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The Basis of Muscle Regeneration

DOI: 10.1155/2014/612471

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Abstract:

Muscle regeneration recapitulates many aspects of embryonic myogenesis and is an important homeostatic process of the adult skeletal muscle, which, after development, retains the capacity to regenerate in response to appropriate stimuli, activating the muscle compartment of stem cells, namely, satellite cells, as well as other precursor cells. Moreover, significant evidence suggests that while stem cells represent an important determinant for tissue regeneration, a “qualified” environment is necessary to guarantee and achieve functional results. It is therefore plausible that the loss of control over these cell fate decisions could lead to a pathological transdifferentiation, leading to pathologic defects in the regenerative process. This review provides an overview about the general aspects of muscle development and discusses the cellular and molecular aspects that characterize the five interrelated and time-dependent phases of muscle regeneration, namely, degeneration, inflammation, regeneration, remodeling, and maturation/functional repair. 1. Muscle Regeneration Recapitulates Many Aspects of Development Regenerative potential, robust in lower vertebrates, is gradually lost in higher vertebrates such as mammals [1–5]. Nevertheless, mammalian tissues, including skeletal muscle, are capable of homeostasis and regeneration, partially recapitulating the embryonic developmental program. Muscle development and regeneration share common features because the molecular program that underlines prenatal development is reactivated for tissue reconstruction after injury [6–8] (Figure 1). Regenerative medicine has therefore gained important insights through the study of developmental biology. Figure 1: Schematic representation of muscle formation during embryonic development and adult regeneration. (a) Developmental myogenesis occurs in two distinct waves of differentiation that are characterized by a specific and sequential pattern of muscle-related gene expression (red arrows). Skeletal muscles are derived from somites, which receive signals from the neighboring tissues, namely, axial structures (neural tube and notochord), dorsal ectoderm, and lateral mesoderm that in turn induce the activation (blue arrows) of muscle regulatory factors. Shh (from the notochord) and Wnt1/3 and Wnt11 and IGFs (from dorsal neural tube) signaling have been demonstrated to regulate the expression of Myf5. Pax3 and Myf5 independently regulate MyoD expression, whereas Myf5 regulates the transient expression of MRF4. Myf5 and MyoD independently activate the expression of Myogenin,

References

[1]  J. P. Brockes, “Amphibian limb regeneration: rebuilding a complex structure,” Science, vol. 276, no. 5309, pp. 81–87, 1997.
[2]  E. M. Tanaka, “Regeneration: if they can do it, why can't we?” Cell, vol. 113, no. 5, pp. 559–562, 2003.
[3]  L. E. Iten and S. V. Bryant, “Forelimb regeneration from different levels of amputation in the newt, Notophthalmus viridescens: length, rate, and stages,” Wilhelm Roux's Archives of Developmental Biology, vol. 173, no. 4, pp. 263–282, 1973.
[4]  E. M. Tanaka, A. A. F. Gann, P. B. Gates, and J. P. Brockes, “Newt myotubes reenter the cell cycle by phosphorylation of the retinoblastoma protein,” Journal of Cell Biology, vol. 136, no. 1, pp. 155–165, 1997.
[5]  M. Kragl, D. Knapp, E. Nacu et al., “Cells keep a memory of their tissue origin during axolotl limb regeneration,” Nature, vol. 460, no. 7251, pp. 60–65, 2009.
[6]  S. Tajbakhsh and G. Cossu, “Establishing myogenic identity during somitogenesis,” Current Opinion in Genetics and Development, vol. 7, no. 5, pp. 634–641, 1997.
[7]  T. J. Hawke and D. J. Garry, “Myogenic satellite cells: physiology to molecular biology,” Journal of Applied Physiology, vol. 91, no. 2, pp. 534–551, 2001.
[8]  S. B. P. Chargé and M. A. Rudnicki, “Cellular and molecular regulation of muscle regeneration,” Physiological Reviews, vol. 84, no. 1, pp. 209–238, 2004.
[9]  M. Goulding, A. Lumsden, and A. J. Paquette, “Regulation of Pax-3 expression in the dermomyotome and its role in muscle development,” Development, vol. 120, no. 4, pp. 957–971, 1994.
[10]  B. A. Williams and C. P. Ordahl, “Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification,” Development, vol. 120, no. 4, pp. 785–796, 1994.
[11]  E. Bober, T. Franz, H. Arnold, P. Gruss, and P. Tremblay, “Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells,” Development, vol. 120, no. 3, pp. 603–612, 1994.
[12]  G. Daston, E. Lamar, M. Olivier, and M. Goulding, “Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse,” Development, vol. 122, no. 3, pp. 1017–1027, 1996.
[13]  P. Tremblay, S. Dietrich, M. Mericskay, F. R. Schubert, Z. Li, and D. Paulin, “A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors,” Developmental Biology, vol. 203, no. 1, pp. 49–61, 1998.
[14]  B. Jostes, C. Walther, and P. Gruss, “The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system,” Mechanisms of Development, vol. 33, no. 1, pp. 27–37, 1990.
[15]  P. Seale, L. A. Sabourin, A. Girgis-Gabardo, A. Mansouri, P. Gruss, and M. A. Rudnicki, “Pax7 is required for the specification of myogenic satellite cells,” Cell, vol. 102, no. 6, pp. 777–786, 2000.
[16]  A. Mansouri, A. Stoykova, M. Torres, and P. Gruss, “Dysgenesis of cephalic neural crest derivatives in Pax7-/-mutant mice,” Development, vol. 122, no. 3, pp. 831–838, 1996.
