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The Function and Regulation of Vasa-Like Genes in Germ-Cell C O M Development M E N

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The Function and Regulation of Vasa-Like Genes in Germ-Cell C O M Development M E N http://genomebiology.com/2000/1/3/reviews/1017.1 Minireview The function and regulation of vasa-like genes in germ-cell c o m development m e n Erez Raz t Address: Department for Developmental Biology, Institute for Biology I, Freiburg University, 79104 Freiburg, Germany. E-mail: [email protected] r e v i Published: 1 September 2000 e w Genome Biology 2000, 1(3):reviews1017.1–1017.6 s The electronic version of this article is the complete one and can be found online at http://genomebiology.com/2000/1/3/reviews/1017 © GenomeBiology.com (Print ISSN 1465-6906; Online ISSN 1465-6914) r e ports Abstract The vasa gene, essential for germ-cell development, was originally identified in Drosophila, and has since been found in other invertebrates and vertebrates. Analysis of these vasa homologs has revealed a highly conserved role for Vasa protein among different organisms, as well as some important differences in its regulation. deposited research Germ-cell development in vertebrates and location. In mutants in which the formation of this morpho- invertebrates logically characteristic cytoplasm is disrupted, germ-cell for- In sexually reproducing organisms, primordial germ cells mation is impaired (reviewed in [5]). The pole plasm is (PGCs) give rise to gametes that are responsible for the characterized by the presence of the polar granules, electron- refereed research development of a new organism in the next generation. dense structures not delimited by a membrane that contain These cells must remain totipotent - able to differentiate into many RNAs and proteins and that are associated with mito- each and every cell type of all the different organs. In many chondria. The distribution of the pole plasm correlates with organisms, maintenance of totipotency is achieved by the the site of PGC formation. On the basis of their unique mor- specification of germ cells early in embryogenesis: a small phology, germ plasm components have also been identified in group of cells is set aside to follow a unique pathway of dif- other organisms such as C. elegans (where they are termed P ferentiation into gametes (reviewed in [1-3]). granules), Xenopus laevis (germinal granules), chick and zebrafish [1-3,6-9]. Information on the specification of PGCs has been gained interactions from detailed microscopical analysis, embryological experi- The specification of the germline is different in mammals. ments (for example transplantation of cells or cytoplasm) and Several lines of evidence argue that here inherited cytoplas- gene identification through genetic screens for maternal-effect mic factors do not have a role in germ-cell specification, but mutations in Drosophila and Caenorhabditis elegans that germ cells are induced through cellular interactions (reviewed in [1-4]). The main conclusion from these two inver- during gastrulation (reviewed in [1-3]). Morphologically dis- tebrate model organisms is that asymmetrical localization of tinct germ plasm has not so far been identified in early mam- cytoplasmic determinants - the germ plasm - is responsible for malian embryos. In addition, mouse eggs from which the information the early specification of the germline lineage. The importance animal or vegetal pole was experimentally removed devel- of localized cytoplasmic determinants for germ-cell develop- oped into fertile mice, arguing against any polarity in the egg ment has been most clearly shown in Drosophila. Here, for that is functionally important for germ-cell specification [10]. example, cytoplasmic germ plasm determinants concentrated Mouse germ cells arise just before and during early gastrula- at the posterior pole of the embryo in pole plasm can direct tion, around the proximal part of the epiblast adjacent to the cells towards a germ-cell fate when transplanted to an ectopic extra-embryonic region. Transplantation experiments 2 Table 1 Genome Expression and function of vasa homologs* Biology Species Gene RNA expression RNA localization Protein expression Protein localization Function References Fruit fly vasa Early embryo: uniform, followed No Germ cells: as soon as they Oocyte and cleavage-stage Early embryogenesis: [13,14,16, Vol 1No3 (Drosophila by specific expression in form and throughout embryonic embryos: in polar granules, abdomen development, 17,40,41] melanogaster) germ cells. Ovary: uniform in development. Ovary: germline nuclear bodies and dense nanos mRNA translation, nurse cells and oocyte. stem cells, nurse cells, oocytes. cytoplasmic masses. formation of pole plasm Testis: early stage spermatocytes Testis: early stages of and germ cells. and germline stem cells. spermatogenesis. Oogenesis: germline