Abstract
Skeletal muscles are part of the musculoskeletal system which also includes nerves, tendons, connective tissue, bones and blood vessels. Here we review the development of axial and limb muscles in amniotes within the context of their surrounding tissues in vivo. We highlight the reciprocal dialogue mediated by signalling factors between cells of these adjacent tissues and developing muscles and also demonstrate its importance from the onset of muscle cell differentiation well into foetal development. Early embryonic tissues secrete factors which are important regulators of myogenesis. However, later muscle development relies on other tissue collaborators, such as developing nerves and connective tissue, which are in turn influenced by the developing muscles themselves. We conclude that skeletal muscle development in vivo is a compelling example of the importance of reciprocal interactions between developing tissues for the complete and coordinated development of a functional system.
References
Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235(5):1194–1218
Engel AG, Franzini-Armstrong C (2004) Myology, vol 1, 3rd edn. Mc Graw Hill Professional
Biressi S, Molinaro M, Cossu G (2007) Cellular heterogeneity during vertebrate skeletal muscle development. Dev Biol 308(2):281–293
Emerson CPJ, Hauschka SD (2004) The embryonic origin of muscle. In: Myology, vol 1, 3rd edn. Mc Graw Hill Professional, pp 3–44
Tajbakhsh S (2009) Skeletal muscle stem cells in developmental versus regenerative myogenesis. J Intern Med 266(4):372–389
Buckingham M, Rigby PW (2014) Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell 28(3):225–238. doi:10.1016/j.devcel.2013.12.020
Bryson-Richardson RJ, Currie PD (2008) The genetics of vertebrate myogenesis. Nat Rev Genet 9(8):632–646. doi:10.1038/nrg2369
Merrell AJ, Ellis BJ, Fox ZD, Lawson JA, Weiss JA, Kardon G (2015) Muscle connective tissue controls development of the diaphragm and is a source of congenital diaphragmatic hernias. Nat Genet 47(5):496–504. doi:10.1038/ng.3250
Mayeuf-Louchart A, Montarras D, Bodin C, Kume T, Vincent SD, Buckingham M (2016) Endothelial cell specification in the somite is compromised in Pax3-positive progenitors of Foxc1/2 conditional mutants, with loss of forelimb myogenesis. Development 143(5):872–879. doi:10.1242/dev.128017
Yumoto N, Kim N, Burden SJ (2012) Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses. Nature 489(7416):438–442. doi:10.1038/nature11348
Burden SJ, Yumoto N, Zhang W (2013) The role of MuSK in synapse formation and neuromuscular disease. Cold Spring Harb Perspect Biol 5(5):a009167. doi:10.1101/cshperspect.a009167
Theis S, Patel K, Valasek P, Otto A, Pu Q, Harel I, Tzahor E, Tajbakhsh S, Christ B, Huang R (2010) The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 137(17):2961–2971. doi:10.1242/dev.049726
Pu Q, Patel K, Huang R (2015) The lateral plate mesoderm: a novel source of skeletal muscle. Results Probl Cell Differ 56:143–163. doi:10.1007/978-3-662-44608-9_7
Dequéant ML, Pourquié O (2008) Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet 9(5):370–382. doi:10.1038/nrg2320
Pourquié O (2004) The chick embryo: a leading model in somitogenesis studies. Mech Dev 121(9):1069–1079. doi:10.1016/j.mod.2004.05.002
Andrade RP, Palmeirim I, Bajanca F (2007) Molecular clocks underlying vertebrate embryo segmentation: a 10-year-old hairy-go-round. Birth Defects Res C Embryo Today 81(2):65–83. doi:10.1002/bdrc.20094
Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435(7044):948–953
