Advertisement

Spatiotemporal Pattern Formation in Early Development: A Review of Primitive Streak Formation and Somitogenesis

  • S. Schnell
  • K. J. Painter
  • P. K. Maini
  • H. G. Othmer
Part of the The IMA Volumes in Mathematics and its Applications book series (IMA, volume 121)

Abstract

The basic body plan of a number of vertebrates results from two processes that occur early in the development of the blastoderm: large scale rearrangements of tissue via a process called gastrulation, and axial subdivision of tissue in a process called somitogenesis. The first step of gastrulation in avians is formation of the primitive streak, which marks the first clear manifestation of the anterior-posterior axis. Cell movements that occur through the streak ultimately convert the single layeredblastoderm into a trilaminar blastoderm comprising prospective endodermal, mesodermal and ectodermal tissue. During streak formation a group of cells moves anteriorly as a coherent column from the posterior end of the blastoderm, and as it proceeds other cells stream over the lateral edges of the furrow left behind. The anterior end of the streak is a specialized structure called Hensen’s node, which serves as an organizing center for later axis formation and determination of the left-right asymmetry of the body. Soon after the primitive streak forms, Hensen’s node regresses towards the tail, leaving the notochord and a pair of segmental plates parallel to the primitive streak in its wake. The posterior end of the segmental plate moves down the cranio-caudal axis with the node, as more cells are added to it by cell division within the plate and by cells entering from the primitive streak. A pair of somites forms from the anterior ends of the two plates at regular intervals. Despite the fact that much is known about the basic biological processes, the mechanisms that underlie the formation of the primitive streak and somitogenesis are still unknown, and elucidating them is one of the major unsolved problems in developmental biology. Mathematical modelling has been a useful tool in this process, as it provides a framework in which to study the outcome of proposed interactions and can make experimentally testable predictions. In this paper we outline the biological background of these processes and reviewexisting models of them.

Key words

Primitive streak formation somitogenesis theoretical models math-ematical models Hox genes c-hairy-1 Notch-Delta genes 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. [1]
    M. Abercrombie, The effects of antero-posterior reversal of lengths of the primitive streak in the, Phil. Trans. Roy. Soc. Lond. B., 234 (1950), pp. 317–338.CrossRefGoogle Scholar
  2. [2]
    H. Aoyama and K. Asamoto, Determination of somite cells: Independence of cell differentiation and morphogenesis, Development, 104 (1988), pp. 15–28.Google Scholar
  3. [3]
    Y. Azar and H. Eyal-Giladi, Marginal zone cells, the primitive streak inducing component of the primary hypoblast in the chick., J. Embryol. Exp. Morphol., 52 (1979), pp. 79–88.Google Scholar
  4. [4]
    —, Interaction of epiblast and hypoblast in the formation of the primitive streak and the embryonic axis in the chick, as revealed by hypoblast rotation experiments., J. Embryol. Exp. Morphol., 61 (1981), pp. 133–144.Google Scholar
  5. [5]
    R. Bachvarova, Establishment of anterior-posterior polarity in avian embryos, Curr. Opin. Gen. Dev., 9 (1999), pp. 411–416.CrossRefGoogle Scholar
  6. [6]
    R. Bachvarova, I. Skromme, and C.D. Stern, Induction of primitive streak and hensen’s node by the posterior marginal zone in the early chick embryo, Development, 125 (1998), pp. 3521–3534.Google Scholar
