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Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution
Abstract
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, we found that the Qdots preferentially co-localized with lipid rafts in the membrane of intact trout gill epithelial cells – a model 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 withmore »
- Authors:
-
[1];
[1]
- BATTELLE (PACIFIC NW LAB)
- COLUMBIA BASIN COLLEGE
- University of Wisconsin-Madison
- UNIVERSITY OF WISCONSIN
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1597658
- Report Number(s):
- PNNL-SA-146870
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Science Nano
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 1
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Mensch, Arielle C., Melby, Eric S., Laudadio, Elizabeth, Foreman-Ortiz, Isabel U., Zhang, Yongqian, Dohnalkova, Alice, Hu, Dehong, Pedersen, Joel A., Hamers, Robert J., and Orr, Galya. Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution. United States: N. p., 2020.
Web. doi:10.1039/C9EN00996E.
Mensch, Arielle C., Melby, Eric S., Laudadio, Elizabeth, Foreman-Ortiz, Isabel U., Zhang, Yongqian, Dohnalkova, Alice, Hu, Dehong, Pedersen, Joel A., Hamers, Robert J., & Orr, Galya. Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution. United States. doi:10.1039/C9EN00996E.
Mensch, Arielle C., Melby, Eric S., Laudadio, Elizabeth, Foreman-Ortiz, Isabel U., Zhang, Yongqian, Dohnalkova, Alice, Hu, Dehong, Pedersen, Joel A., Hamers, Robert J., and Orr, Galya. Wed .
"Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution". United States. doi:10.1039/C9EN00996E.
@article{osti_1597658,
title = {Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution},
author = {Mensch, Arielle C. and Melby, Eric S. and Laudadio, Elizabeth and Foreman-Ortiz, Isabel U. and Zhang, Yongqian and Dohnalkova, Alice and Hu, Dehong and Pedersen, Joel A. and Hamers, Robert J. and Orr, Galya},
abstractNote = {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, we found that the Qdots preferentially co-localized with lipid rafts in the membrane of intact trout gill epithelial cells – a model 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.},
doi = {10.1039/C9EN00996E},
journal = {Environmental Science Nano},
number = 1,
volume = 7,
place = {United States},
year = {2020},
month = {1}
}
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DOI: 10.1039/C9EN00996E
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Works referenced in this record:
Nanomaterials and Global Sustainability
journal, March 2017
- Hamers, Robert J.
- Accounts of Chemical Research, Vol. 50, Issue 3
Toxic Potential of Materials at the Nanolevel
journal, February 2006
- Nel, A.
- Science, Vol. 311, Issue 5761
Biological Responses to Engineered Nanomaterials: Needs for the Next Decade
journal, June 2015
- Murphy, Catherine J.; Vartanian, Ariane M.; Geiger, Franz M.
- ACS Central Science, Vol. 1, Issue 3
Physicochemical Properties Determine Nanomaterial Cellular Uptake, Transport, and Fate
journal, July 2012
- Zhu, Motao; Nie, Guangjun; Meng, Huan
- Accounts of Chemical Research, Vol. 46, Issue 3
Cellular uptake of nanoparticles: journey inside the cell
journal, January 2017
- Behzadi, Shahed; Serpooshan, Vahid; Tao, Wei
- Chemical Society Reviews, Vol. 46, Issue 14
Nanoparticle Adhesion to the Cell Membrane and Its Effect on Nanoparticle Uptake Efficiency
journal, January 2013
- Lesniak, Anna; Salvati, Anna; Santos-Martinez, Maria J.
- Journal of the American Chemical Society, Vol. 135, Issue 4
Passive Transport of C 60 Fullerenes through a Lipid Membrane: A Molecular Dynamics Simulation Study
journal, February 2008
- Bedrov, Dmitry; Smith, Grant D.; Davande, Hemali
- The Journal of Physical Chemistry B, Vol. 112, Issue 7
Cell Membranes Open “Doors” for Cationic Nanoparticles/Biomolecules: Insights into Uptake Kinetics
journal, November 2013
- Lin, Jiaqi; Alexander-Katz, Alfredo
- ACS Nano, Vol. 7, Issue 12
Physical Principles of Nanoparticle Cellular Endocytosis
journal, August 2015
- Zhang, Sulin; Gao, Huajian; Bao, Gang
- ACS Nano, Vol. 9, Issue 9
Mechanisms of Quantum Dot Nanoparticle Cellular Uptake
journal, May 2009
- Zhang, Leshuai W.; Monteiro-Riviere, Nancy A.
