Balbiani cytoplasm in oocytes of a primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani body (mitochondrial cloud) of Xenopus laevis oocytes

Żelazowska, Monika; Kilarski, Wincenty; Biliński, S; Podder, Daniel D.; Kloc, Małgorzata

doi:10.1007/s00441-007-0403-9

Cited by 39 publications

(64 citation statements)

References 27 publications

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“…This agrees with the recent identification of ovarian buc in the Chinese sturgeon ( Acipenser sinensis ) representing the primitive Acipenseriformes with estimated origin time about 390 mya [37, 38]. The Balbiani body and specification pattern of the sturgeon PGCs were shown to closely resemble that of anurans, and injected zebrafish Buc-GFP accumulated at the cleavage furrows similar to our salmon study [39, 40]. Together with the localization of sturgeon dazl in the Balbiani body [41], the results suggest the involvement of Buc in the germ plasm assembly of this basal ray-finned fish.…”

Section: Discussionsupporting

confidence: 91%

Multiplicity of Buc copies in Atlantic salmon contrasts with loss of the germ cell determinant in primates, rodents and axolotl

et al. 2016

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BackgroundThe primordial germ cells (PGCs) giving rise to gametes are determined by two different mechanisms in vertebrates. While the germ cell fate in mammals and salamanders is induced by zygotic signals, maternally delivered germ cell determinants specify the PGCs in birds, frogs and teleost fish. Assembly of the germ plasm in the oocyte is organized by the single Buc in zebrafish, named Velo1 in Xenopus, and by Oskar in Drosophila. Secondary loss of oskar in several insect lineages coincides with changes in germline determination strategies, while the presence of buc in mammals suggests functions not associated with germline formation.ResultsTo clarify the evolutionary history of buc we searched for the gene in genomes available from various chordates. No buc sequence was found in lamprey and chordate invertebrates, while the gene was identified in a conserved syntenic region in elephant shark, spotted gar, teleosts, Comoran coelacanth and most tetrapods. Rodents have probably lost the buc gene, while a premature translation stop was found in primates and in Mexican axolotl lacking germ plasm. In contrast, several buc and buc-like (bucL) paralogs were identified in the teleosts examined, including zebrafish, and the tetraploid genome of Atlantic salmon harbors seven buc and bucL genes. Maternal salmon buc1a, buc2a and buc2b mRNAs were abundant in unfertilized eggs together with dnd and vasa mRNAs. Immunostained salmon Buc1a was restricted to cleavage furrows in 4-cell stage embryos similar to a fluorescent zebrafish Buc construct injected in salmon embryos. Salmon Buc1a and Buc2a localized together with DnD, Vasa and Dazl within the Balbiani body of early oocytes.ConclusionsBuc probably originated more than 400 million years ago and might have played an ancestral role in assembling germ plasm. Functional redundancy or subfunctionalization of salmon Buc paralogs in germline formation is suggested by the maternally inherited mRNAs of three salmon buc genes, the localized Buc1a in the cleavage furrows and the distribution of Buc1a and Buc2a in the Balbiani body during oogenesis. The extra-ovarian expression of salmon buc genes and the presence of a second zebrafish bucL gene suggest additional functions not related to germ cell specification.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0809-7) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 91%

Multiplicity of Buc copies in Atlantic salmon contrasts with loss of the germ cell determinant in primates, rodents and axolotl

et al. 2016

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“…The Chinese sturgeon BB/MC, however, seems to diffuse in the cytoplasm of early developing oocytes by in situ hybridization and MitoTracker staining, similar to the Russian sturgeon BB/ MC distribution at stage II and stage III, while the Russian sturgeon BB/MC is concentrated around the germinal vesicle at stage I. There was little difference in the characterization of BB/MC distribution in Russian and Chinese sturgeon, because the antisense probes taken by Zelazowska et al (2007) belonged to Drosophila and Xenopus, not itself and were hydrolyzed to fragments of 20-50 bp, which would include much non-specific hybridization, resulting in abundant germ plasm RNA concentrated around the germinal vesicle. In summary, based on in situ hybridization of germ plasm RNA, dazl and colocalization MitoTracker and Dazl, we confirmed the sturgeon BB/MC distribution in the cytosolic of early developing oocytes and partial co-localization with dazl.…”

Section: Discussionmentioning

confidence: 69%

“…Bars (a, d) 50 μm, (b, e) 20 μm shown that dazl RNA of Xenopus (Chang et al 2004), zebrafish (Kosaka et al 2007), gible carp (Peng et al 2009), medaka (Xu et al 2009) and trout (Li et al 2011) are concentrated within the BB/MC, a spherical-shaped structure. Nonetheless, in Acipenser gueldenstaedtii (Zelazowska et al 2007), oocytes contain two different zones of cytoplasm, the homogeneous ooplasm and granular ooplasm, with the granular ooplasm corresponding to the BB/MC. In sharp contrast to Xenopus and teleost BB/MC, by electron microscopy, in situ hybridization and immunostaining (Zelazowska et al 2007), the BB/MC surrounds the germinal vesicle and homogeneous ooplasm distributes in the oocyte periphery at stage I.…”

