Expression Patterns and Gonadotropin Regulation of the TGF-β II Receptor (Bmpr2) during Ovarian Development in the Ricefield Eel Monopterus albus

Bmpr2 plays a central role in the regulation of reproductive development in mammals, but its role during ovarian development in fish is still unclear. To ascertain the function of bmpr2 in ovarian development in the ricefield eel, we isolated and characterized the bmpr2 cDNA sequence; the localization of Bmpr2 protein was determined by immunohistochemical staining; and the expression patterns of bmpr2 in ovarian tissue incubated with FSH and hCG in vitro were analyzed. The full-length bmpr2 cDNA was 3311 bp, with 1061 amino acids encoded. Compared to other tissues, bmpr2 was abundantly expressed in the ovary and highly expressed in the early yolk accumulation (EV) stages of the ovary. In addition, a positive signal for Bmpr2 was detected in the cytoplasm of oocytes in primary growth (PG) and EV stages. In vitro, the expression level of gdf9, the ligand of bmpr2, in the 10 ng/mL FSH treatment group was significantly higher after incubation for 4 h than after incubation for different durations. However, bmpr2 expression in the 10 ng/mL FSH treatment group at 2 h, 4 h and 10 h was significantly lower. Importantly, the expression level of bmpr2 and gdf9 in the 100 IU/mL hCG group had similar changes that were significantly decreased at 4 h and 10 h. In summary, Bmpr2 might play a pivotal role in ovarian growth in the ricefield eel, and these results provide a better understanding of the function of bmpr2 in ovarian development and the basic data for further exploration of the regulatory mechanism of gdf9 in oocyte development.

[1]  Deying Yang,et al.  Estradiol Upregulates the Expression of the TGF-β Receptors ALK5 and BMPR2 during the Gonadal Development of Schizothorax prenanti , 2021, Animals : an open access journal from MDPI.

[2]  Sudhir Kumar,et al.  MEGA11: Molecular Evolutionary Genetics Analysis Version 11 , 2021, Molecular biology and evolution.

[3]  Peer Bork,et al.  SMART: recent updates, new developments and status in 2020 , 2020, Nucleic Acids Res..

[4]  A. Kowalska,et al.  Comparison of responses to artificial spawning of ruffe (Gymnocephalus cernua) specimens captured from their natural habitat to those produced in cultured conditions. , 2020, Animal reproduction science.

[5]  A. Falahati,et al.  Spatiotemporal expression of activin receptor-like kinase-5 and bone morphogenetic protein receptor type II in the ovary of shortfinned eel, Anguilla australis. , 2020, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[6]  D. Kucharczyk,et al.  Comparison of artificial spawning effectiveness of hCG, CPH and GnRHa in combination with dopamine inhibitors in a wild strain of ide Leuciscus idus (L.) in hatchery conditions. , 2020, Animal reproduction science.

[7]  Haiyang Yu,et al.  Growth differentiation factor 9 (gdf9) and bone morphogenetic protein 15 (bmp15) are potential intraovarian regulators of steroidogenesis in Japanese flounder (Paralichthys olivaceus). , 2020, General and comparative endocrinology.

[8]  Deying Yang,et al.  Expression and regulation of Smad2 by gonadotropins in the protogynous hermaphroditic ricefield eel (Monopterus albus) , 2020, Fish Physiology and Biochemistry.

[9]  Hiroshi I. Suzuki,et al.  TGF-β Signaling in Cellular Senescence and Aging-Related Pathology , 2019, International journal of molecular sciences.

[10]  M. Sarkar,et al.  Transcriptional and translational abundance of Bone morphogenetic protein (BMP) 2, 4, 6, 7 and their receptors BMPR1A, 1B and BMPR2 in buffalo ovarian follicle and the role of BMP4 and BMP7 on estrogen production and survival of cultured granulosa cells. , 2018, Research in veterinary science.

[11]  Yulan Chu,et al.  The role of FSH and TGF-β superfamily in follicle atresia , 2018, Aging.

[12]  J. Lim,et al.  Clinical significance linked to functional defects in bone morphogenetic protein type 2 receptor, BMPR2 , 2017, BMB reports.

[13]  P. Johnson,et al.  Bone morphogenetic protein 15 may promote follicle selection in the hen. , 2016, General and comparative endocrinology.

[14]  E. Kistanova,et al.  Tribulus terrestris Alters the Expression of Growth Differentiation Factor 9 and Bone Morphogenetic Protein 15 in Rabbit Ovaries of Mothers and F1 Female Offspring , 2016, PloS one.