Kalcheim C, Kahane N, Cinnamon Y, Ben-Yair R (2006) Mechanisms of lineage segregation in the avian dermomyotome. Anat Embryol (Berl) 211(Suppl 1):31–36
Atit R, Sgaier SK, Mohamed OA, Taketo MM, Dufort D, Joyner AL, Niswander L, Conlon RA (2006) β-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev Biol 296(1):164–176. doi:10.1016/j.ydbio.2006.04.449
Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scimè A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454(7207):961–967. doi:10.1038/nature07182
Esner M, Meilhac SM, Relaix F, Nicolas JF, Cossu G, Buckingham ME (2006) Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome. Development 133(4):737–749. doi:10.1242/dev.02226
Ben-Yair R, Kalcheim C (2008) Notch and bone morphogenetic protein differentially act on dermomyotome cells to generate endothelium, smooth, and striated muscle. J Cell Biol 180(3):607–618. doi:10.1083/jcb.200707206
Yvernogeau L, Auda-Boucher G, Fontaine-Perus J (2012) Limb bud colonization by somite-derived angioblasts is a crucial step for myoblast emigration. Development 139(2):277–287. doi:10.1242/dev.067678
Ben-Yair R, Kalcheim C (2005) Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132(4):689–701
Hollway G, Currie P (2005) Vertebrate myotome development. Birth Defects Res C Embryo Today 75(3):172–179
Thorsteinsdóttir S, Deries M, Cachaço AS, Bajanca F (2011) The extracellular matrix dimension of skeletal muscle development. Dev Biol 354(2):191–207. doi:10.1016/j.ydbio.2011.03.015
Venters SJ, Thorsteinsdóttir S, Duxson MJ (1999) Early development of the myotome in the mouse. Dev Dyn 216(3):219–232
Pu Q, Abduelmula A, Masyuk M, Theiss C, Schwandulla D, Hans M, Patel K, Brand-Saberi B, Huang R (2013) The dermomyotome ventrolateral lip is essential for the hypaxial myotome formation. BMC Dev Biol 13:37. doi:10.1186/1471-213X-13-37
Gros J, Manceau M, Thomé V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435(7044):954–958
Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S (2005) Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19(12):1426–1431
Christ B, Jacob M, Jacob HJ (1983) On the origin and development of the ventrolateral abdominal muscles in the avian embryo. An experimental and ultrastructural study. Anat Embryol (Berl) 166(1):87–101
Cinnamon Y, Kahane N, Kalcheim C (1999) Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126(19):4305–4315
Deries M, Schweitzer R, Duxson MJ (2010) Developmental fate of the mammalian myotome. Dev Dyn 239(11):2898–2910. doi:10.1002/dvdy.22425
Deries M, Collins JJ, Duxson MJ (2008) The mammalian myotome: a muscle with no innervation. Evol Dev 10(6):746–755
Tosney KW, Landmesser LT (1985) Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. J Neurosci 5(9):2345–2358
Hurren B, Collins JJ, Duxson MJ, Deries M (2015) First neuromuscular contact correlates with onset of primary myogenesis in rat and mouse limb muscles. PLoS One 10(7):e0133811. doi:10.1371/journal.pone.0133811
Cohen A (1938) Myotome fusion in the embryo of Amblystoma punctatum after treatment with lithium and other agents. J Exp Zool 79(3):461–473
Pourquie O, Coltey M, Teillet MA, Ordahl C, Le Douarin NM (1993) Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. Proc Natl Acad Sci USA 90(11):5242–5246
Strudel G (1955) L’action morphogène du tube nerveux et de la corde sur la differénciation des vertèbres et des muscles vertébraux chez l’embryon de poulet. Arch Anat Pathol (Paris) 44(3):209–235
Murtaugh LC, Zeng L, Chyung JH, Lassar AB (2001) The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMP-dependent axial chondrogenesis. Dev Cell 1(3):411–422
