MiR-31 targets HSD17B14 and FSHR, and miR-20b targets HSD17B14 to affect apoptosis and steroid hormone metabolism of porcine ovarian granulosa cells

Gao, Siyuan; Zhao, Jing; Xu, Qiang; Guo, Yanli; Liu, Mingzheng; Zhang, Chunlei; Schinckel, A. P.; Zhou, Bo

doi:10.1016/j.theriogenology.2021.12.014

Cited by 10 publications

(12 citation statements)

References 39 publications

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“…The results showed that gga-miR-449b-5p inhibited the expression of the steroid synthesis-related genes StAR, 3β-HSD and CYP19A1 and the production of P4 and E2. This result is consistent with the previous results concerning the validation of miRNA function in steroid the synthesis of GCs [ 35 , 37 , 43 ].…”

Section: Discussionsupporting

confidence: 93%

“…Many studies have shown that functional miRNAs play an important role in regulating ovarian function, follicular development and atresia, cell proliferation and apoptosis, steroid hormone synthesis and even ovarian cancer [ 26 , 27 , 28 , 29 ]. In mammals, miR-383, miR-323-3p, miR-320a, miR-130a-3p, miR-1246, miR-31 and miR-20b influence steroid hormone synthesis in granulosa cells [ 30 , 31 , 32 , 33 , 34 , 35 ], and miR-214-3p, miR-324-3p and miR-335-5p promote granulosa cell proliferation in the ovary [ 36 , 37 , 38 ]. Unfortunately, in poultry, the study of functional miRNAs in ovarian development and function of laying hens still lags behind.…”

Section: Introductionmentioning

confidence: 99%

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gga-miR-449b-5p Regulates Steroid Hormone Synthesis in Laying Hen Ovarian Granulosa Cells by Targeting the IGF2BP3 Gene

Zhang

et al. 2022

Animals

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MiRNAs have been found to be involved in the regulation of ovarian function as important post-transcriptional regulators, including regulators of follicular development, steroidogenesis, cell atresia, and even the development of ovarian cancer. In this study, we evaluated the regulatory role of gga-miR-449b-5p in follicular growth and steroid synthesis in ovarian granulosa cells (GCs) of laying hens through qRT‒PCR, ELISAs, western blotting and dual-luciferase reporter assays, which have been described in our previous study. We demonstrated that gga-miR-449b-5p was widely expressed in granulosa and theca layers of the different-sized follicles, especially in the granulosa layer. The gga-miR-449b-5p had no significant effect on the proliferation of GCs, but could significantly regulate the expression of key steroidogenesis-related genes (StAR and CYP19A1) (p < 0.01) and the secretion of P4 and E2 (p < 0.01 and p < 0.05). Further research showed that gga-miR-449b-5p could target IGF2BP3 and downregulate the mRNA and protein expression of IGF2BP3 (p < 0.05). Therefore, this study suggests that gga-miR-449b-5p is a potent regulator of the synthesis of steroid hormones in GCs by targeting the expression of IGF2BP3 and may contribute to a better understanding of the role of functional miRNAs in laying hen ovarian development.

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Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

gga-miR-449b-5p Regulates Steroid Hormone Synthesis in Laying Hen Ovarian Granulosa Cells by Targeting the IGF2BP3 Gene

Zhang

et al. 2022

Animals

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“…In germ cells, miR-301a-5p was involved in the transforming growth factor-beta (TGF-β) signaling pathway by targeting TGF-β2 to promote cell development [ 42 ]. In porcine ovarian GCs, miR-31 targets 17-beta-hydroxysteroid dehydrogenase 14 (HSD17B14) and follicle-stimulating hormone receptor, and miR-20b targets HSD17B14 to affect cell apoptosis and the P4 concentration [ 43 ]. Similarly, we found miR-1246 affects the P4 synthesis in BGCs by targeting StAR.…”

Section: Discussionmentioning

confidence: 99%

Kisspeptin-10 Promotes Progesterone Synthesis in Bovine Ovarian Granulosa Cells via Downregulation of microRNA-1246

et al. 2022

Genes

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The objective of this study was to clarify the effect of kisspeptin-10 (kp-10) on the synthesis of progesterone (P4) in bovine granulosa cells (BGCs) and its mechanisms via microRNA 1246 (miR-1246). According to the results, we found that treating with kp-10 for 24 h could increase P4 level, the mRNA expression of the steroidogenesis-related gene steroidogenic acute regulatory protein (StAR), free cholesterol content, and decrease miR-1246 expression in BGCs. Overexpression of miR-1246 significantly inhibited P4 synthesis, StAR mRNA expression, and free cholesterol content in BGCs, whereas underexpression of miR-1246 significantly reversed this effect in BGCs. Additionally, overexpression of miR-1246 counteracted the accelerative effect of kp-10 on P4 synthesis, StAR mRNA expression, and free cholesterol content in BGCs. Conversely, underexpression of miR-1246 enhanced the accelerative effect of kp-10 on P4 synthesis, StAR mRNA expression, and free cholesterol content in BGCs. Meanwhile, results of dual-luciferase reporter assays indicated that miR-1246 targeted the 3′UTR of StAR in BGCs. These results demonstrated that kp-10 induced P4 synthesis in BGCs by promoting free cholesterol transport via regulating expression of miR-1246/StAR.

