Spatiotemporal Expression of Bone Morphogenetic Protein Family Ligands and Receptors in the Zebrafish Ovary: A Potential Paracrine-Signaling Mechanism for Oocyte-Follicle Cell Communication

• Published in: Biology of reproduction Vol. 85; no. 5; pp. 977 - 986
• Main Authors: WUN LI, Cheuk, WEI GE
• Format: Journal Article
• Language: English
• Published: Madison, WI Society for the Study of Reproduction 01-11-2011
• Subjects: Animals; Biological and medical sciences; Bone Morphogenetic Protein 2 - metabolism; Bone Morphogenetic Protein 4 - metabolism; Bone Morphogenetic Protein Receptors - metabolism; Cell Communication - physiology; Cells, Cultured; Danio rerio; Female; Freshwater; Fundamental and applied biological sciences. Psychology; Ligands; Models, Animal; Oocytes - cytology; Oocytes - physiology; Ovarian Follicle - cytology; Ovarian Follicle - physiology; Ovary - metabolism; Paracrine Communication - physiology; Phosphorylation; Phylogeny; Smad Proteins - metabolism; Teleostei; Tissue Distribution; Vertebrates: reproduction; Zebrafish - metabolism; Zebrafish Proteins - metabolism; Folliculogenesis; Ligand; bone morphogenetic protein (BMP); Germinal cell; Ovary; Signal transduction; Reproduction; follicular development; Bone morphogenetic protein; Female genital system; Development; zebrafish; Oocyte; Biological receptor
• ISSN: 0006-3363; 1529-7268
• DOI: 10.1095/biolreprod.111.092239

The bone morphogenetic proteins (BMPs), originally identified by their abilities to induce bone and/or cartilage formation, have been reported to be involved in various growth and differentiation processes, including reproduction. Although mammalian models are more frequently used to study the BMP system in reproduction, we have extended the study to the zebrafish, an excellent model for studying female reproduction in teleosts. Reverse transcription-PCR analysis revealed the expression of the Bmp ligands (bmp2a, bmp2b, bmp4, bmp6, and bmp7a) and the type II Bmp receptors (bmpr2a and bmpr2b) in various tissues, including the ovary. Spatiotemporal distribution of these Bmp ligands and receptors in the ovary was then investigated in this study. Reverse transcription-PCR on isolated follicle layers and denuded oocytes demonstrated that all Bmp ligands examined were exclusively or abundantly expressed in the oocyte, whereas the two receptors were expressed exclusively in the follicle layers, strongly suggesting a potential paracrine signaling from the oocyte towards the follicle layer by various Bmp ligands. This supports the current view that instead of being passively controlled and nurtured by the follicle layer for its growth and development, the oocyte may play an active role by releasing various growth differentiation factors to regulate follicle layer function. Quantitative analysis of temporal expression profiles during folliculogenesis revealed an increased expression of bmp2a, bmp2b, bmp4, and bmp6 from primary growth (stage I) to previtellogenic (stage II) stages, followed by steady declines toward the end of folliculogenesis when the follicles became fully grown. On the contrast, the BMP receptors (bmpr2a and bmpr2b) consistently showed an increase in expression during folliculogenesis, with the peak levels reached at the full-grown stage prior to final oocyte maturation. The spatiotemporal expression patterns of the Bmp family in the zebrafish follicles provide important insights into potential roles for Bmps during follicle development as oocyte-derived factors. Further experiments using recombinant zebrafish Bmp4 showed that Bmp4 had an inhibitory effect on spontaneous oocyte maturation in vitro, but not 17alpha,20beta-dihydroxy-4-pregnen-3-one (DHP)-induced oocyte maturation in vitro.