Abstract
The biological tissues of a developing organism are built and reshaped by intra-embryonic forces. Such morphogenetic forces can be assessed and measured similarly to residual stresses. We will discuss in vivo measurements of morphogenetic stress using two quantitative laser-microsurgery techniques. The first uses a laser to drill a sub-cellular hole in a sheet of epithelial cells. The subsequent dynamic retraction of surrounding cells allows one to infer the local mechanical stress. The second uses a laser to isolate a single cell from the rest of a cell sheet. Isolation is accomplished on a microsecond time scale by holographically shaping a single laser pulse. The subsequent retraction (or expansion) of the isolated cell allows one to separate and quantify the effects of cell-internal and cell-external stresses in the determination of cell shape. Both types of experiment are strongly supported by cell-level finite element models. We will discuss application of these techniques and models to the time-dependent biomechanics of epithelial tissues during early fruit fly embryogenesis – specifically during the processes of germband retraction and dorsal closure.
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Refernces
Schajer GS (1988) Measurement of non-uniform residual stresses using the hole-drilling method. J Eng Mater Technol Trans ASME 110:338–343
ASTM (2008) Standard test method for determining residual stresses by the hole-drilling strain-gage method. ASTM Standard E837-08
Ma X, Lynch HE, Scully PC, Hutson MS (2009) Probing embryonic tissue mechanics with laser hole-drilling. Phys Biol 6:036004
Yeung T, Georges PC, Flanagan LA, Marq B, Ortiz M, Funaki M, Zahir N, Ming W, Weaver V, Janmey PA (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure and adhesion. Cell Motil Cytoskeleton 60:24–34
Hutson MS, Tokutake Y, Chang MS, Bloor JW, Venakides S, Kiehart DP, Edwards GS (2003) Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300:145–149
Hutson MS, Ma X (2007) Plasma and cavitation dynamics during pulsed laser microsurgery in vivo. Phys Rev Lett 99:158104
Hutson MS, Veldhuis J, Ma X, Lynch HE, Cranston PG, Brodland GW (2009) Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics. Biophys J 97:3075–3085
Jayasinghe AK, Rohner J, Hutson MS (2011) Holographic UV laser microsurgery. Biomed Opt Expr 2:2590–2599
Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471–490
Solon J, Kaya-Çopur A, Colombelli J, Brunner D (2009) Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137:1331–1342
Rauzi M, Verant P, Lecuit T, Lenne PF (2008) Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol 10:1401–1410
Fernandez-Gonzalez R, Simoes Sde M, Roper JC, Eaton S, Zallen JA (2009) Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 17:736–743
Fernandez-Gonzalez R, Zallen JA (2011) Oscillatory behaviors and hierarchical assembly of contractile structures in intercalating cells. Phys Biol 8:045005
Lecuit T, Lenne PF (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8:633–644
Azevedo D, Antunes M, Prag S, Ma X, Hacker U, Brodland GW, Hutson MS, Solon J, Jacinto A (2011) DRhoGEF2 regulates cellular tension and cell pulsations in the amnioserosa during Drosophila dorsal closure. PLoS One 6:e23964
Bownes M (1975) A photographic study of development in the living embryo of Drosophila melanogaster. J Embryol Exp Morphol 33:789–801
Kiehart DP, Tokutake Y, Chang M-S, Hutson MS, Wiemann JM, Peralta XG, Toyama Y, Wells AR, Rodriguez A, Edwards GS (2006) Ultraviolet laser microbeam for dissection of Drosophila embryos. In: Celis JE (ed) Cell biology: a laboratory handbook, vol 3. Academic, New York, pp 87–103
Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin
Bement WM, Forscher P, Mooseker MS (1993) A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J Cell Biol 121:565–578
Kiehart DP (1999) Wound healing: the power of the purse string. Curr Biol 9:R602–R605
Chen HH, Brodland GW (2000) Cell-level finite element studies of viscous cells in planar aggregates. J Biomech Eng 122:394–401
Brodland GW, Viens D, Veldhuis JH (2007) A new cell-based FE model for the mechanics of embryonic epithelia. Comput Methods Biomech Biomed Engin 10:121–128
Brodland GW, Clausi DA (1995) Cytoskeletal mechanics of neurulation: Insights obtained from computer simulations. Biochem Cell Biol Biochimie Et Biol Cell 73:545–553
Chen X, Brodland GW (2008) Multi-scale finite element modeling allows the mechanics of amphibian neurulation to be elucidated. Phys Biol 5:15
Hiramoto O (1969) Mechanical properties of the protoplasm of the sea urchin egg. Exp Cell Res 56:201–208
Gerchberg RW, Saxton WO (1972) Practical algorithm for determination of phase from image and diffraction plane pictures. Optik 35:237–246
Blanchard GB, Murugesu S, Adams RJ, Martinez-Arias A, Gorfinkiel N (2010) Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137:2743–2752
Jayasinghe AK, Crews SM, Mashburn DN, Hutson MS (2013) Apical oscillations in amnioserosa cells couple to basolateral dynamics and are cell autonomous. Biophys J. http://dx.doi.org/10.1016/j.bpj.2013.05.027
Peralta XG, Toyama Y, Tokutake Y, Hutson MS, Venakides S, Kiehart DP, Edwards GS (2007) Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys J 92:2583–2596
Acknowledgements
This work supported by the National Science Foundation (IOB-0545679), the Human Frontier Science Program (RGP0021/2007C), the National Institutes of Health (1R01GM099107), the Natural Sciences and Engineering Research Council of Canada (NSERC).
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Hutson, M.S., Brodland, G.W., Ma, X., Lynch, H.E., Jayasinghe, A.K., Veldhuis, J. (2014). Measuring and Modeling Morphogenetic Stress in Developing Embryos. In: Barthelat, F., Zavattieri, P., Korach, C., Prorok, B., Grande-Allen, K. (eds) Mechanics of Biological Systems and Materials, Volume 4. Conference Proceedings of the Society for Experimental Mechanics Series. Springer, Cham. https://doi.org/10.1007/978-3-319-00777-9_15
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