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 journalArticle

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

Fingerprint

Nanostructures
Nanoparticles
Lipids
corona
Nanostructured materials
lipid
Lipid bilayers
Lipid Bilayers
Ligands
Membranes
ligand
Membrane Lipids
Computer Simulation
membrane
Inventions
Ions
computer simulation
Membrane Fluidity
Food Chain
nanoparticle

Keywords

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

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry
  • Environmental Chemistry
  • Chemical Engineering(all)
  • Biochemistry, medical
  • Materials Chemistry

Cite this

Olenick, L. L., Troiano, J. M., Vartanian, A., Melby, E. S., Mensch, A. C., Zhang, L., ... Geiger, F. M. (2018). Lipid Corona Formation from Nanoparticle Interactions with Bilayers. Chem, 4(11), 2709-2723. https://doi.org/10.1016/j.chempr.2018.09.018

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

In: Chem, Vol. 4, No. 11, 08.11.2018, p. 2709-2723.

Research output: Contribution to journalArticle

Olenick, LL, Troiano, JM, Vartanian, A, Melby, ES, Mensch, AC, Zhang, L, Hong, J, Mesele, O, Qiu, T, Bozich, J, Lohse, S, Zhang, X, Kuech, TR, Millevolte, A, Gunsolus, I, McGeachy, AC, Doğangün, M, Li, T, Hu, D, Walter, SR, Mohaimani, A, Schmoldt, A, Torelli, MD, Hurley, KR, Dalluge, J, Chong, G, Feng, ZV, Haynes, CL, Hamers, RJ, Pedersen, JA, Cui, Q, Hernandez, R, Klaper, R, Orr, G, Murphy, CJ & Geiger, FM 2018, 'Lipid Corona Formation from Nanoparticle Interactions with Bilayers', Chem, vol. 4, no. 11, pp. 2709-2723. https://doi.org/10.1016/j.chempr.2018.09.018
Olenick LL, Troiano JM, Vartanian A, Melby ES, Mensch AC, Zhang L et al. Lipid Corona Formation from Nanoparticle Interactions with Bilayers. Chem. 2018 Nov 8;4(11):2709-2723. https://doi.org/10.1016/j.chempr.2018.09.018
Olenick, Laura L. ; Troiano, Julianne M. ; Vartanian, Ariane ; Melby, Eric S. ; Mensch, Arielle C. ; Zhang, Leili ; Hong, Jiewei ; Mesele, Oluwaseun ; Qiu, Tian ; Bozich, Jared ; Lohse, Samuel ; Zhang, Xi ; Kuech, Thomas R. ; Millevolte, Augusto ; Gunsolus, Ian ; McGeachy, Alicia C. ; Doğangün, Merve ; Li, Tianzhe ; Hu, Dehong ; Walter, Stephanie R. ; Mohaimani, Aurash ; Schmoldt, Angela ; Torelli, Marco D. ; Hurley, Katherine R. ; Dalluge, Joe ; Chong, Gene ; Feng, Z. Vivian ; Haynes, Christy L. ; Hamers, Robert J. ; Pedersen, Joel A. ; Cui, Qiang ; Hernandez, Rigoberto ; Klaper, Rebecca ; Orr, Galya ; Murphy, Catherine J. ; Geiger, Franz M. / Lipid Corona Formation from Nanoparticle Interactions with Bilayers. In: Chem. 2018 ; Vol. 4, No. 11. pp. 2709-2723.
@article{464733cf404046789ad89c2f7f7b89d3,
title = "Lipid Corona Formation from Nanoparticle Interactions with Bilayers",
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.",
keywords = "SDG3: Good health and well-being, mechanisms of nanoparticle-specific toxicology, nano-bio interface, sustainability",
author = "Olenick, {Laura L.} and Troiano, {Julianne M.} and Ariane Vartanian and Melby, {Eric S.} and Mensch, {Arielle C.} and Leili Zhang and Jiewei Hong and Oluwaseun Mesele and Tian Qiu and Jared Bozich and Samuel Lohse and Xi Zhang and Kuech, {Thomas R.} and Augusto Millevolte and Ian Gunsolus and McGeachy, {Alicia C.} and Merve Doğang{\"u}n and Tianzhe Li and Dehong Hu and Walter, {Stephanie R.} and Aurash Mohaimani and Angela Schmoldt and Torelli, {Marco D.} and Hurley, {Katherine R.} and Joe Dalluge and Gene Chong and Feng, {Z. Vivian} and Haynes, {Christy L.} and Hamers, {Robert J.} and Pedersen, {Joel A.} and Qiang Cui and Rigoberto Hernandez and Rebecca Klaper and Galya Orr and Murphy, {Catherine J.} and Geiger, {Franz M.}",
year = "2018",
month = "11",
day = "8",
doi = "10.1016/j.chempr.2018.09.018",
language = "English (US)",
volume = "4",
pages = "2709--2723",
journal = "Chem",
issn = "2451-9294",
publisher = "Elsevier Inc.",
number = "11",

}

TY - JOUR

T1 - Lipid Corona Formation from Nanoparticle Interactions with Bilayers

AU - Olenick, Laura L.

AU - Troiano, Julianne M.

AU - Vartanian, Ariane

AU - Melby, Eric S.

AU - Mensch, Arielle C.

AU - Zhang, Leili

AU - Hong, Jiewei

AU - Mesele, Oluwaseun

AU - Qiu, Tian

AU - Bozich, Jared

AU - Lohse, Samuel

AU - Zhang, Xi

AU - Kuech, Thomas R.

AU - Millevolte, Augusto

AU - Gunsolus, Ian

AU - McGeachy, Alicia C.

AU - Doğangün, Merve

AU - Li, Tianzhe

AU - Hu, Dehong

AU - Walter, Stephanie R.

AU - Mohaimani, Aurash

AU - Schmoldt, Angela

AU - Torelli, Marco D.

AU - Hurley, Katherine R.

AU - Dalluge, Joe

AU - Chong, Gene

AU - Feng, Z. Vivian

AU - Haynes, Christy L.

AU - Hamers, Robert J.

AU - Pedersen, Joel A.

AU - Cui, Qiang

AU - Hernandez, Rigoberto

AU - Klaper, Rebecca

AU - Orr, Galya

AU - Murphy, Catherine J.

AU - Geiger, Franz M.

PY - 2018/11/8

Y1 - 2018/11/8

N2 - 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.

AB - 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.

KW - SDG3: Good health and well-being

KW - mechanisms of nanoparticle-specific toxicology

KW - nano-bio interface

KW - sustainability

UR - http://www.scopus.com/inward/record.url?scp=85057201369&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85057201369&partnerID=8YFLogxK

U2 - 10.1016/j.chempr.2018.09.018

DO - 10.1016/j.chempr.2018.09.018

M3 - Article

AN - SCOPUS:85057201369

VL - 4

SP - 2709

EP - 2723

JO - Chem

JF - Chem

SN - 2451-9294

IS - 11

ER -