Kahane N, Ribes V, Kicheva A, Briscoe J, Kalcheim C (2013) The transition from differentiation to growth during dermomyotome-derived myogenesis depends on temporally restricted hedgehog signaling. Development 140(8):1740–1750. doi:10.1242/dev.092726
Borycki AG, Brunk B, Tajbakhsh S, Buckingham M, Chiang C, Emerson CP Jr (1999) Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 126(18):4053–4063
Kruger M, Mennerich D, Fees S, Schafer R, Mundlos S, Braun T (2001) Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development 128(5):743–752
Anderson C, Thorsteinsdóttir S, Borycki AG (2009) Sonic hedgehog-dependent synthesis of laminin α1 controls basement membrane assembly in the myotome. Development 136(20):3495–3504. doi:10.1242/dev.036087
Borello U, Berarducci B, Murphy P, Bajard L, Buffa V, Piccolo S, Buckingham M, Cossu G (2006) The Wnt/β-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 133(18):3723–3732. doi:10.1242/dev.02517
Gros J, Serralbo O, Marcelle C (2009) WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature 457(7229):589–593
Tajbakhsh S, Borello U, Vivarelli E, Kelly R, Papkoff J, Duprez D, Buckingham M, Cossu G (1998) 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 125(21):4155–4162
Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124(20):3955–3963
Pourquié O, Fan CM, Coltey M, Hirsinger E, Watanabe Y, Breant C, Francis-West P, Brickell P, Tessier-Lavigne M, Le Douarin NM (1996) Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84(3):461–471
Hirsinger E, Duprez D, Jouve C, Malapert P, Cooke J, Pourquié O (1997) Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124(22):4605–4614
Linker C, Lesbros C, Gros J, Burrus LW, Rawls A, Marcelle C (2005) β-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis. Development 132(17):3895–3905. doi:10.1242/dev.01961
Marmigère F, Ernfors P (2007) Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 8(2):114–127. doi:10.1038/nrn2057
Rickmann M, Fawcett JW, Keynes RJ (1985) The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol 90:437–455
Rios AC, Serralbo O, Salgado D, Marcelle C (2011) Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473(7348):532–535. doi:10.1038/nature09970
Deries M, Gonçalves AB, Vaz R, Martins GG, Rodrigues G, Thorsteinsdóttir S (2012) Extracellular matrix remodeling accompanies axial muscle development and morphogenesis in the mouse. Dev Dyn 241(2):350–364. doi:10.1002/dvdy.23703
Martins GG, Rifes P, Amândio R, Rodrigues G, Palmeirim I, Thorsteinsdóttir S (2009) Dynamic 3D cell rearrangements guided by a fibronectin matrix underlie somitogenesis. PLoS One 4(10):e7429. doi:10.1371/journal.pone.0007429
Serralbo O, Marcelle C (2014) Migrating cells mediate long-range WNT signaling. Development 141(10):2057–2063. doi:10.1242/dev.107656
Bajanca F, Luz M, Raymond K, Martins GG, Sonnenberg A, Tajbakhsh S, Buckingham M, Thorsteinsdóttir S (2006) Integrin α6β1-laminin interactions regulate early myotome formation in the mouse embryo. Development 133(9):1635–1644. doi:10.1242/dev.02336
Tosney KW, Dehnbostel DB, Erickson CA (1994) Neural crest cells prefer the myotome’s basal lamina over the sclerotome as a substratum. Dev Biol 163(2):389–406. doi:10.1006/dbio.1994.1157
Koblar SA, Krull CE, Pasquale EB, McLennan R, Peale FD, Cerretti DP, Bothwell M (2000) Spinal motor axons and neural crest cells use different molecular guides for segmental migration through the rostral half-somite. J Neurobiol 42(4):437–447
Halperin-Barlev O, Kalcheim C (2011) Sclerotome-derived Slit1 drives directional migration and differentiation of Robo2-expressing pioneer myoblasts. Development 138(14):2935–2945. doi:10.1242/dev.065714
