Embryotropic actions of follistatin: paracrine and autocrine mediators of oocyte competence and embryo developmental progression

Rajput, Sandeep; Lee, KyungBon; Guo, Zhenhua; Liu, Di; Folger, Joseph K.; Smith, George W.

doi:10.1071/rd13282

Cited by 19 publications

(21 citation statements)

References 120 publications

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“…BMP15 and GDF9) or associated growth factor binding proteins (e.g. follistatin) have been shown to regulate oocyte maturation and (or) early embryogenesis in cattle [10,28,29]. However, little is known about role of specific SMAD signaling pathways in regulation of early embryogenesis.…”

Section: Discussionmentioning

confidence: 98%

Evidence Supporting a Role for SMAD2/3 in Bovine Early Embryonic Development: Potential Implications for Embryotropic Actions of Follistatin1

Zhang

Rajput

Lee³

et al. 2015

Biology of Reproduction

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The TGF-beta-SMAD signaling pathway is involved in regulation of various aspects of female reproduction. However, the intrinsic functional role of SMADs in early embryogenesis remains poorly understood. Previously, we demonstrated that treatment with follistatin, an activin (TGF-beta superfamily ligand)-binding protein, is beneficial for bovine early embryogenesis and specific embryotropic actions of follistatin are dependent on SMAD4. Because SMAD4 is a common SMAD that can bind both SMAD2/3 and SMAD1/5, the objective of this study was to further determine the intrinsic role of SMAD2/3 in the control of early embryogenesis and delineate if embryotropic actions of follistatin in early embryos are SMAD2/3 dependent. By using a combination of pharmacological and small interfering RNA-mediated inhibition of SMAD2/3 signaling in the presence or absence of follistatin treatment, our results indicate that SMAD2 and SMAD3 are both required for bovine early embryonic development and stimulatory actions of follistatin on 8- to 16-cell and that blastocyst rates, but not early cleavage, are muted when SMAD2/3 signaling is inhibited. SMAD2 deficiency also results in reduced expression of the bovine trophectoderm cell-specific gene CTGF. In conclusion, the present work provides evidence supporting a functional role of SMAD2/3 in bovine early embryogenesis and that specific stimulatory actions of follistatin are not observed in the absence of SMAD2/3 signaling.

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Section: Discussionmentioning

confidence: 98%

Evidence Supporting a Role for SMAD2/3 in Bovine Early Embryonic Development: Potential Implications for Embryotropic Actions of Follistatin1

Zhang

Rajput

Lee³

et al. 2015

Biology of Reproduction

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“…Alternatively, if activin concentrations are altered in the preovulatory follicle, this could potentially affect oocyte quality or subsequent luteal function. Increased expression of FST by the oocyte has also been linked to enhanced oocyte quality as assessed by improved early embryo development (Rajput et al 2013). However, it should be noted that it is unclear if the positive effects of FST on oocyte quality and embryo development are due to neutralisation of activin as treatment with activin A mimicked FST actions, albeit with less potency (Rajput et al 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Increased expression of FST by the oocyte has also been linked to enhanced oocyte quality as assessed by improved early embryo development (Rajput et al 2013). However, it should be noted that it is unclear if the positive effects of FST on oocyte quality and embryo development are due to neutralisation of activin as treatment with activin A mimicked FST actions, albeit with less potency (Rajput et al 2013). A key pathway that may be affected by increased activin secretion is luteinisation of the granulosa cells and subsequent luteal function.…”

Section: Discussionmentioning

confidence: 99%

“…The activin pathway has been postulated to be involved in regulation of multiple reproductive processes including ovarian follicular development (Knight et al 2012), luteinisation of the follicular cells (Myers et al 2008, Kayani et al 2009), early embryo development (Rajput et al 2013) and uterine function during implantation of the conceptus (Singh et al 2011). As a member of the transforming growth factor beta superfamily of growth factors, activin forms from the dimerisation of two b-subunits of inhibin (INHB), with different combinations forming functionally different isoforms (Knight 1996, Mellor et al 2003.…”

