Skip to main content

Advertisement

SpringerLink
Log in

Formation and differentiation of the avian sclerotome

  • Review
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

The avian sclerotome forms by epitheliomesenchymal transition of the ventral half-somite. Sclerotome development is characterized by a craniocaudal polarization, resegmentation, and axial identity. Its formation is controlled by signals from the notochord, the neural tube, the lateral plate mesoderm, and the myotome. These signals and crosstalk between somite cells lead to the separation of various subdomains, such as the central and ventral sclerotomes that express Pax1 under the control of Sonic hedgehog and Noggin, and the dorsal and lateral sclerotome that do not express Pax1 and are controlled by Bmp-4. Further subdomains that give rise to specific derivatives are the syndetome, neurotome, meningotome, and arthrotome. The molecular control of subdomain formation and cell type specification is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3A, B
Fig. 4
Fig. 5A,B
Fig. 6A–F
Fig. 7

Similar content being viewed by others

References

  • Akazawa H, Komuro I, Sugitani Y, Yazaki Y, Nagai R, Noda T (2000) Targeted disruption of the homeobox transcription factor Bapx1 results in lethal skeletal dysplasia with asplenia and gastroduodenal malformation. Genes Cells 5:499–513

    Article  CAS  PubMed  Google Scholar 

  • Amthor H, Conolly D, Patel K, Brand-Saberi B, Wilkinson DG, Cooke J, Christ B (1996) The expression and regulation of follistatin and a follistatin-like gene (flik) during avian somite compartmentalization and myogenesis. Dev Biol 178:343–362

    Article  CAS  PubMed  Google Scholar 

  • Aoyama H (1993) Developmental plasticity of the prospective dermatome and the prospective sclerotome region of an avian somite. Dev Growth Differ 35:507–519

    Google Scholar 

  • Aoyama H, Asamoto K (1988) Determination of somite cells: independence of cell differentiation and morphogenesis. Development 104:15–28

    CAS  PubMed  Google Scholar 

  • Aoyama H, Asamoto K (2000) The developmental fate of the rostral/caudal half of a somite for vertebra and rib formation: experimental confirmation of the resegmentation theory using chick-quail chimeras. Mech Dev 99:71–82

    Article  CAS  PubMed  Google Scholar 

  • Avery G, Chow M, Holtzer H (1956) An experimental analysis of the development of the spinal column. V. Reactivity of chick somites. J Exp Zool 132:409–426

    Google Scholar 

  • Bagnall KM, Higgins S, Sanders EJ (1988) The contribution made by a single somite to the vertebral column: experimental evidence in support for resegmentation using the chick-quail chimera model. Development 103:69–85

    CAS  PubMed  Google Scholar 

  • Bagnall KM, Higgins S, Sanders EJ (1989) The contribution made by a single somite to tissues within a body segment and assessment of their integration with similar cells from adjacent segments. Development 107:931–943

    CAS  PubMed  Google Scholar 

  • Balfour FM (1881) Handbuch der vergleichenden Embryologie. 2. Band, Fischer Jena

  • Balling R, Neubüser A, Christ B (1996) Pax genes and sclerotome development. Semin Cell Dev Biol 7:129–136

    Article  Google Scholar 

  • Barnes GL, Hsu CW, Mariani BD, Tuan RS (1996) Chicken Pax-1 gene: Structure and expression during embryonic somite development. Differentiation 61:13–23

    Article  CAS  PubMed  Google Scholar 

  • Barnes GL, Alexander PG, Hsu CW, Maviani BD, Tuan RS (1997) Cloning and characterization of chicken Paraxis: a regulator of paraxial mesoderm development and somite formation. Dev Biol 189:95–111

    Article  CAS  PubMed  Google Scholar 

  • Behrens A, Haigh J, Mechta-Grigoriou F, Nagy A, Yaniv M, Wagner EF (2003) Impaired intervertebral disc formation in the absence of Jun. Development 130:103–109

    Article  CAS  PubMed  Google Scholar 

  • Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhon S, Ling KW, Sham MH, Koopman P, Tam PP, Cheak KS (1997) SOX9 directly regulates the type-II collagen gene. Nat Genet 16:174–178

    CAS  PubMed  Google Scholar 

  • Bettenhausen B, Hrabe de Angelis M, Simon D, Guenet JL, Gossler A (1995) Transient and restricted expression during mouse embryogenesis of DiI1, a murine gene closely related to Drosophila Delta. Development 121:2407–2418

    CAS  PubMed  Google Scholar 

  • Bi W, Huang W, Whitworth DJ, Deng JM, Thang Z, Behringer RR, De Crombrugghe B (2001) Happloinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci USA 98:6698–6703

    Article  CAS  PubMed  Google Scholar 

  • Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G (2004) A Twist code determines the onset of osteoblast differentiation. Dev Cell 6:423–435

    Article  CAS  PubMed  Google Scholar 

  • Blechschmidt E (1961) Die vorgeburtliche Entwicklungsstadien des menschen. Karger, Basel

  • Böhme C (1973) Lichtmikroskopische Untersuchungen über die Struktur des Leptomeninx encephalis bei Gallus domesticus. Z Anat Entwickl-Gesch 140:215–236

    Google Scholar 

  • Boncinelli E, Simeone A, Acompora D, Mavilio F (1991) HOX gene activation by retinoic acid. Trends Genet 7:329

    CAS  PubMed  Google Scholar 

  • Borycki AG, Strunk K, Savary R, Emerson CP Jr (1997) Distinct signal/response mechanisms regulate pax 1 and QmyoD activation in sclerotomal and myotomal lineages of quail somites. Dev Biol 185:185–200

    Article  CAS  PubMed  Google Scholar 

  • Borycki AG, Mendham L, Emerson CP Jr (1998) Control of somite patterning by Sonic hedgehog and its downstream signal response genes. Development 125:777–790

    CAS  PubMed  Google Scholar 

  • Brand-Saberi B, Ebensperger C, Wilting J, Balling R, Christ B (1993) The ventralizing effect of the notochord on somite differentiation in chick embryos. Anat Embryol 188:239–245

    CAS  PubMed  Google Scholar 

  • Brand-Saberi B, Wilting J, Ebensperger C, Christ B (1996) The formation of somite compartments in the avian embryo. Int J Dev Biol 40:411–420

    CAS  PubMed  Google Scholar 

  • Brand-Saberi B, Christ B (2000) Evolution and development of distinct cell lineages derived from somites. In: Ordahl CP (ed) Somitogenesis. Current topics in developmental biology, vol 47. Academic Press, New York, pp 255–296

