Abstract
Hypaxial muscle is the anatomical term commonly used when referring to all the ventrally located musculature in the body of vertebrates, including muscles of the body wall and the limbs. Yet these muscles had very humble beginnings when vertebrates evolved from their chordate ancestors, and complex anatomical changes and changes in underlying gene regulatory networks occurred. This review summarises the current knowledge and controversies regarding the development and evolution of hypaxial muscles.
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Notes
- 1.
The phrase “bony” vertebrate as a more colloquial term for osteichthyans is somewhat misleading since mineralised bone was already present in stem group gnathostomes and was secondarily lost in sharks and rays, (Zhu et al. 2013).
References
Ahmed MU, Cheng L, Dietrich S (2006) Establishment of the epaxial-hypaxial boundary in the avian myotome. Dev Dyn 235(7):1884–1894
Alvares LE, Schubert FR, Thorpe C, Mootoosamy RC, Cheng L, Parkyn G, Lumsden A, Dietrich S (2003) Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev Cell 5(3):379–390
Beattie CE, Eisen JS (1997) Notochord alters the permissiveness of myotome for pathfinding by an identified motoneuron in embryonic zebrafish. Development 124(3):713–720
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
Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376(6543):768–771. doi:10.1038/376768a0
Bober E, Franz T, Arnold H-H, Gruss P, Tremblay P (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120:603–612
Borycki A-G, Li J, Jin F, Emerson CP (1999) Pax3 functions in cell survival and in Pax7 regulation. Development 126:1665–1674
Brohmann H, Jagla K, Birchmeier C (2000) The role of Lbx1 in migration of muscle precursor cells. Development 127(2):437–445
Brunet I, Di Nardo AA, Sonnier L, Beurdeley M, Prochiantz A (2007) The topological role of homeoproteins in the developing central nervous system. Trends Neurosci 30(6):260–267
Bryson-Richardson RJ, Currie PD (2008) The genetics of vertebrate myogenesis. Nat Rev Genet 9(8):632–646
Buckingham M (2006) Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev 16(5):525–532
Chen F, Liu KC, Epstein JA (1999) Lbx2, a novel murine homeobox gene related to the Drosophila ladybird genes is expressed in the developing urogenital system, eye and brain. Mech Dev 84(1–2):181–184
Cheng L, Alvares LE, Ahmed MU, El-Hanfy AS, Dietrich S (2004) The epaxial-hypaxial subdivision of the avian somite. Dev Biol 274(2):348–369
Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41:245–258
Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186
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 166:87–101
Clack JA (2002) Gaining ground. The origin and evolution of tetrapods. Indiana University Press, Bloomington, IN
Cohn MJ, Izpisua-Belmonte JC, Abud H, Heath JK, Tickle C (1995) Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80(5):739–746
Cole NJ, Hall TE, Don EK, Berger S, Boisvert CA, Neyt C, Ericsson R, Joss J, Gurevich DB, Currie PD (2011) Development and evolution of the muscles of the pelvic fin. PLoS Biol 9(10):1001168. doi:10.1371/journal.pbio.1001168
Currie PD, Ingham PW (1996) Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382(6590):452–455
Devoto SH, Melancon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122(11):3371–3380
Dietrich S (1999) Regulation of hypaxial muscle development. Cell Tissue Res 296(1):175–182
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
Dietrich S, Schubert FR, Healy C, Sharpe PT, Lumsden A (1998) Specification of the hypaxial musculature. Development 125(12):2235–2249
Durland JL, Sferlazzo M, Logan M, Burke AC (2008) Visualizing the lateral somitic frontier in the Prx1Cre transgenic mouse. J Anat 212(5):590–602. doi:10.1111/j.1469-7580.2008.00879.x
Fan CM, Lee CS, Tessier-Lavigne M (1997) A role for WNT proteins in induction of dermomyotome. Dev Biol 191(1):160–165
Fernandez-Jaen A, Suela J, Fernandez-Mayoralas DM, Fernandez-Perrone AL, Wotton KR, Dietrich S, Castellanos MD, Cigudosa JC, Calleja-Perez B, Lopez-Martin S (2014) Microduplication 10q24.31 in a Spanish girl with scoliosis and myopathy: the critical role of LBX. Am J Med Genet A 168:2074–8
Fetcho JR (1987) A review of the organization and evolution of motoneurons innervating the axial musculature of vertebrates. Brain Res 434(3):243–280
Franz T, Kothary R, Surani MAH, Halata Z, Grim M (1993) The Splotch mutation interferes with muscle development in the limbs. Anat Embryol 187:153–160
Freitas R, Gomez-Skarmeta JL, Rodrigues PN (2014) New frontiers in the evolution of fin development. J Exp Zool (Mol Dev Evol) 9999B:1–13