[17]  J. A. Epstein, D. N. Shapiro, J. Cheng, P. Y. P. Lam, and R. L. Maas, “Pax3 modulates expression of the c-met receptor during limb muscle development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 9, pp. 4213–4218, 1996.
[18]  F. Bladt, D. Riethmacher, S. Isenmann, A. Aguzzi, and C. Birchmeier, “Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud,” Nature, vol. 376, no. 6543, pp. 768–771, 1995.
[19]  S. J. Tapscott, “The circuitry of a master switch: myod and the regulation of skeletal muscle gene transcription,” Development, vol. 132, no. 12, pp. 2685–2695, 2005.
[20]  C. A. Berkes and S. J. Tapscott, “MyoD and the transcriptional control of myogenesis,” Seminars in Cell and Developmental Biology, vol. 16, no. 4-5, pp. 585–595, 2005.
[21]  S. Tajbakhsh, E. Bober, C. Babinet, S. Pournin, H. Arnold, and M. Buckingham, “Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle,” Developmental Dynamics, vol. 206, pp. 291–300, 1996.
[22]  M.-O. Ott, E. Bober, G. Lyons, H. Arnold, and M. Buckingham, “Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo,” Development, vol. 111, no. 4, pp. 1097–1107, 1991.
[23]  R. Sp?rle, T. Günther, M. Struwe, and K. Schughart, “Severe defects in the formation of epaxial musculature in open brain (opb) mutant mouse embryos,” Development, vol. 122, no. 1, pp. 79–86, 1996.
[24]  M. Buckingham, “Making muscle in mammals,” Trends in Genetics, vol. 8, no. 4, pp. 144–149, 1992.
[25]  D. Sassoon, G. Lyons, W. E. Wright et al., “Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis,” Nature, vol. 341, no. 6240, pp. 303–307, 1989.
[26]  M. A. Rudnicki, P. N. J. Schnegelsberg, R. H. Stead, T. Braun, H. H. Arnold, and R. Jaenisch, “MyoD or Myf-5 is required for the formation of skeletal muscle,” Cell, vol. 75, no. 7, pp. 1351–1359, 1993.
[27]  P. Hasty, A. Bradley, J. H. Morris et al., “Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene,” Nature, vol. 364, no. 6437, pp. 501–506, 1993.
[28]  Y. Nabeshima, K. Hanaoka, M. Hayasaka et al., “Myogenin gene disruption results in perinatal lethality because of severe muscle defect,” Nature, vol. 364, no. 6437, pp. 532–535, 1993.
[29]  L. Kassar-Duchossoy, B. Gayraud-Morel, D. Gomès et al., “Mrf4 determines skeletal muscle identity in Myf5: Myod double-mutant mice,” Nature, vol. 431, pp. 466–471, 2004.
[30]  A. Musaro, M. G. C. de Angelis, A. Germani, C. Ciccareli, M. Molinaro, and B. M. Zani, “Enhanced expression of myogenic regulatory genes in aging skeletal muscle,” Experimental Cell Research, vol. 221, no. 1, pp. 241–248, 1995.
[31]  E. I. Dedkov, T. Y. Kostrominova, A. B. Borisov, and B. M. Carlson, “MyoD and myogenin protein expression in skeletal muscles of senile rats,” Cell and Tissue Research, vol. 311, no. 3, pp. 401–416, 2003.
[32]  D. Palacios and P. L. Puri, “The epigenetic network regulating muscle development and regeneration,” Journal of Cellular Physiology, vol. 207, no. 1, pp. 1–11, 2006.
[33]  E. A. Miska, E. Langley, D. Wolf, C. Karlsson, J. Pines, and T. Kouzarides, “Differential localization of HDAC4 orchestrates muscle differentiation,” Nucleic Acids Research, vol. 29, no. 16, pp. 3439–3447, 2001.
[34]  M. Haberland, R. L. Montgomery, and E. N. Olson, “The many roles of histone deacetylases in development and physiology: implications for disease and therapy,” Nature Reviews Genetics, vol. 10, no. 1, pp. 32–42, 2009.
[35]  T. E. Callis, Z. Deng, J.-F. Chen, and D.-Z. Wang, “Muscling through the microRNA world,” Experimental Biology and Medicine, vol. 233, no. 2, pp. 131–138, 2008.
[36]  E. van Rooij, N. Liu, and E. N. Olson, “MicroRNAs flex their muscles,” Trends in Genetics, vol. 24, no. 4, pp. 159–166, 2008.
[37]  A. H. Williams, N. Liu, E. van Rooij, and E. N. Olson, “MicroRNA control of muscle development and disease,” Current Opinion in Cell Biology, vol. 21, no. 3, pp. 461–469, 2009.
[38]  D. P. Bartel, “MicroRNAs: genomics, biogenesis, mechanism, and function,” Cell, vol. 116, no. 2, pp. 281–297, 2004.
[39]  N. S. Asli, M. E. Pitulescu, and M. Kessel, “MicroRNAs in organogenesis and disease,” Current Molecular Medicine, vol. 8, no. 8, pp. 698–710, 2008.
[40]  J. F. Chen, E. M. Mandel, J. M. Thomson et al., “The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation,” Nature Genetics, vol. 38, no. 2, pp. 228–233, 2006.
[41]  R. Couteaux, J. Mira, and A. d'Albis, “Regeneration of muscles after cardiotoxin injury. I. Cytological aspects,” Biology of the Cell, vol. 62, no. 2, pp. 171–182, 1988.
