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Osteomeles Schwerinae Extract and Its Major Compounds Inhibit Methylglyoxal-Induced Apoptosis in Human Retinal Pigment Epithelial Cells

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Osteomeles Schwerinae Extract and Its Major Compounds Inhibit Methylglyoxal-Induced Apoptosis in Human Retinal Pigment Epithelial Cells molecules Communication Osteomeles schwerinae Extract and Its Major Compounds Inhibit Methylglyoxal-Induced Apoptosis in Human Retinal Pigment Epithelial Cells 1, 2, , 2 1 3 Bo-Jeong Pyun y , Young Sook Kim * y, Ik Soo Lee , Dong Ho Jung , Joo-Hwan Kim and Jin Sook Kim 1,* 1 Herbal Medicine Division, Korea Institute of Oriental Medicine, 1672 Yuseongdae-ro, Yuseong-gu, Daejeon 34054, Korea; [email protected] (B.-J.P.); [email protected] (D.H.J.) 2 Research Infrastructure Team, Herbal Medicine Division, Korea Institute of Oriental Medicine, Daejeon 34054, Korea; [email protected] 3 Department of Life Science, Gachon University, Seongnam, Kyonggi-do 13120, Korea; [email protected] * Correspondence: [email protected] (Y.S.K.); [email protected] (J.S.K.) These authors contributed equally to this work. y Academic Editor: Masahide Hamaguchi Received: 29 April 2020; Accepted: 31 May 2020; Published: 3 June 2020 Abstract: The accumulation and formation of advanced glycation end products (AGEs) are related to diabetes and age-related disease. Osteomeles schwerinae C. K. Schneid. (Rosaceae, OSSC) is used traditionally for the treatment of various diseases in Asia. Previous studies have shown that OSSC elicits preventive effects in an in vivo model of diabetes. This study was to evaluate the antiapoptotic effects of dried leaves and twigs of OSSC extract and its major compounds in ARPE-19 cells—spontaneously arising human retinal pigment epithelial cells—under diabetic conditions. To examine the effects of an OSSC extract and its active compounds (acetylvitexin, hyperoside and quercitrin) on apoptosis in methylglyoxal (MG, the active precursor in the formation of AGEs)-treated ARPE-19 cells and the mechanism by which these effects occur, apoptosis was measured using flow cytometry analysis. Protein expression levels of phospho-p53 (p-p53), Bax and Bcl-2 were determined by western blot analyses. The OSSC extract inhibited apoptosis in MG-treated ARPE-19 cells in a dose-dependent manner. The major compounds also reduced the rate of apoptosis. Both the extract and major compounds also inhibited the expression of p-p53 and Bax and increased the levels of Bcl-2 that had been previously reduced by MG treatment. The OSSC extract (0.1 µg/mL) and its major compounds (0.01 µM) attenuated apoptosis in ARPE-19 cells under toxic diabetic conditions by downregulating of expression of p-p53 and Bax. OSSC may serve as an alternative therapy to retard the development of diabetic retinopathy. Keywords: Osteomeles schwerinae; diabetic retinopathy; methylglyoxal; apoptosis; human retinal pigment epithelial cells 1. Introduction The accumulation of advanced glycation end products (AGEs) is accelerated under conditions of chronic hyperglycemia and many age-related diseases [1]. Retinal pigment epithelial cells (ARPE-19 cells) are critical for the maintenance and survival of photoreceptors, as well as for the apoptosis of the RPE (retinal pigment epithelium) related to oxidative stress, inflammation and AGEs [2–4]. Methylglyoxal (MG), a highly reactive dicarbonyl compound, is an AGE precursor whose levels have been shown to increase in experimental and clinical diabetes [1]. Elevated MG levels have been shown to induce reactive oxygen species (ROS) production and apoptosis in various Molecules 2020, 25, 2605; doi:10.3390/molecules25112605 www.mdpi.com/journal/molecules Molecules 2020, 25, 2605 2 of 7 cell types [5–7]. Current research is focused on therapeutic and nutritional interventions to prevent apoptosis in diabetic retinopathy (DR) [8]. Osteomeles schwerinae C. K. Schneid. (OSSC), belonging to the family Rosaceae, is a perennial evergreen shrub, native to China that is harvested in the wild and used for local food [9]. Furthermore, this plant that has been used as a traditional Chinese medicine for the treatment of laryngopharyngitis, diarrhea, dysentery, folliculitis and hyperglycemia [10,11]. Previous studies have shown that OSSC ameliorates retinal endothelial cell apoptosis via the regulation of AGEs accumulation in the spontaneously diabetic torii rats [6,12]. Hyperoside, a compound of OSSC extract, has demonstrated significant inhibition of aldose reductase [13], the key enzyme in the polyol pathway during the pathogenesis of diabetic cataracts [14]. Furthermore, herbal extracts and their major compounds have been used for the treatment of diabetes and diabetic complications [15]. Here, we investigated whether an OSSC extract and its maker compounds could inhibit apoptosis in ARPE-19Molecules cells2020, 25 treated, x with MG, thereby demonstrating their potential use to prevent the development2 of 7 of DRCurrent by inhibiting research apoptosis is focused in on cultured therapeutic RPE and under nutritional toxic diabetic interventions conditions. to prevent apoptosis in diabetic retinopathy (DR) [8]. 