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Effect of Different Anthocyanidin Glucosides on Lutein Uptake By molecules Article Effect of Different Anthocyanidin Glucosides on Lutein Uptake by Caco-2 Cells, and Their Combined Activities on Anti-Oxidation and Anti-Inflammation In Vitro and Ex Vivo Minh Anh Thu Phan 1,*, Martin Bucknall 2 and Jayashree Arcot 1,* ID 1 Food and Health Cluster, School of Chemical Engineering, UNSW, Sydney, NSW 2052, Australia 2 Mark Wainwright Analytical Centre, UNSW, Sydney, NSW 2052, Australia; [email protected] * Correspondence: [email protected] (M.A.T.P.); [email protected] (J.A.); Tel.: +61-2-9385-5360 (J.A.) Academic Editors: Natália Martins and Derek J. McPhee Received: 23 July 2018; Accepted: 11 August 2018; Published: 14 August 2018 Abstract: The interactive effects on anti-oxidation and anti-inflammation of lutein combined with each of the six common anthocyanidin glucosides were studied in both chemical and cellular systems. The combined phytochemicals showed an antagonism in the inhibition of lipid oxidation in a liposomal membrane, but showed an additive effect on cellular antioxidant activity in Caco-2 cells. Lutein was an active lipoxygenase inhibitor at 2–12 µM while anthocyanins were inactive. The concentration of lutein when it was used in combination with anthocyanins was 25–54% higher than when lutein was used alone (i.e., IC50 = 1.2 µM) to induce 50% of lipoxygenase inhibition. Only the combination of lutein with malvidin-3-glucoside showed anti-inflammatory synergy in the suppression of interleukin-8, and the synergy was seen at all three ratios tested. Some mixtures, however, showed anti-inflammatory antagonism. The presence of anthocyanins (5–7.5 µM) did not affect lutein uptake (2.5–5 µM) by Caco-2 cells. Keywords: anthocyanins; lutein; interaction; cellular antioxidant activity; anti-inflammatory activity; cellular uptake interference 1. Introduction Lutein is a xanthophyll carotenoid mainly present in dark green leafy vegetables [1]. Lutein shows antioxidant and anti-inflammatory activities by targeting reactive oxygen species, and downregulating inflammatory proteins and pro-inflammatory cytokines [2]. Lutein is one of the three xanthophyll carotenoids that can cross the blood-brain barrier and selectively accumulate in the retina and brain tissues [1,3,4]. The xanthophyll lutein is often co-ingested with other plant phytochemicals such as carotenoids and/or flavonoids in a normal human diet containing plant-based foods. Anthocyanins are one of the largest classes of flavonoids and are present abundantly in many fruits and vegetables [5]. Thus, there are chances for lutein and anthocyanins to be concurrently consumed in a meal, after which they can interact with each other during digestion and absorption to effect biological activities. Water-soluble phytochemicals may interfere with the uptake of lipid-soluble bioactive compounds [6]. For instance, lutein uptake by Caco-2 cells is impaired by the flavonoid naringenin, but is not affected by (+)-catechin, a phenolic acid, or vitamin C [1]. Absorption interference between phytochemicals may result in changes on combined biological effects of the compounds [6]. We have published a paper reporting that anthocyanins increase β-carotene uptake by Caco-2 cells to levels that trigger β-carotene’s pro-oxidant activity, which results in an antagonistic cellular antioxidant effect seen Molecules 2018, 23, 2035; doi:10.3390/molecules23082035 www.mdpi.com/journal/molecules Molecules 2018, 23, x 2 of 12 Moleculeswhich 2018results, 23, 2035 in an antagonistic cellular antioxidant effect seen in some combinations2 of [7]. 11 Phytochemical interactions on cellular uptake and biological activities are often studied separately, so the mutual influences between these aspects are not well addressed. This study aimed to ininvestigate some combinations the effect [of7]. different Phytochemical common interactions anthocyanidin on cellular glucosides uptake on andlutein biological uptake by activities Caco-2 arecells, often and studied the separately,combined soeffects the mutual of anthocyanins influences between and lutein these aspectson oxidative are not wellinhibition addressed. and Thisanti-inflammation study aimed to in investigate both chemical the effectand cellular of different models. common anthocyanidin glucosides on lutein uptake by Caco-2 cells, and the combined effects of anthocyanins and lutein on oxidative inhibition and2. Results anti-inflammation and Discussion in both chemical and cellular models. 