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The Protective Effect and Mechanism of Catalpol on High Glucose-Induced

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The Protective Effect and Mechanism of Catalpol on High Glucose-Induced Chen et al. BMC Complementary and Alternative Medicine (2019) 19:244 https://doi.org/10.1186/s12906-019-2656-8 RESEARCHARTICLE Open Access The protective effect and mechanism of catalpol on high glucose-induced podocyte injury Yan Chen1†, Qingpu Liu1†, Zengfu Shan1, Yingying Zhao1, Meng Li1, Baiyan Wang2, Xiaoke Zheng1,3* and Weisheng Feng1,3* Abstract Background: Catalpol, a natural iridoid glycoside in Rehmannia glutinosa, can alleviate proteinuria associated with diabetic nephropathy (DN), however, whether catalpol has a protective effect against podocyte injury in DN remains unclear. Methods: In this study, we used a high glucose (HG)-induced podocyte injury model to evaluate the protective effect and mechanism of catalpol against HG-induced podocyte injury. Cell viability was determined by the 3-(4,5- dimethylthiazolyl-2-yl)-2,5-diphenyltetrazolium bromide (MTT) method. The levels of lactate dehydrogenase (LDH), superoxide dismutase (SOD) and malondialdehyde (MDA) were measured by commercial assay kits. Cell apoptosis and reactive oxygen species (ROS) were determined by using flow cytometry. Tumour necrosis factor α (TNF- α), interleukin-1β (IL-1β) and interleukin-6 (IL-6) levels were determined by enzyme-linked immunosorbent assay (ELISA). The protein expression levels of B-cell lymphoma-2 (Bcl-2), Bcl2-associated x (Bax), cleaved caspase-3, nicotinamide adenine dinucleotide phosphateoxidaseenzyme4(NOX4),toll-likereceptor4(TLR4), myeloid differentiation primary response gene 88 (MyD88), p38 mitogen-activated protein kinase (p38 MAPK), phosphorylated p38 MAPK (p-p38 MAPK), nuclear factor kappa B inhibitor alpha (IκBα) and phosphorylated IκBα (p-IκBα) were measured by western blotting. In addition, Bcl-2, Bax, caspase-3 and nuclear factor kappa B (NF-κB) levels were determined by immunofluorescence staining. Results: Catalpol significantly increased cell viability and decreased LDH release in HG-induced podocyte injury. Catalpol significantly decreased ROS generation, apoptosis, level of MDA, levels of inflammatory cytokine TNF-α,IL-1β,andIL-6and increased SOD activity in HG-induced podocyte injury. Moreover, catalpol significantly decreased expression of cleaved caspase-3, Bax, NOX4, TLR4, MyD88, p-p38 MAPK, p-IκBα and NF-κB nuclear translocation, as well as increased Bcl-2 expression in HG-induced podocyte injury. Conclusion: Catalpol can protect against podocyte injury by ameliorating apoptosis and inflammation. These protective effects may be attributed to the inhibition of NOX4, which alleviates ROS generation and suppression of the TLR4/MyD88 and p38 MAPK signaling pathways to prevent NF-κB activation. Therefore, catalpol could be a promising drug for the prevention of DN. Keywords: Rehmannia glutinosa, Catalpol, Podocyte injury, Diabetic nephropathy, Mechanism * Correspondence: [email protected]; [email protected] †Yan Chen and Qingpu Liu contributed equally to this work. 1College of Pharmacy, Henan University of Chinese Medicine, Zhengzhou, Henan 450046, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Chen et al. BMC Complementary and Alternative Medicine (2019) 19:244 Page 2 of 10 Background proteinuria, which is closely related to podocyte injury Diabetes mellitus is a common endocrine disease that in DN [16, 17]. However, it is still unclear whether catal- leads to many dangerous complications, including diabetic pol has a protective effect against podocyte injury in nephropathy (DN). The number of DN patients is DN. In this study, we investigated the protective effect of expected to rise to 642 million by 2040 [1, 2]. DN, one of catalpol in an HG-induced podocyte injury model and the leading causes of end-stage renal disease (ESRD) we further explored the possible mechanism of catalpol worldwide, is characterized by the appearance of microal- against HG-induced podocyte injury. buminuria as the earliest clinical manifestation [3, 4]. From a clinical perspective, although the treatments for Methods hyperglycaemia and hypertension are the major treat- Materials ments used for DN [5], these treatments are not enough Catalpol was purchased from Nanjing Spring & Autumn to reverse the progression of DN. Biological Engineering Co., Ltd. (Jiangsu, China), Roswell Podocytes play a pivotal role in the pathogenesis of DN Park Memorial Institute (RPMI) 1640 medium was pur- [6]. In its