[42]  A. d'Albis, R. Couteaux, C. Janmot, A. Roulet, and J. C. Mira, “Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysis,” European Journal of Biochemistry, vol. 174, no. 1, pp. 103–110, 1988.
[43]  A. Musarò, K. McCullagh, A. Paul et al., “Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle,” Nature Genetics, vol. 27, no. 2, pp. 195–200, 2001.
[44]  L. Pelosi, C. Giacinti, C. Nardis et al., “Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines,” The FASEB Journal, vol. 21, no. 7, pp. 1393–1402, 2007.
[45]  R. Matsuda, A. Nishikawa, and H. Tanaka, “Visualization of dystrophic muscle fibers in Mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle,” The Journal of Biochemistry, vol. 118, no. 5, pp. 959–964, 1995.
[46]  M. D. Grounds, “Phagocytosis of necrotic muscle in muscle isografts is influenced by the strain, age, and sex of host mice,” Journal of Pathology, vol. 153, no. 1, pp. 71–82, 1987.
[47]  J. G. Tidball and M. Wehling-Henricks, “Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo,” Journal of Physiology, vol. 578, no. 1, pp. 327–336, 2007.
[48]  M. Summan, G. L. Warren, R. R. Mercer et al., “Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study,” The American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 290, no. 6, pp. R1488–R1495, 2006.
[49]  J. G. Tidball, “Inflammatory processes in muscle injury and repair,” The American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 288, no. 2, pp. R345–R353, 2005.
[50]  C. F. P. Teixeira, S. R. Zamunér, J. P. Zuliani et al., “Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom,” Muscle and Nerve, vol. 28, no. 4, pp. 449–459, 2003.
[51]  R. A. Fielding, T. J. Manfredi, W. Ding, M. A. Fiatarone, W. J. Evans, and J. G. Cannon, “Acute phase response in exercise III. Neutrophil and IL-1β accumulation in skeletal muscle,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 265, no. 1, part 2, pp. R166–R172, 1993.
[52]  A. N. Belcastro, G. D. Arthur, T. A. Albisser, and D. A. Raj, “Heart, liver, and skeletal muscle myeloperoxidase activity during exercise,” Journal of Applied Physiology, vol. 80, no. 4, pp. 1331–1335, 1996.
[53]  T. K. Kishimoto and R. Rothlein, “Integrins, ICAMs, and selectins: role and regulation of adhesion molecules in neutrophil recruitment to inflammatory sites,” Advances in Pharmacology, vol. 25, pp. 117–169, 1994.
[54]  W. A. Muller, “Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response,” Trends in Immunology, vol. 24, no. 6, pp. 327–334, 2003.
[55]  B. Walzog and P. Gaehtgens, “Adhesion molecules: the path to a new understanding of acute inflammation,” News in Physiological Sciences, vol. 15, no. 3, pp. 107–113, 2000.
[56]  M. Sixt, R. Hallmann, O. Wendler, K. Scharffetter-Kochanek, and L. M. Sorokin, “Cell adhesion and migration properties of β2-integrin negative polymorphonuclear granulocytes on defined extracellular matrix molecules: relevance for leukocyte extravasation,” The Journal of Biological Chemistry, vol. 276, no. 22, pp. 18878–18887, 2001.
[57]  F. X. Pizza, J. M. Peterson, J. H. Baas, and T. J. Koh, “Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice,” Journal of Physiology, vol. 562, no. 3, pp. 899–913, 2005.
[58]  B. A. St. Pierre and J. G. Tidball, “Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension,” Journal of Applied Physiology, vol. 77, no. 1, pp. 290–297, 1994.
[59]  L. Arnold, A. Henry, F. Poron et al., “Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 1057–1069, 2007.
[60]  M. Saclier, S. Cuvellier, M. Magnan, R. Mounier, and B. Chazaud, “Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration,” The FEBS Journal, vol. 280, no. 17, pp. 4118–4130, 2013.
[61]  I. S. McLennan, “Resident macrophages (ED2- and ED3-positive) do not phagocytose degenerating rat skeletal muscle fibres,” Cell and Tissue Research, vol. 272, no. 1, pp. 193–196, 1993.
[62]  H. Honda, H. Kimura, and A. Rostami, “Demonstration and phenotypic characterization of resident macrophages in rat skeletal muscle,” Immunology, vol. 70, no. 2, pp. 272–277, 1990.
[63]  A. Pimorady-Esfahani, M. D. Grounds, and P. G. McMenamin, “Macrophages and dendritic cells in normal and regenerating murine skeletal muscle,” Muscle Nerve, vol. 20, pp. 158–166, 1997.
[64]  T. Varga, R. Mounier, P. Gogolak, S. Poliska, B. Chazaud, and L. Nagy, “Tissue LyC6- macrophages are generated in the absence of circulating LyC6- monocytes and Nur77 in a model of muscle regeneration,” Journal of Immunology, vol. 191, no. 11, pp. 5695–5701, 2013.
[65]  F. Geissmann, S. Jung, and D. R. Littman, “Blood monocytes consist of two principal subsets with distinct migratory properties,” Immunity, vol. 19, no. 1, pp. 71–82, 2003.
[66]  F. Geissmann, C. Auffray, R. Palframan et al., “Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses,” Immunology and Cell Biology, vol. 86, no. 5, pp. 398–408, 2008.
[67]  B. Chazaud, M. Brigitte, H. Yacoub-Youssef et al., “Dual and beneficial roles of macrophages during skeletal muscle regeneration,” Exercise and Sport Sciences Reviews, vol. 37, no. 1, pp. 18–22, 2009.
