Vertebrate Myogenesis pp 99-122 | Cite as
The Avian Embryo as a Model System for Skeletal Myogenesis
Abstract
This review will focus on the use of the chicken and quail as model systems to analyze myogenesis and as such will emphasize the experimental approaches that are strongest in these systems—the amenability of the avian embryo to manipulation and in ovo observation. During somite differentiation, a wide spectrum of developmental processes occur such as cellular differentiation, migration, and fusion. Cell lineage studies combined with recent advancements in cell imaging allow these biological phenomena to be readily observed and hypotheses tested extremely rapidly—a strength that is restricted to the avian system. A clear weakness of the chicken in the past has been genetic approaches to modulate gene function. Recent advances in the electroporation of expression vectors, siRNA constructs, and use of tissue specific reporters have opened the door to increasingly sophisticated experiments that address questions of interest not only to the somite/muscle field in particular but also fundamental to biology in general. Importantly, an ever-growing body of evidence indicates that somite differentiation in birds is indistinguishable to that of mammals; therefore, these avian studies complement the complex genetic models of the mouse.
Keywords
Satellite Cell Myogenic Differentiation Asymmetric Cell Division Dorsal Neural Tube Planar Cell Polarity PathwayNotes
Acknowledgments
We would like to thank Dr Olivier Serralbo and Daniel Sieiro Mosti for their critical reading of the manuscript and Phoebe Kipen for her help with the artwork. The National Health and Medical Research Council (NHMRC) and the Australian Research Council (ARC) support the work in our laboratory. Christophe Marcelle is a Senior Research Fellow of the National Health and Medical Research Council (NHMRC).
References
- Axelrod JD (2010) Delivering the lateral inhibition punchline: it’s all about the timing. Sci Signal 3:pe38–pe38. doi: 10.1126/scisignal.3145pe38 PubMedGoogle Scholar
- Bénazéraf B, Pourquié O (2013) Formation and segmentation of the vertebrate body axis. Annu Rev Cell Dev Biol 29:1–26. doi: 10.1146/annurev-cellbio-101011-155703 PubMedGoogle Scholar
- Bentzinger CF, Wang YX, Rudnicki MA (2012) Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol 4:a008342–a008342. doi: 10.1101/cshperspect.a008342 PubMedPubMedCentralGoogle Scholar
- 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 132:689–701PubMedGoogle Scholar
- 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 180:607–618. doi: 10.1083/jcb.200707206 PubMedPubMedCentralGoogle Scholar
- Ben-Yair R, Kahane N, Kalcheim C (2003) Coherent development of dermomyotome and dermis from the entire mediolateral extent of the dorsal somite. Development 130:4325–4336. doi: 10.1242/dev.00667 PubMedGoogle Scholar
- Ben-Yair R, Kahane N, Kalcheim C (2011) LGN-dependent orientation of cell divisions in the dermomyotome controls lineage segregation into muscle and dermis. Development 138:4155–4166. doi: 10.1242/dev.065169 PubMedGoogle Scholar
- Biressi S, Rando TA (2010) Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 21:845–854. doi: 10.1016/j.semcdb.2010.09.003 PubMedPubMedCentralGoogle Scholar
- Biressi S, Molinaro M, Cossu G (2007) Cellular heterogeneity during vertebrate skeletal muscle development. Dev Biol 308:281–293. doi: 10.1016/j.ydbio.2007.06.006 PubMedGoogle Scholar
- Borello U, Berarducci B, Murphy P et al (2006) The Wnt/beta-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 133:3723–3732. doi: 10.1242/dev.02517 PubMedGoogle Scholar
- Borycki AG, Brunk B, Tajbakhsh S et al (1999) Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 126:4053–4063PubMedGoogle Scholar