  • Brent AE, Tabin CJ (2002) Developmental regulation of somite derivatives: muscle, cartilage and tendon. Curr Opin Genet Dev 12:548–557

    Article  CAS  PubMed  Google Scholar 

  • Brent AE, Schweitzer R, Tabin CJ (2003) A somitic compartment of tendon progenitors. Cell 113:235–248

    Article  CAS  PubMed  Google Scholar 

  • Bronner-Fraser M (1986) Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev Biol 115:44–55

    CAS  PubMed  Google Scholar 

  • Brown D, Wagner D, Li X, Richardson JA, Olson EN (1999) Dual role of the basic helix-loop-helix transcription factor scleraxis in mesoderm formation and chondrogenesis during mouse embryogenesis. Development 126:4317–4329

    CAS  PubMed  Google Scholar 

  • Buchberger A, Schwarzer M, Brand T, Pabst O, Seidl K, Arnold H.H. (1998) Chicken winged-helix transcription factor cFKH-1 prefigures axial and appendicular skeletal structures during chicken embryogenesis. Dev Dyn 212:94–101

    Article  CAS  PubMed  Google Scholar 

  • Burgess R, Rawls A, Brown D, Bradley A, Olson EN (1996) Requirement of the paraxis gene for somite formation and musculoskeletal patterning. Nature 384:570–573

    Article  CAS  PubMed  Google Scholar 

  • Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346

    CAS  PubMed  Google Scholar 

  • Burke AC (2000) Hox genes and the global patterning of the somitic mesoderm. Curr Top Dev Biol 47:155

    Article  CAS  PubMed  Google Scholar 

  • Bussen M, Petry M, Schuster-Gossler K, Leitges M, Gosslr A, Kispert A (2004) The T-box transcription factor Tbx18 maintains the separation of anterior and posterior somite compartments. Genes Dev 18:1209–1221

    Article  PubMed  Google Scholar 

  • Buttitta L, Mo R, Hui CC, Fan CM (2003) Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 130:6233–6243

    Article  CAS  PubMed  Google Scholar 

  • Capdevila J, Tabin C, Johnson RL (1998) Control of dorsoventral somite patterning by Wnt-1 and β-catenin. Dev Biol 193:182–194

    Article  CAS  PubMed  Google Scholar 

  • Carmeliet P (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med 6:389–395

    Article  CAS  PubMed  Google Scholar 

  • Cauthen CA, Berdougo E, Sandler J, Burrus LW (2001) Comparative analysis of the expression patterns of Wnts and Frizzleds during early myogenesis in chick embryos. Mech Dev 104:133–138

    Article  CAS  PubMed  Google Scholar 

  • Chen Z-F, Behringer RR (1995) Twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev 9:686–699

    CAS  PubMed  Google Scholar 

  • Chiang C, Litingtung Y, Le E, Young KF, Corden JL, Westphal H, Beachy PA (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 393:407–413

    Article  Google Scholar 

  • Christ B (1970) Experimente zur Lageentwickung der Somiten. Verh Anat Ges 64:555–564

    CAS  PubMed  Google Scholar 

  • Christ B (1975) Die Entwicklung der Körperwandmetamerie, experimentelle Untersuchungen an Hühnerembryonen. Habilitationsschrift, Ruhr-Universität Bochum

  • Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol 191:381–396

    CAS  PubMed  Google Scholar 

  • Christ B, Wilting J (1992) From somites to vertebral column. Ann Anat 174:23–32

    CAS  Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1972) Experimentelle Untersuchungen zur Somitenentstehung beim Hühnerembryo. Z Anat Entwickl.-Gesch. 138:82–97

    Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1974) Experimentelle Untersuchungen zur Entwicklung der Brustwand beim Hühnerembryo. Experientia (Basel) 30:1449–1451

  • Christ B, Jacob HJ, Jacob M (1979) Über die Gestaltungsfunktionen der Somiten bei der Entwicklung der Körperwand von Hühnerembryonen. Verh Anat Ges 73:509–518

    Google Scholar 

  • Christ B, Huang R, Wilting J (2000) The development of the avian vertebral column. Anat Embryol 202:179–194

    Article  CAS  PubMed  Google Scholar 

  • Christ B, Brand-Saberi B, Grim M, Wilting J (1992) Local signalling in dermomyotomal cell type specification. Anat Embryol 186:505–510

    CAS  PubMed  Google Scholar 

  • Christ B, Schmidt C, Huang R, Wilting J, Brand-Saberi B (1998) Segmentation of the vertebrate body. Anat Embryol 197:1–8

    Article  CAS  PubMed  Google Scholar 

  • Condie BG, Capecchi MR (1993) Mice homozygous for a targeted disruption of Hoxs-3 (Hox-4.1) exhibit anterior transformations of the first and second cervical vertebrae, the atlas and axis. Development 119:579

    CAS  PubMed  Google Scholar 

  • Corning HK (1881) Über die sogenannte Neugliederung der Wirbelsäule und über das Schicksal der Urwirbelhöhle bei Reptilien. Morph Jb 17:611–622

    Google Scholar 

  • Cserjesi P, Brwon D, Ligon KL, Lyons GE, Copeland N, Gilbert DJ, Jenkins NA, Olson EN (1995) Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 121:1099–1110

    CAS  PubMed  Google Scholar 

  • Davies JA, Cook GM, Stern CD, Keynes RJ (1990) Isolation from chick somites of a glycoprotein fraction that causes collapses of dorsal root ganglion growth cones. Neuron 4:11–19

    Article  CAS  PubMed  Google Scholar 

  • Debby-Brafmann A, Burstyn-Cohen T, Klar A, kalcheim C (1999) F-spondin is expressed in somite regions avoided by neural crest cells and mediates the inhibition of distinct somitic domains to neural crest migration. Neuron 22:475–488

    Article  PubMed  Google Scholar 

  • Del Amo FF, Smith DE, Swiatek PJ, Gendron Maguire M, Greenspan RJ, McMahon AP, Gridley T (1992) Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115:737–744

    PubMed  Google Scholar 

  • del Barco Barrantes I, Elia AJ, Wunsch K, De Angelis MH, Mak TW, Rossant J, Conlon RA, Gossler A, de la Pompa JL (1999) Interaction between Notch signalling and Lunatic fringe during somite boundary formation in the mouse. Curr Biol 9:470–480

