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The Antagonism of 6-Shogaol in High-Glucose-Activated NLRP3

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The Antagonism of 6-Shogaol in High-Glucose-Activated NLRP3 Chen et al. Cell Biosci (2020) 10:5 https://doi.org/10.1186/s13578-019-0372-1 Cell & Bioscience RESEARCH Open Access The antagonism of 6-shogaol in high-glucose-activated NLRP3 infammasome and consequent calcifcation of human artery smooth muscle cells Te‑Chuan Chen1, Chia‑Kung Yen2, Ying‑Chen Lu2, Chung‑Sheng Shi3,4, Rong‑Ze Hsieh3,5, Shun‑Fu Chang5* and Cheng‑Nan Chen6* Abstract Background: Vascular calcifcation is the major reason for high mortality of cardiovascular complications for diabe‑ tes. Interleukin (IL)‑1β has been implicated in this pathogenesis, but its precise role and clinical evidence have not been clearly identifed. Hence, this study was aimed to investigate whether high concentration of glucose (HG), which mimics the hyperglycemia environment, could initiate vascular calcifcation through NLRP3/IL‑1β infammasome and the underlying mechanism. Recently, 6‑shogaol, a major ginger derivate, has been elucidated its pharmaceutic role for various diseases. Therefore, the aims of this study also determined 6‑shogaol efect in vascular calcifcation of HG initiation. Result: Human artery smooth muscle cells (HASMCs) were used in this study. Glucose concentrations at 5 and 25 mM were defned as normal and HG status, respectively. The results showed that HG could increase the NLRP3, cleaved caspase 1, and pro/mature IL‑1β levels to induce the expressions of bone‑related matrix proteins and subse‑ quent HASMC calcifcation. This process was regulated by Akt activation and reactive oxygen species (ROS) produc‑ tion. Moreover, 6‑shogaol could inhibit the Akt/ROS signaling and NLRP3/caspase 1/IL‑1β infammasome and hence attenuated HASMC calcifcation. Conclusions: This study elucidates the detailed mechanism of HG‑initiated HASMC calcifcation through NLRP3/cas‑ pase 1/IL‑1β infammasome and indicates a potential therapeutic role of 6‑shogaol in vascular calcifcation complica‑ tion of diabetes. Keywords: 6‑Shogaol, Interleukin‑1β, NLRP3 Infammasome, Vascular calcifcation, Smooth muscle cells Background Vascular calcifcation is highly prevalent for the patients with diabetes and chronic renal diseases and contrib- utes to the further increased morbidity and mortality of cardiovascular complications. Although the therapeu- *Correspondence: [email protected]; [email protected] tic strategy for reducing blood glucose level has been 5 Department of Medical Research and Development, Chang Gung Memorial Hospital, Chiayi, Taiwan extensively investigated, the vascular calcifcation devel- 6 Department of Biochemical Science and Technology, National Chiayi opment in diabetes patients have still remained [1–5]. University, Chiayi 600, Taiwan Vascular calcifcation pathogenesis is a complex process Full list of author information is available at the end of the article © The Author(s) 2020. 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://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Chen et al. Cell Biosci (2020) 10:5 Page 2 of 10 with a phenotypic switch of vascular smooth muscle cells and status. And, 6-shogaol is the most dominant one (VSMCs) to osteoblast- or chondrocyte-like cells, which [30]. However, the molecular mechanism and metabolic initiates the upregulation and deposition of calcium fate of shogaols, including 6-shogaol, in antagonizing phosphate and mineralization-related proteins, includ- and improving the status of these diseases have not been ing osteopontin (OPN), osteocalcin (OCN), and alkaline clearly identifed. Terefore, the precise pharmaceutic phosphatase (ALP), in calcifcation regions and hence efects and targets of 6-shogaol should be further eluci- results in the stifening of vessel walls [6–8]. Moreover, dated and understood in order to more widely using it in the signaling related to the bone/cartilage growth, includ- the clinical application for various diseases therapy. ing the bone morphogenetic proteins, Akt signaling, and In this study, we investigated the role of NLRP3 infam- runx2 transcription activity, has also been associated masome in vascular calcifcation in response to high glu- with the occurrence of vascular calcifcation complica- cose environment and the possible antagonized role of tion of diabetes [8–12]. Currently, the