[15]  Patricia A. Johnson,et al.  The domestic chicken: Causes and consequences of an egg a day. , 2015, Poultry science.

[16]  T. Iwanaga,et al.  Bone morphogenetic proteins are mediators of luteolysis in the human corpus luteum. , 2015, Endocrinology.

[17]  D. Kucharczyk,et al.  Changes in European eel ovary development and body and ovary chemistry during stimulated maturation under controlled conditions: preliminary data , 2014, Aquaculture International.

[18]  W. Guo,et al.  Reference gene selection for real-time RT-PCR normalization in rice field eel (Monopterus albus) during gonad development , 2014, Fish Physiology and Biochemistry.

[19]  S. Sealfon,et al.  Growth Differentiation Factor 9 (GDF9) Forms an Incoherent Feed-forward Loop Modulating Follicle-stimulating Hormone β-Subunit (FSHβ) Gene Expression* , 2014, The Journal of Biological Chemistry.

[20]  S. Franks,et al.  Expression of TGF-beta superfamily growth factors, their receptors, the associated SMADs and antagonists in five isolated size-matched populations of pre-antral follicles from normal human ovaries. , 2014, Molecular human reproduction.

[21]  J. Morera,et al.  BMP system expression in GCs from polycystic ovary syndrome women and the in vitro effects of BMP4, BMP6, and BMP7 on GC steroidogenesis. , 2013, European journal of endocrinology.

[22]  Johan Smitz,et al.  Molecular control of oogenesis. , 2012, Biochimica et biophysica acta.

[23]  Zhi He,et al.  Growth differentiation factor 9 (Gdf9) was localized in the female as well as male germ cells in a protogynous hermaphroditic teleost fish, ricefield eel Monopterus albus. , 2012, General and comparative endocrinology.

[24]  E. De Ponti,et al.  Cumulus cell-oocyte complexes retrieved from antral follicles in IVM cycles: relationship between COCs morphology, gonadotropin priming and clinical outcome , 2012, Journal of Assisted Reproduction and Genetics.

[25]  John A. Phillips III,et al.  BMPR2 expression is suppressed by signaling through the estrogen receptor , 2012, Biology of Sex Differences.

[26]  W. Ge,et al.  Spatiotemporal Expression of Bone Morphogenetic Protein Family Ligands and Receptors in the Zebrafish Ovary: A Potential Paracrine-Signaling Mechanism for Oocyte-Follicle Cell Communication1 , 2011, Biology of reproduction.

[27]  Anne Poupon,et al.  Mapping the Follicle-Stimulating Hormone-Induced Signaling Networks , 2011, Front. Endocrin..

[28]  M. Hosoe,et al.  Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries , 2011, Reproductive biology and endocrinology : RB&E.

[29]  L. Cheng,et al.  Expression of GDF-9, BMP-15 and their receptors in mammalian ovary follicles , 2010, Journal of Molecular Histology.

[30]  B. Vanderhyden,et al.  Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. , 2010, Canadian journal of physiology and pharmacology.

[31]  N. Sakuragi,et al.  Growth differentiation factor-9 mediates follicle-stimulating hormone-thyroid hormone interaction in the regulation of rat preantral follicular development. , 2009, Endocrinology.

[32]  P. Knaus,et al.  Recent advances in BMP receptor signaling. , 2009, Cytokine & growth factor reviews.

[33]  Martin M Matzuk,et al.  The mammalian ovary from genesis to revelation. , 2009, Endocrine reviews.

[34]  G. Murdoch,et al.  Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. , 2009, Reproduction.

[35]  Z. Wang,et al.  Stage-specific expression of bone morphogenetic protein type I and type II receptor genes: Effects of follicle-stimulating hormone on ovine antral follicles. , 2009, Animal reproduction science.

[36]  C. Hill,et al.  Tgf-beta superfamily signaling in embryonic development and homeostasis. , 2009, Developmental cell.

[37]  B. Fisch,et al.  Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. , 2008, Fertility and sterility.

[38]  Y. Mu,et al.  Expression of bone morphogenetic proteins and receptors in porcine cumulus-oocyte complexes during in vitro maturation. , 2008, Animal reproduction science.

[39]  C. Mummery,et al.  Two novel type II receptors mediate BMP signalling and are required to establish left-right asymmetry in zebrafish. , 2008, Developmental biology.

[40]  Patricia A Hunt,et al.  Human female meiosis: what makes a good egg go bad? , 2008, Trends in genetics : TIG.

[41]  J. Juengel,et al.  Patterns of Expression of Messenger RNAs Encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 During Follicular Development and Characterization of Ovarian Follicular Populations in Ewes Carrying the Woodlands FecX2W Mutation1 , 2007, Biology of reproduction.

