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Curcumin Loaded Nanoliposomes Localization by Nanoscale Characterization International Journal of Molecular Sciences Article Curcumin Loaded Nanoliposomes Localization by Nanoscale Characterization 1, , 1, 2 3 Elmira Arab-Tehrany * y, Kamil Elkhoury y , Gregory Francius , Loic Jierry , Joao F. Mano 4 , Cyril Kahn 1 and Michel Linder 1 1 LIBio, Université de Lorraine, F-54000 Nancy, France; [email protected] (K.E.); [email protected] (C.K.); [email protected] (M.L.) 2 LCPME, CNRS-Université de Lorraine, F-54600 Villers-lès-Nancy, France; [email protected] 3 Institut Charles Sadron, CNRS-Université de Strasbourg, F-67034 Strasbourg, France; [email protected] 4 Department of Chemistry, CICECO—Aveiro Institute of Materials, University of Aveiro, 3810-193 Aveiro, Portugal; [email protected] * Correspondence: [email protected]; Tel.: +33-3-72-74-41-05 These authors contributed equally to this work. y Received: 10 September 2020; Accepted: 26 September 2020; Published: 1 October 2020 Abstract: Curcumin is a hydrophobic drug gaining growing attention because of its high availability, its innocuity, and its anticancer, antitumoral, and antioxidative activity. However, its poor bioavailability in the human body, caused by its low aqueous solubility and fast degradation, presents a big hurdle for its oral administration. Here, we used nano-vesicles made of phospholipids to carry and protect curcumin in its membrane. Various curcumin amounts were encapsulated in the produced phospholipid system to form drug-loaded liposomes. Curcumin’s Concentration was evaluated using UV-visible measurements. The maximal amount of curcumin that could be added to liposomes was assessed. Nuclear magnetic resonance (NMR) analyses were used to determine curcumin’s interactions and localization within the phospholipid membrane of the liposomes. X-ray scattering (SAXS) and atomic force microscopy (AFM) experiments were performed to characterize the membrane structure and organization, as well as its mechanical properties at the nanoscale. Conservation of the membrane’s properties is found with the addition of curcumin in various amounts before saturation, allowing the preparation of a defined nanocarrier with desired amounts of the drug. Keywords: curcumin; liposomes; nanoscale characterization; drug-phospholipid interaction 1. Introduction Curcumin is a hydrophobic drug extracted from Curcuma longa, generally known as a spice or as a natural yellow pigment [1,2]. It is non-toxic, largely consumed, and easily obtained. For centuries, crude curcumin, a traditional Asian medicine, was used as a food spice and dietary supplement [3,4]. Curcumin or its family, curcuminoids, exhibits many potential benefits and pharmacological activities such as anti-cancer, anti-Alzheimer, antifungal, antibacterial, antioxidant, and anti-inflammatory agents [5–7]. Curcumin is Generally Recognized as Safe (GRAS) by the FDA, which strengthens its case as a potential natural drug [8]. However, its hydrophobic nature makes it practically insoluble in water which increases the rate of its metabolism resulting in poor bioavailability for humans after oral administration [9–11]. To improve the bioavailability of fragile and hydrophobic drugs, nanocarriers have been developed to protect the encapsulated drug from enzymatic degradation, provide controlled release, alter their Int. J. Mol. Sci. 2020, 21, 7276; doi:10.3390/ijms21197276 www.mdpi.com/journal/ijms Int. J. Mol. Sci. Sci. 20202020,, 2121,, x 7276 FOR PEER REVIEW 2 of 14 alter their pharmacokinetics, prolong their residence in plasma, and improve their cytoprotective and pharmacokinetics,antioxidant effects prolong [12,13]. theirThe residencetargeted delivery in plasma, and and cellular improve internalization their cytoprotective of curcumin and antioxidant are also eimprovedffects [12, 13by]. its The encapsulation targeted delivery in nanoparticles and cellular and internalization nanoemulsions of curcumin [14]. It is areimportant, also improved however, by itsthat encapsulation the chosen nanocarrier in nanoparticles is non-toxic and nanoemulsions and biodegradable, [14]. It as is important,well as able however, to provide that a thehigh chosen drug nanocarrierloading efficiency is non-toxic and a controlled and biodegradable, drug release, as well whil ase presenting able to provide additional a high biological drug loading benefits efficiency when andadministered a controlled with drug the drug. release, Regarding while presenting these constr additionalaints, liposomes biological are benefitsa promising when delivery administered system withdue to the their drug. phospholipid Regarding bilayer these constraints, structure, which liposomes is similar are a to promising the cellular delivery membrane. system Liposomes