precise mecha- 6-shogaol in this process. We found that NLRP3, cleaved nisms about how high blood glucose afects the vascular caspase 1, and pro/mature IL-1β proteins could be upreg- calcifcation pathogenesis in diabetes patients has not ulated to initiate human artery SMC (HASMC) calcif- been completely elucidated. Terefore, more detailed cation under high concentration of glucose stimulation. investigation and understanding is still urgent and nec- Moreover, this NLRP3 infammasome upregulation was essary for further improving the development of diabetes resulted from the Akt activation and ROS production. and its vascular calcifcation complications. Furthermore, we also demonstrated the antagonized role Vascular calcifcation derived from atherosclero- of 6-shogaol in NLRP3 infammasome activation and sis and diabetes has been demonstrated to be a chronic subsequent HASMC calcifcation. Our fndings provide infammation event, which is regulated by infamma- new insights into the understanding of NLRP3 infamma- tory cytokines such as tumor necrosis factor (TNF)-α some-initiated HASMC calcifcation under high glucose and interleukin (IL)-1β. Terefore, infammasome sys- stimulation and indicate a potential pharmaceutic role of tem has recently been implicated in the pathogenesis of 6-shogaol in cardiovascular complication of diabetes. vascular calcifcation [13–15]. NLRP3 complex, which is composed of NLRP3 protein, adaptor protein ASC, and Results caspase 1, has been indicated as one of important infam- High concentration of glucose (HG) initiates HASMC masomes because of its regulatory role in autoimmune calcifcation and infammation [16–18]. After receiving the stimula- OPN, OCN, and ALP, the well-known bone matrix pro- tions, intracellular NLRP3 level upregulation and sub- teins, inductions have been recognized as the markers of sequent caspase 1 activation could cleave the pro-IL-1β vascular calcifcation. HASMCs were kept as the controls and pro-IL-18 into mature and active IL-1β and IL-18 or were treated with 5 mM (normal concentration of and then consequently elicit infammatory responses glucose, NG) or 25 mM (high concentration of glucose, and diseases development [16–18]. Accumulating data HG) glucose or 25 mM mannitol (M) for 3, 7, and 14 days has indicated that infammasomes, including NLRP3 and then the mRNA and protein expressions of OPN, complex, are the important regulatory systems for the OCN and ALP were examined. Cells treated with HG development of chronic metabolic diseases. In this study, signifcantly induced the OPN, OCN, and ALP mRNA we further examine whether high concentration of glu- (Fig. 1a–c) and protein (Fig. 1d) expression within 3 days cose, mimics the hyperglycemia environment of diabe- and persisted for 14 days in HASMCs compared to the tes patients, stimulates vascular calcifcation through the controls and NG-/mannitol-treated cells. Moreover, we NLRP3 infammasome system. determined whether HG treatment initiates the HASMC Ginger has been widely used as the favoring agent and calcifcation. Cells were kept as the controls or were spice in the beverage and cooking in all over the world. treated with NG, mannitol, or HG for 14 days and then Accumulating data has also demonstrated the pharma- the HASMC calcifcation was examined. Cells treated ceutic role of ginger in various diseases such as anti-can- with NG and mannitol had no efect on the HASMC cal- cer [19, 20], anti-arthritis [21, 22], anti-gastrointestinal cifcation. However, cells treated with HG initiated an disease [23, 24], anti-infammation [25], anti-oxidation increase in HASMC calcifcation (Fig. 1e). [26], and anti-atherosclerosis [27–29]. It has been found that the pharmaceutic function of ginger is elicited by HG activates NLRP3 infammasome to modulate HASMC the nature of its bioactive compounds, including gin- calcifcation gerols and their dehydrated products, shogaols. Gener- Recently, NLRP3 infammasome has been implicated in ally, shogaols have been suggested to be more efective various diseases development. We determined whether than gingerols in attenuating the patients’ uncomfortable NLRP3 infammasome constituents, including NLRP3, Chen et al. Cell Biosci (2020) 10:5 Page 3 of 10 Fig. 1 HG initiates HASMC calcifcation. a–d HASMCs were kept as the controls or were treated with 5 mM (normal concentration of glucose, NG) or 25 mM (high
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