- Toxicological Sciences, Vol. 110, Issue 1
Functional rafts in cell membranes
journal, June 1997
- Simons, Kai; Ikonen, Elina
- Nature, Vol. 387, Issue 6633
The mystery of membrane organization: composition, regulation and roles of lipid rafts
journal, March 2017
- Sezgin, Erdinc; Levental, Ilya; Mayor, Satyajit
- Nature Reviews Molecular Cell Biology, Vol. 18, Issue 6
Nanoparticles Meet Cell Membranes: Probing Nonspecific Interactions using Model Membranes
journal, December 2013
- Chen, Kai Loon; Bothun, Geoffrey D.
- Environmental Science & Technology, Vol. 48, Issue 2
Wide Varieties of Cationic Nanoparticles Induce Defects in Supported Lipid Bilayers
journal, January 2008
- Leroueil, Pascale R.; Berry, Stephanie A.; Duthie, Kristen
- Nano Letters, Vol. 8, Issue 2
Peripheral Membrane Proteins Facilitate Nanoparticle Binding at Lipid Bilayer Interfaces
journal, August 2018
- Melby, Eric S.; Allen, Caley; Foreman-Ortiz, Isabel U.
- Langmuir, Vol. 34, Issue 36
Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes
journal, August 2015
- Jacobson, Kurt H.; Gunsolus, Ian L.; Kuech, Thomas R.
- Environmental Science & Technology, Vol. 49, Issue 17
Phospholipid Composition Modulates Carbon Nanodiamond-Induced Alterations in Phospholipid Domain Formation
journal, April 2015
- Chakraborty, Aishik; Mucci, Nicolas J.; Tan, Ming Li
- Langmuir, Vol. 31, Issue 18
Interactions of Poly(amidoamine) Dendrimers with Survanta Lung Surfactant: The Importance of Lipid Domains
journal, October 2008
- Erickson, Blake; DiMaggio, Stassi C.; Mullen, Douglas G.
- Langmuir, Vol. 24, Issue 19
Synthetic and Natural Polycationic Polymer Nanoparticles Interact Selectively with Fluid-Phase Domains of DMPC Lipid Bilayers
journal, September 2005
- Mecke, Almut; Lee, Dong-Kuk; Ramamoorthy, Ayyalusamy
- Langmuir, Vol. 21, Issue 19
Continuous Flow Atomic Force Microscopy Imaging Reveals Fluidity and Time-Dependent Interactions of Antimicrobial Dendrimer with Model Lipid Membranes
journal, December 2013
- Lind, Tania Kjellerup; Zielińska, Paulina; Wacklin, Hanna Pauliina
- ACS Nano, Vol. 8, Issue 1
Nanoscale Heterogeneities Drive Enhanced Binding and Anomalous Diffusion of Nanoparticles in Model Biomembranes
journal, January 2018
- Chelladurai, Roobala; Debnath, Koushik; Jana, Nikhil R.
- Langmuir, Vol. 34, Issue 4
Quaternary Amine-Terminated Quantum Dots Induce Structural Changes to Supported Lipid Bilayers
journal, September 2018
- Mensch, Arielle C.; Buchman, Joseph T.; Haynes, Christy L.
- Langmuir, Vol. 34, Issue 41
Curvature-driven adsorption of cationic nanoparticles to phase boundaries in multicomponent lipid bilayers
journal, January 2019
- Sheavly, Jonathan K.; Pedersen, Joel A.; Van Lehn, Reid C.
- Nanoscale, Vol. 11, Issue 6
The interaction of lipid-liganded gold clusters (Aurora ™) with lipid bilayers
journal, January 2019
- Sot, Jesús; Mendanha-Neto, Sebastião A.; Busto, Jon V.