  7. [7]
    R. Bellairs, The development of somites in the chick embryo, J. Embryol. Exp. Morph., 11 (1963), pp. 697–714.Google Scholar
  8. [8]
    —, The segmentation of somites in the chick embryo, Bull. Zool., 47 (1980), pp. 245–252.CrossRefGoogle Scholar
  9. [9]
    R. Bellairs, D.A. Ede, and J.W. Lash, eds., Somites in Developing Embryos, Plenum Press, New York, NY, USA; London, UK, 1986.Google Scholar
  10. [10]
    R. Bellairs and M. Osmond, The Atlas of Chick Development, Academic Press, London, 1998.Google Scholar
  11. [11]
    R. Bellairs and M. Veini, An experimental analysis of somite segmentation in the chick embryo., J. Embryol. Exp. Morph., 55 (1980), pp. 93–108.Google Scholar
  12. [12]
    J. Butler, E. Cosmos, and P. Cauwenbergs, Positional signals: Evidence for a possible role in muscle fibre-type patterning of the embryonic avian limb, Development, 102 (1988), pp. 763–772.Google Scholar
  13. [13]
    M. Callebaut and E.V. Nueten, Rauber’s (koller’s) sickle: the early gastrulation organizer of the avian blastoderm., Eur. J. Morph., 32 (1994), pp. 35–48.Google Scholar
  14. [14]
    M. Callebaut, E. Van Nueten, F. Harrisson, L. Van Nassauw, A. Schrevens, and H. Bortier, Avian gastrulation and neurulation are not impaired by the removal of the marginal zone at the unincubated blastoderm stage, Eur. J. Morphol., 35 (1997), pp. 69–77.CrossRefGoogle Scholar
  15. [15]
    D. Canning and C. Stern, Changes in the expression of the carbohydrate epitope hnk-1 associated with mesoderm induction in the chick embryo., Development, 104 (1988), pp. 643–655.Google Scholar
  16. [16]
    M. Catala, M.-A. Teillet, and N.M.L. Douarin, Organization and development of the tail bud analyzed with the quail-chick chimera system, Mech. Dev., 51 (1995), pp. 51–65.CrossRefGoogle Scholar
  17. [17]
    K. Chada, J. Magram, and F. Constantini, An embryonic pattern of expression of a human fetal globin gene in transgenic mice, Nature, 319 (1986), pp. 685–689.CrossRefGoogle Scholar
  18. [18]
    E.A.G. Chernoff and S.R. Hilfer, Calcium dependence and contraction in somite formation, Tiss. Cell., 14 (1982), pp. 435–449.CrossRefGoogle Scholar
  19. [19]
    A. Chevallier, Role of the somitic mesoderm in the development of the thorax in bird embryos. II. Origin of thoracic and appendicular musculature, J. Embryol. Exp. Morphol., 49 (1979), pp. 73–88.Google Scholar
  20. [20]
    A. Chevallier, M. Kieny, and A. Mauger, Limb-somite relationship: origin of the limb musculature, Journal of Embryology and Experimental Morphology, 41 (1977), pp. 245–258.Google Scholar
  21. [21]
    —, Limb-somite relationship: Effects of removal of somitic mesoderm on the wing musculature, J. Embryol. Exp. Morph., 43 (1978), pp. 263–278.Google Scholar
  22. [22]
    J. Cooke, A gene that resuscitates a theory — somitogenesis and a molecular oscillator, Trends in Genetics (Personal edition), 14 (1998), pp. 85–88.Google Scholar
  23. [23]
    J. Cooke, S. Takada, and A. Mcmahon, Experimental control of axial pattern in the chick blastoderm by local expression of wnt and activin: the role of hnk-1 positive cells., Dev. Biol., 164 (1994), pp. 513–527.CrossRefGoogle Scholar
  24. [24]
    J. Cooke and E.C. Zeeman, A clock and wavefront model for control of the number of repeated structures during animal morphogenesis, Journal of Theoretical Biology, 58 (1976), pp. 455–476.CrossRefGoogle Scholar
  25. [25]