due to their are phospholipidnano-scale systems bilayer widely structure, used which for the is encapsulation, similar to the cellulardelivery, membrane. and controlled Liposomes release areof biologically nano-scale systemsactive agents widely [15–17]. used The for theunique encapsulation, architecture delivery, of liposomes andcontrolled allows the releaseloading of of biologically hydrophobic active and agentshydrophilic [15–17 therapeutic]. The unique molecules; architecture their of liposomes charge and allows surface the loading properties of hydrophobic can be tuned and hydrophilic to enable therapeuticstability during molecules; storage, their control charge over and the surface drug-release properties rate, canand beto tunedmeet specific to enable therapeutic stability during needs storage,[18,19]. All control these over features thedrug-release allow liposomal rate, nanoformulations and to meet specific to improve therapeutic the needsdrug therapeutic [18,19]. All index these featuresand decrease allow its liposomal side effects nanoformulations [20]. to improve the drug therapeutic index and decrease its side eMadeffects [of20 ].phospholipids, amphiphilic molecules commonly found in cells membrane and essentialMade for of its phospholipids, structure [21–24], amphiphilic liposomes molecules can encapsulate commonly and found protect in cells hydrophobic membrane and drugs essential in its formembrane its structure before [21 fusion–24], liposomes with the cantargeted encapsulate cell membranes, and protect and hydrophobic thus allowing drugs the in drug its membrane release at beforesufficient fusion concentration with the targeted[25]. Moreover, cell membranes, the surface andof liposomes thus allowing can also the be drug functionalized release at to su ffifurthercient concentrationincrease its targeting [25]. Moreover, efficiency the [26,27]. surface ofPreviously, liposomes curcumin can also be has functionalized been encapsulated to further in increaseliposomes its targetingderived from efficiency natural [26 lecithin,27]. Previously, to assess its curcumin release in has simulated been encapsulated environments in liposomes and its effect derived on breast from naturalcancer cells lecithin and to primary assess its cortical release neurons in simulated [9,10,28,29]. environments Recently, and Sarkar its effect and on Bose breast showed cancer cellsthat andcurcumin primary loaded cortical liposomes neurons released [9,10,28 ,from29]. Recently,3D printe Sarkard calcium and phosphate Bose showed scaffold that curcuminwas cytotoxic loaded to liposomesbone cancer released cells (osteosarcoma) from 3D printed while calcium promoting phosphate the viability scaffold and was proliferation cytotoxic of to healthy bone cancer bone cells (osteosarcoma)(osteoblasts) [30]. while promoting the viability and proliferation of healthy bone cells (osteoblasts) [30]. However, the drug-carrier interactions betweenbetween liposomes and curcumin are still poorly comprehended. The The goal goal of of this this study study is isto to addr addressess the the influence influence of encapsulated of encapsulated curcumin curcumin on the on theliposomal liposomal carrier carrier for forvarious various amounts amounts of ofloaded loaded drug drug and and understand understand interactions interactions at at the the molecular molecular level beforebefore aa potentialpotential useuse asas aa drugdrug/drug-carrier/drug-carrier couple.couple. The innocuity of the used curcumin and the phospholipids was of major interest in the design of the drug/drug-carrier drug/drug-carrier couple, as well as their origins and the presencepresence ofof phospholipidsphospholipids inin cellscells membrane.membrane. A multiscale approach was used to study the interaction between curcumin and the phospholipid membrane of liposomes, which to be employed as a drug carrier to protect,protect, transport,transport, andand deliverdeliver curcumin.curcumin. 2. Results and Discussion 2. Results and Discussion 2.1. Curcumin Purity 2.1. Curcumin Purity Curcumin dissolved in methanol/chloroform or deuterated chloroform was analyzed by HPLC and 1CurcuminH NMR, respectively.dissolved in Accordingmethanol/chloroform to the absorbance or deuterated at l = 425chloroform nm, we was observed analyzed two by peaks HPLC at 1 8.49and minH NMR, and 8.02 respectively. min with anAccording area of 5% to the and absorbance 95% of the total,at l = 425 for demethoxycurcuminnm, we observed two and peaks curcumin, at 8.49 respectively.min and 8.02 Analysesmin with ofan commercialarea of 5% and curcumin 95% of show the total, peaks for with demethoxycurcumin an area of 5%, 15%, and and curcumin, 80% for bisdemethoxycurcumin,respectively. Analyses of demethoxycurcumin, commercial
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