Surface Functionalization of Nanoparticles with Polyethylene Glycol: Effects on Protein Adsorption and Cellular Uptake

ACS Nano

Volumn 9, Issue 7, 2015, Pages 6996-7008

  Pelaz, Beatriz ^a   Del Pino, Pablo ^b   Maffre, Pauline ^c   Hartmann, Raimo ^a   Gallego, Marta ^b   Rivera Fernández, Sara ^d   De La Fuente, Jesus M ^d   Nienhaus, G Ulrich ^c,e   Parak, Wolfgang J ^a,b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b CIC BIOMAGUNE   (Spain)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF ZARAGOZA   (Spain)

^e University of Illinois at Urbana Champaign   (United States)

Author keywords

fibrinogen; fluorescence correlation spectroscopy; human serum albumin; nanoparticle; polyethylene glycol; polymer coating; protein corona

Indexed keywords

ADSORPTION; BODY FLUIDS; CELL CULTURE; COATINGS; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; NANOPARTICLES; PLASTIC COATINGS; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; POLYETHYLENES; POLYMERS; SPECTROSCOPIC ANALYSIS;

FIBRINOGEN; FLUORESCENCE CORRELATION SPECTROSCOPY; HUMAN SERUM ALBUMINS; POLYMER COATING; PROTEIN CORONAS;

PROTEINS;

ALBUMINOID; FIBRINOGEN; MACROGOL DERIVATIVE; NANOPARTICLE;

3T3 CELL LINE; ADSORPTION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; FIBROBLAST; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

3T3 CELLS; ADSORPTION; ALBUMINS; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; FIBRINOGEN; FIBROBLASTS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NANOPARTICLES; POLYETHYLENE GLYCOLS;

EID: 84938152097     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b01326     Document Type: Article

References (110)

