MicroRNA-10b suppresses goat granulosa cell proliferation by targeting brain-derived neurotropic factor

Peng, Jian; An, Xiaoya; Fěng, Fang; Gao, Kun; Xin, Haiyun; Han, Peng; Bao, Lijuan; Ma, Haidong

doi:10.1016/j.domaniend.2015.09.005

Cited by 24 publications

(10 citation statements)

References 37 publications

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“…It was also reported that miR-10 could repress proliferation in porcine granulosa cells19. However, the function of the miR-10 family is still unknown in other species, such as humans, mice and rats.…”

Section: Resultsmentioning

confidence: 99%

Conserved miR-10 family represses proliferation and induces apoptosis in ovarian granulosa cells

Yang

Cheung

et al. 2017

Sci Rep

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Granulosa cells (GCs) are essential somatic cells in the ovary and play an important role in folliculogenesis. Brain-derived neurotropic factor (BDNF) and the TGF-β pathway have been identified as a critical hormone and signalling pathway, respectively, in GCs. In this study, we found that a conserved microRNA family that includes miR-10a and miR-10b repressed proliferation and induced apoptosis in human, mouse, and rat GCs (hGCs, mGCs and rGCs, respectively). Moreover, essential hormones and growth factors in the follicle, such as FSH, FGF9 and some ligands in the TGF-β pathway (TGFβ1, Activin A, BMP4 and BMP15), inhibited miR-10a and miR-10b expression in GCs. In contrast, the miR-10 family suppressed many key genes in the TGF-β pathway, suggesting a negative feedback loop between the miR-10 family and the TGF-β pathway in GCs. By using bioinformatics approaches, RNA-seq, qPCR, FISH, immunofluorescence, Western blot and luciferase reporter assays, BDNF was identified as a direct target of the miR-10 family in GCs. Additionally, reintroduction of BDNF rescued the effects of miR-10a and miR-10b in GCs. Collectively, miR-10a and miR-10b repressed GC development during folliculogenesis by repressing BDNF and the TGF-β pathway. These effects by the miR-10 family on GCs are conserved among different species.

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Section: Resultsmentioning

confidence: 99%

Conserved miR-10 family represses proliferation and induces apoptosis in ovarian granulosa cells

Yang

Cheung

et al. 2017

Sci Rep

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“…miRs are gene expression modulators and act at the posttranscriptional level to control protein production of target genes [27, 28]. miR-10b targets the cognition network gene BDNF and is negatively correlated with BDNF levels [53, 54]. For example, Jiang and Zhu [55] have demonstrated that BDNF is a direct target of miR-10b and BDNF expression negatively correlates with the expression of miR-10b in rat hippocampus under chronic stress depression induced by sleep deprivation.…”

Section: Discussionmentioning

confidence: 99%

Adverse Maternal Environment Alters MicroRNA-10b-5p Expression and Its Epigenetic Profile Concurrently with Impaired Hippocampal Neurogenesis in Male Mouse Hippocampus

Ke¹,

Huang²,

Fu³

et al. 2021

Dev Neurosci

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An adverse maternal environment (AME) predisposes adult offspring toward cognitive impairment in humans and mice. However, the underlying mechanisms remain poorly understood. Epigenetic changes in response to environmental exposure may be critical drivers of this change. Epigenetic regulators, including microRNAs, have been shown to affect cognitive function by altering hippocampal neurogenesis which is regulated in part by brain-derived neurotropic factor (BDNF). We sought to investigate the effects of AME on miR profile and their epigenetic characteristics, as well as neurogenesis and BDNF expression in mouse hippocampus. Using our mouse model of AME which is composed of maternal Western diet and prenatal environmental stress, we found that AME significantly increased hippocampal miR-10b-5p levels. We also found that AME significantly decreased DNA methylation and increased accumulations of active histone marks H3 lysine (K) 4me3, H3K14ac, and H3K36me3 at miR-10b promoter. Furthermore, AME significantly decreased hippocampal neurogenesis by decreasing cell numbers of Ki67+ (proliferation marker), NeuroD1+ (neuronal differentiation marker), and NeuN+ (mature neuronal marker) in the dentate gyrus (DG) region concurrently with decreased hippocampal BDNF protein levels. We speculate that the changes in epigenetic profile at miR-10b promoter may contribute to upregulation of miR-10b-5p and subsequently lead to decreased BDNF levels in a model of impaired offspring hippocampal neurogenesis and cognition in mice.

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“…One of those, miR-10b, was previously shown to be expressed in bovine embryos (Goossens et al, 2013), oocytes (Abd El Naby et al, 2013), follicles, and ovarian tissues (Huang et al, 2011; Gebremedhn et al, 2015). Several studies have shown that miR-10b plays important roles in cell apoptosis, cell proliferation, cell migration, and invasion in human cancer cells (Wang et al, 2007; Liao et al, 2014; Chen et al, 2016; Zhen et al, 2016; Zhu et al, 2016; Guan et al, 2018), mouse cells (Tan et al, 2018), and goat granulosa cells (Peng et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…MiR-10b was also shown to be more abundant in the culture medium of degenerate embryos compared with that of blastocysts, and more abundant in the culture medium of slow-cleaving embryos compared with that of intermediate-cleaving embryos, indicating that overexpression of miR-10b has a negative influence on preimplantation embryo development in cattle (Lin et al, 2019). Previously, miR-10b has been shown to regulate cell invasion, apoptosis, viability, and migration in multiple cell lines in human, mouse, and goat (Chen et al, 2016; Li et al, 2016; Peng et al, 2016; Zhen et al, 2016; Zhu et al, 2016; Tan et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Bta-miR-10b Secreted by Bovine Embryos Negatively Impacts Preimplantation Embryo Quality

et al. 2019

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In a previous study, we found miR-10b to be more abundant in a conditioned culture medium of degenerate embryos compared to that of blastocysts. Here, we show that miR-10b mimics added to the culture medium can be taken up by embryos. This uptake results in an increase in embryonic cell apoptosis and aberrant expression of DNA methyltransferases ( DNMTs ). Using several algorithms, Homeobox A1 ( HOXA1 ) was identified as one of the potential miR-10b target genes and dual-luciferase assay confirmed HOXA1 as a direct target of miR-10b. Microinjection of si- HOXA1 into embryos also resulted in an increase in embryonic cell apoptosis and downregulation of DNMTs . Cell progression analysis using Madin–Darby bovine kidney cells (MDBKs) showed that miR-10b overexpression and HOXA1 knockdown results in suppressed cell cycle progression and decreased cell viability. Overall, this work demonstrates that miR-10b negatively influences embryo quality and might do this through targeting HOXA1 and/or influencing DNA methylation.

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MicroRNA-10b suppresses goat granulosa cell proliferation by targeting brain-derived neurotropic factor

Cited by 24 publications

References 37 publications

Conserved miR-10 family represses proliferation and induces apoptosis in ovarian granulosa cells

Conserved miR-10 family represses proliferation and induces apoptosis in ovarian granulosa cells

Adverse Maternal Environment Alters MicroRNA-10b-5p Expression and Its Epigenetic Profile Concurrently with Impaired Hippocampal Neurogenesis in Male Mouse Hippocampus

Bta-miR-10b Secreted by Bovine Embryos Negatively Impacts Preimplantation Embryo Quality

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