2. Results and Discussion 2.1. Effects of Lutein-Anthocyanin Combinations on Oxidative Inhibition in Chemical and Cellular Models 2.1. Effects of Lutein-Anthocyanin Combinations on Oxidative Inhibition in Chemical and Cellular Models 2.1.1. Inhibitory Effect on Liposome Peroxidation 2.1.1. InhibitoryThe percentage Effect onof thiobarbituric Liposome Peroxidation acid reagent species (%TBARS) inhibition when lutein was presentThe percentagealone was of39%, thiobarbituric and when acidanthocyanins reagent species were present (%TBARS) alone, inhibition %TBARS when inhibition lutein waswas present14–43%. alone Lutein was combined 39%, and with when each anthocyanins of the tested were anthocyanins present alone, did %TBARS not enhance inhibition the inhibitory was 14–43%. effect Luteinon lipid combined peroxidation with eachin the of liposomal the tested membrane. anthocyanins The did expected not enhance additive the effects inhibitory of TBARS effect inhibition on lipid peroxidationof lutein-anthocyanin in the liposomal mixtures membrane. were 48–66%, The but expected the actual additive effects effects of the ofmixtures TBARS were inhibition less than of lutein-anthocyanin35% (Figure 1). This mixtures indicates were that 48–66%,lutein and but anth theocyanins actual effects showed of the an mixturesantagonistic were interaction less than at 35% the (Figureinterface1). of This the indicates liposomal that membrane. lutein and Lutein anthocyanins is a xanthophyll showed carotenoid an antagonistic characterized interaction with at polar the interfacegroups at of the the two liposomal ends of membrane.its molecule. Lutein Lutein is can a xanthophyllposition itself carotenoid in parallel characterized closely to the withpolar polarheads groupsof the atmembrane, the two ends or it of can its molecule.span the molecule Lutein can acro positionss the membrane itself in parallel withclosely the polar to theends polar anchoring heads of to thethe membrane, polar lipid orheads it can [8]. span Anthocyanin the molecule compounds across the ar membranee normally with positioned the polar in ends the aqueous anchoring region to the of polarthe membrane lipid heads [outer8]. Anthocyanin monolayer compounds[9]. Such orientations are normally of positioned the compounds in the aqueous in the regionlipid bilayer of the membranemembrane outer may monolayer enable them [9]. to Such interact orientations and form of the lutein-anthocyanin compounds in the adducts, lipid bilayer which membrane result in may the enablereduced them capability to interact of and lipid form peroxidation lutein-anthocyanin inhibition. adducts, The which formation result inof theadducts reduced between capability other of lipidcarotenoids peroxidation and flavonoids, inhibition. for The example: formation β-carotene of adducts and between green tea other polyphenolic carotenoids compounds and flavonoids, [10] or forβ-carotene example: andβ-carotene daidzein and [11], green has tea been polyphenolic previously compounds reported to [10 impart] or β-carotene antioxidant and antagonism daidzein [11 ],in hasliposomes. been previously reported to impart antioxidant antagonism in liposomes. 80 60 40 * * * 20 * TBARS inhibition (%) TBARS inhibition * * 0 LUT-CG LUT-DG LUT-MG LUT-PNG LUT-PLG LUT-PTG Combination FigureFigure 1. 1. LiposomeLiposome peroxidation inhibitory inhibitory activity activity of of different different lutein-anthocyanin lutein-anthocyanin combinations combinations (1:1 (1:1ratio). ratio). The horizontal The horizontal lines illustra lineste illustrate the expected the additive expected effect additive of lutein-anthocyanin effect of lutein-anthocyanin combinations. combinations.Asterisk-marked Asterisk-marked columns indicate columns a significant indicate difference a significant (p < 0.05) difference between (p <the 0.05) observed between effect the of observedthe mixture effect with of its the calculated mixture additive with its effect. calculated Calculation additive of the effect. expected Calculation additive of effect the was expected based additiveon an equation effect was of basedFuhrman on anet al. equation [12]: TBARS of FuhrmanA + TBARS et al.L − [12 TBARS]: TBARSA × ATBARS+ TBARSL/100L (TBARS− TBARSA andA ×TBARSTBARSL Lare/100 %TBARS (TBARS Ainhibitionand TBARS of Lanthocyaninare %TBARS alon inhibitione and oflutein anthocyanin alone respectively), alone and lutein which alone was respectively),calculated following which was an calculatedequation given following in [7]. an equationTBARS: thiobarbituric given in [7]. TBARS:acid reagent thiobarbituric species, acidLUT: reagentlutein, species,CG: kuromanin LUT: lutein, CG:chloride, kuromanin DG: chloride,myrtillin DG: chloride, myrtillin MG: chloride, oenin MG: chloride, oenin chloride, PNG: PNG:peonidin-3-glucoside peonidin-3-glucoside chloride, chloride, PLG: PLG: callistephin callistephin chloride, chloride, PTG: PTG: petunidin-3-glucoside petunidin-3-glucoside chloride. chloride. Molecules 2018, 23, 2035 3 of 11 2.1.2. Cellular Antioxidant Activity (CAA) The interactive effects on anti-oxidation
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