1. Nel, A. E.; Madler, L.; Velegol, D.; Xia, T.; Hoek, E. M. V.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557
2. Monopoli, M. P.; Walczyk, D.; Campbell, A.; Elia, G.; Lynch, I.; Bombelli, F. B.; Dawson, K. A. Physical-Chemical Aspects of Protein Corona: Relevance to in Vitro and in Vivo Biological Impacts of Nanoparticles J. Am. Chem. Soc. 2011, 133, 2525-2534
3. Akesson, A.; Cardenas, M.; Elia, G.; Monopoli, M. P.; Dawson, K. A. The Protein Corona of Dendrimers: PAMAM Binds and Activates Complement Proteins in Human Plasma in a Generation Dependent Manner RSC Adv. 2012, 2, 11245-11248
4. Hamad, I.; Al-Hanbali, O.; Hunter, A. C.; Rutt, K. J.; Andresen, T. L.; Moghimi, S. M. Distinct Polymer Architecture Mediates Switching of Complement Activation Pathways at the Nanosphere-Serum Interface: Implications for Stealth Nanoparticle Engineering ACS Nano 2010, 4, 6629-6638
5. Zhang, Y.; Kohler, N.; Zhang, M. Q. Surface Modification of Superparamagnetic Magnetite Nanoparticles and Their Intracellular Uptake Biomaterials 2002, 23, 1553-1561
6. Xie, J.; Xu, C.; Kohler, N.; Hou, Y.; Sun, S. Controlled PEGylation of Monodisperse Fe3O4 Nanoparticles for Reduced Non-specific Uptake by Macrophage Cells Adv. Mater. 2007, 19, 3163-3166
7. Ryman-Rasmussen, J. P.; Riviere, J. E.; Monteiro-Riviere, N. A. Variables Influencing Interactions of Untargeted Quantum Dot Nanoparticles with Skin Cells and Identification of Biochemical Modulators Nano Lett. 2007, 7, 1344-1348
8. Hak, S.; Helgesen, E.; Hektoen, H. H.; Huuse, E. M.; Jarzyna, P. A.; Mulder, W. J. M.; Haraldseth, O.; Davies, C. L. The Effect of Nanoparticle Polyethylene Glycol Surface Density on Ligand-Directed Tumor Targeting Studied in Vivo by Dual Modality Imaging ACS Nano 2012, 6, 5648-5658
9. Gref, R.; Lück, M.; Quellec, P.; Marchand, M.; Dellacherie, E.; Harnisch, S.; Blunk, T.; Müller, R. H. 'Stealth' Corona-Core Nanoparticles Surface Modified by Polyethylene Glycol (PEG): Influences of the Corona (PEG Chain Length and Surface Density) and of the Core Composition on Phagocytic Uptake and Plasma Protein Adsorption Colloids Surf., B 2000, 18, 301-313
10. He, Q.; Zhang, J.; Shi, J.; Zhu, Z.; Zhang, L.; Bu, W.; Guo, L.; Chen, Y. The Effect of PEGylation of Mesoporous Silica Nanoparticles on Nonspecific Binding of Serum Proteins and Cellular Responses Biomaterials 2010, 31, 1085-1092
11. Dai, Q.; Walkey, C.; Chan, W. C. W. Polyethylene Glycol Backfilling Mitigates the Negative Impact of the Protein Corona on Nanoparticle Cell Targeting Angew. Chem., Int. Ed. 2014, 53, 5093-5096
12. Ballou, B.; Lagerholm, B. C.; Ernst, L. A.; Bruchez, M. P.; Waggoner, A. S. Noninvasive Imaging of Quantum Dots in Mice Bioconjugate Chem. 2004, 15, 79-86
13. Daou, T. J.; Li, L.; Reiss, P.; Josserand, V.; Texier, I. Effect of Poly(ethylene glycol) Length on the in Vivo Behavior of Coated Quantum Dots Langmuir 2009, 25, 3040-3044
14. Lipka, M.; Semmler-Behnke, M.; Sperling, R. A.; Wenk, A.; Takenaka, S.; Schleh, C.; Kissel, T.; Parak, W. J.; Kreyling, W. G. Biodistribution of PEG-Modified Gold Nanoparticles Following Intratracheal Instillation and Intravenous Injection Biomaterials 2010, 31, 6574-6581
15. von Maltzahn, G.; Park, J.-H.; Agrawal, A.; Bandaru, N. K.; Das, S. K.; Sailor, M. J.; Bhatia, S. N. Computationally Guided Photothermal Tumor Therapy Using Long-Circulating Gold Nanorod Antennas Cancer Res. 2009, 69, 3892-3900
