Dynamics of avian ovarian follicle development: Cellular mechanisms of granulosa cell differentiation

Johnson, A. L.; Woods, Dori C.

doi:10.1016/j.ygcen.2008.11.012

Cited by 163 publications

(129 citation statements)

References 35 publications

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“…These effects on ID expression are completely blocked by treatment with the selective MAP kinase/ERK inhibitor, U0126. We have recently provided evidence that changes in ID protein expression can modulate FSHR mRNA expression in undifferentiated granulosa cells (Johnson et al 2008a, Johnson & Woods 2009. In the present studies, BMP2 treatment was found to increase ID1, ID3, and ID4 expression (Fig.…”

Section: Discussionsupporting

confidence: 67%

“…using selective MAP kinase pathway inhibitors) promotes FSHR expression, and when combined with FSH treatment, potentiates FSHR expression plus promotes granulosa cell differentiation . Together, these findings have formed the basis of a working model predicting that active MAP kinase signaling precludes premature differentiation of granulosa cells in all prehierarchal follicles except the follicle destined for selection (Johnson & Woods 2009). Accordingly, granulosa cell differentiation associated with preovulatory follicle growth is proposed to occur only following selective release from inhibitory MAP kinase/ERK signaling.…”

Section: Introductionmentioning

confidence: 93%

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Bone morphogenetic protein 2 inhibits FSH responsiveness in hen granulosa cells

Haugen¹,

Johnson²

2010

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Prior to follicle selection into the preovulatory hierarchy, hen granulosa cells from prehierarchal follicles remain undifferentiated, as defined in part by the virtual absence of LHR mRNA expression and inability to produce progesterone. It has previously been proposed that prior to follicle selection, granulosa cells are actively maintained in an undifferentiated state by epidermal growth factor receptor ligands (EGFRL) signaling via the MAP kinase/extracellular regulated kinase pathway. Moreover, there is recent evidence that EGFRL/MAP kinase signaling modulates FSH receptor (FSHR) transcription, in part, via inhibitor of differentiation/DNA-binding (ID) proteins. In the present studies with undifferentiated granulosa, recombinant human (rh) bone morphogenetic protein 2 (BMP2) induced the phosphorylation of SMAD1/5/8, and blocked transforming growth factor b and FSH-induced FSHR expression and progesterone production. Significantly, BMP2 rapidly induced mRNAs encoding betacellulin and EGF, plus ID proteins (ID1, ID3, and ID4). Alternatively, the bioactivity of BMPs can be modulated by one or more BMP antagonists, including noggin (NOG). NOG mRNA is expressed by both hen granulosa and theca tissues from prehierarchal follicles. Pretreatment of cultured granulosa with rh NOG reversed both the stimulatory effects of BMP2 on ID1, ID3, and ID4 expression and the inhibitory effects of BMP2 on FSHR mRNA levels and progesterone production. Collectively, these data provide evidence that prior to follicle selection, BMP2 signaling contributes toward maintaining granulosa cells in an undifferentiated state. The actions of BMP2 are, at least in part, mediated indirectly via enhanced EGFRL expression and ERBB receptor-mediated MAP kinase signaling, and can be modulated by the autocrine/paracrine production of NOG.

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Section: Discussionsupporting

confidence: 67%

Section: Introductionmentioning

confidence: 93%

Bone morphogenetic protein 2 inhibits FSH responsiveness in hen granulosa cells

Haugen¹,

Johnson²

2010

Reproduction

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“…MAPK signaling (Johnson & Woods 2009). Together, the actions of EGFRL/MAPK signaling with the proposed inhibitory actions of AMH signaling on FSH responsiveness in hen granulosa cells may serve to regulate the process of follicle selection.…”

