MiRNA-202 impacts proliferation and apoptosis of granulose cells
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1 MiRNA-202 impacts proliferation and apoptosis of granulose cells Liqiong Huang, Bo Zheng*, Yi He Department of Obstetrics and Gynecology, Xianning Central Hospital, The First Affiliated Hospital Of Hubei University Of Science And Technology, Hubei, , China * Corresponding author huanglq1977@163.com Abstract: Accelerated apoptosis of granulosa cells is one of the causes influencing follicle atresia and contributes to the etiology of polycystic ovarian syndrome (PCOS). During our previous work, we found that mir-202 was up-regulated in dehydroandrosterone-induced rat PCOS model. The aim of this study was to investigate the impact of mir-202 on proliferation and apoptosis of granulose cells and its possible molecular mechanism. Human granulose cell line KGN cells were treated with testosterone (10 μmol/l). Expression of mir-202 was detected with RT-PCR. Cellular growth was measured by MTT method. The KGN cells were then transfected with mir-202 mimic or inhibitor. After transfection, growth curves of the cells from day 1 to day 4 were measured by MTT method. Cellular apoptosis rate was measured by flow cytometry after 48 hours. Meanwhile, mrna expression of TGFBR2, a potential target of mir-202 encoding transforming growth factor beta receptor II, was detected by RT-PCR. Protein levels of TGFBR2 and its down-stream factors were detected by western blot. The results showed that over-expressing mir-202 accelerated apoptosis and inhibited growth; reducing mir-202 promoted cellular growth and inhibited apoptosis. Up-regulation of mir-202 led to down-regulation of TGFBR2. Subsequently, down-stream PI3K/Akt signaling pathway was suppressed and proapoptosis proteins Bax, caspase-3, and caspase-9 increased in the transfectants with mir-202 mimic. Transfecting mir-202 inhibitor produced the opposite effect. In conclusion, mir-202 promoted apoptosis of human 18
2 granulose cells by suppressing the TGF signaling pathway and promoting the expression of apoptosis-related proteins. Keywords: mir-202, granulose cells, apoptosis, transforming growth factor beta 19
3 Introduction Granulosa cells are important cell types during mammalian ovarian follicular development. Mammalian follicular development is a complex process involving multiple steps. Only limited numbers of follicles undergo ovulation and the others undergo atresia. Follicle atresia is triggered by apoptosis of granulose cells. Excessive apoptosis prevents the transformation of androgen to estrogen, and interferes with normal follicle development and formation of oocytes (1). Accelerated apoptosis of granulose cells is one of the causes leading to polycystic ovarian syndrome (PCOS) (2). The cellular and molecular mechanisms underlying granulose cell apoptosis is not fully elucidated. During our previous studies, we found that mir-202 was up-regulated in dehydroandrosterone-induced rat PCOS model (unpublished data). mir-202 is a tumor suppressor and regulates cellular proliferation and apoptosis in several cancers such as pancreatic cancer (3) and cervical cancer (4). The targetscan database ( indicates that TGFBR2 is a potential target of mir-202 (Figure 1A). TGFBR2 encodes transforming growth factor beta (TGF-β) receptor II. By binding to TGF-β, the TGF-β signaling pathway is activated and initiates its down-stream reactions. The TGF-β superfamily members are crucial regulators of follilcle development (5). TGF-β signaling could promote juvenile granulose cell tumorigenesis by suppressing apoptosis (6). These previous studies gave us the hint that mir-202 might be involved in follicle atresia. The aim of this study was to investigate the impact of mir-202 on proliferation and apoptosis of granulose cells and its possible molecular mechanism. Materials and methods Materials DMEM, fetal bovine serum (FBS), glutamine, penicillin, and streptomycin were purchased from HyClone (GE Healthcare, Logan, USA). The nucleotides used in transfection and RT-PCR were synthesized by Sangon Biotech (Shanghai, China). The 20
