Interaction of lutein with phosphatidylcholine bilayers

doi:10.1016/0005-2736(86)90525-0

Biochimica et Biophysica Acta (BBA) - Biomembranes

Volume 860, Issue 2, 21 August 1986, Pages 286-292

https://doi.org/10.1016/0005-2736(86)90525-0 Get rights and content

Abstract

The interaction of lutein, an inhibitory uncoupler of mitochondrial oxidative phosphorylation, with phospholipid bilayers has been examined employing a variety of physical methods. Differential calorimetric scans revealed that incorporation of lutein into aqueous dispersions of dipalmitoylphosphatidylcholine broadened the main transition endotherm and decreased the transition enthalpy as well as the size of the cooperative unit without change in the temperature of transition. Permeability of the bilayer to ascorbate was enhanced significantly by the presence of lutein. The trapped volume of the vesicles was decreased. Incorporation of lutein broadened the NMR peaks of both the acyl side-chain methylene and terminal methyl protons without and change in the line-width of the choline head-group methyl proton signal. This indicated the ability of the compound to integrate deep into the hydrophobic regions of the phospholipids bilayer distal to the polar regions. These results suppor our earlier biochemical studies which revealed that the deleterious action of lutein on mitochondrial oxidative phosporylation could be due to its stability to interact with membrane components and perturb the structure.

