{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T00:58:29Z","timestamp":1760057909280,"version":"build-2065373602"},"reference-count":53,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2025,3,2]],"date-time":"2025-03-02T00:00:00Z","timestamp":1740873600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>Supported lipid bilayers (SLBs) that model neuronal membranes are needed to explore the role of membrane lipids in the misfolding and aggregation of amyloid proteins associated with neurodegenerative diseases, including Parkinson\u2019s and Alzheimer\u2019s disease. The neuronal membranes include not only phospholipids, but also significant amounts of cholesterol, sphingomyelin, and gangliosides, which are critical to its biological function. In this study, we explored the conditions for the formation of an SLB, for the five-component lipid mixture composed of zwitterionic 1,2-Dioleoyl-sn-glycero-3-phosphocholine (DOPC), anionic 1,2-dioleoyl- sn-glycero-3-phospho-L-serine (DOPS), nonionic cholesterol (Chol), zwitterionic sphingomyelin (SM), and anionic ganglioside (GM), using the quartz crystal microbalance with dissipation monitoring (QCM-D) technique, by varying experimental parameters such as pH, buffer type, temperature, vesicle size, and osmotic stress. SLB formation from this multicomponent lipid system was found challenging because the vesicles adsorbed intact on the quartz crystal and failed to rupture. For most of the variables tested, other than osmotic stress, we found no or only partial vesicle rupture leading to either a supported layer of vesicles or a partial SLB that included unruptured vesicles. When osmotic stress was applied to the vesicles already adsorbed on the surface, by having a different salt concentration in the rinse buffer that follows vesicle flow compared to that of the dilution buffer during vesicle flow and adsorption, vesicle rupture increased, but it remained incomplete. In contrast, when osmotic stress was applied during vesicle flow and adsorption on the surface, by having different salt concentrations in the dilution buffer in which vesicles flowed compared to the hydration buffer in which vesicles were prepared, complete vesicle rupture and successful formation of a rigid SLB was demonstrated. The robustness of this approach to form SLBs by applying osmotic stress during vesicle adsorption was found to be independent of the number of lipid components, as shown by SLB formation from the 1-, 2-, 3-, 4-, and 5-component lipid systems.<\/jats:p>","DOI":"10.3390\/biom15030362","type":"journal-article","created":{"date-parts":[[2025,3,3]],"date-time":"2025-03-03T07:37:17Z","timestamp":1740987437000},"page":"362","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Formation of a Neuronal Membrane Model: A Quartz Crystal Microbalance with Dissipation Monitoring Study"],"prefix":"10.3390","volume":"15","author":[{"given":"Elaheh","family":"Kamaloo","sequence":"first","affiliation":[{"name":"Department of Chemical Engineering, Worcester Polytechnic Institute, Worcester, MA 01609, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Terri A.","family":"Camesano","sequence":"additional","affiliation":[{"name":"Department of Chemical Engineering, Worcester Polytechnic Institute, Worcester, MA 01609, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ramanathan","family":"Nagarajan","sequence":"additional","affiliation":[{"name":"US Army Combat Capabilities Development Command Soldier Center, Natick, MA 01760, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,3,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/S0006-3495(85)83882-0","article-title":"Supported phospholipid bilayers","volume":"47","author":"Tamm","year":"1985","journal-title":"Biophys. J."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3035","DOI":"10.1016\/S0006-3495(03)74722-5","article-title":"Pathways of lipid vesicle deposition on solid surfaces: A combined QCM-D and AFM study","volume":"85","author":"Richter","year":"2003","journal-title":"Biophys. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3422","DOI":"10.1529\/biophysj.104.053728","article-title":"Following the formation of supported lipid bilayers on mica: A study combining AFM, QCM-D, and Ellipsometry","volume":"88","author":"Richter","year":"2005","journal-title":"Biophys. J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"3497","DOI":"10.1021\/la052687c","article-title":"Formation of solid-supported lipid bilayers: An integrated view","volume":"22","author":"Richter","year":"2006","journal-title":"Langmuir"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.ymeth.2014.02.005","article-title":"Fluorescence correlation and lifetime correlation spectroscopy applied to the study of supported lipid bilayer models of the cell membrane","volume":"68","author":"Basit","year":"2014","journal-title":"Methods"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Lind, T.K., and C\u00e1rdenas, M. (2016). Understanding the formation of supported lipid bilayers via vesicle fusion\u2014A case that exemplifies the need for the complementary method approach. Biointerphases, 11.","DOI":"10.1116\/1.4944830"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"10598","DOI":"10.1021\/acs.langmuir.7b02459","article-title":"Time-resolved neutron reflectivity during supported membrane formation by vesicle fusion","volume":"33","author":"Koutsioubas","year":"2017","journal-title":"Langmuir"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"102118","DOI":"10.1016\/j.cis.2020.102118","article-title":"Design and use of model membranes to study biomolecular interactions using complementary surface-sensitive techniques","volume":"27","author":"Clifton","year":"2020","journal-title":"Adv. Colloid Interface Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1016\/j.cocis.2013.06.004","article-title":"Model cell membranes: Techniques to form complex biomimetic supported lipid bilayers via vesicle fusion","volume":"18","author":"Hardy","year":"2013","journal-title":"Curr. Opin. Colloid Interface Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1016\/S0006-3495(98)74057-3","article-title":"Surface specific kinetics of lipid vesicle adsorption measured with a quartz crystal microbalance","volume":"75","author":"Keller","year":"1998","journal-title":"Biophys. J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"5443","DOI":"10.1103\/PhysRevLett.84.5443","article-title":"Formation of supported membranes from vesicles","volume":"84","author":"Keller","year":"2000","journal-title":"Phys. Rev. Lett."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1038\/nprot.2010.65","article-title":"Quartz crystal microbalance with dissipation monitoring of supported lipid bilayers on various substrates","volume":"5","author":"Cho","year":"2010","journal-title":"Nat. Protoc."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"21755","DOI":"10.1021\/jp053482f","article-title":"Dissipation-enhanced quartz crystal microbalance studies on the experimental parameters controlling the formation of supported lipid bilayers","volume":"109","author":"Seantier","year":"2005","journal-title":"J. Phys. Chem. B"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"7564","DOI":"10.1073\/pnas.81.23.7564","article-title":"Antigen presentation by supported planar membranes containing affinity-purified I-Ad","volume":"81","author":"Watts","year":"1984","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/0304-4157(86)90016-X","article-title":"Supported planar membranes in studies of cell-cell recognition in the immune system","volume":"864","author":"McConnell","year":"1986","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1006\/jcis.2001.8060","article-title":"Protein adsorption on supported phospholipid bilayers","volume":"246","author":"Larsson","year":"2002","journal-title":"J. Colloid Interface Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1176","DOI":"10.1093\/glycob\/cwp103","article-title":"QCM-D studies of human norovirus VLPs binding to glycosphingolipids in supported lipid bilayers reveal strain-specific characteristics","volume":"19","author":"Rydell","year":"2009","journal-title":"Glycobiology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4648","DOI":"10.1039\/c3sm50628b","article-title":"Electrostatically driven interaction of silica-supported lipid bilayer nanoplatforms and a nerve growth factor-mimicking peptide","volume":"9","author":"Travaglia","year":"2013","journal-title":"Soft Matter"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1016\/j.bbalip.2013.12.012","article-title":"Validity and applicability of membrane model systems for studying interactions of peripheral membrane proteins with lipids","volume":"1841","author":"Czogalla","year":"2014","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Feng, Y., Zhang, Y., Liu, G., Liu, X., and Gao, S. (2021). Interaction of graphene oxide with artificial cell membranes: Role of anionic phospholipid and cholesterol in nanoparticle attachment and membrane disruption. Colloids Surf. B Biointerfaces, 202.","DOI":"10.1016\/j.colsurfb.2021.111685"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"15228","DOI":"10.1021\/jp209658y","article-title":"Characterization of supported lipid bilayer disruption by chrysophsin-3 using QCM-D","volume":"115","author":"Wang","year":"2011","journal-title":"J. Phys. