Bone morphogenetic protein 6 promotes FSH receptor and anti-Müllerian hormone mRNA expression in granulosa cells from hen prehierarchal follicles

Ocón-Grove, Olga M.; Poole, Daniel; Johnson, A. L.

doi:10.1530/rep-11-0271

Cited by 65 publications

(50 citation statements)

References 35 publications

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“…During a second phase of growth, a subpopulation of follicles increases to a diameter of 3-8 mm. This development, and in particular FSHR expression within the granulosa, is regulated by a variety of growth factors in a positive (BMP4 and BMP6) or negative (epidermal growth factor receptor ligands; EGFRLs) fashion (31,32). In mammals, AMH reportedly reduces "FSH responsiveness" in small growing follicles.…”

Section: Follicular Development At Sexual Maturationmentioning

confidence: 99%

The avian ovary and follicle development: some comparative and practical insights

Johnson¹

2014

Turk J Vet Anim Sci

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This review focuses on recent research related to the avian ovary and, in particular, cellular mechanisms mediating embryonic growth of the ovary, postembryonic follicular development, and the process of follicular selection. Attention is drawn to a variety of fundamental, yet unresolved, aspects of ovarian function, several of which are uniquely related to avian reproductive strategies. Some notable differences in ovarian function between birds and the most closely related extant group, the crocodilians, are illustrated. Moreover, because the sauropsid (reptilian and avian) and synapsid (mammalian) lineages diverged shortly after the emergence of amniotes some 340 million years ago, consideration is given to both derived and convergent characteristics of ovarian function in avian species versus those in eutherian mammals. Two examples of divergent characteristics are the differences in sex-determining mechanisms between birds and mammals and the requirement for progesterone synthesized within the follicular granulosa as a requirement for ovulation in virtually all species of birds, compared to the site of synthesis and role for estradiol in mammals. As an example of a convergent process, both birds and select mammals (e.g., humans, cattle, and horses) typically ovulate a single egg per reproductive cycle, yet the processes associated with follicular selection occur via unique mechanisms. Finally, reference is made to several practical outcomes from studies of the avian ovary, including applications within the poultry industry and use of the domestic hen ovary as a model for human ovarian cancer.

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Section: Follicular Development At Sexual Maturationmentioning

confidence: 99%

The avian ovary and follicle development: some comparative and practical insights

Johnson¹

2014

Turk J Vet Anim Sci

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“…Granulosa cells (approximately 500 000 cells per well) from 6-to 8-mm follicles or the second largest (F2) follicle were preplated for 3-4 h at 408C in an atmosphere of 95% air: 5% CO 2 in 12-well polystyrene culture plates (Beckton Dickinson) containing 1 ml of complete medium, which consisted of Dulbecco modified Eagle medium/high glucose (DMEM; Thermo Scientific HyClone) containing 2.5% FBS (PAA Laboratories), 0.1 mM nonessential amino acids (Invitrogen), plus 1% antibioticantimycotic mixture (Invitrogen). In initial experiments, granulosa cells were cultured with complete medium in the absence or presence of BMP4 for 23 h and then challenged (after replacement with fresh medium) with 10 ng FSH/ml [15] for 1 h (for cAMP) or 3 h (for P4). In follow-up studies, NOGGIN (100 ng/ ml) [15] or TGFa (10 ng/ml) was added 1 h prior to BMP4.…”

Section: Granulosa Cell Culturesmentioning

confidence: 99%

“…In initial experiments, granulosa cells were cultured with complete medium in the absence or presence of BMP4 for 23 h and then challenged (after replacement with fresh medium) with 10 ng FSH/ml [15] for 1 h (for cAMP) or 3 h (for P4). In follow-up studies, NOGGIN (100 ng/ ml) [15] or TGFa (10 ng/ml) was added 1 h prior to BMP4. In addition, 1-h incubations were conducted with freshly collected granulosa cells from 6-to 8-mm follicles to measure FSH-induced cAMP.…”

Section: Granulosa Cell Culturesmentioning

confidence: 99%

“…These factors include TGFb [2,13] and activin A [2,13,14]. In addition, bone morphogenetic protein 6 (BMP6) was found to promote FSHR expression following 24 h of culture, and this resulted in the acquisition of FSH responsiveness plus the initiation of granulosa cell differentiation [15]. Treatment with vitamin D was also found to increase FSHR expression; however, that effect may be indirectly attributed to an inhibition of antiMullerian hormone (AMH) activity [16].…”

Section: Introductionmentioning

confidence: 99%

“…In this regard, BMP2 was found to suppress TGFb1-induced FSHR expression, and this inhibitory effect was attributed to enhanced epidermal growth factor receptor ligand (EGFRL) expression and inhibitory MAPK signaling [19]. Moreover, AMH has been implicated in restricting early follicle development and FSHR expression [20,21], yet perhaps paradoxically, BMP6 was found to enhance AMH expression [15]. Accordingly, it has been proposed that prior to selection, the maintenance of prehierarchal follicles requires a balance between multiple differentiation-inducing versus -inhibiting factors.…”

