Localization of germ plasm‐related structures during sea urchin oogenesis

Background: Animal germ cells have specific organelles that are similar to ribonucleoprotein complex, called germ plasm, which is accumulated in eggs. Germ plasm is essential for inherited mechanism of germ line segregation in early embryogenesis. Sea urchins have early germ line segregation in early embryogenesis. Nevertheless, organization of germ plasm‐related organelles and their molecular composition are still unclear. Another issue is whether maternally accumulated germ plasm exists in the sea urchin eggs. Results: I analyzed intracellular localization of germ plasm during oogenesis in sea urchin Strongylocentrotus intermedius by using morphological approach and immunocytochemical detection of Vasa, a germ plasm marker. All ovarian germ cells have germ plasm‐related organelles in the form of germ granules, Balbiani bodies, and perinuclear nuage found previously in germ cells in other animals. Maternal germ plasm is accumulated in late oogenesis at the cell periphery. Cytoskeletal drug treatment showed an association of Vasa‐positive granules with actin filaments in the egg cortex. Conclusions: All female germ cells of sea urchins have germ plasm‐related organelles. Eggs have a maternally accumulated germ plasm associated with cortical cytoskeleton. These findings correlate with early segregation of germ line in sea urchins. Developmental Dynamics 245:56–66, 2016. © 2015 Wiley Periodicals, Inc.

[1]  M. Kloc,et al.  Balbiani body, nuage and sponge bodies--term plasm pathway players. , 2014, Arthropod structure & development.

[2]  G. Wessel,et al.  Piwi regulates Vasa accumulation during embryogenesis in the sea urchin , 2014, Developmental dynamics : an official publication of the American Association of Anatomists.

[3]  C. Extavour,et al.  Identification of a putative germ plasm in the amphipod Parhyale hawaiensis , 2013, EvoDevo.

[4]  A. Wikramanayake,et al.  Differential Regulation of Disheveled in a Novel Vegetal Cortical Domain in Sea Urchin Eggs and Embryos: Implications for the Localized Activation of Canonical Wnt Signaling , 2013, PloS one.

[5]  Zhi‐Feng Zhang,et al.  Gonadogenesis and expression pattern of the vasa gene in the sea cucumber Apostichopus japonicus during early development , 2013, Molecular reproduction and development.

[6]  P. Lasko.  The DEAD-box helicase Vasa: evidence for a multiplicity of functions in RNA processes and developmental biology. , 2013, Biochimica et biophysica acta.

[7]  G. Wessel,et al.  Lessons for inductive germline determination , 2013, Molecular reproduction and development.

[8]  Zhifeng Zhang,et al.  Expression pattern of vasa in gonads of sea cucumber Apostichopus japonicus during gametogenesis and reproductive cycle. , 2013, Gene expression patterns : GEP.

[9]  M. Mochii,et al.  Ectopic formation of primordial germ cells by transplantation of the germ plasm: direct evidence for germ cell determinant in Xenopus. , 2012, Developmental biology.

[10]  G. Wessel,et al.  Autonomy in specification of primordial germ cells and their passive translocation in the sea urchin , 2012, Development.

[11]  K. Mowry,et al.  Principles and roles of mRNA localization in animal development , 2012, Development.

[12]  H. le Guyader,et al.  Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. , 2012, Developmental biology.

[13]  M. Mullins,et al.  Maternal and zygotic control of zebrafish dorsoventral axial patterning. , 2011, Annual review of genetics.

[14]  A. Reunov.  Premeiotic transformation of germ plasm-related structures during the sea urchin spermatogenesis , 2011, Zygote.

[15]  G. Wessel,et al.  The DEAD-box RNA helicase Vasa functions in embryonic mitotic progression in the sea urchin , 2011, Development.

[16]  E. R. Gavis,et al.  Transport of Germ Plasm on Astral Microtubules Directs Germ Cell Development in Drosophila , 2011, Current Biology.

[17]  M. Kloc,et al.  Nuage morphogenesis becomes more complex: two translocation pathways and two forms of nuage coexist in Drosophila germline syncytia , 2011, Cell and Tissue Research.

[18]  O. Serov,et al.  Isolation of oogonia from ovaries of the sea urchin Strongylocentrotus nudus , 2010, Cell and Tissue Research.

[19]  James M Smith,et al.  Germ cell specification and ovary structure in the rotifer Brachionus plicatilis , 2010, EvoDevo.

[20]  A. Ramos,et al.  Building RNA-protein granules: insight from the germline. , 2010, Trends in cell biology.

[21]  Celina E. Juliano,et al.  Nanos functions to maintain the fate of the small micromere lineage in the sea urchin embryo. , 2010, Developmental biology.

[22]  S. Strome,et al.  P granule assembly and function in Caenorhabditis elegans germ cells. , 2010, Journal of andrology.

[23]  Ben Ewen-Campen,et al.  The molecular machinery of germ line specification , 2010, Molecular reproduction and development.

[24]  M. J. Belzunce,et al.  Induction to maturation of the sea urchin Paracentrotus lividus (Lamarck, 1816) under laboratory conditions , 2009, Environmental technology.

[25]  T. Minokawa,et al.  Role of the nanos homolog during sea urchin development , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[26]  Celina E. Juliano,et al.  An evolutionary transition of vasa regulation in echinoderms , 2009, Evolution & development.

[27]  M. Saitou.  Germ cell specification in mice. , 2009, Current opinion in genetics & development.

[28]  N. Nakatsuji,et al.  Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: Germinal granules in mammals , 2009, Molecular and Cellular Endocrinology.