    I. Del Barco Barrantes, A.J. Ella, K. Wünsch, M.H. De Angelis, T.W. Mak, J. Rossant, R.A. Conlon, A. Gossler, and J.L. De La Pompa, Interaction between notch signalling and lunatic fringe during somite boundary formation in the mouse, Curr. Biol., 9 (1999), pp. 470–480.CrossRefGoogle Scholar
  26. [26]
    J. Duband, S. Dufour, K. Hatta, M. Takeichi, G.M. Edelman, and J.P. Thiery, Adhesion molecules during somitogenesis in the avian embryo, J. Cell Biol., 104 (1987), pp. 1361–1374.CrossRefGoogle Scholar
  27. [27]
    Y. Evrard, Y. Lun, A. Aulehla, L. Gan, and R.L. Johnson, lunatic fringe is an essential mediator of somite segmentation and patterning, Nature, 394 (1998), pp. 377–381.Google Scholar
  28. [28]
    H. Eyal-Giladi, Gradual establishment of cell commitments during the early states of chick development, Cell Differ., 14 (1984), pp. 245–255.CrossRefGoogle Scholar
  29. [29]
    —, Establishment of the axis in chordates: facts and speculations, Development, 124 (1997), pp. 2285–2296.Google Scholar
  30. [30]
    H. Eyal-Giladi and O. Khaner, The chick’s marginal zone and primitive streak formation, Dev. Biol., 134 (1989), pp. 215–221.CrossRefGoogle Scholar
  31. [31]
    H. Eyal-Giladi and S. Kochav, From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. i. general morphology, Dev. Biol., 49 (1976), pp. 321–337.CrossRefGoogle Scholar
  32. [32]
    O.P. Flint, D.A. Ede, O.K. Wilby, and J. Proctor, Control of somite number in normal and Amputated mutant mouse embryos: an experimental and a theoretical analysis, Journal of Embryology and Experimental Morphology, 45 (1978), pp. 189–202.Google Scholar
  33. [33]
    H. Forsberg, F. Crozet, and N.A. Brown, Waves of mouse lunatic fringe expression, in four-hour cycles at two-hour intervals, precede somite boundary formation., Curr. Biol., 8 (1998), pp. 1027–1030.CrossRefGoogle Scholar
  34. [34]
    S.J. Gaunt, Mouse homeobox gene transcripts occupy different but overlapping domains in embryonic germ layers and organs: A comparison of Hox-3.1 and Hox-1.5, Development (Cambridge), 103 (1988), pp. 135–144.Google Scholar
  35. [35]
    S.F. Gilbert, Developmental Biology, Sinauer Associates, fifth ed., 1997.Google Scholar
  36. [36]
    A. Gossler and M. Hrabe De Angelis, Somitogenesis, in Curr. Topics in Dev. Biol., vol. 38, Academic Press, 1998, pp. 225–287. Jackson Laboratory, Bar Harbor, Maine 04609, USA.Google Scholar
  37. [37]
    C. Grabowski, The effects of the excision of hensen’s node on the early development of the chick embryo, J. Exp. Zool., 133 (1956), pp. 301–344.CrossRefGoogle Scholar
  38. [38]
    V. Hamburger and H. Hamilton, A series of normal stages in the development of the chick embryo.Google Scholar
  39. [39]
    Y. Hatada and C.D. Stern, A fate map of the epiblast of the early chick embryo, Development, 120 (1994), pp. 2879–2889.Google Scholar
  40. [40]
    P.W.H. Holland and B.L.M. Hogan, Expression of homeo box genes during development: A review, Genes. Dev., 2 (1988), pp. 773–782.CrossRefGoogle Scholar
  41. [41]
    J. Izpisua-Belmonte, E.D. Robertis, K. Storey, and C. Stern, The homeobox gene goosecoid and the origin of organizer cells in the early chick blastoderm., Cell., 74 (1993), pp. 645–659.CrossRefGoogle Scholar
  42. [42]
    A. Jacobson and S. Meier, Somites in Developing Embryos, vol. 118 of NATO ASI series. Series A, Life sciences, New York: Plenum Press., 1986, ch. Somitomeres: The primordial body segments, pp. 1–16.Google Scholar
  43. [43]
    K. Joubin and C. Stern, Molecular interactions continuously define the organizer during cell movements of gastrulation, Cell, 98 (1999), pp. 559–571.CrossRefGoogle Scholar
  44. [44]