    Article  PubMed  Google Scholar 

  • Deutsch U, Dressler GR, Gruss P (1988) Pax 1, a member of paired box homologous murine gene family, is expressed in segmented structures during development. Cell 53:617

    CAS  PubMed  Google Scholar 

  • Dietrich S, Schubert FR, Gruss P (1993) Altered Pax gene expression in mouse notochord mutants: The notochord is required to initiate and maintain ventral identity in the somite. Mech Dev 44:189–207

    Article  CAS  PubMed  Google Scholar 

  • Dietrich S, Schubert FR, Lumsden A (1997) Control of dorsoventral pattern in the chick paraxial mesoderm. Development 124:3895–3908

    CAS  PubMed  Google Scholar 

  • Dockter JL (2000) Sclerotome induction and differentiation. In: Ordahl CP (ed) Somitogenesis, part 2. Academic Press, London, pp 77–127

  • Duband J-L, Dufour S, Hatta K, Takeichi M, Edelman GM, Thiery JP (1987) Adhesion molecules during somitogenesis in the avian embryo. J Cell Biol 104:1361

    Article  CAS  PubMed  Google Scholar 

  • Duboule D, Dollé P (1989) The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J 8:1497–1505

    CAS  PubMed  Google Scholar 

  • Duboule D, Morata G (1994) Colinearity and functional hierarchy among genes of the homeotic complexes. Trend Genet 10:358–364

    Article  CAS  Google Scholar 

  • Dubrulle J, McGrew MJ, Pourquié O (2001) FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106:219–232

    Article  CAS  PubMed  Google Scholar 

  • Duong TD, Erickson CA (2004) MMP-2 plays an essential role in producing epithelial-mesenchymal transformations in the avian embryo. Dev Dyn 229:42–53

    Article  CAS  PubMed  Google Scholar 

  • Ebensperger C, Wilting J, Brand-Saberi B, Mizutani Y, Christ B, Balling R, Koseki H (1995) Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos. Anat Embryol 191:297–310

    CAS  PubMed  Google Scholar 

  • Ebner V von (1888) Urwirbel und Neugliederung der Wirbelsäule. Sitzungsber Akad Wiss Wien III/97:194–206

  • 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 42:33–48

    Article  CAS  PubMed  Google Scholar 

  • Eickholdt BJ, Mackenzie SL, Graham A, Walsh FS, Doherty P (1999) Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development 126:2181–2189

    PubMed  Google Scholar 

  • Evans DJR (2003) Contribution of somitic cells to the avian ribs. Dev Biol 256:114–126

    Article  CAS  PubMed  Google Scholar 

  • Ewan KBR, Everett AW (1992) Evidence for resegmentation in the formation of the vertebral column using the novel approach of retroviral-mediated gene transfer. Exp Cell Res 198:315–320

    CAS  PubMed  Google Scholar 

  • Fan C-M, Tessier-Lavigne M (1994) Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79:1175–1186

    Article  CAS  PubMed  Google Scholar 

  • Fan C-M, Porter JA, Chiang C, Chang DT, Beachy PA, Tessier-Lavigne M (1995) Long-range sclerotome induction by sonic hedgehog: direct role of the amino-terminal claevage product and modulation by the cyclic AMP signaling pathway. Cell 81:457–465

    CAS  PubMed  Google Scholar 

  • Folkman J, D’Amore P (1996) Blood vessel formation: what is its molecular basis? Cell 87:1153–1155

    Article  CAS  PubMed  Google Scholar 

  • Freitas C, Rodrigues S, Charrier JB, Teillet MA, Palmeirim I (2001) Evidence for medial/lateral specification and positional information within the presomitic mesoderm. Development 128:5139–5147

    CAS  PubMed  Google Scholar 

  • Füchtbauer E-M (1995) Expression of m-twist during postimplantation development of the mouse. Dev Dyn 204:316–322

    PubMed  Google Scholar 

  • Furumoto TA, Miura N, Akasaka T, Mizutani-Koseki Y, Sudo H, Fukuda K, Mackawa M, Yuara S, Fu Y, Moriya H, Taneguchi M, Imai K, Dahl E, Balling R, Parlowa M, Gossler A, Koseki H (1999) Notochord-dependent expression of MFH 1 and Pax1 cooperates to maintain the proliferation of sclerotome cells during the vertebral column development. Dev Biol 210:15–29

    Article  CAS  PubMed  Google Scholar 

  • Goldstein RS, Teillet MA, Kalcheim C (1990) The microenvironment created by grafting multiple rostral half-somites is mitogenic for neural crest cells. Proc Natl Acad Sci USA 87:4476–4480

    CAS  PubMed  Google Scholar 

  • Goldstein RS, Kalcheim C (1992) Determination of epithelial half-somites in skeletal morphogenesis. Development 116:441–445

    CAS  PubMed  Google Scholar 

  • Goldstein RS, Avivi C, Geffen R (1995) Initial axial level-dependent differences in size of avian dorsal root ganglia are imposed by the sclerotome. Dev Biol 168:214–222

    Article  CAS  PubMed  Google Scholar 

  • Gossler A, Hrabe de Angelis M (1998) Somitogenesis. Curr Top Dev Biol 38:225–287

    CAS  PubMed  Google Scholar 

  • Graham A, Papalopulu N, Krumlauf R (1989) The murine and Drosophila homeobox clusters have common features of organization and expression. Cell 5:367–378

    Article  Google Scholar 

  • Grass S, Arnold HH, Braun T (1996) Alterations in somite patterning of Myf-5-deficient mice. A possible role for FGF-4 and FGF-6. Development 122:141–150

    CAS  PubMed  Google Scholar 

  • Grobstein C, Holtzer H (1955) In vitro studies of cartilage induction in mouse somite mesoderm. J Exp Zool 128:333–356

    Google Scholar 

  • Gruss P, Kessel M (1991) Axial specification in higher vertebrates. Curr Opin Genet Dev 1:204–210

    CAS  PubMed  Google Scholar 

  • Hagedorn M, Balke M, Schmidt A, Bloch W, Kurz H, Javerzat S, Rousseau B, Wilting J, Bikfalvi A (2004) VEGF coordinates interaction of pericytes and endothelial cells during vasculogenesis and experimental angiogenesis. Dev Dyn 230:23–33

    Article  CAS  PubMed  Google Scholar 

  • Halata Z, Grim M, Christ B (1990) Origin of spinal cord meninges sheaths of peripheral nerves and cutaneous receptors including Merkel cells. An experimental and ultrastructural study with avian chimeras. Anat Embryol 182:529–537

