Stem cell activation in skeletal muscle regeneration

Cellular and Molecular Life Sciences

Volumn 72, Issue 9, 2015, Pages 1663-1677

  Fu, Xin ^a   Wang, Huating ^b   Hu, Ping ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

DNA methylation; Epigenetics; Growth factors; Non coding RNA; Quiescent stem cells; Satellite cells

Indexed keywords

ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENETIC EPIGENESIS; HUMAN; METABOLISM; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; EPIGENESIS, GENETIC; HUMANS; MUSCLE, SKELETAL; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELLS;

EID: 84939988925     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1819-5     Document Type: Review

References (213)

1. Stump CS et al (2006) The metabolic syndrome: role of skeletal muscle metabolism. Ann Med 38(6):389-402
2. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493-495
3. Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93(1):23-67
4. Relaix F, Marcelle C (2009) Muscle stem cells. Curr Opin Cell Biol 21(6):748-753
5. Cosgrove BD et al (2009) A home away from home: challenges and opportunities in engineering in vitro muscle satellite cell niches. Differentiation Res Biol Divers 78(2-3):185-194
6. Aziz A, Sebastian S, Dilworth FJ (2012) The origin and fate of muscle satellite cells. Stem cell reviews 8(2):609-622
7. Pannerec A, Marazzi G, Sassoon D (2012) Stem cells in the hood: the skeletal muscle niche. Trends Mol Med 18(10):599-606
8. Pallafacchina G, Blaauw B, Schiaffino S (2013) Role of satellite cells in muscle growth and maintenance of muscle mass. Nutr Metab Cardiovasc Dis 23(Suppl 1):S12-S18
9. Yusuf F, Brand-Saberi B (2012) Myogenesis and muscle regeneration. Histochem Cell Biol 138(2):187-199
10. Biressi S, Rando TA (2010) Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 21(8):845-854
11. Montarras D, L'Honore A, Buckingham M (2013) Lying low but ready for action: the quiescent muscle satellite cell. FEBS J 280(17):4036-4050
12. Brack AS, Rando TA (2012) Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 10(5):504-514
13. Ceafalan LC, Popescu BO, Hinescu ME (2014) Cellular players in skeletal muscle regeneration. BioMed Res Int 2014:957014
14. Bischoff R (1975) Regeneration of single skeletal muscle fibers in vitro. Anat Rec 182(2):215-235
15. Konigsberg IR (1963) Clonal analysis of myogenesis. Science 140(3573):1273-1284
16. Konigsberg UR, Lipton BH, Konigsberg IR (1975) The regenerative response of single mature muscle fibers isolated in vitro. Dev Biol 45(2):260-275
17. Moss FP, Leblond CP (1970) Nature of dividing nuclei in skeletal muscle of growing rats. J Cell Biol 44(2):459-462
18. Reznik M (1969) Thymidine-3H uptake by satellite cells of regenerating skeletal muscle. J Cell Biol 40(2):568-571
19. Snow MH (1977) Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. II. An autoradiographic study. Anat Rec 188(2):201-217
20. Yaffe D (1969) Cellular aspects of muscle differentiation in vitro. Curr Top Dev Biol 4:37-77
21. Hutcheson DA et al (2009) Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for beta-catenin. Genes Dev 23(8):997-1013
22. Gros J et al (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435(7044):954-958
23. Relaix F et al (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435(7044):948-953
24. Harel I et al (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16(6):822-832
25. Allbrook DB, Han MF, Hellmuth AE (1971) Population of muscle satellite cells in relation to age and mitotic activity. Pathology 3(3):223-243
26. Schmalbruch H, Hellhammer U (1976) The number of satellite cells in normal human muscle. Anat Rec 185(3):279-287
27. Lindstrom M, Thornell LE (2009) New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol 132(2):141-157
28. Sajko S et al (2004) Frequency of M-cadherin-stained satellite cells declines in human muscles during aging. J Histochem Cytochem 52(2):179-185