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.colsurfb.2014.01.036","article-title":"Antimicrobial peptide alamethicin insertion into lipid bilayer: A QCM-D exploration","volume":"116","author":"Wang","year":"2014","journal-title":"Colloids Surf. B Biointerfaces"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.bpc.2014.09.003","article-title":"Differentiating antimicrobial peptides interacting with lipid bilayer: Molecular signatures derived from quartz crystal microbalance with dissipation monitoring","volume":"196","author":"Wang","year":"2015","journal-title":"Biophys. Chem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.bpc.2015.05.006","article-title":"Size dependence of gold nanoparticle interactions with a supported lipid bilayer: A QCM-D study","volume":"203\u2013204","author":"Bailey","year":"2015","journal-title":"Biophys. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1242\/jcs.071233","article-title":"Lipid map of the mammalian cell","volume":"124","year":"2011","journal-title":"J. Cell Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1016\/j.bpj.2017.10.017","article-title":"Computational lipidomics of the neuronal plasma membrane","volume":"113","author":"Carpenter","year":"2017","journal-title":"Biophys. J."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1038\/nrm.2017.138","article-title":"Understanding the diversity of membrane lipid composition","volume":"19","author":"Harayama","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4455","DOI":"10.1038\/s41467-024-48734-y","article-title":"Lipidome atlas of the adult human brain","volume":"15","author":"Osetrova","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1021\/jz4024354","article-title":"Amyloid aggregation: Role of biological membranes and the aggregate\u2212membrane system","volume":"5","author":"Bucciantini","year":"2014","journal-title":"J. Phys. Chem. Lett."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1039\/B912598A","article-title":"Influence of phase separating lipids on supported lipid bilayer formation at SiO2 surfaces","volume":"12","author":"Sundh","year":"2010","journal-title":"Phys. Chem. Chem. Phys."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1039\/C5EN00098J","article-title":"Formation of supported lipid bilayers containing phase-segregated domains and their interaction with gold nanoparticles","volume":"3","author":"Melby","year":"2016","journal-title":"Environ. Sci. Nano"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"8929","DOI":"10.1039\/c3cp44517h","article-title":"Effects of membrane interaction and aggregation of amyloid \u03b2-peptide on lipid mobility and membrane domain structure","volume":"15","author":"Sasahara","year":"2013","journal-title":"Phys. Chem. Chem. Phys."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1111\/febs.12807","article-title":"Amyloid aggregation and deposition of human islet amyloid polypeptide at membrane interfaces","volume":"281","author":"Sasahara","year":"2014","journal-title":"FEBS J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"8420","DOI":"10.1039\/c3sm50443c","article-title":"Simulation of edge facilitated adsorption and critical concentration induced rupture of vesicles at a surface","volume":"9","author":"Plunkett","year":"2013","journal-title":"Soft Matter"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"6997","DOI":"10.1021\/la900181c","article-title":"Formation of supported bilayers on silica substrates","volume":"25","author":"Anderson","year":"2009","journal-title":"Langmuir"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1016\/j.colsurfb.2010.09.023","article-title":"Simulations of lipid vesicle rupture induced by an adjacent supported lipid bilayer patch","volume":"82","author":"Allerbo","year":"2011","journal-title":"Colloids Surf. B Biointerfaces"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2131","DOI":"10.1039\/C6CP07930J","article-title":"Investigating how vesicle size influences vesicle adsorption on titanium oxide: A competition between steric packing and shape deformation","volume":"19","author":"Ferhan","year":"2017","journal-title":"Phys. Chem. Chem. Phys."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Swana, K.W., Camesano, T.A., and Nagarajan, R. (2022). Formation of a fully anionic supported lipid bilayer to model bacterial inner membrane for QCM-D studies. Membranes, 12.","DOI":"10.3390\/membranes12060558"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1238\/Physica.Regular.059a00391","article-title":"Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: Continuum mechanics approach","volume":"59","author":"Voinova","year":"1999","journal-title":"Phys. Scr."