Cell motility driving mediolateral intercalation in explants of Xenopus laevis.

In Xenopus, convergence and extension are produced by active intercalation of the deep mesodermal cells between one another along the mediolateral axis (mediolateral cell intercalation), to form a narrower, longer array. The cell motility driving this intercalation is poorly understood. A companion paper shows that the endodermal epithelium organizes the outermost mesodermal cells immediately beneath it to undergo convergence and extension, and other evidence suggests that these deep cells are the most active participants in mediolateral intercalation (Shih, J. and Keller, R. (1992) Development 116, 887-899). In this paper, we shave off the deeper layers of mesodermal cells, which allows us to observe the protrusive activity of the mesodermal cells next to the organizing epithelium with high resolution video microscopy. These mesodermal cells divide in the early gastrula and show rapid, randomly directed protrusive activity. At the early midgastrula stage, they begin to express a characteristic sequence of behaviors, called mediolateral intercalation behavior (MIB): (1) large, stable, filiform and lamelliform protrusions form in the lateral and medial directions, thus making the cells bipolar; (2) these protrusions are applied directly to adjacent cell surfaces and exert traction on them, without contact inhibition; (3) as a result, the cells elongate and align parallel to the mediolateral axis and perpendicular to the axis of extension; (4) the elongate, aligned cells intercalate between one another along the mediolateral axis, thus producing a longer, narrower array. Explants of essentially a single layer of deep mesodermal cells, made at stage 10.5, converge and extend by mediolateral intercalation. Thus by stage 10.5 (early midgastrula), expression of MIB among deep mesodermal cells is physiologically and mechanically independent of the organizing influence of the endodermal epithelium, described previously (Shih, J. and Keller, R. (1992) Development 116 887-899), and is the fundamental cell motility underlying mediolateral intercalation and convergence and extension of the body axis.

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

[2]  R. W. Morgan,et al.  Changes in the cell cycle during early amphibian development , 1966 .

[3]  J. Cooke Properties of the primary organization field in the embryo of Xenopus laevis. IV. Pattern formation and regulation following early inhibition of mitosis. , 1973, Journal of embryology and experimental morphology.

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

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

[6]  N. Nakatsuji,et al.  Conditioning of a culture substratum by the ectodermal layer promotes attachment and oriented locomotion by amphibian gastrula mesodermal cells. , 1983, Journal of cell science.

[7]  R. Keller Cell rearrangement in morphogenesis , 1987 .

[8]  L. Browder,et al.  Developmental biology : a comprehensive synthesis , 1985 .

[9]  P. Tibbetts,et al.  Mediolateral cell intercalation in the dorsal, axial mesoderm of Xenopus laevis. , 1989, Developmental biology.

[10]  J. Shih,et al.  The epithelium of the dorsal marginal zone of Xenopus has organizer properties. , 1992, Development.

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

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

[13]  J. Brockes,et al.  Monoclonal antibodies identify blastemal cells derived from dedifferentiating muscle in newt limb regeneration , 1984, Nature.

[14]  R. Winklbauer Mesodermal cell migration during Xenopus gastrulation. , 1990, Developmental biology.

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

[16]  R. Keller,et al.  The Cellular Basis of Gastrulation in Xenopus laevis: Active, Postinvolution Convergence and Extension by Mediolateral Interdigitation , 1984 .

[17]  B. B. Mishell,et al.  Selected Methods in Cellular Immunology , 1980 .

[18]  V. Foe,et al.  Mitotic domains reveal early commitment of cells in Drosophila embryos. , 1989, Development.

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

[20]  J. Holtfreter A study of the mechanics of gastrulation , 1944 .

[21]  J. Gerhart Cell-cell interactions in early development , 1991 .

[22]  N. Nakatsuji,et al.  Cell locomotion in vitro by Xenopus laevis gastrula mesodermal cells. , 1982, Cell motility.

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

[24]  R. Keller,et al.  The cellular basis of epiboly: an SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis. , 1980, Journal of embryology and experimental morphology.

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

[26]  J Hardin,et al.  Cell Behaviour During Active Cell Rearrangement: Evidence and Speculations , 1987, Journal of Cell Science.

[27]  N. Satoh ‘METACHRONOUS’ CLEAVAGE AND INITIATION OF GASTRULATION IN AMPHIBIAN EMBRYOS , 1977, Development, growth & differentiation.

[28]  R. Keller,et al.  Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants. , 1991, Development.

[29]  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 .

[30]  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 .

[31]  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 .

[32]  G. Oster,et al.  Cell rearrangement and segmentation in Xenopus: direct observation of cultured explants. , 1989, Development.

[33]  A G Jacobson,et al.  Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. , 1976, The Journal of experimental zoology.

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

[35]  J. Shih,et al.  Planar induction of convergence and extension of the neural plate by the organizer of Xenopus , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

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

[37]  R. Winklbauer,et al.  Directional mesoderm cell migration in the Xenopus gastrula. , 1991, Developmental biology.

[38]  L. Browder The Cellular Basis of Morphogenesis , 1986, Developmental Biology.

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

[40]  A. Wood,et al.  Analysis of In Vivo Cell Movement Using Transparent Tissue Systems , 1987, Journal of Cell Science.

[41]  S. Maruyama,et al.  Structure and developmental tendency of the dorsal marginal zone in the early amphibian gastrula. , 1971, Journal of embryology and experimental morphology.

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

[43]  J. Trinkaus,et al.  In vivo Analysis of Convergent Cell Movements in The Germ Ring of Fundulus , 1991 .

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

[45]  J. Shih,et al.  The cellular basis of the convergence and extension of the Xenopus neural plate , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[46]  M. S. Cooper,et al.  Cell intercalation during notochord development in Xenopus laevis. , 1989, The Journal of experimental zoology.

[47]  J. Braun,et al.  Improved fluorescent compounds for tracing cell lineage. , 1985, Developmental biology.

[48]  G. Odell,et al.  Neurulation and the cortical tractor model for epithelial folding. , 1986, Journal of embryology and experimental morphology.

[49]  R. R. Bensley,et al.  Embryonic Development and Induction , 1938, The Yale Journal of Biology and Medicine.

[50]  J. Holtfreter A study of the mechanics of gastrulation. Part I , 1943 .

[51]  T. Dettlaff CELL DIVISIONS, DURATION OF INTERKINETIC STATES AND DIFFERENTIATION IN EARLY STAGES OF EMBRYONIC DEVELOPMENT. , 1964, Advances in morphogenesis.