29. Bareja A, Billin AN (2013) Satellite cell therapy - from mice to men. Skelet Muscle 3(1):2
30. Schultz E (1996) Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol 175(1):84-94
31. Campion DR et al (1981) Changes in the satellite cell population during postnatal growth of pig skeletal muscle. J Anim Sci 52(5):1014-1018
32. Mesires NT, Doumit ME (2002) Satellite cell proliferation and differentiation during postnatal growth of porcine skeletal muscle. Am J Physiol Cell Physiol 282(4):C899-C906
33. Kuang S et al (2006) Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol 172(1):103-113
34. Seale P et al (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102(6):777-786
35. Alfaro LA et al (2011) CD34 promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration. Stem Cells 29(12):2030-2041
36. Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191(2):270-283
37. Zammit PS et al (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166(3):347-357
38. Schultz E, McCormick KM (1994) Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123:213-257
39. Wozniak AC et al (2005) Signaling satellite-cell activation in skeletal muscle: markers, models, stretch, and potential alternate pathways. Muscle Nerve 31(3):283-300
40. Anderson JE (2000) A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 11(5):1859-1874
41. Kondoh K, Sunadome K, Nishida E (2007) Notch signaling suppresses p38 MAPK activity via induction of MKP-1 in myogenesis. J Biol Chem 282(5):3058-3065
42. Jones NC et al (2005) The p38alpha/beta MAPK functions as a molecular switch to activate the quiescent satellite cell. J Cell Biol 169(1):105-116
43. Zhang K, Sha J, Harter ML (2010) Activation of Cdc6 by MyoD is associated with the expansion of quiescent myogenic satellite cells. J Cell Biol 188(1):39-48
44. 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
45. Gayraud-Morel B et al (2012) Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells. J Cell Sci 125(Pt 7):1738-1749
46. Machida YJ, Hamlin JL, Dutta A (2005) Right place, right time, and only once: replication initiation in metazoans. Cell 123(1):13-24
47. Sorrentino V et al (1990) Cell proliferation inhibited by MyoD1 independently of myogenic differentiation. Nature 345(6278):813-815
48. Halevy O et al (1995) Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267(5200):1018-1021
49. Asakura A et al (2007) Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle. Proc Natl Acad Sci USA 104(42):16552-16557
50. Rocheteau P et al (2012) A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148(1-2):112-125
51. Kuang S et al (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129(5):999-1010
52. Shea KL et al (2010) Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6(2):117-129
53. Sanes JR (2003) The basement membrane/basal lamina of skeletal muscle. J Biol Chem 278(15):12601-12604
54. Allen RE et al (1995) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165(2):307-312
55. Tatsumi R et al (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194(1):114-128
56. Sheehan SM et al (2000) HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 23(2):239-245
57. Maina F et al (1996) Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell 87(3):531-542
58. Wozniak AC, Anderson JE (2007) Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236(1):240-250
59. Bischoff R (1990) Interaction between satellite cells and skeletal muscle fibers. Development 109(4):943-952
60. Toumi H, F'Guyer S, Best TM (2006) The role of neutrophils in injury and repair following muscle stretch. J Anat 208(4):459-470
61. Orimo S et al (1991) Analysis of inflammatory cells and complement C3 in bupivacaine-induced myonecrosis. Muscle Nerve 14(6):515-520
62. Fielding RA (1993) Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol 265(1 Pt 2):R166-R172
63. Kharraz Y et al (2013) Macrophage plasticity and the role of inflammation in skeletal muscle repair. Mediators Inflamm 2013:491497