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1016\/S0956-5663(02)00050-7","article-title":"\u2018Missing mass\u2019 effect in biosensor\u2019s QCM applications","volume":"17","author":"Voinova","year":"2002","journal-title":"Biosens. Bioelectron."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.cplett.2015.10.053","article-title":"Mechanism of rupture of single adsorbed vesicles","volume":"641","author":"Zhdanov","year":"2015","journal-title":"Chem. Phys. Lett."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1080\/00268949108035656","article-title":"Adhesion of vesicles and membranes","volume":"202","author":"Lipowsky","year":"1991","journal-title":"Mol. Cryst. Liq. Cryst."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"084702","DOI":"10.1063\/1.3687351","article-title":"Adsorbed liposome deformation studied with quartz crystal microbalance","volume":"136","author":"Reviakine","year":"2012","journal-title":"J. Chem. Phys."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2200625","DOI":"10.1002\/pssa.202200625","article-title":"QCM-D study of the formation of solid-supported artificial lipid membranes: State-of-the-art, recent advances, and perspectives","volume":"220","author":"Bar","year":"2023","journal-title":"Phys. Status Solidi A"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"11677","DOI":"10.1021\/la7020963","article-title":"Comparison of liposomes formed by sonication and extrusion: Rotational and translational diffusion of an embedded chromophore","volume":"23","author":"Lapinski","year":"2007","journal-title":"Langmuir"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2806","DOI":"10.1021\/bi00631a035","article-title":"A simple method for the preparation of homogeneous phospholipid vesicles","volume":"16","author":"Barenholz","year":"1977","journal-title":"Biochemistry"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2554","DOI":"10.1021\/jp983996x","article-title":"Formation and spreading of lipid bilayers on planar glass supports","volume":"103","author":"Cremer","year":"1999","journal-title":"J. Phys. Chem. B"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3907","DOI":"10.1529\/biophysj.107.116525","article-title":"Specific and selective peptide-membrane interactions revealed using quartz crystal microbalance","volume":"93","author":"Mechler","year":"2007","journal-title":"Biophys. J."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1021\/la0263920","article-title":"Intact vesicle adsorption and supported biomembrane formation from vesicles in solution: Influence of surface chemistry, vesicle size, temperature, and osmotic pressure","volume":"19","author":"Reimhult","year":"2003","journal-title":"Langmuir"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1039\/C3SM50947H","article-title":"Formation of supported lipid bilayers on silica: Relation to lipid phase transition temperature and liposome size","volume":"10","author":"Jing","year":"2014","journal-title":"Soft Matter"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"4598","DOI":"10.1021\/la100275v","article-title":"Quantification of the layer of hydration of a supported lipid bilayer","volume":"26","author":"Zwang","year":"2010","journal-title":"Langmuir"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"11986","DOI":"10.1021\/acs.langmuir.7b02764","article-title":"Effects of flow and bulk vesicle concentration on supported lipid bilayer formation","volume":"33","author":"Bailey","year":"2017","journal-title":"Langmuir"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1016\/j.bpj.2010.04.072","article-title":"Material properties of lipid microdomains: Force-volume imaging study of the effect of cholesterol on lipid microdomain rigidity","volume":"99","author":"An","year":"2010","journal-title":"Biophys. J."}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/15\/3\/362\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:45:45Z","timestamp":1760028345000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/15\/3\/362"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,2]]},"references-count":53,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,3]]}},"alternative-id":["biom15030362"],"URL":"https:\/\/doi.org\/10.3390\/biom15030362","relation":{},"ISSN":["2218-273X"],"issn-type":[{"type":"electronic","value":"2218-273X"}],"subject":[],"published":{"date-parts":[[2025,3,2]]}}}