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Formation and differentiation of the avian sclerotome

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.

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References

  1. 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

  2. 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

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

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

  5. 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

  6. 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

  7. 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

  8. 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

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

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

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

  12. 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

  13. 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

  14. 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

  15. 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

  16. 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

  17. 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

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

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

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

  21. 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

  22. 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

  23. 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

  24. 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

  25. 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

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

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

  28. 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

  29. 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

  30. 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

  31. 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

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

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

  34. 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

  35. 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

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

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

  38. 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

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

  40. 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

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

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

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

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

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

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

  47. 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

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

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

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

  51. 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

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

  53. 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

  54. 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

  55. 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

  56. 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

  57. 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

  58. 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

  59. 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

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

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

  62. 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

  63. 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

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

  65. 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

  66. 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

  67. 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

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

  69. 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

  70. 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

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

  72. 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

  73. 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

  74. 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

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

  76. 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

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

  78. 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

  79. 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

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

  81. 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

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

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

  84. 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

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

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

  87. 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

  88. 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

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

  90. 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

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

  92. 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

  93. 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

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

  95. 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

  96. 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

  97. 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

  98. 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

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

  100. 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

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

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

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

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

  105. 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

  106. 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

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

  108. 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)

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

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

  111. 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

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

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

  114. 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

  115. 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

  116. 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

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

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

  119. 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

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

  121. 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

  122. 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

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

  124. 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

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

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

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

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

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

  130. 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

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

  132. 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

  133. 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

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

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

  136. 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

  137. 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

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

  139. 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

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

  141. 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

  142. 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

  143. 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

  144. 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

  145. 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

  146. 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

  147. 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

  148. 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

  149. 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

  150. 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

  151. 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

  152. 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

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

  154. 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

  155. 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

  156. 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

  157. 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

  158. 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

  159. 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

  160. 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

  161. 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

  162. 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

  163. 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

  164. 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)

  165. 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)

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

  167. 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

  168. 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

  169. 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

  170. 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

  171. 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

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

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

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

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

  176. 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

  177. 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

  178. 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

  179. 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

  180. 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

  181. 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

  182. 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

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

  184. 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

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

  186. 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

  187. 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

  188. 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

  189. 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

  190. 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

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

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

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

  194. 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

  195. 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

  196. 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)

  197. 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

  198. 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

  199. 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

  200. 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

  201. 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

  202. 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

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

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

  205. 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

  206. 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

  207. 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

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

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

  210. 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

  211. 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

  212. 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

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

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

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

  216. 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

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

  218. 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

  219. 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

  220. 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

  221. 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

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

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

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

  225. 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

  226. 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

  227. 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

  228. 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

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

  230. 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

  231. 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

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

  233. 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

  234. 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

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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.

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Correspondence to Bodo Christ.

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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

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Keywords

  • Avian embryo
  • Somite
  • Sclerotome
  • Sclerotomal subdomains
  • Differentiation
  • Vertebral column