, C. H. & Ryall, J. G. A metabolic link to skeletal muscle wasting and regeneration. Front. Physiol. 5, 32 (2014).
48. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. & Young, R. A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 (2007).
49. Mourikis, P. et al. A critical requirement for Notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30, 243-252 (2012).
50. Bjornson, C. R. et al. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30, 232-242 (2012).
51. Wen, Y. et al. Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol. Cell. Biol. 32, 2300-2311 (2012).
52. Kopan, R. & Ilagan, M. X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233 (2009).
53. Olguin, H. C. & Olwin, B. B. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev. Biol. 275, 375-388 (2004).
54. Olguin, H. C., Yang, Z., Tapscott, S. J. & Olwin, B. B. Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J. Cell Biol. 177, 769-779 (2007).
55. Gopinath, S. D., Webb, A. E., Brunet, A. & Rando, T. A. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Rep. 2, 414-426 (2014).
56. Cheung, T. H. et al. Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482, 524-528 (2012).
57. Sato, T. Yamamoto, T. & Sehara-Fujisawa, A. miR-195/497 induce postnatal quiescence of skeletal muscle stem cells. Nat. Commun. 5, 4597 (2014).
58. Zismanov, V. et al. Phosphorylation of eIF2α is a translational control mechanism regulating muscle stem cell quiescence and self-renewal. Cell Stem Cell 18, 79-90 (2015).
59. Allen, R. E., Dodson, M. V. & Luiten, L. S. Regulation of skeletal muscle satellite cell proliferation by bovine pituitary fibroblast growth factor. Exp. Cell Res. 152, 154-160 (1984).
60. Gospodarowicz, D., Weseman, J. & Moran, J. Presence in brain of a mitogenic agent promoting proliferation of myoblasts in low density culture. Nature 256, 216-219 (1975).
61. Tatsumi, R., Hattori, A., Ikeuchi, Y., Anderson, J. E. & Allen, R. E. Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol. Biol. Cell 13, 2909-2918 (2002).
62. Sheehan, S. M., Tatsumi, R., Temm-Grove, C. J. & Allen, R. E. HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 23, 239-245 (2000).
63. Schiaffino, S. & Mammucari, C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1, 4 (2011).
64. Chen, S. E., Jin, B. & Li, Y. P. TNF-α regulates myogenesis and muscle regeneration by activating p38 MAPK. Am. J. Physiol. Cell Physiol. 292, C1660-C1671 (2007).
65. Li, Y. P. TNF-α is a mitogen in skeletal muscle. Am. J. Physiol. Cell Physiol. 285, C370-C376 (2003).
66. Rodgers, J. T. et al. mTORC1 controls the adaptive transition of quiescent stem cells from G0 to GAlert. Nature 510, 393-396 (2014).
67. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
68. Bracken, A. P. & Helin, K. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat. Rev. Cancer 9, 773-784 (2009).
69. Palacios, D. et al. TNF/p38α/Polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7, 455-469 (2010).
70. Juan, A. H. et al. Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev. 25, 789-794 (2011).
71. Woodhouse, S., Pugazhendhi, D., Brien, P. & Pell, J. M. Ezh2 maintains a key phase of muscle satellite cell expansion but does not regulate terminal differentiation. J. Cell Sci. 126, 565-579 (2013).
72. Blum, R., Vethantham, V., Bowman, C., Rudnicki, M. & Dynlacht, B. D. Genome-wide identification of enhancers in skeletal muscle: the role of MyoD1. Genes Dev. 26, 2763-2779 (2012).
73. Cao, Y. et al. Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev. Cell 18, 662-674 (2010).
74. Zhang, K., Sha, J. & Harter, M. L. Activation of Cdc6 by MyoD is associated with the expansion of quiescent myogenic satellite cells. J. Cell Biol. 188, 39-48 (2010).
75. Hu, P., Geles, K. G., Paik, J. H., De Pinho, R. A. & Tjian, R. Codependent activators direct myoblast-specific MyoD transcription. Dev. Cell 15, 534-546 (2008).
76. Troy, A. et al. Coordination of satellite cell activation and self-renewal by Par-complex-dependent asymmetric activation of p38α/β MAPK. Cell Stem Cell 11, 541-553 (2012).
77. Hausburg, M. A. et al. Post-transcriptional regulation of satellite cell quiescence by TTP-mediated mRNA decay. eLife 4, e03390 (2015).
78. Diao, Y. et al. 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, 231-241 (2012).
79. Kawabe, Y., Wang, Y. X., McKinnell, I. W., Bedford, M. T. & Rudnicki, M. A. Carm1 regulates Pax7 transcriptional activity through MLL1/2 recruitment during asymmetric satellite stem cell divisions. Cell Stem Cell 11, 333-345 (2012).