    CAS  PubMed  Google Scholar 

  • Hall BK (1977) Chondrogenesis of the somitic mesoderm. Adv Anat Embryol Cell Biol 53:3

    CAS  Google Scholar 

  • Hanincec P, Grim M (1990) Localization of dipeptidylpeptidase IV and alkaline phosphatase in developing spinal cord meninges and peripheral nerve covernings of the rat. Int J Devl Neuroscience 8:175–185

    Article  Google Scholar 

  • Hatschek (1980) Cited after Williams LW (1910) The somites of the chick. Am J Anat 11:55–100

    Google Scholar 

  • Hatta K, Takagi S, Hajime F, Takeichi M (1987) Spatial and temporal expression patern of n-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol 120:215–227

    CAS  PubMed  Google Scholar 

  • Healy C, Uwanohgo D, Sharpe PT (1996) Expression of the chicken Sox 9 gene marks the onset of cartilage differentiation. Ann N Y Acad Sci 785:261–262

    CAS  PubMed  Google Scholar 

  • Hebrok M, Wertz K, Füchtbauer EM (1994) M-twist is an inhibitor of muscle differentiation. Dev Biol 165:537–544

    Article  CAS  PubMed  Google Scholar 

  • Henderson DJ, Conway SJ, Copp AJ (1999) Rib truncations and fusions in the Sp2H mouse reveal a role for Pax3 in specification of the ventro-lateral and posterior parts of the somite. Dev Biol 209:143–158

    Article  CAS  PubMed  Google Scholar 

  • Henkemeyer M, Marengere LEM, McGlade J, Olivier JP, Conlon R, Holmyard D, Letwin K, Pawson T (1994) Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 9:1001–1008

    CAS  PubMed  Google Scholar 

  • Hirano S, Hirako R, Kajita N, Norita M (1995) Morphological analysis of the role of the neural tube and notochord in the development of somites. Anat Embryol 192:445–457

    CAS  PubMed  Google Scholar 

  • Hirsinger E, Duprez D, Jouve C, Malapert P, Cooke J, Pourquié O (1997) Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP 4 in avian somite patterning. Development 124:4605–4614

    CAS  PubMed  Google Scholar 

  • His W (1868) Untersuchungen über die erste Anlage des Wirbelthierleibes. Die erste Entwicklung des Hühnchens im Ei. Vogel, Leipzig

  • Hoang BH, Thomas JT, Abdul-Karim FW, Correia KM, Conlon RA, Luyten FP, Ballock RT (1998) Expression pattern of two Frizzled-related genes, Frzb-1 and Sfrp-1 during mouse embryogenesis suggests a role for modulating action of Wnt family members. Dev Dyn 212:364–374

    Article  CAS  PubMed  Google Scholar 

  • Hochstetter F (1934) Über die Entwicklung und Differenzierung der Hüllen des Rückenmarkers beim Menschen. Morph Jb 74:1–104

    Google Scholar 

  • Hogan KA, Ambler CA, Chapman DL, Bautch VL (2003) The neural tube patterns vessels developmentally using the VEGF signaling pathway. Development 131:1503–1513

    Article  Google Scholar 

  • Holtzer H (1951) Morphogenetic influence of the spinal cord on the axial skeleton and musculature. Anat Rec 109:373–374

    Google Scholar 

  • Holtzer H (1952a) An experimental analysis of the development of the spinal column: the dispensability of the notochord. J Exp Zool 121:573–591

    Google Scholar 

  • Holtzer H (1952b) An experimental analysis of the development of the spinal column. I. Response of precartilage cells to size variations of the spinal cord. J Exp Zool 121:121–148

    Google Scholar 

  • Holtzer H, Detwiler SR (1953) An experimental analysis of the development of the spinal column. III. Induction of skeletogenous cells. J Exp Zool 123:335–366

    Google Scholar 

  • Holtzer H, Detwiler SR (1954) The dependence of somitic differentiation on the neural axis. Anat Rec 118:390

    Google Scholar 

  • Hornik C, Brand-Saberi B, Rudloff S, Schmidt C, Christ B, Füchtbauer E-M (2004) Twist is an integrator of SHH, FGF and BMP signaling. (submitted)

  • Hrabe de Angelis M, McIntyre J, Gossler A (1997) Maintenance of somite borders in mice requires the Delta homologue DII1. Nature 386:717–721

    Article  PubMed  Google Scholar 

  • Huang R; Zhi Q, Wilting J, Christ B (1994) The fate of somitocoele cells in avian embryos. Anat Embryol 190:243–250

    CAS  PubMed  Google Scholar 

  • Huang R, Zhi Q, Neubüser A, Müler TS, Brand-Saberi B, Christ B, Wilting J (1996) Function of somite and somitocoele cells in the formation of the vertebral motion segment in avian embryo. Acta Anat 155:231–241

    CAS  Google Scholar 

  • Huang R, Zhi Q, Brand-Saberi B, Christ B (2000a) New experimental evidence for somite resegmentation. Anat Embryol 202:195–200

    Article  CAS  PubMed  Google Scholar 

  • Huang R, Zhi Q, Wilting J, Christ B (2000b) Sclerotomal origin of the ribs. Development 127:527–532

    CAS  PubMed  Google Scholar 

  • Huang R, Stolte D, Kurz H, Ehehalt F, Cann GM, Stockdale FE, Patel K, Christ B (2003) Ventral axial organs regulate expression of myotomal Fgf-8 that influences rib development. Dev Biol 255:30–47

    Article  CAS  PubMed  Google Scholar 

  • Iida K, Koseki H, Kakinuma H, Kato M, Mizutani-Koseki Y, Ohuchi H, Yoshioka H, Noji S, Kawamura K, Kataoka Y, Ueno F, Taneguchi M, Yoshida N, Sugiyama T, Miura N (1997) Essential role of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 124:4627–4638

    CAS  PubMed  Google Scholar 

  • Ikeya M, Takada S (1998) Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125:4969–4976

    CAS  PubMed  Google Scholar 

  • Jacob M, Christ B, Jacob H-J (1975a) Über die regionale Determination des paraxialen Mesoderms junger Hühnerembryonen. Verh Anat Ges 69:263–269

    CAS  PubMed  Google Scholar 

  • Jacob M, Jacob HJ, Christ B (1975b) Die frühe Differenzierung des chordanahen Bindegewebes. Raster- und transmissionselektronenmikroskopische Untersuchungen an Hühnerembryonen. Experientia 31:1083–1086

