Mammalian skeletal muscles are derived from mesoderm segments flanking the embryonic midline. Upon receiving inductive cues from the adjacent neural tube, lateral plate mesoderm, and surface ectoderm, muscle precursors start to delaminate, migrate to their final destinations and proliferate. Muscle precursor cells become committed to the myogenic fate, become differentiated muscle cells, and fuse to form myofibers. Myofibers then fuse together to form the muscle groups. Muscle precursor cells have the ability to proliferate, and differentiate during development, while a subset remains capable of regeneration and repair of local injuries in adulthood. When the process of muscle development is perturbed such as in muscular dystrophies and injuries, ways to intervene and allow for proper muscle development or repair are the focus of regenerative medicine. Thus, understanding the developmental program of muscle at the genetic, cellular, and molecular levels has become a major focus of skeletal muscle regeneration research in the last few years. 1. Introduction Movement and locomotion are common characteristics of all living animals. The vertebrate musculature system that includes cardiac, smooth, and skeletal muscles makes both activities possible. Skeletal muscle is the dominant type of musculature making up about 40% of the adult human body weight, and it is a key player in energy metabolism. Skeletal muscles are attached to bones in the body and their contractions are under voluntary control, unlike cardiac and smooth muscles. Skeletal muscles are composed of many bundles of long, thin, multinucleated myofibers that are made up from cells that systemically proliferate and differentiate throughout development. Adult mature muscles maintain a population of self-renewing cells, satellite cells, which are capable of regeneration and repair. 2. The Genesis of the Muscle Skeletal muscles of the trunk derive from the paraxial somitic mesoderm, whereas skeletal muscles of the head derive mostly from the prechordal and nonsomitic paraxial head mesoderm. Somites develop in a rostral (head) to caudal (tail) order as a result of the segmentation of the presomitic (paraxial) mesoderm that lies on each side of the neural tube and notochord [1]. Somites give rise to the progenitor cells of muscle, cartilage, bone, connective tissue, and dermis, forming between embryonic day (E) E8.0 and E13.0 in mice. As individual somites mature, they receive signals from the adjacent notochord, neural tube, ectoderm, and lateral plate mesoderm (LPM) [2]. In the trunk, the medial and
References
[1]
B. Christ and C. P. Ordahl, “Early stages of chick somite development,” Anatomy and Embryology, vol. 191, no. 5, pp. 381–396, 1995.
[2]
A. E. Munsterberg and A. B. Lassar, “Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite,” Development, vol. 121, no. 3, pp. 651–660, 1995.
[3]
C.-M. Fan and M. Tessier-Lavigne, “Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog,” Cell, vol. 79, no. 7, pp. 1175–1186, 1994.
[4]
R. L. Johnson, E. Laufer, R. D. Riddle, and C. Tabin, “Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites,” Cell, vol. 79, no. 7, pp. 1165–1173, 1994.
[5]
J. Wallin, J. Wilting, H. Koseki, R. Fritsch, B. Christ, and R. Balling, “The role of Pax-1 in axial skeleton development,” Development, vol. 120, no. 5, pp. 1109–1121, 1994.
[6]
R. Huang and B. Christ, “Origia of the epaxial and hypaxial myotome in avian embryos,” Anatomy and Embryology, vol. 202, no. 5, pp. 369–374, 2000.
[7]
R. J. Bryson-Richardson and P. D. Currie, “The genetics of vertebrate myogenesis,” Nature Reviews Genetics, vol. 9, no. 8, pp. 632–646, 2008.
[8]
A.-G. Borycki, B. Brunk, S. Tajbakhsh, M. Buckingham, C. Chiang, and C. P. Emerson Jr., “Sonic hedgehog controls epaxial muscle determination through Myf5 activation,” Development, vol. 126, no. 18, pp. 4053–4063, 1999.
[9]
S. Tajbakhsh, U. Borello, E. Vivarelli et al., “Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5,” Development, vol. 125, no. 21, pp. 4155–4162, 1998.
[10]
L. Cheng, L. E. Alvares, M. U. Ahmed, A. S. El-Hanfy, and S. Dietrich, “The epaxial-hypaxial subdivision of the avian somite,” Developmental Biology, vol. 274, no. 2, pp. 348–369, 2004.
[11]
B. Christ and B. Brand-Saberi, “Limb muscle development,” International Journal of Developmental Biology, vol. 46, no. 7, pp. 905–914, 2002.
