Follicle-stimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells

Yao, Nan; Yang, Baiqing; Liu, Yu; Tan, Xinyu; Lu, Cailing; Yuan, Xiaohui; Ma, Xu

doi:10.1007/s12020-010-9345-1

Cited by 88 publications

(75 citation statements)

References 42 publications

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“…Northern blotting analyses confirmed that these represented actual differences in tissue miRNA expression and therefore they are likely to play a role in the regulation of follicular differentiation. Interestingly, four of the nine miRNAs identified as being highly expressed in follicles were previously reported to be upregulated by FSH in rat granulosa cells whereas miR-21, which was expressed at low levels in sheep follicles, was downregulated by FSH (Yao et al 2010b). miRNAs and ovarian follicular differentiation Wang et al 2011), including roles in modulating inflammation, innate immunity and angiogenesis (Chen et al 2004, Otsuka et al 2008, Yamakuchi et al 2008, Liu et al 2009, Guo et al 2010, Jennewein et al 2010, Kuhn et al 2010, Sheedy et al 2010, Caporali et al 2011, Shatseva et al 2011, all of which are intrinsically associated with ovulation and early luteogenesis (Espey & Richards 2002).…”

Section: Discussionmentioning

confidence: 99%

Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary

McBride

Carré²,

Sontakke³

et al. 2012

Reproduction

166

152

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Little is known about the involvement of microRNAs (miRNAs) in the follicular-luteal transition. The aim of this study was to identify genome-wide changes in miRNAs associated with follicular differentiation in sheep. miRNA libraries were produced from samples collected at defined stages of the ovine oestrous cycle and representing healthy growing follicles, (diameter, 4.0-5.5 mm), pre-ovulatory follicles (6.0-7.0 mm), early corpora lutea (day 3 post-oestrus) and late corpora lutea (day 9). A total of 189 miRNAs reported in sheep or other species and an additional 23 novel miRNAs were identified by sequencing these libraries. miR-21, miR-125b, let-7a and let-7b were the most abundant miRNAs overall, accounting for 40% of all miRNAs sequenced. Examination of changes in cloning frequencies across development identified nine different miRNAs whose expression decreased in association with the follicular-luteal transition and eight miRNAs whose expression increased during this transition. Expression profiles were confirmed by northern analyses, and experimentally validated targets were identified using miRTarBase. A majority of the 29 targets identified represented genes known to be actively involved in regulating follicular differentiation in vivo. Finally, luteinisation of follicular cells in vitro resulted in changes in miRNA levels that were consistent with those identified in vivo, and these changes were temporally associated with changes in the levels of putative miRNA targets in granulosa cells. In conclusion, this is the first study to characterise genome-wide miRNA profiles during different stages of follicle and luteal development. Our data identify a subset of miRNAs that are potentially important regulators of the follicular-luteal transition.

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Section: Discussionmentioning

confidence: 99%

Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary

McBride

Carré²,

Sontakke³

et al. 2012

Reproduction

166

152

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“…Thus, miRNA-145 may not necessarily lead to the modulation of specific predicted functions or targets, but it has been reported to function as a regulator of cell proliferation and as a tumor suppressor (20,69,79,84). A number of studies have attempted to identify and characterize miRNAs in adrenal and gonadal tissues and cells (18,24,45,47,48,50,54,63,68,80,81,83), but information about their potential targets or hormonal regulation is generally lacking except in a few instances. For example, miRNA-378 has been reported to regulate estradiol production in porcine granulosa cells by targeting aromatase (47).…”

Section: Discussionmentioning

confidence: 99%

“…Using H295R human adrenocortical cells, it was shown that miRNA-21 increases aldosterone secretion and cell proliferation, although no specific target for this miRNA was reported (68). Very recently, Yao et al (81) reported that expression of a large number of miRNAs is either upregulated or downregulated in cultured rat granulosa cells in response to FSH stimulation. Surprisingly, the expression of both miRNA-125a-5p and miRNA125b-5p was found to be upregulated in response to 12 h of FSH treatment.…”

Section: Discussionmentioning

confidence: 99%

MicroRNAs 125a and 455 Repress Lipoprotein-Supported Steroidogenesis by Targeting Scavenger Receptor Class B Type I in Steroidogenic Cells