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Electrical properties of phosphatidylcholine bilayers containing canthaxanthin or β-carotene, investigated by electrochemical impedance spectroscopy
2017, Journal of Electroanalytical Chemistry
Citation Excerpt :
Hereby, the better understanding of the physicochemical properties of carotenoids and their interactions with lipids is necessary to clarify the exact mechanism of their function in biological membranes. Numerous studies using the model systems have showed several effects of carotenoids on the structure and dynamics of lipid membranes e.g. nuclear magnetic resonance [16], light scattering [17], differential scanning calorimetry [18] or electron spin resonance [19]. In spite of such a broad experimental approach, the behavior of carotenoids, especially CAN and βC, in biological membranes is not unequivocally determined [20].
Electrochemical impedance spectroscopy technique was applied to study bilayer membranes formed with egg yolk phosphatidylcholine containing as an additional component one of two carotenoid pigments: canthaxanthin or β-carotene. The results show that both carotenoids present in the lipid membranes at relatively low concentration modify significantly electrical capacitance and electrical resistance of the membranes. Domain structures appear as a result of interactions between components within analyzed bilayers. The equilibrium of domain formation can explain the deviation from the additivity rule. This equilibrium was described by mathematical equations as well as verified experimentally. Moreover, the surface area of domains was calculated and their stoichiometry was proposed.
Properties of β-carotene and retinoic acid in mixed monolayers with dipalmitoylphosphatidylcholine (DPPC) and Solutol
2014, Colloids and Surfaces A: Physicochemical and Engineering Aspects
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In the past decades an extensive effort for better understanding of the co-packing of carotenoids and lipids inside the membranes and their molecular interactions has been undertaken. The structural properties and molecular dynamics of lipid lamellar phases in the presence of carotenoids have been studied by various experimental methods: nuclear magnetic resonance [1], electron paramagnetic resonance [2], light scattering [3], differential scanning calorimetry (DSC) [4] and X-ray diffractometry [5]. It was shown, that β-carotene (βC) had fluidizing behavior by decreasing the order within phospholipid membranes [2,6].
The liposoluble vitamins and carotenoids are sensitive molecules and their antioxidant properties can be dramatically affected when included in membrane environment or in encapsulated carriers as liposomes or lipid nanocapsules (LNCs). The formation and state of mixed monolayers at air–water interface of β-carotene (βC) or retinoic acid (RA) with dipalmitoylphosphatidylcholine (DPPC) as simplest membrane model or with Solutol (Sol) which forms the soft layer covering the LNCs were studied by means of surface pressure (π) and surface potential (ΔV) measurements. The mutual miscibility and interfacial organization of components in studied mixed monolayers was found to strongly depend on their composition. It was suggested a better inclusion of βC small quantities in pure DPPC monolayer at low surface pressure than for films with more βC at higher surface pressure. The measurements of surface properties were complemented by Atomic Force Microscopy (AFM) as a suitable technique for direct visualization at nanoscale level of the monolayer microheterogeneity and the presence of interfacial structures. It was also found that the addition of bigger amounts of βC led to the appearance of stripe like phase which is more deeply formed at higher surface pressure.
Molecular characteristics of astaxanthin and β-carotene in the phospholipid monolayer and their distributions in the phospholipid bilayer
2001, Chemistry and Physics of Lipids
The molecular characteristics of the monolayers of astaxanthin with polar group on the β-ionone ring in the molecule and β-carotene without polar group and their interactions in mixed carotenoid–phospholipid monolayers and the effects of carotenoids on the phase behavior of the phospholipid bilayers were examined by the monolayer technique and differential scanning calorimetry (DSC). We found from the monolayer study that β-carotene had an amphiphilic nature. The molecular assembly of astaxanthin in the monolayer at the hydrophobic/hydrophilic interface was more stable than that of β-carotene. Dimyristoylphosphatidylcholine (DMPC) in the monolayer was miscible with astaxanthin in the range of 0–0.4 mol fractions of astaxanthin, but not fully miscible with β-carotene even at low concentrations below 0.1 mol fraction of β-carotene. Surface potential and compression/expansion cycles of β-carotene monolayer indicated the formation of molecular aggregates by itself. DSC study showed that when small amount of astaxanthin was added, the transition temperature of dipalmitoylphosphatidylcholine (DPPC) was markedly shifted to lower temperatures and that the transition peak was asymmetrically broadened, indicative of a significant depression in cooperativity of the gel to liquid–crystalline transition. The asymmetric DSC endothermic bands of DPPC incorporating small amounts of astaxanthin were well fit by deconvolution into two to three domains containing different concentrations of astaxanthin. On the contrary, the incorporation of β-carotene resulted in a small depression of the main transition temperature with a slight broadening of the transition peak, suggesting a small miscibility of β-carotene with the phospholipid bilayer or a formation of aggregates of β-carotene in the membranes. These results suggest that there would be a high localized concentration in the phase separated membrane for astaxanthin or β-carotene to function effectively as scavenger.
Dipalmitoylphosphatidylcholine membranes modified with zeaxanthin: Numeric study of membrane organisation