[42]  Bernhard Schmierer,et al.  TGFβ–SMAD signal transduction: molecular specificity and functional flexibility , 2007, Nature Reviews Molecular Cell Biology.

[43]  W. Ge,et al.  Growth Differentiation Factor 9 and Its Spatiotemporal Expression and Regulation in the Zebrafish Ovary1 , 2007, Biology of reproduction.

[44]  B. Tsang,et al.  Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage. , 2006, Molecular endocrinology.

[45]  Phil G Knight,et al.  TGF-beta superfamily members and ovarian follicle development. , 2006, Reproduction.

[46]  Takashi Shimizu,et al.  Hormonal regulation of expression of growth differentiation factor-9 receptor type I and II genes in the bovine ovarian follicle. , 2006, Reproduction.

[47]  W. Ge,et al.  Cloning of Smad2, Smad3, Smad4, and Smad7 from the goldfish pituitary and evidence for their involvement in activin regulation of goldfish FSHbeta promoter activity. , 2005, General and comparative endocrinology.

[48]  J. R. Figueiredo,et al.  Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats , 2005, Molecular reproduction and development.

[49]  M. Matzuk,et al.  Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. , 2004, Human reproduction.

[50]  H. Lankinen,et al.  Immunoneutralization of Growth Differentiation Factor 9 Reveals It Partially Accounts for Mouse Oocyte Mitogenic Activity1 , 2004, Biology of reproduction.

[51]  M. Hunter,et al.  Immunohistochemical localization of the bone morphogenetic protein receptors in the porcine ovary , 2004, Journal of anatomy.

[52]  S. Roy,et al.  Growth Differentiation Factor-9 and Stem Cell Factor Promote Primordial Follicle Formation in the Hamster: Modulation by Follicle-Stimulating Hormone1 , 2004, Biology of reproduction.

[53]  A. Hsueh,et al.  Growth differentiation factor-9 signaling in the ovary , 2003, Molecular and Cellular Endocrinology.

[54]  S. Shimasaki,et al.  Reproductive Biology and Endocrinology Open Access the Spatiotemporal Expression Pattern of the Bone Morphogenetic Protein Family in Rat Ovary Cell Types during the Estrous Cycle , 2022 .

[55]  J. Juengel,et al.  Growth Differentiation Factor 9 and Bone Morphogenetic Protein 15 Are Essential for Ovarian Follicular Development in Sheep1 , 2002, Biology of reproduction.

[56]  U. Vitt,et al.  Bone Morphogenetic Protein Receptor Type II Is a Receptor for Growth Differentiation Factor-91 , 2002, Biology of reproduction.

[57]  B. Campbell,et al.  Effect of bone morphogenetic protein 2 (BMP2) on oestradiol and inhibin A production by sheep granulosa cells, and localization of BMP receptors in the ovary by immunohistochemistry. , 2002, Reproduction.

[58]  W. Ge,et al.  Gonadotropin regulation of activin βA and activin type IIA receptor expression in the ovarian follicle cells of the zebrafish, Danio rerio , 2002, Molecular and Cellular Endocrinology.

[59]  B. Gülekli,et al.  In vitro maturation and fertilization of oocytes from unstimulated normal ovaries, polycystic ovaries, and women with polycystic ovary syndrome. , 2001, Fertility and sterility.

[60]  Shin Yamamoto,et al.  Bone Morphogenetic Protein-15 Inhibits Follicle-stimulating Hormone (FSH) Action by Suppressing FSH Receptor Expression* , 2001, The Journal of Biological Chemistry.

[61]  J. Trant,et al.  Molecular Biology of Channel Catfish Gonadotropin Receptors: 1. Cloning of a Functional Luteinizing Hormone Receptor and Preovulatory Induction of Gene Expression1 , 2001, Biology of reproduction.

[62]  David F. Albertini,et al.  Growth differentiation factor-9 is required during early ovarian folliculogenesis , 1996, Nature.

[63]  S. McGrath,et al.  Oocyte-specific expression of growth/differentiation factor-9. , 1995, Molecular endocrinology.

[64]  G. J. Van Der Kraak Role of calcium in the control of steroidogenesis in preovulatory ovarian follicles of the goldfish. , 1991, General and comparative endocrinology.

[65]  D. O. Norris,et al.  Effects of mammalian gonadotropins (LH, FSH, HCG) and gonadal steroids on TSH-induced metamorphosis of Ambystoma tigrinum (Amphibia: Caudata). , 1973, General and comparative endocrinology.