    R. Keller, Vital dye mapping of the gastrula and neurula of xenopus laevis. i. prospective areas and morphogenetic movements of the superficial layer, Dev. Biol., 42 (1975), pp. 222–241.CrossRefGoogle Scholar
  45. [45]
    —, The cellular basis of epiboly: An sem study of deep cell rearrangement during gastrulation in xenopus laevis, J. Embryol. Exp. Morphol., 60 (1980), pp. 201–234.Google Scholar
  46. [46]
    R. Keller, J. Shih, and P. Wilson, Cell Motility, Control, and Function of Convergence and Extension During Gastrulation in Xenopus, in Gastrulation: Movements, Patterns, and Molecules, au]W. C. R. Keller and F. Griffen, eds., Plenum Press, New York, NY, USA; London, UK, 1991.Google Scholar
  47. [47]
    M. Kessel, Respecification of vertebral identities by retinoic acid, Development (Cambridge), 115 (1992), pp. 487–501.Google Scholar
  48. [48]
    M. Kessel and P. Gruss, Homeotic transformations of murine prevertebrae and concomitant alteration of Hox codes induced by retinoic acid, Cell, 67 (1991), pp. 89–104.CrossRefGoogle Scholar
  49. [49]
    R. J. Keynes and C.D. Stern, Mechanisms of vertebrate segmentation, Development (Cambridge), 103 (1988), pp. 413–429.Google Scholar
  50. [50]
    O. Khaner, Axis determination in the avian embryo, Curr. Topics in Dev. Biol., 28 (1993), pp. 155–180.CrossRefGoogle Scholar
  51. [51]
    —, The rotated hypoblast of the chicken embryo does not initiate an ectopic axis in the epiblast, Proc. Nat. Acad. Sci. USA, 92 (1995), pp. 10733–10737.Google Scholar
  52. [52]
    —, The ability to initiate an axis in the avian blastula is concentrated mainly at a posterior site., Dev Biol, 194 (1998), pp. 257–266. Department of Cell and Animal Biology, Hebrew University, Jerusalem, Israel.Google Scholar
  53. [53]
    O. Khaner and H. Eyal-Giladi, The embryo forming potency of the posterior marginal zone in stage x through xii of the chick., Dev. Biol., 115 (1986), pp. 275–281.CrossRefGoogle Scholar
  54. [54]
    —, The chick’s marginal zone and primitive streak formation. I Coordinative effect of induction and inhibition, Developmental Biology, 134 (1989), pp. 206–214.CrossRefGoogle Scholar
  55. [55]
    M. Kieny, A. Mauger, and P. Sengel, Early regionalization of somite mesoderm as studied by the development of axil skeleton of the chick embryo, Dev. Biol., 28 (1972), pp. 142–161.CrossRefGoogle Scholar
  56. [56]
    S. Kochav and H. Eyal-giladi, Bilateral symmetry in chick embryo, determination by gravity, Science, 171 (1971), pp. 1027–1029.CrossRefGoogle Scholar
  57. [57]
    R. Krumlauf, Hox genes in vertebrate development, Cell, 78 (1994), pp. 191–201.CrossRefGoogle Scholar
  58. [58]
    M. Levin, Left-right asymmetry and the chick embryo, Sem. Cell. Dev. Biol., (1998).Google Scholar
  59. [59]
    K. Linask, C. Ludwig, M. D. Hang, X. Liu, and K. K. G. L. Radice, N-Cadherin/Catenin-mediated morphoregulation of somite formation, Dev. Biol., 202 (1998), pp. 85–102.CrossRefGoogle Scholar
  60. [60]
    M. McGrew, J. Dale, S. Fraboulet, and O. Pourquié, The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos, Curr. Biol., 8 (1998), pp. 979–982.CrossRefGoogle Scholar
  61. [61]
    M.J. McGrew and O. Pourquie, Somitogenesis: segmenting a vertebrate, Current opinion in genetics and development, 8 (1998), pp. 487–493.CrossRefGoogle Scholar
  62. [62]
    S. Meier, Development of the chick embryo mesoblast: Formation of the embryonic axis and establishment of the metameric pattern. Dev. Biol., 73 (1979), pp. 24–45.CrossRefGoogle Scholar
  63. [63]
    H. Meinhardt, Models of Biological Pattern Formation, Academic Press, New York, USA, 1982.Google Scholar
  64. [64]