    CAS  PubMed  Google Scholar 

  • Jen WC, Wettstein D, Turner D, Chitnis A, Kintner C (1997) The Notch ligand, X-Delta-1, mediates segmentation of the paraxial mesoderm in Xenopus embryos. Development 124:1169–1178

    CAS  PubMed  Google Scholar 

  • Johnson RL, Läufer E, Riddle RD, Tabin C (1994) Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79:1165–1173

    Article  PubMed  Google Scholar 

  • Johnson J, Rhee J, Parsons SM, Brown D, Olson EN, Rawls A (2001) The anterior/posterior polarity of somites is disrupted in paraxis-deficient mice. Dev Biol 229:176

    Article  CAS  PubMed  Google Scholar 

  • Kaestner KH, Bleckmann SC, Monaghan AP, Scholondorff J, Mincheva A, Lichter P, Schutz G (1996) Clustered arrangement of winged helix 1 genes fkh-6 and MFH 1. Possible implications for mesoderm development. Development 122:1751–1758

    CAS  PubMed  Google Scholar 

  • Kahane N, Cinnamon Y, Kalcheim C (1998) The origin and fate of pioneer myotomal cells in the avian embryo. Mech Dev 74:59–73

    Article  CAS  PubMed  Google Scholar 

  • Kerr RSE, Newgreen DF (1997) Isolation and characterization of chondroitin sulfate proteoglycans from embryonic quail that influence neural crest cell behavior. Dev Biol 192:108–115

    Article  CAS  PubMed  Google Scholar 

  • Kessel M, Balling R, Gruss P (1990) Variations of cervical vertebrae after expression of a Hox-1.1 transgene mice. Cell 61:301

    CAS  PubMed  Google Scholar 

  • Kessel M (1991) Molecular coding of axial positions by Hox genes. Semin Dev Biol 2:367

    Google Scholar 

  • Kessel M (1992) Respecification of vertebral identities by retinoic acid. Development 115:487

    CAS  PubMed  Google Scholar 

  • Kessel M, Gruss P (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:89–104

    CAS  PubMed  Google Scholar 

  • Keynes RJ, Stern CD (1984) Segmentation in the vertebrate nervous system. Nature 310:786–789

    CAS  PubMed  Google Scholar 

  • Kieny M, Mauger A, Sengel P (1972) Early regionalization of somitic mesoderm as studied by the development of axial skeleton of the chick embryo. Dev Biol 28:142–161

    CAS  PubMed  Google Scholar 

  • Klessinger S, Christ B (1996) Axial structures control laterality in the distribution pattern of endothelial cells. Anat Embryol 193:319–330

    CAS  PubMed  Google Scholar 

  • Koseki H, Wallin J, Wilting J, Mizutani Y, Kispert A, Ebensperger C, Herrmann BG, Christ B, Balling R (1993) A role of Pax-1 as a mediator of notochordal signals during the dorso-ventral specification of vertebrae. Development 119:649–660

    CAS  PubMed  Google Scholar 

  • Kostic D Capecchi MR (1994) Targeted disruption of the murine Hoxa-4 and Hoxa-6 genes result in homeotic transformations of the vertebral column. Mech Dev 46:231–247

    Article  CAS  PubMed  Google Scholar 

  • Kraus F, Haenig B, Kispert A (2001) Cloning and expression analysis of the mouse T-box gene Tbx 18. Mech Dev 100:83–86

    Article  CAS  PubMed  Google Scholar 

  • Krumlauf R (1994) Hox genes in vertebrate development. Cell 78:191

    Article  CAS  PubMed  Google Scholar 

  • Kurz H, Gärtner T, Eggli PS, Christ B (1996) First blood vessels in the avian neural tube are formed by a combination of dorsal angioblast immigration and ventral sprouting of endothelial cells. Dev Biol 173:133–147

    Article  CAS  PubMed  Google Scholar 

  • Landolt RM, Vaugham L, Winterhalter KH, Zimmermann DR (1995) Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration an axon outgrowth. Development 121:2303

    CAS  PubMed  Google Scholar 

  • Lash J, Holtzer S, Holtzer H (1957) An experimental analysis of the development of the spinal column. Exp Cell Res 13:292–303

    CAS  PubMed  Google Scholar 

  • Lash JW, Hommes FA, Zilliken F (1962) Induction of cell differentiation. I. The in vitro induction of vertebral cartilage with a low-molecular-weight tissue component. Biochim Biophys Acta 56:313–319

    Article  CAS  PubMed  Google Scholar 

  • Layer PG, Alber A, Rathjen FG (1988) Sequential activation of butyrylcholinesterase in motoneurons and myotoms preceding growth of motor axons. Development 102:387–396

    CAS  PubMed  Google Scholar 

  • Lee C, Buttitta L, May N, Kispert A, Fan C (2000) SHH-N upregulates Sfrp2 to mediate its competitive interaction with WNT4 in the somitic mesoderm. Development 127:109–118

    CAS  PubMed  Google Scholar 

  • Lee C, Buttitta L, Fan CM (2001) Evidence that the WNT-inducible growth arrest-specific gene 1 encodes an antagonist of sonic hedgehog signaling in the somite. Proc Natl Acad Sci USA 98:11347–11352

    Article  CAS  PubMed  Google Scholar 

  • Leitges M, Neidhardt L, Haenig B, Herrmann BG, Kispert A (2000) The paired homeobox gene Uncx4.1 specifies pedicles transverse processes and proximal ribs of the vertebral column. Development 127:2259–2267

    CAS  PubMed  Google Scholar 

  • Lettice LA, Purdie LA, Carlson GJ, Kilanowski F, Dorin J, Hill RE (1999) The mouse bagpipe gene controls development of axial skeleton, skull and spleen. Proc Natl Acad Sci USA 96:9655–9700

    Article  Google Scholar 

  • Lufkin T, Mark M, Hart CP, Dollé P, Le Meur M, Chambon P (1992) Homeotoc transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature 359:835–841

    Article  CAS  PubMed  Google Scholar 

  • Mackie EJ, Tucker RP, Halfter W, Chiquet-Evishmann R, Epperlein H-H (1988) The distribution of tenascin coincides with pathway of neural crest cell migration. Development 102:237–256

    CAS  PubMed  Google Scholar 

  • Mankoo BS, Skuntz S, Hassegan I, Grigorieven E, Cabdia AL, Wright CVW, Arnheiter H, Pachnis V (2003) The concerted action of Meox homeobox genes is required upstream of genetic pathways essential for the formation, patterning and differentiation of somites. Development 130:4655–4664

