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Formation and Localization of Cytoplasmic Domains in Leech and Ascidian Zygotes

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Formation and Localization of Cytoplasmic Domains in Leech and Ascidian Zygotes Inl. J. D<\. lIio!. ~!: 1075-1U8~ 119981 Formation and localization of cytoplasmic domains in leech and ascidian zygotes JUAN FERNANDEZ", FABRICE ROEGIERS2, VIVIANA CANTILLANA' and CHRISTIAN SARDET2 rDeparramento de 8;010g(8, Facu/rad de Ciencias, Universidad de Chile, Santiago. Chile and 2Unire de 8iologie Cellula ire Marine URA 671 CNRS/Universite Pierre et Marie Curie, Observatoire Station Zoologique, Villefranche~sur-Mer, France CONTENTS Introduction u .." .................................................. 1075 Leech and ascidian oocytes. zygotes and embryos .............................. 1076 Formationand localization of cytoplasmic domains. 1078 Fertilization and meiotic events Pronuclear movements and interphase events Mitotic events and the partitioning at cytoplasmic domains Mechanisms and perspectives . "............ 1080 Fertilization and early meiotic events Late meiotic events Interphase and mitotic events Summary ........................ ......................... 1082 KEY WORDS: It'all (llId mr;d;,l1l :')Kotn, ()'toIJ/(l\/1I;( doma;lI'. OOIJ/"'I1I;( wgug"t;fm, :..\golf' ntfHkfll,tol/ Introduction coming from Drosophila embryos, has shown that determinants can be heterogeneously distributed macromolecules whose location Most eggs display an heterogeneous distribution ot organelles may be or may not be necessarily coincident with microscopically and cytoskeletal elements established during oogenesis and/or identifiable structures (Davidson. 1986: St Johnston and Nusslein- aher tertilization and subsequent cell cycles (see Capco, 1995). Vol hard. 1992: Nusslein-Volhard, 1996). The best example of a Heterogeneities are easily visualized in eggs that have microscopi- determinant associated with a structure is that of the oskar mRNA in cally discernible cytoplasmic domains due to HH::!accumulation of Drusopflila. As a result or cytoskeletal reoryalli.latiorls, oskar mRNA organelles and sometimes pigmented vesicles or granules is normally present in a distinct cytoplasmic domain known as "germ (Fernandez. 1980: Sardet et al" 1994). These distinct cytoplasmic plasm". Ectopic localization of this mRNA promotes the appearance domains were first perceived a century ago in eggs of protostomes of germ plasm and functional pole cells in ectopic regions of the and deuterostomes, including those of leeches, sea urchins, blastula (Ephrussi and Lehmann. 1992). Except for germ plasms. ascidians, molluscs and insects (Whitman, 1878: Boveri. 1895: which exhibit common structural and biochemical features in egg Conklin. 1897,1905: Wilson, 1925). The presence of naturally-marked cytoplasmic regions has al- --- lowed cell lineage analysis and the demonstration that cell fate ,\/Jl'r/,'iflli(J//J rw'ri ill rhjl 1m/wI: .\T. .mim,tl Ic'ltlpl.l,m: (;"\1\. rt'1111tl,nnw- ;HI,IClil1~ hod\-; <:H, dIlHloT1; <:R. Ctll1lranioll lil1~; (:Y. nt.I,lc'T: fR, depended on the presence or absence of particular domains. Early ('ndt'ptHlI1il" l'l'UCllhll1l; FJ.:. It'II1.llt" kan(ll1It..-e~: (;S, gr.n" 'lit II: 111' P:I, observations formed the basis of a theory of "cytoplasmic localiza- irHI'ilullrillhll'phau': K,\I, J..antHII('Tt"; \IH,lIwridillllal 1I.1I1I\'1If flllllr;lrtinl1: tion" (Wilson. 1925). It was gradually recognized that visible as well :'IIF. IIIOt1,I'[t"r fiber'\: \11. tir~1 lIu'I,ll'ha'>t" olllleio,i,= \In. mOIl.',I('r; \11', as invisible cytoplasmic regions might contain 'determinants' that 1II.lle prulIIl1lc"us: \IS, meiotiC' 'pilUllt'; PI\,lir'l pCII.\! hl,(h; PI',pt'linudt,'u" caused the cells thHt inherited these domains to follow different p].I'1II dom.till: PR. pu].lr riuj,{: ~C. 'penn ll'l1lru:'UlIIl': :0.:'\. SPt'rIt1lll1ch:u': differentiation programs. In the last 2 decades evidence, principally \"1". \'eK"lallt'lopla'll1: Z:\. I~~oll' Illlclt'll', ---- .Address for reprints: Departamento de Biologla. Facultad de Ciencias, Universidad de Chile, Casil1a 653, Santiago, Chile. FAX: 56.2 271 2983. e.mail: [email protected] 021 ~-6!82/98/S I0.00 ~ l'IH"'l'r~\\ f'rinlc.JmSp4in 1076 J. Femdnde: el al. from a wide variety of species (electron dense RNA-rich granules acrosome and flagellum as well as the single sperm mitochondrion immersed in a "nuage" of mitochondria, see Rango and Lehman, are found nearby (Fernandez ef al., 1994). In rare cases polyspermy 1996), other recognizable cytoplasmic domains exhibit a widely occurs, and sperm nuclei are found at the periphery of the egg in both different structure, compositionand localization(Sardet et al., 1994; hemispheres. Capco, 1995). This is reflected in the various names given to them Study of the embryology of leeches goes back to Whitman (myoplasm, pole