Wong K, Park HT, Wu JY, Rao Y (2002) Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr Opin Genet Dev 12(5):583–591
Kablar B, Krastel K, Tajbakhsh S, Rudnicki MA (2003) Myf5 and MyoD activation define independent myogenic compartments during embryonic development. Dev Biol 258(2):307–318
Ikeya M, Takada S (1998) Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125(24):4969–4976
Amthor H, Christ B, Patel K (1999) A molecular mechanism enabling continuous embryonic muscle growth—a balance between proliferation and differentiation. Development 126(5):1041–1053
Dietrich S, Schubert FR, Healy C, Sharpe PT, Lumsden A (1998) Specification of the hypaxial musculature. Development 125(12):2235–2249
Amthor H, Connolly D, Patel K, Brand-Saberi B, Wilkinson DG, Cooke J, Christ B (1996) The expression and regulation of follistatin and a follistatin-like gene during avian somite compartmentalization and myogenesis. Dev Biol 178(2):343–362
Cinnamon Y, Kahane N, Bachelet I, Kalcheim C (2001) The sub-lip domain—a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development 128(3):341–351
Van Ho AT, Hayashi S, Brohl D, Aurade F, Rattenbach R, Relaix F (2011) Neural crest cell lineage restricts skeletal muscle progenitor cell differentiation through Neuregulin1-ErbB3 signaling. Dev Cell 21(2):273–287. doi:10.1016/j.devcel.2011.06.019
Delfini MC, De La Celle M, Gros J, Serralbo O, Marics I, Seux M, Scaal M, Marcelle C (2009) The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway. Dev Biol 333(2):229–237. doi:10.1016/j.ydbio.2009.05.544
Vinagre T, Moncaut N, Carapuco M, Novoa A, Bom J, Mallo M (2010) Evidence for a myotomal Hox/Myf cascade governing nonautonomous control of rib specification within global vertebral domains. Dev Cell 18(4):655–661. doi:10.1016/j.devcel.2010.02.011
Brent AE, Braun T, Tabin CJ (2005) Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development. Development 132(3):515–528
Babiuk RP, Zhang W, Clugston R, Allan DW, Greer JJ (2003) Embryological origins and development of the rat diaphragm. J Comp Neurol 455(4):477–487. doi:10.1002/cne.10503
Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138(12):2401–2415. doi:10.1242/dev.040972
Murphy M, Kardon G (2011) Origin of vertebrate limb muscle the role of progenitor and myoblast populations. Curr Top Dev Biol 96:1–32. doi:10.1016/B978-0-12-385940-2.00001-2
Duprez D (2002) Signals regulating muscle formation in the limb during embryonic development. Int J Dev Biol 46(7):915–925
Francis-West PH, Antoni L, Anakwe K (2003) Regulation of myogenic differentiation in the developing limb bud. J Anat 202(1):69–81
Lee AS, Harris J, Bate M, Vijayraghavan K, Fisher L, Tajbakhsh S, Duxson M (2013) Initiation of primary myogenesis in amniote limb muscles. Dev Dyn 242(9):1043–1055. doi:10.1002/dvdy.23998
Vasyutina E, Birchmeier C (2006) The development of migrating muscle precursor cells. Anat Embryol (Berl) 211(Suppl 1):37–41. doi:10.1007/s00429-006-0118-9
Brand-Saberi B, Muller TS, Wilting J, Christ B, Birchmeier C (1996) Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo. Dev Biol 179(1):303–308. doi:10.1006/dbio.1996.0260
Dietrich S, Abou-Rebyeh F, Brohmann H, Bladt F, Sonnenberg-Riethmacher E, Yamaai T, Lumsden A, Brand-Saberi B, Birchmeier C (1999) The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126(8):1621–1629
Relaix F, Polimeni M, Rocancourt D, Ponzetto C, Schafer BW, Buckingham M (2003) The transcriptional activator PAX3-FKHR rescues the defects of Pax3 mutant mice but induces a myogenic gain-of-function phenotype with ligand-independent activation of Met signaling in vivo. Genes Dev 17(23):2950–2965. doi:10.1101/gad.281203
Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C (2005) CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev 19(18):2187–2198. doi:10.1101/gad.346205
Swartz ME, Eberhart J, Pasquale EB, Krull CE (2001) EphA4/ephrin–A5 interactions in muscle precursor cell migration in the avian forelimb. Development 128(23):4669–4680
Linker C, Lesbros C, Stark MR, Marcelle C (2003) Intrinsic signals regulate the initial steps of myogenesis in vertebrates. Development 130(20):4797–4807. doi:10.1242/dev.00688
Scaal M, Bonafede A, Dathe V, Sachs M, Cann G, Christ B, Brand-Saberi B (1999) SF/HGF is a mediator between limb patterning and muscle development. Development 126(21):4885–4893
Heymann S, Koudrova M, Arnold H, Koster M, Braun T (1996) Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. Dev Biol 180(2):566–578
Itoh N, Mima T, Mikawa T (1996) Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122(1):291–300
Anakwe K, Robson L, Hadley J, Buxton P, Church V, Allen S, Hartmann C, Harfe B, Nohno T, Brown AM, Evans DJ, Francis-West P (2003) Wnt signalling regulates myogenic differentiation in the developing avian wing. Development 130(15):3503–3514
Ladher RK, Church VL, Allen S, Robson L, Abdelfattah A, Brown NA, Hattersley G, Rosen V, Luyten FP, Dale L, Francis-West PH (2000) Cloning and expression of the Wnt antagonists Sfrp-2 and Frzb during chick development. Dev Biol 218(2):183–198. doi:10.1006/dbio.1999.9586
Hu JK, McGlinn E, Harfe BD, Kardon G, Tabin CJ (2012) Autonomous and nonautonomous roles of Hedgehog signaling in regulating limb muscle formation. Genes Dev 26(18):2088–2102. doi:10.1101/gad.187385.112
Anderson C, Williams VC, Moyon B, Daubas P, Tajbakhsh S, Buckingham ME, Shiroishi T, Hughes SM, Borycki AG (2012) Sonic hedgehog acts cell-autonomously on muscle precursor cells to generate limb muscle diversity. Genes Dev 26(18):2103–2117. doi:10.1101/gad.187807.112
Geetha-Loganathan P, Nimmagadda S, Prols F, Patel K, Scaal M, Huang R, Christ B (2005) Ectodermal Wnt-6 promotes Myf5-dependent avian limb myogenesis. Dev Biol 288(1):221–233. doi:10.1016/j.ydbio.2005.09.035
Hutcheson DA, Zhao J, Merrell A, Haldar M, Kardon G (2009) Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for β-catenin. Genes Dev 23(8):997–1013
Amthor H, Christ B, Weil M, Patel K (1998) The importance of timing differentiation during limb muscle development. Curr Biol 8(11):642–652
Robson LG, Hughes SM (1996) The distal limb environment regulates MyoD accumulation and muscle differentiation in mouse-chick chimaeric limbs. Development 122(12):3899–3910
Clase KL, Mitchell PJ, Ward PJ, Dorman CM, Johnson SE, Hannon K (2000) FGF5 stimulates expansion of connective tissue fibroblasts and inhibits skeletal muscle development in the limb. Dev Dyn 219(3):368–380. doi:10.1002/1097-0177(2000)9999:9999<:AID-DVDY1056>3.0.CO;2-8
Marics I, Padilla F, Guillemot JF, Scaal M, Marcelle C (2002) FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129(19):4559–4569
Mok GF, Cardenas R, Anderton H, Campbell KH, Sweetman D (2014) Interactions between FGF18 and retinoic acid regulate differentiation of chick embryo limb myoblasts. Dev Biol 396(2):214–223. doi:10.1016/j.ydbio.2014.10.004
Ashby PR, Wilson SJ, Harris AJ (1993) Formation of primary and secondary myotubes in aneural muscles in the mouse mutant peroneal muscular-atrophy. Dev Biol 156(2):519–528
Ross JJ, Duxson MJ, Harris AJ (1987) Neural determination of muscle fibre numbers in embryonic rat lumbrical muscles. Development 100(3):395–409
