Skip to main content
Springer Nature Link
Log in

Measurement of in vivo Stress Resultants in Neurulation-stage Amphibian Embryos

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

In order to obtain the first quantitative measurements of the in vivo stresses in early-stage amphibian embryos, we developed a novel instrument that uses a pair of parallel wires that are glued to the surface of an embryo normal to the direction in which the stress is to be determined. When a slit is made parallel to the wires and between them, tension in the surrounding tissue causes the slit to open. Under computer control, one of the wires is moved so as to restore the original wire spacing, and the steady-state closure force is determined from the degree of wire flexure. A cell-level finite element model is used to convert the wire bending force to an in-plane stress since the wire force is not proportional to the slit length. The device was used to measure stress resultants (force carried per unit of slit length) on the dorsal, ventral and lateral aspects of neurulation-stage axolotl (Ambystoma mexicanum) embryos. The resultants were anisotropic and varied with location and developmental stage, with values ranging from −0.17 mN/m to 1.92 mN/m. In general, the resultants could be decomposed into patterns associated with internal pressure in the embryo, bending of the embryo along its mid-sagittal plane and neural tube closure. The patterns of stress revealed by the experiments support a number of current theories about the mechanics of neurulation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.

Similar content being viewed by others

References

  1. Adams D. S., R. Keller, M. A. Koehl (1990) The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus Laevis. Dev. Biol. 110:115–130

    CAS  Google Scholar 

  2. Asashima M., G. M. Malacinski, S. C. Smith (1989) Surgical manipulation of embryos. In: J. B. Armstrong, G. M. Malacinski (eds) Developmental Biology of the Axolotl. New York: Oxford University Press. 263–265

    Google Scholar 

  3. Beer F. P., E. R. Johnston, J. T. DeWolf (2005) Mechanics of Materials. New York: McGraw-Hill Science

    Google Scholar 

  4. Belousov L. V., J. G. Dorfman, V. G. Cherdantzev (1975) Mechanical stresses and morphological patterns in amphibian embryos. J. Embryol. Exp. Morphol. 34(3):559–574

    Google Scholar 

  5. Belousov L. V., N. N. Luchinskaia (1995) Mechanically dependent heterotopias of the axial rudiments in clawed toad embryos. Ontogenez 26(3):213–222

    PubMed  CAS  Google Scholar 

  6. Belousov L. V., N. N. Luchinskaia, A. G. Zaraiskii (1999) Tensotaxis-collective movement of embryonic cells up along the gradients of mechanical tensions. Russ. J. Dev. Biol. 30:220–228

    CAS  Google Scholar 

  7. Belousov L. V., S. V. Saveliev, I. I. Naumidi, V. V. Novoselov (1994) Mechanical stresses in embryonic tissues: Patterns, morphogenetic role, and involvement in regulatory feedback. Int. Rev. Cytol. 150:1–34

    Google Scholar 

  8. Bordzilovskaya N. P., T. A. Dettlaff, S. T. Duhon, G. M. Malacinski (1989) Developmental-stage series of exolotl embryos. In: J. B. Armstrong, G. M. Malacinski (eds.) Developmental Biology of the Axolotl. New York: Oxford University Press. 201–219

    Google Scholar 

  9. Brodland G. W. (2006). Do lamellipodia have the mechanical capacity to drive convergent extension? Int. J. Dev. Biol. 50:151–155

    Article  PubMed  CAS  Google Scholar 

  10. Brodland G. W., D. I.-L. Chen, J. H. Veldhuis (2006) A cell-based constitutive model for embryonic epithelia and other planar aggregates of biological cells. Int. J. Plasticity 22:965–995

    Article  Google Scholar 

  11. Brodland G. W., J. H. Veldhuis (2003) A computer model for reshaping of cells in epithelia due to in-plane deformation and annealing. Comput. Methods Biomech. Biomed. Eng. 6(2):89–98

    Article  Google Scholar 

  12. Burnside M. B., A. G. Jacobson (1968) Analysis of morphogenetic movements in the neural plate of the newt Taricha torosa. Dev. Biol. 18:537–552

    Article  PubMed  CAS  Google Scholar 

  13. Clausi D. A., G. W. Brodland (1993) Mechanical evolution of theories of neurulation using computer simulations. Dev. Biol. 118:1013–1023

    Google Scholar 

  14. Chen H. H., G. W. Brodland (2000) Cell-level finite element studies of viscous cells in planar aggregates. ASME J. Biomech. Eng. 122:394–401

    Article  CAS  Google Scholar 

  15. Chen X., G. W. Brodland (2006) The mechanics of early embryo development: Insights from finite element modeling. Solid Mech. Appl. 140: 459–469

    Google Scholar 

  16. Davidson L. A., A. M. Ezin, R. Keller (2002) Embryonic wound healing by apical contraception and ingression in Xenopus laevis. Cell Motil. Cytoskel. 53:163–176

    Article  Google Scholar 

  17. Davidson L. A., G. F. Oster, R. E. Keller, M. A. R. Koehl (1999) Measurements of mechanical properties of the blastula wall reveal which hypothesized mechanisms of primary investigation are physically plausible in the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 209:221–238