- Braun T, Gautel M (2011) Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev 12:349–361. doi: 10.1038/nrm3118 Google Scholar
- Brill G, Kahane N, Carmeli C et al (1995) Epithelial-mesenchymal conversion of dermatome progenitors requires neural tube-derived signals: characterization of the role of Neurotrophin-3. Development 121:2583–2594PubMedGoogle Scholar
- Bryson-Richardson RJ, Currie PD (2008) The genetics of vertebrate myogenesis. Nat Rev 9:632–646. doi: 10.1038/nrg2369 Google Scholar
- Buckingham M, Vincent SD (2009) Distinct and dynamic myogenic populations in the vertebrate embryo. Curr Opin Genet Dev 19:444–453PubMedGoogle Scholar
- Burgess R, Rawls A, Brown D et al (1996) Requirement of the paraxis gene for somite formation and musculoskeletal patterning. Nature 384:570–573. doi: 10.1038/384570a0 PubMedGoogle Scholar
- Butterfield NC, McGlinn E, Wicking C (2010) Chapter nine—The molecular regulation of vertebrate limb patterning. In: Koopman P (ed) Organogenesis in development. Academic, San Diego, CA, pp 319–341Google Scholar
- Cheung TH, Quach NL, Charville GW et al (2012) Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482:524–528. doi: 10.1038/nature10834 PubMedPubMedCentralGoogle Scholar
- Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol 191:381–396PubMedGoogle Scholar
- Chuai M, Dormann D, Weijer CJ (2009) Imaging cell signalling and movement in development. Semin Cell Dev Biol 20:947–955. doi: 10.1016/j.semcdb.2009.09.001 PubMedGoogle Scholar
- Cinnamon Y, Kahane N, Kalcheim C (1999) Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126:4305–4315PubMedGoogle Scholar
- 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 128:341–351PubMedGoogle Scholar
- Cinnamon Y, Ben-Yair R, Kalcheim C (2006) Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves. Development 133:1101–1112. doi: 10.1242/dev.02291 PubMedGoogle Scholar
- Couly GF, Coltey PM, Le Douarin NM (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15PubMedGoogle Scholar
- Dale JK, Maroto M, Dequeant ML et al (2003) Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421:275–278. doi: 10.1038/nature01244 PubMedGoogle Scholar
- Delfini M-C, La Celle DM, Gros J et al (2009) The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway. Dev Biol 333:229–237. doi: 10.1016/j.ydbio.2009.05.544 PubMedGoogle Scholar
- Denetclaw WF, Ordahl CP (2000) The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. Development 127:893–905PubMedGoogle Scholar
- Denetclaw WF, Christ B, Ordahl CP (1997) Location and growth of epaxial myotome precursor cells. Development 124:1601–1610PubMedGoogle Scholar
- Denetclaw WFJ, Berdougo E, Venters SJ, Ordahl CP (2001) Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome. Development 128:1745–1755PubMedGoogle Scholar
- Duprez D (2002) Signals regulating muscle formation in the limb during embryonic development. Int J Dev Biol 46:915–925PubMedGoogle Scholar
- Eichmann A, Marcelle C, Bréant C, Le Douarin NM (1993) Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech Dev 42:33–48PubMedGoogle Scholar
- Eichmann A, Corbel C, Nataf V et al (1997) Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proc Natl Acad Sci 94:5141–5146PubMedPubMedCentralGoogle Scholar
- Eloy-Trinquet S, Nicolas J-F (2002a) Cell coherence during production of the presomitic mesoderm and somitogenesis in the mouse embryo. Development 129:3609–3619PubMedGoogle Scholar
- Eloy-Trinquet S, Nicolas J-F (2002b) Clonal separation and regionalisation during formation of the medial and lateral myotomes in the mouse embryo. Development 129:111–122PubMedGoogle Scholar
- Ema M, Takahashi S, Rossant J (2006) Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood 107:111–117. doi: 10.1182/blood-2005-05-1970 PubMedGoogle Scholar
