Bone morphogenetic protein 15 and growth differentiation factor 9 expression in the ovary of European sea bass (Dicentrarchus labrax): Cellular localization, developmental profiles, and response to unilateral ovariectomy

García-López, Ángel; Sánchez-Amaya, María Isabel; Halm, Silke; Astola, Antonio; Prat, Francisco

doi:10.1016/j.ygcen.2011.09.011

Cited by 29 publications

(18 citation statements)

References 61 publications

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“…It also matches the size of ≈ 60 kDa described for the native Japanese eel proAmh [12] and the 62 kDa fragment detected in black porgy testes [44]. The predominance of proAmh in sea bass testis agrees with observations in eel testis and also with findings in fish ovaries for other TGF-β factors such as Bmp15 and Gdf9 [45,46,47] and could be related to the dependence of binding of the noncovalent complex (AmhN,C) to the Amhr2 for the generation of the mature AmhC [48] To produce a biologically active sea bass Amh, we expressed in CHO cells an engineered sea bass amh cDNA that contained an optimized cleavage site for in vivo proteolytic processing by CHO cell convertases including furin. Although this strategy worked with rat and human recombinant AMHs [38,39,40], endogenous cleavage of recombinant sea bass Amh was highly inefficient.…”

Section: Sea Bass Amh Proteinsupporting

confidence: 87%

Conserved Anti-Müllerian Hormone: Anti-Müllerian Hormone Type-2 Receptor Specific Interaction and Intracellular Signaling in Teleosts1

Rocha

Zanuy

Gómez

2016

Biology of Reproduction

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In higher vertebrates, anti-Müllerian hormone (AMH) is required for Müllerian duct regression in fetal males. AMH is also produced during postnatal life in both sexes regulating steroidogenesis and early stages of folliculogenesis. Teleosts lack Müllerian ducts, but Amh has been identified in several species including European sea bass. However, information on Amh type-2 receptor (Amhr2), the specific receptor for Amh binding, is restricted to a couple of fish species. Here, we report on cloning sea bass amhr2, the production of a recombinant sea bass Amh, and the functional analysis of this ligand-receptor couple. Phylogenetic analysis revealed that sea bass amhr2 segregates with Amhr2 from other vertebrates. This piscine receptor is capable of activating Smad proteins. Antibodies raised against sea bass Amh were used to study native and recombinant Amh, revealing proteins in the range of 66-70 kDa corresponding to the full length Amh. Once proteolytically treated, recombinant sea bass Amh generates a 12 kDa C-terminal mature protein, suggesting that contrary to what has been described for other fish Amh proteins, this protein is processed in a similar way as mammalian AMH. The mature sea bass Amh is a biologically active protein able to bind sea bass Amhr2 and, surprisingly, also human AMHR2. In prepubertal sea bass testes, Amh was detected by immunohistochemistry mostly in Sertoli cells surrounding early germ-cell generations. During spermatogenesis, a weaker staining signal could be observed in Sertoli cells surrounding spermatocytes.

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Section: Sea Bass Amh Proteinsupporting

confidence: 87%

Conserved Anti-Müllerian Hormone: Anti-Müllerian Hormone Type-2 Receptor Specific Interaction and Intracellular Signaling in Teleosts1

Rocha

Zanuy

Gómez

2016

Biology of Reproduction

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“…By Western blot, BMP15 protein was detected in ovine follicular fluid primarily as the unprocessed promature form, suggesting that the mature form was present at low or undetectable levels in ovarian tissue (McNatty et al, 2006); when in-vitro expression systems were used, however, BMP15 was detected in multiple forms by Western blot (Liao et al, 2003a(Liao et al, , 2003bMcIntosh et al, 2008;Otsuka et al, 2000) Protein expression confirmed that 6 and 8 mm follicles translated BMP15 mRNA ( Figure 2). This pattern of expression was similar to another oviparous vertebrate, the European seabass, in which BMP15 mRNA was detected during early stages of follicle development but protein expression was at low or undetectable levels until the lipid vesicle stage or beginning of secondary growth phase (García-López et al, 2011). In addition, in the rat ovary, expression of BMP15 mRNA and protein detected by in situ hybridization and immunohistochemistry also increased with follicle development (Otsuka et al, 2000).…”