Freitas R, Zhang G, Cohn MJ (2006) Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442(7106):1033–1037
Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220:268–274
Goodrich ES (1958) Studies on the structure and development of vertebrates, 2nd edn. Dover, New York
Gray H (1995) Gray’s anatomy, 38th edn. Churchill Livingstone, Edinburgh, London
Grifone R, Demignon J, Giordani J, Niro C, Souil E, Bertin F, Laclef C, Xu PX, Maire P (2007) Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Dev Biol 302(2):602–616
Grifone R, Demignon J, Houbron C, Souil E, Niro C, Seller MJ, Hamard G, Maire P (2005) Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 132(9):2235–2249
Gross MK, Moran-Rivard L, Velasquez T, Nakatsu MN, Jagla K, Goulding M (2000) Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127(2):413–424
Hammond KL, Baxendale S, McCauley DW, Ingham PW, Whitfield TT (2009) Expression of patched, prdm1 and engrailed in the lamprey somite reveals conserved responses to Hedgehog signaling. Evol Dev 11(1):27–40
Hayashi K, Ozawa E (1995) Myogenic cell migration from somites is induced by tissue contact with medial region of the presumptive limb mesoderm in chick embryos. Development 121:661–669
Jagla K, Dollé P, Mattei M-G, Jagla T, Schuhbaur B, Dretzen G, Bellard F, Bellard M (1995) Mouse Lbx1 and human LBX1 define a novel mammalian homeobox gene family related to the Drosophila ladybird genes. Mech Dev 53:345–356
Jagla T, Bellard F, Lutz Y, Dretzen G, Bellard M, Jagla K (1998) ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. Development 125(18):3699–3708
Kanamoto T, Terada K, Yoshikawa H, Furukawa T (2006) Cloning and expression pattern of lbx3, a novel chick homeobox gene. Gene Expr Patterns 6(3):241–246
Kardon G, Harfe BD, Tabin CJ (2003) A Tcf4-positive mesodermal population provides a prepattern for vertebrate limb muscle patterning. Dev Cell 5(6):937–944
Kiehn O (2011) Development and functional organization of spinal locomotor circuits. Curr Opin Neurobiol 21(1):100–109. doi:10.1016/j.conb.2010.09.004
Kusakabe R, Kuraku S, Kuratani S (2011) Expression and interaction of muscle-related genes in the lamprey imply the evolutionary scenario for vertebrate skeletal muscle, in association with the acquisition of the neck and fins. Dev Biol 350(1):217–227. doi:10.1016/j.ydbio.2010.10.029
Layalle S, Volovitch M, Mugat B, Bonneaud N, Parmentier ML, Prochiantz A, Joliot A, Maschat F (2011) Engrailed homeoprotein acts as a signaling molecule in the developing fly. Development 138(11):2315–2323. doi:10.1242/dev.057059
Lewis KE, Eisen JS (2003) From cells to circuits: development of the zebrafish spinal cord. Prog Neurobiol 69(6):419–449
Lours-Calet C, Alvares LE, El-Hanfy AS, Gandesha S, Walters EH, Sobreira DR, Wotton KR, Jorge EC, Lawson JA, Kelsey Lewis A, Tada M, Sharpe C, Kardon G, Dietrich S (2014) Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures. Dev Biol 390(2):231–246. doi:10.1016/j.ydbio.2014.03.003
Mackenzie S, Walsh FS, Graham A (1998) Migration of hypoglossal myoblast precursors. Dev Dyn 213(4):349–358
Martin BL, Harland RM (2001) Hypaxial muscle migration during primary myogenesis in Xenopus laevis. Dev Biol 239(2):270–280. doi:10.1006/dbio.2001.0434
Martin BL, Harland RM (2006) A novel role for lbx1 in Xenopus hypaxial myogenesis. Development 133(2):195–208
Matsuura M, Nishihara H, Onimaru K, Kokubo N, Kuraku S, Kusakabe R, Okada N, Kuratani S, Tanaka M (2008) Identification of four Engrailed genes in the Japanese lamprey, Lethenteron japonicum. Dev Dyn 237(6):1581–1589
Maurya AK, Tan H, Souren M, Wang X, Wittbrodt J, Ingham PW (2011) Integration of Hedgehog and BMP signalling by the engrailed2a gene in the zebrafish myotome. Development 138(4):755–765. doi:10.1242/dev.062521
Mennerich D, Braun T (2001) Activation of myogenesis by the homeobox gene Lbx1 requires cell proliferation. EMBO J 20(24):7174–7183
Mennerich D, Schafer K, Braun T (1998) Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech Dev 73(2):147–158
Minchin JE, Williams VC, Hinits Y, Low S, Tandon P, Fan CM, Rawls JF, Hughes SM (2013) Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion. Development 140(14):2972–2984. doi:10.1242/dev.090050
Montell DJ (2008) Morphogenetic cell movements: diversity from modular mechanical properties. Science 322(5907):1502–1505
Murakami Y, Tanaka M (2011) Evolution of motor innervation to vertebrate fins and limbs. Dev Biol 355(1):164–172. doi:10.1016/j.ydbio.2011.04.009
Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G (2011) Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138(17):3625–3637. doi:10.1242/dev.064162
Neyt C, Jagla K, Thisse C, Thisse B, Haines L, Currie PD (2000) Evolutionary origins of vertebrate appendicular muscle. Nature 408(6808):82–86