- Esner M, Meilhac SM, Relaix F et al (2006) Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome. Development 133:737–749. doi: 10.1242/dev.02226 PubMedGoogle Scholar
- Fraser SE, Harland RM (2000) The molecular metamorphosis of experimental embryology. Cell 100:41–55PubMedGoogle Scholar
- Fukada S-I, Uezumi A, Ikemoto M et al (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25:2448–2459. doi: 10.1634/stemcells.2007-0019 PubMedGoogle Scholar
- Gerhart J, Neely C, Elder J et al (2007) Cells that express MyoD mRNA in the epiblast are stably committed to the skeletal muscle lineage. J Cell Biol 178:649–660. doi: 10.1083/jcb.200703060 PubMedPubMedCentralGoogle Scholar
- Gros J, Scaal M, Marcelle C (2004) A two-step mechanism for myotome formation in chick. Dev Cell 6:875–882. doi: 10.1016/j.devcel.2004.05.006 PubMedGoogle Scholar
- Gros J, Manceau M, Thomé V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435:954–958. doi: 10.1038/nature03572 PubMedGoogle Scholar
- Gros J, Serralbo O, Marcelle C (2009) WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature 457:589–593. doi: 10.1038/nature07564 PubMedGoogle Scholar
- Harel I, Nathan E, Tirosh-Finkel L et al (2009) Distinct Origins and Genetic Programs of head muscle satellite cells. Dev Cell 16(6):822–832. doi: 10.1016/j.devcel.2009.05.007 PubMedPubMedCentralGoogle Scholar
- Ho ATV, Hayashi S, Bröhl D et al (2011) Neural crest cell lineage restricts skeletal muscle progenitor cell differentiation through Neuregulin1-ErbB3 signaling. Dev Cell 21:273–287. doi: 10.1016/j.devcel.2011.06.019 PubMedGoogle Scholar
- Holowacz T, Zeng L, Lassar AB (2006) Asymmetric localization of numb in the chick somite and the influence of myogenic signals. Dev Dyn 235:633–645. doi: 10.1002/dvdy.20672 PubMedPubMedCentralGoogle Scholar
- Houzelstein D, Cheraud Y, Auda-Boucher G et al (2000) The expression of the homeobox gene Msx1 reveals two populations of dermal progenitor cells originating from the somites. Development 127:2155–2164PubMedGoogle Scholar
- Hoyle NP, Ish-Horowicz D (2013) Transcript processing and export kinetics are rate-limiting steps in expressing vertebrate segmentation clock genes. Proc Natl Acad Sci 110:E4316–E4324. doi: 10.1073/pnas.1308811110 PubMedPubMedCentralGoogle Scholar
- Huber TL, Kouskoff V, Joerg Fehling H et al (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432:625–630. doi: 10.1038/nature03122 PubMedGoogle Scholar
- Itasaki N, Bel-Vialar S, Krumlauf R (1999) ‘Shocking’ developments in chick embryology: electroporation and in ovo gene expression. Nat Cell Biol 1:E203–E207. doi: 10.1038/70231 PubMedGoogle Scholar
- Jory A, Le Roux I, Gayraud-Morel B et al (2009) Numb promotes an increase in skeletal muscle progenitor cells in the embryonic somite. Stem Cells 27:2769–2780. doi: 10.1002/stem.220 PubMedGoogle Scholar
- Jouve C, Palmeirim I, Henrique D et al (2000) Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127:1421–1429PubMedGoogle Scholar
- Kahane N, Cinnamon Y, Kalcheim C (1998a) The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development 125:4259–4271PubMedGoogle Scholar
- Kahane N, Cinnamon Y, Kalcheim C (1998b) The origin and fate of pioneer myotomal cells in the avian embryo. Mech Dev 74:59–73. doi: 10.1016/S0925-4773(98)00066-5 PubMedGoogle Scholar
- Kahane N, Cinnamon Y, Bachelet I, Kalcheim C (2001) The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development 128:2187–2198PubMedGoogle Scholar
- Kahane N, Cinnamon Y, Kalcheim C (2002) The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development 129:2675–2687PubMedGoogle Scholar
- Kardon G, Campbell JK, Tabin CJ (2002) Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev Cell 3:533–545. doi: 10.1016/S1534-5807(02)00291-5 PubMedGoogle Scholar