16. Cho, W. S.; Cho, M.; Jeong, J.; Choi, M.; Han, B. S.; Shin, H. S.; Hong, J.; Chung, B. H.; Jeong, J.; Cho, M. H. Size-Dependent Tissue Kinetics of PEG-Coated Gold Nanoparticles Toxicol. Appl. Pharmacol. 2010, 245, 116-123
17. Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. W. Mediating Tumor Targeting Efficiency of Nanoparticles through Design Nano Lett. 2009, 9, 1909-1915
18. Kingshott, P.; Thissen, H.; Griesser, H. J. Effects of Cloud-Point Grafting, Chain Length, and Density of PEG Layers on Competitive Adsorption of Ocular Proteins Biomaterials 2002, 23, 2043-2056
19. Pasche, S.; De Paul, S. M.; Voros, J.; Spencer, N. D.; Textor, M. Poly(l -lysine)-graft-Poly(ethylene glycol) Assembled Monolayers on Niobium Oxide Surfaces: A Quantitative Study of the Influence of Polymer Interfacial Architecture on Resistance to Protein Adsorption by ToF-SIMS and in Situ OWLS Langmuir 2003, 19, 9216-9225
20. Moros, M.; Pelaz, B.; Lopez-Larrubia, P.; Garcia-Martin, M. L.; Grazu, V.; de la Fuente, J. M. Engineering Biofunctional Magnetic Nanoparticles for Biotechnological Applications Nanoscale 2010, 2, 1746-1755
21. Wattendorf, U.; Merkle, H. P. PEGylation as a Tool for the Biomedical Engineering of Surface Modified Microparticles J. Pharm. Sci. 2008, 97, 4655-4669
22. Pozzi, D.; Colapicchioni, V.; Caracciolo, G.; Piovesana, S.; Capriotti, A. L.; Palchetti, S.; De Grossi, S.; Riccioli, A.; Amenitsch, H.; Lagana, A. Effect of Polyethyleneglycol (PEG) Chain Length on the Bio-Nano-Interactions between PEGylated Lipid Nanoparticles and Biological Fluids: From Nanostructure to Uptake in Cancer Cells Nanoscale 2014, 6, 2782-2792
23. Gordon, D. L.; Rice, J. L. Opsonin-Dependent and Independent Surface Phagocytosis of S. aureus Proceeds Independently of Complement and Complement Receptors Immunology 1988, 64, 709-714
24. Waku, T.; Matsusaki, M.; Kaneko, T.; Akashi, M. PEG Brush Peptide Nanospheres with Stealth Properties and Chemical Functionality Macromolecules 2007, 40, 6385-6392
25. Orts-Gil, G.; Natte, K.; Thiermann, R.; Girod, M.; Rades, S.; Kalbe, H.; Thuenemann, A. F.; Maskos, M.; Oesterle, W. On the Role of Surface Composition and Curvature on Biointerface Formation and Colloidal Stability of Nanoparticles in a Protein-Rich Model System Colloids Surf., B 2013, 108, 110-119
26. Bargheer, D.; Nielsen, J.; Gebel, G.; Heine, M.; Salmen, S. C.; Stauber, R.; Weller, H.; Heeren, J.; Nielsen, P. The Fate of a Designed Protein Corona on Nanoparticles in Vitro and in Vivo Beilstein J. Nanotechnol. 2015, 6, 36-46
27. Torrisi, V.; Graillot, A.; Vitorazi, L.; Crouzet, Q.; Marletta, G.; Loubat, C.; Berret, J. F. Preventing Corona Effects: Multiphosphonic Acid Poly(ethylene glycol) Copolymers for Stable Stealth Iron Oxide Nanoparticles Biomacromolecules 2014, 15, 3171-3179
28. Treuel, L.; Brandholt, S.; Maffre, P.; Wiegele, S.; Shang, L.; Nienhaus, G. U. Impact of Protein Modification on the Protein Corona on Nanoparticles and Nanoparticle-Cell Interactions ACS Nano 2014, 8, 503-513
29. McPherson, T.; Kidane, A.; Szleifer, I.; Park, K. Prevention of Protein Adsorption by Tethered Poly(ethylene oxide) Layers: Experiments and Single-Chain Mean-Field Analysis Langmuir 1998, 14, 176-186
