Skip to main content
Log in

Dynamics and mechanisms of posterior axis elongation in the vertebrate embryo

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

During development, the vertebrate embryo undergoes significant morphological changes which lead to its future body form and functioning organs. One of these noticeable changes is the extension of the body shape along the antero-posterior (A–P) axis. This A–P extension, while taking place in multiple embryonic tissues of the vertebrate body, involves the same basic cellular behaviors: cell proliferation, cell migration (of new progenitors from a posterior stem zone), and cell rearrangements. However, the nature and the relative contribution of these different cellular behaviors to A–P extension appear to vary depending upon the tissue in which they take place and on the stage of embryonic development. By focusing on what is known in the neural and mesodermal tissues of the bird embryo, I review the influences of cellular behaviors in posterior tissue extension. In this context, I discuss how changes in distinct cell behaviors can be coordinated at the tissue level (and between tissues) to synergize, build, and elongate the posterior part of the embryonic body. This multi-tissue framework does not only concern axis elongation, as it could also be generalized to morphogenesis of any developing organs.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Keller RE, Danilchik M, Gimlich R, Shih J (1985) The function and mechanism of convergent extension during gastrulation of Xenopus laevis. J Embryol Exp Morphol 89(Suppl):185–209

    PubMed  Google Scholar 

  2. Keller R, Davidson L, Edlund A et al (2000) Mechanisms of convergence and extension by cell intercalation. Philos Trans R Soc Lond B Biol Sci 355:897–922. https://doi.org/10.1098/rstb.2000.0626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Shindo A (2018) Models of convergent extension during morphogenesis. Wiley Interdiscip Rev Dev Biol. https://doi.org/10.1002/wdev.293

    Article  PubMed  Google Scholar 

  4. Beck CW (2015) Development of the vertebrate tailbud. Wiley Interdiscip Rev Dev Biol 4:33–44. https://doi.org/10.1002/wdev.163

    Article  CAS  PubMed  Google Scholar 

  5. Griffith CM, Wiley MJ, Sanders EJ (1992) The vertebrate tail bud: three germ layers from one tissue. Anat Embryol (Berl) 185:101–113

    Article  CAS  Google Scholar 

  6. Takada S, Stark KL, Shea MJ et al (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8:174–189. https://doi.org/10.1101/gad.8.2.174

    Article  CAS  PubMed  Google Scholar 

  7. Bertrand N, Médevielle F, Pituello F (2000) FGF signalling controls the timing of Pax6 activation in the neural tube. Development 127:4837–4843

    CAS  PubMed  Google Scholar 

  8. Diez del Corral R, Olivera-Martinez I, Goriely A et al (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40:65–79

    Article  CAS  Google Scholar 

  9. 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  Google Scholar 

  10. Wilson L, Maden M (2005) The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282:1–13. https://doi.org/10.1016/j.ydbio.2005.02.027

    Article  CAS  PubMed  Google Scholar 

  11. Hubaud A, Pourquié O (2014) Signalling dynamics in vertebrate segmentation. Nat Rev Mol Cell Biol 15:709–721. https://doi.org/10.1038/nrm3891

    Article  CAS  PubMed  Google Scholar 

  12. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92. https://doi.org/10.1002/jmor.1050880104

    Article  CAS  PubMed  Google Scholar 

  13. Patten I, Kulesa P, Shen MM et al (2003) Distinct modes of floor plate induction in the chick embryo. Development 130:4809–4821. https://doi.org/10.1242/dev.00694

    Article  CAS  PubMed  Google Scholar 

  14. Catala M, Teillet MA, De Robertis EM, Le Douarin ML (1996) A spinal cord fate map in the avian embryo: while regressing, Hensen’s node lays down the notochord and floor plate thus joining the spinal cord lateral walls. Development 122:2599–2610

    CAS  PubMed  Google Scholar 

  15. Selleck MA, Stern CD (1991) Fate mapping and cell lineage analysis of Hensen’s node in the chick embryo. Development 112:615–626

