The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.

The peripheral lungs are a potential entrance portal for nanoparticles into the human body due to their large surface area. The fact that nanoparticles can be deposited in the alveolar region of the lungs is of interest for pulmonary drug delivery strategies and is of equal importance for toxicologi...

Full description

Bibliographic Details
Main Authors: Christian A Ruge, Ulrich F Schaefer, Jennifer Herrmann, Julian Kirch, Olga Cañadas, Mercedes Echaide, Jesús Pérez-Gil, Cristina Casals, Rolf Müller, Claus-Michael Lehr
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3393659?pdf=render
_version_ 1818926504190410752
author Christian A Ruge
Ulrich F Schaefer
Jennifer Herrmann
Julian Kirch
Olga Cañadas
Mercedes Echaide
Jesús Pérez-Gil
Cristina Casals
Rolf Müller
Claus-Michael Lehr
author_facet Christian A Ruge
Ulrich F Schaefer
Jennifer Herrmann
Julian Kirch
Olga Cañadas
Mercedes Echaide
Jesús Pérez-Gil
Cristina Casals
Rolf Müller
Claus-Michael Lehr
author_sort Christian A Ruge
collection DOAJ
description The peripheral lungs are a potential entrance portal for nanoparticles into the human body due to their large surface area. The fact that nanoparticles can be deposited in the alveolar region of the lungs is of interest for pulmonary drug delivery strategies and is of equal importance for toxicological considerations. Therefore, a detailed understanding of nanoparticle interaction with the structures of this largest and most sensitive part of the lungs is important for both nanomedicine and nanotoxicology. Astonishingly, there is still little known about the bio-nano interactions that occur after nanoparticle deposition in the alveoli. In this study, we compared the effects of surfactant-associated protein A (SP-A) and D (SP-D) on the clearance of magnetite nanoparticles (mNP) with either more hydrophilic (starch) or hydrophobic (phosphatidylcholine) surface modification by an alveolar macrophage (AM) cell line (MH-S) using flow cytometry and confocal microscopy. Both proteins enhanced the AM uptake of mNP compared with pristine nanoparticles; for the hydrophilic ST-mNP, this effect was strongest with SP-D, whereas for the hydrophobic PL-mNP it was most pronounced with SP-A. Using gel electrophoretic and dynamic light scattering methods, we were able to demonstrate that the observed cellular effects were related to protein adsorption and to protein-mediated interference with the colloidal stability. Next, we investigated the influence of various surfactant lipids on nanoparticle uptake by AM because lipids are the major surfactant component. Synthetic surfactant lipid and isolated native surfactant preparations significantly modulated the effects exerted by SP-A and SP-D, respectively, resulting in comparable levels of macrophage interaction for both hydrophilic and hydrophobic nanoparticles. Our findings suggest that because of the interplay of both surfactant lipids and proteins, the AM clearance of nanoparticles is essentially the same, regardless of different intrinsic surface properties.
first_indexed 2024-12-20T02:58:10Z
format Article
id doaj.art-c7c1074bf59248dc9680ce1d7c957ed5
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-20T02:58:10Z
publishDate 2012-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-c7c1074bf59248dc9680ce1d7c957ed52022-12-21T19:55:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0177e4077510.1371/journal.pone.0040775The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.Christian A RugeUlrich F SchaeferJennifer HerrmannJulian KirchOlga CañadasMercedes EchaideJesús Pérez-GilCristina CasalsRolf MüllerClaus-Michael LehrThe peripheral lungs are a potential entrance portal for nanoparticles into the human body due to their large surface area. The fact that nanoparticles can be deposited in the alveolar region of the lungs is of interest for pulmonary drug delivery strategies and is of equal importance for toxicological considerations. Therefore, a detailed understanding of nanoparticle interaction with the structures of this largest and most sensitive part of the lungs is important for both nanomedicine and nanotoxicology. Astonishingly, there is still little known about the bio-nano interactions that occur after nanoparticle deposition in the alveoli. In this study, we compared the effects of surfactant-associated protein A (SP-A) and D (SP-D) on the clearance of magnetite nanoparticles (mNP) with either more hydrophilic (starch) or hydrophobic (phosphatidylcholine) surface modification by an alveolar macrophage (AM) cell line (MH-S) using flow cytometry and confocal microscopy. Both proteins enhanced the AM uptake of mNP compared with pristine nanoparticles; for the hydrophilic ST-mNP, this effect was strongest with SP-D, whereas for the hydrophobic PL-mNP it was most pronounced with SP-A. Using gel electrophoretic and dynamic light scattering methods, we were able to demonstrate that the observed cellular effects were related to protein adsorption and to protein-mediated interference with the colloidal stability. Next, we investigated the influence of various surfactant lipids on nanoparticle uptake by AM because lipids are the major surfactant component. Synthetic surfactant lipid and isolated native surfactant preparations significantly modulated the effects exerted by SP-A and SP-D, respectively, resulting in comparable levels of macrophage interaction for both hydrophilic and hydrophobic nanoparticles. Our findings suggest that because of the interplay of both surfactant lipids and proteins, the AM clearance of nanoparticles is essentially the same, regardless of different intrinsic surface properties.http://europepmc.org/articles/PMC3393659?pdf=render
spellingShingle Christian A Ruge
Ulrich F Schaefer
Jennifer Herrmann
Julian Kirch
Olga Cañadas
Mercedes Echaide
Jesús Pérez-Gil
Cristina Casals
Rolf Müller
Claus-Michael Lehr
The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.
PLoS ONE
title The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.
title_full The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.
title_fullStr The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.
title_full_unstemmed The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.
title_short The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles.
title_sort interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles
url http://europepmc.org/articles/PMC3393659?pdf=render
work_keys_str_mv AT christianaruge theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT ulrichfschaefer theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT jenniferherrmann theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT juliankirch theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT olgacanadas theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT mercedesechaide theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT jesusperezgil theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT cristinacasals theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT rolfmuller theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT clausmichaellehr theinterplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT christianaruge interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT ulrichfschaefer interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT jenniferherrmann interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT juliankirch interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT olgacanadas interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT mercedesechaide interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT jesusperezgil interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT cristinacasals interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT rolfmuller interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles
AT clausmichaellehr interplayoflungsurfactantproteinsandlipidsassimilatesthemacrophageclearanceofnanoparticles