early stages, DN is primarily a glomerular chased from Gibco (Gibco Company, USA), and foetal disease, podocyte loss is generally found in DN patients bovine serum (FBS) was purchased from Scitecher Co., and multiple studies have provided a correlation between Ltd. (Oxford, MS, USA). Lactate dehydrogenase (LDH), podocyte loss and albuminuria in DN [7–9]. Podocytes, malondialdehyde (MDA) and superoxide dismutase which are highly specialized and terminally differentiated (SOD) kits were provided by Jiancheng Bioengineering visceral epithelial cells, make up the glomerular filtration Institute (Jiangsu, China). Glucose and reactive oxygen barrier, cover the surface of the glomerular basement species (ROS) assay kit were purchased from Solarbio membrane, and play a key role in maintaining selective Life Sciences (Beijing, China). Antibodies for caspase-3 glomerular filtration [10]. Accumulating evidence suggests (ab13847), B-cell lymphoma-2 (Bcl-2) (ab59348), Bcl2- that podocyte injury is one of the main risk factors for associated x (Bax) (ab32503), nicotinamide adenine DN, and that alleviating podocyte injury can improve DN dinucleotide phosphate oxidase enzyme 4 (NOX4) [11–13]. However, there is a lack of effective therapeutic (ab133303), nuclear factor kappa B (NF-κB) (ab32536), drug to alleviate podocyte injury. TLR4 (ab22048) and MyD88 (ab135693) were purchased Catalpol (Fig. 1), an iridoid glycoside, is the chief active from Abcam (Cambridge, MA, USA). Antibody for β- component extracted from the root of Rehmannia actin (AC026) was purchased from Abclonal (Boston, glutinosa, which has long been used in traditional USA). Antibodies for p38 mitogen-activated protein Chinese medicine. Catalpol has been reported to have a kinase (p38 MAPK) (#8690), phosphorylated p38 MAPK wide range of pharmacological activities, including those (p-p38 MAPK) (#4511), nuclear factor kappa B inhibitor against DN [14, 15]. Several previous studies have shown alpha (IκBα) (#4814) and phosphorylated IκBα (p-IκBα) that catalpol can improve renal function and decrease (#2859) were purchased from Cell Signaling Technology (Danvers, MA, USA). Cell culture Conditionally immortalized mouse podocytes were pro- vided by the National Infrastructure of Cell Line Resource (Beijing, China). Podocytes were cultured in RPMI 1640 medium supplemented with 10% FBS, 100 U/mL penicillin, 0.1 mg/ml streptomycin and 10 U/mL of mouse recombinant interferon-γ (IFN-γ) (PeproTech, California, USA) at 33 °C in a humidified atmosphere containing 5% CO2. Podocytes were cultured in RPMI 1640 medium without IFN-γ at 37 °C for 10–14 days to induce differentiation. Cell viability Cell viability was determined by the 3-(4, 5- dimethylthiazolyl-2-yl)-2,5-diphenyltetrazolium bromide (MTT) method according to the manufacturer’s instruc- tion. Briefly, podocytes were plated in 96-well plates at a density of 4 × 103 cells/well and incubated with normal Fig. 1 The structure of catalpol glucose (NG, 5.5 mM glucose+ 34.5 mM mannitol), high Chen et al. BMC Complementary and Alternative Medicine (2019) 19:244 Page 3 of 10 glucose (HG, 40 mM glucose) and HG with catalpol at 10 5 cells/well and incubated with NG, HG or HG with different concentrations (1, 5, 10 μM) for 72 h. Mannitol catalpol as described for the cell viability assay. At the end (34.5 mM) was added to the NG group for osmotic con- of the treatment, the podocytes were washed with PBS trol [18]. Then, an MTT solution (5 mg/mL) was added three times and homogenized in 0.5 mL of buffer solution. to each well, and the podocytes were incubated for 4 h The homogenates were centrifuged, and the supernatants at 37 °C. The supernatants were then aspirated, and were used to measure the SOD activity and MDA level. 150 μL of dimethyl sulfoxide (DMSO) was added to SOD activity and MDA level were detected in terms of solubilize formazan crystals with shaking for 10 min. absorbance readings measured at 450 nm and 530 nm Absorbance readings of the test and control samples wavelength respectively with a microplate reader (Thermo were measured at 490 nm with a microplate reader Scientific, Boston, USA). (Thermo Scientific, Boston, USA) and cell viability is expressed in terms of the percentage viability, which was Determination of inflammatory cytokine levels in calculated as the ratio of the absorbance of a treated podocytes sample to the absorbance of the untreated control Inflammatory cytokines, tumour necrosis factor α (TNF- sample multiplied by 100. α), interleukin-1β (IL-1β) and interleukin-6 (IL-6)
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