30. Michel, R.; Pasche, S.; Textor, M.; Castner, D. G. Influence of PEG Architecture on Protein Adsorption and Conformation Langmuir 2005, 21, 12327-12332
31. Pasche, S.; Vörös, J.; Griesser, H. J.; Spencer, N. D.; Textor, M. Effects of Ionic Strength and Surface Charge on Protein Adsorption at PEGylated Surfaces J. Phys. Chem. B 2005, 109, 17545-17552
32. Mrksich, M.; Whitesides, G. M. Using Self-Assembled Monolayers To Understand the Interactions of Man-Made Surfaces with Proteins and Cells Annu. Rev. Biophys. Biomol. Struct. 1996, 25, 55-78
33. Ostuni, E.; Chapman, R. G.; Holmlin, R. E.; Takayama, S.; Whitesides, G. M. A Survey of Structure-Property Relationships of Surfaces That Resist the Adsorption of Protein Langmuir 2001, 17, 5605-5620
34. Mrksich, M.; Chen, C. S.; Xia, Y.; Dike, L. E.; Ingber, D. E.; Whitesides, G. M. Controlling Cell Attachment on Contoured Surfaces with Self-Assembled Monolayers of Alkanethiolates on Gold Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 10775-10778
35. Zhang, M.; Desai, T.; Ferrari, M. Proteins and Cells on PEG Immobilized Silicon Surfaces Biomaterials 1998, 19, 953-960
36. Jeon, S. I.; Lee, J. H.; Andrade, J. D.; De Gennes, P. G. Protein-Surface Interactions in the Presence of Polyethylene Oxide: I. Simplified Theory J. Colloid Interface Sci. 1991, 142, 149-158
37. Sofia, S. J.; Premnath, V.; Merrill, E. W. Poly(ethylene oxide) Grafted to Silicon Surfaces: Grafting Density and Protein Adsorption Macromolecules 1998, 31, 5059-5070
38. Piehler, J.; Brecht, A.; Valiokas, R.; Liedberg, B.; Gauglitz, G. A High-Density Poly(ethylene glycol) Polymer Brush for Immobilization on Glass-Type Surfaces Biosens. Bioelectron. 2000, 15, 473-483
39. Sheth, S. R.; Leckband, D. Measurements of Attractive Forces between Proteins and End-Grafted Poly(ethylene glycol) Chains Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 8399-8404
40. Klapper, Y.; Vranceanu, M.; Ishitsuka, Y.; Evans, D.; Scheider, D.; Nienhaus, G. U.; Leneweit, G. Surface Energy of Phospholipid Bilayers and the Correlation to Their Hydration J. Colloid Interface Sci. 2013, 390, 267-274
41. Yang, Z.; Galloway, J. A.; Yu, H. Protein Interactions with Poly(ethylene glycol) Self-Assembled Monolayers on Glass Substrates: Diffusion and Adsorption Langmuir 1999, 15, 8405-8411
42. Heyes, C. D.; Kobitski, A. Y.; Amirgoulova, E. V.; Nienhaus, G. U. Biocompatible Surfaces for Specific Tethering of Individual Protein Molecules J. Phys. Chem. B 2004, 108, 13387-13394
43. Amirgoulova, E. V.; Groll, J.; Heyes, C. D.; Ameringer, T.; Röcker, C.; Möller, M.; Nienhaus, G. U. Biofunctionalized Polymer Surfaces Exhibiting Minimal Interaction towards Immobilized Proteins ChemPhysChem 2004, 5, 552-555
44. Groll, J.; Amirgoulova, E. V.; Ameringer, T.; Heyes, C. D.; Röcker, C.; Nienhaus, G. U.; Möller, M., Biofunctionalized, Ultrathin Coatings of Cross-Linked Star-Shaped Poly(ethylene oxide) Allow Reversible Folding of Immobilized Proteins J. Am. Chem. Soc. 2004, 126, 4234-4239
45. Heyes, C. D.; Groll, J.; Möller, M.; Nienhaus, G. U. Synthesis, Patterning and Applications of Star-Shaped Poly(ethylene glycol) Biofunctionalized Surfaces Mol. BioSyst. 2007, 3, 419-430
46. Harder, P.; Grunze, M.; Dahint, R.; Whitesides, G. M.; Laibinis, P. E. Molecular Conformation in Oligo(ethylene glycol)-Terminated Self-Assembled Monolayers on Gold and Silver Surfaces Determines Their Ability To Resist Protein Adsorption J. Phys. Chem. B 1998, 102, 426-436
