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Berberine Exerts a Protective Effect on Rats with Polycystic Ovary Syndrome

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Berberine Exerts a Protective Effect on Rats with Polycystic Ovary Syndrome Shen et al. Reproductive Biology and Endocrinology (2021) 19:3 https://doi.org/10.1186/s12958-020-00684-y RESEARCH Open Access Berberine exerts a protective effect on rats with polycystic ovary syndrome by inhibiting the inflammatory response and cell apoptosis Hao-Ran Shen1†, Xiao Xu1† and Xue-Lian Li1,2* Abstract Background: Polycystic ovary syndrome (PCOS) is a common endocrine disease of the female reproductive system that seriously affects women’s health. Berberine (BBR) has many pharmacological properties and is used as an insulin sensitizer. This study aimed to investigate the effect of BBR on PCOS and explore its related mechanisms. Methods: Forty-two rats were randomly divided into the following six groups (n = 7 per group): control, control + BBR, PCOS-normal diet (ND), PCOS-ND + BBR, PCOS-high-fat diet (HFD), and PCOS-HFD + BBR. The PCOS rat models were established by injecting rats with dehydroepiandrosterone. Further, the rats were gavaged with BBR (150 mg/ kg/d) for 6 weeks. Then, the body weight, HOMA-IR, and testosterone levels of all rats were determined. Cell apoptosis of ovary granulosa cells was determined by a TUNEL assay kit. Real-time quantification PCR (RT-qPCR) and western blotting were utilized to evaluate the expression of TLR4, LYN, PI3K, Akt, NF-kB, TNF-α, IL-1, IL-6,andcaspase-3. Results: BBR reduced the levels of insulin resistance and testosterone in PCOS rats. Additionally, the cell apoptosis rate increased significantly in PCOS rats (P < 0.05) and decreased after BBR treatment (P < 0.05). The results of RT-qPCR and western blotting showed that the expression levels of TLR4, LYN, PI3K, Akt, NF-kB, TNF-α, IL-1, IL-6,andcaspase-3 significantly increased in PCOS rats, while BBR suppressed their expression levels. Conclusions: BBR may relieve PCOS pathology and IR values by inhibiting cell apoptosis and by regulating the expression levels of TLR4, LYN, PI3K, Akt, NF-kB, TNF-α, IL-1, IL-6,andcaspase-3. Keywords: Polycystic ovary syndrome, Berberine, Insulin resistance, Testosterone, Cell apoptosis Background hirsutism, acne, insulin resistance (IR), and hyperandro- Polycystic ovary syndrome (PCOS) is one of the most genemia [3]. PCOS is associated with obesity, diabetes, common endocrine disorders, affecting 4–10% of the hypertension, endometrial cancer, and cardiovascular women of reproductive age [1, 2]. The clinical symptoms disease [4–7]. Some adverse symptoms of PCOS can be of PCOS include irregular menstrual cycles, infertility, ameliorated by regulating the menstrual cycle (oral contraceptive), by reducing blood testosterone levels * Correspondence: [email protected] (glucocorticoids), by improving IR (metformin), and by †Hao-Ran Shen and Xiao Xu contribute equally to this work and are co-first inducing ovulation (clomiphene) [8, 9]. However, long- authors. term drug treatments may result in gastrointestinal dis- 1Department of Gynecology, Obstetrics & Gynecology Hospital of Fudan University, No. 419 Fangxie Road, Shanghai 200011, P.R. China comfort, diarrhea, and other serious side effects that ad- 2Shanghai Key Laboratory of Female Reproductive Endocrine-Related versely affect the patient’s standard of living. Therefore, Diseases, No. 419 Fangxie Road, Shanghai 200011, P.R. China © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Shen et al. Reproductive Biology and Endocrinology (2021) 19:3 Page 2 of 11 the development of alternative treatment strategies for fed with an ND and injected with DHEA. The other rats women with PCOS is urgently needed. were fed with an ND and injected with 0.2 ml of sesame In recent years, increasing evidence has shown that oil (control and control + BBR groups). The main energy natural plant-based products may play a role in the materials of an ND and an HFD are shown in Table 1. treatment and management of PCOS [10, 11]. Berberine Methylene blue staining was used to examine the (BBR), a small molecule alkaloid isolated from plants, is changes of vaginal epithelial cells in the DHEA-treated the major active component of the Chinese herb rhi- rats under an optical microscope. The PCOS model was zoma coptidis (Huanglian) [12]. BBR has a variety of considered successful if the vaginal epithelial cells were pharmacological properties, including anti-inflammatory, continuously