2000, Biochimica et Biophysica Acta - Biomembranes
Citation Excerpt :
The results of the research carried out in the last decade show, in addition, that carotenoid pigments and in particular polar carotenoids, xanthophylls, are important biomolecules modifying the structural and dynamic properties of lipid membranes (see [3] for a review). Several experimental techniques have been applied to study the effect of carotenoid pigments on lipid membranes such as electron spin resonance [4–8], nuclear magnetic resonance [9,10], differential scanning calorimetry [11,12], circular dichroism [13], ultrasound absorption [14–16], quasi-elastic light scattering [17,18], fluorescence labelling of a lipid phase [19] and the interior of carotenoid pigmented liposomes [20]. In general, carotenoid pigments modify lipid membranes in a fashion similar to cholesterol, except the effect of xanthophylls is approximately twice as strong as this one observed in the case of cholesterol.
The model of a dipalmitoylphosphatidylcholine (DPPC) bilayer containing a xanthophyll pigment zeaxanthin (ZEA) is proposed. The model is based on the ten-state Pink-Green-Chapman model of a lipid monolayer. The Monte Carlo method of computer simulation has been applied. Our model of the lipid membrane consists of two lipid monolayers with ZEA molecules spanning the lipid bilayer. The concentration of ZEA molecules is assumed to be conserved. Within the model, the interactions between lipid monolayers in a bilayer exist through ZEA molecules only. The experimental data concerning the aggregation of ZEA in DPPC from the literature and from our research were applied as a criterion to fit the model parameters. The model gives the dependences of the main phase transition temperature on ZEA/DPPC molar ratio, the percentage of ZEA in a monomeric form on ZEA/DPPC molar ratio and on temperature. The dependences obtained within the model and the experimental ones are in qualitative agreement. The influence of intermolecular interaction parameters on ZEA aggregation has been discussed. The differences between the model and the experimental results concerning mainly the pattern of ZEA aggregation have been discussed. Analyses of the lipid microconfiguration allow to advance the hypothesis concerning the influence of ZEA on the membrane permeability.
Competitive carotenoid and cholesterol incorporation into liposomes: Effects on membrane phase transition, fluidity, polarity and anisotropy
2000, Chemistry and Physics of Lipids
Pure 1,2-dipalmitoyl-sn-glycero-3-phosphorylcholine (DPPC) or mixed DPPC:1,2-dipalmitoyl phosphatidyletanolamine (DPPE):1,2-dipalmitoyl diphosphatidylserine (DPPS) (17:5:3) liposomes were incorporated with 5 mol% dietary carotenoids (β-carotene, lutein and zeaxanthin) or with cholesterol (16 and 48 mol%) in the absence or presence of 15 mol% carotenoids, respectively. The carotenoid incorporation yields ranged from 0.42 in pure to 0.72 in mixed phospholipid liposomes. They decreased significantly, from 3 to 14%, in the corresponding cholesterol-doped liposomes, respectively. Highest incorporation yields were achieved by zeaxanthin and lutein in phospholipid liposomes while in cholesterol-containing liposomes, lutein was highest incorporated. The effects on membrane structure and dynamics were determined by differential scanning calorimetry, steady-state fluorescence and anisotropy measurements. Polar carotenoids and cholesterol cause similar, dose-dependent effects: ordering and rigidification revealed by broadening of the transition peak, and increase of anisotropy. Membrane hydrophobicity is determined by cholesterol content and carotenoid polarity. In cholesterol-doped liposomes, β-carotene is less incorporated than in cholesterol-free liposomes. Our observations suggest effects of carotenoids, even at much lower effective concentrations than cholesterol (8 to 80-fold), on membrane structure and dynamics. Although they are minor constituents of animal membranes, carotenoids may act as modulators of membrane phase transition, fluidity, polarity and permeability, and therefore, can influence the membrane physiology and pathology.
Exogenously incorporated ketocarotenoids in large unilamellar vesicles. Protective activity against peroxidation
2000, Biochimica et Biophysica Acta - Biomembranes
Citation Excerpt :
Incorporation into the bilayer is likely to influence the ability of both xanthophylls to act as antioxidants. Apolar carotenes have been reported to perturb the acyl chain packing and to increase bilayer permeability [23,28,29]. It might happen that canthaxanthin played this role in our system, thus reducing its antioxidant properties due to a higher accessibility of the lipids to the external oxidative agent.
The ability of astaxanthin and canthaxanthin as chain-breaking antioxidants was studied in Cu²⁺-initiated peroxidation of phosphatidylcholine large unilamellar vesicles (LUVs). Both carotenoids increased the lag period that precedes the maximum rate of lipid peroxidation, though astaxanthin showed stronger activity. For these experiments, different amounts of xanthophylls were exogenously added to previously made LUVs, non-incorporated pigment being afterwards removed. Differential scanning calorimetry assays with L-β,γ-dimyristoyl-α-phosphatidylcholine LUVs demonstrated that xanthophylls incorporated as described interact with the lipid matrix becoming interspersed among the phospholipid molecules.

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Regular paperInteraction of lutein with phosphatidylcholine bilayers

Abstract

FEBS Lett.

Methods Enzymol.

Chem. Phys. Lipid

Biochim. Biophys. Acta

J. Mol. Biol.

FEBS Lett.

J. Biol. Chem.

Biochim. Biophys. Acta

Nature (London)

Plant Physiol.

Plant Physiol.

Curr. Sci.

Indian J. Biochem. Biophys.

The Biochemistry of the Carotenoids

Biochim. Biophys. Acta

Essays Biochem.

Methods Membrane Biol.

Biochemistry

Regular paper
Interaction of lutein with phosphatidylcholine bilayers