Section: Introductionmentioning

confidence: 99%

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Bone Morphogenetic Protein 4 Supports the Initial Differentiation of Hen (Gallus gallus) Granulosa Cells

Kim

Ocón-Grove

Johnson

2013

Biology of Reproduction

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In the hen ovary, selection of a follicle into the preovulatory hierarchy occurs from a small cohort of prehierarchal (6-8 mm) follicles. Prior to follicle selection the granulosa layer remains in an undifferentiated state despite elevated follicle-stimulating hormone receptor (FSHR) expression. The present studies describe a role for bone morphogenetic protein 4 (BMP4) in supporting FSHR mRNA expression in granulosa cells from prehierarchal follicles and promoting differentiation at follicle selection. Culture of undifferentiated granulosa cells in culture medium alone resulted in a significant decline in levels of FSHR mRNA (by ~80% compared to freshly collected cells). By comparison, granulosa cultured with BMP4 (10-100 ng/ml) maintained FSHR and expression at approximately in vivo levels. Because both granulosa and theca tissues from prehierarchal follicles express BMP4, it is suggested that BMP4 acts in a paracrine and/or autocrine fashion to support elevated FSHR expression prior to follicle selection. Granulosa cells cultured with BMP4 for 24 h also initiated FSH-induced cAMP production and indirectly initiated anti-Mullerian hormone (AMH), CYP11A, and STAR expression plus progesterone production. However, pretreatment with the BMP antagonist NOGGIN or the mitogen-activated protein kinase (MAPK) agonist transforming growth factor alpha attenuated or blocked each action promoted by BMP4. We conclude that prior to and immediately after selection, BMP4 serves to support FSHR expression within the granulosa layer, yet prior to selection, multiple factors (including inhibitory MAPK signaling, AMH, and BMP antagonists) can modulate FSHR expression and suppress FSH-mediated cell signaling to prevent granulosa cell differentiation prior to follicle selection.

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Implication of SLIT3‐ROBO1/ROBO2 in granulosa cell proliferation, differentiation and follicle selection in the prehierarchical follicles of hen ovary

Qin

et al. 2018

Cell Biology International

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The SLIT/ROBO pathway has been implicated in prehierarchical follicular development of hen ovary by an intrafollicular autocrine and/or paracrine fashion. SLIT3, one of the key components of the SLIT/ROBO family, serves as a ligand that potentially interacts with the four receptors, ROBO1, ROBO2, ROBO3 and ROBO4. But the exact roles and regulatory mechanism of SLIT3 in chicken ovarian follicle development remain largely unclear. The present study was conducted to investigate the potential roles and molecular regulation of SLIT3 in granulosa cell (GC) proliferation, differentiation and follicle selection within the prehierarchical follicles of hen ovary. We found that SLIT3 interacts physically with the four ROBO receptors, but the expression of the ROBO1 and ROBO2 genes are more susceptible to the regulation of SLIT3 ligand than that of the ROBO3 and ROBO4 genes. Moreover, the siRNA‐mediated knockdown of SLIT3 in the follicular GCs leads to a significant increase in cell proliferation. Conversely, overexpression of SLIT3 results in a remarkable reduction in GC proliferation. Furthermore, the overexpressed SLIT3 has notably decreased the mRNA and protein expression levels of follicle‐stimulating hormone (FSHR), growth and differentiation factor 9 (GDF9), steroidogenic acute regulatory protein (STAR) and cytochrome P450 11A1 (CYP11A1) in the GCs. These results indicated that SLIT3 may play an inhibitory effect on GC proliferation, differentiation and follicle selection, and these suppressive actions of SLIT3 in the GC proliferation can be prohibited by the siRNA‐mediated knockdown of ROBO1 and ROBO2 receptors. The current data provide a basis for further investigation of molecular mechanisms of SLIT3‐ROBO1/2 pathway in controlling the prehierarchical follicle development of the hen ovary.

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Bone morphogenetic protein 6 promotes FSH receptor and anti-Müllerian hormone mRNA expression in granulosa cells from hen prehierarchal follicles

Cited by 65 publications

References 35 publications

The avian ovary and follicle development: some comparative and practical insights

The avian ovary and follicle development: some comparative and practical insights

Bone Morphogenetic Protein 4 Supports the Initial Differentiation of Hen (Gallus gallus) Granulosa Cells

Implication of SLIT3‐ROBO1/ROBO2 in granulosa cell proliferation, differentiation and follicle selection in the prehierarchical follicles of hen ovary

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