64. Saclier M et al (2013) Differentially activated macrophages orchestrate myogenic precursor cell fate during human skeletal muscle regeneration. Stem Cells 31(2):384-396
65. Tidball JG, Villalta SA (2010) Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integr Comp Physiol 298(5):R1173-R1187
66. Mackey AL (2007) The influence of anti-inflammatory medication on exercise-induced myogenic precursor cell responses in humans. J Appl Physiol (1985) 103(2):425-431
67. Mikkelsen UR et al (2011) Local NSAID infusion does not affect protein synthesis and gene expression in human muscle after eccentric exercise. Scand J Med Sci Sports 21(5):630-644
68. Ziltener JL, Leal S, Fournier PE (2010) Non-steroidal anti-inflammatory drugs for athletes: an update. Ann Phys Rehabil Med 53(4):278-282 282-8
69. Ziche M, Morbidelli L (2000) Nitric oxide and angiogenesis. J Neurooncol 50(1-2):139-148
70. Anderson JE, Wozniak AC (2004) Satellite cell activation on fibers: modeling events in vivo - an invited review. Can J Physiol Pharmacol 82(5):300-310
71. Abou-Khalil R et al (2009) Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell 5(3):298-309
72. Miyazawa K et al (1994) Proteolytic activation of hepatocyte growth factor in response to tissue injury. J Biol Chem 269(12):8966-8970
73. Zarnegar R, Michalopoulos GK (1995) The many faces of hepatocyte growth factor: from hepatopoiesis to hematopoiesis. J Cell Biol 129(5):1177-1180
74. Bladt F et al (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376(6543):768-771
75. Brand-Saberi B et al (1996) Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo. Dev Biol 179(1):303-308
76. Heymann S et al (1996) Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. Dev Biol 180(2):566-578
77. Rodgers JT et al (2014) mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature 510(7505):393-396
78. Tatsumi R et al (2001) Mechanical stretch induces activation of skeletal muscle satellite cells in vitro. Exp Cell Res 267(1):107-114
79. Leshem Y et al (2000) Hepatocyte growth factor (HGF) inhibits skeletal muscle cell differentiation: a role for the bHLH protein twist and the cdk inhibitor p27. J Cell Physiol 184(1):101-109
80. Khan MA et al (2013) Twist: a molecular target in cancer therapeutics. Tumour Biol 34(5):2497-2506
81. Filippin LI et al (2009) Nitric oxide and repair of skeletal muscle injury. Nitric Oxide 21(3-4):157-163
82. Stamler JS, Meissner G (2001) Physiology of nitric oxide in skeletal muscle. Physiol Rev 81(1):209-237
83. Rubinstein I et al (1998) Involvement of nitric oxide system in experimental muscle crush injury. J Clin Invest 101(6):1325-1333
84. Park CS et al (1996) Neuronal isoform of nitric oxide synthase is expressed at low levels in human retina. Cell Mol Neurobiol 16(4):499-515
85. Rigamonti E et al (2013) Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage. J Immunol 190(4):1767-1777
86. Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288(2):R345-R353
87. Ganea E et al (2007) Matrix metalloproteinases: useful and deleterious. Biochem Soc Trans 35(Pt 4):689-691
88. Darmani H et al (2004) Expression of nitric oxide synthase and transforming growth factor-beta in crush-injured tendon and synovium. Mediators Inflamm 13(5-6):299-305
89. Serra C et al (2011) The role of GH and IGF-I in mediating anabolic effects of testosterone on androgen-responsive muscle. Endocrinology 152(1):193-206
90. Sandri M et al (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117(3):399-412
91. Song YH et al (2013) The therapeutic potential of IGF-I in skeletal muscle repair. Trends in endocrinology and metabolism: TEM 24(6):310-319
92. Yamaguchi M et al (2012) The CLOCK 3111T/C SNP is associated with morning gastric motility in healthy young women. Physiol Behav 107(1):87-91
93. Hill M, Wernig A, Goldspink G (2003) Muscle satellite (stem) cell activation during local tissue injury and repair. J Anat 203(1):89-99