    CAS  PubMed  Google Scholar 

  16. Hatada Y, Stern CD (1994) A fate map of the epiblast of the early chick embryo. Development 120:2879–2889

    CAS  PubMed  Google Scholar 

  17. Brown JM, Storey KG (2000) A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal fates. Curr Biol 10:869–872

    Article  CAS  Google Scholar 

  18. Iimura T, Yang X, Weijer CJ, Pourquié O (2007) Dual mode of paraxial mesoderm formation during chick gastrulation. Proc Natl Acad Sci USA 104:2744–2749. https://doi.org/10.1073/pnas.0610997104

    Article  CAS  PubMed  Google Scholar 

  19. Psychoyos D, Stern CD (1996) Fates and migratory routes of primitive streak cells in the chick embryo. Development 122:1523–1534

    CAS  PubMed  Google Scholar 

  20. Catala M, Teillet MA, Le Douarin NM (1995) Organization and development of the tail bud analyzed with the quail-chick chimaera system. Mech Dev 51:51–65

    Article  CAS  Google Scholar 

  21. Cambray N, Wilson V (2007) Two distinct sources for a population of maturing axial progenitors. Development 134:2829–2840. https://doi.org/10.1242/dev.02877

    Article  CAS  PubMed  Google Scholar 

  22. McGrew MJ, Sherman A, Lillico SG et al (2008) Localised axial progenitor cell populations in the avian tail bud are not committed to a posterior Hox identity. Development 135:2289–2299. https://doi.org/10.1242/dev.022020

    Article  CAS  PubMed  Google Scholar 

  23. Knezevic V, De Santo R, Mackem S (1998) Continuing organizer function during chick tail development. Development 125:1791–1801

    CAS  PubMed  Google Scholar 

  24. Iimura T, Pourquié O (2008) Manipulation and electroporation of the avian segmental plate and somites in vitro. Methods Cell Biol 87:257–270. https://doi.org/10.1016/S0091-679X(08)00213-6

    Article  CAS  PubMed  Google Scholar 

  25. Rupp PA, Rongish BJ, Czirok A, Little CD (2003) Culturing of avian embryos for time-lapse imaging. Biotechniques 34:274–278

    Article  CAS  Google Scholar 

  26. Chapman SC, Collignon J, Schoenwolf GC, Lumsden A (2001) Improved method for chick whole-embryo culture using a filter paper carrier. Dev Dyn 220:284–289. https://doi.org/10.1002/1097-0177(20010301)220:3%3c284:AID-DVDY1102%3e3.0.CO;2-5

    Article  CAS  PubMed  Google Scholar 

  27. Yang X, Dormann D, Münsterberg AE, Weijer CJ (2002) Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3:425–437

    Article  CAS  Google Scholar 

  28. Mathis L, Kulesa PM, Fraser SE (2001) FGF receptor signalling is required to maintain neural progenitors during Hensen’s node progression. Nat Cell Biol 3:559–566. https://doi.org/10.1038/35078535

    Article  CAS  PubMed  Google Scholar 

  29. Sweetman D, Wagstaff L, Cooper O et al (2008) The migration of paraxial and lateral plate mesoderm cells emerging from the late primitive streak is controlled by different Wnt signals. BMC Dev Biol 8:63. https://doi.org/10.1186/1471-213X-8-63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ciruna B, Rossant J (2001) FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell 1:37–49. https://doi.org/10.1016/S1534-5807(01)00017-X

    Article  CAS  PubMed  Google Scholar 

  31. Iimura T, Pourquié O (2006) Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 442:568–571. https://doi.org/10.1038/nature04838

    Article  CAS  PubMed  Google Scholar 

  32. Denans N, Iimura T, Pourquié O (2015) Hox genes control vertebrate body elongation by collinear Wnt repression. Elife. https://doi.org/10.7554/eLife.04379

    Article  PubMed  PubMed Central  Google Scholar 

  33. Wacker SA, McNulty CL, Durston AJ (2004) The initiation of Hox gene expression in Xenopus laevis is controlled by Brachyury and BMP-4. Dev Biol 266:123–137. https://doi.org/10.1016/j.ydbio.2003.10.011