80. Crist, C. G., Montarras, D. & Buckingham, M. 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 (2012).
81. McKinnell, I. W. et al. Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat. Cell Biol. 10, 77-84 (2008).
82. Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A. & Tajbakhsh, S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148, 112-125 (2012).
83. Kuang, S., Kuroda, K., Le Grand, F. & Rudnicki, M. A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129, 999-1010 (2007).
84. Shinin, V., Gayraud-Morel, B., Gomes, D. & Tajbakhsh, S. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat. Cell Biol. 8, 677-687 (2006).
85. Tierney, M. T. et al. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat. Med. 20, 1182-1186 (2014).
86. Price, F. D. et al. Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nat. Med. 20, 1174-1181 (2014).
87. Yennek, S., Burute, M., Thery, M. & Tajbakhsh, S. Cell adhesion geometry regulates non-random DNA segregation and asymmetric cell fates in mouse skeletal muscle stem cells. Cell Rep. 7, 961-970 (2014).
88. Ono, Y. et al. Muscle stem cell fate is controlled by the cell-polarity protein Scrib. Cell Rep. 10, 1135-1148 (2015).
89. Le Grand, F., Jones, A. E., Seale, V., Scime, A. & Rudnicki, M. A. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4, 535-547 (2009).
90. Chakkalakal, J. V. et al. Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state. Development 141, 1649-1659 (2014).
91. Kim, H. J. & Bar-Sagi, D. Modulation of signalling by Sprouty: a developing story. Nat. Rev. Mol. Cell Biol. 5, 441-450 (2004).
92. Brack, A. S. et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810 (2007).
93. Fry, C. S. et al. Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat. Med. 21, 76-80 (2015).
94. Jackson, J. R. et al. Reduced voluntary running performance is associated with impaired coordination as a result of muscle satellite cell depletion in adult mice. Skelet. Muscle 5, 41 (2015).
95. Sousa-Victor, P. et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506, 316-321 (2014).
96. Bernet, J. D. et al. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat. Med. 20, 265-271 (2014).
97. Cosgrove, B. D. et al. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat. Med. 20, 255-264 (2014).
98. Collins, C. A., Zammit, P. S., Ruiz, A. P., Morgan, J. E. & Partridge, T. A. A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25, 885-894 (2007).
99. Munoz-Espin, D. & Serrano, M. Cellular senescence: from physiology to pathology. Nat. Rev. Mol. Cell Biol. 15, 482-496 (2014).
100. Papaconstantinou, J. et al. Attenuation of p38α MAPK stress response signaling delays the in vivo aging of skeletal muscle myofibers and progenitor cells. Aging 7, 718-733 (2015).
101. Sun, L. et al. JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J. Cell Biol. 179, 129-138 (2007).
102. Sheehan, S. M. & Allen, R. E. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J. Cell. Physiol. 181, 499-506 (1999).
103. Conboy, M. J., Conboy, I. M. & Rando, T. A. Heterochronic parabiosis: historical perspective and methodological considerations for studies of aging and longevity. Aging Cell 12, 525-530 (2013).
104. Conboy, I. M., Conboy, M. J., Smythe, G. M. & Rando, T. A. Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577 (2003).
105. Conboy, I. M. et al. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764 (2005).
106. Villeda, S. A. et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477, 90-94 (2011).
107. Salpeter, S. J. et al. Systemic regulation of the age-related decline of pancreatic β-cell replication. Diabetes 62, 2843-2848 (2013).
108. Carlson, M. E. et al. Relative roles of TGF-β1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 8, 676-689 (2009).
109. Carlson, M. E., Hsu, M. & Conboy, I. M. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454, 528-532 (2008).
110. Liu, H. et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317, 803-806 (2007).
111. Biressi, S., Miyabara, E. H., Gopinath, S. D., Carlig, P. M. & Rando, T. A. A. Wnt-TGFβ2 axis induces a fibrogenic program in muscle stem cells from dystrophic mice. Sci. Transl. Med. 6, 267ra176 (2014).
112. Carter, C. S. Oxytocin pathways and the evolution of human behavior. Annu. Rev. Psychol. 65, 17-39 (2014).
113. Elabd, C. et al. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat. Commun. 5, 4082 (2014).
114. McPherron, A. C., Huynh, T. V. & Lee, S. J. Redundancy of myostatin and growth/differentiation factor 11 function. BMC Dev. Biol. 9, 24 (2009).
115. Loffredo, F. S. et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 153, 828-839 (2013).
116. Poggioli, T. et al. Circulating growth differentiation factor 11/8 levels decline with age. Circ. Res. 118, 29-37 (2016).