    Article  CAS  PubMed  Google Scholar 

  • Mankoo BS, Collins NS, Ashby P, Grigoriera E, Pevny LH, Candia A, Wright CVE, Rigby PWJ, Pachnis V (1999) Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature 400:69–73

    Article  CAS  PubMed  Google Scholar 

  • Mansouri A, Yokota Y, Wehr R, Copeland NG, Jenkins NA, Gruss P (1997) Paired-related murine homeobox gene expressed in the developing sclerotome, kidney and nervous system. Dev Dyn 210:53–65

    Article  CAS  PubMed  Google Scholar 

  • Mansouri A, Voss AK, Thomas T, Yokota Y, Gruss P (2000) Uncx4.1 is required for the formation of the pedicles and proximal ribs and acts upstream of Pax-9. Development 127:2251–2258

    CAS  PubMed  Google Scholar 

  • Marin F, Nieto MA (2004) Expression of chicken slug and snail in mesenchymal components of the developing central nervous system. Dev Dyn 230:144–148

    Article  CAS  PubMed  Google Scholar 

  • Marti E, Takada R, Bumcrot DA, Sasaki H, McMahon AP (1995) Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121:2537–2547

    CAS  PubMed  Google Scholar 

  • McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283

    Article  CAS  PubMed  Google Scholar 

  • McMahon JA, Takada S, Zimmermann LB, Fan CM, Harland RM, McMahon AP (1998) Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev 12:1438–1452

    CAS  PubMed  Google Scholar 

  • Medina-Martinez O, Bradley A, Ramirez-Solis R (2000) A large targeted deletion of Hoxb1-Hoxb9 produces a series of single-segment anterior homeotic transformations. Dev Biol 222:71

    Article  CAS  PubMed  Google Scholar 

  • Miura N, Wanaka A, Tohyama M, Tanaka K (1993) MFH 1, a new member of the forkhead domain family is expressed in developing mesenchyme. FEBS Lett 326:171–176

    Article  CAS  PubMed  Google Scholar 

  • Monsoro-Burq AH, Le Douarin NM (2000) Duality of molecular signaling involved in vertebral chondrogenesis. In: Ordahl CP (ed) Somitogenesis, part 2. Academic Press, London, pp 43–75

  • Monsoro-Burq AH, Duprez D, Watanabe Y, Bontoux M, Vincent C, Brickell P, Le Douarin N (1996) The role of bone morphogenetic proteins in vertebral development. Development 122:3607–3616

    PubMed  Google Scholar 

  • Müller TS, Ebensperger C, Neubüser A, Koseki H, Balling R, Christ B, Wilting J (1996) Expression of avian Pax-1 and Pax-9 in the sclerotomes is controlled by axial and lateral tissues, but intrinsically regulated in pharyngeal endoderm. Dev Biol 178:403–417

    Article  PubMed  Google Scholar 

  • Murtaugh LC, Chyung JH, Lassar AB (1999) Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13:225–237

    CAS  PubMed  Google Scholar 

  • Murtaugh LC, Zeng I, Chyung JH, Lassar AB (2001) The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMP-dependent axial chondrogenesis. Dev Cell 1:411–422

    Article  CAS  PubMed  Google Scholar 

  • Neidhardt L, Lispert A, Hermann BG (1997) A mouse gene of the paired-related homeobox class expressed in the caudal somite compartment and in the developing vertebral column, kidney and nervous system. Dev Genes Evol 207:330–339

    Article  CAS  Google Scholar 

  • Neubüser A, Koseki H, Balling R (1995) Characterisation and developmental expression of Pax9, a paired-box-containing gene related to Pax1. Dev Biol 170:701

    Article  PubMed  Google Scholar 

  • Nimmagadda S, Geetha Loganathan P, Wilting J, Christ B, Huang R (2004a) Expression pattern of VEGFR-2 (Quek1) during quail development. Anat Embryol (in press)

  • Nimmagadda S, Geetha Loganathan P, Christ B, Huang R (2004b) BMP-4 and noggin control embryonic blood vessel formation by antagonistic regulation of VEGFR-2 (Quek1) expression. (submitted)

  • Noll M (1993) Evolution and role of Pax genes. Curr Opin Genet Dev 3:595–605

    Article  CAS  PubMed  Google Scholar 

  • Norris WE, Stern CD, Keynes RJ (1989) Molecular differences between the rostral and caudal halves of the sclerotome in the chick embryo. Development 105:541

    CAS  PubMed  Google Scholar 

  • Oakley RA, Tosney KW (1991) Peanut agglutinin and chondroitin-6-sulfate are molecular markers for tissues that act as barriers to axon advance in the avian embryo. Dev Biol 147–156

  • Ohta K, Nakamura M, Hirokawa K, Tanaka S, Iwama A, Suda T, Ando M, Tanaka H (1996) The receptor tyrosine kinase, Cek8, is transiently expressed on subtypes of motoneurons in the spinal cord during development. Mech Dev 54:59–69

    Article  CAS  PubMed  Google Scholar 

  • Olivera-Martinez I, Coltey M, Dhouailly D, Pourquié O (2000) Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras. Development 127:4611–4617

    CAS  PubMed  Google Scholar 

  • Olivera-Martinez I, Thelu J, Teillet MA, Dohouailly D (2001) Dorsal dermis development depends on a signal from the dorsal neural tube, which can be substituted by Wnt-1. Mech Dev 100:233–244

    Article  CAS  PubMed  Google Scholar 

  • O’Rahilly R, Müller F (1986) The meninges in human development. J Neuropath Exp Neurol 45:588–608

    CAS  PubMed  Google Scholar 

  • Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114:339–353

    CAS  PubMed  Google Scholar 

  • Ostrovsky D, Sanger JW, Lash JW (1988) Somitogenesis in the mouse embryo. Cell Differ 23:17–26

    Article  CAS  PubMed  Google Scholar 

  • Pardanaud L, Dieterlen-Lievré F (1993) Emergence of endothelial and hemopoietic cells in the avian embryo. Anat Embryol 187:107–114

    CAS  PubMed  Google Scholar 

  • Pardanaud L, Luton D, Progent M, Bourcheix LM, Catala M, Dieterlen-Lievre F (1996) Two distinct endothelial lineages in ontogeny, one of them related to hemopiesis. Development 122:1363–1371

    CAS  PubMed  Google Scholar 

  • Parker LH, Schmidt M, Jin S-W, Gray AM, Beis D, Pham T, Frantz G, Palmieri S, Hillan K, Stainier DYR, de Sauvage FJ, Ye W (2004) The endothelial-cell-derived secreted factor Egfl7 regulates vascular tube formation. Nature 428:754