[12]
G. Kardon, B. D. Harfe, and C. J. Tabin, “A Tcf4-positive mesodermal population provides a prepattern for vertebrate limb muscle patterning,” Developmental Cell, vol. 5, no. 6, pp. 937–944, 2003.
[13]
R. Sambasivan, S. Kuratani, and S. Tajbakhsh, “An eye on the head: the development and evolution of craniofacial muscles,” Development, vol. 138, no. 12, pp. 2401–2415, 2011.
[14]
S. Dietrich, F. Abou-Rebyeh, H. Brohmann et al., “The role of SF/HGF and c-Met in the development of skeletal muscle,” Development, vol. 126, no. 8, pp. 1621–1629, 1999.
[15]
S. Dietrich, F. R. Schubert, C. Healy, P. T. Sharpe, and A. Lumsden, “Specification of the hypaxial musculature,” Development, vol. 125, no. 12, pp. 2235–2249, 1998.
[16]
L. E. Alvares, F. R. Schubert, C. Thorpe et al., “Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors,” Developmental Cell, vol. 5, no. 3, pp. 379–390, 2003.
[17]
R. C. Mootoosamy and S. Dietrich, “Distinct regulatory cascades for head and trunk myogenesis,” Development, vol. 129, no. 3, pp. 573–583, 2002.
[18]
F. Relaix, D. Rocancourt, A. Mansouri, and M. Buckingham, “A Pax3/Pax7-dependent population of skeletal muscle progenitor cells,” Nature, vol. 435, no. 7044, pp. 948–953, 2005.
[19]
L. Kassar-Duchossoy, E. Giacone, B. Gayraud-Morel, A. Jory, D. Gomès, and S. Tajbakhsh, “Pax3/Pax7 mark a novel population of primitive myogenic cells during development,” Genes and Development, vol. 19, no. 12, pp. 1426–1431, 2005.
[20]
F. R. Schubert, P. Tremblay, A. Mansouri et al., “Early mesodermal phenotypes in Splotch suggest a role for Pax3 in the formation of epithelial somites,” Developmental Dynamics, vol. 222, no. 3, pp. 506–521, 2001.
[21]
F. Relaix, D. Rocancourt, A. Mansouri, and M. Buckingham, “Divergent functions of murine Pax3 and Pax7 in limb muscle development,” Genes and Development, vol. 18, no. 9, pp. 1088–1105, 2004.
[22]
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.
[23]
E. Bober, T. Franz, H.-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.
[24]
R. Grifone, J. Demignon, C. Houbron et al., “Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo,” Development, vol. 132, no. 9, pp. 2235–2249, 2005.
[25]
R. Grifone, J. Demignon, J. Giordani et al., “Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo,” Developmental Biology, vol. 302, no. 2, pp. 602–616, 2007.
[26]
C. Niro, J. Demignon, S. Vincent et al., “Six1 and Six4 gene expression is necessary to activate the fast-type muscle gene program in the mouse primary myotome,” Developmental Biology, vol. 338, no. 2, pp. 168–182, 2010.
[27]
H. Weintraub, V. J. Dwarki, I. Verma et al., “Muscle-specific transcriptional activation by MyoD,” Genes and Development, vol. 5, no. 8, pp. 1377–1386, 1991.
[28]
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.
[29]
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.
[30]
T. Braun, M. A. Rudnicki, H.-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.
[31]
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.
[32]
M. Maroto, R. Reshef, A. E. Münsterberg, S. Koester, M. Goulding, and A. B. Lassar, “Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue,” Cell, vol. 89, no. 1, pp. 139–148, 1997.
[33]
M. K. Gross, L. Moran-Rivard, T. Velasquez, M. N. Nakatsu, K. Jagla, and M. Goulding, “Lbx1 is required for muscle precursor migration along a lateral pathway into the limb,” Development, vol. 127, no. 2, pp. 413–424, 2000.
[34]
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.
[35]
B. Kablar, K. Krastel, C. Ying, A. Asakura, S. J. Tapscott, and M. A. Rudnicki, “MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle,” Development, vol. 124, no. 23, pp. 4729–4738, 1997.
[36]
Y. Wang and R. Jaenisch, “Myogenin can substitute for Myf5 in promoting myogenesis but less efficiently,” Development, vol. 124, no. 13, pp. 2507–2513, 1997.
[37]
R. Eckner, T.-P. Yao, E. Oldread, and D. M. Livingston, “Interaction and functional collaboration of p300/CBP and bHLH proteins in muscle and B-cell differentiation,” Genes and Development, vol. 10, no. 19, pp. 2478–2490, 1996.