Section: Introductionmentioning

confidence: 99%

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Activin A and follistatin during the oestrous cycle and early pregnancy in ewes

O’Connell¹,

McNatty²,

Hurst³

et al. 2016

Journal of Endocrinology

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The activin pathway has been postulated to be involved in regulation of multiple reproductive processes important for survival of the conceptus. These processes include luteinisation of the follicular cells and thus function of the corpus luteum, early embryo development and uterine function including implantation of the conceptus. Therefore, the aim of the current study was to determine whether the concentrations of activin A and follistatin (FST), an activin-binding protein, differed between ewes with a lifetime history of enhanced or reduced embryonic survival (ES). The mRNAs encoding FST and activin A (inhibin beta A subunit; INHBA) were present in the uterus and abundant in the uterine luminal or glandular epithelia by day 18 of gestation. A peak of activin A was observed in the systemic circulation around the time of oestrus, and activin A concentrations were elevated in animals with reduced ES during the oestrous cycle and early gestation. Concentrations of activin A in uterine fluid were approximately twofold greater on day 16 of gestation in ewes with reduced ES compared to those with enhanced ES. No consistent differences in FST were observed between these groups. Treatment of luteinising ovine granulosa cells with activin A in vitro suppressed progesterone secretion providing evidence of a potential pathway whereby increased concentrations of activin A may decrease ES.

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“…In mammals, oocytes specific genes play a key role in regulation of the reproductive process and are critical to both ovarian folliculogenesis and early embryogenesis (Rajput et al 2013). The products of these genes which are expressed, stored and secreted during oogenesis control the follicular microenvironment and promote oocyte competence for successful fertilization and subsequent embryonic development (De Sousa et al 1998).…”

Section: Introductionmentioning

confidence: 99%

Requirement of the transcription factor USF1 in bovine oocyte and early embryonic development

et al. 2015

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Upstream stimulating factor 1 (USF1) is a basic helix loop helix transcription factor that specifically binds to E-box DNA motifs, known cis-elements of key oocyte expressed genes essential for oocyte and early embryo development. However, the functional and regulatory role of USF1 in bovine oocyte and embryo development is not understood. In this study, we demonstrated that USF1 mRNA is maternal in origin and expressed in a stage specific manner during the course of oocyte maturation and preimplantation embryonic development. Immunocytochemical analysis showed detectable USF1 protein during oocyte maturation and early embryonic development with increased abundance at 8–16 cell stage of embryo development, suggesting a potential role in embryonic genome activation. Knockdown of USF1 in germinal vesicle stage oocytes did not impact meiotic maturation or cumulus expansion, but caused significant changes in mRNA abundance for genes associated with oocyte developmental competence. Furthermore, siRNA mediated depletion of USF1 in presumptive zygote stage embryos demonstrated that USF1 is required for early embryonic development to the blastocyst stage. A similar (USF2) yet unique (TWIST2) expression pattern during oocyte and early embryonic development for related E-box binding transcription factors known to cooperatively bind USF1 suggest a potential link to USF1 action. This study demonstrates that USF1 is a maternally derived transcription factor required for bovine early embryonic development which also functions in regulation of JY-1, GDF9 and FST genes associated with oocyte competence.

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Embryotropic actions of follistatin: paracrine and autocrine mediators of oocyte competence and embryo developmental progression

Cited by 19 publications

References 120 publications

Evidence Supporting a Role for SMAD2/3 in Bovine Early Embryonic Development: Potential Implications for Embryotropic Actions of Follistatin1

Evidence Supporting a Role for SMAD2/3 in Bovine Early Embryonic Development: Potential Implications for Embryotropic Actions of Follistatin1

Activin A and follistatin during the oestrous cycle and early pregnancy in ewes

Requirement of the transcription factor USF1 in bovine oocyte and early embryonic development

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