plasm, teloplasm). Yet common mechanisms must (1878,1887), who was the first investigator to attempt cell lineage be at work in the formation, positioning and maintenance of these analysis using glossiphoniid leech embryos. Embryonic develop- domains. Cytoskeletal elements (microtubules, microfilaments and ment in leeches was first considered to be essentially determinate possibly intermediate filaments) have been implicated in the progres- and to rely on invariant and independent cell lineages (Mori. 1932). sive formation, positioning and relocation of these domains with More recently it was shown that development of some cell lines respect to the embryonic axes (Sardet et al.. 1994; Fernandez and also depends on cell interactions (Blair and Weisblat, 1984; Olea, 1995; Etkin, 1997; Gard el aI., 1997). There is also increasing Shankland, 1987) and that indeterminacy and transtating take evidence that cytoskeleton-associated motors, and their membrane place under certain experimental conditions (Shankland and receptors, are a major factor in the transport, anchorage and possibly Weisblat, 1984; Weisblat and Blair, 1984). Like many protostome in the function of mRNAs and other determinants (Glatzer and embryos, the leech embryo undergoes spiral cleavage. A series of Ephrussi, 1996; Bassell and Singer, 1997; Gavis, 1997; Goodson el unequal stereotyped divisions results in blastomeres of different al., 1997). size, position, structure and fate. These give rise to precursor cells Leech and ascidian eggs were among the first cells in which whose descendants can be unambiguously identified (Fernandez formation of microscopically visible domains were associated with and Olea, 1982; Weisblat el.aI.., 1987). A particularfeature of leech cell fate determination (Whitman, 1878; Conklin, 1905). In this development is that the ectoderm and mesoderm are produced by review, we compare the nature of the cytoplasmic domains and the a discrete number of stem cells (telobiasts), located at the caudal mechanisms responsible fortheir localizations in leech and ascidian end of the embryo, that inherit particular cytoplasmic domains zygotes. We also consider their importance for development. (teloplasms) (Fernandez, 1980; Fernandez and Stent, 1980). Recent reviews, books and papers have appeared that deal with These domains, originally located at both the animal and vegetal these and other species (Sardet el. al., 1994; Capco, 1995; King. poles of the zygote, are produced through a series of cytoplasmic 1996; Pilon and Weisblat, 1997). rearrangements that will be described and discussed in this review. Another interesting feature of leech embryonic development deals Leech and ascidian oocytes, zygotes and embryos with segmentation. Leeches have a constant number of segments (32) with an additional non-segmented prostomium. The leech Leeches are protandric annelids that lay cocoons containing embryo is a particularly convenient model for the study of the from a few to several dozen eggs fertilized in the ovaries. Diameter cellular and molecular events involved in segment determination of laid zygotes ranges from about 100 ~m (Hirudinid leeches) to and organization (Fernandez and Stent, 1980; Weisblat el. al." several mm (Glossiphoniid leeches). Some species breed several 1988,1994; Shankland el al., 1991). times a year (Hel.obde/./a) while others (Theromyzon) breed only Ascidians are hermaphroditic marine invertebrates once in their life and then die. The hirudinid leech Hirudomedicinalis (urochordates. tunicates) with a small genome. Most species and the glossiphoniid leeches Hel.obde/./a robusta, Hel.obde/./a exhibit indirect embryonic development but a few species develop triserialis and Theromyzon rude have been used for developmen- directly (Satoh, 1994). Most ascidians develop rapidly into simple tal studies at cellular and molecular level. swimming tadpoles whose organization is typical of the chordate Atthe beginning of the breeding season, when leeches are males, embryo. Within days of hatching, tadpole embryos attach to the the animals copulate. The transmitted sperm is retained inside the substrate and metamorphose into a reproductive sessile adult. body for periods of weeks to months. The animals then become Ascidians are deuterostome organisms characterized by stere- female and produce mature oocytes that are fertilized internally otypic bilaterally symmetrical cleavage divisions that produce a before proceeding to first metaphase (MI) of meiosis. As soon as the blastula with a relatively small number of cells in a few hours. The zygotes are laid, development is initiated. In some leeches fate of these blastomeres, up to the tadpole and juvenile stages, (Theromyzon) development is direct while in others (Hirudo) it is has been partly or completely traced in Ciona intestinalis, Phallusia indirect, giving rise to a cryptolarva.
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