94. Owino V, Yang SY, Goldspink G (2001) Age-related loss of skeletal muscle function and the inability to express the autocrine form of insulin-like growth factor-1 (MGF) in response to mechanical overload. FEBS Lett 505(2):259-263
95. Hill M, Goldspink G (2003) Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J Physiol (London) 549(2):409-418
96. Yang SY, Goldspink GE (2002) Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522(1-3):156-160
97. Dobrowolny G et al (2005) Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol 168(2):193-199
98. Pallafacchina G et al (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
99. Dong Y et al (2013) Interactions between p-Akt and Smad3 in injured muscles initiate myogenesis or fibrogenesis. Am J Physiol Endocrinol Metab 305(3):E367-E375
100. Perez-Ruiz A, Gnocchi VF, Zammit PS (2007) Control of Myf5 activation in adult skeletal myonuclei requires ERK signalling. Cell Signal 19:1671-1680
101. Elia D et al (2007) Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: involvement of MAPK/EIK and PI3 K/Akt pathways. Biochimica Et Biophysica Acta -Mol Cell Res 1773(9):1438-1446
102. Lovett FA et al (2006) Convergence of Igf2 expression and adhesion signalling via RhoA and p38 MAPK enhances myogenic differentiation. J Cell Sci 119(23):4828-4840
103. Takaesu G et al (2006) Activation of p38 alpha/beta MAPK in myogenesis via binding of the scaffold protein JLP to the cell surface protein Cdo. J Cell Biol 175(3):383-388
104. Riuzzi F, Sorci G, Donato R (2006) The amphoterin (HMGB1)/receptor for advanced glycation end products (RAGE) pair modulates myoblast proliferation, apoptosis, adhesiveness, migration, and invasiveness. Functional inactivation of RAGE in L6 myoblasts results in tumor formation in vivo. J Biol Chem 281(12):8242-8253
105. Riuzzi F, Sorci G, Donato R (2007) RAGE expression in rhabdomyosarcoma cells results in myogenic differentiation and reduced proliferation, migration, invasiveness, and tumor growth. Am J Pathol 171(3):947-961
106. Riuzzi F et al (2012) HMGB1-RAGE regulates muscle satellite cell homeostasis through p38-MAPK- and myogenin-dependent repression of Pax7 transcription. J Cell Sci 125(Pt 6):1440-1454
107. Sorci G et al (2004) Amphoterin stimulates myogenesis and counteracts the antimyogenic factors basic fibroblast growth factor and S100B via RAGE binding. Mol Cell Biol 24(11):4880-4894
108. Kastner S et al (2000) Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J Histochem Cytochem 48(8):1079-1096
109. Floss T, Arnold HH, Braun T (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11(16):2040-2051
110. 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
111. Yablonka-Reuveni Z, Seger R, Rivera AJ (1999) Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47(1):23-42
112. Scata KA et al (1999) FGF receptor availability regulates skeletal myogenesis. Exp Cell Res 250(1):10-21
113. Fedorov YV, Rosenthal RS, Olwin BB (2001) Oncogenic Ras-induced proliferation requires autocrine fibroblast growth factor 2 signaling in skeletal muscle cells. J Cell Biol 152(6):1301-1305
114. Jones NC et al (2001) ERK1/2 is required for myoblast proliferation but is dispensable for muscle gene expression and cell fusion. J Cell Physiol 186(1):104-115
115. Liu Y, Schneider MF (2014) FGF2 activates TRPC and Ca(2 +) signaling leading to satellite cell activation. Front Physiol 5:38
116. Louvi A, Artavanis-Tsakonas S (2012) Notch and disease: a growing field. Semin Cell Dev Biol 23(4):473-480
117. Castel D et al (2013) Dynamic binding of RBPJ is determined by Notch signaling status. Genes Dev 27(9):1059-1071
118. Schuster-Gossler K, Cordes R, Gossler A (2007) Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc Natl Acad Sci USA 104(2):537-542
119. Vasyutina E et al (2007) RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc Natl Acad Sci USA 104(11):4443-4448