    Article  CAS  PubMed  Google Scholar 

  34. Mallo M, Wellik DM, Deschamps J (2010) Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344:7–15. https://doi.org/10.1016/j.ydbio.2010.04.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Deschamps J, Duboule D (2017) Embryonic timing, axial stem cells, chromatin dynamics, and the Hox clock. Genes Dev 31:1406–1416. https://doi.org/10.1101/gad.303123.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Brown JM, Storey KG (2000) A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal fates. Curr Biol 10:869–872

    Article  CAS  Google Scholar 

  37. Martin BL, Kimelman D (2012) Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev Cell 22:223–232. https://doi.org/10.1016/j.devcel.2011.11.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cambray N, Wilson V (2002) Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. Development 129:4855–4866

    CAS  PubMed  Google Scholar 

  39. Tzouanacou E, Wegener A, Wymeersch FJ et al (2009) Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev Cell 17:365–376. https://doi.org/10.1016/j.devcel.2009.08.002

    Article  CAS  PubMed  Google Scholar 

  40. Beddington RS, Rashbass P, Wilson V (1992) Brachyury–a gene affecting mouse gastrulation and early organogenesis. Development 116:157–165

    Google Scholar 

  41. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749–765. https://doi.org/10.1016/S0896-6273(03)00497-5

    Article  CAS  Google Scholar 

  42. Olivera-Martinez I, Harada H, Halley PA, Storey KG (2012) Loss of FGF-dependent mesoderm identity and rise of endogenous retinoid signalling determine cessation of body axis elongation. PLoS Biol 10:e1001415. https://doi.org/10.1371/journal.pbio.1001415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wymeersch FJ, Huang Y, Blin G et al (2016) Position-dependent plasticity of distinct progenitor types in the primitive streak. Elife 5:e10042. https://doi.org/10.7554/eLife.10042

    Article  PubMed  PubMed Central  Google Scholar 

  44. Aires R, Jurberg AD, Leal F et al (2016) Oct4 is a key regulator of vertebrate trunk length diversity. Dev Cell 38:262–274. https://doi.org/10.1016/j.devcel.2016.06.021

    Article  CAS  PubMed  Google Scholar 

  45. Gouti M, Delile J, Stamataki D et al (2017) A gene regulatory network balances neural and mesoderm specification during vertebrate trunk development. Dev Cell 41(243–261):e7. https://doi.org/10.1016/j.devcel.2017.04.002

    Article  CAS  Google Scholar 

  46. Koch F, Scholze M, Wittler L et al (2017) Antagonistic activities of Sox2 and brachyury control the fate choice of neuro-mesodermal progenitors. Dev Cell 42(514–526):e7. https://doi.org/10.1016/j.devcel.2017.07.021

    Article  CAS  Google Scholar 

  47. Amin S, Neijts R, Simmini S et al (2016) Cdx and T brachyury co-activate growth signaling in the embryonic axial progenitor niche. Cell Rep 17:3165–3177. https://doi.org/10.1016/j.celrep.2016.11.069

    Article  CAS  PubMed  Google Scholar 

  48. Oginuma M, Moncuquet P, Xiong F et al (2017) A gradient of glycolytic activity coordinates FGF and Wnt signaling during elongation of the body axis in amniote embryos. Dev Cell 40(342–353):e10. https://doi.org/10.1016/j.devcel.2017.02.001

    Article  CAS  Google Scholar 

  49. Takemoto T, Uchikawa M, Yoshida M et al (2011) Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470:394–398. https://doi.org/10.1038/nature09729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Goto H, Kimmey SC, Row RH et al (2017) FGF and canonical Wnt signaling cooperate to induce paraxial mesoderm from tailbud neuromesodermal progenitors through regulation of a two-step epithelial to mesenchymal transition. Development 144:1412–1424. https://doi.org/10.1242/dev.143578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Akai J, Halley PA, Storey KG (2005) FGF-dependent Notch signaling maintains the spinal cord stem zone. Genes Dev 19:2877–2887. https://doi.org/10.1101/gad.357705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Glickman NS, Kimmel CB, Jones MA, Adams RJ (2003) Shaping the zebrafish notochord. Development 130:873–887

    Article  CAS  Google Scholar 

  53. Keller R, Cooper MS, Danilchik M et al (1989) Cell intercalation during notochord development in Xenopus laevis. J Exp Zool 251:134–154. https://doi.org/10.1002/jez.1402510204