    —, Somites in Developing Embryos, vol. 118 of NATO ASI series. Series A, Life sciences, New York: Plenum Press., 1986, ch. Models of segmentation, pp. 179–189.Google Scholar
  65. [65]
    E. Mitrani and Y. Shimoni, Induction by soluble factors of organized axial structures in chick epiblasts, Science, 247 (1990), pp. 1092–1094.CrossRefGoogle Scholar
  66. [66]
    P. Nieuwkoop, Origin and establishment of embryonic polar axes in amphibian development, Curr. Topics Dev. Biol., 11 (1977), pp. 115–132.CrossRefGoogle Scholar
  67. [67]
    S. Nonaka, Y. Tanaka, Y. Okada, S. Takeda, A. Harada, Y. Kanai, M. Kido, and N. Hirokawa, Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid lacking kifSb motor protein, Cell, 95 (1998), pp. 829–837.CrossRefGoogle Scholar
  68. [68]
    Y. Okada, S. Nonaka, Y. Tanaka, Y. Saijoh, H. Hamada, and N. Hirokawa, Abnormal nodal flow precedes situs inversus in iv and inv mice, Molecular Cell, 4 (1999), pp. 459–468.CrossRefGoogle Scholar
  69. [69]
    D.-J. Packard, R. Zheng, and D.C. Turner, Somite pattern regulation in the avian segmental plate mesoderm, Development, 117 (1993), pp. 779–791.Google Scholar
  70. [70]
    D.S.-J. Packard and A.G. Jacobson, The influence of axial structures on chick somite formation, Dev. Biol., 53 (1976), pp. 36–48.CrossRefGoogle Scholar
  71. [71]
    K.J. Painter, P.K. Maini, and H.G. Othmer, A chemotactic model for the advance and retreat of the primitive streak in avian development, Bull. Math. Biol., 62 (2000). To appear.Google Scholar
  72. [72]
    I. Palmeirim, D. Henrique, D. Ish-Horowicz, and O. Pourquie, Avian hairy gene expression identifies a molecular clock linked to vertbrate segmentation and somitogenesis, Cell, 91 (1997), pp. 639–648.CrossRefGoogle Scholar
  73. [73]
    E. Palsson and H.G. Othmer, A model for individual and collective cell movement in dictyostelium discoideum, Proc. Nat. Acad. Sci, (2000). Submitted.Google Scholar
  74. [74]
    V. Panin, V. Papayannopoulos, R. Wilson, and K.D. Irvine, Fringe modulates notchligand interactions, Nature, 387 (1997), pp. 908–912.CrossRefGoogle Scholar
  75. [75]
    P. Penner and I. Brick, Acetylcholinesterase and polyingression in the epiblast of the primitive streak chick embryo., Roux’s Arch. Dev. Biol., 193 (1984), pp. 234–241.Google Scholar
  76. [76]
    A.A. Polezhaev, A mathematical model of the mechanism of vertebrate somitic segmentation, Journal of Theoretical Biology, (1992).Google Scholar
  77. [77]
    —, Mathematical model of segmentation in somitogenesis in vertebrates, Biophysics, 40 (1995), pp. 583–589.Google Scholar
  78. [78]
    —, Mathematical modelling of the mechanism of vertebrate somitic segmentation, J. Biol. Sys., 3 (1995), pp. 1041–1051.CrossRefGoogle Scholar
  79. [79]
    O. Pourquié, Clocks regulating developmental processes, Curr. Opin. Neurobiol., 8 (1998), pp. 665–670.CrossRefGoogle Scholar
  80. [80]
    O. Pourquié, Notch around the clock, Curr. Opin. Gen. Dev., 9 (1999), pp. 559–565.CrossRefGoogle Scholar
  81. [81]
    D.R.N. Primmett, W.E. Norris, G.J. Carlson, R.J. Keynes, and C.D. Stern, Periodic segmental anomalies induced by heat shock in the chick embryo are associated with the cell cycle, Development (Cambridge), 105 (1989), pp. 119–130.Google Scholar
  82. [82]
    D.R.N. Primmett, C.D. Stern, and R.J. Keynes, Heat shock causes repeated segmental anomalies in the chick embryo, Development (Cambridge), 104 (1988), pp. 331–339.Google Scholar
  83. [83]
    D. Psychoyos and C.D. Stern, Fates and migratory routes of primitive streak cells in the chick embryo. Development (Cambridge), 122 (1996), p. 1523.Google Scholar