120. Mourikis P et al (2012) Cell-autonomous Notch activity maintains the temporal specification potential of skeletal muscle stem cells. Development 139(24):4536-4548
121. Bjornson CR et al (2012) Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30(2):232-242
122. Mourikis P et al (2012) A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30(2):243-252
123. Liu L et al (2013) Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep 4(1):189-204
124. Delfini MC et al (2000) Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 127(23):5213-5224
125. Brack AS et al (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
126. Conboy IM, Rando TA (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3(3):397-409
127. Mourikis P, Tajbakhsh S (2014) Distinct contextual roles for Notch signalling in skeletal muscle stem cells. BMC Dev Biol 14:2
128. Clevers H, Nusse R (2012) Wnt/beta-catenin signaling and disease. Cell 149(6):1192-1205
129. Polesskaya A, Seale P, Rudnicki MA (2003) Wnt signaling induces the myogenic specification of resident CD45 + adult stem cells during muscle regeneration. Cell 113(7):841-852
130. Perez-Ruiz A et al (2008) beta-Catenin promotes self-renewal of skeletal-muscle satellite cells. J Cell Sci 121(Pt 9):1373-1382
131. Brack AS et al (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807-810
132. Naito AT et al (2012) Complement C1q activates canonical Wnt signaling and promotes aging-related phenotypes. Cell 149(6):1298-1313
133. Simons M, Mlodzik M (2008) Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42:517-540
134. Le Grand F et al (2009) Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4(6):535-547
135. Bentzinger CF et al (2013) Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell 12(1):75-87
136. Weiss A, Attisano L (2013) The TGFbeta superfamily signaling pathway. Wiley interdisciplinary reviews. Dev Biol 2(1):47-63
137. Vaidya TB et al (1989) Fibroblast growth factor and transforming growth factor beta repress transcription of the myogenic regulatory gene MyoD1. Mol Cell Biol 9(8):3576-3579
138. Martin JF, Li L, Olson EN (1992) Repression of myogenin function by TGF-beta 1 is targeted at the basic helix-loop-helix motif and is independent of E2A products. J Biol Chem 267(16):10956-10960
139. Li X, McFarland DC, Velleman SG (2009) Transforming growth factor-beta1-induced satellite cell apoptosis in chickens is associated with beta1 integrin-mediated focal adhesion kinase activation. Poult Sci 88(8):1725-1734
140. Kollias HD, McDermott JC (2008) Transforming growth factor-beta and myostatin signaling in skeletal muscle. J Appl Physiol (1985) 104(3):579-587
141. Joulia-Ekaza D, Cabello G (2007) The myostatin gene: physiology and pharmacological relevance. Curr Opin Pharmacol 7(3):310-315
142. McCroskery S et al (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162(6):1135-1147
143. Amthor H et al (2002) The regulation and action of myostatin as a negative regulator of muscle development during avian embryogenesis. Dev Biol 251(2):241-257
144. McFarlane C et al (2008) Myostatin signals through Pax7 to regulate satellite cell self-renewal. Exp Cell Res 314(2):317-329
145. 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
146. Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609-652
147. Cornelison DD et al (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239(1):79-94
148. Quinlan JG et al (1995) Radiation inhibition of mdx mouse muscle regeneration: dose and age factors. Muscle Nerve 18(2):201-206
149. Cornelison DD et al (2004) Essential and separable roles for syndecan-3 and syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18(18):2231-2236
150. Carmeli E et al (2004) Matrix metalloproteinases and skeletal muscle: a brief review. Muscle Nerve 29(2):191-197
151. Ferre PJ et al (2007) Longitudinal analysis of gene expression in porcine skeletal muscle after post-injection local injury. Pharm Res 24(8):1480-1489
