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Protection of Polyphenols Against Glyco-Oxidative Stress: Involvement of Glyoxalase Pathway

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Protection of Polyphenols Against Glyco-Oxidative Stress: Involvement of Glyoxalase Pathway antioxidants Article Protection of Polyphenols against Glyco-Oxidative Stress: Involvement of Glyoxalase Pathway 1, 2, 2, 1, , Laura Cianfruglia y , Camilla Morresi y, Tiziana Bacchetti * , Tatiana Armeni * z 1, and Gianna Ferretti z 1 Department of Clinical Sciences, Section of Biochemistry, Biology and Physics, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy; [email protected] (L.C.); [email protected] (G.F.) 2 Department of Life and Environmental Sciences, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy; [email protected] * Correspondence: [email protected] (T.B.); [email protected] (T.A.) These authors share first authorship. y Research Center of Health Education and Promotion, Polytechnic University of Marche, Via Brecce Bianche, z 60131 Ancona, Italy. Received: 14 September 2020; Accepted: 14 October 2020; Published: 16 October 2020 Abstract: Chronic high glucose (HG) exposure increases methylglyoxal (MGO)-derived advanced glycation end-products (AGEs) and is involved in the onset of pathological conditions, such as diabetes, atherosclerosis and chronic-degenerative diseases. Under physiologic conditions the harmful effects of MGO are contrasted by glyoxalase system that is implicated in the detoxification of Reactive Carbonyl Species (RCS) and maintain the homeostasis of the redox environment of the cell. Polyphenols are the most abundant antioxidants in the diet and present various health benefits. Aims of the study were to investigate the effects of HG-chronic exposure on glyco-oxidation and glyoxalase system in intestinal cells, using CaCo-2 cells. Moreover, we studied the effect of apple polyphenols on glyco-oxidative stress. Our data demonstrated that HG-treatment triggers glyco-oxidation stress with a significant increase in intracellular Reactive Oxygen Species (ROS), lipid peroxidation, AGEs, and increase of Glyoxalase I (GlxI) activity. On the contrary, Glyoxalase II (GlxII) activity was lower in HG-treated cells. We demonstrate that apple polyphenols exert a protective effect against oxidative stress and dicarbonyl stress. The increase of total antioxidant capacity and glutathione (GSH) levels in HG-treated cells in the presence of apple polyphenols was associated with a decrease of GlxI activity. Keywords: methylglyoxal; glyoxalase system; AGEs (advanced glycation end-products); glutathione; hyperglycemia 1. Introduction Glyoxalase system is an important enzymatic system implicated in the detoxification of reactive carbonyl species (RCS) such as glyoxal (GO), methylglyoxal (MGO), and 3-deoxyglucosone (3-DG). In general, α-oxoaldehydes are products of glycolytic metabolism and can be formed during lipid peroxidation, or glycation. The effects of MGO, the most reactive metabolite, have been widely studied [1,2]. Accumulation of MGO to toxic level inhibits cell growth and induces cell death [3,4]. In fact, an abnormal accumulation of RCS triggers dicarbonyl stress, resulting in the formation of advanced glycation end-products (AGEs) and DNA modification. MGO can react also with other biomolecules such as nucleotides and basic phospholipids, thus yielding AGEs [5,6]. The increase in RCS contribute to cell and tissue dysfunction and is involved in ageing and in the molecular mechanisms of various chronic disease such as dyslipidemia, obesity, and vascular complications of diabetes [7,8]. Antioxidants 2020, 9, 1006; doi:10.3390/antiox9101006 www.mdpi.com/journal/antioxidants Antioxidants 2020, 9, x FOR PEER REVIEW 2 of 15 Antioxidants 2020, 9, 1006 2 of 15 mechanisms of various chronic disease such as dyslipidemia, obesity, and vascular complications of diabetes [7,8]. SeveralSeveral studiesstudies have have shown shown that that the the harmful harmful effect effsects of MGO of MGO are contrasted are contrasted by glyoxalase by glyoxalase system system[9,10]. Glyoxalase [9,10]. Glyoxalase system comprises system comprises two consecutive two consecutive enzymes: enzymes:glyoxalase glyoxalaseI (GlxI) and Iglyoxalase (GlxI) and II glyoxalase(GlxII). D-Lactate II (GlxII). is a D-Lactate final product is a and final glutathione product and (GSH) glutathione is used as (GSH) cofactor isused [11]. asGlyoxalase cofactor I [ 11(EC]. Glyoxalase4.4.1.5), a lactoylglutathione I (EC 4.4.1.5), a lactoylglutathione lyase, catalyzes lyase, the isomerization catalyzes the isomerizationof the hemithioacetal of the hemithioacetal formed non- formedenzymatically non-enzymatically from MGO from and MGO reduced and reducedGSH to GSH form to S-D-lactoylglutathione. form S-D-lactoylglutathione. Glyoxalase Glyoxalase II (EC II (EC3.1.2.6), 3.1.2.6), hydroxyacylglutathione