Lipid Corona Formation from Nanoparticle Interactions with Bilayers

Laura L. Olenick, Julianne M. Troiano, Ariane Vartanian, Eric S. Melby, Arielle C. Mensch, Leili Zhang, Jiewei Hong, Oluwaseun Mesele, Tian Qiu, Jared Bozich, Samuel Lohse, Xi Zhang, Thomas R. Kuech, Augusto Millevolte, Ian Gunsolus, Alicia C. McGeachy, Merve Doğangün, Tianzhe Li, Dehong Hu, Stephanie R. WalterAurash Mohaimani, Angela Schmoldt, Marco D. Torelli, Katherine R. Hurley, Joe Dalluge, Gene Chong, Z. Vivian Feng, Christy L. Haynes, Robert J. Hamers, Joel A. Pedersen, Qiang Cui, Rigoberto Hernandez, Rebecca Klaper, Galya Orr, Catherine J. Murphy, Franz M. Geiger

Research output: Contribution to journalArticlepeer-review

17 Scopus citations

Abstract

Although mixing nanoparticles with certain biological molecules can result in coronas that afford some control over how engineered nanomaterials interact with living systems, corona formation mechanisms remain enigmatic. Here, we report results from experiments and computer simulations that provide concrete lines of evidence for spontaneous lipid corona formation without active mixing upon attachment to stationary and suspended lipid bilayer membranes. Experiments show that polycation-wrapped particles disrupt the tails of zwitterionic lipids, increase bilayer fluidity, and leave the membrane with reduced ζ potentials. Computer simulations suggest that the contact ion pairing between the lipid head groups and the polycations' ammonium groups leads to the formation of stable, albeit fragmented, lipid bilayer coronas. The mechanistic insight regarding lipid corona formation can be used to improve control over nano-bio interactions and to help understand why some nanomaterial-ligand combinations are detrimental to organisms but others are not. Engineered nanoparticles hold not only promise for technological innovation but also possible unforeseen risks for organisms upon inadvertent release into the environment. Here, mechanistic insight is provided regarding spontaneous lipid corona formation from nanomaterial-membrane interactions that can be used to improve control over nano-bio interactions and to help understand why some nanomaterial-ligand combinations are detrimental to organisms but others are not. We identify ion pairing between the lipid head groups and certain ligands coating nanoparticles having diameters below 10 nm as a necessary condition for the formation of fragmented lipid coronas that engender new properties (ζ potential, stickiness, and composition) departing from the original particle formulation. These insights help predict the impact that the increasingly widespread use of engineered nanomaterials has on their fate once they enter the food chain, which many of them may eventually do. Mechanisms of corona formation around nanomaterials remain enigmatic. Here, we provide evidence for spontaneous lipid corona formation that engenders new particle properties without the need for active mixing upon attachment to stationary and suspended lipid bilayer membranes. The mechanism of lipid corona formation can be used to improve control over nano-bio interactions and to help understand why some nanomaterial-ligand combinations are detrimental to organisms but others are not.

Original languageEnglish (US)
Pages (from-to)2709-2723
Number of pages15
JournalChem
Volume4
Issue number11
DOIs
StatePublished - Nov 8 2018

Bibliographical note

Funding Information:
This work was supported by the National Science Foundation Center for Chemical Innovation Program through the Center for Sustainable Nanotechnology under grant no. CHE-1503408 . J.M.T. and A.C.M. gratefully acknowledge support through a National Science Foundation Graduate Research Fellowship. S.R.W. was supported by an Arnold O. Beckman Scholarship of the Chicago chapter of the Achievement Rewards for College Scientists foundation. F.M.G. gratefully acknowledges support from a Friedrich Wilhelm Bessel Prize from the Alexander von Humboldt Foundation . Part of this research was performed in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the Department of Energy's Office of Biological and Environmental Research and located at the Pacific Northwest National Laboratory. R.J.H. acknowledges the National Science Foundation through XSEDE resources provided by Stampede under grant number CTS090079 . Additional computing resources were provided by the Maryland Advanced Research Computing Center.

Keywords

  • SDG3: Good health and well-being
  • mechanisms of nanoparticle-specific toxicology
  • nano-bio interface
  • sustainability

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