[68]  R. D. Stout, C. Jiang, B. Matta, I. Tietzel, S. K. Watkins, and J. Suttles, “Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences,” The Journal of Immunology, vol. 175, no. 1, pp. 342–349, 2005.
[69]  A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati, “The chemokine system in diverse forms of macrophage activation and polarization,” Trends in Immunology, vol. 25, no. 12, pp. 677–686, 2004.
[70]  S. S. Rabinowitz and S. Gordon, “Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli,” Journal of Experimental Medicine, vol. 174, no. 4, pp. 827–836, 1991.
[71]  M. P. Ramprasad, W. Fischer, J. L. Witztum, G. R. Sambrano, O. Quehenberger, and D. Steinberg, “The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 21, pp. 9580–9584, 1995.
[72]  B. B. Krippendorf and D. A. Riley, “Distinguishing unloading-versus reloading-induced changes in rat soleus muscle,” Muscle & Nerve, vol. 16, no. 1, pp. 99–108, 1993.
[73]  B. Deng, M. Wehling-Henricks, S. A. Villalta, Y. Wang, and J. G. Tidball, “IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration,” Journal of Immunology, vol. 189, no. 7, pp. 3669–3680, 2012.
[74]  T. Lawrence and G. Natoli, “Transcriptional regulation of macrophage polarization: enabling diversity with identity,” Nature Reviews Immunology, vol. 11, no. 11, pp. 750–761, 2011.
[75]  R. Mounier, M. Théret, L. Arnold et al., “AMPKα1 regulates macrophage skewing at the time of resolution of inflammation during skeletal muscle regeneration,” Cell Metabolism, vol. 18, no. 2, pp. 251–264, 2013.
[76]  D. Sag, D. Carling, R. D. Stout, and J. Suttles, “Adenosine 5′-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype,” Journal of Immunology, vol. 181, no. 12, pp. 8633–8641, 2008.
[77]  V. Krishnan and B. C. Yaden, “Macrofinancing efficient remodeling of damaged muscle tissue,” Cell Metabolism, vol. 18, no. 2, pp. 149–151, 2013.
[78]  Y. Bordon, “Macrophages: metabolic master prompts a change of tack,” Nature Reviews Immunology, vol. 13, p. 706, 2013.
[79]  O. Takeuch and S. Akira, “Epigenetic control of macrophage polarization,” European Journal of Immunology, vol. 41, no. 9, pp. 2490–2493, 2011.
[80]  S. Banerjee, H. Cui, N. Xie et al., “miR-125a-5p regulates differential activation of macrophages and inflammation,” The Journal of Biological Chemistry, vol. 288, no. 49, pp. 35428–35436, 2013.
[81]  S. Banerjee, N. Xie, H. Cui et al., “MicroRNA let-7c regulates macrophage polarization,” Journal of Immunology, vol. 190, no. 12, pp. 6542–6549, 2013.
[82]  J. G. Tidball and S. A. Villalta, “Regulatory interactions between muscle and the immune system during muscle regeneration,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 298, no. 5, pp. R1173–R1187, 2010.
[83]  S. A. Villalta, H. X. Nguyen, B. Deng, T. Gotoh, and J. G. Tidbal, “Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy,” Human Molecular Genetics, vol. 18, no. 3, pp. 482–496, 2009.
[84]  M. R. Douglas, K. E. Morrison, M. Salmon, and C. D. Buckley, “Why does inflammation persist: a dominant role for the stromal microenvironment?” Expert Reviews in Molecular Medicine, vol. 4, no. 25, pp. 1–18, 2002.
[85]  A. Mauro, “Satellite cell of skeletal muscle fibers,” The Journal of Biophysical and Biochemical Cytology, vol. 9, pp. 493–495, 1961.
[86]  J. Scharner and P. S. Zammit, “The muscle satellite cell at 50: the formative years,” Skeletal Muscle, vol. 1, no. 1, article 28, 2011.
[87]  B. Gayraud-Morel, F. Chrétien, and S. Tajbakhsh, “Skeletal muscle as a paradigm for regenerative biology and medicine,” Regenerative Medicine, vol. 4, no. 2, pp. 293–319, 2009.
[88]  P. S. Zammit, J. P. Golding, Y. Nagata, V. Hudon, T. A. Partridge, and J. R. Beauchamp, “Muscle satellite cells adopt divergent fates: a mechanism for self-renewal?” The Journal of Cell Biology, vol. 166, no. 3, pp. 347–357, 2004.
[89]  R. Tatsumi, J. E. Anderson, C. J. Nevoret, O. Halevy, and R. E. Allen, “HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells,” Developmental Biology, vol. 194, no. 1, pp. 114–128, 1998.
[90]  A. Irintchev, M. Zeschnigk, A. Starzinski-Powitz, and A. Wernig, “Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles,” Developmental Dynamics, vol. 199, no. 4, pp. 326–337, 1994.
[91]  D. J. Garry, Q. Yang, R. Bassel-Duby, and R. S. Williams, “Persistent expression of MNF identifies myogenic stem cells in postnatal muscles,” Developmental Biology, vol. 188, no. 2, pp. 280–294, 1997.
[92]  G. Mechtersheimer, M. Staudter, and P. Moller, “Expression of the natural killer (NK) cell-associated antigen CD56(Leu- 19), which is identical to the 140-kDa isoform of N-CAM, in neural and skeletal muscle cells and tumors derived therefrom,” Annals of the New York Academy of Sciences, vol. 650, pp. 311–316, 1992.
[93]  D. D. Cornelison, M. S. Filla, H. M. Stanley, A. C. Rapraeger, and B. B. Olwin, “Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration,” Developmental Biology, vol. 239, no. 1, pp. 79–94, 2001.