Section: Discussionsupporting

confidence: 73%

Bone morphogenetic protein 15 may promote follicle selection in the hen

Stephens

Johnson

2016

General and Comparative Endocrinology

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In the hen, optimal ovulation rate depends on selection of a single follicle into the pre-ovulatory hierarchy. Follicle selection is associated with increased oocyte growth and changes in gene expression in granulosa cells surrounding the oocyte, in preparation for ovulation. This study investigated the expression, function and regulation of bone morphogenetic protein-15 (BMP15) during follicle development in the hen. BMP15 mRNA expression was analyzed in the ooplasm and granulosa cells of 3mm follicles and was confirmed to be primarily in the ooplasm. BMP15 was detected by immunoblotting in 6 and 8mm follicles near the time of follicle selection. Expression of mRNA for BMP15 receptors (BMPR1B and BMPR2) in granulosa cells increased with follicle size, indicating that BMP15 may play an important role around follicle selection. The function of BMP15 was examined by culturing granulosa cells from 3-5mm and 6-8mm follicles with recombinant human BMP15 (rhBMP15). BMP15 increased expression of follicle stimulating hormone receptor (FSHR) mRNA and decreased anti-Müllerian hormone (AMH) mRNA and occludin (OCLN), factors associated with follicle maturation and growth in the hen. Hormonal regulation of BMP15 was assessed by whole follicle culture with estradiol (E2) which increased BMP15 mRNA expression. The distinct expression pattern of BMP15 and its receptors, coupled with the effects of BMP15 to increase FSHR mRNA and decrease AMH mRNA and OCLN mRNA and protein expression suggest that the oocyte may have a role in follicle selection in the chicken.

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“…In previtellogenic oocytes, the levels of gdf9 mRNA were higher than those of bmp15 , which can be explained by its critical role during early stages of follicular development, specifically during recruitment [ 16 ]. Furthermore, this observation supports the hypotheses for European sea bass where it has been suggested that gdf9 expression appears not to be regulated by gonadotropins [ 37 ]. By contrast, spawned eggs showed higher levels of bmp15 mRNA in comparison with gdf9 expression, which agree with the principal role proposed for bmp15 in zebrafish, in maintaining egg quality and preventing ovulation of an immature oocyte [ 23 ].…”

Section: Discussionsupporting

confidence: 89%

Growth differentiation factor 9 and bone morphogenetic protein 15 expression in previtellogenic oocytes and during early embryonic development of Yellow-tail Kingfish Seriola lalandi

et al. 2014

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BackgroundDuring fish oocyte maturation, specific molecules are expressed and accumulated within oocyte until fertilization and embryo development. Special attention have been paid in members of the transforming growth factor (TGF-β) superfamily; growth differentiation factor 9 (GDF9/gdf9) and bone morphogenetic protein 15 (BMP15/bmp15), which exert regulatory functions during oocyte maturation and follicle development. However, little attention has been paid to the involvement of these molecules during embryogenesis considering its importance for the formation of a good quality egg and subsequent embryo survival. The purpose of this study was to analyze the expression of gdf9 and bmp15 in previtellogenic oocytes and during early embryonic development in Seriola lalandi, a pelagic fish with increasing prospect for its aquaculture development, which however, show high mortality at embryo and larval stages.ResultsThrough RT-qPCR it was found that gdf9 expression was higher in previtellogenic oocytes decreasing after ovulation. This expression profile agrees with its participation in early stages of the follicular development. The transcripts for bmp15 also showed the highest levels in previtellogenic oocytes, however this expression was lower than obtained with gdf9. Conversely, in recently spawned oocytes mRNA bmp15 levels were highest than observed to gdf9. This, is consequent with the main role proposed for this growth factor at the final fish oocyte maturation: avoid the ovulation of an immature oocyte. During embryo development, low levels of mRNA were detected to gdf9, with an increase in 48 H post-fertilization embryos. The bmp15 expression did not change throughout development and was higher than gdf9 at 16 cells, blastula and appearance embryos stages.ConclusionsBoth (gdf9 and bmp15) expression profiles in previtellogenic oocytes and newly spawned eggs are consistent with the described functions for these growth factors in vertebrate ovarian physiology in early and late stages of the follicular development. So, these genes could be considered as quality biomarkers at these stages. However, further studies of these proteins throughout folliculogenesis, are necessaries to fully understand their functions during the oocyte formation. In addition, the persistent expression of these growth factors during development, allows us to speculate possible roles in embryonic processes, which must also be addressed.

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Bone morphogenetic protein 15 and growth differentiation factor 9 expression in the ovary of European sea bass (Dicentrarchus labrax): Cellular localization, developmental profiles, and response to unilateral ovariectomy

Cited by 29 publications

References 61 publications

Conserved Anti-Müllerian Hormone: Anti-Müllerian Hormone Type-2 Receptor Specific Interaction and Intracellular Signaling in Teleosts1

Conserved Anti-Müllerian Hormone: Anti-Müllerian Hormone Type-2 Receptor Specific Interaction and Intracellular Signaling in Teleosts1

Bone morphogenetic protein 15 may promote follicle selection in the hen

Growth differentiation factor 9 and bone morphogenetic protein 15 expression in previtellogenic oocytes and during early embryonic development of Yellow-tail Kingfish Seriola lalandi

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