[29]  Isabelle S. Peter,et al.  Genomic control of patterning. , 2009, The International journal of developmental biology.

[30]  D. McClay,et al.  Vasa protein expression is restricted to the small micromeres of the sea urchin, but is inducible in other lineages early in development. , 2008, Developmental biology.

[31]  C. Extavour.  Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. , 2007, Integrative and comparative biology.

[32]  M. Dougherty,et al.  Organization of cytokeratin cytoskeleton and germ plasm in the vegetal cortex of Xenopus laevis oocytes depends on coding and non-coding RNAs: three-dimensional and ultrastructural analysis. , 2007, Experimental cell research.

[33]  K. Kawakami,et al.  Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis , 2007, Mechanisms of Development.

[34]  A. Spradling,et al.  Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body , 2007, Proceedings of the National Academy of Sciences.

[35]  A. Egaña,et al.  Strongylocentrotus drobachiensis oocytes maintain a microtubule organizing center throughout oogenesis: Implications for the establishment of egg polarity in sea urchins , 2007, Molecular reproduction and development.

[36]  Celina E. Juliano,et al.  Germ line determinants are not localized early in sea urchin development, but do accumulate in the small micromere lineage. , 2006, Developmental biology.

[37]  C. Ettensohn.  The Emergence of Pattern in Embryogenesis: Regulation of β-Catenin Localization During Early Sea Urchin Development , 2006, Science's STKE.

[38]  M. Lesser,et al.  Nutritive Phagocyte Incubation Chambers Provide a Structural and Nutritive Microenvironment for Germ Cells of Strongylocentrotus droebachiensis, the Green Sea Urchin , 2005, The Biological Bulletin.

[39]  K. Suprenant,et al.  Seawi--a sea urchin piwi/argonaute family member is a component of MT-RNP complexes. , 2005, RNA.

[40]  C. Sardet,et al.  Maternal determinants and mRNAs in the cortex of ascidian oocytes, zygotes and embryos , 2005, Biology of the cell.

[41]  Andrew D. Johnson,et al.  Gene expression in the axolotl germ line: Axdazl, Axvh, Axoct‐4, and Axkit , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[42]  P. Macdonald,et al.  Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components , 2004, Journal of Cell Science.

[43]  M. Akam,et al.  Mechanisms of germ cell specification across the metazoans: epigenesis and preformation , 2003, Development.

[44]  A. Spradling,et al.  A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis , 2003, Development.

[45]  W. Theurkauf,et al.  Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior , 2002, Nature Cell Biology.

[46]  C. Nüsslein-Volhard,et al.  Zebrafish vasa RNA but Not Its Protein Is a Component of the Germ Plasm and Segregates Asymmetrically before Germline Specification , 2000, The Journal of cell biology.

[47]  Y. Matsui,et al.  Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development , 2000, Mechanisms of Development.

[48]  S. Strome,et al.  Launching the germline in Caenorhabditis elegans: regulation of gene expression in early germ cells. , 1999, Development.

[49]  K. Miller,et al.  The actin cytoskeleton is required for maintenance of posterior pole plasm components in the Drosophila embryo , 1999, Mechanisms of Development.

[50]  D. McClay,et al.  Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. , 1999, Development.

[51]  N. Hopkins,et al.  Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. , 1997, Development.

[52]  C. Wylie,et al.  A Kinesin-like Protein Is Required for Germ Plasm Aggregation in Xenopus , 1996, Cell.

[53]  E. Davidson,et al.  Postembryonic segregation of the germ line in sea urchins in relation to indirect development. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[54]  E. Bonder,et al.  Sea urchin egg 100-kDa dynamin-related protein: identification of and localization to intracellular vesicles. , 1993, Developmental Biology.

[55]  S. Smiley.  The Dynamics of Oogenesis and the Annual Ovarian Cycle of Stichopus californicus (Echinodermata: Holothuroidea) , 1988 .

[56]  K. E. Dixon,et al.  Relocation and reorganization of germ plasm in Xenopus embryos after fertilization. , 1988, Development.

[57]  J. Henson,et al.  Filamentous actin organization in the unfertilized sea urchin egg cortex. , 1988, Developmental biology.

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

[59]  G. Schatten,et al.  Taxol inhibits the nuclear movements during fertilization and induces asters in unfertilized sea urchin eggs , 1982, The Journal of cell biology.

[60]  K. Okazaki.  Spicule Formation by Isolated Micromeres of the Sea Urchin Embryo , 1975 .

[61]  V. Vacquier.  The isolation of intact cortical granules from sea urchin eggs: calcium lons trigger granule discharge. , 1975, Developmental biology.

[62]  L. Pikó,et al.  MITOCHONDRIAL DNA REPLICATION IN SEA URCHIN OOCYTES , 1974, The Journal of cell biology.

[63]  A. Mahowald,et al.  Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Jan Ellenberg,et al.  Light microscopy of echinoderm embryos. , 2004, Methods in cell biology.

[65]  M. Kloc,et al.  The Balbiani body and germ cell determinants: 150 years later. , 2004, Current topics in developmental biology.

[66]  M. L. King,et al.  Germ plasm and molecular determinants of germ cell fate. , 2000, Current topics in developmental biology.

[67]  I. Spector,et al.  Latrunculins--novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. , 1989, Cell motility and the cytoskeleton.

[68]  E. M. Eddy,et al.  Germ plasm and the differentiation of the germ cell line. , 1975, International review of cytology.

[69]  Development and Stem Cells Research Article , 2022 .