DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution

Journal Article · · Environmental Science: Nano
DOI: https://doi.org/10.1039/C9EN00996E · OSTI ID:1597658

The initial interactions of engineered nanoparticles (NPs) with living cells are governed by physicochemical properties of the NP and the molecular composition and structure of the cell membrane. Eukaryotic cell membranes contain lipid rafts – liquid-ordered nanodomains involved in membrane trafficking and molecular signaling. However, the impact of these membrane structures on cellular interactions of NPs remains unclear. Here we investigate the role of membrane domains in the interactions of primary amine-terminated quantum dots (Qdots) with liquid-ordered domains or lipid rafts in model membranes and intact cells, respectively. Using correlative atomic force and fluorescence microscopy, we found that the Qdots preferentially localized to boundaries between liquid-ordered and liquid-disordered phases in supported bilayers. The Qdots also induced holes at these phase boundaries. Using super resolution fluorescence microscopy (STORM), we found that the Qdots preferentially co-localized with lipid rafts in the membrane of intact trout gill epithelial cells – a model cell type for environmental exposures. Our observations uncovered preferential interactions of amine-terminated Qdots with liquid-ordered domains and their boundaries, possibly due to membrane curvature at phase boundaries creating energetically favorable sites for NP interactions. The preferential interaction of the Qdots with lipid rafts supports their potential internalization via lipid raft-mediated endocytosis and interactions with raft-resident signaling molecules.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1597658
Report Number(s):
PNNL-SA--146870
Journal Information:
Environmental Science: Nano, Journal Name: Environmental Science: Nano Journal Issue: 1 Vol. 7; ISSN 2051-8153; ISSN ESNNA4
Publisher:
Royal Society of ChemistryCopyright Statement
Country of Publication:
United States
Language:
English

References (60)