Section: Discussionmentioning

confidence: 99%

“…Nonetheless, in Acipenser gueldenstaedtii (Zelazowska et al 2007), oocytes contain two different zones of cytoplasm, the homogeneous ooplasm and granular ooplasm, with the granular ooplasm corresponding to the BB/MC. In sharp contrast to Xenopus and teleost BB/MC, by electron microscopy, in situ hybridization and immunostaining (Zelazowska et al 2007), the BB/MC surrounds the germinal vesicle and homogeneous ooplasm distributes in the oocyte periphery at stage I. At stage II, the BB/MC extends toward the oocyte plasma.…”

Section: Discussionmentioning

confidence: 99%

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Differential expression of fertility genes boule and dazl in Chinese sturgeon (Acipenser sinensis), a basal fish

Yue

et al. 2015

Cell Tissue Res

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The gene family DAZ (deleted in Azoospermia), including boule, dazl and DAZ, performs highly conserved functions in germ cell development and fertility across animal phyla. Differential expression patterns have been demonstrated for the family members in invertebrates and vertebrates including fish. Here, we report the identification of boule and dazl and their expression at both RNA and protein levels in developing and mature gonads of Chinese sturgeon (Acipenser sinensis). Firstly, the isolation of the boule and dazl genes in Chinese sturgeon and the observation of the two genes in coelacanth suggest that dazl originated after the divergence of bony fish from cartilaginous fish but before the emergence of the Actinistia. Quantitative real-time PCR and western blot analyses reveal that boule and dazl RNA and proteins are restricted to the testis and ovary. In situ hybridization and fluorescent immunohistochemistry show that the bisexual mitotic and meiotic germ cell expression of dazl RNA and protein is conserved in vertebrates, while Chinese sturgeon boule RNA and protein exhibit mitotic and meiotic expression in the testis, and also likely display mitotic and meiotic expression in female. Moreover, we directly demonstrate for the first time that sturgeon Balbiani body/mitochondrial cloud disperses in the cytoplasm of early developing oocytes and co-localizes with Dazl to some extent. Finally, urbilaterian boule may also have an ancestral function in oogenesis. Taken together, these results provide useful information on the evolution of DAZ family genes, expression patterns and functions in animal reproduction.

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“…During the first phase of oocyte development, numerous types of RNA and many other macromolecules are synthesized and localized into the specific regions of the oocyte cytoplasm. They are involved in the deposition of maternal determinants and the patterning of the embryo (Howley and Ho 2000;Żelazowska et al 2007). Previtellogenic oocytes exhibit essential changes in the organization of the nucleus, i.e., the germinal vesicle (GV), and cytoplasm.…”

Section: Introductionmentioning

confidence: 99%

Possible participation of mitochondria in lipid yolk formation in oocytes of paddlefish and sturgeon

Żelazowska

Kilarski

2007

Cell Tissue Res

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The ovary of paddlefish and sturgeons (Acipenseriformes) is composed of discrete units: the ovarian nests and ovarian follicles. The ovarian nests comprise oogonia and numerous early dictyotene oocytes surrounded by somatic prefollicular cells. Each ovarian follicle consists of a spherical oocyte and a layer of follicular cells situated on a thick basal lamina, encompassed by thecal cells. The cytoplasm of previtellogenic oocytes is differentiated into two distinct zones: the homogeneous and granular zones. The homogeneous cytoplasm is organelle-free, whereas the granular cytoplasm contains numerous organelles, including mitochondria and lipid droplets. We have analyzed the cytoplasm of early dictyotene and previtellogenic oocytes ultrastructurally and histologically. In the cytoplasm of early dictyotene oocytes, two morphologically different types of mitochondria can be distinguished: (1) with well-developed cristae and (2) with distorted and fused cristae. In previtellogenic oocytes, the mitochondria of the second type show various stages of cristae distortion; they contain and release material morphologically similar to that of lipid droplets and eventually degenerate. This process of mitochondrial transformation is accompanied by an accumulation of lipid droplets that form a single large accumulation (lipid body) located in the vicinity of the oocyte nucleus (germinal vesicle). The lipid body eventually disperses in the oocyte center. The possible participation of these mitochondria in the formation of oocyte lipid droplets is discussed.

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Balbiani cytoplasm in oocytes of a primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani body (mitochondrial cloud) of Xenopus laevis oocytes

Cited by 39 publications

References 27 publications

Multiplicity of Buc copies in Atlantic salmon contrasts with loss of the germ cell determinant in primates, rodents and axolotl

Multiplicity of Buc copies in Atlantic salmon contrasts with loss of the germ cell determinant in primates, rodents and axolotl

Differential expression of fertility genes boule and dazl in Chinese sturgeon (Acipenser sinensis), a basal fish

Possible participation of mitochondria in lipid yolk formation in oocytes of paddlefish and sturgeon

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