152. Fukushima K et al (2007) Activation and localization of matrix metalloproteinase-2 and -9 in the skeletal muscle of the muscular dystrophy dog (CXMDJ). BMC Musculoskelet Disord 8:54
153. Kherif S et al (1999) Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles. Dev Biol 205(1):158-170
154. Yamada M et al (2008) Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. Int J Biochem Cell Biol 40(10):2183-2191
155. Yamada M et al (2006) Matrix metalloproteinases are involved in mechanical stretch-induced activation of skeletal muscle satellite cells. Muscle Nerve 34(3):313-319
156. Liu H et al (2010) TIMP3: a physiological regulator of adult myogenesis. J Cell Sci 123(Pt 17):2914-2921
157. Relaix F et al (2006) Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172(1):91-102
158. Sambasivan R et al (2009) Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell 16(6):810-821
159. Zanou N, Gailly P (2013) Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cell Mol Life Sci 70(21):4117-4130
160. Hu P et al (2008) Codependent activators direct myoblast-specific MyoD transcription. Dev Cell 15(4):534-546
161. Riuzzi F et al (2014) RAGE signaling deficiency in rhabdomyosarcoma cells causes upregulation of PAX7 and uncontrolled proliferation. J Cell Sci 127(Pt 8):1699-1711
162. Boldrin L et al (2009) Mature adult dystrophic mouse muscle environment does not impede efficient engrafted satellite cell regeneration and self-renewal. Stem Cells 27(10):2478-2487
163. Kumar D et al (2009) Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells. Mol Biol Cell 20(14):3170-3177
164. Yajima H et al (2010) Six family genes control the proliferation and differentiation of muscle satellite cells. Exp Cell Res 316(17):2932-2944
165. Lee H, Habas R, Abate-Shen C (2004) MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304(5677):1675-1678
166. Liu Y et al (2013) Six1 regulates MyoD expression in adult muscle progenitor cells. PLoS One 8(6):e67762
167. Beauchamp JR et al (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151(6):1221-1234
168. Rantanen J et al (1995) Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab Invest 72(3):341-347
169. Hansen KH et al (2008) A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10(11):1291-1300
170. Barski A et al (2007) High-resolution profiling of histone methylations in the human genome. Cell 129(4):823-837
171. Palacios D et al (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
172. Sebastian S et al (2009) MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci USA 106(12):4719-4724
173. McKinnell IW et al (2008) Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat Cell Biol 10(1):77-84
174. Fulco M et al (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14(5):661-673
175. Rathbone CR, Booth FW, Lees SJ (2008) FoxO3a preferentially induces p27Kip1 expression while impairing muscle precursor cell-cycle progression. Muscle Nerve 37(1):84-89
176. Fulco M et al (2003) Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell 12(1):51-62
177. Zhao X et al (2005) Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications. Mol Cell Biol 25(19):8456-8464
178. Guarani V et al (2011) Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature 473(7346):234-238
179. Tang AH, Rando TA (2014) Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation. EMBO J 33(23):2782-2797
180. Taylor SM, Jones PA (1979) Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17(4):771-779
181. Acharyya S et al (2010) TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in duchenne muscular dystrophy. PLoS One 5(8):e12479
182. Fan H et al (2012) Sulforaphane causes a major epigenetic repression of myostatin in porcine satellite cells. Epigenetics: Off J DNA Methylation Soc 7(12):1379-1390
183. Erriquez D, Perini G, Ferlini A (2013) Non-coding RNAs in muscle dystrophies. Int J Mol Sci 14(10):19681-19704
184. Kirby TJ, McCarthy JJ (2013) MicroRNAs in skeletal muscle biology and exercise adaptation. Free Radic Biol Med 64:95-105