47. Wang, R. L. C.; Kreuzer, H. J.; Grunze, M. Molecular Conformation and Solvation of Oligo(ethylene glycol)-Terminated Self-Assembled Monolayers and Their Resistance to Protein Adsorption J. Phys. Chem. B 1997, 101, 9767-9773
48. Sperling, R. A.; Pellegrino, T.; Li, J. K.; Chang, W. H.; Parak, W. J. Electrophoretic Separation of Nanoparticles with a Discrete Number of Functional Groups Adv. Funct. Mater. 2006, 16, 943-948
49. Sperling, R. A.; Liedl, T.; Duhr, S.; Kudera, S.; Zanella, M.; Lin, C.-A. J.; Chang, W. H.; Braun, D.; Parak, W. J. Size Determination of (Bio-) Conjugated Water-Soluble Colloidal Nanoparticles: A Comparison of Different Techniques J. Phys. Chem. C 2007, 111, 11552-11559
50. Parak, W. J.; Pellegrino, T.; Micheel, C. M.; Gerion, D.; Williams, S. C.; Alivisatos, A. P. Conformation of Oligonucleotides Attached to Gold Nanocrystals Probed by Gel Electrophoresis Nano Lett. 2003, 3, 33-36
51. Pellegrino, T.; Sperling, R. A.; Alivisatos, A. P.; Parak, W. J. Gel Electrophoresis of Gold-DNA Nanoconjugates J. Biomed. Biotechnol. 2007, 2007, 26796
52. Brandenberger, C.; Mühlfeld, C.; Ali, Z.; Lenz, A.-G.; Schmid, O.; Parak, W. J.; Gehr, P.; Rothen-Rutishauser, B. Quantitative Evaluation of Cellular Uptake and Trafficking of Plain and Polyethylene Glycol-Coated Gold Nanoparticles Small 2010, 6, 1669-1678
53. Van Hoecke, K.; De Schamphelaer, K. A. C.; Ali, Z.; Zhang, F.; Elsaesser, A.; Rivera Gil, P.; Parak, W. J.; Smagghe, G.; Janssen, C. R. Ecotoxicity and Uptake of Polymer Coated Gold Nanoparticles Nanotoxicology 2013, 7, 37-47
54. Rivera Gil, P.; Jimenez de Aberasturi, D.; Wulf, V.; Pelaz, B.; del Pino, P.; Zhao, Y.; de la Fuente, J.; Ruiz de Larramendi, I.; Rojo, T.; Liang, X.-J. The Challenge To Relate the Physicochemical Properties of Colloidal Nanoparticles to Their Cytotoxicity Acc. Chem. Res. 2013, 46, 743-749
55. Chithrani, B. D.; Ghazan, A. A.; Chan, C. W. Determining the Size and the Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells Nano Lett. 2006, 6, 662-668
56. Pellegrino, T.; Kudera, S.; Liedl, T.; Javier, A. M.; Manna, L.; Parak, W. J. On the Development of Colloidal Nanoparticles towards Multifunctional Structures and Their Possible Use for Biological Applications Small 2005, 1, 48-63
57. Logie, J.; Owen, S. C.; McLaughlin, C. K.; Shoichet, M. S. PEG-Graft Density Controls Polymeric Nanoparticle Micelle Stability Chem. Mater. 2014, 26, 2847-2855
58. Nazarenus, M.; Zhang, Q.; Soliman, M. G.; del Pino, P.; Pelaz, B.; Carregal Romero, S.; Rejman, J.; Rothen-Ruthishauser, B.; Clift, M. J. D.; Zellner, R. In Vitro Interaction of Colloidal Nanoparticles with Mammalian Cells: What Have We Learned Thus Far? Beilstein J. Nanotechnol. 2014, 5, 1477-1490
59. Zhang, F.; Lees, E.; Amin, F.; Rivera Gil, P.; Yang, F.; Mulvaney, P.; Parak, W. J. Polymer-Coated Nanoparticles: A Universal Tool for Biolabelling Experiments Small 2011, 7, 3113-3127
60. Röcker, C.; Pötzl, M.; Zhang, F.; Parak, W. J.; Nienhaus, G. U. A Quantitative Fluorescence Study of Protein Monolayer Formation on Colloidal Nanoparticles Nat. Nanotechnol. 2009, 4, 577-580
61. Jiang, X.; Weise, S.; Hafner, M.; Röcker, 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, S5-S13