    Article  CAS  PubMed  Google Scholar 

  54. Ellis K, Bagwell J, Bagnat M (2013) Notochord vacuoles are lysosome-related organelles that function in axis and spine morphogenesis. J Cell Biol 200:667–679. https://doi.org/10.1083/jcb.201212095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Adams DS, Keller R, Koehl MA (1990) The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus laevis. Development 110:115–130

    CAS  PubMed  Google Scholar 

  56. Catala M, Teillet MA, Le Douarin NM (1995) Organization and development of the tail bud analyzed with the quail-chick chimaera system. Mech Dev 51:51–65

    Article  CAS  Google Scholar 

  57. Sausedo RA, Schoenwolf GC (1994) Quantitative analyses of cell behaviors underlying notochord formation and extension in mouse embryos. Anat Rec 239:103–112. https://doi.org/10.1002/ar.1092390112

    Article  CAS  PubMed  Google Scholar 

  58. Sausedo RA, Schoenwolf GC (1993) Cell behaviors underlying notochord formation and extension in avian embryos: quantitative and immunocytochemical studies. Anat Rec 237:58–70. https://doi.org/10.1002/ar.1092370107

    Article  CAS  PubMed  Google Scholar 

  59. Schoenwolf GC (2018) Contributions of the chick embryo and experimental embryology to understanding the cellular mechanisms of neurulation. Int J Dev Biol 62:49–55. https://doi.org/10.1387/ijdb.170288gs

    Article  CAS  PubMed  Google Scholar 

  60. Schoenwolf GC (1984) Histological and ultrastructural studies of secondary neurulation in mouse embryos. Am J Anat 169:361–376. https://doi.org/10.1002/aja.1001690402

    Article  CAS  PubMed  Google Scholar 

  61. Schoenwolf GC, Delongo J (1980) Ultrastructure of secondary neurulation in the chick embryo. Am J Anat 158:43–63. https://doi.org/10.1002/aja.1001580106

    Article  CAS  PubMed  Google Scholar 

  62. Dady A, Havis E, Escriou V et al (2014) Junctional neurulation: a unique developmental program shaping a discrete region of the spinal cord highly susceptible to neural tube defects. J Neurosci 34:13208–13221. https://doi.org/10.1523/JNEUROSCI.1850-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Schoenwolf GC (1985) Shaping and bending of the avian neuroepithelium: morphometric analyses. Dev Biol 109:127–139

    Article  CAS  Google Scholar 

  64. Nishimura T, Honda H, Takeichi M (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149:1084–1097. https://doi.org/10.1016/j.cell.2012.04.021

    Article  CAS  PubMed  Google Scholar 

  65. López-Escobar B, Caro-Vega JM, Vijayraghavan DS et al (2018) The non-canonical Wnt-PCP pathway shapes the mouse caudal neural plate. Development. https://doi.org/10.1242/dev.157487

    Article  PubMed  PubMed Central  Google Scholar 

  66. Roszko I, Faure P, Mathis L (2007) Stem cell growth becomes predominant while neural plate progenitor pool decreases during spinal cord elongation. Dev Biol 304:232–245. https://doi.org/10.1016/j.ydbio.2006.12.050

    Article  CAS  PubMed  Google Scholar 

  67. Sausedo RA, Smith JL, Schoenwolf GC (1997) Role of nonrandomly oriented cell division in shaping and bending of the neural plate. J Comp Neurol 381:473–488. https://doi.org/10.1002/(SICI)1096-9861(19970519)381:4%3c473:AID-CNE7%3e3.0.CO;2-%23

    Article  CAS  PubMed  Google Scholar 

  68. Ciruna B, Jenny A, Lee D et al (2006) Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439:220–224. https://doi.org/10.1038/nature04375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Shimokita E, Takahashi Y (2011) Secondary neurulation: fate-mapping and gene manipulation of the neural tube in tail bud. Dev Growth Differ 53:401–410. https://doi.org/10.1111/j.1440-169X.2011.01260.x