    Article  CAS  PubMed  Google Scholar 

  • Peters H, Doll U, Niessing J (1995) Differential expression of the chicken Pax-1 and Pax-9 gene. In situ hybridization and immunohistochemical analysis. Dev Dyn 203:1–16

    CAS  PubMed  Google Scholar 

  • Peters H, Wilm B, Sakai N, Imai K, Maas R, Balling R (1999) Pax 1 and Pax 9 synergistically regulate vertebral column development. Development 126:5399–5407

    CAS  PubMed  Google Scholar 

  • Pourquié O, Coltey M, Bréant C, Le Douarin NM (1995) Control of somite patterning by signals from the lateral plate. Proc Natl Acad Sci USA 92:3219–3223

    PubMed  Google Scholar 

  • 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 of BMP4. Cell 84:461–471

    Article  PubMed  Google Scholar 

  • Reaume AG, Conlon RA, Zirngibl R, Yamaguchi TP, Rossant J (1992) Expression analysis of a Notch homologue in the mouse embryo. Dev Biol 154:377–387

    CAS  PubMed  Google Scholar 

  • Remak R (1850) Untersuhcungen über die Entwicklung der Wirbelthiere. Reimer, Berlin

  • Rickmann M, Fawcett LW, 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 Morph 90:437

    CAS  PubMed  Google Scholar 

  • Rida PCG, Le Minh N, Jiang Y-J (2004) A Notch feeling of somite segmentation and beyond. Dev Biol 265:2–22

    Article  CAS  PubMed  Google Scholar 

  • Ring C, Hassell J, Halfter W (1996) Expression pattern of collagen IX and potential role in the segmentation of the peripheral nervous system. Dev Biol 180:41

    Article  CAS  PubMed  Google Scholar 

  • Robinson V, Smith A, Felnniken AM, Wilkinson DG (1997) Roles of Eph receptors and ephrins in neural crest pathfinding. Cell Tissue Res 290:265–274

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo I, Hill RE, Balling R, Münsterberg A, Imai K (2003) Pax1 and Pax9 activate Bapx1 to induce chondrogenic differentiation in the sclerotome. Development 130:473–482

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo I, Bovolenta P, Mankoo BS, Imai K (2004) Meox homeodomain proteins are required for Bapx1 expression in the sclerotome and activate its transcription by direct binding to its promoter. Mol Cell Biol 24:2757–2766

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Niedenführ M, Dathe V, Jacob HJ, Pröls F, Christ B (2003) Spatial and temporal pattern of Wnt-6 expression during chick development. Anat Embryol 206:447–451

    PubMed  Google Scholar 

  • Saga Y, Takeda H (2001) The making of the somite: molecular events in vertebrate segmentation. Nat Rev Genet 2:835–845

    Article  CAS  PubMed  Google Scholar 

  • Sanders EJ (1997) Cell death in the avian sclerotome. Dev Biol 192:551–563

    Article  CAS  PubMed  Google Scholar 

  • Sanders EJ, Parker E (2001) Ablation of axial structures activates apoptotic pathways in somite cells of the chick embryo. Anat Embryol 204:389–398

    Article  CAS  PubMed  Google Scholar 

  • Schmidt C, Christ B, Patel K, Brand-Saberi B (1998) Experimental induction of BMP-4 expression leads to apoptosis in the paraxial and lateral plate mesoderm. Dev Biol 202:253–263

    Article  CAS  PubMed  Google Scholar 

  • Schmidt C, Stoeckelhuber M, McKinnell I, Putz R, Christ B, Patel K (2004) Wnt 6 regulates the epithelialisation process of the segmental plate mesoderm leading to somite formation. Dev Biol 271:198–209

    Article  CAS  PubMed  Google Scholar 

  • Schrägle J, Huang R, Christ B, Pröls F (2004) Control of the temporal and spatial Uncx4.1 expression in the paraxial mesoderm of avian embryos. Anat Embryol (in press)

  • Schubert FR, Mootoosamy RC, Walters EH, Graham A, Tumiotto L, Münsterberg AE, Lumsden A, Dietrich S (2002) Wnt6 marks sites of epithelial transformations in the chick embryo. Mech Dev 114:143–148

    Article  CAS  PubMed  Google Scholar 

  • Schweitzer R, Chyung JH, Murtaugh LC, Brent AE, Rosen V, Olson EN, Lassar A, Tabin CJ (2001) Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments. Development 128:3855–3866

    CAS  PubMed  Google Scholar 

  • Smits O, Lefebre V (2003) Sox 5 and Sox 6 are required for notochord extracellular matrix sheath formation, notochord cell survival and development of the nucleus pulposus of intervertebral discs. Development 130:1135–1148

    Article  CAS  PubMed  Google Scholar 

  • Solursh M, Fischer M, Meier S, Singley CT (1979) The role of extracellular matrix in the formation of the sclerotome. J. Embryol Exp Morph 54:75–98

    CAS  Google Scholar 

  • Spicer DB, Rhee J, Cheung WL, Lassar AB (1996) Inhibition of myogenic bHLH and MEF 2 transcription factors by the bHLH protein twist. Science 272:476–1480

    PubMed  Google Scholar 

  • Stern C, Sisodaya S, Keynes R (1986) Interactions between neurites and somite cells: inhibition and stimulation of nerve growth in the chick embryo. J Embryol Exp Morph 91:209–226

    CAS  PubMed  Google Scholar 

  • Stockdale FE, Nikovits W Jr, Christ B (2000) Molecular and cellular biology of avian somite development. Dev Dyn 219:304–321

    Article  CAS  PubMed  Google Scholar 

  • Stolte D, Huang R, Christ B (2002) Spatial and temporal pattern of Fgf-8 expression during chicken development. Anat Embryol 205:1–6

    Article  CAS  PubMed  Google Scholar 

  • Strudel G (1955) L’action morphogène du tube nerveux et de la corde sur la differenciation des vertèbres et des muscles vertebraux chez l’embryon de poulet. Arch Anat Microsc Morphol Exp 44:209–235

    CAS  Google Scholar 

  • Strudel G (1962) Induction de cartilage in vitro par l’extrait de tube nerveux et de chorde de l’embryon de poulet. Dev Biol 4:67–86