Delfini MC, Hirsinger E, Pourquié O, Duprez D (2000) Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 127(23):5213–5224
Vasyutina E, Lenhard DC, Birchmeier C (2007) Notch function in myogenesis. Cell Cycle 6(12):1451–1454
Mourikis P, Gopalakrishnan S, Sambasivan R, Tajbakhsh S (2012) Cell-autonomous Notch activity maintains the temporal specification potential of skeletal muscle stem cells. Development 139(24):4536–4548. doi:10.1242/dev.084756
Cusella-De Angelis MG, Molinari S, Le Donne A, Coletta M, Vivarelli E, Bouche M, Molinaro M, Ferrari S, Cossu G (1994) Differential response of embryonic and fetal myoblasts to TGF β: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120(4):925–933
Messina G, Biressi S, Monteverde S, Magli A, Cassano M, Perani L, Roncaglia E, Tagliafico E, Starnes L, Campbell CE, Grossi M, Goldhamer DJ, Gronostajski RM, Cossu G (2010) Nfix regulates fetal-specific transcription in developing skeletal muscle. Cell 140(4):554–566. doi:10.1016/j.cell.2010.01.027
Harris AJ, Duxson MJ, Fitzsimons RB, Rieger F (1989) Myonuclear birthdates distinguish the origins of primary and secondary myotubes in embryonic mammalian skeletal muscles. Development 107(4):771–784
Auda-Boucher G, Jarno V, Fournier-Thibault C, Butler-Browne G, Fontaine-Pérus J (1997) Acetylcholine receptor formation in mouse-chick chimera. Exp Cell Res 236(1):29–42
Hughes DS, Ontell M (1992) Morphometric analysis of the developing, murine aneural soleus muscle. Dev Dyn 193(2):175–184
Wilson SJ, Harris AJ (1993) Formation of myotubes in aneural rat muscles. Dev Biol 156(2):509–518. doi:10.1006/dbio.1993.1097
Duxson MJ, Usson Y, Harris AJ (1989) The origin of secondary myotubes in mammalian skeletal muscles: ultrastructural studies. Development 107:743–750
Ko CP, Robitaille R (2015) Perisynaptic Schwann cells at the neuromuscular synapse: adaptable, multitasking glial cells. Cold Spring Harb Perspect Biol 7(10):a020503. doi:10.1101/cshperspect.a020503
Darabid H, Perez-Gonzalez AP, Robitaille R (2014) Neuromuscular synaptogenesis: coordinating partners with multiple functions. Nat Rev Neurosci 15(11):703–718
Burden SJ (2002) Building the vertebrate neuromuscular synapse. J Neurobiol 53(4):501–511
Washabaugh CH, Ontell MP, Shand SH, Bradbury N, Kant JA, Ontell M (2007) Neuronal control of myogenic regulatory factor accumulation in fetal muscle. Dev Dyn 236(3):732–745. doi:10.1002/dvdy.21078
Weatherbee SD, Anderson KV, Niswander LA (2006) LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133(24):4993–5000. doi:10.1242/dev.02696
Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, Hubbard SR, Dustin ML, Burden SJ (2008) Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135(2):334–342. doi:10.1016/j.cell.2008.10.002
Kardon G (1998) Muscle and tendon morphogenesis in the avian hind limb. Development 125(20):4019–4032
Mathew SJ, Hansen JM, Merrell AJ, Murphy MM, Lawson JA, Hutcheson DA, Hansen MS, Angus-Hill M, Kardon G (2011) Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 138(2):371–384. doi:10.1242/dev.057463
Hasson P, DeLaurier A, Bennett M, Grigorieva E, Naiche LA, Papaioannou VE, Mohun TJ, Logan MP (2010) Tbx4 and Tbx5 acting in connective tissue are required for limb muscle and tendon patterning. Dev Cell 18(1):148–156. doi:10.1016/j.devcel.2009.11.013
Hasson P (2011) “Soft” tissue patterning: muscles and tendons of the limb take their form. Dev Dyn 240(5):1100–1107. doi:10.1002/dvdy.22608