[94]  J. R. Beauchamp, L. Heslop, D. S. W. Yu et al., “Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells,” Journal of Cell Biology, vol. 151, no. 6, pp. 1221–1234, 2000.
[95]  D. Volonte, Y. Liu, and F. Galbiati, “The modulation of caveolin-1 expression controls satellite cell activation during muscle repair,” FASEB Journal, vol. 19, no. 2, pp. 237–239, 2005.
[96]  K. Schmidt, G. Glaser, A. Wernig, M. Wegner, and O. Rosorius, “Sox8 is a specific marker for muscle satellite cells and inhibits myogenesis,” The Journal of Biological Chemistry, vol. 278, no. 32, pp. 29769–29775, 2003.
[97]  H. J. Lee, W. G?ring, M. Ochs et al., “Sox15 is required for skeletal muscle regeneration,” Molecular and Cellular Biology, vol. 24, no. 19, pp. 8428–8436, 2004.
[98]  T. L. Jesse, R. LaChance, M. F. Iademarco, and D. C. Dean, “Interferon regulatory factor-2 is a transcriptional activator in muscle where it regulates expression of vascular cell adhesion molecule-1,” Journal of Cell Biology, vol. 140, no. 5, pp. 1265–1276, 1998.
[99]  V. F. Gnocchi, R. B. White, Y. Ono, J. A. Ellis, and P. S. Zammit, “Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells,” PLoS ONE, vol. 4, no. 4, Article ID e5205, 2009.
[100]  R. I. Sherwood, J. L. Christensen, I. M. Conboy et al., “Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle,” Cell, vol. 119, no. 4, pp. 543–554, 2004.
[101]  S. Fukada, A. Uezumi, M. Ikemoto et al., “Molecular signature of quiescent satellite cells in adult skeletal muscle,” Stem Cells, vol. 25, no. 10, pp. 2448–2459, 2007.
[102]  S. Fukada, M. Yamaguchi, H. Kokubo et al., “Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers,” Development, vol. 138, no. 21, pp. 4609–4619, 2011.
[103]  F. Relaix, D. Montarras, S. Zaffran et al., “Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells,” Journal of Cell Biology, vol. 172, no. 1, pp. 91–102, 2006.
[104]  M. Buckingham, “Skeletal muscle progenitor cells and the role of Pax genes,” Comptes Rendus—Biologies, vol. 330, no. 6-7, pp. 530–533, 2007.
[105]  S. Creuzet, L. Lescaudron, Z. Li, and J. Fontaine-Pérus, “MyoD, myogenin, and desmin-nls-lacZ transgene emphasize the distinct patterns of satellite cell activation in growth and regeneration,” Experimental Cell Research, vol. 243, no. 2, pp. 241–253, 1998.
[106]  Z. Yablonka-Reuveni and A. J. Rivera, “Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers,” Developmental Biology, vol. 164, no. 2, pp. 588–603, 1994.
[107]  P. S. Zammit, T. A. Partridge, and Z. Yablonka-Reuveni, “The skeletal muscle satellite cell: the stem cell that came in from the cold,” Journal of Histochemistry & Cytochemistry, vol. 54, no. 11, pp. 1177–1191, 2006.
[108]  K. Day, G. Shefer, A. Shearer, and Z. Yablonka-Reuveni, “The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny,” Developmental Biology, vol. 340, no. 2, pp. 330–343, 2010.
[109]  Z. Yablonka-Reuveni, M. A. Rudnicki, A. J. Rivera, M. Primig, J. E. Anderson, and P. Natanson, “The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD,” Developmental Biology, vol. 210, no. 2, pp. 440–455, 1999.
[110]  L. Boldrin, F. Muntoni, and J. E. Morgan, “Are human and mouse satellite cells really the same?” Journal of Histochemistry and Cytochemistry, vol. 58, no. 11, pp. 941–955, 2010.
[111]  K. Day, G. Shefer, J. B. Richardson, G. Enikolopov, and Z. Yablonka-Reuveni, “Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells,” Developmental Biology, vol. 304, no. 1, pp. 246–259, 2007.
[112]  Y. Nagata, H. Kobayashi, M. Umeda et al., “Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells,” Journal of Histochemistry and Cytochemistry, vol. 54, no. 4, pp. 375–384, 2006.
[113]  F. Relaix and P. S. Zammit, “Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage,” Development, vol. 139, no. 16, pp. 2845–2856, 2012.
[114]  Z. Yablonka-Reuveni, K. Day, A. Vine, and G. Shefer, “Defining the transcriptional signature of skeletal muscle stem cells,” Journal of Animal Science, vol. 86, supplement 14, pp. E207–E216, 2008.
[115]  I. M. Conboy and T. A. Rando, “The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis,” Developmental Cell, vol. 3, no. 3, pp. 397–409, 2002.
[116]  S. Kuang, K. Kuroda, F. Le Grand, and M. A. Rudnicki, “Asymmetric self-renewal and commitment of satellite stem cells in muscle,” Cell, vol. 129, no. 5, pp. 999–1010, 2007.
[117]  K. Schuster-Gossler, R. Cordes, and A. Gossler, “Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 2, pp. 537–542, 2007.
[118]  C. R. R. Bjornson, T. H. Cheung, L. Liu, P. V. Tripathi, K. M. Steeper, and T. A. Rando, “Notch signaling is necessary to maintain quiescence in adult muscle stem cells,” Stem Cells, vol. 30, no. 2, pp. 232–242, 2012.