4 MTT cell proliferation assay kit and Annexin V binding apoptosis assay kit were purchased from Sangon Biotech (Shanghai, China). The antibodies used in western blot were purchased from Boster Biological Technology (Wuhan, China). Cell culture and treatment Human ovarian granulose-like cell line KGN, a human granulose cell tumor-derived cell line, was used in this study. The cells were obtained from the American Type Culture Collection (ATCC, Manassas, USA). The cells were cultured in DMEM supplemented with 10% FBS, 2 mmol/l glutamine, 100 units/ml penicillin, and 100 g/ml streptomycin. The incubation environment was 37ºC in a humidified atmosphere of 95% air and 5% CO 2. To test the influence of androgen on mir-202 expression, the KGN cells were cultured to 70% and treated with 10 mmol/l testosterone (dissolved in sesame oil). Menstruum sesames oil was used as the control. The cell viability was tested on day1, 2, 3, and 4 by MTT method. After 4 days, the cells were harvested and used for detection of mir-202 expression. The test the influence of mir-202 on proliferation and apoptosis of granulose cells, the KGN cells were transfected with has-mir-202 mimics (5 -UUCCUAUGCAUAUACUUCUUU-3 ) or has-mir-202 inhibitors (5 -UUCCCAUGCCCUAUACCUCU-3 )using the Lipofectamine RNAiMAX transfection reagent (ThermoFisher Scientific, Carlsbad, USA). The cells were inoculated in 6-well plates ( cells/well) and grew overnight before transfection. The cell viability was assessed daily from day 1 to day 4 after transfection, and then harvested for flow cytometry and molecular assays. MTT analysis On each time after transfection, 20 μl MTT reagent (5 μg/ul) was added to each well and the plates were incubated at 37ºC for 4 hours. The medium was discarded, and 150 μl DMSO was added and vortexed for 10 min. The absorbance at 560 nm was measured with a microplate reader. Flow cytometry analysis 21
5 105 cells were detected for each sample. The cells were suspended in 100 ul binding buffer. Five ul of FITC-conjugated annexin V (0.5μg/ml) and 5ul of propidium iodide (1 μg/ml) were added to the cell suspensions. After incubation at room temperature for 15 min, 400 ul binding buffer was added and the samples were analyzed by flow cytometer. Real-time RT-PCR analysis Total RNA was extracted using the Trizol reagent (ThermoFisher Scientific, Carlsbad, USA). The RNA integrity and concentration were assessed using denaturing formaldehyde gel electrophoresis. Total RNA (30 ng) was then reverse-transcribed into cdna using the TaqMan microrna Reverse Transcription Kit (Applied Biosystems, Foster City, USA). Quantitative RT-CPR was performed on ABI 7300 Real-Time PCR System (Applied Biosystems, Foster City, USA). The qrt-pcr conditions were as follows: 95ºC for 10 min followed by 40 cycles at 95ºC for 15 s and 60ºC for 15 s. The fold change of target mrnas was calculated using the 2 -ΔΔCT method with GAPDH or U6 as an internal control (7). The following primers were used: mir-202 forward 5 -GCTGGAGAGGTATAGGGCA-3 and mir-202 reverse 5 -ACGCTTCACGAATTTGCGTGTC-3 ; U6 forward 5 -CTCGCTTCGGCAGCAC A-3 and U6 reverse 5 -AACGCTTCACGAATTTGCGT-3 ; TGFBR2 forward 5 -CTAACCTGCTGCCTGTGTGA-3 and TGFBR2 reverse 5 -TCTGGAGCCATGT ATCTTGC-3; GAPDH forward 5 -TGCACCACCAACTGCTTAG-3 and GAPDH reverse 5 -GAGGCAGGGATGATGTTC-3. The protein bands were examined by enhanced chemiluminescence method. Western blot assay Total protein was extracted using protein extraction kit from Sangon Biotech (Shanghai, China). Protein concentrations were determined by Bradford method. For each sample, 50 ug of protein was separated on a 10% SDS-polyacrylamide gel and transferred onto polyvinylidene fluoride membranes (GE Healthcare, San Francisco, USA). Following transfer, the membranes were blocked with 5% non-fat milk, and then incubated overnight with primary antibodies (1:2000 dilutions) at 4 C. The 22
6 primary antibodies used were as follows: rabbit anti-tgfbr2, rabbit anti-pi3 kinase P85α, rabbit anti-phospho-akt1 (T450), rabbit anti-caspase-3, rabbit anti-caspase-9, rabbit anti-bax, rabbit anti-bcl-2, and rabbit anti-gapdh. The next day, membranes were incubated for 1 h at room temperature with horseradish-peroxidase-conjugated secondary antibody (goat anti-rabbit IgG, 1:1000). Statistical analysis All experiments were repeated at least three times and representative data were presented here. All statistical analyses were conducted using Microsoft Excel 2010 and the SAS software version 9.1. The results were expressed as mean ± SD (standard deviation). Difference between two groups was evaluated by Student s t-test. A value of P<0.05 was considered statistically significant. Results mir-202 expression and cellular growth in testosterone-treated KGN cells First we tested whether androgen had an effect on the growth of cells in vitro. As shown in Figure 1B, the cells treated with testosterone showed significantly lower viability compared with the blank control group or the menstruum group (P<0.05). Treatment with testosterone also increased mir-202 expression level by 79% (P<0.01) while reduced TGFBR2 expression level by 35% (P<0.05), as shown in Figure 1C. The results suggested that androgen could induce mir-202 expression and suppress cellular growth. 23