185. Chen JF et al (2010) microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J Cell Biol 190(5):867-879
186. Cacchiarelli D et al (2011) miR-31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy. EMBO Rep 12(2):136-141
187. Cheung TH et al (2012) Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482(7386):524-528
188. Naguibneva I et al (2006) The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat Cell Biol 8(3):278-284
189. van Rooij E, Liu N, Olson EN (2008) MicroRNAs flex their muscles. Trends in genetics: TIG 24(4):159-166
190. Chen JF, Callis TE, Wang DZ (2009) microRNAs and muscle disorders. J Cell Sci 122(Pt 1):13-20
191. Eisenberg I, Alexander MS, Kunkel LM (2009) miRNAS in normal and diseased skeletal muscle. J Cell Mol Med 13(1):2-11
192. Ge Y, Chen J (2011) MicroRNAs in skeletal myogenesis. Cell Cycle 10(3):441-448
193. Liu N et al (2012) microRNA-206 promotes skeletal muscle regeneration and delays progression of Duchenne muscular dystrophy in mice. J Clin Invest 122(6):2054-2065
194. Ge Y, Sun Y, Chen J (2011) IGF-II is regulated by microRNA-125b in skeletal myogenesis. J Cell Biol 192(1):69-81
195. Cardinali B et al (2009) Microrna-221 and microrna-222 modulate differentiation and maturation of skeletal muscle cells. PLoS One 4(10):e7607
196. Maciotta S et al (2012) Hmgb3 is regulated by microRNA-206 during muscle regeneration. PLoS One 7(8):e43464
197. Dormoy-Raclet V (2013) HuR and miR-1192 regulate myogenesis by modulating the translation of HMGB1 mRNA. Nat Commun 4:2388
198. Riuzzi F et al (2012) HMGB1-RAGE regulates muscle satellite cell homeostasis through p38-MAPK- and myogenin-dependent repression of Pax7 transcription. J Cell Sci 125(6):1440-1454
199. Koning M et al (2012) A global downregulation of microRNAs occurs in human quiescent satellite cells during myogenesis. Differentiation 84(4):314-321
200. Neguembor MV, Jothi M, Gabellini D (2014) Long noncoding RNAs, emerging players in muscle differentiation and disease. Skelet Muscle 4(1):8
201. Legnini I et al (2014) A feedforward regulatory loop between HuR and the long noncoding RNA linc-MD1 controls early phases of myogenesis. Mol Cell 53(3):506-514
202. Watts R et al (2013) Myostatin-induced inhibition of the long noncoding RNA Malat1 is associated with decreased myogenesis. Am J Physiol Cell Physiol 304(10):C995-C1001
203. Sunwoo H et al (2009) MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res 19(3):347-359
204. Caretti G et al (2006) The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 11(4):547-560
205. Hube F et al (2011) Steroid receptor RNA activator protein binds to and counteracts SRA RNA-mediated activation of MyoD and muscle differentiation. Nucleic Acids Res 39(2):513-525
206. Lu L et al (2013) Genome-wide survey by ChIP-seq reveals YY1 regulation of lincRNAs in skeletal myogenesis. EMBO J 32(19):2575-2588
207. Twayana S et al (2013) Biogenesis and function of non-coding RNAs in muscle differentiation and in Duchenne muscular dystrophy. Biochem Soc Trans 41(4):844-849
208. Brannan CI et al (1990) The product of the H19 gene may function as an RNA. Mol Cell Biol 10(1):28-36
209. Gabory A, Jammes H, Dandolo L (2010) The H19 locus: role of an imprinted non-coding RNA in growth and development. BioEssays News Rev Mol Cell Dev Biol 32(6):473-480
210. Onyango P, Feinberg AP (2011) A nucleolar protein, H19 opposite tumor suppressor (HOTS), is a tumor growth inhibitor encoded by a human imprinted H19 antisense transcript. Proc Natl Acad Sci USA 108(40):16759-16764
211. Ripoche MA et al (1997) Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev 11(12):1596-1604
212. Forne T et al (1997) Loss of the maternal H19 gene induces changes in Igf2 methylation in both cis and trans. Proc Natl Acad Sci USA 94(19):10243-10248
213. Li Z et al (2012) An HMGA2-IGF2BP2 axis regulates myoblast proliferation and myogenesis. Dev Cell 23(6):1176-1188