Reorganization of cytoplasm in the zebrafish oocyte and egg during early steps of ooplasmic segregation

The aim of this work is to determine when and how ooplasmic segregation is initiated in the zebrafish egg. To this end, the organization of the ooplasm and vitelloplasm were examined in oocytes and eggs shortly after activation. Ooplasmic segregation, initiated in the stage V oocyte, led to the formation of ooplasmic domains rich in organelles, and ribonucleoproteins. A linear array of closely arranged peripheral yolk globules separated an outer domain of ectoplasm from an inner domain of interconnected endoplasmic lacunae. The structure of this yolk array and the distribution of microinjected labeled tracers suggests that it may provide a barrier limiting ooplasm transit. Loosely arranged yolk globules at the animal hemisphere allow wide connections between the endoplasm and a preblastodisc domain. Activation caused further segregation of ooplasm, reorganization of endoplasmic lacunae, and blastodisc growth. The presence of an endoplasmic cytoskeleton suggests that these changes may be driven by microtubules and microfilaments. Developmental Dynamics 235:656–671, 2006. © 2006 Wiley‐Liss, Inc.

[1]  Juan Fernández,et al.  Confocal and video imaging of cytoskeleton dynamics in the leech zygote. , 2004, Developmental biology.

[2]  J. Fernández,et al.  Formation of polar cytoplasmic domains (teloplasms) in the leech egg is a three-step segregation process. , 1998, The International journal of developmental biology.

[3]  R. Ho,et al.  mRNA localization patterns in zebrafish oocytes , 2000, Mechanisms of Development.

[4]  A. Gore,et al.  Localization of transcripts of the Zebrafish morphogen Squint is dependent on egg activation and the microtubule cytoskeleton , 2002, Mechanisms of Development.

[5]  N. Hart,et al.  Scanning electron microscope studies of sperm incorporation into the zebrafish (Brachydanio) egg. , 1987, The Journal of experimental zoology.

[6]  T. Sugiyama,et al.  Vegetal localization of the maternal mRNA encoding an EDEN-BP/Bruno-like protein in zebrafish , 2000, Mechanisms of Development.

[7]  N. Hart,et al.  Cytoskeleton in teleost eggs and early embryos: contributions to cytoarchitecture and motile events. , 1995, Current topics in developmental biology.

[8]  K. K. Hisaoka,et al.  The normal developmental stages of the zebrafish, brachydanio rerio (hamilton‐buchanan) , 1958 .

[9]  A. Hyman,et al.  Preparation of modified tubulins. , 1991, Methods in enzymology.

[10]  R. Wallace,et al.  Stages of oocyte development in the zebrafish, Brachydanio rerio , 1993, Journal of morphology.

[11]  C. Devillers.  Structural and Dynamic Aspects of the Development of the Teleostean Egg , 1961 .

[12]  J. Oppenheimer.  The development of isolated blastoderms of Fundulus heteroclitus , 1936 .

[13]  N. Hart,et al.  Cortical granule exocytosis and cell surface reorganization in eggs of Brachydanio. , 1980, The Journal of experimental zoology.

[14]  W. Han,et al.  In vitro oocyte maturation in the zebra fish, Brachydanio rerio, and the fertilization and development of the mature egg. , 1993, Chinese journal of biotechnology.

[15]  Uwe Strähle,et al.  Dynamic microtubules and specification of the zebrafish embryonic axis , 1997, Current Biology.

[16]  Robert C. Schirone,et al.  Effect of temperature on early embryological development of the zebra fish, Brachydanio rerio† , 1968 .

[17]  V V Ivanenkov,et al.  Surface polarization in loach eggs and two-cell embryos: correlations between surface relief, endocytosis and cortex contractility. , 1990, The International journal of developmental biology.

[18]  Andrew L. Miller,et al.  A wave of free cytosolic calcium traverses zebrafish eggs on activation. , 1999, Developmental biology.

[19]  S. Webb,et al.  Calcium transients accompany ooplasmic segregation in zebrafish embryos , 1998, Development, growth & differentiation.

[20]  B. Bowerman.  Maternal Control of Polarity and Patterning during Embryogenesis in the Nematode Caenorhabditis elegans , 1999 .

[21]  Takashi Shimizu.  Ooplasmic segregation in theTubifex egg: Mode of pole plasm accumulation and possible involvement of microfilaments , 1982, Wilhelm Roux's archives of developmental biology.

[22]  W. Wood,et al.  Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos , 1983, Cell.

[23]  R. Baker,et al.  Ionophore-Induced Calcium Waves Activate Unfertilized Zebrafish (Dank rerio) Eggs. , 1996, The Biological bulletin.

[24]  W. Jeffery,et al.  A yellow crescent cytoskeletal domain in ascidian eggs and its role in early development. , 1983, Developmental biology.

[25]  R. Ho,et al.  Characterization of the zebrafish Orb/CPEB-related RNA-binding protein and localization of maternal components in the zebrafish oocyte , 1998, Mechanisms of Development.

[26]  N. Hart,et al.  The sperm entry site during fertilization of the zebrafish egg: Localization of actin , 1992, Molecular reproduction and development.

[27]  F. Pelegri.  Maternal factors in zebrafish development , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[28]  C. Firlit,et al.  Further studies on the embryonic development of the zebrafish, Brachydanio rerio (Hamilton‐Buchanan) , 1960 .

[29]  Juan Fernández,et al.  Reorganization and translocation of the ectoplasmic cytoskeleton in the leech zygote by condensation of cytasters and interactions of dynamic microtubules and actin filaments. , 2002, Cell motility and the cytoskeleton.

[30]  C. Sardet,et al.  Fertilization and ooplasmic movements in the ascidian egg. , 1989, Development.

[31]  Andrew L. Miller,et al.  On the mechanism of ooplasmic segregation in single‐cell zebrafish embryos , 2000, Development, growth & differentiation.

[32]  J. Fernández.  Embryonic development of the glossiphoniid leech Theromyzon rude: characterization of developmental stages. , 1980, Developmental biology.

[33]  H. Katow.  Obstruction of Blastodisc Formation by Cytochalasin B in the Zebrafish, Brachydanio rerio , 1983, Development, growth & differentiation.

[34]  E. Roosen-Runge.  ON THE EARLY DEVELOPMENT—BIPOLAR DIFFERENTIATION AND CLEAVAGE—OF THE ZEBRA FISH, BRACHYDANIO RERIO , 1938 .

[35]  V. Greenhut,et al.  Observations on the cortical reaction in eggs of Brachydanio rerio as seen with the scanning electron microscope , 1977 .

[36]  H. W. Beams,et al.  Scanning electron microscope studies on blastodisc formation in the zebrafish, Brachydanio rerio , 1985 .

[37]  S Gupta,et al.  Ooplasmic Segregation in the Medaka (Oryzias latipes) Egg. , 1993, The Biological bulletin.

[38]  M. Danilchik,et al.  Deep cytoplasmic rearrangements during early development in Xenopus laevis. , 1991, Development.

[39]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[40]  D. Crisp.  Experimental embryology of marine and fresh-water invertebrates Edited by G. Reverberi. Pp xxiii + 587. North Holland Publishing Company, Amsterdam. 1971. Hfl. 100 , 1972 .

[41]  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.