- Kassar-Duchossoy L, Giacone E, Gayraud-Morel B et al (2005) Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Gene Dev 19:1426–1431. doi: 10.1101/gad.345505 PubMedPubMedCentralGoogle Scholar
- Knoblich JA (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev 11:849–860. doi: 10.1038/nrm3010 Google Scholar
- Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010. doi: 10.1016/j.cell.2007.03.044 PubMedPubMedCentralGoogle Scholar
- Kulesa PM, McKinney MC, McLennan R (2013) Developmental imaging: the avian embryo hatches to the challenge. Birth Defects Res C Embryo Today 99:121–133. doi: 10.1002/bdrc.21036 PubMedGoogle Scholar
- Lagha M, Kormish JD, Rocancourt D et al (2008) Pax3 regulation of FGF signaling affects the progression of embryonic progenitor cells into the myogenic program. Genes Dev 22:1828–1837. doi: 10.1101/gad.477908 PubMedPubMedCentralGoogle Scholar
- Le Douarin NM, Barq G (1969) Use of Japanese quail as “biological markers” in experimental embryology. C R Acad Sci Hebd Seances Acad Sci D 269:1543–1546PubMedGoogle Scholar
- Le Lièvre CS, Le Douarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34:125–154PubMedGoogle Scholar
- Lecuit T, Le Goff L (2007) Orchestrating size and shape during morphogenesis. Nature 450:189–192. doi: 10.1038/nature06304 PubMedGoogle Scholar
- Lewis J (2003) Autoinhibition with transcriptional delay: a simple mechanism for the Zebrafish somitogenesis oscillator. Curr Biol 13:1398–1408PubMedGoogle Scholar
- Li R (2013) The art of choreographing asymmetric cell division. Dev Cell 25:439–450. doi: 10.1016/j.devcel.2013.05.003 PubMedGoogle Scholar
- Li L, Cserjesi P, Olson EN (1995) Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Dev Biol 172:280–292. doi: 10.1006/dbio.1995.0023 PubMedGoogle Scholar
- Linker C, Lesbros C, Stark MR, Marcelle C (2003) Intrinsic signals regulate the initial steps of myogenesis in vertebrates. Development 130:4797–4807. doi: 10.1242/dev.00688 PubMedGoogle Scholar
- Linker C, Lesbros C, Gros J et al (2005) beta-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis. Development 132:3895–3905. doi: 10.1242/dev.01961 PubMedGoogle Scholar
- Luga V, Zhang L, Viloria-Petit AM et al (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151:1542–1556. doi: 10.1016/j.cell.2012.11.024 PubMedGoogle Scholar
- Majumdar A, Vainio S, Kispert A et al (2003) Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130:3175–3185. doi: 10.1242/dev.00520 PubMedGoogle Scholar
- Manceau M, Gros J, Savage K et al (2008) Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes Dev 22:668–681. doi: 10.1101/gad.454408 PubMedPubMedCentralGoogle Scholar
- Marcelle C, Eichmann A, Halevy O et al (1994) Distinct developmental expression of a new avian fibroblast growth factor receptor. Development 120:683–694PubMedGoogle Scholar
- Marcelle C, Wolf J, Bronner-Fraser M (1995) The in vivo expression of the FGF receptor FREK mRNA in avian myoblasts suggests a role in muscle growth and differentiation. Dev Biol 172:100–114. doi: 10.1006/dbio.1995.0008 PubMedGoogle Scholar
- Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955–3963PubMedGoogle Scholar
- Marcelle C, Lesbros C, Linker C (2002) Somite patterning: a few more pieces of the puzzle. Results Probl Cell Differ 38:81–108PubMedGoogle Scholar
- Marics I, Padilla F, Guillemot J-F et al (2002) FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129:4559–4569PubMedGoogle Scholar
- Mascré G, Dekoninck S, Drogat B et al (2012) Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489:257–262. doi: 10.1038/nature11393 PubMedGoogle Scholar
- McDermott A, Gustafsson M, Elsam T et al (2005) Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 132:345–357. doi: 10.1242/dev.01537 PubMedGoogle Scholar
