Precise quantification of nanoparticle internalization

ACS Nano

Volumn 7, Issue 6, 2013, Pages 4933-4945

  Gottstein, Claudia ^a   Wu, Guohui ^a   Wong, Benjamin J ^a   Zasadzinski, Joseph Anthony ^a  

^a University of California   (United States)

Author keywords

confocal laser scanning microscopy; drug delivery; flow cytometry; nanoparticle internalization; polyethylene glycol; reticuloendothelial system; vesosomes

Indexed keywords

BIOMEDICAL APPLICATIONS; CONFOCAL LASER SCANNING MICROSCOPY; HIGH-THROUGHPUT ANALYSIS; NANOPARTICLE INTERNALIZATIONS; PHYSICAL AND CHEMICAL PROPERTIES; RETICULOENDOTHELIAL SYSTEMS; THERAPEUTIC APPLICATION; VESOSOMES;

CELLS; COATINGS; CONFOCAL MICROSCOPY; CYTOLOGY; DIAGNOSIS; DRUG DELIVERY; FLOW CYTOMETRY; MATHEMATICAL MODELS; MEDICAL APPLICATIONS; POLYETHYLENE GLYCOLS;

NANOPARTICLES;

NANOPARTICLE; POLYSTYRENE DERIVATIVE;

ANIMAL; ARTICLE; CELL LINE; CHEMISTRY; CYTOLOGY; HUMAN; MACROPHAGE; METABOLISM; MONONUCLEAR PHAGOCYTE; MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; HUMANS; MACROPHAGES; MICE; MONONUCLEAR PHAGOCYTE SYSTEM; NANOPARTICLES; POLYSTYRENES;

EID: 84879651577     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn400243d     Document Type: Article

References (39)