Wang H, Noulet F, Edom-Vovard F, Tozer S, Le Grand F, Duprez D (2010) Bmp signaling at the tips of skeletal muscles regulates the number of fetal muscle progenitors and satellite cells during development. Dev Cell 18(4):643–654. doi:10.1016/j.devcel.2010.02.008
Lejard V, Blais F, Guerquin MJ, Bonnet A, Bonnin MA, Havis E, Malbouyres M, Bidaud CB, Maro G, Gilardi-Hebenstreit P, Rossert J, Ruggiero F, Duprez D (2011) EGR1 and EGR2 involvement in vertebrate tendon differentiation. J Biol Chem 286(7):5855–5867. doi:10.1074/jbc.M110.153106
Edom-Vovard F, Schuler B, Bonnin MA, Teillet MA, Duprez D (2002) Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev Biol 247(2):351–366
Kutchuk L, Laitala A, Soueid-Bomgarten S, Shentzer P, Rosendahl AH, Eilot S, Grossman M, Sagi I, Sormunen R, Myllyharju J, Maki JM, Hasson P (2015) Muscle composition is regulated by a Lox-TGFβ feedback loop. Development 142(5):983–993. doi:10.1242/dev.113449
Tozer S, Bonnin MA, Relaix F, Di Savino S, Garcia-Villalba P, Coumailleau P, Duprez D (2007) Involvement of vessels and PDGFB in muscle splitting during chick limb development. Development 134(14):2579–2591. doi:10.1242/dev.02867
Mourikis P, Tajbakhsh S (2014) Distinct contextual roles for Notch signalling in skeletal muscle stem cells. BMC Dev Biol 14:2. doi:10.1186/1471-213X-14-2
Prols F, Sagar, Scaal M (2016) Signaling filopodia in vertebrate embryonic development. Cell Mol Life Sci 73(5):961–974. doi:10.1007/s00018-015-2097-6
Muller P, Rogers KW, Yu SR, Brand M, Schier AF (2013) Morphogen transport. Development 140(8):1621–1638. doi:10.1242/dev.083519
Sagar, Prols F, Wiegreffe C, Scaal M (2015) Communication between distant epithelial cells by filopodia-like protrusions during embryonic development. Development 142(4):665–671. doi:10.1242/dev.115964
Sanders TA, Llagostera E, Barna M (2013) Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning. Nature 497(7451):628–632. doi:10.1038/nature12157
Ayers KL, Mteirek R, Cervantes A, Lavenant-Staccini L, Therond PP, Gallet A (2012) Dally and Notum regulate the switch between low and high level Hedgehog pathway signalling. Development 139(17):3168–3179. doi:10.1242/dev.078402
Venters SJ, Thorsteinsdóttir S, Duxson MJ (1999) Early development of the myotome in the mouse. Dev Dyn 216(3):219–232
Brent AE, Tabin CJ (2004) FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development 131(16):3885–3896. doi:10.1242/dev.01275
Tosney KW (1987) Proximal tissues and patterned neurite outgrowth at the lumbosacral level of the chick embryo: deletion of the dermamyotome. Dev Biol 122(2):540–558
Kablar B, Rudnicki MA (1999) Development in the absence of skeletal muscle results in the sequential ablation of motor neurons from the spinal cord to the brain. Dev Biol 208(1):93–109
Chal J, Oginuma M, Al Tanoury Z, Gobert B, Sumara O, Hick A, Bousson F, Zidouni Y, Mursch C, Moncuquet P, Tassy O, Vincent S, Miyanari A, Bera A, Garnier JM, Guevara G, Hestin M, Kennedy L, Hayashi S, Drayton B, Cherrier T, Gayraud-Morel B, Gussoni E, Relaix F, Tajbakhsh S, Pourquie O (2015) Differentiation of pluripotent stem cells to muscle fiber to model Duchenne muscular dystrophy. Nat Biotechnol 33(9):962–969. doi:10.1038/nbt.3297
Rooney JE, Knapp JR, Hodges BL, Wuebbles RD, Burkin DJ (2012) Laminin-111 protein therapy reduces muscle pathology and improves viability of a mouse model of merosin-deficient congenital muscular dystrophy. Am J Pathol 180(4):1593–1602. doi:10.1016/j.ajpath.2011.12.019
von Maltzahn J, Renaud JM, Parise G, Rudnicki MA (2012) Wnt7a treatment ameliorates muscular dystrophy. Proc Natl Acad Sci USA 109(50):20614–20619. doi:10.1073/pnas.1215765109