Nanoscale Heterogeneities Drive Enhanced Binding and Anomalous Diffusion of Nanoparticles in Model Biomembranes journal January 2018
Crystalline Hydration Structure at the Membrane–Fluid Interface of Model Lipid Rafts Indicates a Highly Reactive Boundary Region journal November 2011
HIV gp41–mediated membrane fusion occurs at edges of cholesterol-rich lipid domains journal April 2015
Continuous Flow Atomic Force Microscopy Imaging Reveals Fluidity and Time-Dependent Interactions of Antimicrobial Dendrimer with Model Lipid Membranes journal December 2013
Boundary region between coexisting lipid phases as initial binding sites for Escherichia coli alpha-hemolysin: A real-time study journal July 2014
Three-dimensional total-internal reflection fluorescence nanoscopy with nanometric axial resolution by photometric localization of single molecules journal January 2021
High-Resolution Correlative Microscopy: Bridging the Gap between Single Molecule Localization Microscopy and Atomic Force Microscopy journal July 2015
Cellular uptake and intracellular localization of poly (acrylic acid) nanoparticles in a rainbow trout (Oncorhynchus mykiss) gill epithelial cell line, RTgill-W1 journal November 2017
Partitioning of nanoscale particles on a heterogeneous multicomponent lipid bilayer journal January 2018
Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion journal April 2016
Progress in the Correlative Atomic Force Microscopy and Optical Microscopy journal April 2017
Domain Structure in Model Membrane Bilayers Investigated by Simultaneous Atomic Force Microscopy and Fluorescence Imaging journal September 2003
Tracking microdomain dynamics in cell membranes journal January 2009
Mechanisms of Quantum Dot Nanoparticle Cellular Uptake journal May 2009
Physicochemical Properties Determine Nanomaterial Cellular Uptake, Transport, and Fate journal July 2012
Nanoparticle Adhesion to the Cell Membrane and Its Effect on Nanoparticle Uptake Efficiency journal January 2013
Interactions of Poly(amidoamine) Dendrimers with Survanta Lung Surfactant: The Importance of Lipid Domains journal October 2008
Special issue on ultrafine particles: where are they from and how do they affect us? journal March 2020
The Intrinsic Resolution Limit in the Atomic Force Microscope: Implications for Heights of Nano-Scale Features journal August 2011
Physical Principles of Nanoparticle Cellular Endocytosis journal August 2015
Gill cell culture systems as models for aquatic environmental monitoring journal February 2014
Synthetic and Natural Polycationic Polymer Nanoparticles Interact Selectively with Fluid-Phase Domains of DMPC Lipid Bilayers journal September 2005
Phospholipid Composition Modulates Carbon Nanodiamond-Induced Alterations in Phospholipid Domain Formation journal April 2015
Correlated Fluorescence-Atomic Force Microscopy of Membrane Domains: Structure of Fluorescence Probes Determines Lipid Localization journal March 2006
A Toxicologic Review of Quantum Dots: Toxicity Depends on Physicochemical and Environmental Factors journal February 2006
Cellular uptake of nanoparticles: journey inside the cell journal January 2017
Aggregation of nanoparticles on one and two-component bilayer membranes journal November 2014
Expression of GM1, a marker of lipid rafts, defines two subsets of human monocytes with differential endocytic capacity and lipopolysaccharide responsiveness journal April 2007
Modulating interactions between ligand-coated nanoparticles and phase-separated lipid bilayers by varying the ligand density and the surface charge journal January 2018
Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes journal August 2015
Cell Membranes Open “Doors” for Cationic Nanoparticles/Biomolecules: Insights into Uptake Kinetics journal November 2013
Effects of Ceramide on Liquid-Ordered Domains Investigated by Simultaneous AFM and FCS journal June 2006
Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging journal November 2011
Impact of lithiated cobalt oxide and phosphate nanoparticles on rainbow trout gill epithelial cells text January 2019
Curvature-driven adsorption of cationic nanoparticles to phase boundaries in multicomponent lipid bilayers journal January 2019
Lipid phase influences the binding of Bacillus thuringiensis Cyt2Aa2 toxin on model lipid membranes journal April 2019
Dynamic atomic force microscopy methods journal September 2002
Real-Time Analysis of the Effects of Cholesterol on Lipid Raft Behavior Using Atomic Force Microscopy journal March 2003
Cholesterol-Dependent Nanomechanical Stability of Phase-Segregated Multicomponent Lipid Bilayers journal July 2010
Poly-L-Lysine-Induced Morphology Changes in Mixed Anionic/Zwitterionic and Neat Zwitterionic-Supported Phospholipid Bilayers journal October 2006
The multi-tasked life of GM1 ganglioside, a true factotum of nature journal July 2015
Impact of lithiated cobalt oxide and phosphate nanoparticles on rainbow trout gill epithelial cells journal November 2018
Peripheral Membrane Proteins Facilitate Nanoparticle Binding at Lipid Bilayer Interfaces journal August 2018
Quaternary Amine-Terminated Quantum Dots Induce Structural Changes to Supported Lipid Bilayers journal September 2018
The mystery of membrane organization: composition, regulation and roles of lipid rafts journal March 2017
Nanoparticles Meet Cell Membranes: Probing Nonspecific Interactions using Model Membranes journal December 2013
Nanomaterials and Global Sustainability journal March 2017
Wide Varieties of Cationic Nanoparticles Induce Defects in Supported Lipid Bilayers journal January 2008
Quantum dots: from fluorescence to chemiluminescence, bioluminescence, electrochemiluminescence, and electrochemistry journal January 2017
Passive Transport of C 60 Fullerenes through a Lipid Membrane:  A Molecular Dynamics Simulation Study journal February 2008
The interaction of lipid-liganded gold clusters (Aurora ™) with lipid bilayers journal January 2019
Biological Responses to Engineered Nanomaterials: Needs for the Next Decade journal June 2015
Functional rafts in cell membranes journal June 1997
Clathrin to Lipid Raft-Endocytosis via Controlled Surface Chemistry and Efficient Perinuclear Targeting of Nanoparticle journal August 2015
Correlative atomic force microscopy quantitative imaging-laser scanning confocal microscopy quantifies the impact of stressors on live cells in real-time journal May 2018
ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging journal May 2014
Fiji: an open-source platform for biological-image analysis journal June 2012
DNA Nanostructure-Programmed Like-Charge Attraction at the Cell-Membrane Interface journal September 2018
Toxic Potential of Materials at the Nanolevel journal February 2006
Preparation of DOPC and DPPC Supported Planar Lipid Bilayers for Atomic Force Microscopy and Atomic Force Spectroscopy journal February 2013