- Montarras D, L’honoré A, Buckingham M (2013) Lying low but ready for action: the quiescent muscle satellite cell. FEBS J 280:4036–4050. doi: 10.1111/febs.12372 PubMedGoogle Scholar
- Morosan-Puopolo G, Balakrishnan-Renuka A, Yusuf F, Chen J, Dai F et al (2014) Wnt11 is required for oriented migration of dermogenic progenitor cells from the dorsomedial lip of the avian dermomyotome. PLoS One 9(3):e92679. doi: 10.1371/journal.pone.0092679 PubMedPubMedCentralGoogle Scholar
- Munsterberg AE, Kitajewski J, Bumcrot DA et al (1995) Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev 9:2911–2922PubMedGoogle Scholar
- Murphy M, Kardon G (2011) Chapter one—Origin of vertebrate limb muscle: the role of progenitor and myoblast populations. In: Pavlath GK (ed) Curr Top Dev Biol. 1–32Google Scholar
- Nakamura H, Funahashi J (2013) Electroporation: past, present and future. Dev Growth Differ 55:15–19. doi: 10.1111/dgd.12012 PubMedGoogle Scholar
- Nakamura H, Katahira T, Sato T et al (2004) Gain- and loss-of-function in chick embryos by electroporation. The Chick in Developmental Biology 121:1137–1143. doi: 10.1016/j.mod.2004.05.013 Google Scholar
- Noden DM (1990) Origins and assembly of avian embryonic blood vessels. Ann N Y Acad Sci 588:236–249. doi: 10.1111/j.1749-6632.1990.tb13214.x PubMedGoogle Scholar
- Ohata E, Tadokoro R, Sato Y et al (2009) Notch signal is sufficient to direct an endothelial conversion from non-endothelial somitic cells conveyed to the aortic region by CXCR4. Dev Biol 335:33–42. doi: 10.1016/j.ydbio.2009.08.010 PubMedGoogle Scholar
- Olivera-Martinez I, Coltey M, Dhouailly D, Pourquie O (2000) Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras. Development 127:4611–4617PubMedGoogle Scholar
- Olivera-Martinez I, Thélu J, Teillet M-A, Dhouailly D (2001) Dorsal dermis development depends on a signal from the dorsal neural tube, which can be substituted by Wnt-1. Mech Dev 100:233–244PubMedGoogle Scholar
- Olivera-Martinez I, Missier S, Fraboulet S et al (2002) Differential regulation of the chick dorsal thoracic dermal progenitors from the medial dermomyotome. Development 129:4763–4772PubMedGoogle Scholar
- Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114:339–353PubMedGoogle Scholar
- Ordahl CP, Berdougo E, Venters SJ, Denetclaw WFJ (2001) The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 128:1731–1744PubMedGoogle Scholar
- Özbudak EM, Pourquié O (2008) The vertebrate segmentation clock: the tip of the iceberg. Curr Opin Genet Dev 18:317–323. doi: 10.1016/j.gde.2008.06.007 PubMedGoogle Scholar
- Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648PubMedGoogle Scholar
- Paluch E, Heisenberg C-P (2009) Biology and physics of cell shape changes in development. Curr Biol 19:R790–R799. doi: 10.1016/j.cub.2009.07.029 PubMedGoogle Scholar
- Pardanaud L, Luton D, Prigent M et al (1996) Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development 122:1363–1371PubMedGoogle Scholar
- Picard CA, Marcelle C (2013) Two distinct muscle progenitor populations coexist throughout amniote development. Dev Biol 373:141–148PubMedGoogle Scholar
- Pouget C, Gautier R, Teillet M-A, Jaffredo T (2006) Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development 133:1013–1022. doi: 10.1242/dev.02269 PubMedGoogle Scholar
- Pourquié O (2011) Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 145:650–663. doi: 10.1016/j.cell.2011.05.011 PubMedPubMedCentralGoogle Scholar
- Pourquié O, Fan C-M, Coltey M et al (1996) Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84:461–471. doi: 10.1016/S0092-8674(00)81291-X PubMedGoogle Scholar
- Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–953PubMedGoogle Scholar
- Rios AC, Marcelle C (2009) Head muscles: aliens who came in from the cold? Dev Cell 16:779–780. doi: 10.1016/j.devcel.2009.06.004 PubMedGoogle Scholar
