Deep cytoplasmic rearrangements during early development in Xenopus laevis.

The egg of the frog Xenopus is cylindrically symmetrical about its animal-vegetal axis before fertilization. Midway through the first cell cycle, the yolky subcortical cytoplasm rotates 30 degrees relative to the cortex and plasma membrane, usually toward the side of the sperm entry point. Dorsal embryonic structures always develop on the side away from which the cytoplasm moves. Details of the deep cytoplasmic movements associated with the cortical rotation were studied in eggs vitally stained during oogenesis with a yolk platelet-specific fluorescent dye. During the first cell cycle, eggs labelled in this way develop a complicated swirl of cytoplasm in the animal hemisphere. This pattern is most prominent on the side away from which the vegetal yolk moves, and thus correlates in position with the prospective dorsal side of the embryo. Although the pattern is initially most evident near the egg's equator or marginal zone, extensive rearrangements associated with cleavage furrowing (cytoplasmic ingression) relocate portions of the swirl to vegetal blastomeres on the prospective dorsal side.

[1]  R. Elinson.  The Amphibian Egg Cortex in Fertilization and Early Development , 1980 .

[2]  J. Gerhart,et al.  High-frequency twinning of Xenopus laevis embryos from eggs centrifuged before first cleavage. , 1986, Developmental biology.

[3]  W. W. Ballard.  Cortical ingression during cleavage of Amphibian eggs, studied by means of vital dyes , 1955 .

[4]  H. Kageura,et al.  Pattern regulation in defect embryos of Xenopus laevis. , 1984, Developmental biology.

[5]  M. Kirschner,et al.  Evidence for a functional role of the cytoskeleton in determination of the dorsoventral axis in Xenopus laevis eggs. , 1983, Journal of embryology and experimental morphology.

[6]  J M Slack,et al.  Fate map for the 32-cell stage of Xenopus laevis. , 1987, Development.

[7]  G. Oster,et al.  Kinematics of gray crescent formation in Xenopus eggs: the displacement of subcortical cytoplasm relative to the egg surface. , 1986, Developmental biology.

[8]  P. Grant,et al.  The amphibian gray crescent region--a site of developmental information? , 1972, Developmental biology.

[9]  M. Danilchik,et al.  The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. I. Independence in undisturbed embryos. , 1988, Developmental biology.

[10]  R. Elinson.  Cytoplasmic phases in the first cell cycle of the activated frog egg. , 1983, Developmental biology.

[11]  J. Gerhart,et al.  Spatial and Temporal Changes in the Amphibian Egg , 1981 .

[12]  L. Anderson,et al.  Functional transformations accompanying the initiation of a terminal growth phase in the cecropia moth oocyte. , 1968, Developmental biology.

[13]  P. Nieuwkoop,et al.  Origin and establishment of embryonic polar axes in amphibian development. , 1977, Current topics in developmental biology.

[14]  R. Gimlich.  Acquisition of developmental autonomy in the equatorial region of the Xenopus embryo. , 1986, Developmental biology.

[15]  J. Gerhart,et al.  Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. , 1989, Development.

[16]  J. Gerhart,et al.  Localization and induction in early development of Xenopus. , 1984, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  M. Klymkowsky,et al.  4 – Whole-Mount Analyses of Cytoskeletal Reorganization and Function during Oogenesis and Early Embryogenesis in Xenopus 1 , 1989 .

[18]  J. Gerhart,et al.  The anterior extent of dorsal development of the Xenopus embryonic axis depends on the quantity of organizer in the late blastula. , 1990, Development.

[19]  H. Takasaki,et al.  Dorsal Blastomeres in the Equatorial Region of the 32‐Cell Xenopus Embryo Autonomously Produce Progeny Committed to the Organizer , 1989 .

[20]  J. Gerhart.  Mechanisms Regulating Pattern Formation in the Amphibian Egg and Early Embryo , 1980 .

[21]  K. Kao,et al.  The Location of Dorsal Information in Frog Early Development , 1989, Development, growth & differentiation.

[22]  C. Phillips,et al.  Expression of Epi 1, an epidermis-specific marker in Xenopus laevis embryos, is specified prior to gastrulation. , 1988, Developmental biology.