62. Maffre, P.; Nienhaus, K.; Amin, F.; Parak, W. J.; Nienhaus, G. U. Characterization of Protein Adsorption onto FePt Nanoparticles Using Dual-Focus Fluorescence Correlation Spectroscopy Beilstein J. Nanotechnol. 2011, 2, 374-383
63. Nienhaus, G. U.; Maffre, P.; Nienhaus, K. Studying the Protein Corona on Nanoparticles by FCS Methods Enzymol. 2013, 519, 115-137
64. Maffre, P.; Brandholt, S.; Nienhaus, K.; Shang, L.; Parak, W. J.; Nienhaus, G. U. Effects of Surface Functionalization on the Adsorption of Human Serum Albumin onto Nanoparticles: A Fluorescence Correlation Spectroscopy Study Beilstein J. Nanotechnol. 2014, 5, 2036-2047
65. Klapper, Y.; Maffre, P.; Shang, L.; Ekdahl, K. N.; Nilsson, B.; Hettler, S.; Dries, M.; Gerthsen, D.; Nienhaus, G. U. Low Affinity Binding of Plasma Proteins to Lipid-Coated Quantum Dots As Observed by in Situ Fluorescence Correlation Spectroscopy Nanoscale 2015, 7, 9980-9984
66. Ferrer, M. L.; Duchowicz, R.; Carrasco, B.; de la Torre, J. G.; Acuña, A. U. The Conformation of Serum Albumin in Solution: A Combined Phosphorescence Depolarization-Hydrodynamic Modeling Study Biophys. J. 2001, 80, 2422-2430
67. Vroman, L. Effect of Adsorbed Proteins on Wettability of Hydrophilic and Hydrophobic Solids Nature 1962, 196, 476-477
68. Noh, H.; Vogler, E. A. Volumetric Interpretation of Protein Adsorption: Competition from Mixtures and the Vroman Effect Biomaterials 2007, 28, 405-422
69. Jung, S.-Y.; Lim, S.-M.; Albertorio, F.; Kim, G.; Gurau, M. C.; Yang, R. D.; Holden, M. A.; Cremer, P. S. The Vroman Effect: A Molecular Level Description of Fibrinogen Displacement J. Am. Chem. Soc. 2003, 125, 12782-12786
70. Hirsh, S. L.; McKenzie, D. R.; Nosworthy, N. J.; Denman, J. A.; Sezerman, O. U.; Bilek, M. M. M. The Vroman Effect: Competitive Protein Exchange with Dynamic Multilayer Protein Aggregates Colloids Surf., B 2013, 103, 395-404
71. Hühn, D.; Kantner, K.; Geidel, C.; Brandholt, S.; De Cock, I.; Soenen, S. J. H.; Rivera Gil, P.; Montenegro, J.-M.; Braeckmans, K.; Müllen, K. Polymer-Coated Nanoparticles Interacting with Proteins and Cells: Focusing on the Sign of the Net Charge ACS Nano 2013, 7, 3253-3263
72. Caballero-Díaz, E.; Pfeiffer, C.; Kastl, L.; Rivera Gil, P.; Simonet, B.; Valcárcel, M.; Jiménez-Lamana, J.; Laborda, F.; Parak, W. J. The Toxicity of Silver Nanoparticles Depends on Their Uptake by Cells and Thus on Their Surface Chemistry Part. Part. Syst. Charact. 2013, 30, 1079-1085
73. del Pino, P.; Pelaz, B.; Zhang, Q.; Maffre, P.; Nienhaus, G. U.; Parak, W. J. Protein Corona Formation around Nanoparticles: From the Past to the Future Mater. Horiz. 2014, 1, 301-313
74. Huang, R.; Carney, R. P.; Ikuma, K.; Stellacci, F.; Lau, B. L. T. Effects of Surface Compositional and Structural Heterogeneity on Nanoparticle-Protein Interactions: Different Protein Configurations ACS Nano 2014, 8, 5402-5412
75. Dominguez-Medina, S.; McDonough, S.; Swanglap, P.; Landes, C. F.; Link, S. In Situ Measurement of Bovine Serum Albumin Interaction with Gold Nanospheres Langmuir 2012, 28, 9131-9139
76. Dobrovolskaia, M. A.; Neun, B. W.; Man, S.; Ye, X.; Hansen, M.; Patri, A. K.; Crist, R. M.; McNeil, S. E. Protein Corona Composition Does Not Accurately Predict Hematocompatibility of Colloidal Gold Nanoparticles Nanomedicine 2014, 10, 1453-1463