  84. [84]
    —, Restoration of the organizer after radical ablation of hensen’s node and the anterior primitive streak in the chick embryo, Development, 122 (1996), pp. 3263–3273.Google Scholar
  85. [85]
    G.L. Radice, H. Rayburn, H. Matsunami, K.A. Knudsen, M. Takeichi, and R.O. Hynes, Developmental defects in mouse embryos lacking n-Cadherin, Dev. Biol., 181 (1997), pp. 64–78.CrossRefGoogle Scholar
  86. [86]
    M.N. Roy, V.E. Prince, and R.K. Ho, Heat shock produces periodic somitic disturbances in the zebrafish embryo, Mech. Dev., 85 (1999), pp. 27–34.CrossRefGoogle Scholar
  87. [87]
    S. Schnell and P.K. Maini, Clock and induction model for somitogenesis, Dev. Dyn., 217 (2000), To appear.Google Scholar
  88. [88]
    G.C. Schoenwolf, Cell movements in the epiblast during gastrulation and neuralation in avian embryoes, in Gastrulation, R. Keller, ed., Plenum Press, New York, NY, USA; London, UK, 1991, pp. 1–28.CrossRefGoogle Scholar
  89. [89]
    M. Selleck and C. Stern, Fate mapping and cell lineage analysis of hensen’s node in the chick embryo, Development, 112 (1991), pp. 615–626.Google Scholar
  90. [90]
    —, Formation and Differentiation of Early Embryonic Mesoderm, Plenum Press, New York, 1992, ch. Evidence for stem cells in the mesoderm of Hensen’s node and their role in embryonic pattern formation, pp. 23–31.CrossRefGoogle Scholar
  91. [91]
    S.B. Shah, I. Skromne, C.R. Hume, D.S. Kessler, K.J. Lee, C.D. Stern, and J. Dodd, Misexpression of chick Vgl in the marginal zone induces primitive streak formation, Development (Cambridge), 124 (1997), pp. 5127–5138. Department of Physiology and Cellular Biophysics, College of Physicians and Surgeons of Columbia University, New York, NY 10032, USA.Google Scholar
  92. [92]
    J.M.W. Slack, From Egg to Embryo. Regional specification in early development, Cambridge: Cambridge University Press, 1991.CrossRefGoogle Scholar
  93. [93]
    N. Spratt, Location of org anspecific regions and their relationship to the development of the primitive streak in the early chick blastoderm, J. Exp. Zool., 89 (1942), pp. 69–101.CrossRefGoogle Scholar
  94. [94]
    —, Regression and shortening of the primitive streak in the explanted chick blastoderm., J. Exp. Zool., 104 (1947), pp. 69–100.CrossRefGoogle Scholar
  95. [95]
    —, Some problems and principles of development, Am. Zool., 6 (1966), pp. 215–254.Google Scholar
  96. [96]
    N. Spratt and H. Haas, Integrative mechanisms in development of the early chick blastoderm. I Regulative potentiality of separate parts, J. Exp. Zool., 145 (1960), pp. 97–137.CrossRefGoogle Scholar
  97. [97]
    C Stern, Gastrulation: Movements, Patterns, and Molecules, Plenum, New York, 1991, ch. Mesodorm formation in the chick embryo revisited., pp. 29–41.Google Scholar
  98. [98]
    C. Stern and D. Canning, Origin of cells giving rise to mesoderm and endoderm in the chick embryo., Nature, 343 (1990), pp. 273–275.CrossRefGoogle Scholar
  99. [99]
    C.D. Stern, The marginal zone and its contribution to the hypoblast and primitive streak of the chick embryo, Development (Cambridge), 109 (1990), p. 667.Google Scholar
  100. [100]
    C.D. Stern and R. Bellairs, Mitotic activity during somite segmentation in the early chick embryo, Anat. Embryol. (Berl.), 169 (1984), pp. 97–102.CrossRefGoogle Scholar
  101. [101]
    C.D. Stern, S.E. Fraser, R.J. Keynes, and D.R.N. Primmett, A cell lineage analysis of segmentation in the chick embryo, Development (Cambridge), 104Supplement (1988), pp. 231–244.Google Scholar
  102. [102]