hydroxyacylglutathione hydrolase, hydrolase, catalyzes catalyzes the the hydrolysis hydrolysis of ofS-D-lactoylglutathione S-D-lactoylglutathione to toD- D-lacticlactic acid acid and and restores restores the the GSH GSH molecule molecule spent spent in in the the first first reaction reaction [12] [12 ](Figure (Figure 1).1). Figure 1. Methylglyoxal (MGO) formation from intermediates of glucose, protein and fat metabolism, Figure 1. Methylglyoxal (MGO) formation from intermediates of glucose, protein and fat metabolism, and its degradation by the Glyoxalase System. Glyoxalase I (GlxI) converts hemithioacetal formed from and its degradation by the Glyoxalase System. Glyoxalase I (GlxI) converts hemithioacetal formed glutathione (GSH) and methylglyoxal (MGO) into S-D-Lactoylglutathione (SLG) which is hydrolyzed from glutathione (GSH) and methylglyoxal (MGO) into S-D-Lactoylglutathione (SLG) which is by Glyoxalase II (GlxII) to D-lactic acid and GSH. Abbreviations: AGEs, advanced glycation end hydrolyzed by Glyoxalase II (GlxII) to D-lactic acid and GSH. Abbreviations: AGEs, advanced products; DHAP, dihydroxacetone phosphate; ROS, reactive oxygen species; GSH, reduced glutathione; glycation end products; DHAP, dihydroxacetone phosphate; ROS, reactive oxygen species; GSH, GR, glutathione reductase. reduced glutathione; GR, glutathione reductase. Metabolic dysfunction involved in an increase of MGO, and consequently AGEs formation is associatedMetabolic with andysfunction increased Reactiveinvolved Oxygen in an increase Species of (ROS) MGO, formation and consequently [13]. Dicarbonyl AGEs stressformation can be is increasedassociated by with oxidative an increased stress. In Reactive fact, oxidative Oxygen stress Spec canies (ROS) lead to formation a depletion [13]. of GSH Dicarbonyl thus compromising stress can be theincreased pathway by of oxidative glyoxalases stress. that detoxifyIn fact, fromoxidative MGO bystress using can GSH lead [14 to]. Hyperglycemia,a depletion of associatedGSH thus withcompromising diabetes, increased the pathway MGO andof glyoxalases ROS formation. that Fordetoxify instance, from incubation MGO by of erythrocytesusing GSH with[14]. highHyperglycemia, concentrations associated of glucose with increases diabetes, the formationincreased ofMGO MGO and metabolized ROS formation. to D-lactic For acid instance, by the glyoxalaseincubation pathway.of erythrocytes This increase with high was concentrat proportionalions toof glucoseglucoseconcentrations increases the formation ranging from of MGO 5 to 100metabolized mM and itto has D-lactic been proposedacid by the that glyoxalase the glyoxalase pathway. system This could increase be implicated was proportional in the progress to glucose of chronicconcentrations clinical complicationsranging from 5 associated to 100 mM with and diabetes it has been mellitus proposed [15,16 that]. the glyoxalase system could be implicatedSeveral studies in the have progress shown of thatchronic glyoxalase clinical systemcomplications has a physio-pathologicalassociated with diabetes role inmellitus other chronic[15,16]. diseases. Indeed, it was shown that GlxI reduced dicarbonyl and oxidative stress and preventedSeveral age-related studies have endothelial shown dysfunction,that glyoxalase a major system contributor has a physio-pathological to cardiovascular role disease in other [17]. Dicarbonylchronic diseases. stress is Indeed, a mediator it was that contributesshown that to GlxI vascular reduced complications dicarbonyl and and obesity oxidative diabetes-related stress and andprevented is involved age-related in cerebrovascular endothelial diseases dysfunction, and neurological a major contributor disorders to [18 cardiovascular,19]. Therefore, disease a growing [17]. Dicarbonyl stress is a mediator that contributes to vascular complications and obesity diabetes- interest is devoted to molecules able to decrease dicarbonyl stress targeting the glyoxalase system. related and is involved in cerebrovascular diseases and neurological disorders [18,19]. Therefore, a Our recent study has shown that high glucose concentration triggers an increase of levels of intracellular Antioxidants 2020, 9, 1006 3 of 15 ROS, lipid peroxidation, and formation of fluorescent AGEs and GA-modified proteins in intestinal cells [20]. Aims of the study were to investigate the effects of high glucose chronic exposure on glyco-oxidation and glyoxalase system in intestinal cells, using CaCo-2 cells. Moreover, we studied the effect of apple polyphenols on glyco-oxidative stress. The CaCo-2 cell line is an important tool in assessing various gastrointestinal functions and is widely used to investigate gastrointestinal oxidant metabolism on a cellular level [21]. In CaCo-2 cells, antioxidant enzymes include glutathione peroxidase, catalase, and paraoxonase-2 (PON2) [22]. Glyoxalase activities
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