Physicochemical properties of nanoparticles regulate translocation across pulmonary surfactant monolayer and formation of lipoprotein corona

ACS Nano

Volumn 7, Issue 12, 2013, Pages 10525-10533

  Hu, Guoqing ^a   Jiao, Bao ^a   Shi, Xinghua ^a   Valle, Russell P ^b   Fan, Qihui ^b   Zuo, Yi Y ^b  

^a INSTITUTE OF MECHANICS   (China)

^b University of Hawaii at Manoa   (United States)

Author keywords

molecular dynamics; nanoparticle; protein corona; pulmonary surfactant

Indexed keywords

HYDROPHILIC NANOPARTICLES; HYDROPHOBIC NANOPARTICLES; PHYSICOCHEMICAL PROPERTY; PROTEIN CORONAS; PULMONARY DRUG DELIVERY; PULMONARY SURFACTANTS; SURFACTANT FILMS; TOXICOLOGICAL EFFECTS;

CATALYST ACTIVITY; HYDROPHOBICITY; LIPOPROTEINS; MOLECULAR DYNAMICS; PHOSPHOLIPIDS;

NANOPARTICLES;

BIOLOGICAL PRODUCT; CALFACTANT; HYDROXYAPATITE; LIPID; LIPOPROTEIN; LUNG SURFACTANT; NANOPARTICLE; POLYSTYRENE DERIVATIVE;

ADSORPTION; ANIMAL; ARTICLE; CATTLE; CHEMICAL PHENOMENA; CHEMISTRY; COMPUTER SIMULATION; DRUG DELIVERY SYSTEM; DRUG EFFECT; INHALATIONAL DRUG ADMINISTRATION; LIPID BILAYER; LUNG; MOLECULAR DYNAMICS; NANOTECHNOLOGY; PROTEIN TRANSPORT;

ADMINISTRATION, INHALATION; ADSORPTION; ANIMALS; BIOLOGICAL PRODUCTS; CATTLE; COMPUTER SIMULATION; DRUG DELIVERY SYSTEMS; DURAPATITE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; LIPIDS; LIPOPROTEINS; LUNG; MOLECULAR DYNAMICS SIMULATION; NANOPARTICLES; NANOTECHNOLOGY; POLYSTYRENES; PROTEIN TRANSPORT; PULMONARY SURFACTANTS;

EID: 84891351921     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn4054683     Document Type: Article

References (55)

