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Cu Nanoparticle-Loaded Nanovesicles with Antibiofilm nanomaterials Article Cu Nanoparticle-Loaded Nanovesicles with Antibiofilm Properties. Part I: Synthesis of New Hybrid Nanostructures Lucia Sarcina 1, Pablo García-Manrique 2,3,4 , Gemma Gutiérrez 3,4, Nicoletta Ditaranto 1 , Nicola Cioffi 1 , Maria Matos 3,4,* and Maria del Carmen Blanco-López 2,4,* 1 Department of Chemistry, Università degli Studi di Bari Aldo Moro, via Orabona 4, 70125 Bari, Italy; [email protected] (L.S.); [email protected] (N.D.); nicola.cioffi@uniba.it (N.C.) 2 Department of Physical and Analytical Chemistry, University of Oviedo, Julián Clavería 8, 33006 Oviedo, Spain; [email protected] (P.G.-M.); [email protected] (G.G.) 3 Department of Chemical and Environmental Engineering, University of Oviedo, Julián Clavería 8, 33006 Oviedo, Spain 4 Instituto Universitario de Biotecnología de Asturias, University of Oviedo, 33006 Oviedo, Spain * Correspondence: [email protected] (M.M.); [email protected] (M.d.C.B.-L.) Received: 2 July 2020; Accepted: 4 August 2020; Published: 6 August 2020 Abstract: Copper nanoparticles (CuNPs) stabilized by quaternary ammonium salts are well known as antimicrobial agents. The aim of this work was to study the feasibility of the inclusion of CuNPs in nanovesicular systems. Liposomes are nanovesicles (NVs) made with phospholipids and are traditionally used as delivery vehicles because phospholipids favor cellular uptake. Their capacity for hydrophilic/hydrophobic balance and carrier capacity could be advantageous to prepare novel hybrid nanostructures based on metal NPs (Me-NPs). In this work, NVs were loaded with CuNPs, which have been reported to have a biofilm inhibition effect. These hybrid materials could improve the effect of conventional antibacterial agents. CuNPs were electro-synthesized by the sacrificial anode electrolysis technique in organic media and characterized in terms of morphology through transmission electron microscopy (TEM). The NVs were prepared by the thin film hydration method in aqueous media, using phosphatidylcholine (PC) and cholesterol as a membrane stabilizer. The nanohybrid systems were purified to remove non-encapsulated NPs. The size distribution, morphology and stability of the NV systems were studied. Different quaternary ammonium salts in vesicular systems made of PC were tested as stabilizing surfactants for the synthesis and inclusion of CuNPs. The entrapment of charged metal NPs was demonstrated. NPs attached preferably to the membrane, probably due to the attraction of their hydrophobic shell to the phospholipid bilayers. The high affinity between benzyl-dimethyl-hexadecyl-ammonium chloride (BDHAC) and PC allowed us to obtain stable hybrid NVs c.a. 700 nm in diameter. The stability of liposomes increased with NP loading, suggesting a charge-stabilization effect in a novel antibiofilm nanohybrid material. Keywords: hybrid nanostructures; nanovesicles; nanoparticles; copper; antibiofilm 1. Introduction A biofilm is commonly defined as a complex community of microorganisms adherent on a surface and organized in a polymeric matrix, usually containing exopolysaccharide [1–3]. These structures have a heterogenic network of aqueous compartments interposed between glycocalyx-enclosed microorganism in stalk- or mushroom-like structures [3], holding more than one single microbial species. The biofilm resistance issue could be considered phenotypic. Bacteria in biofilm present a higher antimicrobial resistance (AMR) compared to planktonic forms [3]. Nanomaterials 2020, 10, 1542; doi:10.3390/nano10081542 www.mdpi.com/journal/nanomaterials Nanomaterials 2020, 10, x FOR PEER REVIEW 2 of 14 Nanomaterials 2020, 10, 1542 2 of 14 microbial species. The biofilm resistance issue could be considered phenotypic. Bacteria in biofilm present a higher antimicrobial resistance (AMR) compared to planktonic forms [3]. PreventionPrevention andand destructiondestruction ofof biofilmsbiofilms isis aa challengingchallenging tasktask requiringrequiring knowledgeknowledge fromfrom severalseveral scientificscientific researchresearch branches. Due Due to toAMR AMR mechanis mechanisms,ms, there there is an is urgent an urgent need needto search to search for novel for novelefficient effi cientformulations. formulations. A reported A reported effective effective stra strategytegy to todevelop develop more more efficient efficient materials toto preventprevent/minimize/minimize biofilmbiofilm formationformation isis surfacesurface modificationmodification throughthrough thethe additionaddition ofof metalmetal particlesparticles (Cu,(Cu, Zn,Zn, Ti,Ti, Ag) Ag) to to polymeric polymeric blends blends [ 4[4–8]–8] or or biopolymers biopolymers suchsuch asas starchstarch solutions solutions [ 9[9].]