    Article  PubMed  Google Scholar 

  70. Le Douarin NM, Teillet MA, Catala M (1998) Neurulation in amniote vertebrates: a novel view deduced from the use of quail-chick chimeras. Int J Dev Biol 42:909–916

    PubMed  Google Scholar 

  71. Chal J, Pourquié O (2009) Patterning and differentiation of the vertebrate spine. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  72. Yin C, Kiskowski M, Pouille P-A et al (2008) Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J Cell Biol 180:221–232. https://doi.org/10.1083/jcb.200704150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Yen WW, Williams M, Periasamy A et al (2009) PTK7 is essential for polarized cell motility and convergent extension during mouse gastrulation. Development 136:2039–2048. https://doi.org/10.1242/dev.030601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Bénazéraf B, Francois P, Baker RE et al (2010) A random cell motility gradient downstream of FGF controls elongation of an amniote embryo. Nature 466:248–252. https://doi.org/10.1038/nature09151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Delfini M-C, Dubrulle J, Malapert P et al (2005) Control of the segmentation process by graded MAPK/ERK activation in the chick embryo. Proc Natl Acad Sci USA 102:11343–11348. https://doi.org/10.1073/pnas.0502933102

    Article  CAS  PubMed  Google Scholar 

  76. Kulesa PM, Fraser SE (2002) Cell dynamics during somite boundary formation revealed by time-lapse analysis. Science 298:991–995. https://doi.org/10.1126/science.1075544

    Article  CAS  PubMed  Google Scholar 

  77. Stern CD, Fraser SE, Keynes RJ, Primmett DR (1988) A cell lineage analysis of segmentation in the chick embryo. Development 104(Suppl):231–244

    PubMed  Google Scholar 

  78. Lawton AK, Nandi A, Stulberg MJ et al (2013) Regulated tissue fluidity steers zebrafish body elongation. Development 140:573–582. https://doi.org/10.1242/dev.090381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Das D, Chatti V, Emonet T, Holley SA (2017) Patterned disordered cell motion ensures vertebral column symmetry. Dev Cell 42(170–180):e5. https://doi.org/10.1016/j.devcel.2017.06.020

    Article  CAS  Google Scholar 

  80. Bénazéraf B, Beaupeux M, Tchernookov M et al (2017) Multi-scale quantification of tissue behavior during amniote embryo axis elongation. Development 144:4462–4472. https://doi.org/10.1242/dev.150557

    Article  CAS  PubMed  Google Scholar 

  81. Wilson PA, Oster G, Keller R (1989) Cell rearrangement and segmentation in Xenopus: direct observation of cultured explants. Development 105:155–166

    CAS  PubMed  Google Scholar 

  82. Steventon B, Duarte F, Lagadec R et al (2016) Species-specific contribution of volumetric growth and tissue convergence to posterior body elongation in vertebrates. Development 143:1732–1741. https://doi.org/10.1242/dev.126375

    Article  CAS  PubMed  Google Scholar 

  83. Huss D, Benazeraf B, Wallingford A et al (2015) A transgenic quail model that enables dynamic imaging of amniote embryogenesis. Development 142:2850–2859. https://doi.org/10.1242/dev.121392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Schoenwolf GC, Yuan S (1995) Experimental analyses of the rearrangement of ectodermal cells during gastrulation and neurulation in avian embryos. Cell Tissue Res 280:243–251

    Article  CAS  Google Scholar 

  85. Smith JL, Schoenwolf GC (1989) Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation. J Exp Zool 250:49–62. https://doi.org/10.1002/jez.1402500107

    Article  CAS  PubMed  Google Scholar 

  86. Psychoyos D, Stern CD (1996) Restoration of the organizer after radical ablation of Hensen’s node and the anterior primitive streak in the chick embryo. Development 122:3263–3273

    CAS  PubMed  Google Scholar 

  87. Charrier J-B, Catala M, Lapointe F et al (2005) Cellular dynamics and molecular control of the development of organizer-derived cells in quail-chick chimeras. Int J Dev Biol 49:181–191. https://doi.org/10.1387/ijdb.041962jc

    Article  CAS  PubMed  Google Scholar 

  88. Charrier JB, Teillet MA, Lapointe F, Le Douarin NM (1999) Defining subregions of Hensen’s node essential for caudalward movement, midline development and cell survival. Development 126:4771–4783