cyst development, oocyte Raz differentiation, gurken mRNA translation, oocyte polarity, translation of oskar mRNA. Mouse Mvh Testis: spermatocytes and early No Germ cells: as they arrive at the Granules near nucleus in Testis: required in PGCs [19, (Mus spermatids. Ovary: ND genital ridge. Ovary: early stages pachytene-diplotene during premeiotic stages of 20,38] musculus) of oogenesis. Decreases during spermatocytes. After spermatogenesis for maturation. Not detected in meiosis: a large perinuclear sperm differentiation before mature oocytes. Testis: in granule up to spermatid nucleus pachytene spermatocyte spermatogonium to round elongation. Sperm: corresponds stage. Male mutants: PGC spermatid stages. to that of the ‘chromatoid body’. proliferation defects. Female mutants: fertile and show no defects of oogenesis. Zebrafish vasa Maternally supplied to embryo. One-cell embryo: ring between Maternal protein uniformly Associated with germinal vesicle ND [6,9,23,31] (Danio rerio) From the 32-cell stage, detected yolk and cytoplasm. Two- to distributed during blastula stages. in early oogenesis. From late in four blastomeres. Gastrulation: four-cell embryo: near cleavage At late blastula, distinct expression blastula on, associated with expressed in four PGC clusters as furrow, inherited by four cells. in PGCs as expression in somatic nuclear envelope in a pattern they migrate towards the gonad. Then asymmetrically localized cells decreases. distinct from that of the RNA Testis: spermatogenesis, excluding and distributed between mature spermatozoa. Ovary: all dividing blastomeres until late stages of oogenesis. blastula, when it fills PGCs’ cytoplasm. Late oogenesis: oocyte cortex. Planarian DjvlgA Testis: DjvlgA in spermatogonia, No ND ND ND [26] (Dugesia DjvlgB spermatocytes, spermatids. japonica) DjvlgB only in spermatocytes. Ovary: both expressed in oocytes. Outside gonad DjvlgA expressed in totipotent neoblasts. Frog XVLG1 Gonad in both sexes. Ovary: all stages No Oocytes and unfertilized eggs. Embryos: appears to be perinuclear. Survival or differentiation of PGCs. [22,42-44] (Xenopus laevis) of oogenesis. Gastrulation: PGC- Blastula and gastrula: all cells, intensity specific expression. of staining decreasing with time. After gastrulation: level increases in PGCs. Chick Cvh Testis: spermatogonia to mature ND Embryos: maternal protein from the Cleaving embryos: basal part of ND [8] (Gallus gallus) spermatocytes. Ovary: ND one-cell stage. Before gastrulation: cleavage furrows.Testis: granular Cvh-positive PGCs in center of area staining in spermatocytes. Ovary: pellucida. Migrating and post-migratory underneath plasma membrane, near PGCs. Testis: spermatogonia to round germ-plasm-associated organelles and spermatids. Ovary: immature oocytes. molecules such as mitochondria and spectrin. http://genomebiology.com/2000/1/3/reviews/1017.3 showed that, at these stages, these cells are not yet committed to the germline, and when grafted into distal positions they [28,45] can develop into somatic tissues [1,2]. Consistent with the comment notion of germ-cell induction through cell-cell interactions, distal cells that would develop as somatic cells can develop VASA into germ cells when grafted into the region where germ cells ty [30] normally form [1,2]. Indeed, formation of the founding popu- ired for g1h-4 lation of PGCs in the mouse was shown to depend on the and function of at least one extracellular factor - bone mor- phogentic protein 4 (Bmp4) [3]. (RNAi), with many cells reviews glh-1/4 not proceeding beyond pachytene. G1h-1 g1h-2 Some of the methodologies used in the invertebrate models cannot be applied to vertebrates. In particular, the maternal- effect screens that were instrumental in analyzing the speci- fication of PGCs in invertebrates are not practicable in the frog, chick or mouse. Fortunately, such screens can be carried out in the zebrafish [11], although in this system too, it would be very difficult to achieve saturation for all mater- nal-effect mutations involved in PGC specification using reports classical forward genetic analysis. later stages. spermatogenesis defective in hed light on the function of gene in a certain class organism. ND, not determined. Homologs of vasa in invertebrates and vertebrates The vasa gene was originally identified in Drosophila as a maternal-effect gene required for the formation of the deposited research abdominal segments and for germ-cell specification [12]. The Vasa protein can be detected in the germline cells of Drosophila throughout their development and in early embryos it is specifically localized to polar granules, which well as in PGCs that have not yet reached this target. Testis: spermatogonia, spermatocysts and within a compact perinuclear body. spermatids. Ovary: oocytes. chromosomal region of localization. In adult oocytes no subcellular arehave
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