77. Halperin, A. Polymer Brushes That Resist Adsorption of Model Proteins: Design Parameters Langmuir 1999, 15, 2525-2533
78. Gon, S.; Santore, M. M. Sensitivity of Protein Adsorption to Architectural Variations in a Protein-Resistant Polymer Brush Containing Engineered Nanoscale Adhesive Sites Langmuir 2011, 27, 15083-15091
79. Gon, S.; Bendersky, M.; Ross, J. L.; Santore, M. M. Manipulating Protein Adsorption Using a Patchy Protein-Resistant Brush Langmuir 2010, 26, 12147-12154
80. Park, H.-W.; Choi, J.; Ohn, K.; Lee, H.; Kim, J. W.; Won, Y.-Y. Study of the Air-Water Interfacial Properties of Biodegradable Polyesters and Their Block Copolymers with Poly(ethylene glycol) Langmuir 2012, 28, 11555-11566
81. Schneck, E.; Schollier, A.; Halperin, A.; Moulin, M.; Haertlein, M.; Sferrazza, M.; Fragneto, G. Neutron Reflectometry Elucidates Density Profiles of Deuterated Proteins Adsorbed onto Surfaces Displaying Poly(ethylene glycol) Brushes: Evidence for Primary Adsorption Langmuir 2013, 29, 14178-14187
82. Backmann, N.; Kappeler, N.; Braun, T.; Huber, F.; Lang, H.-P.; Gerber, C.; Lim, R. Y. H. Sensing Surface PEGylation with Microcantilevers Beilstein J. Nanotechnol. 2010, 1, 3-13
83. Perry, J. L.; Reuter, K. G.; Kai, M. P.; Herlihy, K. P.; Jones, S. W.; Luft, J. C.; Napier, M.; Bear, J. E.; DeSimone, J. M. PEGylated PRINT Nanoparticles: The Impact of PEG Density on Protein Binding, Macrophage Association, Biodistribution, and Pharmacokinetics Nano Lett. 2012, 12, 5304-5310
84. Sacchetti, C.; Motamedchaboki, K.; Magrini, A.; Palmieri, G.; Mattei, M.; Bernardini, S.; Rosato, N.; Bottini, N.; Bottini, M. Surface Polyethylene Glycol Conformation Influences the Protein Corona of Polyethylene Glycol-Modified Single-Walled Carbon Nanotubes: Potential Implications on Biological Performance ACS Nano 2013, 7, 1974-1989
85. Lee, J. H.; Jeong, B. J.; Lee, H. B. Plasma Protein Adsorption and Platelet Adhesion onto Comb-like PEO Gradient Surfaces J. Biomed. Mater. Res. 1997, 34, 105-114
86. Rabanel, J.-M.; Hildgen, P.; Banquy, X. Assessment of PEG on Polymeric Particles Surface, a Key Step in Drug Carrier Translation J. Controlled Release 2014, 185, 71-87
87. Hafner, A. M.; Burschowsky, D.; Corthesy, B.; Textor, M.; Merkle, H. P. Surface Assembly of Poly(I:C) on PEGylated Microspheres to Shield from Adverse Interactions with Fibroblasts J. Controlled Release 2012, 159, 204-214
88. Amin, F.; Yushchenko, D. A.; Montenegro, J. M.; Parak, W. J. Integration of Organic Fluorophores in the Surface of Polymer-Coated Colloidal Nanoparticles for Sensing the Local Polarity of the Environment ChemPhysChem 2012, 13, 1030-1035
89. Choi, J. Y.; Park, E. J.; Chang, S. H.; Kang, T. J. Solvent Effects on the Solvatochromism of 7-Aminocoumarin Derivatives in Neat and Binary Solvent Mixtures: Correlation of the Electronic Transition Energies with the Solvent Polarity Parameters Bull. Korean Chem. Soc. 2009, 30, 1452-1458
90. Berezin, M. Y.; Lee, H.; Akers, W.; Achilefu, S. Near Infrared Dyes as Lifetime Solvatochromic Probes for Micropolarity Measurements of Biological Systems Biophys. J. 2007, 93, 2892-2899
91. Kollman, J. M.; Pandi, L.; Sawaya, M. R.; Riley, M.; Doolittle, R. F. Crystal Structure of Human Fibrinogen Biochemistry 2009, 48, 3877-3886
92. Deng, Z. J.; Liang, M.; Monteiro, M.; Toth, I.; Minchin, R. F. Nanoparticle-Induced Unfolding of Fibrinogen Promotes Mac-1 Receptor Activation and Inflammation Nat. Nanotechnol. 2011, 6, 39-44