    CAS  PubMed  Google Scholar 

  89. van Nes J, de Graaff W, Lebrin F et al (2006) The Cdx4 mutation affects axial development and reveals an essential role of Cdx genes in the ontogenesis of the placental labyrinth in mice. Development 133:419–428. https://doi.org/10.1242/dev.02216

    Article  CAS  PubMed  Google Scholar 

  90. Takada S, Stark KL, Shea MJ et al (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8:174–189. https://doi.org/10.1101/gad.8.2.174

    Article  CAS  PubMed  Google Scholar 

  91. Herrmann BG, Labeit S, Poustka A et al (1990) Cloning of the T gene required in mesoderm formation in the mouse. Nature 343:617–622. https://doi.org/10.1038/343617a0

    Article  CAS  PubMed  Google Scholar 

  92. Duband JL, Dufour S, Hatta K et al (1987) Adhesion molecules during somitogenesis in the avian embryo. J Cell Biol 104:1361–1374

    Article  CAS  Google Scholar 

  93. Zamir EA, Czirók A, Cui C et al (2006) Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements. Proc Natl Acad Sci USA 103:19806–19811. https://doi.org/10.1073/pnas.0606100103

    Article  CAS  PubMed  Google Scholar 

  94. Filla MB, Czirók A, Zamir EA et al (2004) Dynamic imaging of cell, extracellular matrix, and tissue movements during avian vertebral axis patterning. Birth Defects Res C Embryo Today 72:267–276. https://doi.org/10.1002/bdrc.20020

    Article  CAS  PubMed  Google Scholar 

  95. Czirók A, Rongish BJ, Little CD (2004) Extracellular matrix dynamics during vertebrate axis formation. Dev Biol 268:111–122. https://doi.org/10.1016/j.ydbio.2003.09.040

    Article  CAS  PubMed  Google Scholar 

  96. George EL, Georges-Labouesse EN, Patel-King RS et al (1993) Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119:1079–1091

    CAS  PubMed  Google Scholar 

  97. Yang JT, Rayburn H, Hynes RO (1993) Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 119:1093–1105

    CAS  PubMed  Google Scholar 

  98. Girós A, Grgur K, Gossler A, Costell M (2011) α5β1 integrin-mediated adhesion to fibronectin is required for axis elongation and somitogenesis in mice. PLoS One 6:e22002. https://doi.org/10.1371/journal.pone.0022002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Dray N, Lawton A, Nandi A et al (2013) Cell-fibronectin interactions propel vertebrate trunk elongation via tissue mechanics. Curr Biol 23:1335–1341. https://doi.org/10.1016/j.cub.2013.05.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Serwane F, Mongera A, Rowghanian P et al (2017) In vivo quantification of spatially varying mechanical properties in developing tissues. Nat Methods 14:181–186. https://doi.org/10.1038/nmeth.4101

    Article  CAS  PubMed  Google Scholar 

  101. Agero U, Glazier JA, Hosek M (2010) Bulk elastic properties of chicken embryos during somitogenesis. Biomed Eng Online 9:19. https://doi.org/10.1186/1475-925X-9-19

    Article  PubMed  PubMed Central  Google Scholar 

  102. Zhou J, Kim HY, Davidson LA (2009) Actomyosin stiffens the vertebrate embryo during crucial stages of elongation and neural tube closure. Development 136:677–688. https://doi.org/10.1242/dev.026211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Mongera A, Rowghanian P, Gustafson HJ, et al. (2018) A fluid-to-solid jamming transition underlies vertebrate body axis elongation. Nature. https://doi.org/10.1038/s41586-018-0479-2

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The author thanks Rusty Lansford, David Huss, Cathy Soula, Eric Theveneau, Ben Steventon, Daniela Roellig and Octavian Voiculescu for reading and giving critical comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bertrand Bénazéraf.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bénazéraf, B. Dynamics and mechanisms of posterior axis elongation in the vertebrate embryo. Cell. Mol. Life Sci. 76, 89–98 (2019). https://doi.org/10.1007/s00018-018-2927-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-018-2927-4

Keywords

Navigation