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

Li, Guo; Xu, Haoran; Li, Yajun; Liu, Hongyu; Zhao, Jing; Lu, Wenfa; Wang, Jun

doi:10.3390/genes13020298

Cited by 7 publications

(7 citation statements)

References 46 publications

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“…A kisspeptin-induced increase in P4 secretion and expression of STAR, CYP11A1 and HSD3B1 has also been reported in cultured chicken GC ( Xiao et al 2011 ). More recently, kisspeptin-10 was shown to increase P4 production and STAR mRNA expression by bovine GCs cultured in medium supplemented with 10% FCS ( Guo et al 2022 ). As such, these observations are indicative of a positive role for kisspeptin in promoting P4 synthesis, although possible effects on other ovarian steroids were not reported.…”

Section: Discussionmentioning

confidence: 99%

“…With regard to steroidogenesis, it was reported that progesterone (P4) production by rat luteal cells was stimulated by kisspeptin ( Peng et al 2013 ), while hCG-induced P4 production by rat GC was attenuated by a kisspeptin antagonist, kisspeptin 234 ( Laoharatchatathanin et al 2015 ). Kisspeptin was also shown to increase P4 production by porcine GC ( Basini et al 2018 ) and bovine GC ( Guo et al 2022 ). The above reports suggest a potential role of locally produced kisspeptins in the control of ovarian function.…”

Section: Introductionmentioning

confidence: 99%

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Does kisspeptin exert a local modulatory effect on bovine ovarian steroidogenesis?

Mattar

Cheewasopit

Samir

et al. 2023

Reproduction and Fertility

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Kisspeptin, a hypothalamic neuropeptide encoded by the KISS1 gene, has a pivotal role in promoting GnRH secretion in mammals. Kisspeptin and its receptor (KISS1R) are also expressed in certain peripheral tissues including gonads, suggesting intra-gonadal roles. Such actions at the level of the bovine ovary have not been explored previously. The current aims were to determine whether KISS1 and its receptor (KISS1R) are expressed in the bovine ovary and whether kisspeptin or a kisspeptin antagonist can modulate ovarian steroid production by cultured ovarian cells. Granulosa (GC) and theca interna (TC) were collected from antral follicles (3-18 mm) categorized into five class sizes. Early, mid and regressing corpora lutea (CL) were also collected for RT-qPCR analysis of KISS1 and KISS1R expression. Bovine TC and GC cultured under both non-luteinizing (serum-free) and luteinizing (serum-supplemented) conditions were treated for 4 days with kisspeptin-10 (10-10-10-6M) or kisspeptin antagonist (p234; 10-10-10-6M), alone and in combination with either FSH (GC), LH (TC) or forskolin (luteinized GC/TC). Steroid secretion (GC: oestradiol, progesterone; TC: androstenedione, progesterone; luteinized GC/TC: progesterone) was measured by ELISA and viable cell number determined by neutral red uptake assay. KISS1 and KISS1R transcripts were detected in TC, GC and CL with significant differences between follicle categories and CL stages. However, neither kisspeptin-10 nor kisspeptin antagonist affected steroid secretion or viable cell number in any of the four ovarian cell culture models. As such, the hypothesis that kisspeptin has a direct intra-ovarian role to modulate follicular or luteal steroidogenesis, or cell proliferation/survival, is not supported.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Does kisspeptin exert a local modulatory effect on bovine ovarian steroidogenesis?

Mattar

Cheewasopit

Samir

et al. 2023

Reproduction and Fertility

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“…Kisspeptin can regulate animal reproduction by regulating follicular development through the paracrine or autocrine pathway in the gonads. Kisspeptin treatment promotes progesterone secretion in cultured bovine granulosa cells [ 24 ], while transfection of the kiss1 gene into porcine ovarian granulosa cells promotes steroid secretion [ 25 ]. Our research group also showed that kisspeptin could promote the secretion of steroid hormones and cell proliferation in ovarian granulosa cells of Tan sheep in vitro (unpublished data), but the specific molecular mechanism remains unclear.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have indicated that kisspeptin-10 could significantly change the expression of circulating miRNAs (let-7e, miR-100-5p, and others) obtained from the plasma of gonads of Senegalese Sole, affecting their reproduction [ 26 ]. Kisspeptin-10 has been reported to induce progesterone synthesis in bovine granulosa cells by regulating the expression of miR-146-targeted StAR genes [ 24 ]. Therefore, we speculate that kisspeptin affects ovarian granulosa cell function by modulating miRNA and mRNA expression.…”

Section: Discussionmentioning

confidence: 99%

Integrative Analysis of miRNA-mRNA in Ovarian Granulosa Cells Treated with Kisspeptin in Tan Sheep

Dai

Kang

Yang

et al. 2022

Animals

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Kisspeptin is a peptide hormone encoded by the kiss-1 gene that regulates animal reproduction. Our studies revealed that kisspeptin can regulate steroid hormone production and promote cell proliferation in ovarian granulosa cells of Tan sheep, but the mechanism has not yet been fully understood. We speculated that kisspeptin might promote steroid hormone production and cell proliferation by mediating the expression of specific miRNA and mRNA in granulosa cells. Accordingly, after granulosa cells were treated with kisspeptin, the RNA of cells was extracted to construct a cDNA library, and miRNA-mRNA sequencing was performed. Results showed that 1303 expressed genes and 605 expressed miRNAs were identified. Furthermore, eight differentially expressed miRNAs were found, and their target genes were significantly enriched in progesterone synthesis/metabolism, hormone biosynthesis, ovulation cycle, and steroid metabolism regulation. Meanwhile, mRNA was significantly enriched in steroid biosynthesis, IL-17 signaling pathway, and GnRH signaling pathway. Integrative analysis of miRNA-mRNA revealed that the significantly different oar-let-7b targets eight genes, of which EGR1 (early growth response-1) might play a significant role in regulating the function of granulosa cells, and miR-10a regulates lipid metabolism and steroid hormone synthesis by targeting HNRNPD. Additionally, PPI analysis revealed genes that are not miRNA targets but crucial to other biological processes in granulosa cells, implying that kisspeptin may also indirectly regulate granulosa cell function by these pathways. The findings of this work may help understand the molecular mechanism of kisspeptin regulating steroid hormone secretion, cell proliferation, and other physiological functions in ovarian granulosa cells of Tan sheep.

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“…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%

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

Cited by 7 publications

References 46 publications

Does kisspeptin exert a local modulatory effect on bovine ovarian steroidogenesis?

Does kisspeptin exert a local modulatory effect on bovine ovarian steroidogenesis?

Integrative Analysis of miRNA-mRNA in Ovarian Granulosa Cells Treated with Kisspeptin in Tan Sheep

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

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