The dorsal involuting marginal zone stiffens anisotropically during its convergent extension in the gastrula of Xenopus laevis.

Physically, the course of morphogenesis is determined by the distribution and timing of force production in the embryo and by the mechanical properties of the tissues on which these forces act. We have miniaturized a standard materials-testing procedure (the stress-relaxation test) to measure the viscoelastic properties of the dorsal involuting marginal zone, prechordal mesoderm, and vegetal endoderm of Xenopus laevis embryos during gastrulation. We focused on the involuting marginal zone, because it undergoes convergent extension (an important and wide-spread morphogenetic process) and drives involution, blastopore closure and elongation of the embryonic axis. We show that the involuting marginal zone stiffens during gastrulation, stiffening is a special property of this region rather than a general property of the whole embryo, stiffening is greater along the anteroposterior axis than the mediolateral axis and changes in the cytoskeleton or extracellular matrix are necessary for stiffening, although changes in cell-cell adhesions or cell-matrix adhesions are not ruled out. These findings provide a baseline of data on which future experiments can be designed and make specific, testable predictions about the roles of the cytoskeleton, extracellular matrix and intercellular adhesion in convergent extension, as well as predictions about the morphogenetic role of convergent extension in early development.

[1]  R. Keller,et al.  Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis. , 1988, Development.

[2]  Stephen A. Wainwright,et al.  Mechanical Design in Organisms , 2020 .

[3]  J. Trinkaus,et al.  On the convergent cell movements of gastrulation in Fundulus. , 1992, The Journal of experimental zoology.

[4]  S. Vogel Life in Moving Fluids: The Physical Biology of Flow , 1981 .

[5]  G. Oster,et al.  How do sea urchins invaginate? Using biomechanics to distinguish between mechanisms of primary invagination. , 1995, Development.

[6]  J. Shih,et al.  The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser. , 1992, Development (Cambridge, England). Supplement.

[7]  D. DeSimone,et al.  Role of the extracellular matrix in amphibian gastrulation. , 1992, Current topics in developmental biology.

[8]  G. Oster,et al.  Notochord morphogenesis in Xenopus laevis: simulation of cell behavior underlying tissue convergence and extension. , 1991, Development.

[9]  D. M. Miyamoto,et al.  Formation of the notochord in living ascidian embryos. , 1985, Journal of embryology and experimental morphology.

[10]  R. Keller Chapter 5 Early Embryonic Development of Xenopus laevis , 1991 .

[11]  C. Kintner,et al.  The effects of N-cadherin misexpression on morphogenesis in xenopus embryos , 1990, Neuron.

[12]  R. Winklbauer,et al.  Mesoderm Cell Migration in the Xenopus Gastrula , 1991 .

[13]  R. Keller,et al.  The cellular basis of amphibian gastrulation. , 1986, Developmental biology.

[14]  J. Shih,et al.  Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. , 1992, Development.

[15]  D. Fristrom,et al.  Apical cell shape changes during Drosophila imaginal leg disc elongation: a novel morphogenetic mechanism. , 1991, Development.

[16]  G. Oster,et al.  The mechanical basis of cell rearrangement. I. Epithelial morphogenesis during Fundulus epiboly. , 1990, Development.

[17]  J. Gurdon,et al.  Normal table of Xenopus laevis (Daudin) , 1995 .

[18]  M. Takeichi,et al.  Ectopic expression of N-cadherin perturbs histogenesis in Xenopus embryos. , 1990, Development.

[19]  C. Kimmel,et al.  Cell movements during epiboly and gastrulation in zebrafish. , 1990, Development.

[20]  R. Keller,et al.  Induction of neuronal differentiation by planar signals in Xenopus embryos , 1993, Developmental dynamics : an official publication of the American Association of Anatomists.

[21]  Steven M. Block,et al.  Force and velocity measured for single kinesin molecules , 1994, Cell.

[22]  H. Spemann Embryonic development and induction , 1938 .

[23]  Steven Vogel,et al.  Life's Devices: The Physical World of Animals and Plants , 1988 .

[24]  C. Ettensohn,et al.  Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. , 1985, Developmental biology.

[25]  E. J. Ambrose,et al.  CELL MOVEMENTS. , 1965, Endeavour.

[26]  I. Álvarez,et al.  Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. , 1989, Development.

[27]  N. Akkas Biomechanics of Cell Division , 1987, Nato ASI Series.

[28]  D. Ransom,et al.  Integrin Expression in Early Amphibian Embryos: cDNA Cloning and Characterization of Xenopus β1, β2, β3, and β6 Subunits , 1993 .

[29]  R. Keller,et al.  Vital Dye Mapping of the Gastrula and Neurula of Xenopus Laevis , 1975 .

[30]  R. Keller,et al.  Xenopus gastrulation without a blastocoel roof , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[31]  Toshio Yanagida,et al.  Sub-piconewton force fluctuations of actomyosin in vitro , 1991, Nature.

[32]  M. Huggins Viscoelastic Properties of Polymers. , 1961 .

[33]  R. Keller Early embryonic development of Xenopus laevis. , 1991, Methods in cell biology.

[34]  G. Schoenwolf,et al.  Mechanisms of neurulation: traditional viewpoint and recent advances. , 1990, Development.

[35]  C. Kintner Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain , 1992, Cell.

[36]  J. Mittenthal,et al.  The Mechanics of Morphogenesis in Multicellular Embryos , 1990 .

[37]  Louis Y. Cheng,et al.  The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation , 1986 .

[38]  S.W. Moore A fiber optic system for measuring dynamic mechanical properties of embryonic tissues , 1994, IEEE Transactions on Biomedical Engineering.

[39]  J. Spudich,et al.  Single myosin molecule mechanics: piconewton forces and nanometre steps , 1994, Nature.

[40]  B. Kay,et al.  Xenopus laevis : practical uses in cell and molecular biology , 1991 .

[41]  K D Irvine,et al.  Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. , 1994, Development.

[42]  J. Shih,et al.  Cell motility driving mediolateral intercalation in explants of Xenopus laevis. , 1992, Development.

[43]  M. Guille Methods in cell biology vol. 36. Xenopus laevis: Practical uses in cell and molecular biology : edited by Brian K. Kay and H. Benjamin Peng, Academic Press; San Diego, 1991; xxii + 718 pages. £58.00, $115.00. ISBN 0-12-564136-2 , 1993 .

[44]  P. Alberch,et al.  The mechanical basis of morphogenesis. I. Epithelial folding and invagination. , 1981, Developmental biology.

[45]  Carmen R. Domingo,et al.  Pintallavis, a gene expressed in the organizer and midline cells of frog embryos: involvement in the development of the neural axis. , 1992 .

[46]  J. Shih,et al.  Cell Motility, Control and Function of Convergence and Extension during Gastrulation in Xenopus , 1991 .

[47]  R. Keller,et al.  Vital dye mapping of the gastrula and neurula of Xenopus laevis: I. Prospective areas and morphogenetic movements of the superficial layer , 1976 .

[48]  N. Akkas Biomechanics of Active Movement and Deformation of Cells , 1990, NATO ASI Series.

[49]  J. Gerhart,et al.  Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage. , 1980, Developmental biology.