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Original Article the Expression Pattern of Fibroblast Growth Factor 10 and Its Receptors During Buffalo Follicular Development

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Original Article the Expression Pattern of Fibroblast Growth Factor 10 and Its Receptors During Buffalo Follicular Development Int J Clin Exp Pathol 2018;11(10):4934-4941 www.ijcep.com /ISSN:1936-2625/IJCEP0083076 Original Article The expression pattern of fibroblast growth factor 10 and its receptors during buffalo follicular development Shanshan Du1,2, Xiaohua Liu1, Kai Deng1, Wenting Zhou1, Fenghua Lu1, Deshun Shi1 1Guangxi High Education Key Laboratory for Animal Reproduction and Biotechnology, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi University, Nanning 530004, Guangxi, China; 2Center for Reproductive Medicine, The Third Affiliated Hospital of Zhengzhou University, Zhengzhou 450000, Henan, China Received July 24, 2018; Accepted August 25, 2018; Epub October 1, 2018; Published October 15, 2018 Abstract: This study explored the expression and localization of fibroblast growth factor (FGF) 10 and its receptors (FGF receptor 1 and FGF receptor 2, FGFR1 and FGFR2) during buffalo follicular development, laying a founda- tion for the further study of FGF signaling pathways in follicular development and oogenesis. Granulosa cells and ovarian follicles were extracted from buffalo ovaries, and in vitro maturation culture of oocytes was conducted. Immunohistochemistry was performed to detect the expression of FGF10 and its receptors FGFR1 and FGFR2. In addition, immunofluorescence staining was used to detect the expression of FGF10 in buffalo cumulus oocyte complexes (COCs). Moreover, mRNA levels of FGF10, sub-types of FGFR1 and FGFR2 (FGFR1b and FGFR2b) were measured using qRT-PCR. Immunohistochemistry results showed that FGF10 and its receptors FGFR1 and FGFR2 appeared to have positive responses in buffalo primordial follicles, primary follicles, secondary follicles, and mature follicle oocytes and granulosa cells, and mature follicle basal membrane cells. However, no expression of FGF10 mRNA was detected in granulosa cells from follicles of different diameters, but immunofluorescence results showed that FGF10 could be detected in both cumulus cells and oocytes. With an increase in the vitro maturation time of buffalo COCs, FGF10 and receptor sub-types FGFR1b and FGFR2b mRNA expression also gradually increased, and significantly higher than before maturation. In summary, FGF10 and its receptors may be involved in the process of buffalo follicular development and oocyte maturation. Keywords: Buffalo, FGF10, FGFR, follicular development, oocyte Introduction first meiotic prophase [2]. Therefore, oocytes are required from the very beginning of follicu- Follicular development is a highly complex and lar development. Follicular cells and granulosa precisely regulated process. A follicle is a func- cells also play a role in follicular development. tional organizational unit of the ovary, a place In the process of follicle growth and develop- of development of oocytes and secreting sex ment, the granulosa cells, the theca cells, the hormones [1]. A large number of follicles at dif- oocytes and the stromal cells can also secrete ferent stages are stored in the ovaries. a series of cytokines to promote and/or regu- According to the shape and developmental late the differentiation, development and matu- degree of the follicle, the follicle can be divided ration process of oocytes [2, 3]. into the primordial follicle, the developing folli- cle, and the mature follicle, and the developing Fibroblast growth factors (FGFs) play important follicle is divided into primary follicle and sec- roles in follicular development in a variety of ondary follicle. Follicles are composed of mammals. FGFs were discovered in brain and oocytes, granulosa cells, and theca cells. pituitary extracts in the 1930s [4]. They were Ovarian follicular development starts from the named for their ability to promote the growth of generation of primordial follicles in which squa- fibroblasts. However, the substance was not mous somatic cells, often called pre-granulosa isolated and purified until 1974 [5]. FGFs are a cells, encircle a primary oocyte arrested at the family with a wide range of physiological func- FGF10 expression pattern during buffalo follicular development tions, including initiating the transcription of saline and quickly transferred to the laboratory. downstream target genes by binding to FGFRs Appropriate ovarian tissue was selected and to activate signaling pathways [6-9]. FGFRs not fixed in 4% paraformaldehyde (Sigma-Aldrich). only promote cell proliferation and differentia- Follicles were extracted from the ovaries to tion, but they also play an important role in the obtain cumulus and oocyte complexes. The formation and repair of various tissues and present study was approved by the Animal organs, the development of follicles and embry- Ethics Committee of Guangxi University. os, the occurrence and metastasis of tumors, and the metabolism of blood glucose and lipids Granulosa cell collection [10-16]. The functional diversity of FGF family