117. Olson, K. A. et al. Association of growth differentiation factor 11/8, putative anti-ageing factor, with cardiovascular outcomes and overall mortality in humans: analysis of the Heart and Soul and HUNT3 cohorts. Eur. Heart J. 36, 3426-3434 (2015).
118. Sinha, M. et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344, 649-652 (2014).
119. Egerman, M. A. et al. GDF11 increases with age and inhibits skeletal muscle regeneration. Cell Metab. 22, 164-174 (2015).
120. Hathout, Y. et al. Large-scale serum protein biomarker discovery in Duchenne muscular dystrophy. Proc. Natl Acad. Sci. USA 112, 7153-7158 (2015).
121. Smith, S. C. et al. GDF11 does not rescue aging-related pathological hypertrophy. Circ. Res. 117, 926-932 (2015).
122. Rahimov, F. & Kunkel, L. M. The cell biology of disease: cellular and molecular mechanisms underlying muscular dystrophy. J. Cell Biol. 201, 499-510 (2013).
123. Klingler, W., Jurkat-Rott, K., Lehmann-Horn, F. & Schleip, R. The role of fibrosis in Duchenne muscular dystrophy. Acta Myol. 31, 184-195 (2012).
124. Blau, H. M., Webster, C. & Pavlath, G. K. Defective myoblasts identified in Duchenne muscular dystrophy. Proc. Natl Acad. Sci. USA 80, 4856-4860 (1983).
125. Yablonka-Reuveni, Z. & Anderson, J. E. Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers. Dev. Dyn. 235, 203-212 (2006).
126. Luz, M. A., Marques, M. J. & Santo Neto, H. Impaired regeneration of dystrophin-deficient muscle fibers is caused by exhaustion of myogenic cells. Braz. J. Med. Biol. Res. 35, 691-695 (2002).
127. Heslop, L., Morgan, J. E. & Partridge, T. A. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J. Cell Sci. 113, 2299-2308 (2000).
128. Jiang, C. et al. Notch signaling deficiency underlies age-dependent depletion of satellite cells in muscular dystrophy. Dis. Model. Mech. 7, 997-1004 (2014).
129. Dumont, N. A. et al. Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division. Nat. Med. 21, 1455-1463 (2015).
130. Sacco, A. et al. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143, 1059-1071 (2010).
131. Kottlors, M. & Kirschner, J. Elevated satellite cell number in Duchenne muscular dystrophy. Cell Tissue Res. 340, 541-548 (2010).
132. Vieira, N. M. et al. Muscular dystrophy in a family of Labrador Retrievers with no muscle dystrophin and a mild phenotype. Neuromuscul. Disord. 25, 363-370 (2015).
133. Vieira, N. M. et al. Jagged 1 rescues the Duchenne muscular dystrophy phenotype. Cell 163, 1204-1213 (2015).
134. Boldrin, L., Zammit, P. S. & Morgan, J. E. Satellite cells from dystrophic muscle retain regenerative capacity. Stem Cell Res. 14, 20-29 (2015).
135. Relaix, F., Rocancourt, D., Mansouri, A. & Buckingham, M. A. Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953 (2005).
136. Kassar-Duchossoy, L. et al. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19, 1426-1431 (2005).
137. Ono, Y. et al. Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. J. Cell Sci. 125, 1309-1317 (2012).
138. Sander, J. D. & Joung, J. K. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347-355 (2014).
139. Gilbert, P. M. et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081 (2010).
140. Briggs, D. & Morgan, J. E. Recent progress in satellite cell/myoblast engraftment - relevance for therapy. FEBS J. 280, 4281-4293 (2013).
141. Asakura, A. et al. Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle. Proc. Natl Acad. Sci. USA 104, 16552-16557 (2007).
142. Fu, X. et al. Combination of inflammation-related cytokines promotes long-term muscle stem cell expansion. Cell Res. 25, 655-673 (2015).
143. Elster, J. L. et al. Skeletal muscle satellite cell migration to injured tissue measured with 111In-oxine and high-resolution SPECT imaging. J. Muscle Res. Cell Motil. 34, 417-427 (2013).
144. Bentzinger, C. F. et al. Wnt7a stimulates myogenic stem cell motility and engraftment resulting in improved muscle strength. J. Cell Biol. 205, 97-111 (2014).
145. Laplante, M. & Sabatini, D. M. mTOR signaling in growth control and disease. Cell 149, 274-293 (2012).
146. Cerletti, M., Jang, Y. C., Finley, L. W., Haigis, M. C. & Wagers, A. J. Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10, 515-519 (2012).
147. Tang, A. H. & Rando, T. A. Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation. EMBO J. 33, 2782-2797 (2014).
148. +-dependent SIRT1 deacetylase translates a metabolic switch into regulatory epigenetics in skeletal muscle stem cells. Cell Stem Cell 16, 171-183 (2015).