[119]  P. Mourikis, R. Sambasivan, D. Castel, P. Rocheteau, V. Bizzarro, and S. Tajbakhsh, “A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state,” Stem Cells, vol. 30, no. 2, pp. 243–252, 2012.
[120]  Y. Wen, P. Bi, W. Liu, A. Asakura, C. Keller, and S. Kuang, “Constitutive Notch Activation Upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells,” Molecular and Cellular Biology, vol. 32, no. 12, pp. 2300–2311, 2012.
[121]  R. M. George, S. Biressi, B. J. Beres et al., “Numb-deficient satellite cells have regeneration and proliferation defects,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, pp. 18549–18554, 2013.
[122]  A. S. Brack, I. M. Conboy, M. J. Conboy, J. Shen, and T. A. Rando, “A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis,” Cell Stem Cell, vol. 2, no. 1, pp. 50–59, 2008.
[123]  A. J. Wagers, “Wnt not, waste not,” Cell Stem Cell, vol. 2, no. 1, pp. 6–7, 2008.
[124]  Z. Yan, S. Choi, X. Liu et al., “Highly coordinated gene regulation in mouse skeletal muscle regeneration,” The Journal of Biological Chemistry, vol. 278, no. 10, pp. 8826–8836, 2003.
[125]  L. Giordani and P. L. Puri, “Epigenetic control of skeletal muscle regeneration: integrating genetic determinants and environmental changes,” FEBS Journal, vol. 280, no. 17, pp. 4014–4025, 2013.
[126]  D. Cacchiarelli, J. Martone, E. Girardi et al., “MicroRNAs involved in molecular circuitries relevant for the duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway,” Cell Metabolism, vol. 12, no. 4, pp. 341–351, 2010.
[127]  T. H. Cheung, N. L. Quach, G. W. Charville et al., “Maintenance of muscle stem-cell quiescence by microRNA-489,” Nature, vol. 482, no. 7386, pp. 524–528, 2012.
[128]  R. Bischoff, “The satellite cell and muscle regeneration,” in Myology, A. G. Engel and C. Franzini-Armstrong, Eds., pp. 97–118, McGraw-Hill, New York, NY, USA, 1994.
[129]  E. Schultz and B. H. Lipton, “Skeletal muscle satellite cells: changes in proliferation potential as a function of age,” Mechanisms of Ageing and Development, vol. 20, no. 4, pp. 377–383, 1982.
[130]  M. D. Grounds and J. K. McGeachie, “A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis,” Cell and Tissue Research, vol. 250, no. 3, pp. 563–569, 1987.
[131]  F. P. Moss and C. P. Leblond, “Satellite cells as the source of nuclei in muscles of growing rats,” Anatomical Record, vol. 170, no. 4, pp. 421–435, 1971.
[132]  E. Schultz, “Satellite cell proliferative compartments in growing skeletal muscles,” Developmental Biology, vol. 175, no. 1, pp. 84–94, 1996.
[133]  P. Rocheteau, B. Gayraud-Morel, I. Siegl-Cachedenier, M. A. Blasco, and S. Tajbakhsh, “A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division,” Cell, vol. 148, no. 1-2, pp. 112–125, 2012.
[134]  S. Günther, J. Kim, S. Kostin, C. Lepper, C. Fan, and T. Braun, “Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells,” Cell Stem Cell, vol. 13, pp. 590–601, 2013.
[135]  S. Oustanina, G. Hause, and T. Braun, “Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification,” EMBO Journal, vol. 23, no. 16, pp. 3430–3439, 2004.
[136]  C. Lepper, S. J. Conway, and C. M. Fan, “Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements,” Nature, vol. 460, no. 7255, pp. 627–631, 2009.
[137]  J. von Maltzahn, A. E. Jones, R. J. Parks, and M. A. Rudnicki, “Pax7 is critical for the normal function of satellite cells in adult skeletal muscle,” Proceedings of the National Academy of Sciences of the USA, vol. 110, no. 41, pp. 16474–16479, 2013.
[138]  G. Messina, S. Biressi, and G. Cossu, “Non muscle stem cells and muscle regeneration,” in Skeletal Muscle Repair and Regeneration, S. Schiaffino and T. Partridge, Eds., Advances in Muscle Research, pp. 65–84, Springer, Dordrecht, The Netherlands, 2008.
[139]  L. de Angelis, L. Berghella, M. Coletta et al., “Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration,” Journal of Cell Biology, vol. 147, no. 4, pp. 869–877, 1999.
[140]  S. Kuang, S. B. Chargé, P. Seale, M. Huh, and M. A. Rudnicki, “Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis,” Journal of Cell Biology, vol. 172, no. 1, pp. 103–113, 2006.
[141]  A. Polesskaya, P. Seale, and M. A. Rudnicki, “Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration,” Cell, vol. 113, no. 7, pp. 841–852, 2003.
[142]  T. Tamaki, A. Akatsuka, K. Ando et al., “Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle,” The Journal of Cell Biology, vol. 157, no. 4, pp. 571–577, 2002.
[143]  K. J. Mitchell, A. Pannérec, B. Cadot et al., “Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development,” Nature Cell Biology, vol. 12, no. 3, pp. 257–266, 2010.
[144]  M. C. Valero, H. D. Huntsman, J. Liu, K. Zou, and M. D. Boppart, “Eccentric exercise facilitates mesenchymal stem cell appearance in skeletal muscle,” PLoS ONE, vol. 7, no. 1, Article ID e29760, 2012.