    A. Streit, K. Lee, I. Woo, C. Roberts, T. Jessell, and C. Stern, Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo, Development, 125 (1998), pp. 507–519.Google Scholar
  103. [103]
    D. Summerbell and M. Maden, Retinole acid, a developmental signalling molecule, Trends in neurosciences (Regular ed.), 13 (1990), pp. 142–147.CrossRefGoogle Scholar
  104. [104]
    P.P.L. Tam and P.A. Trainor, Specification and segmentation of the paraxial mesoderm, Anat. Embryol. (Berl.), 189 (1994), pp. 275–305.CrossRefGoogle Scholar
  105. [105]
    L. Vakaet, Chimeras in Developmental Biology, Academic Press, London, 1984, ch. Early development of birds.Google Scholar
  106. [106]
    M. Veini and R. Bellairs, Somites in Developing Embryos, vol. 118 of NATO ASI series. Series A, Life sciences, New York: Plenum Press., 1986, ch. Heat shock effects in chick embryos, pp. 135–145.Google Scholar
  107. [107]
    F. Wachtlet, B. Christ, and H.J. Jacob, Grafting experiments on determination and migratory behaviour of presomitic, somitic and somatopleural cells in avian embryos, Anat. Embryol. (Berl.), 164 (1982), pp. 369–378.CrossRefGoogle Scholar
  108. [108]
    C. Waddington, Induction by the endodrem in birds., Roux’s Arch. Dev. Biol., 128 (1933), pp. 502–521.Google Scholar
  109. [109]
    Y. Wei and T. Mikawa, Formation of the avian primitive streak from spatially restricted blastoderm: evidence for polarized cell division in the elongating streak, Development, 127 (2000), pp. 87–96.Google Scholar
  110. [110]
    R.G. Weisblat, C.J. Wedeen, and R.G. Kostriken, Evolution of developmental mechanisms: Spatial and temporal modes of rostrocaudal patterning, Curr. Top. Dev. Biol., 29 (1994), pp. 101–134.CrossRefGoogle Scholar
  111. [111]
    O.K. Wilby and D.A. Ede, A model for generating the pattern of cartilage skeletal elements in the embryonic chick limb, Journal of Theoretical Biology, 52 (1975), pp. 199–217.CrossRefGoogle Scholar
  112. [112]
    S. Yuan, D. Darnell, and G. Schoenwolf, Identification of inducing, responding and suppressing regions in an experimental model of notochord formation in avian embryos, Dev. Biol., 172 (1995), pp. 567–584.CrossRefGoogle Scholar
  113. [113]
    —, Mesodermal patterning during avian gastrulation and neurulation: experimental induction of notochord from non-notochordal precursor cells, Dev. Genets., 17 (1995), pp. 38–54.CrossRefGoogle Scholar
  114. [114]
    S. Yuan and G. Schoenwolf, De novo induction of the organizer and formation of the primitive streak in an experimental model of notochord reconstitution in avian embryos, Development, 125 (1998), pp. 201–213.Google Scholar
  115. [115]
    —, Reconstitution of the organizer is both sufficient and required to reestablish a fully patterned body plan in avian embryos, Development, 126 (1999), pp. 2461–22473.Google Scholar
  116. [116]
    Y.P. Yuan, J. Schultz, M. Mlodzik, and P. Bork, Secreted fringe-like signalling molecules may be glycosyl-transferases, Cell, 88 (1997), pp. 9–11.CrossRefGoogle Scholar
  117. [117]
    N. Zhang and T. Gridley, Defect in somite formation in lunatic fringe-deficient mice, Nature, 394 (1998), pp. 374–377.CrossRefGoogle Scholar
  118. [118]
    T. Ziv, Y. Shimoni, and E. Mitrani, Activin can generate ectopic axial structures in chick blastoderm expiants, Development, 115 (1992), pp. 689–694.Google Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • S. Schnell
    • 1
  • K. J. Painter
    • 2
  • P. K. Maini
    • 1
  • H. G. Othmer
    • 2
  1. 1.Centre for Mathematical Biology, Mathematical InstituteOxford UniversityOxfordUK
  2. 2.Department of MathematicsUniversity of MinnesotaMinneapolisUSA

Personalised recommendations