[38]
P. L. Puri, V. Sartorelli, X.-J. Yang et al., “Differential roles of p300 and PCAF acetyltransferases in muscle differentiation,” Molecular Cell, vol. 1, no. 1, pp. 35–45, 1997.
[39]
V. Sartorelli, P. L. Puri, Y. Hamamori et al., “Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program,” Molecular Cell, vol. 4, no. 5, pp. 725–734, 1999.
[40]
P. H. Francis-West, L. Antoni, and K. Anakwe, “Regulation of myogenic differentiation in the developing limb bud,” Journal of Anatomy, vol. 202, no. 1, pp. 69–81, 2003.
[41]
M. Murphy and G. Kardon, “Origin of vertebrate limb muscle: the role of progenitor and myoblast populations,” Current Topics in Developmental Biology, vol. 96, pp. 1–32, 2011.
[42]
K. Kitamura, H. Miura, S. Miyagawa-Tomita et al., “Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism,” Development, vol. 126, no. 24, pp. 5749–5758, 1999.
[43]
M.-F. Lu, C. Pressman, R. Dyer, R. L. Johnson, and J. F. Martin, “Function of rieger syndrome gene in left-right asymmetry and craniofacial development,” Nature, vol. 401, no. 6750, pp. 276–278, 1999.
[44]
C. R. Lin, C. Kloussi, S. O'Connell et al., “Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis,” Nature, vol. 401, no. 6750, pp. 279–282, 1999.
[45]
P. J. Gage, H. Suh, and S. A. Camper, “Dosage requirement of Pitx2 for development of multiple organs,” Development, vol. 126, no. 20, pp. 4643–4651, 1999.
[46]
H. P. Shih, M. K. Gross, and C. Kioussi, “Expression pattern of the homeodomain transcription factor Pitx2 during muscle development,” Gene Expression Patterns, vol. 7, no. 4, pp. 441–451, 2007.
[47]
A. L'Honoré, J.-F. Ouimette, M. Lavertu-Jolin, and J. Drouin, “Pitx2 defines alternate pathways acting through MyoD during limb and somitic myogenesis,” Development, vol. 137, no. 22, pp. 3847–3856, 2010.
[48]
T. Hilton, M. K. Gross, and C. Kioussi, “Pitx2-dependent occupancy by histone deacetylases is associated with t-box gene regulation in mammalian abdominal tissue,” Journal of Biological Chemistry, vol. 285, no. 15, pp. 11129–11142, 2010.
[49]
D. Eng, H. Y. Ma, J. Xu, H. P. Shih, M. K. Gross, and C. Kiouss, “Loss of abdominal muscle in Pitx2 mutants associated with altered axial specification of lateral plate mesoderm,” PLoS ONE, vol. 7, no. 7, Article ID e42228, 2012.
[50]
C. Kioussi, P. Briata, S. H. Baek et al., “Identification of a Wnt/Dvl/β-catenin → Pitx2 pathway mediating cell-type-specific proliferation during development,” Cell, vol. 111, no. 5, pp. 673–685, 2002.
[51]
A. L. Campbell, H.-P. Shih, J. Xu, M. K. Gross, and C. Kioussi, “Regulation of motility of myogenic cells in filling limb muscle anlagen by Pitx2,” PLoS ONE, vol. 7, no. 4, Article ID e35822, 2012.
[52]
C. Birchmeier and H. Brohmann, “Genes that control the development of migrating muscle precursor cells,” Current Opinion in Cell Biology, vol. 12, no. 6, pp. 725–730, 2000.
[53]
E. Lozano-Velasco, A. Contreras, C. Crist, F. Hernández-Torres, D. Franco, and A. E. Aránega, “Pitx2c modulates Pax3+/Pax7+ cell populations and regulates Pax3 expression by repressing miR27 expression during myogenesis,” Developmental Biology, vol. 357, no. 1, pp. 165–178, 2011.
[54]
A. J. Harris, M. J. Duxson, R. B. Fitzsimons, and F. Rieger, “Myonuclear birthdates distinguish the origins of primary and secondary myotubes in embryonic mammalian skeletal muscles,” Development, vol. 107, no. 4, pp. 771–784, 1989.
[55]
D. A. Hutcheson, J. Zhao, A. Merrell, M. Haldar, and G. Kardon, “Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for β-catenin,” Genes and Development, vol. 23, no. 8, pp. 997–1013, 2009.
[56]
G. Messina, S. Biressi, S. Monteverde et al., “Nfix regulates fetal-specific transcription in developing skeletal muscle,” Cell, vol. 140, no. 4, pp. 554–566, 2010.