[145]  M. N. Wosczyna, A. A. Biswas, C. A. Cogswell, and D. J. Goldhamer, “Multipotent progenitors resident in the skeletal muscle interstitium exhibit robust BMP-dependent osteogenic activity and mediate heterotopic ossification,” Journal of Bone and Mineral Research, vol. 27, no. 5, pp. 1004–1017, 2012.
[146]  A. Asakura, P. Seale, A. Girgis-Gabardo, and M. A. Rudnicki, “Myogenic specification of side population cells in skeletal muscle,” Journal of Cell Biology, vol. 159, no. 1, pp. 123–134, 2002.
[147]  E. Gussoni, Y. Soneoka, C. D. Strickland et al., “Dystrophin expression in the mdx mouse restored by stem cell transplantation,” Nature, vol. 401, no. 6751, pp. 390–394, 1999.
[148]  A. Uezumi, T. Ito, D. Morikawa et al., “Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle,” Journal of Cell Science, vol. 124, no. 21, pp. 3654–3664, 2011.
[149]  A. Uezumi, S. Fukada, N. Yamamoto, S. Takeda, and K. Tsuchida, “Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle,” Nature Cell Biology, vol. 12, no. 2, pp. 143–152, 2010.
[150]  S. E. Mutsaers, J. E. Bishop, G. McGrouther, and G. J. Laurent, “Mechanisms of tissue repair: from wound healing to fibrosis,” The International Journal of Biochemistry & Cell Biology, vol. 29, no. 1, pp. 5–17, 1997.
[151]  A. W. Joe, L. Yi, A. Natarajan et al., “Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis,” Nature Cell Biology, vol. 12, no. 2, pp. 153–163, 2010.
[152]  M. D. Grounds, “Complexity of extracellular matrix and skeletal muscle regeneration,” in Skeletal Muscle Repair and Regeneration, S. Schiaffino and T. Partridge, Eds., Advances in Muscle Research, pp. 269–301, Springer, Amsterdam, The Netherlands, 2008.
[153]  C. J. Mann, E. Perdiguero, Y. Kharraz et al., “Aberrant repair and fibrosis development in skeletal muscle,” Skeletal Muscle, vol. 1, no. 1, article 21, 2011.
[154]  G. Lluri, G. D. Langlois, B. McClellan, P. D. Soloway, and D. M. Jaworski, “Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates neuromuscular junction development via a beta1 integrin-mediated mechanism,” Journal of Neurobiology, vol. 66, no. 12, pp. 1365–1377, 2006.
[155]  Y. Li, W. Foster, B. M. Deasy et al., “Transforming growth factor–β1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis,” The American Journal of Pathology, vol. 164, no. 3, pp. 1007–1019, 2004.
[156]  P. E. Mozdziak, P. M. Pulvermacher, and E. Schultz, “Muscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading,” Journal of Applied Physiology, vol. 91, no. 1, pp. 183–190, 2001.
[157]  P. O. Mitchell and G. K. Pavlath, “Skeletal muscle atrophy leads to loss and dysfunction of muscle precursor cells,” American Journal of Physiology: Cell Physiology, vol. 287, no. 6, pp. C1753–C1762, 2004.
[158]  C. R. Slater and S. Schiaffino, “Skeletal muscle repair and regeneration,” in Advances in Muscle Research, S. Schiaffino and T. Partridge, Eds., pp. 303–334, Springer, Amsterdam, The Netherlands, 2008.
[159]  S. Sartore, L. Gorza, and S. Schiaffino, “Fetal myosin heavy chains in regenerating muscle,” Nature, vol. 298, no. 5871, pp. 294–296, 1982.
[160]  R. G. Whalen, J. B. Harris, G. S. Butler-Browne, and S. Sesodia, “Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles,” Developmental Biology, vol. 141, no. 1, pp. 24–40, 1990.
[161]  K. Esser, P. Gunning, and E. Hardeman, “Nerve-dependent and -independent patterns of mRNA expression in regenerating skeletal muscle,” Developmental Biology, vol. 159, no. 1, pp. 173–183, 1993.
[162]  M. Vinciguerra, A. Musaro, and N. Rosenthal, “Regulation of muscle atrophy in aging and disease,” Advances in Experimental Medicine and Biology, vol. 694, pp. 211–233, 2010.
[163]  B. M. Scicchitano, E. Rizzuto, and A. Musarò, “Counteracting muscle wasting in aging and neuromuscular diseases: the critical role of IGF-1,” Aging, vol. 1, no. 5, pp. 451–457, 2009.
[164]  S. Carosio, M. G. Berardinelli, M. Aucello, and A. Musarò, “Impact of ageing on muscle cell regeneration,” Ageing Research Reviews, vol. 10, no. 1, pp. 35–42, 2011.
[165]  A. L. Serrano, C. J. Mann, B. Vidal, E. Ardite, E. Perdiguero, and P. Mu?oz-Cánoves, “Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease,” Current Topics in Developmental Biology, vol. 96, pp. 167–201, 2011.
[166]  B. M. Carlson and J. A. Faulkner, “Muscle transplantation between young and old rats: age of host determines recovery,” The American Journal of Physiology: Cell Physiology, vol. 256, no. 6, pp. C1262–C1266, 1989.
[167]  B. M. Carlson, E. I. Dedkov, A. B. Borisov, and J. A. Faulkner, “Skeletal muscle regeneration in very old rats,” Journals of Gerontology A Biological Sciences and Medical Sciences, vol. 56, no. 5, pp. B224–B233, 2001.
[168]  I. M. Conboy, M. J. Conboy, A. J. Wagers, E. R. Girma, I. L. Weismann, and T. A. Rando, “Rejuvenation of aged progenitor cells by exposure to a young systemic environment,” Nature, vol. 433, no. 7027, pp. 760–764, 2005.