[23]  G. Malacinski,et al.  Experimental analyses of cytoplasmic rearrangements which follow fertilization and accompany symmetrization of inverted Xenopus eggs. , 1984, Journal of embryology and experimental morphology.

[24]  G. Greenhouse,et al.  Analysis of trypan blue induced teratogenesis in Rana pipiens embryos. , 1968, Teratology.

[25]  T. M. Harris.  PREGASTRULAR MECHANISMS IN THE MORPHOGENESIS OF THE SALAMANDER AMBYSTOMA MACULATUM. , 1964, Developmental biology.

[26]  P. Ancel,et al.  Recherches sur le déterminisme de la symétrie bilatérale dans l'œuf des amphibiens , 1948 .

[27]  R. Elinson.  Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. , 1975, Developmental biology.

[28]  P. Pasceri,et al.  Two UV-sensitive targets in dorsoanterior specification of frog embryos. , 1989, Development.

[29]  B. Rowning,et al.  A transient array of parallel microtubules in frog eggs: potential tracks for a cytoplasmic rotation that specifies the dorso-ventral axis. , 1988, Developmental biology.

[30]  G. Malacinski,et al.  Destruction of components of the neural induction system of the amphibian egg with ultraviolet irradiation. , 1977, Developmental biology.

[31]  M. Wakahara.  Specification and Establishment of Dorsal‐Ventral Polarity in Eggs and Embryos of Xenopus laevis , 1989, Development, growth & differentiation.

[32]  J. Cleine,et al.  The effect of egg rotation on the differentiation of primordial germ cells in Xenopus laevis. , 1985, Journal of embryology and experimental morphology.

[33]  J. Gerhart,et al.  Early cellular interactions promote embryonic axis formation in Xenopus laevis. , 1984, Developmental biology.

[34]  J. J. Pasteels.  THE MORPHOGENETIC ROLE OF THE CORTEX OF THE AMPHIBIAN EGG. , 1964, Advances in morphogenesis.

[35]  J. Gerhart,et al.  Subcortical rotation in Xenopus eggs: an early step in embryonic axis specification. , 1987, Developmental biology.

[36]  J. Gerhart,et al.  Differentiation of the animal-vegetal axis in Xenopus laevis oocytes. I. Polarized intracellular translocation of platelets establishes the yolk gradient. , 1987, Developmental biology.

[37]  J. Gerhart,et al.  Experimental control of the site of embryonic axis formation in Xenopus laevis eggs centrifuged before first cleavage. , 1985, Developmental biology.

[38]  J. Gurdon,et al.  All components required for the eventual activation of muscle-specific actin genes are localized in the subequatorial region of an uncleaved amphibian egg. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Gerhart,et al.  Axis determination in eggs of Xenopus laevis: a critical period before first cleavage, identified by the common effects of cold, pressure and ultraviolet irradiation. , 1983, Developmental biology.

[40]  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.

[41]  Elmer S. West.  From the U. S. A. , 1965 .

[42]  C. Waddington,et al.  Teratogenic Effects of Trypan Blue on Amphibian Embryos , 1956 .

[43]  P. Cardellini.  Reversal of dorsoventral polarity in Xenopus laevis embryos by 180° rotation of the animal micromeres at the eight-cell stage , 1988 .

[44]  J. Dumont.  Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals , 1972, Journal of morphology.

[45]  J. Gerhart,et al.  Amphibian Early DevelopmentResearch supports a stepwise view of amphibian development in which each stage builds on the previous one , 1986 .

[46]  M. Wakahara.  Modification of Dorsal‐Ventral Polarity in Xenopus laevis Embryos Following Withdrawal of Egg Contents before First Cleavage , 1986, Development, growth & differentiation.

[47]  Y. Kobayakawa,et al.  A cytoplasmic determinant for dorsal axis formation in an early embryo of Xenopus laevis. , 1990, Development.

[48]  J. Gerhart,et al.  A reinvestigation of the role of the grey crescent in axis formation in Xenopus laevis , 1981, Nature.

[49]  C. Phillips.  Spatial changes in poly(A) concentrations during early embryogenesis in Xenopus laevis: analysis by in situ hybridization. , 1985, Developmental biology.