- Chemistry and Physics of Lipids, Vol. 218
Progress in the Correlative Atomic Force Microscopy and Optical Microscopy
journal, April 2017
- Zhou, Lulu; Cai, Mingjun; Tong, Ti
- Sensors, Vol. 17, Issue 4
Correlated Fluorescence-Atomic Force Microscopy of Membrane Domains: Structure of Fluorescence Probes Determines Lipid Localization
journal, March 2006
- Shaw, James E.; Epand, Raquel F.; Epand, Richard M.
- Biophysical Journal, Vol. 90, Issue 6
Domain Structure in Model Membrane Bilayers Investigated by Simultaneous Atomic Force Microscopy and Fluorescence Imaging
journal, September 2003
- Burns, A. R.
- Langmuir, Vol. 19, Issue 20
Effects of Ceramide on Liquid-Ordered Domains Investigated by Simultaneous AFM and FCS
journal, June 2006
- Chiantia, Salvatore; Kahya, Nicoletta; Ries, Jonas
- Biophysical Journal, Vol. 90, Issue 12
Correlative atomic force microscopy quantitative imaging-laser scanning confocal microscopy quantifies the impact of stressors on live cells in real-time
journal, May 2018
- Bhat, Supriya V.; Sultana, Taranum; Körnig, André
- Scientific Reports, Vol. 8, Issue 1
High-Resolution Correlative Microscopy: Bridging the Gap between Single Molecule Localization Microscopy and Atomic Force Microscopy
journal, July 2015
- Odermatt, Pascal D.; Shivanandan, Arun; Deschout, Hendrik
- Nano Letters, Vol. 15, Issue 8
Quantum dots: from fluorescence to chemiluminescence, bioluminescence, electrochemiluminescence, and electrochemistry
journal, January 2017
- Yao, Jun; Li, Lin; Li, Pingfan
- Nanoscale, Vol. 9, Issue 36
A Toxicologic Review of Quantum Dots: Toxicity Depends on Physicochemical and Environmental Factors
journal, February 2006
- Hardman, Ron
- Environmental Health Perspectives, Vol. 114, Issue 2
Gill cell culture systems as models for aquatic environmental monitoring
journal, February 2014
- Bury, N. R.; Schnell, S.; Hogstrand, C.
- Journal of Experimental Biology, Vol. 217, Issue 5
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
- Felix, Lindsey C.; Ortega, Van A.; Goss, Greg G.
- Aquatic Toxicology, Vol. 192
Fiji: an open-source platform for biological-image analysis
journal, June 2012
- Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin
- Nature Methods, Vol. 9, Issue 7
ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging
journal, May 2014
- Ovesný, Martin; Křížek, Pavel; Borkovec, Josef
- Bioinformatics, Vol. 30, Issue 16
Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging
journal, November 2011
- Dempsey, Graham T.; Vaughan, Joshua C.; Chen, Kok Hao
- Nature Methods, Vol. 8, Issue 12
Real-Time Analysis of the Effects of Cholesterol on Lipid Raft Behavior Using Atomic Force Microscopy
journal, March 2003
- Lawrence, Jared C.; Saslowsky, David E.; Michael Edwardson, J.
- Biophysical Journal, Vol. 84, Issue 3
The Intrinsic Resolution Limit in the Atomic Force Microscope: Implications for Heights of Nano-Scale Features
journal, August 2011
- Santos, Sergio; Barcons, Victor; Christenson, Hugo K.
- PLoS ONE, Vol. 6, Issue 8
Dynamic atomic force microscopy methods
journal, September 2002
- García, R.
- Surface Science Reports, Vol. 47, Issue 6-8
Preparation of DOPC and DPPC Supported Planar Lipid Bilayers for Atomic Force Microscopy and Atomic Force Spectroscopy
journal, February 2013
- Attwood, Simon; Choi, Youngjik; Leonenko, Zoya
- International Journal of Molecular Sciences, Vol. 14, Issue 2
Crystalline Hydration Structure at the Membrane–Fluid Interface of Model Lipid Rafts Indicates a Highly Reactive Boundary Region
journal, November 2011
- Sheikh, Khizar H.; Jarvis, Suzanne P.
