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Combined Melatonin and Poricoic Acid a Inhibits Renal Fibrosis Through TAJ0010.1177/2040622319869116Therapeutic Advances in Chronic DiseaseD-Q Chen, G Cao 869116research-article20192019 Therapeutic Advances in Chronic Disease Original Research Ther Adv Chronic Dis Combined melatonin and poricoic acid A 2019, Vol. 10: 1–19 DOI:https://doi.org/10.1177/2040622319869116 10.1177/ inhibits renal fibrosis through modulating 2040622319869116https://doi.org/10.1177/2040622319869116 © The Author(s), 2019. Article reuse guidelines: the interaction of Smad3 and β-catenin sagepub.com/journals- pathway in AKI-to-CKD continuum permissions Dan-Qian Chen, Gang Cao, Hui Zhao, Lin Chen, Tian Yang, Ming Wang, Nosratola D. Vaziri, Yan Guo and Ying-Yong Zhao Abstract Background: Acute kidney injury (AKI) is one of the major risk factors for progression to chronic kidney disease (CKD) and renal fibrosis. However, effective therapies remain poorly understood. Here, we examined the renoprotective effects of melatonin and poricoic acid A (PAA) isolated from the surface layer of Poria cocos, and investigated the effects of combined therapy on the interaction of TGF-β/Smad and Wnt/β-catenin in a rat model of renal ischemia-reperfusion injury (IRI) and hypoxia/reoxygenation (H/R) or TGF-β1-induced HK-2 cells. Methods: Western blot and immunohistochemical staining were used to examine protein expression, while qRT-PCR was used to examine mRNA expression. Coimmunoprecipitation, chromatin immunoprecipitation, RNA interference, and luciferase reporter gene analysis were employed to explore the mechanisms of PAA and melatonin’s renoprotective effects. Results: PAA and combined therapy exhibited renoprotective and antifibrotic effects, but the Correspondence to: Ying-Yong Zhao underlying mechanisms were different during AKI-to-CKD continuum. Melatonin suppressed Faculty of Life Science & Medicine, Northwest Smad-dependent and Smad-independent pathways, while PAA selectively inhibited Smad3 University, No. 229 Taibai phosphorylation through distrupting the interactions of Smad3 with TGFβRI and SARA. Further North Road, Xi’an, Shaanxi 710069, China studies demonstrated that the inhibitory effects of melatonin and PAA were partially depended zyy@nwu.edu.cn; on Smad3, especially PAA. Melatonin and PAA also inhibited the Wnt/β-catenin pathway and zhaoyybr@163.com Dan-Qian Chen its profibrotic downstream targets, and PAA performed better. We further determined that Hui Zhao IRI induced a nuclear Smad3/β-catenin complex, while melatonin and PAA disturbed the Lin Chen Tian Yang interaction of Smad3 and β-catenin, and supplementing with PAA could enhance the inhibitory Ming Wang Faculty of Life Science effects of melatonin on the TGF-β/Smad and Wnt/β-catenin pathways. & Medicine, Northwest Conclusions: Combined melatonin and PAA provides a promising therapeutic strategy to treat University, Xi’an, Shaanxi, China renal fibrosis during the AKI-to-CKD continuum. Gang Cao School of Pharmacy, Zhejiang Chinese Medical Keywords: melatonin, poricoic acid A, renal fibrosis, renal ischemia-reperfusion injury, TGF-β/ University, Hangzhou, China Smad, Wnt/β-catenin Nosratola D. Vaziri Division of Nephrology Received: 28 February 2019; revised manuscript accepted: 22 July 2019. and Hypertension, School of Medicine, University of California Irvine, CA, USA Yan Guo Faculty of Life Science Introduction factor for the development and progression of & Medicine, Northwest Patients surviving episodes of acute kidney injury chronic kidney disease (CKD), and, in particular, University, Shaanxi, China Department of Internal (AKI) can recover their renal function without fur- for promoting the transition of CKD to end-stage Medicine, University ther consequences for many years. However, recent renal disease (ESRD) ultimately requiring dialy- of New Mexico, 1–3 Comprehensive Cancer evidence based on epidemiological investigations sis. AKI and CKD have been seen as an inte- Center, Albuquerque, and outcome analyses showed that AKI is a risk grated clinical syndrome.4 Hypoxia, inflammation, NM, USA journals.sagepub.com/home/taj 1 Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). Therapeutic Advances in Chronic Disease 10 microvascular rarefaction, and dysbiosis of gut Although the molecular mechanisms underlying microbiota have been linked to the AKI-to-CKD the AKI-to-CKD continuum have been partly continuum.2,5,6 Renal ischemia/reperfusion injury revealed, no intervention has proved very effec- (IRI) has been used widely to investigate renal tive to block the AKI-to-CKD continuum. fibrosis from AKI to progressive CKD.7–10 