    CAS  PubMed  Google Scholar 

  • Sudo H, Takahashi Y, Tonegawa A, Arase Y, Aoyama H, Mizutani-Koseki Y, Moriya H, Wilting J, Christ B, Koseki H (2001) Inductive signals from the somatopleure mediated by bone morphogenetic proteins are essential for the formation of the sternal component of avian ribs. Dev Biol 232:284–300

    Article  CAS  PubMed  Google Scholar 

  • Takeichi M (1988) The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102:630–655

    Google Scholar 

  • Tallquist MD, Weismann KE, Hellström M, Soriano P (2000) Early myotome specification regulates PDGFA expression and axial skeleton development. Development 127:5059–5070

    CAS  PubMed  Google Scholar 

  • Tan S-S, Crossin KL, Hoffman S, Edelman GM (1987) Asymmetric expression in somite of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc Natl Acad Sci USA 84:7988–7981

    Google Scholar 

  • Teillet M-A, Kalcheim C, Le Douarin NM (1987) Formation of the dorsal root ganglion in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. Dev Biol 120:329

    CAS  PubMed  Google Scholar 

  • Teillet M-A, Watanabe Y, Jeffs P, Duprez D, Lapointe F, Le Douarin NM (1998) Sonic hedgehog is required for survival of both myogenic and chondrogenic somitic lineages. Development 125:2019–2030

    CAS  PubMed  Google Scholar 

  • Töndury G (1958) Entwicklungsgeschichte und Fehlbildungen der Wirbelsäule. Hippokrates, Stuttgart

  • Tosney KW (1991) Cell and cell-interactions that guide motor axons in the developing chick embryo. Bio Essays 13:17–24

    CAS  Google Scholar 

  • Trelstad RL (1977) Mesenchymal cell polarity and morphogenesis of chick cartilage. Dev Biol 59:153–163

    CAS  PubMed  Google Scholar 

  • Tribioli C, Lufkin T (1999) The murine Bapx 1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development 126:5699–5711

    CAS  PubMed  Google Scholar 

  • Verbout AJ (1985) The development of the vertebral column. Adv Anat Embryol Cell Biol 90:1–122

    CAS  PubMed  Google Scholar 

  • Wagner J, Schmidt C, Nikovits W Jr, Christ B (2000) Compartmentalization of the somite and myogenesis in chick embryos are influenced by Wnt-expression. Dev Biol 228:86–94

    Article  CAS  PubMed  Google Scholar 

  • Wallin J, Wilting J, Koseki H, Fritsch R, Christ B, Balling R (1994) The role of Pax-1 in axial skeleton development. Development 120:1109–1121

    CAS  PubMed  Google Scholar 

  • Walther C, Guenet J-L, Simon D, Deutsch U, Jostes B, Goulding M, Plachow D, Balling R, Gruss P (1991) Pax: A murine multigene family of paired box containing genes. Genomics 11:424–434

    CAS  PubMed  Google Scholar 

  • Wang HU, Anderson DJ (1997) Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest cell migration and motor axon outgrowth. Neuron 18:383

    Article  CAS  PubMed  Google Scholar 

  • Watanabe Y, Le Douarin NM (1996) A role for BMP-4 in the development of subcutaneous cartilage. Mech Dev 57:69–78

    Article  CAS  PubMed  Google Scholar 

  • Wheelock M, Knudsen K (1991) N-cadherin-associated proteins in chicken muscle. Differentiation 46:35–42

    CAS  PubMed  Google Scholar 

  • Williams LW (1910) The somites of the chick. Am J Anat 11:55–100

    Google Scholar 

  • Winnier GE, Hargett L, Hogan BLM (1997) The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryos. Genes Dev 11:926–940

    CAS  PubMed  Google Scholar 

  • Wilting J, Kurz H, Brand-Saberi B, Steding G, Yang YX, Hasselhorn MM, Epperlein HH, Christ B (1994) Kinetics and differentiation of somite cells forming the vertebral column: studies on human and chick embryos. Anat Embryol 190:573–581

    CAS  PubMed  Google Scholar 

  • Wilting J, Ebensperger C, Müller TS, Koseki H, Wallin J, Christ B (1995a) Pax-1 in the development of the cervico-occipital transitional zone. Anat Embryol 192:221–227

    CAS  PubMed  Google Scholar 

  • Wilting J, Brand-Saberi B, Huang R, Zhi Q, Köntges G, Kühlewein M, Ordahl CP, Christ B (1995b) The angiogenic potential of the avian somite. Dev Dyn 202:165–171

    CAS  PubMed  Google Scholar 

  • Wilting J, Brand-Saberi B, Kurz H, Christ B (1995c) Development of the embryonic vascular system. Cell Mol Biol Res 41:219–232

    CAS  PubMed  Google Scholar 

  • Wilting J, Papoutsi M, Schneider M, Christ B (2000) The lymphatic endothelium of the avian wing is of somitic origin. Dev Dyn 217:271–278

    Article  CAS  PubMed  Google Scholar 

  • Wilting J, Papoutsi M, Othmanm-Hassan K, Rodriguez-Niedenführ M, Pröls F, Tomarev S, Eichmann A (2001) Development of the avian lymphatic system. Microsc Res Tech 55:81–91

    Article  CAS  PubMed  Google Scholar 

  • Wilting J, Christ B, Yuan Li, Eichmann A (2003) Cellular and molecular mechanisms of embryonic haemangiogenesis and lymphangiogenesis. Naturwissenschaften 90:433–448

    Article  CAS  PubMed  Google Scholar 

  • Zakány J, Kmita M, Alarcon P, de la Pompa JL, Duboule D (2001) Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106:207–217

    Article  PubMed  Google Scholar 

  • Zeng L, Kempf H, Murtaugh LC, Sato ME, Lassar AB (2002) Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis. Genes Dev 16:1990–2005

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the members of our laboratory who have contributed to this work, Ulrike Uhl for typing the manuscript, and Dr. Chaya Kalcheim and Dr. Baljinder Mankoo for their comments. We also thank the Deutsche Forschungsgemeinschaft for continuous financial support.

Author information

Authors and Affiliations

  1. Institute of Anatomy and Cell Biology II, University of Freiburg, Albertstrasse 17, 79104 , Freiburg, Germany

    Bodo Christ, Ruijin Huang & Martin Scaal

Authors
  1. Bodo Christ
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruijin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Scaal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bodo Christ.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Christ, B., Huang, R. & Scaal, M. Formation and differentiation of the avian sclerotome. Anat Embryol 208, 333–350 (2004). https://doi.org/10.1007/s00429-004-0408-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-004-0408-z

Keywords

Search

Navigation