1. Patton, J. S.; Byron, P. R. Inhaling Medicines: Delivering Drugs to the Body through the Lungs Nat. Rev. Drug Discovery 2007, 6, 67-74
2. Bailey, M. M.; Berkland, C. J. Nanoparticle Formulations in Pulmonary Drug Delivery Med. Res. Rev. 2009, 29, 196-212
3. Oberdorster, G.; Oberdorster, E.; Oberdorster, J. Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles Environ. Health Perspect. 2005, 113, 823-839
4. Nel, A.; Xia, T.; Madler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science 2006, 311, 622-627
5. Nel, A. E.; Madler, L.; Velegol, D.; Xia, T.; Hoek, E. M.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557
6. Monopoli, M. P.; Aberg, C.; Salvati, A.; Dawson, K. A. Biomolecular Coronas Provide the Biological Identity of Nanosized Materials Nat. Nanotechnol. 2012, 7, 779-786
7. Zuo, Y. Y.; Veldhuizen, R. A.; Neumann, A. W.; Petersen, N. O.; Possmayer, F. Current Perspectives in Pulmonary Surfactant-Inhibition, Enhancement and Evaluation Biochim. Biophys. Acta 2008, 1778, 1947-1977
8. McCormack, F. X.; Whitsett, J. A. The Pulmonary Collectins, SP-A and SP-D, Orchestrate Innate Immunity in the Lung J. Clin. Invest. 2002, 109, 707-712
9. Perez-Gil, J. Structure of Pulmonary Surfactant Membranes and Films: The Role of Proteins and Lipid-Protein Interactions Biochim. Biophys. Acta 2008, 1778, 1676-1695
10. Whitsett, J. A.; Weaver, T. E. Hydrophobic Surfactant Proteins in Lung Function and Disease N. Engl. J. Med. 2002, 347, 2141-2148
11. Schleh, C.; Muhlfeld, C.; Pulskamp, K.; Schmiedl, A.; Nassimi, M.; Lauenstein, H. D.; Braun, A.; Krug, N.; Erpenbeck, V. J.; Hohlfeld, J. M. The Effect of Titanium Dioxide Nanoparticles on Pulmonary Surfactant Function and Ultrastructure Respir. Res. 2009, 10, 90
12. Beck-Broichsitter, M.; Ruppert, C.; Schmehl, T.; Guenther, A.; Betz, T.; Bakowsky, U.; Seeger, W.; Kissel, T.; Gessler, T. Biophysical Investigation of Pulmonary Surfactant Surface Properties upon Contact with Polymeric Nanoparticles In Vitro Nanomed. 2011, 7, 341-350
13. Bakshi, M. S.; Zhao, L.; Smith, R.; Possmayer, F.; Petersen, N. O. Metal Nanoparticle Pollutants Interfere with Pulmonary Surfactant Function in Vitro Biophys. J. 2008, 94, 855-868
14. Sachan, A. K.; Harishchandra, R. K.; Bantz, C.; Maskos, M.; Reichelt, R.; Galla, H. J. High-Resolution Investigation of Nanoparticle Interaction with a Model Pulmonary Surfactant Monolayer ACS Nano 2012, 6, 1677-1687
15. Fan, Q.; Wang, Y. E.; Zhao, X.; Loo, J. S.; Zuo, Y. Y. Adverse Biophysical Effects of Hydroxyapatite Nanoparticles on Natural Pulmonary Surfactant ACS Nano 2011, 5, 6410-6416
16. Qiao, R.; Roberts, A. P.; Mount, A. S.; Klaine, S. J.; Ke, P. C. Translocation of C60 and its Derivatives across a Lipid Bilayer Nano Lett. 2007, 7, 614-619
17. Wong-Ekkabut, J.; Baoukina, S.; Triampo, W.; Tang, I. M.; Tieleman, D. P.; Monticelli, L. Computer Simulation Study of Fullerene Translocation through Lipid Membranes Nat. Nanotechnol. 2008, 3, 363-368
18. Shi, X.; von dem Bussche, A.; Hurt, R. H.; Kane, A. B.; Gao, H. Cell Entry of One-Dimensional Nanomaterials Occurs by Tip Recognition and Rotation Nat. Nanotechnol. 2011, 6, 714-719
19. Loo, S. C.; Moore, T.; Banik, B.; Alexis, F. Biomedical Applications of Hydroxyapatite Nanoparticles Curr. Pharm. Biotechnol. 2010, 11, 333-342
20. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T.; Dawson, K. A. Nanoparticle Size and Surface Properties Determine the Protein Corona with Possible Implications for Biological Impacts Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 14265-14270