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“…Other studies have shown that the overexpression of miR-17-5p significantly reduces E2F1 activity, while E2F1 knockdown promotes porcine granulosa cell growth and upregulates marker genes of follicle development, such as those encoding the LH receptor, cytochrome P450 19A1, and amphiregulin, thereby promoting E 2 synthesis [ 36 , 37 ]. A recent study reported that miR-31 directly binds to the target genes HSD17B14 and FSHR to maintain the balance between proliferation and apoptosis of porcine ovarian granulosa cells and regulate steroid hormone metabolism [ 32 ].…”

Section: Discussionmentioning

confidence: 99%

“…In addition, miRNAs play a very important role in the regulation of granulosa cell apoptosis. Several miRNAs in mammals, such as miR-130a, miR-31, miR-20b, miR-143, and miR-92a, have been reported to be involved in the regulation of proliferation and apoptosis of granulosa cells, and synthesis and secretion of hormones [ 30 , 31 , 32 ].…”

Section: Introductionmentioning

confidence: 99%

Upregulation of miR-33 Exacerbates Heat-Stress-Induced Apoptosis in Granulosa Cell and Follicular Atresia of Nile Tilapia (Oreochromis niloticus) by Targeting TGFβ1I1

Qiang

Tao

et al. 2022

Genes

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High temperature affects egg quality and increases follicular atresia in teleosts. The present study aimed to explore the regulated mechanism of ovary syndrome of Nile tilapia (Oreochromis niloticus) exposed to heat stress. To this end, we conducted histological and biochemical analyses and integrated miRNA-target gene analyses. The histochemical analyses confirmed that heat stress promoted the apoptosis of granulosa cell and therefore resulted in increased follicular atresia in the ovary. Heat stress led to the differential expression of multiple miRNAs (miR-27e, -27b-3p, -33, -34a -133a-5p, and -301b-5p). In a luciferase activity assay, miR-33 bound to the 3′-untranslated region (UTR) of the TGFβ1I1 (transforming growth factor-β1-induced transcript 1) gene and inhibited its expression. A TGFβ1I1 gene signal was detected in the granulosa cells of Nile tilapia by immunohistochemical analysis. Up-regulation of the miR-33 of tilapia at 6 d and 12 d exposed to heat (34.5 °C ± 0.5 °C) had significant down-regulation of the TGFβ1I1 expression of the gene and protein in tilapia ovaries. An miRNA-target gene integrated analysis revealed that miR-33 and TGFβ1I1 function in an apoptosis-related signal pathway. The signal transduction of the vascular endothelial growth factor (VEGF) family members VEGFA and its receptor (KDR) in the heat-stressed group decreased significantly compared with the control group. Transcript-levels of the Bax and Caspase-3 as apoptotic promotors were activated and Bcl-2 and Caspase-8 as apoptotic inhibitors were suppressed in the heat-stressed tilapia. These results suggest that heat stress increases the expression of miR-33, which targets TGFβ1I1 and inhibits its expression, resulting in decreased levels of follicle-stimulating hormone and 17β-estradiol and increased apoptosis by suppressing VEGF signaling, eventually inducing follicular atresia. In conclusion, our results show that the miR-33/TGFβ1I1 axis of Nile tilapia is involved in the follicular development of broodstock, and can suppress VEGF signaling to accelerate follicular atresia. Our findings demonstrate the suppressive role of miR-33 during oocyte development in Nile tilapia.

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MiR-31 targets HSD17B14 and FSHR, and miR-20b targets HSD17B14 to affect apoptosis and steroid hormone metabolism of porcine ovarian granulosa cells

Cited by 10 publications

References 39 publications

gga-miR-449b-5p Regulates Steroid Hormone Synthesis in Laying Hen Ovarian Granulosa Cells by Targeting the IGF2BP3 Gene

gga-miR-449b-5p Regulates Steroid Hormone Synthesis in Laying Hen Ovarian Granulosa Cells by Targeting the IGF2BP3 Gene

Kisspeptin-10 Promotes Progesterone Synthesis in Bovine Ovarian Granulosa Cells via Downregulation of microRNA-1246

Upregulation of miR-33 Exacerbates Heat-Stress-Induced Apoptosis in Granulosa Cell and Follicular Atresia of Nile Tilapia (Oreochromis niloticus) by Targeting TGFβ1I1

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