- Rios AC, Serralbo O, Salgado D, Marcelle C (2011) Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473:532–535. doi: 10.1038/nature09970 PubMedGoogle Scholar
- Rios AC, Marcelle C, Serralbo O (2012) Gene loss-of-function and live imaging in chick embryos. Methods Mol Biol 839:105–117. doi: 10.1007/978-1-61779-510-7_9 PubMedGoogle Scholar
- Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I et al (2012) A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148:112–125. doi: 10.1016/j.cell.2011.11.049 PubMedGoogle Scholar
- Rong PM, Teillet MA, Ziller C, Le Douarin NM (1992) The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 115:657–672PubMedGoogle Scholar
- Rossant J, Tam PPL (2002) Mouse development. In: Patterning, morphogenesis, and organogenesis. Academic, San Diego, pp xiii–xvGoogle Scholar
- Sambasivan R, Gayraud-Morel B, Dumas G et al (2009) Distinct regulatory cascades govern extraocular and branchiomeric muscle progenitor cell fates. Dev Cell 16:810–821PubMedGoogle Scholar
- Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138:2401–2415. doi: 10.1242/dev.040972 PubMedGoogle Scholar
- Sassoon D, Lyons G, Wright WE et al (1989) Expression of two myogenic regulatory factors myogenin and MyoDl during mouse embryogenesis. Nature 341:303–307. doi: 10.1038/341303a0 PubMedGoogle Scholar
- Sato Y, Watanabe T, Saito D et al (2008) Notch mediates the segmental specification of angioblasts in somites and their directed migration toward the dorsal aorta in avian embryos. Dev Cell 14:890–901PubMedGoogle Scholar
- Scaal M, Christ B (2004) Formation and differentiation of the avian dermomyotome. Anat Embryol 208:411–424. doi: 10.1007/s00429-004-0417-y PubMedGoogle Scholar
- Scaal M, Füchtbauer E-M, Brand-Saberi B (2001) cDermo-1 expression indicates a role in avian skin development. Anat Embryol 203(1):1–7. doi: 10.1007/PL00008244 PubMedGoogle Scholar
- Scaal M, Gros J, Lesbros C, Marcelle C (2004) In ovo electroporation of avian somites. Dev Dyn 229:643–650. doi: 10.1002/dvdy.10433 PubMedGoogle Scholar
- Schuster-Gossler K, Cordes R, Gossler A (2007) Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc Natl Acad Sci U S A 104:537–542. doi: 10.1073/pnas.0608281104 PubMedPubMedCentralGoogle Scholar
- Selleck MA, Stern CD (1991) Fate mapping and cell lineage analysis of Hensen’s node in the chick embryo. Development 112:615–626PubMedGoogle Scholar
- Sengel P (1971) The organogenesis and arrangement of cutaneous appendages in birds. Adv Morphog 9:181–230PubMedGoogle Scholar
- Serralbo O, Picard CA, Marcelle C (2013) Long term, inducible gene loss-of-function in the chicken embryo. Genesis 51(3):372–380. doi: 10.1002/dvg.22388 PubMedGoogle Scholar
- Shalaby F, Rossant J, Yamaguchi TP et al (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62–66. doi: 10.1038/376062a0 PubMedGoogle Scholar
- Stern CD (2005) The chick: a great model system becomes even greater. Dev Cell 8:9–17. doi: 10.1016/j.devcel.2004.11.018 PubMedGoogle Scholar
- Stern CD, Fraser SE (2001) Tracing the lineage of tracing cell lineages. Nat Cell Biol 3:E216–E218. doi: 10.1038/ncb0901-e216 PubMedGoogle Scholar
- Stern HM, Brown AM, Hauschka SD (1995) Myogenesis in paraxial mesoderm: preferential induction by dorsal neural tube and by cells expressing Wnt-1. Development 121:3675–3686PubMedGoogle Scholar
- Summerbell D, Ashby PR, Coutelle O et al (2000) The expression of Myf5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors. Development 127:3745–3757PubMedGoogle Scholar
- Tajbakhsh S, Bober E, Babinet C et al (1996) 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. Dev Dyn 206:291–300PubMedGoogle Scholar
- Tajbakhsh S, Borello U, Vivarelli E et al (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 125:4155–4162PubMedGoogle Scholar