2. Results Osteomeles schwerinae C. K. Schneid. (OSSC), belonging to the family Rosaceae, is a perennial evergreen shrub, native to China that is harvested in the wild and used for local food [9]. 2.1. Effects of the OSSC Extract and Its Major Compounds on the Viability of MG-Treated Cells Furthermore, this plant that has been used as a traditional Chinese medicine for the treatment of laryngopharyngitis,After treatment with diarrhea, 500 µM dysentery, MG for 24 folliculitis h, cell viability and hyperglycemia was not significantly [10,11]. Previous changed. studies However, have at a concentrationshown that of 1000OSSCµ M,ameliorates cell viability retinal was significantlyendothelial cell decreased apoptosis to 65%via (Figurethe regulation1A). FITC-conjugated of AGEs annexinaccumulation V and PI werein the used spontaneously to monitor diabetic the progression torii rats of [6,12]. apoptosis. Hyperoside, The percentage a compound of early of OSSC apoptotic (annexinextract, V has positive demonstrated/PI negative) significant and inhibition late apoptotic of aldose/necrotic reductase cells [13], (annexin the key enzyme V positive-negative in the polyol /PI pathway during the pathogenesis of diabetic cataracts [14]. Furthermore, herbal extracts and their positive) were determined. As shown in Figure1B, the percentage of apoptotic cells was significantly major compounds have been used for the treatment of diabetes and diabetic complications [15]. increasedHere, from we 6.11% investigated (control) whether to 99.68% an (atOSSC 5 mMextract MG). and MG its increasedmaker compounds the rate could of apoptosis inhibit in a concentration-dependentapoptosis in ARPE-19 cells manner. treated with MG, thereby demonstrating their potential use to prevent the developmentIn a previous of DR study, by inhibiting the purities apoptosis of maker in cultured compounds RPE under of toxic OSSC diabetic extract conditions. were analyzed by HPLC [12]. Here, we evaluated whether the extract and its maker compounds could affect cell viability2. Results in MG-treated ARPE-19 cells. As shown in Figure1C, MG inhibited cellular proliferation, and pretreatment with the OSSC extract and its maker compounds significantly attenuated this 2.1. Effects of the OSSC Extract and Its Major Compounds on the Viability of MG-Treated Cells inhibitory effect. After treatment with 500 μM MG for 24 h, cell viability was not significantly changed. However, 2.2. Eatff ectsa concentration of the OSSC of Extract 1000 μ andM, cell Its Makerviability Compounds was significantly on MG-Induced decreased Apoptosis to 65% (Figure 1A). FITC- conjugated annexin V and PI were used to monitor the progression of apoptosis. The percentage of As shown in Figure2A,B, MG increased the rate of apoptosis up to 30%; the OSSC extract and early apoptotic (annexin V positive /PI negative) and late apoptotic/necrotic cells (annexin V positive- eachnegative maker compound /PI positive) attenuatedwere determined. the MG-induced As shown in Figure increase 1B, in the apoptosis. percentageThe of apoptotic effectsof cells hyperoside was weresignificantly indistinguishable increased from from the 6.11% normal (control) control. to To 99 assess.68% (at the 5 emMffects MG). of the MG OSSC increased extract the and rate its of maker compoundsapoptosis on in apoptosis-related a concentration-dependent factors involvedmanner. in apoptosis, we examined the expression levels of p-p53, BaxIn and a previous Bcl-2 by study, western the purities blot analysis. of maker MG compounds induced aof 2.3- OSSC and extract 1.4-fold were increase analyzed in theby HPLC expression of p-p53[12]. andHere, Bax, we evaluated whereas whether the OSSC theextract extract and it itss maker major compounds compounds could reduced affect cell the viability levels of in these factors.MG-treated Bcl-2 levels ARPE-19 were reducedcells. As 0.8-fold shown afterin Figure MG treatment, 1C, MG inhibited whereas thecellular OSSC proliferation, extract and itsand maker compoundspretreatment increased with the Bcl-2 OSSC levels extract (Figure and its2C). maker compounds significantly attenuated this inhibitory effect. (A) Figure 1. Cont. Molecules 2020, 25, 2605 3 of 7 Molecules 2020, 25, x 3 of 7 (B) Figure 1.FigureEffects 1. Effects of the Osteomelesof the Osteomeles schwerinae schwerinaeC. K. C.Schneid. K. Schneid. (OSSC) (OSSC) extract extract andand its major compounds compounds on the viabilityon the viability of methylglyoxal of methylglyoxal (MG)-treated (MG)-treated cells; cells; (A (A)) proliferation proliferation rates. rates. Data Data are are representative representative of of threethree independent independent experiments experiments and and areare expressedexpressed
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