21. Casals, C.; Canadas, O. Role of Lipid Ordered/Disordered Phase Coexistence in Pulmonary Surfactant Function Biochim. Biophys. Acta 2012, 1818, 2550-2562
22. Chavarha, M.; Loney, R. W.; Kumar, K.; Rananavare, S. B.; Hall, S. B. Differential Effects of the Hydrophobic Surfactant Proteins on the Formation of Inverse Bicontinuous Cubic Phases Langmuir 2012, 28, 16596-16604
23. Baoukina, S.; Tieleman, D. P. Lung Surfactant Protein SP-B Promotes Formation of Bilayer Reservoirs from Monolayer and Lipid Transfer between the Interface and Subphase Biophys. J. 2011, 100, 1678-1687
24. Baoukina, S.; Tieleman, D. P. Direct Simulation of Protein-Mediated Vesicle Fusion: Lung Surfactant Protein B Biophys. J. 2010, 99, 2134-2142
25. Zhang, H.; Fan, Q.; Wang, Y. E.; Neal, C. R.; Zuo, Y. Y. Comparative Study of Clinical Pulmonary Surfactants Using Atomic Force Microscopy Biochim. Biophys. Acta 2011, 1808, 1832-1842
26. Keating, E.; Zuo, Y. Y.; Tadayyon, S. M.; Petersen, N. O.; Possmayer, F.; Veldhuizen, R. A. A Modified Squeeze-Out Mechanism for Generating High Surface Pressures with Pulmonary Surfactant Biochim. Biophys. Acta 2012, 1818, 1225-1234
27. Baoukina, S.; Monticelli, L.; Risselada, H. J.; Marrink, S. J.; Tieleman, D. P. The Molecular Mechanism of Lipid Monolayer Collapse Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 10803-10808
28. Vollhardt, D.; Retter, U. Nucleation in Insoluble Monolayers 0.1. Nucleation and Growth-Model for Relaxation of Metastable Monolayers J. Phys. Chem. 1991, 95, 3723-3727
29. Zhang, H.; Wang, Y. E.; Fan, Q.; Zuo, Y. Y. On the Low Surface Tension of Lung Surfactant Langmuir 2011, 27, 8351-8358
30. Marrink, S. J.; de Vries, A. H.; Mark, A. E. Coarse Grained Model for Semiquantitative Lipid Simulations J. Phys. Chem. B 2004, 108, 750-760
31. Monticelli, L.; Kandasamy, S. K.; Periole, X.; Larson, R. G.; Tieleman, D. P.; Marrink, S. J. The MARTINI Coarse-Grained Force Field: Extension to Proteins J. Chem. Theory Comput. 2008, 4, 819-834
32. Kendall, M.; Holgate, S. Health Impact and Toxicological Effects of Nanomaterials in the Lung Respirology 2012, 17, 743-758
33. Nemmar, A.; Hamoir, J.; Nemery, B.; Gustin, P. Evaluation of Particle Translocation across the Alveolo-Capillary Barrier in Isolated Perfused Rabbit Lung Model Toxicology 2005, 208, 105-113
34. Chen, J.; Tan, M.; Nemmar, A.; Song, W.; Dong, M.; Zhang, G.; Li, Y. Quantification of Extrapulmonary Translocation of Intratracheal-Instilled Particles in Vivo in Rats: Effect of Lipopolysaccharide Toxicology 2006, 222, 195-201
35. Mills, N. L.; Amin, N.; Robinson, S. D.; Anand, A.; Davies, J.; Patel, D.; de la Fuente, J. M.; Cassee, F. R.; Boon, N. A.; Macnee, W. et al. Do Inhaled Carbon Nanoparticles Translocate Directly into the Circulation in Humans? Am. J. Respir. Crit. Care Med. 2006, 173, 426-431
36. Salvador-Morales, C.; Townsend, P.; Flahaut, E.; Venien-Bryan, C.; Vlandas, A.; Green, M. L. H.; Sim, R. B. Binding of Pulmonary Surfactant Proteins to Carbon Nanotubes; Potential for Damage to Lung Immune Defense Mechanisms Carbon 2007, 45, 607-617
37. Kapralov, A. A.; Feng, W. H.; Amoscato, A. A.; Yanamala, N.; Balasubramanian, K.; Winnica, D. E.; Kisin, E. R.; Kotchey, G. P.; Gou, P.; Sparvero, L. J. et al. Adsorption of Surfactant Lipids by Single-Walled Carbon Nanotubes in Mouse Lung upon Pharyngeal Aspiration ACS Nano 2012, 6, 4147-4156
38. Schulze, C.; Schaefer, U. F.; Ruge, C. A.; Wohlleben, W.; Lehr, C. M. Interaction of Metal Oxide Nanoparticles with Lung Surfactant Protein A Eur. J. Pharm. Biopharm. 2011, 77, 376-383