- Tam P (1981) The control of somitogenesis in mouse embryos. J Embryol Exp Morphol 65:103–128PubMedGoogle Scholar
- Teillet M, Watanabe Y, Jeffs P et al (1998) Sonic hedgehog is required for survival of both myogenic and chondrogenic somitic lineages. Development 125:2019–2030PubMedGoogle Scholar
- Thiery JP, Acloque H, Huang RYJ, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139:871–890. doi: 10.1016/j.cell.2009.11.007 PubMedGoogle Scholar
- Towers M, Tickle C (2009) Growing models of vertebrate limb development. Development 136:179–190. doi: 10.1242/dev.024158 PubMedGoogle Scholar
- Tozer S, Bonnin M-A, Relaix F et al (2007) Involvement of vessels and PDGFB in muscle splitting during chick limb development. Development 134:2579–2591. doi: 10.1242/dev.02867 PubMedGoogle Scholar
- Uchikawa M (2008) Enhancer analysis by chicken embryo electroporation with aid of genome comparison. Dev Growth Differ 50:467–474. doi: 10.1111/j.1440-169X.2008.01028.x PubMedGoogle Scholar
- Vasyutina E, Birchmeier C (2006) The development of migrating muscle precursor cells. Anat Embryol 211(Suppl 1):37–41. doi: 10.1007/s00429-006-0118-9 PubMedGoogle Scholar
- Vasyutina E, Lenhard DC, Wende H et al (2007) RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc Natl Acad Sci U S A 104:4443–4448. doi: 10.1073/pnas.0610647104 PubMedPubMedCentralGoogle Scholar
- Venters SJ, Ordahl CP (2005) Asymmetric cell divisions are concentrated in the dermomyotome dorsomedial lip during epaxial primary myotome morphogenesis. Anat Embryol 209:449–460. doi: 10.1007/s00429-005-0461-2 PubMedGoogle Scholar
- Vladar EK, Antic D, Axelrod JD (2009) Planar cell polarity signaling: the developing cell’s compass. Cold Spring Harb Perspect Biol 1:a002964–a002964. doi: 10.1101/cshperspect.a002964 PubMedPubMedCentralGoogle Scholar
- Wahl MB, Deng C, Lewandoski M, Pourquié O (2007) FGF signaling acts upstream of the NOTCH and WNT signaling pathways to control segmentation clock oscillations in mouse somitogenesis. Development 134:4033–4041. doi: 10.1242/dev.009167 PubMedGoogle Scholar
- Wallingford JB (2012) Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu Rev Cell Dev Biol 28:627–653. doi: 10.1146/annurev-cellbio-092910-154208 PubMedGoogle Scholar
- Wigle JT, Oliver G (1999) Prox1 function is required for the development of the murine lymphatic system. Cell 98:769–778PubMedGoogle Scholar
- Wilting J, Becker J (2006) Two endothelial cell lines derived from the somite. Anat Embryol 211:57–63. doi: 10.1007/s00429-006-0120-2 PubMedGoogle Scholar
- Wilting J, Eichmann A, Christ B (1997) Expression of the avian VEGF receptor homologues Quek1 and Quek2 in blood-vascular and lymphatic endothelial and non-endothelial cells during quail embryonic development. Cell Tissue Res 288:207–223. doi: 10.1007/s004410050807 PubMedGoogle Scholar
- Yamaguchi TP, Bradley A, McMahon AP, Jones S (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211–1223PubMedGoogle Scholar
- Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93:23–67. doi: 10.1152/physrev.00043.2011 PubMedPubMedCentralGoogle Scholar
- Yokota Y, Saito D, Tadokoro R, Takahashi Y (2011) Genomically integrated transgenes are stably and conditionally expressed in neural crest cell-specific lineages. Dev Biol 353:382–395PubMedGoogle Scholar
- Yusuf F, Brand-Saberi B (2006) The eventful somite: patterning, fate determination and cell division in the somite. Anat Embryol 211:21–30. doi: 10.1007/s00429-006-0119-8 PubMedGoogle Scholar
- Yvernogeau L, Auda-Boucher G, Fontaine-Perus J (2012) Limb bud colonization by somite-derived angioblasts is a crucial step for myoblast emigration. Development 139:277–287. doi: 10.1242/dev.067678 PubMedGoogle Scholar