Renal Pharma cologic treatment to block the AKI-to- fibrosis is always the common ultimate result of CKD continuum is urgently needed. In recent CKD, which is characterized by the process of epi- years, natural products have shown renoprotec- thelial-to-mesenchymal transition (EMT) and tive and antifibrotic effects.20–24 The surface layer excessive accumulation and deposition of extracel- of Poria Cocos (SLPC) exerts renoprotective lular matrix (ECM) components.11 Renal fibrosis is effects,25–29 and also has antifibrotic effects via induced by the activation of a large number of regulation of the TGF-β/Smad and Wnt/β- growth factors, cytokines, chemokines and toxins, catenin pathways.30,31 Poricoic acid A (PAA), as a among which transforming growth factor-β1 main triterpenoid compound of SLPC,32 exhibits (TGF-β1) and β-catenin are the central mediators a good antifibrotic effect in vivo and in vitro. in renal fibrosis.12,13 Additionally, melatonin, a secretory product of the pineal gland, has been reported to have antifi- The TGF-β/Smad and Wnt/β-catenin pathways brotic effect in the kidney.33–35 Although mela- play a significant role in fibrogenesis of the kid- tonin and PAA significantly alleviate renal ney. TGF-β signaling is a central mediator in fibrosis, their underlying mechanism remains renal fibrosis of progressive CKD.11,14 TGF-β undefined. In this study, we reveal the molecular exerts its profibrotic effect by transforming growth mechanism of a combined melatonin and PAA factor-β receptor II (TGFβRII), transforming intervention on the AKI-to-CKD continuum in growth factor-β receptor I (TGFβRI), and its renal IRI rats and hypoxia/reoxygenation (H/R) intracellular mediators Smads. The combination or TGF-β1 induced epithelial cells. Elucidating of TGF-β1 and TGFβRII recruits and phospho- the molecular mechanism of the inhibitory effect rylates TGFβRI, which causes phosphorylation of melatonin and PAA treatment on the AKI-to- of Smad2 and Smad3 via the junction of adaptor CKD continuum will support the development of proteins such as Smad anchor for receptor activa- therapeutic options to prevent progression from tion (SARA).15 The phosphorylations of Smad2 AKI to CKD. and Smad3 regulate downstream profibrotic fac- tor expressions. Smad4 also contributes to TGF- β1-induced fibrogenesis,16 while Smad7 is a Materials and methods negative regulator of the TGF-β/Smad pathway by inhibition of Smad2 and Smad3 phosphoryla- Materials tion.17 In the normal situation, the Wnt/β-catenin Melatonin was purchased from Sigma-Aldrich pathway is silent in adult kidney; once an injury (M5250, St. Louis, MO, USA). DMEM/F-12 occurs, Wnt/β-catenin signaling is reactive.12,15 and fetal bovine serum were purchased from Sustained activation of the Wnt/β-catenin path- Thermo Fisher Scientific (New York, NY, USA). way plays a decisive role in driving the AKI-to- SLPC was purchased from Shaanxi Medicinal CKD continuum and accelerates renal fibrosis.7 Materials Company (Xi’an, Shaanxi, China). The Profibrotic and fibrotic genes, including snail1, primary antibodies were purchased from Abcam twist, plasminogen activator inhibitor-1 (PAI-1), (Cambridge, MA, USA), Millipore (Billerica, fibroblast-specific protein 1 (Fsp-1) and matrix MA, USA), CST (Danvers, MA, USA), BD metalloproteinase-7 (MMP-7), are the down- Transduction Laboratories (San Jose, CA, USA), stream targets of Wnt/β-catenin signaling.18 Since Santa Cruz (Dallas, TX, USA), and Proteintech renin-angiotensin system (RAS) components are (Wuhan, Hubei, China). also directly downstream of Wnt/β-catenin sign- aling, the activation of Wnt/β-catenin signaling Primary antibodies against collagen I (ab34710, could upregulate the expression of RAS compo- Abcam), alpha smooth muscle actin (α-SMA, nents to accelerate kidney injury.19 Hence, inhibi- ab7817, Abcam), fibronectin (ab2413, Abcam), tion of the TGF-β/Smad and Wnt/β-catenin vimentin (ab92547, Abcam), E-cadherin pathways plays a critical role in attenuating renal (ab76055, Abcam), Wnt1 (ab85060, Abcam), fibrosis. dephosphorylated active β-catenin (05-665, 2 journals.sagepub.com/home/taj D-Q Chen, G Cao et al. Millipore), phosphorylated active β-catenin Northwest University (Permit Number: (Ser33/37/Thr41) (9561, CST), β-catenin SYXK2010-004). Male Sprague-Dawley rats (610154, BD Transduction Laboratories), snail1 with an age of 7 weeks old, weighing 180–200 g, (ab180714, Abcam), twist (ab50581, Abcam), were purchased from the Central Animal MMP-7 (ab5706, Abcam), PAI-1 (612024, BD Breeding House of Fourth Military Medical Transduction Laboratories), TGF-β1 (ab92486,
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