Kawashima K, Fujii T (2008) Basic and clinical aspects of non-neuronal acetylcholine: overview of non-neuronal cholinergic systems and their biological significance. J Pharmacol Sci 106(2):167–173
Wu H, Xiong WC, Mei L (2010) To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137(7):1017–1033. doi:10.1242/dev.038711
Xiao YT, Xiang LX, Shao JZ (2007) Bone morphogenetic protein. Biochem Biophys Res Commun 362(3):550–553. doi:10.1016/j.bbrc.2007.08.045
Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A (2011) Bone morphogenetic proteins: a critical review. Cell Signal 23(4):609–620. doi:10.1016/j.cellsig.2010.10.003
Li X, Wang C, Xiao J, McKeehan WL, Wang F (2016) Fibroblast growth factors, old kids on the new block. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2015.12.014
Eswarakumar VP, Lax I, Schlessinger J (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16(2):139–149. doi:10.1016/j.cytogfr.2005.01.001
Maki JM (2009) Lysyl oxidases in mammalian development and certain pathological conditions. Histol Histopathol 24(5):651–660
Csiszar K (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70:1–32
Newbern J, Birchmeier C (2010) Nrg1/ErbB signaling networks in Schwann cell development and myelination. Semin Cell Dev Biol 21(9):922–928. doi:10.1016/j.semcdb.2010.08.008
Britsch S (2007) The neuregulin-I/ErbB signaling system in development and disease. Adv Anat Embryol Cell Biol 190:1–65
Demoulin JB, Essaghir A (2014) PDGF receptor signaling networks in normal and cancer cells. Cytokine Growth Factor Rev 25(3):273–283. doi:10.1016/j.cytogfr.2014.03.003
Birchmeier C, Gherardi E (1998) Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol 8(10):404–410
Zhang YW, Vande Woude GF (2003) HGF/SF-met signaling in the control of branching morphogenesis and invasion. J Cell Biochem 88(2):408–417. doi:10.1002/jcb.10358
Yang J, Andre P, Ye L, Yang YZ (2015) The Hedgehog signalling pathway in bone formation. Int J Oral Sci 7(2):73–79. doi:10.1038/ijos.2015.14
Teperino R, Aberger F, Esterbauer H, Riobo N, Pospisilik JA (2014) Canonical and non-canonical Hedgehog signalling and the control of metabolism. Semin Cell Dev Biol 33:81–92. doi:10.1016/j.semcdb.2014.05.007
Maksym RB, Tarnowski M, Grymula K, Tarnowska J, Wysoczynski M, Liu R, Czerny B, Ratajczak J, Kucia M, Ratajczak MZ (2009) The role of stromal-derived factor-1–CXCR7 axis in development and cancer. Eur J Pharmacol 625(1–3):31–40. doi:10.1016/j.ejphar.2009.04.071
Komiya Y, Habas R (2008) Wnt signal transduction pathways. Organogenesis 4(2):68–75
Stanganello E, Scholpp S (2016) Role of cytonemes in Wnt transport. J Cell Sci. doi:10.1242/jcs.182469
Acknowledgments
We thank Christine L. Mummery for her critical comments, our team for useful discussion and André B. Gonçalves for the image in Fig. 2a. We also thank John Harris for giving the anti-MyoD antibody. Pax3 antibody was developed by C.P. Ordahl and was obtained from the Developmental Studies Hybridoma Bank, developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biology, Iowa City, IA52242, USA. M.D. is supported by Fundação para a Ciência e a Tecnologia (FCT) post-doc grant SFRH/BPD/65370/2009 (Portugal). This manuscript is an output of FCT project PTDC/SAU-BID/120130/2010 (Portugal).
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Deries, M., Thorsteinsdóttir, S. Axial and limb muscle development: dialogue with the neighbourhood. Cell. Mol. Life Sci. 73, 4415–4431 (2016). https://doi.org/10.1007/s00018-016-2298-7
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DOI: https://doi.org/10.1007/s00018-016-2298-7