[169]  M. Le Bihan, A. Bigot, S. S. Jensen et al., “In-depth analysis of the secretome identifies three major independent secretory pathways in differentiating human myoblasts,” Journal of Proteomics, vol. 77, pp. 344–356, 2012.
[170]  M. Bencze, E. Negroni, D. Vallese et al., “Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation,” Molecular Therapy, vol. 20, no. 11, pp. 2168–2179, 2012.
[171]  L. Barberi, B. M. Scicchitano, M. De Rossi et al., “Age-dependent alteration in muscle regeneration: the critical role of tissue niche,” Biogerontology, vol. 14, no. 3, pp. 273–292, 2013.
[172]  P. Paliwal, N. Pishesha, D. Wijaya, and I. M. Conboy, “Age dependent increase in the levels of osteopontin inhibits skeletal muscle regeneration,” Aging, vol. 4, no. 8, pp. 553–566, 2012.
[173]  A. Hirata, S. Masuda, T. Tamura et al., “Expression profiling of cytokines and related genes in regenerating skeletal muscle after cardiotoxin injection: a role for osteopontin,” The American Journal of Pathology, vol. 163, no. 1, pp. 203–215, 2003.
[174]  K. Uaesoontrachoon, H. Yoo, E. M. Tudor, R. N. Pike, E. J. Mackie, and C. N. Pagel, “Osteopontin and skeletal muscle myoblasts: association with muscle regeneration and regulation of myoblast function in vitro,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 10, pp. 2303–2314, 2008.
[175]  S. A. Vetrone, E. Montecino-Rodriguez, E. Kudryashova et al., “Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1583–1594, 2009.
[176]  E. R. Barton, L. Morris, A. Musaro, N. Rosenthal, and H. Lee Sweeney, “Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice,” Journal of Cell Biology, vol. 157, no. 1, pp. 137–147, 2002.
[177]  M. Wehling, M. J. Spencer, and J. G. Tidball, “A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice,” Journal of Cell Biology, vol. 155, no. 1, pp. 123–131, 2001.
[178]  S. A. Villalta, C. Rinaldi, B. Deng, G. Liu, B. Fedor, and J. G. Tidball, “Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype,” Human Molecular Genetics, vol. 20, no. 4, pp. 790–805, 2011.
[179]  P. Sousa-Victor, S. Gutarra, L. García-Prat, et al., “Geriatric muscle stem cells switch reversible quiescence into senescence,” Nature, vol. 506, pp. 316–321, 2014.
[180]  B. D. Cosgrove, P. M. Gilbert, E. Porpiglia et al., “Rejuvenation of the muscle stem cell population restores strength to injured aged muscles,” Nature Medicine, vol. 20, pp. 255–264, 2014.
[181]  M. Li and J. C. Izpisua Belmonte, “Ageing: genetic rejuvenation of old muscle,” Nature, vol. 506, pp. 304–305, 2014.
[182]  M. A. Rudnicki, T. Braun, S. Hinuma, and R. Jaenisch, “Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development,” Cell, vol. 71, no. 3, pp. 383–390, 1992.
[183]  L. A. Sabourin, A. Girgis-Gabardo, P. Scale, A. Asakura, and M. A. Rudnicki, “Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle,” Journal of Cell Biology, vol. 144, no. 4, pp. 631–643, 1999.
[184]  D. D. Cornelison, B. B. Olwin, M. A. Rudnicki, and B. J. Wold, “MyoD-/- satellite cells in single-fiber culture are differentiation defective and MRF4 deficient,” Developmental Biology, vol. 224, no. 2, pp. 122–137, 2000.
[185]  T. Braun, M. A. Rudnicki, H.-. Arnold, and R. Jaenisch, “Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death,” Cell, vol. 71, no. 3, pp. 369–382, 1992.
[186]  S. Tajbakhsh, D. Rocancourt, G. Cossu, and M. Buckingham, “Redefining the genetic hierarchies controlling skeletal myogenesis: pax- 3 and Myf-5 act upstream of MyoD,” Cell, vol. 89, no. 1, pp. 127–138, 1997.
[187]  A. Kaul, M. K?ster, H. Neuhaus, and T. Braun, “Myf-5 revisited: loss of early myotome formation does not lead to a rib phenotype in homozygous Myf-5 mutant mice,” Cell, vol. 102, no. 1, pp. 17–19, 2000.
[188]  J. M. Venuti, J. H. Morris, J. L. Vivian, E. N. Olson, and W. H. Klein, “Myogenin is required for late but not early aspects of myogenesis during mouse development,” Journal of Cell Biology, vol. 128, no. 4, pp. 563–576, 1995.
[189]  J. R. Knapp, J. K. Davie, A. Myer, E. Meadows, E. N. Olson, and W. H. Klein, “Loss of myogenin in postnatal life leads to normal skeletal muscle but reduced body size,” Development, vol. 133, no. 4, pp. 601–610, 2006.
[190]  J. L. Vivian, E. N. Olson, and W. H. Klein, “Thoracic skeletal defects in myogenin- and MRF4-deficient mice correlate with early defects in myotome and intercostal musculature,” Developmental Biology, vol. 224, no. 1, pp. 29–41, 2000.
[191]  A. L. Thompson, G. Filatov, C. Chen et al., “A selective role for MRF4 ininnervated adult skeletal muscle: Na(V) 1.4 Na+ channel expression is reduced in MRF4-null mice,” Gene Expression, vol. 12, pp. 289–303, 2005.

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