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Primordial Germ Cell Migration in Zebrafish

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Primordial Germ Cell Migration in Zebrafish Development 126, 5295-5307 (1999) 5295 Printed in Great Britain © The Company of Biologists Limited 1999 DEV3057 Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells Gilbert Weidinger‡, Uta Wolke‡, Marion Köprunner, Michael Klinger* and Erez Raz¶ Department of Developmental Biology, Institute of Biology I, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany *Present address: Faculty of Biology, University of Konstanz, Universitätsstrasse 10, D-78434 Konstanz, Germany ‡These authors contributed equally to this work ¶Author for correspondence (e-mail: [email protected]) Accepted 21 September; published on WWW 9 November 1999 SUMMARY In many organisms, the primordial germ cells have to obtain information on the origin of the positional cues migrate from the position where they are specified towards provided to the germ cells by somatic tissues during their the developing gonad where they generate gametes. migration, we analyzed the migration pattern in mutants, Extensive studies of the migration of primordial germ cells including spadetail, swirl, chordino, floating head, cloche, in Drosophila, mouse, chick and Xenopus have identified knypek and no isthmus. In mutants with defects in axial somatic tissues important for this process and structures, paraxial mesoderm or dorsoventral patterning, demonstrated a role for specific molecules in directing the we find that certain steps of the migration process are cells towards their target. In zebrafish, a unique situation specifically affected. We show that the paraxial mesoderm is found in that the primordial germ cells, as marked by is important for providing proper anteroposterior expression of vasa mRNA, are specified in random positions information to the migrating primordial germ cells and relative to the future embryonic axis. Hence, the migrating that these cells can respond to changes in the global cells have to navigate towards their destination from dorsoventral coordinates. In certain mutants, we observe various starting positions that differ among individual accumulation of ectopic cells in different regions of the embryos. Here, we present a detailed description of the embryo. These ectopic cells can retain both morphological migration of the primordial germ cells during the first 24 and molecular characteristics of primordial germ cells, hours of wild-type zebrafish embryonic development. We suggesting that, in zebrafish at the early stages tested, the define six distinct steps of migration bringing the vasa-expressing cells are committed to the germ cell primordial germ cells from their random positions before lineage. gastrulation to form two cell clusters on either side of the midline by the end of the first day of development. To Key words: Zebrafish, Primordial germ cell, Cell migration, vasa INTRODUCTION cells along the migratory route. Receptor-ligand interaction is required to support migration and survival of the PGCs While the specification mechanisms of primordial germ cells (Bernex et al., 1996; Matsui et al., 1990). Mouse PGCs have (PGCs) and the position where these cells are specified can also been shown to migrate towards explants of target tissue, differ, a common theme for many species is that the germ suggesting that they are attracted towards the genital ridge by cells are formed in regions distinct from the site where the long-range signaling (Godin et al., 1990). Finally, a role for gonad will form. Hence, the PGCs have to migrate towards extracellular matrix (ECM) molecules in the PGC migration the future gonad, a process that has been studied in Xenopus process has been suggested by the finding of specific and particularly in Drosophila and mouse where modern interactions between ECM molecules and PGCs and by the genetic approaches have been applied (reviewed in Howard, phenotype of PGCs lacking specific receptors for components 1998; Rongo et al., 1997; Wylie, 1999). The general of the ECM (e.g., Anderson et al., 1999). In Drosophila, a conclusion from these studies is that the movements of the detailed description of the migration process coupled with PGCs towards the gonadal region, where they associate with genetic analysis allowed the identification of tissues and cells of mesodermal origin, rely on directional cues provided molecules required for PGC migration (reviewed in Howard, by the somatic environment (e.g., Anderson et al., 1999; 1998; Rongo et al., 1997; Williamson and Lehmann, 1996; Jaglarz and Howard, 1994; Matsui et al., 1990; Moore et al., Wylie, 1999). Drosophila PGCs are formed at the posterior 1998; Zhang et al., 1996). A classical example from the pole of the early embryo and then together with somatic cells mouse is that of the c-kit receptor, which is expressed in the participate in the morphogenetic movement forming the PGCs, and its ligand Steel, which is expressed by somatic posterior midgut (PMG). Subsequently, the PGCs actively 5296 G. Weidinger and others migrate through the midgut epithelium towards the gonadal MATERIALS AND METHODS mesoderm with which