1. Galimard, A.; Safi, M.; Ould-Moussa, N.; Montero, D.; Conjeaud, H.; Berret, J.-F. Thirty-Femtogram Detection of Iron in Mammalian Cells Small 2012, 8, 2036-2044
2. Lee, R. J.; Low, P. S. Delivery of Liposomes into Cultured KB Cells via Folate Receptor-mediated Endocytosis J. Biol. Chem. 1994, 269, 3198-3204
3. Sahlin, S.; Hed, J.; Runfquist, I. Differentiation between Attached and Ingested Immune Complexes by a Fluorescence Quenching Cytofluorometric Assay J. Immunol. Methods 1983, 60, 115-124
4. Nuutila, J.; Lilius, E.-M. Flow Cytometric Quantitative Determination of Ingestion by Phagocytes Needs the Distinguishing of Overlapping Populations of Binding and Ingesting Cells Cytometry, Part A 2005, 65A, 93-102
5. Sveum, R. J.; Chused, T. M.; Frank, M. M.; Brown, E. J. A Quantitative Fluorescent Method for Measurement of Bacterial Adherence and Phagocytosis J. Immunol. Methods 1986, 90, 257-264
6. Neumeyer, A.; Bukowski, M.; Veith, M.; Lehr, C.-M.; Daum, N. Propidium Iodide Labeling of Nanoparticles as a Novel Tool for the Quantification of Cellular Binding and Uptake Nanomedicine 2011, 7, 410-419
7. Johnstone, S. A.; Masin, D.; Mayer, L.; Bally, M. B. Surface-associated Serum Proteins Inhibit the Uptake of Phosphatidylserine and Poly(ethylene glycol) Liposomes by Mouse Macrophages Biochim. Biophys. Acta 2001, 1513, 25-37
8. Kostarelos, K.; Lacerda, L.; Pastorin, G.; Wu, W.; Wieckowski, S.; Luangsivilay, J.; Godefroy, S.; Pantarotto, D.; Briand, J.-P.; Muller, S. et al. Cellular Uptake of Functionalized Carbon Nanotubes is Independent of Functional Group and Cell Type Nat. Nanotechnol. 2007, 2, 108-113
9. Basiji, D. A.; Ortyn, W. E.; Liang, L.; Venkatachalam, V.; Morrissey, P. Cellular Image Analysis and Imaging by Flow Cytometry Clin. Lab. Med. 2007, 27, 653-670
10. Barteneva, N. S.; Fasler-Kan, E.; Vorobjev, I. A. Imaging Flow Cytometry: Coping with Heterogeneity in Biological Systems J. Histochem. Cytochem. 2012, 60, 723-733
11. Semmling, M.; Kreft, O.; Muñoz Javier, A.; Sukhorukov, G. B.; Käs, J.; Parak, W. J. A Novel Flow-Cytometry-Based Assay for Cellular Uptake Studies of Polyelectrolyte Microcapsules Small 2008, 4, 1763-1768
12. Pillay, C. S.; Elliott, E.; Dennison, C. Endolysosomal Proteolysis and its Regulation Biochem. J. 2002, 363, 417-429
13. Chen, A. K.; Cheng, Z.; Behlke, M. A.; Tsourkas, A. Assessing the Sensitivity of Commercially Available Fluorophores to the Intracellular Environment Anal. Chem. 2008, 80, 7437-7444
14. Molecular Probes Handbook; Life Technologies Corporation: Grand Island, NY. Online link: www.invitrogen.com/site/us/en/home/References/Molecular-Probes- The-Handbook.html; 2013, accessed May 2013.
15. Graber, M. L.; DiLillo, D. C.; Friedman, B. L.; Pastoriza-Munoz, E. Characteristics of Fluoroprobes for Measuring Intracellular pH Anal. Biochem. 1986, 156, 202-212
16. Walker, S. A.; Kennedy, M. T.; Zasadzinski, J. A. Encapsulation of Bilayer Vesicles by Self-assembly Nature 1997, 387, 61-64
17. Boyer, C.; Zasadzinski, J. Multiple Lipid Compartments Slow Vesicle Contents Release in Lipases and Serum ACS Nano 2007, 1, 176-182
18. Gabizon, A.; Papahadjopoulos, D. Liposome Formulations with Prolonged Circulation Time in Blood and Enhanced Uptake by Tumors Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 6949-53
19. Allen, T.; Sapra, P.; Moase, E. Use of the Post-Insertion Method for the Formation of Ligand-coupled Liposomes Cell. Mol. Biol. Lett. 2002, 7, 889-94
20. Dos Santos, N.; Allen, C.; Doppen, A.-M.; Anantha, M.; Cox, K.; Gallagher, R.; Karlsson, G.; Edwards, K.; Kenner, G.; Samuels, L. et al. Influence of Poly(ethylene glycol) Grafting Density and Polymer Length on Liposomes: Relating Plasma Circulation Lifetimes to Protein Binding Biochim. Biophys. Acta 2007, 1768, 1367-1377