Shen

Kraemer

et al. 2012

Molecular and Cellular Biology

103

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We sought to identify and characterize microRNA (miRNAs) that posttranscriptionally regulate the expression of scavenger receptor class B type I (SR-BI) and SR-BI-linked selective high-density lipoprotein (HDL) cholesteryl ester (CE) transport and steroidogenesis. Four miRNAs (miRNA-125a, miRNA-125b, miRNA-145, and miRNA-455) with a potential to regulate SR-BI were identified in silico and validated by quantitative real-time PCR (qRT-PCR), Western blot analysis, and SR-BI 3= untranslated region (UTR) reporter assays. In vitro treatment of primary rat granulosa cells and MLTC-1 cells with cyclic AMP (cAMP) or in vivo treatment of rat adrenals with adrenocorticotropic hormone (ACTH) decreased the expression of miRNA-125a, miRNA125b, and miRNA-455 and reciprocally increased SR-BI expression. Using luciferase constructs containing the 3= untranslated region of SR-BI combined with miRNA overexpression and mutagenesis, we have provided evidence that steroidogenic SR-BI is a direct target of miRNA-125a and miRNA-455. Moreover, the transfection of Leydig tumor cells with precursor miRNA 125a (pre-miRNA-125a) or pre-miRNA-455 resulted in the suppression of SR-BI at both the transcript and protein levels and reduced selective HDL CE uptake and HDL-stimulated progesterone production. Transfection of liver Hepa 1-6 cells with pre-miRNA125a significantly reduced SR-BI expression and its selective transport function. In contrast, overexpression of miRNA-145 did not affect SR-BI expression or selective HDL CE uptake mediated by SR-BI in steroidogenic cell lines. These data suggest that a trophic hormone and cAMP inversely regulate the expression of SR-BI and miRNA-125a and miRNA-455 in steroidogenic tissues/cells and that both miRNA-125a and miRNA-455, by targeting steroidogenic SR-BI, negatively regulate selective HDL CE uptake and HDL CE-supported steroid hormone production. Circulating lipoproteins, particularly high-density lipoprotein (HDL), deliver cholesteryl esters (CEs) to cells via the "selective" CE pathway, a process in which the HDL core CE is taken into cells without parallel uptake and degradation of the HDL particle itself (5, 53, 55). The HDL CE selective pathway plays a major role in plasma cholesterol metabolism by delivering HDL CE to the liver in the final steps of reverse cholesterol transport for its excretion in bile (67) or for bile acid synthesis (52). Selective uptake of HDL CE also occurs prominently in steroidogenic cells of the adrenal gland and ovary and under certain physiological conditions in testicular Leydig cells, where it provides cholesterol for steroid biosynthesis and for the accumulation of cytoplasmic CE storage droplets (5,32,55,(60)(61)(62)74).Scavenger receptor class B type I is a physiologically relevant HDL receptor (1, 2, 65) which binds HDL particles and mediates selective uptake of HDL CE in vitro (1,3,19,30,62,74) and in vivo (36,39,66,76). Scavenger receptor class B type I (SR-BI) also facilitates the bidirectional flux of free cholesterol (FC) (35) and phospholipids between...

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“…However, cAMP did not increase the levels of miR-21 in cultured granulosa cells but miR-21 spontaneously increased within 12 h after plating, a response that was not affected by the presence of serum in culture media (Carletti et al 2010). Similarly, another study reported that treatment of mouse granulosa cells with FSH increased miR-132 levels but not miR-21 (Yao et al 2010b). Consistent with these findings, we found that treatment of cultured bovine granulosa cells with forskolin (an adenylate cyclase agonist) to promote luteinisation was followed by a decrease in the levels of miR-125b and miR-145, as observed during the follicular-luteal transition in vivo (McBride et al 2012); in contrast, levels of miR-21 and miR-34a spontaneously increased in the cultured cells regardless of treatment with forskolin.…”

Section: Involvement Of Mirnas During Ovulation and The Follicular-lumentioning

confidence: 93%

Involvement of miRNAs in ovarian follicular and luteal development

Donadeu¹,

Schauer²,

Sontakke³

2012

Journal of Endocrinology

162

110

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Although much progress has been made in the genetic dissection of biological networks involved in follicular/luteal development in the mammalian ovary, the gene regulation mechanisms involved are still poorly understood. Over the last 10 years, miRNAs have emerged as master regulators of tissue growth and differentiation in animals. However, compared with other body tissues, little is still known about the functional involvement of miRNAs in the ovary. Several studies have identified miRNA populations specifically associated with the development of follicles and corpora lutea, particularly in relation to the follicular-luteal transition, and the functional involvement of some of these miRNAs has been characterised in vitro and/or in vivo. Specifically, three different miRNAs, miR-224, miR-378 and miR-383, have shown to be involved in regulating aromatase expression during follicle development. In addition, miR-21 has been identified as promoting follicular cell survival during ovulation, and pro-angiogenic miR-17-5p and let-7b were shown to be necessary for normal development of the corpus luteum. Experimental evidence for the involvement of several other miRNAs in different aspects of follicle/luteal development has also been obtained. In addition, many of these studies exemplify the challenges associated with identifying physiologically relevant targets of ovarian miRNAs. Continuous advances in this field will be considerably facilitated by progress in understanding miRNA physiology in other body systems and will eventually lead to a much better understanding of the control of follicular/luteal development. In turn, through the potential offered by miRNA diagnostics and miRNA therapeutics, this new knowledge should bring considerable benefits to reproductive medicine.

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Follicle-stimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells

Cited by 88 publications

References 42 publications

Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary

Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary

MicroRNAs 125a and 455 Repress Lipoprotein-Supported Steroidogenesis by Targeting Scavenger Receptor Class B Type I in Steroidogenic Cells

Involvement of miRNAs in ovarian follicular and luteal development

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