they align and coalesce. Two genes specifically affecting this migration are expressed in somatic Zebrafish maintenance and mutant strains cells (Moore et al., 1998; van Doren et al., 1998; Zhang et Zebrafish (Danio rerio) were maintained as described previously al., 1996, 1997): the wunen gene is required for repulsion of (Westerfield, 1995). Mutant strains used: chordino, dintm84 PGCs, thereby bringing them closer to the mesodermal target (Hammerschmidt et al., 1996); cloche, clom39 (Stainier et al., 1995); whereas columbus functions in attracting them towards the floating-head, flhtk241 (Odenthal et al., 1996); knypek, knym818 (A. Chitnis, K. Artinger and W. Driever, personal communication; gonadal mesoderm. tu29a Until recently, studying the migration of PGCs in fish has Solnica-Krezel et al., 1996); no isthmus, noi (Brand et al., 1996); spadetail, sptb104 (Kimmel et al., 1989); swirl, swrta72a (Mullins et al., relied on their identification by morphological criteria at 1996). relatively late stages, usually around the beginning of somitogenesis (e.g., Gevers et al., 1992). The ability to follow Whole-mount in situ hybridization and histology PGC migration in fish was revolutionized by the cloning of the Two-color in situ hybridization was performed as described by Jowett zebrafish vasa gene homolog, which is exclusively expressed and Lettice (1994) with modifications according to Hauptmann and in PGCs (Olsen et al., 1997; Yoon et al., 1997). vasa was Gerster (1994). In some cases, light-blue color was obtained using a originally identified in Drosophila as a maternal effect gene β-galactosidase-conjugated anti-digoxigenin antibody and X-Gal for required for the formation of the abdominal segments and for subsequent color reaction (Hauptmann, 1999). The following probes germ cell specification (Hay et al., 1988; Lasko and Ashburner, were used for whole-mount in situ mRNA hybridization: din (Miller- 1988; Schüpbach and Wieschaus, 1986). In situ hybridization Bertoglio et al., 1997), gata2 (Detrich et al., 1995), hoxa-2 (Prince et of 4-cell-stage zebrafish embryos showed specific localization al., 1998), myoD (Weinberg et al., 1996), papc (Yamamoto et al., 1998), pax2.1 (formerly paxb, (Krauss et al., 1991)), pax8 (Pfeffer et of the vasa transcript in four stripes at the edges of the first two al., 1998) and vasa (Olsen et al., 1997; Yoon et al., 1997). cleavage planes, suggesting that specification of germ cells is Methacrylate sections were performed using the JB-4 Plus resin achieved by localization of cytoplasmic components as in (Polyscience Inc.) according to the manufacturer’s protocol. other organisms such as Drosophila, C. elegans and Xenopus (Wylie, 1999; Yoon et al., 1997). At the 32-cell stage, the Determination of PGC number transcript is detected in four cells that subsequently divide to vasa-positive cells were counted using a stereomicroscope at ×150 give rise to four cell clusters located close to the blastoderm magnification. The number of vasa-positive PGCs varies among margin at late blastula stages. During subsequent development embryos of the same clutch. Importantly, the number of PGCs may these vasa-expressing cells migrate and at 24 hours also be influenced by the genetic background. For example, mutant postfertilization (hpf) end up in two bilateral rows around the chordino and wild-type siblings in the TL genetic background have anterior end of the yolk extension. These cells that maintain about 25 PGCs at 24 hpf (e.g., Table 1), while embryos with AB genetic background typically have as many as 50 PGCs at 24 hpf (e.g., vasa expression at least up to late larval stages are primordial Table 2). For these reasons, description of mutant phenotypes was done germ cells based on their morphology and position (Yoon et by comparing the PGC number or behavior to wild-type siblings. al., 1997). Additionally, to minimize the variability, analysis of the migration Here we provide a detailed analysis of the early stages of process in wild-type and in mutant embryos was usually performed by PGC migration in zebrafish. We find that this process can be fixing embryos of the same clutch at different times of development. divided into six distinct steps, some of which appear to be shared with somatic tissues, whereas others seem to reflect vasa cDNA amplification and injection of mRNA active migration of PGCs relative to their somatic neighbors. Full-length vasa cDNA (as published by Yoon et al. (1997)) was Analysis of the migration process in mutant embryos shows amplified from ovary cDNA using the following primers: 5′ primer that some of these steps can be specifically affected. This (TCA GGC TCT TCA CGC GTG TCC ACC TGC TAC), 3′ primer allows us to propose which structures or processes are (TTT TGT CAC CAG TAT CCG TCT TTA TTT TGA) (italic sequence involved in directing the migration of the PGCs. As a result is homologous to vasa). Except for a few amino acid changes that we attribute to polymorphisms between strains (identical changes were of abnormal migration, in some mutants we observe detected in independent PCR reactions), the sequence of the cloned accumulation of cells in ectopic regions.
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