21. Cedervall, T.; Lynch, I.; Lindman, S.; BerggaÌŠrd, T.; Thulin, E.; Nilsson, H.; Dawson, K. A.; Linse, S. Understanding the Nanoparticle-protein Corona using Methods to Quantify Exchange Rates and Affinities of Proteins for Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 2050-2055
22. Cedervall, T.; Lynch, I.; Foy, M.; BerggaÌŠrd, T.; Donnelly, S. C.; Cagney, G.; Linse, S.; Dawson, K. A. Detailed Identification of Plasma Proteins Adsorbed on Copolymer Nanoparticles Angew. Chem., Int. Ed. 2007, 46, 5754-5756
23. Vroman, L. Effect of Absorbed Proteins on the Wettability of Hydrophilic and Hydrophobic Solids Nature 1962, 196, 476-477
24. Lundqvist, M.; Stigler, J.; Cedervall, T.; Berggard, T.; Flanagan, M. B.; Lynch, I.; Elia, G.; Dawson, K. The Evolution of the Protein Corona around Nanoparticles: A Test Study ACS Nano 2011, 5, 7503-7509
25. Casals, E.; Pfaller, T.; Duschl, A.; Oostingh, G. J.; Puntes, V. Time Evolution of the Nanoparticle Protein Corona ACS Nano 2010, 4, 3623-3632
26. Walczyk, D.; Bombelli, F. B.; Monopoli, M. P.; Lynch, I.; Dawson, K. A. What the Cell "Sees" in Bionanoscience J. Am. Chem. Soc. 2010, 132, 5761-5768
27. Walkey, C. D.; Chan, W. C. W. Understanding and Controlling the Interaction of Nanomaterials with Proteins in a Physiological Environment Chem. Soc. Rev. 2012, 41, 2780-2799
28. Gebauer, J. S.; Malissek, M.; Simon, S.; Knauer, S. K.; Maskos, M.; Stauber, R. H.; Peukert, W.; Treuel, L. Impact of the Nanoparticle-Protein Corona on Colloidal Stability and Protein Structure Langmuir 2012, 28, 9673-9679
29. 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
30. Safi, M.; Courtois, J.; Seigneuret, M.; Conjeaud, H.; Berret, J. F. The Effects of Aggregation and Protein Corona on the Cellular Internalization of Iron Oxide Nanoparticles Biomaterials 2011, 32, 9353-9363
31. Petri-Fink, A.; Steitz, B.; Finka, A.; Salaklang, J.; Hofmann, H. Effect of Cell Media on Polymer-coated Superparamagnetic Iron Oxide Nanoparticles (SPIONs): Colloidal Stability, Cytotoxicity, and Cellular Uptake Studies Eur. J. Pharm. Biopharm. 2008, 68, 129-137
32. 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
33. Safi, M.; Sarrouj, H.; Sandre, O.; Mignet, N.; Berret, J. F. Interactions between Sub-10-nm Iron and Cerium Oxide Nanoparticles and 3T3 Fibroblasts: the Role of the Coating and Aggregation State Nanotechnology 2010, 21, 145103
34. Huehn, D.; Kantner, K.; Geidel, C.; Brandholt, S.; De Cock, I.; Soenen, S. J. H.; Rivera Gil, P.; Montenegro, J.-M.; Braeckmans, K.; Muellen, K. et al. Polymer-Coated Nanoparticles Interacting with Proteins and Cells: Focusing on the Sign of the Net Charge ACS Nano 2013, 7, 3253-3263
35. Jiang, X.; Weise, S.; Hafner, M.; Roecker, C.; Zhang, F.; Parak, W. J.; Nienhaus, G. U. Quantitative Analysis of the Protein Corona on FePt Nanoparticles Formed by Transferrin Binding. J. R. Soc., Interface 2010, 7 (Suppl 1), S5-S13.
36. Kriete, A.; Papazoglou, E.; Edrissi, B.; Pais, H.; Pourrezaei, K. Automated Quantification of Quantum-dot-labelled Epidermal Growth Factor Receptor Internalization via Multiscale Image Segmentation J. Microsc. 2006, 222, 22-27
37. Schweiger, C.; Hartmann, R.; Zhang, F.; Parak, W.; Kissel, T.; Rivera Gil, P. Quantification of the Internalization Patterns of Superparamagnetic Iron Oxide Nanoparticles with Opposite Charge J. Nanobiotechnol. 2012, 10, 28-38
38. Kisak, E. T.; Coldren, B.; Zasadzinski, J. Nanocompartments Enclosing Vesicles, Colloids and Macromolecules via Interdigitated Lipid Bilayers Langmuir 2002, 18, 284-288
39. Tzur, A.; Moore, J. K.; Jorgensen, P.; Shapiro, H. M.; Kirschner, M. W. Optimizing Optical Flow Cytometry for Cell Volume-Based Sorting and Analysis PLoS One 2011, 6, e16053