- Journal of the American Chemical Society, Vol. 133, Issue 45
Poly-L-Lysine-Induced Morphology Changes in Mixed Anionic/Zwitterionic and Neat Zwitterionic-Supported Phospholipid Bilayers
journal, October 2006
- Spurlin, Tighe A.; Gewirth, Andrew A.
- Biophysical Journal, Vol. 91, Issue 8
Cholesterol-Dependent Nanomechanical Stability of Phase-Segregated Multicomponent Lipid Bilayers
journal, July 2010
- Sullan, Ruby May A.; Li, James K.; Hao, Changchun
- Biophysical Journal, Vol. 99, Issue 2
Expression of GM1, a marker of lipid rafts, defines two subsets of human monocytes with differential endocytic capacity and lipopolysaccharide responsiveness
journal, April 2007
- Moreno-Altamirano, M. Maximina Bertha; Aguilar-Carmona, Israel; Sánchez-García, F. Javier
- Immunology, Vol. 120, Issue 4
Tracking microdomain dynamics in cell membranes
journal, January 2009
- Day, Charles A.; Kenworthy, Anne K.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1788, Issue 1
The multi-tasked life of GM1 ganglioside, a true factotum of nature
journal, July 2015
- Ledeen, Robert W.; Wu, Gusheng
- Trends in Biochemical Sciences, Vol. 40, Issue 7
Clathrin to Lipid Raft-Endocytosis via Controlled Surface Chemistry and Efficient Perinuclear Targeting of Nanoparticle
journal, August 2015
- Chakraborty, Atanu; Jana, Nikhil R.
- The Journal of Physical Chemistry Letters, Vol. 6, Issue 18
Impact of lithiated cobalt oxide and phosphate nanoparticles on rainbow trout gill epithelial cells
journal, November 2018
- Melby, Eric S.; Cui, Yi; Borgatta, Jaya
- Nanotoxicology, Vol. 12, Issue 10
Modulating interactions between ligand-coated nanoparticles and phase-separated lipid bilayers by varying the ligand density and the surface charge
journal, January 2018
- Chen, Xiaojie; Tieleman, D. Peter; Liang, Qing
- Nanoscale, Vol. 10, Issue 5
Partitioning of nanoscale particles on a heterogeneous multicomponent lipid bilayer
journal, January 2018
- Yang, Kai; Yang, Ran; Tian, Xiaodong
- Physical Chemistry Chemical Physics, Vol. 20, Issue 44
DNA Nanostructure-Programmed Like-Charge Attraction at the Cell-Membrane Interface
journal, September 2018
- Ding, Hongming; Li, Jiang; Chen, Nan
- ACS Central Science, Vol. 4, Issue 10
Aggregation of nanoparticles on one and two-component bilayer membranes
journal, November 2014
- Cheung, David L.
- The Journal of Chemical Physics, Vol. 141, Issue 19
HIV gp41–mediated membrane fusion occurs at edges of cholesterol-rich lipid domains
journal, April 2015
- Yang, Sung-Tae; Kiessling, Volker; Simmons, James A.
- Nature Chemical Biology, Vol. 11, Issue 6
Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion
journal, April 2016
- Yang, Sung-Tae; Kiessling, Volker; Tamm, Lukas K.
- Nature Communications, Vol. 7, Issue 1
Lipid phase influences the binding of Bacillus thuringiensis Cyt2Aa2 toxin on model lipid membranes
journal, April 2019
- Tharad, Sudarat; Promdonkoy, Boonhiang; Toca-Herrera, José L.
- Biochemical and Biophysical Research Communications, Vol. 511, Issue 2
Boundary region between coexisting lipid phases as initial binding sites for Escherichia coli alpha-hemolysin: A real-time study
journal, July 2014
- Maté, Sabina M.; Vázquez, Romina F.; Herlax, Vanesa S.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 7