    Article  PubMed  CAS  Google Scholar 

  18. Davis G. S. (1984) Migration-directing liquid properties of embryonic amphibian tissues. Am. Zool. 24:649–655

    Google Scholar 

  19. Elul T., R. Keller (2000) Monopolar protrusive activity: A new morphogenetic cell behavior in the neural plate dependent on vertical interactions with the mesoderm in Xenopus. Dev. Biol. 224:3–19

    Article  PubMed  CAS  Google Scholar 

  20. Ermakov A. S., L. V. Belousov (1998) Morphogenetic and differentiation sequelae to relaxation of mechanical tensions in Xenopus laevis blastula. Ontogenez 29(6):450–458

    PubMed  CAS  Google Scholar 

  21. Farge E. (2003) Mechanical induction of twist in the Drosophila Foregut/Stomodeal primodium. Curr. Biol. 13(16):1365–1377

    Article  PubMed  CAS  Google Scholar 

  22. Flugge W. (1973) Stresses in Shells. 2nd ed. Berlin Heidelberg New York: Springer-Verlag

    Google Scholar 

  23. Gilbert, S. F. Developmental Biology. Sinauer Associates Inc., 2003

  24. Hackett D. A., J. L. Smith, G. C. Schoenwolf (1997) Epidermal ectoderm is required for full elevation and for convergence during bending of the avian neural plate. Dev. Dynam. 210:397–406

    Article  CAS  Google Scholar 

  25. Hibbeler R. C. (1993) Statics and Mechanics of Materials. New Jersey: Prentice Hall

    Google Scholar 

  26. Iles, P. J. W., G. W. Brodland, D. A. Clausi, and S. M. Puddister. Estimation of cellular fabric in embryonic epithelia. Comput. Methods Biomech. Biomed. Eng., 2007, in press

  27. Jacobson A. G., R. Gordon (1976) Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. J. Exp. Zool. 197:191–246

    Article  PubMed  CAS  Google Scholar 

  28. Jacobson C. O., A. Jacobson (1973) Studies on morphogenic movements during neural tube closure in amphibia. Zoon 1:17–21

    Google Scholar 

  29. Kamm R. D. (2002) Cellular fluidmechanics. Annu. Rev. Fluid Mech. 34:211–232

    Article  PubMed  Google Scholar 

  30. Karfunkel P. (1974) The mechanisms of neural tube formation. Int. Rev. Cytol. 38:245–271

    Article  PubMed  CAS  Google Scholar 

  31. Keller R. (2004) Heading away from the rump. Nature 430:305–306

    Article  PubMed  CAS  Google Scholar 

  32. Keller R., et al. (2000) Mechanisms of convergence and extension by cell intercalation. Phil. Trans. Roy. Soc. Lond. B 355: 897–922

    Article  CAS  Google Scholar 

  33. Lewis W. H. (1947) Mechanics if invagination. Anat. Rec. 97:139–156

    Article  Google Scholar 

  34. Ninomiya H., R. P. Elinson, R. Winklbauer (2004) Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning. Nature 430:364–367

    Article  PubMed  CAS  Google Scholar 

  35. Taber L. A. (2006) Biophysical mechanisms of cardiac looping. Int. J. Dev. Biol. 50(2–3):323–332

    Article  PubMed  Google Scholar 

  36. Taber L. A., I. E. Lin, E. B. Clark (1995). Mechanics of cardiac looping. Dev. Dynam. 203: 42–50

    CAS  Google Scholar 

  37. Veldhuis J., G. W. Brodland, C. Wiebe, G. Bootsma (2005) Multiview robotic microscope reveals the in-plane kinematics of amphibian neurulation. Ann. Biomed. Eng. 33:821–828

    Article  PubMed  Google Scholar 

  38. Wallingford J. B., S. E. Fraser, R. M. Harland (2002) Convergent extension: The molecular control of polarized cell movement during embryonic development. Dev. Cell 2:695–706

    Article  PubMed  CAS  Google Scholar 

  39. Wang J. H.-C., B. P. Thampatty (2006) An introductory review of cell mechanobiology. Biomech. Model. Mechanobiol. 5:1–16

    Article  PubMed  CAS  Google Scholar 

  40. Wiebe C., G. W. Brodland (2005) Tensile properties of embryonic epithelia measured using a novel instrument. J. Biomech. 38:2087–2094

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Animals were obtained from the Ambystoma Genetic Stock Center at the University of Kentucky and were cared for in accordance with Canadian Council on Animal Care (CCAC) guidelines. Funding was provided by the Canadian Institutes of Health Research (CIHR). Computer simulations were carried out with the assistance of Mr. Jim Veldhuis.

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, University of Waterloo, Waterloo, ON, Canada, N2L 3G1

    Richard Benko & G. Wayne Brodland

Authors
  1. Richard Benko
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. G. Wayne Brodland
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to G. Wayne Brodland.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benko, R., Brodland, G.W. Measurement of in vivo Stress Resultants in Neurulation-stage Amphibian Embryos. Ann Biomed Eng 35, 672–681 (2007). https://doi.org/10.1007/s10439-006-9250-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-006-9250-1

Keywords