. RecentRecent studiesstudies reportedreported that that carboncarbon/copper/copper nanoparticles nanoparticles (CuNP) (CuNP) hybrids hybrids were were e effectiveffective as as biocides, biocides, with withthe the carboncarbon componentcomponent inin chargecharge ofof capturingcapturing thethe bacteriabacteria andand thethe CuNPsCuNPs responsibleresponsible forfor bacteriabacteria destruction.destruction. Moreover,Moreover, thethe outerouter carboncarbon layerslayers protectedprotected thethe metallicmetallic coppercopper fromfromexternal externaloxidation oxidation [[10].10]. ItIt hashas beenbeen provedproved inin thethe literatureliterature that,that, inin orderorder toto havehave bactericidalbactericidal inhibitoryinhibitory eeffect,ffect, aa surfacesurface shouldshould bebe coveredcovered byby relativelyrelatively hydrophobichydrophobic polymers polymers that that are are positively positively charged charged [ 3[3].]. MetalMetal nanoparticlesnanoparticles (Me-NPs)(Me-NPs) suchsuch asas AuNPs,AuNPs, AgNPsAgNPs oror CuNPsCuNPs displaydisplay uniqueunique propertiesproperties thatthat makemake themthem suitablesuitable atat surfacesurface sciencescience forfor the the development development of of antimicrobial antimicrobial formulations. formulations. PreviousPrevious studiesstudies investigatedinvestigated the the integration integration of of NPs NPs in in biomat biomaterialserials showing showing unique unique recognition, recognition, catalytic, catalytic, and andinhibition inhibition properties properties [6,11–14]. [6,11–14 Especially]. Especially gold gold or orsilver silver NPs NPs are are largely largely used used forfor biomedicalbiomedical applicationapplication since since they they can can be be used used as as biomarkers biomarkers and an drug-deliveryd drug-delivery agents agents with with a bactericidal a bactericidal effect effect [15]. The[15]. antibacterial The antibacterial action action towards towards different different microorganisms microorganisms exerted exerted by polymer by polymer nanocomposites nanocomposites loaded withloaded copper with NPs copper has alreadyNPs has been already proved been [4, 16proved–22],along [4,16–22], with thealong possibility with the to possibility tune the ionic to tune copper the release.ionic copper It is possible release. to It achieve is possible efficient to achieve disinfection efficient by simply disinfection changing by thesimply CuNP changing loading andthe /orCuNP the thicknessloading and/or and formulation the thickness of the and surfactant formulation shell. of Indeed,the surfactant as evident shell. from Indeed, the plots as evident reported from in Figurethe plots1, whenreported a stabilizer in Figure with 1, when four butyl a stabilizer alkyl chains with isfour used butyl to prepare alkyl chains CuNPs, is used the released to prepare plateau CuNPs, copper the amountreleased is plateau around copper 1ppm. amount This value is around decreases 1ppm. as the This length value of decreases the surfactant as the alkyl length chains of the is increased,surfactant alongalkyl withchains the is slowdownincreased, ofalong the kineticswith the andslowdown the kinetic of the constants. kinetics Thisand couldthe kinetic be explained constants. by This the increasecould be in explained the shell thickness,by the increase which in is ablethe shell to modulate thickness, the which copper is ions’ able releaseto modulate from the the surface copper of ions’ the NPrelease core from [21,23 the–25 surface]. Moreover, of the in NP quaternary core [21,23– ammonium25]. Moreover, compounds in quaternary (QAC), bothammonium the fatty-acyl compounds chain length(QAC), distributions both the fatty-acyl and the degreechain oflength C–C saturationdistributions will and significantly the degree affect of antimicrobialC–C saturation activity, will withsignificantly a maximized affect action antimicrobial againstGram activity, positive with bacteriaa maximized when action chain lengthagainst is Gram n = 12–14 positive and bacteria against Gramwhen negativechain length bacteria is n = when 12–14 n and= 14–16 against [26]. Gram negative bacteria when n = 14–16 [26]. FigureFigure 1.1.E Effectffect of of the the alkyl alkyl chain chain length length of of the the stabilizer stabiliz oner on the the copper copper release release concentration concentration and and on the on kineticthe kinetic constant constant for copper for copper nanocomposites nanocomposites with the with same the copper same nanoparticlecopper nanoparticle (CuNP) %(CuNP)w/w loading. %w/w Red:loading. tetra Red: butyl tetra ammonium butyl ammonium chloride chloride (C4); green: (C4); tetragreen: octyl tetra ammonium octyl ammonium chloride chloride (C8); blue: (C8); tetrablue: dodecyltetra dodecyl ammonium ammonium chloride chloride (C12). (C12). SomeSome ofof thethe reportedreported
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