keratinized for 10 consecutive days [19]. antimicrobial, glucose- and cholesterol-reducing, anti- After 12 h of fasting (20,00 to 8:00), the venous blood cancer, and immunomodulatory activities [13–15]. A was extracted from the tails of the PCOS rats. Fasting study by Zhang et al. showed that BBR prevented obesity plasma glucose (FPG) levels were determined by using and IR in high-fat diet (HFD)-fed rats by partially modu- the ACCU-CHEK Performa glucose [20] meter (Roche lating the gut microbiota composition [16]. Additionally, Diabetes Care, USA), and the fasting insulin (FINS) another study indicated that the intake of BBR in the levels were determined using rat insulin ELISA kits short term improved some metabolic and hormonal dis- (Thermo Scientific, USA). In accordance with the orders in women with PCOS, and its related effects homeostasis model assessment of IR (HOMA-IR) might be associated with the changes in body compos- method [21], HOMA-IR = FINS × FPG/22.5. HOMA- ition in obesity and dyslipidemia [17]. However, the IR > 2.8 of the PCOS rats was considered to indicate the mechanisms of BBR in women with PCOS are currently presence of IR [11]. unclear. Subsequently, the rats in the control + BBR, PCOS- Therefore, in this study, a PCOS rat model was estab- HFD + BBR, and PCOS-ND + BBR groups were gavaged lished by injecting rats with dehydroepiandrosterone with BBR (150 mg/kg/d, Sigma-Aldrich, Louis, MO, (DHEA), and the therapeutic effect of BBR on IR in the USA). The BBR was dissolved with 0.5% sodium carbox- PCOS model was investigated. Additionally, the poten- ymethyl cellulose [Sangon Biotech (Shanghai) Co., LTD, tial mechanism of BBR on PCOS was explored by real- Shanghai, China]. The rats in the other groups were time quantification PCR (RT-qPCR) and western blot- gavaged daily with an equal volume of 0.5% sodium car- ting. These results will improve our understanding of boxymethyl cellulose. The treatments were administered the development of PCOS, and may provide a novel clin- for 6 weeks. ical treatment strategy for PCOS. Sample collection Methods At the end of the experiment, the body weights and Ethics statement HOMA-IR of all rats were determined. Further, all rats All animal experiments were conducted in strict accord- were euthanized by cervical dislocation, and serum and ance with the animal ethics standards and with ethics ovary tissue samples were collected from all rats. Add- approval from the Ethics Committee of Obstetrics and itionally, a part of each ovary tissue sample was fixed in Gynecology Hospital of Fudan University (no. [2015]45). polyformic acid solution. The remaining ovary tissue was stored at − 80 °C for subsequent experiments. Animals and treatments Female clean Sprague Dawley rats (6 weeks old, total n = 42) were obtained from the Shanghai Laboratory Histological analysis Animal Centre (SLAC, Shanghai, China), and were adap- For histological analysis, the fixed ovary tissue was em- tively fed for 3 days. The PCOS rat models were estab- bedded in paraffin, sectioned to a thickness of 5 mm, lished following the methods reported by Abramovich and stained with hematoxylin and eosin (HE). Slides et al. [18] with some modifications. The rats were first were scanned using the OPTIKA microscope (M.A.D. randomly divided into the following six groups (n =7 per group): control, control + BBR, PCOS-high fat diet Table 1 The main energy materials of normal diet and high-fat (HFD), PCOS-HFD + BBR, PCOS-normal diet (ND), and diet (kcal/100 g) PCOS-ND + BBR. The rats in the PCOS-HFD and Energy materials Normal diet High-fat diet PCOS-HFD + BBR groups were fed with an HFD and Protein 90.46 87.20 were injected with DHEA (source leaf organisms, Carbohydrate 212.96 207.10 S24516; 6 mg/100 g body weight with 0.2 ml of sesame Fat 48.58 166.20 oil) for 21 days to induce PCOS in IR rat models. The In total 352.00 460.50 rats in the PCOS-ND and PCOS-ND + BBR groups were Shen et al. Reproductive Biology and Endocrinology (2021) 19:3 Page 3 of 11 Co. LTD, Italy) and the morphological changes of the Table 2 The sequences of all primers ovary tissues were observed. Primer Sequence(5′-3′) TLR4-rF GTTCCTTTCCTGCCTGAGACC Serum parameter assay TLR4-rR AGGGTTTCCTGTCAGTACCA According to the manufacturer’s instructions, the levels LYN-rF TGAAGACTCAACCAGTTCCTGA of insulin and testosterone in sera were respectively measured using rat insulin and rat testosterone ELISA LYN-rR TTAGCTTTCCACCACTCCCC kits (KGE010, R&D systems, USA).
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