7 Figure 1. The effect of testosterone on cellular growth and mir-202 expression in KGN cells A, TGFBR2 is predicted by bioinformatics to be a target of mir-202. B, testosterone (10 μmol/l) treatment inhibited cellular viability. C, testosterone induced mir-202 over-expression and suppressed TGFBR2 expression. * P<0.05 vs. the blank control group; ** P<0.01 vs. the blank control group. Influence of mir-202 expression on cellular proliferation and apoptosis To further investigate the influence of mir-202 level on cellular proliferation and apoptosis, the KGN cells were transfected with either mir-202 mimics or mir-202 inhibitors. MTT analysis (Figure 2A) showed that the cell viability was lower in the transfectants with mir-202 mimics. Transfecting mir-202 inhibitors only significantly increased cell viability after 3 days. Cellular apoptosis rate also altered with different mir-202 levels (Figure 2B). Over-expressing mir-202 promoted cellular apoptosis. The apoptosis rate increased from 11.39% in the control group to 20.02% in the mir-202 mimics group. Reducing the concentration of mir-202 was beneficial to lower cellular apoptosis. The cells transfected with mir-202 inhibitors has the lowest apoptosis rate (8.39%) among the three groups. The results indicated that the expression level of mir-202 does affect the proliferation and apoptosis of granulose cells, thus affecting follicle development. 24
8 Figure 2. The effect of mir-202 expression on cellular growth and apoptosis of KGN cells A, transfecting mir-202 mimics inhibited cellular growth and trasfecting mir-202 inhibitors promoted cellular growth. B, transfecting mir-202 mimics promoted cellular apoptosis and trasfecting mir-202 inhibitors inhibited cellular apoptosis. * P<0.05 vs. the blank control group; ** P<0.01 vs. the blank control group. Influence of mir-202 level on expression of TGFBR2 and downstream PI3K/Akt signaling pathway Next, we studied the effect of mir-202 on TGF-β signaling-induced PI3K/Akt. 25
9 RT-PCR detected that there was a negative association between mir-202 expression and TGFBR2 expression (Figure 3A). In another word, mir-202 could regulate expression of TGF-β receptor. PI3K/Akt pathway is a prototypic survival pathway that is commonly activated in many types of diseases. Activation of PI3K/Akt pathway is one of the downstream reactions by binding of TGF-β to its receptors. The results of western blot (Figure 3B) showed that PI3K/Akt pathway was inhibited by over-expression of mir-202. Both PI3K and the active form of Akt (phosphorylated Akt) were down-regulated by transfecting mir-202 mimics. In consistent the effects of mir-202 on cellular proliferation and apoptosis, the protein levels of pro-apoptosis factors caspase-3, caspase-9, and Bax were elevated in the mimic group, whereas anti-apoptosis factor Bcl-2 was decreased when mir-202 was over-expressed. Transfecting mir-202 inhibitors produced the opposite effect of mir-202 mimics. The results suggested that the regulation of mir-202 on cellular growth and apoptosis was achieved by modulating TGF-β receptor 2 expression and changing the activity of the downstream signaling pathway. 26
10 Figure 3. Influence of mir-202 level on expression of TGFBR2 and downstream PI3K/Akt signaling pathway in KGN cells A, transfecting mir-202 mimics inhibited TGFBR2 expression and transfecting mir-202 inhibitors increased TGFBR2 expression. B, transfecting mir-202 mimics inhibited PI3K/Akt pathway and transfecting mir-202 inhibitors activated PI3K/Akt pathway. * P<0.05 vs. the blank control group; ** P<0.01 vs. the blank control group. Discussion Granulosa cells play an important role in the hormone environment within ovary, the development and maturation of oocytes, and the formation and growth of embryos. The balance between apoptosis and anti-apoptosis is disturbed in the ovaries of women with PCOS. The expression of apoptosis-related factors in PCOS ovaries is abnormally higher than normal ovaries (8). In this study, we demonstrated that over-expressing mir-202 in granulose-like KGN cells could inhibit TGFBR2, which encodes TGF-β receptor 2, thereby suppress the activity of PI3K/Akt signaling pathway and induce apoptosis. The effect of mir-202 on cellular growth and apoptosis has been studied a lot in cancers. mir-202 was down-regulated in the peripheral blood of patients with esophageal squamous cell carcinoma and in vitro experiments showed that mir-202 inhibited proliferation, migration, and invasion of cancer cells (9). mir-202 could 27
