The proliferation and migration of immature germ cells in the mussel, Mytilus galloprovincialis: observation of the expression pattern in the M. galloprovincialis vasa-like gene (Myvlg) by in situ hybridization

Obata, Masahiro; Sano, Natsumi; Kimata, Shunsuke; Nagasawa, Kazue; Yoshizaki, Goro; Komaru, Akira

doi:10.1007/s00427-010-0335-3

Cited by 20 publications

(18 citation statements)

References 31 publications

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“…7). In Mytilus (Obata et al 2010) and oysters (Sano et al 2015), for example, vasa transcripts were detected with a low signal also during the spent season in the area in which the gonad forms.…”

Section: Discussionmentioning

confidence: 99%

VASA expression suggests shared germ line dynamics in bivalve molluscs

Milani

Pecci

Ghiselli

et al. 2017

Histochem Cell Biol

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Germ line segregation can occur during embryogenesis or after embryogenesis completion, with multipotent cells able to give rise to both germ and somatic cells in the developing juvenile or even in adulthood. These undifferentiated cells, in some animals, are self-renewing stem cells. In all these cell lineages, the same set of genes, among which vasa, appears to be expressed. We traced VASA expression during the peculiar gonad rebuilding of bivalves to verify its presence from undifferentiated germ cells to mature gametes in an animal taxon in which the mechanism of germ line establishment is still under investigation. We utilized antibodies produced against VASPH, VASA homolog of Ruditapes philippinarum (Subclass Heterodonta), to compare the known expression pattern of R. philippinarum to two species of the Subclass Pteriomorphia, Anadara kagoshimensis and Crassostrea gigas, and another species of the Subclass Heterodonta, Mya arenaria. The immunohistological data obtained support a conserved mechanism of proliferation of “primordial stem cells” among the simple columnar epithelium of the gut, as well as in the connective tissue, contributing to the seasonal gonad reconstitution. Given the taxonomic separation of the analyzed species, we suggest that the process could be shared in bivalve molluscs. The presence of germ cell precursors in the gut epithelium appears to be a feature in common with model organisms, such as mouse, fruit fly, and human. Thus, the comparative study of germ line establishment can add details on bivalve development, but can also help to clarify the role that VASA plays during germ cell specification.Electronic supplementary materialThe online version of this article (doi:10.1007/s00418-017-1560-x) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

VASA expression suggests shared germ line dynamics in bivalve molluscs

Milani

Pecci

Ghiselli

et al. 2017

Histochem Cell Biol

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“…Recently, piwi and vasa genes have been proposed to be ancestrally associated with stem cell character ('stemness'), rather than solely with germline stem cells [20]. In animal lineages such as in the mussel Mytilus galloprovincialis , in which there is restricted expression vasa in the germline [37], there could have been a partial or complete loss of expression of this gene from somatic stem cell lineages. In C. teleta , vasa , nanos and piwi orthologs are all expressed in very similar patterns to one another in both the germline and posterior growth zone, likely in multipotent stem cells.…”

Section: Discussionmentioning

confidence: 99%

Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta

Giani

Yamaguchi

Boyle

et al. 2011

EvoDevo

106

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BackgroundStem cells have a critical role during adult growth and regeneration. Germline stem cells are specialized stem cells that produce gametes during sexual reproduction. Capitella teleta (formerly Capitella sp. I) is a polychaete annelid that reproduces sexually, exhibits adult growth and regeneration, and thus, is a good model to study the relationship between somatic and germline stem cells.ResultsWe characterize expression of the two C. teleta orthologs of piwi, genes with roles in germline development in diverse organisms. Ct-piwi1 and Ct-piwi2 are expressed throughout the life cycle in a dynamic pattern that includes both somatic and germline cells, and show nearly identical expression patterns at all stages examined. Both genes are broadly expressed during embryonic and larval development, gradually becoming restricted to putative primordial germ cells (PGCs) and the posterior growth zone. In juveniles, Ct-piwi1 is expressed in the presumptive gonads, and in reproductive adults, it is detected in gonads and the posterior growth zone. In addition, Ct-piwi1 is expressed in a population of putative PGCs that persist in sexually mature adults, likely in a stem cell niche. Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.ConclusionsIn C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells. It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

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“…Thus, Vasa appears to be a specific marker of germ cells in R. philippinarum , as in other animals (see [12]–[15], [81]–[85]). Up to now, only the distribution of vasa mRNAs was analyzed in molluscs [86]–[91], and this is the first study about the immunolocalization of Vasa protein. Clam gonad is not permanent and the mechanism of its reformation every mating season is not fully documented.…”

Section: Discussionmentioning

confidence: 99%

Doubly Uniparental Inheritance of Mitochondria As a Model System for Studying Germ Line Formation

et al. 2011

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BackgroundDoubly Uniparental Inheritance (DUI) of mitochondria occurs when both mothers and fathers are capable of transmitting mitochondria to their offspring, in contrast to the typical Strictly Maternal Inheritance (SMI). DUI was found in some bivalve molluscs, in which two mitochondrial genomes are inherited, one through eggs, the other through sperm. During male embryo development, spermatozoon mitochondria aggregate in proximity of the first cleavage furrow and end up in the primordial germ cells, while they are dispersed in female embryos.Methodology/Principal FindingsWe used MitoTracker, microtubule staining and transmission electron microscopy to examine the mechanisms of this unusual distribution of sperm mitochondria in the DUI species Ruditapes philippinarum. Our results suggest that in male embryos the midbody deriving from the mitotic spindle of the first division concurs in positioning the aggregate of sperm mitochondria. Furthermore, an immunocytochemical analysis showed that the germ line determinant Vasa segregates close to the first cleavage furrow.Conclusions/SignificanceIn DUI male embryos, spermatozoon mitochondria aggregate in a stable area on the animal-vegetal axis: in organisms with spiral segmentation this zone is not involved in cleavage, so the aggregation is maintained. Moreover, sperm mitochondria reach the same embryonic area in which also germ plasm is transferred. In 2-blastomere embryos, the segregation of sperm mitochondria in the same region with Vasa suggests their contribution in male germ line formation. In DUI male embryos, M-type mitochondria must be recognized by egg factors to be actively transferred in the germ line, where they become dominant replacing the Balbiani body mitochondria. The typical features of germ line assembly point to a common biological mechanism shared by DUI and SMI organisms. Although the molecular dynamics of the segregation of sperm mitochondria in DUI species are unknown, they could be a variation of the mechanism regulating the mitochondrial bottleneck in all metazoans.

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The proliferation and migration of immature germ cells in the mussel, Mytilus galloprovincialis: observation of the expression pattern in the M. galloprovincialis vasa-like gene (Myvlg) by in situ hybridization

Cited by 20 publications

References 31 publications

VASA expression suggests shared germ line dynamics in bivalve molluscs

VASA expression suggests shared germ line dynamics in bivalve molluscs

Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta

Doubly Uniparental Inheritance of Mitochondria As a Model System for Studying Germ Line Formation

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