members is mainly due to the differences in the The buffalo ovary was soaked with 75% alcohol N- and C-terminal sequences on both sides of for 20-30 s, then washed with sterile saline. We the core region. Most of the FGF family mem- then withdrew the follicular fluid with a 10 ml bers are secreted extracellularly. FGF3-8, syringe. The follicles were classified by their FGF10, FGF15, FGF17-19, and FGF21-23 have diameters: follicular diameter ≤ 2 mm, 2 < fol- a typical signal secretion sequence at the licular diameter ≤ 4 mm, 4 < follicular diameter N-terminus of approximately 20 amino acids, ≤ 6 mm, 6 < follicular diameter ≤ 8 mm, follicu- which can be secreted outside the cell and lar diameter > 8 mm. The aspirated follicular combined with receptors. fluid was collected in an EP tube and centri- fuged at 3000 rpm for 10 minutes. The granule FGF10, which was first cloned from rat embryos cells were washed with autoclaved PBS, fol- in 1996, belongs to the FGF7 (FGF3/7/10/22) lowed by centrifugation at 3000 rpm for 5 min. subfamily of 7 subfamilies [10], and it is an Finally, 1 ml of Trizol was added to lyse the essential gene for embryonic development. cells. The cell lysate was stored at -80°C until FGF10 is involved in many life activities such as use. cell proliferation, cell migration, and develop- ment and differentiation [17]. It has been In vitro maturation culture of oocytes reported that FGF10 functions as a paracrine factor [18, 19]. In mice and bovines, FGF10 is A 10 ml sterile syringe was used to extract ovar- expressed in oocytes, while its receptors are ian follicles of 2 to 6 mm above the surface of mainly expressed in cumulus and granulosa the ovary. Then the cumulus oocyte complexes cells [20-22]. During fetal ovary development, (COCs) with uniform cytoplasms and three or primitive, primary and secondary oocytes and more than three cumulus cells were collected granulosa cells exhibit an FGF10 immune under the stereo-microscope. Subsequently, response at different stages. In the mouse the COCs were washed 2-3 times in a washing ovary, FGF10 and its receptors are detected in medium (TCM-199 (Sigma-Aldrich) containing the cytoplasms of the oocytes, and FGFR2 is 2% FBS (Gibco) and 1.2 g HEPES (Sigma- also expressed in follicular cells. Also, the FGF- Aldrich), aggregated into a maturation medium 10 protein has been found in human oocytes (TCM-199 containing 10% FBS and FSH 0.2 and granulosa cells, and it may contribute to μg/ml (Sigma-Aldrich), and matured at 38.5°C, with 5% CO and 100% humidity for 24 h. The human preantral follicle development [23]. 2 oocytes were collected at 0 h, 12 h and 24 h, However, till now, to the best of our knowledge, respectively, and washed 3 times in PBS. Five there is no research about the expression and cells were transferred to an EP tube containing localization of FGF10 and its receptors in buf- Cell-to-cDNA II cell lysis buffer (Beyotime falo. Therefore, this experiment aimed to inves- Institute of Biotechnology) and stored at -80°C tigate the expression pattern of FGF10 and its for experiments. receptors during buffalo follicular development and oocyte maturation. QRT-PCR Materials and methods Total RNA from the granulosa cells was extract- ed using the Trizol reagent (Takara, Japan) in Buffalo ovaries and oocytes collection accordance with the instructions supplied by the manufacturer. The RNA concentration was Buffalo ovaries were obtained from slaughter measured using the NanoDrop ND-1000. Then, house in Nanning, and placed in 37°C normal total RNA was reverse transcribed into cDNAs 4935 Int J Clin Exp Pathol 2018;11(10):4934-4941 FGF10 expression pattern during buffalo follicular development using SuperScript II Reverse Transcriptase Tween-20 in PBS. The slides were incubated (Takara Bio) following the manufacturer’s proto- with a streptavidin-horseradish peroxidase- col. Then real-time quantitative PCR was per- conjugated goat anti-rabbit secondary anti- formed to detect the mRNA expression of buf- body, and diaminobenzidine was added to falo FGF10 and its receptors using the SYBR develop the tissues. Finally, the slides were Green PCR Master Mix reagent (Applied dehydrated, mounted and microscopically Biosystems, USA) by the Applied Biosystems examined under an Olympus microscope. 7500 Real-time PCR System. The reaction sys- tem was 20 μl, including 1 μl cDNA, 0.8 μl prim- Immunofluorescence ers (10 nM), 10 μl SYBR Premix Ex Taq (2X), 0.4 μl ROX Reference Dye II (50X), and 7.8 μl FGF10 was detected in PFA-fixed oocytes and RNase-free water. The reaction conditions were COCs. The COCs and cumulus-depleted oocytes as follows: 95°C for 10 min, 40 cycles of 95°C were washed twice in PBS containing 1% for 15 s and 60°C for 45 s. The primer sequenc- TritonX-100 (Sigma-Aldrich) and 0.3% BSA es were listed as follows: FGF10-forward-5’- (Sigma-Aldrich) for 5 min each time to remove CCTCCTCGTCCGTCTCCTT-3’ and reverse-5’- serum and other components. Then the cells were placed in 4% PFA (Sigma-Aldrich) at room AGCAACAACTCCGATTTCCA-3’; FGFR1b-forwa- temperature for at least one hour and washed rd-5’-ACGTCCTGGTGACGGAGG-3’ and reverse- three times for 5 min each time.
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