[57]
J. J. Mccarthy, J. Mula, M. Miyazaki et al., “Effective fiber hypertrophy in satellite cell-depleted skeletal muscle,” Development, vol. 138, no. 17, pp. 3657–3666, 2011.
[58]
I. W. McKinnell, J. Ishibashi, F. Le Grand et al., “Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex,” Nature Cell Biology, vol. 10, no. 1, pp. 77–84, 2008.
[59]
R. E. Allen, S. M. Sheehan, R. G. Taylor, T. L. Kendall, and G. M. Rice, “Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro,” Journal of Cellular Physiology, vol. 165, no. 2, pp. 307–312, 1995.
[60]
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.
[61]
H. Yin, F. Price, and M. A. Rudnicki, “Satellite cells and the muscle stem cell niche,” Physiological Reviews, vol. 93, no. 1, pp. 23–67, 2013.
[62]
J. Gagan, B. K. Dey, and A. Dutta, “MicroRNAs regulate and provide robustness to the myogenic transcriptional network,” Current Opinion in Pharmacology, vol. 12, no. 3, pp. 383–388, 2012.
[63]
H. Guo, N. T. Ingolia, J. S. Weissman, and D. P. Bartel, “Mammalian microRNAs predominantly act to decrease target mRNA levels,” Nature, vol. 466, no. 7308, pp. 835–840, 2010.
[64]
E. Bernstein, S. Y. Kim, M. A. Carmell et al., “Dicer is essential for mouse development,” Nature Genetics, vol. 35, pp. 215–217, 2003.
[65]
J. R. O'Rourke, S. A. Georges, H. R. Seay et al., “Essential role for Dicer during skeletal muscle development,” Developmental Biology, vol. 311, no. 2, pp. 359–368, 2007.
[66]
Y. Ge and J. Chen, “MicroRNAs in skeletal myogenesis,” Cell Cycle, vol. 10, no. 3, pp. 441–448, 2011.
[67]
B. K. Dey, J. Gagan, and A. Dutta, “miR-206 and -486 induce myoblast differentiation by downregulating Pax7,” Molecular and Cellular Biology, vol. 31, no. 1, pp. 203–214, 2011.
[68]
J. Gagan, B. K. Dey, R. Layer, Z. Yan, and A. Dutta, “MicroRNA-378 targets the myogenic repressor MyoR during myoblast differentiation,” Journal of Biological Chemistry, vol. 286, no. 22, pp. 19431–19438, 2011.
[69]
J.-F. Chen, Y. Tao, J. Li et al., “microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7,” Journal of Cell Biology, vol. 190, no. 5, pp. 867–879, 2010.
[70]
M. I. Rosenberg, S. A. Georges, A. Asawachaicharn, E. Analau, and S. J. Tapscott, “MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206,” Journal of Cell Biology, vol. 175, no. 1, pp. 77–85, 2006.
[71]
C. Anderson, H. Catoe, and R. Werner, “MIR-206 regulates connexin43 expression during skeletal muscle development,” Nucleic Acids Research, vol. 34, no. 20, pp. 5863–5871, 2006.
[72]
Y. Sun, Y. Ge, J. Drnevich, Y. Zhao, M. Band, and J. Chen, “Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis,” Journal of Cell Biology, vol. 189, no. 7, pp. 1157–1169, 2010.
[73]
C. F. Wang and R. L. Tellam, “MicroRNA-26a targets the histone methyltransferase enhancer of zeste homolog 2 during myogenesis,” Journal of Biological Chemistry, vol. 283, no. 15, pp. 9836–9843, 2008.
[74]
A. H. Juan, R. M. Kumar, J. G. Marx, R. A. Young, and V. Sartorelli, “Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells,” Molecular Cell, vol. 36, no. 1, pp. 61–74, 2009.
[75]
H. Wang, R. Garzon, H. Sun et al., “NF-κB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma,” Cancer Cell, vol. 14, no. 5, pp. 369–381, 2008.
[76]
E. van Rooij, L. B. Sutherland, J. E. Thatcher et al., “Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 35, pp. 13027–13032, 2008.
[77]
C. G. Crist, D. Montarras, G. Pallafacchina et al., “Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 32, pp. 13383–13387, 2009.
[78]
W. J. R. Longabaugh, E. H. Davidson, and H. Bolouri, “Visualization, documentation, analysis, and communication of large-scale gene regulatory networks,” Biochimica et Biophysica Acta, vol. 1789, no. 4, pp. 363–374, 2009.