11 directly target cyclin D1 and inhibit the progression of human cervical cancer (4). mir-202 could inhibit the proliferation of lung cancer cell and reduce glucose uptake (10). Down-regulation of mir-202 increased the expression of its target Mxd1 and led to repression of Myc-Max target proteins in pancreatic cancer cells (3). In gastric cancer mir-202 might function as a tumor suppressor by targeting Gli1 (11). These studies indicated that the pro-apoptosis role of mir-202 commonly exists in many diseases. In this study, we found that mir-202 had a negative association with TGFBR2 expression. The TGFBR2 is a candidate gene involved in follicular dynamics (12). TGF-β receptor 2 is critical for activation and transmission of TGF-β signal. Down-regulation of TGF-β receptor 2 was associated with lower TGF-β1 expression and worse prognosis in colon carcinoma (13). Many studies have showed that the pro-cell survival response by activation of P13K/Akt is mediated by TGF-β signal (see review 14). The results of this study demonstrated similar regulational mechanism. However, the direct targeting effect between mir-202 and TGFBR2 needs dual-luciferase reporting assay to confirm. So far as we knew, this is the first paper demonstrating the regulational role of mir-202 in apoptosis and viability in granulose-like cells. The exact role of mir-202 in PCOS women still needs in vivo animal assays and clinical data to confirm. mir-202 may be a potential research target for the study of pathophysiological mechanisms of PCOS and other follicular atresia-related diseases. References 1. Yu YS, Sui HS, Han ZB, et al: Apoptosis in Granulosa cells during follicular atresia: relationship with steroids and insulin-like growth factors. Cell Res 14: , Pierre A, Peigne M, Grynberg M, et al: Loss of LH-induced down-regulation of anti-müllerian hormone receptor expression may contribute to anovulation in women with polycystic ovary syndrome. Human Reprod 28: , Farhana L, Dawson MI, Fontana JA: Down regulation of mir-202 modulates Mxd1 and Sin3A repressor complexes to induce apoptosis of pancreatic cancer cells. Cancer Biol Ther 28
12 16: , Yi Y, Li H, Lv Q, et al: mir-202 inhibits the progression of human cervical cancer through inhibition of cyclin D1. Oncotarget 7: , Fenwick M, Mora JM, Mansour YT, et al: Investigations of TGF-β signaling in preantral follicles of female mice reveal differential roles for bone morphogenetic protein 15. Endocrinology 154: , Mansouriattia N, Tripurani SK, Gokul N, et al: TGFβ signaling promotes juvenile granulosa cell tumorigenesis by suppressing apoptosis. Mol Endocrinol 28: , Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: , Jansen E, Laven JSE, Dommerholt HBR, et al: Abnormal gene expression profiles in human ovaries from polycystic ovary syndrome patients. Mol Endocrinol 18: , Ma G, Zhang F, Dong X, et al: Low expression of microrna-202 is associated with the metastasis of esophageal squamous cell carcinoma. Exp Ther Med 11: , Xia Y, Zhao M, Ding L, et al: MiR-202 mediates metabolic shift in lung cancer cells via targeting HK2. Curr Signal Transd T 10:1, Zhao Y, Li C, Wang M, et al: Decrease of mir-202-3p expression, a novel tumor suppressor, in gastric cancer. PLoS One 8:e69756, Silva PV, Guimaraes SEF, Guimaraes JD, et al: Follicular dynamics and gene expression in granulosa cells, corpora lutea and oocytes from gilts of breeds with low and high ovulation rates. Reprod Fertil Dev 26: , Bacman D, Merkel S, Croner RS, et al: TGF-beta receptor 2 downregulation in tumour-associated stroma worsens prognosis and high-grade tumours show more tumour-associated macrophages and lower TGF-beta1 expression in colon carcinoma: a retrospective study. BMC Cancer 7: , Zhang L, Zhou F, Dijke PT: Signaling interplay between transforming growth factor-β receptor and PI3K/AKT pathways in cancer. Trends Biochem Sci 38: ,
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