39. Ruge, C. A.; Schaefer, U. F.; Herrmann, J.; Kirch, J.; Canadas, O.; Echaide, M.; Perez-Gil, J.; Casals, C.; Muller, R.; Lehr, C. M. The Interplay of Lung Surfactant Proteins and Lipids Assimilates the Macrophage Clearance of Nanoparticles PLoS One 2012, 7, e40775
40. Longo, M. L.; Bisagno, A. M.; Zasadzinski, J. A.; Bruni, R.; Waring, A. J. A Function of Lung Surfactant Protein SP-B Science 1993, 261, 453-456
41. Choe, S.; Chang, R.; Jeon, J.; Violi, A. Molecular Dynamics Simulation Study of a Pulmonary Surfactant Film Interacting with a Carbonaceous Nanoparticle Biophys. J. 2008, 95, 4102-4114
42. Melton, K. R.; Nesslein, L. L.; Ikegami, M.; Tichelaar, J. W.; Clark, J. C.; Whitsett, J. A.; Weaver, T. E. SP-B Deficiency Causes Respiratory Failure in Adult Mice Am. J. Physiol. 2003, 285, L543-L549
43. Simonato, M.; Baritussio, A.; Vedovelli, L.; Lamonica, G.; Carnielli, V. P.; Cogo, P. E. Surfactant Protein B Amount and Kinetics in Newborn Infants: An Optimized Procedure J. Mass Spectrom. 2012, 47, 1415-1419
44. Lesniak, A.; Fenaroli, F.; Monopoli, M. P.; Aberg, C.; Dawson, K. A.; Salvati, A. Effects of the Presence or Absence of a Protein Corona on Silica Nanoparticle Uptake and Impact on Cells ACS Nano 2012, 6, 5845-5857
45. Hellstrand, E.; Lynch, I.; Andersson, A.; Drakenberg, T.; Dahlback, B.; Dawson, K. A.; Linse, S.; Cedervall, T. Complete High-Density Lipoproteins in Nanoparticle Corona FEBS. J. 2009, 276, 3372-3381
46. Sund, J.; Alenius, H.; Vippola, M.; Savolainen, K.; Puustinen, A. Proteomic Characterization of Engineered Nanomaterial-Protein Interactions in Relation to Surface Reactivity ACS Nano 2011, 5, 4300-4309
47. Ruge, C. A.; Kirch, J.; Canadas, O.; Schneider, M.; Perez-Gil, J.; Schaefer, U. F.; Casals, C.; Lehr, C. M. Uptake of Nanoparticles by Alveolar Macrophages Is Triggered by Surfactant Protein A Nanomedicine 2011, 7, 690-693
48. Gasser, M.; Wick, P.; Clift, M. J.; Blank, F.; Diener, L.; Yan, B.; Gehr, P.; Krug, H. F.; Rothen-Rutishauser, B. Pulmonary Surfactant Coating of Multi-Walled Carbon Nanotubes (MWCNTs) Influences their Oxidative and Pro-inflammatory Potential in Vitro Part. Fibre Toxicol. 2012, 9, 17
49. Schleh, C.; Kreyling, W. G.; Lehr, C. M. Pulmonary Surfactant is Indispensable in Order to Simulate the in Vivo Situation Part. Fibre Toxicol. 2013, 10, 6
50. Choi, H. S.; Ashitate, Y.; Lee, J. H.; Kim, S. H.; Matsui, A.; Insin, N.; Bawendi, M. G.; Semmler-Behnke, M.; Frangioni, J. V.; Tsuda, A. Rapid Translocation of Nanoparticles from the Lung Airspaces to the Body Nat. Biotechnol. 2010, 28, 1300-1303
51. Kreyling, W. G.; Hirn, S.; Schleh, C. Nanoparticles in the Lung Nat. Biotechnol. 2010, 28, 1275-1276
52. Poland, C. A.; Duffin, R.; Kinloch, I.; Maynard, A.; Wallace, W. A.; Seaton, A.; Stone, V.; Brown, S.; Macnee, W.; Donaldson, K. Carbon Nanotubes Introduced into the Abdominal Cavity of Mice Show Asbestos-Like Pathogenicity in a Pilot Study Nat. Nanotechnol. 2008, 3, 423-428
53. Ryman-Rasmussen, J. P.; Cesta, M. F.; Brody, A. R.; Shipley-Phillips, J. K.; Everitt, J. I.; Tewksbury, E. W.; Moss, O. R.; Wong, B. A.; Dodd, D. E.; Andersen, M. E. et al. Inhaled Carbon Nanotubes Reach the Subpleural Tissue in Mice Nat. Nanotechnol. 2009, 4, 747-751
54. Ng, S.; Guo, J.; Ma, J.; Loo, S. C. Synthesis of High Surface Area Mesostructured Calcium Phosphate Particles Acta Biomater. 2010, 6, 3772-3781
55. Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: A Package for Molecular Simulation and Trajectory Analysis J. Mol. Model. 2001, 7, 306-317