Nowicki JL, Burke AC (2000) Hox genes and morphological identity: axial versus lateral patterning in the vertebrate mesoderm. Development 127(19):4265–4275
Ochi H, Westerfield M (2009) Lbx2 regulates formation of myofibrils. BMC Dev Biol 9:13. doi:10.1186/1471-213X-9-13
Odemis V, Lamp E, Pezeshki G, Moepps B, Schilling K, Gierschik P, Littman DR, Engele J (2005) Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci 30(4):494–505
Onimaru K, Shoguchi E, Kuratani S, Tanaka M (2011) Development and evolution of the lateral plate mesoderm: comparative analysis of amphioxus and lamprey with implications for the acquisition of paired fins. Dev Biol 359(1):124–136. doi:10.1016/j.ydbio.2011.08.003
Pourquié O, Fan CM, Coltey M, Hirsinger E, Watanabe Y, Bréant 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
Prunotto C, Crepaldi T, Forni PE, Ieraci A, Kelly RG, Tajbakhsh S, Buckingham M, Ponzetto C (2004) Analysis of Mlc-lacZ Met mutants highlights the essential function of Met for migratory precursors of hypaxial muscles and reveals a role for Met in the development of hyoid arch-derived facial muscles. Dev Dyn 231(3):582–591
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
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
Schäfer K, Braun T (1999) Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat Genet 23(2):213–216
Shearman RM, Burke AC (2009) The lateral somitic frontier in ontogeny and phylogeny. J Exp Zool B Mol Dev Evol 312(6):603–612. doi:10.1002/jez.b.21246
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
Thisse B, Heyer V, Lux A, Alunni V, Degrave A, Seiliez I, Kirchner J, Parkhill JP, Thisse C (2004) Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol 77:505–519
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
Tosney KW, Landmesser LT (1985) Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. J Neurosci 5(9):2345–2358
Trainor P, Krumlauf R (2000) Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat Cell Biol 2(2):96–102
Tremblay P, Dietrich S, Meriskay M, Schubert FR, Li Z, Paulin D (1998) A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Dev Biol 203:49–61
Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL (1994) Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79(6):957–970
Tulenko FJ, McCauley DW, Mackenzie EL, Mazan S, Kuratani S, Sugahara F, Kusakabe R, Burke AC (2013) Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins. Proc Natl Acad Sci U S A 110(29):11899–11904. doi:10.1073/pnas.1304210110
Turney BW, Rowan-Hull AM, Brown JM (2003) The innervation of FGF-induced additional limbs in the chick embryo. J Anat 202(1):83–92
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
Watanabe S, Kondo S, Hayasaka M, Hanaoka K (2007) Functional analysis of homeodomain-containing transcription factor Lbx1 in satellite cells of mouse skeletal muscle. J Cell Sci 120(Pt 23):4178–4187. doi:10.1242/jcs.011668
Windner SE, Steinbacher P, Obermayer A, Kasiba B, Zweimueller-Mayer J, Stoiber W (2011) Distinct modes of vertebrate hypaxial muscle formation contribute to the teleost body wall musculature. Dev Genes Evol 221(3):167–178. doi:10.1007/s00427-011-0369-1
Wotton KR, Weierud FK, Dietrich S, Lewis KE (2008) Comparative genomics of Lbx loci reveals conservation of identical Lbx ohnologs in bony vertebrates. BMC Evol Biol 8:171–186
Yang X-M, Vogan K, Gros P, Park M (1996) Expression of the met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice. Development 122(7):2163–2171
Zhu M, Yu X, Ahlberg PE, Choo B, Lu J, Qiao T, Qu Q, Zhao W, Jia L, Blom H, Zhu Y (2013) A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502(7470):188–193. doi:10.1038/nature12617
Acknowledgements
We are grateful to Mohi U. Ahmed, Ashish K. Maurya, Louise Cheng, Erika C. Jorge, Pascal Maire, M. Albert Basson and Philip W. Ingham for agreeing to include currently unpublished data in this review article. The work was supported by the Human Frontier Science Program, Grant No R6Y0056/2004-C201, the European Network of Excellence Myores, Grant No EU LSHG-CT-2004-511978 MYORES, the Association Française contre les Myopathies, Grant No CL/NM/2005.2088/Following number 11378, Groupe A07/06/05 and CA 01/07/05, DRM05/BUIOCE/REFAP/MUSAI/ANGLE.
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Wotton, K.R., Schubert, F.R., Dietrich, S. (2015). Hypaxial Muscle: Controversial Classification and Controversial Data?. In: Brand-Saberi, B. (eds) Vertebrate Myogenesis. Results and Problems in Cell Differentiation, vol 56. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-44608-9_2
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