Section: Bmp6 Promotes Fshr and Amhmentioning

confidence: 99%

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

2012

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A growing body of literature provides evidence of a prominent role for bone morphogenetic proteins (BMPs) in regulating various stages of ovarian follicle development. Several actions for BMP6 have been previously reported in the hen ovary, yet only within postselection (preovulatory) follicles. The initial hypothesis tested herein is that BMP6 increases FSH receptor (FSHR) mRNA expression within the granulosa layer of prehierarchal (6-8 mm) follicles (6-8 GC). BMP6 mRNA is expressed at higher levels within undifferentiated (1-8 mm) follicles compared with selected (R9 mm) follicles. Recombinant human (rh) BMP6 initiates SMAD1, 5, 8 signaling in cultured 6-8 GC and promotes FSHR mRNA expression in a dose-related fashion. In addition, a 21 h preculture with rhBMP6 followed by a 3 h challenge with FSH increases cAMP accumulation, STAR (StAR) expression, and progesterone production. Interestingly, rhBMP6 also increases expression of anti-Mü llerian hormone (AMH) mRNA in cultured 6-8 GC. This related BMP family member has previously been implicated in negatively regulating FSH responsiveness during follicle development. Considering these data, we propose that among the paracrine and/or autocrine actions of BMP6 within prehierarchal follicles is the maintenance of both FSHR and AMH mRNA expression. We predict that before follicle selection, one action of AMH within granulosa cells from 6 to 8 mm follicles is to help suppress FSHR signaling and prevent premature granulosa cell differentiation. At the time of selection, we speculate that the yet undefined signal directly responsible for selection initiates FSH responsiveness. As a result, FSH signaling suppresses AMH expression and initiates the differentiation of granulosa within the selected follicle.

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“…The process of oocyte growth in the avian ovary is tightly associated with the functional differentiation of the granulosa and thecal layers of the maturing follicles [Johnson and Woods, 2009]. Additionally, there are alterations in the typically avian intra-ooplasmic, yolky Balbiani body (formerly called the 'yolk nucleus') of previtellogenic follicles until their material disperses to the outer periphery of the oocyte during later follicular development [Guraya, 1976].…”

Section: Introductionmentioning

confidence: 99%

Expression of Intermediate Filaments in the Balbiani Body and Ovarian Follicular Wall of the Japanese Quail <b><i>(Coturnix japonica)</i></b>

Rodler¹,

Sinowatz²

2013

Cells Tissues Organs

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In the present study, we examined the distribution of 6 groups of intermediate filaments (IFs; cytokeratins, CKs, vimentin, synemin, desmin, glial fibrillary acidic protein and lamins) in oocytes and follicular walls of the Japanese quail (Coturnix japonica) during their development using immunohistochemical and ultrastructural techniques. A distinctly vimentin- and synemin-positive Balbiani body, which is a transient accumulation of organelles (mitochondria, Golgi complex and endoplasmic reticulum) that occurs in the oocytes of all vertebrates including birds, could be detected in the oocytes of primordial and early pre-vitellogenic follicles. In larger pre-vitellogenic follicles, the Balbiani body has dispersed and the positivity of the granulosa cells appeared to concentrate in the basal portion of their cytoplasm. Our ultrastructural data demonstrated that the matrix of the Bal-biani body consists of fine IFs, which may play a role in the formation and dispersion of the Balbiani body. Of the CKs studied (panCK, CK5, CK7, CK8, CK14, CK15, CK18 and CK19), only CK5 showed a slight positive staining in both the theca externa and the Balbiani bodies of pre-vitellogenic oocytes. In conclusion, our data, which describe the changes in avian IF protein expression during folliculogenesis, suggest that the functions of the IFs (vimentin and synemin) of oocytes and follicular walls are not primarily mechanical but may be involved in the transient tethering of mitochondria in the area of the Balbiani body and in the gain of endocrine competence during the differentiation of granulosa cells.

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Dynamics of avian ovarian follicle development: Cellular mechanisms of granulosa cell differentiation

Cited by 163 publications

References 35 publications

Bone morphogenetic protein 2 inhibits FSH responsiveness in hen granulosa cells

Bone morphogenetic protein 2 inhibits FSH responsiveness in hen granulosa cells

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

Expression of Intermediate Filaments in the Balbiani Body and Ovarian Follicular Wall of the Japanese Quail <b><i>(Coturnix japonica)</i></b>

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