93. Brambilla, D.; Verpillot, R.; Le Droumaguet, B.; Nicolas, J.; Taverna, M.; Kona, J.; Lettiero, B.; Hashemi, S. H.; De Kimpe, L.; Canovi, M. PEGylated Nanoparticles Bind to and Alter Amyloid-Beta Peptide Conformation: Toward Engineering of Functional Nanomedicines for Alzheimer's Disease ACS Nano 2012, 6, 5897-5908
94. Carpenter, A.; Jones, T.; Lamprecht, M.; Clarke, C.; Kang, I.; Friman, O.; Guertin, D.; Chang, J.; Lindquist, R.; Moffat, J. CellProfiler: Image Analysis Software for Identifying and Quantifying Cell Phenotypes Genome Biol. 2006, 7, R100
95. de la Fuente, J. M.; Alcantara, D.; Penades, S. Cell Response to Magnetic Glyconanoparticles: Does the Carbohydrate Matter? IEEE Trans. Nanobiosci. 2007, 6, 275-281
96. Moros, M.; Hernáez, B.; Garet, E.; Dias, J. T.; Sáez, B.; Grazú, V.; González-Fernández, á.; Alonso, C.; de la Fuente, J. M. Monosaccharides versus PEG-Functionalized NPs: Influence in the Cellular Uptake ACS Nano 2012, 6, 1565-1577
97. Harakeh, S.; Abdel-Massih, R. M.; Rivera Gil, P.; Sperling, R. A.; Meinhardt, A.; Niedwiecki, A.; Rath, M.; Parak, W. J.; Baydoun, E. The Effect of PEG-Coated Gold Nanoparticles on the Anti-proliferative Potential of Specific Nutrient Synergy Nanotoxicology 2010, 4, 177-185
98. Tenzer, S.; Docter, D.; Kuharev, J.; Musyanovych, A.; Fetz, V.; Hecht, R.; Schlenk, F.; Fischer, D.; Kiouptsi, K.; Reinhardt, C. Rapid Formation of Plasma Protein Corona Critically Affects Nanoparticle Pathophysiology Nat. Nanotechnol. 2013, 8, 772-781
99. Vroman, L.; Adams, A. L.; Fischer, G. C.; Munoz, P. C. Interaction of High Molecular Weight Kininogen, Factor XII, and Fibrinogen in Plasma at Interfaces Blood 1980, 55, 156-159
100. Zhang, G.; Yang, Z.; Lu, W.; Zhang, R.; Huang, Q.; Tian, M.; Li, L.; Liang, D.; Li, C. Influence of Anchoring Ligands and Particle Size on the Colloidal Stability and in Vivo Biodistribution of Polyethylene Glycol-Coated Gold Nanoparticles in Tumor-Xenografted Mice Biomaterials 2009, 30, 1928-1936
101. Duan, X.; Li, Y. Physicochemical Characteristics of Nanoparticles Affect Circulation, Biodistribution, Cellular Internalization, and Trafficking Small 2013, 9, 1521-1532
102. Zhou, W.; Shao, J.; Jin, Q.; Wei, Q.; Tang, J.; Ji, J. Zwitterionic Phosphorylcholine as a Better Ligand for Gold Nanorods Cell Uptake and Selective Photothermal Ablation of Cancer Cells Chem. Commun. 2010, 46, 1479-1481
103. Murthy, A. K.; Stover, R. J.; Hardin, W. G.; Schramm, R.; Nie, G. D.; Gourisankar, S.; Truskett, T. M.; Sokolov, K. V.; Johnston, K. P. Charged Gold Nanoparticles with Essentially Zero Serum Protein Adsorption in Undiluted Fetal Bovine Serum J. Am. Chem. Soc. 2013, 135, 7799-7802
104. Muro, E.; Pons, T.; Lequeux, N.; Fragola, A.; Sanson, N.; Lenkei, Z.; Dubertret, B. Small and Stable Sulfobetaine Zwitterionic Quantum Dots for Functional Live-Cell Imaging J. Am. Chem. Soc. 2010, 132, 4556-4557
105. Wang, T.; Bai, J.; Jiang, X.; Nienhaus, G. U. Cellular Uptake of Nanoparticles by Membrane Penetration: A Study Combining Confocal Microscopy with FTIR Spectroelectrochemistry ACS Nano 2012, 6, 1251-1259
106. Jiang, X.; Röcker, C.; Hafner, M.; Nienhaus, G. U. Endo- and Exocytosis of Zwitterionic Quantum Dot Nanoparticles by Living Cells ACS Nano 2010, 4, 6787-6797
107. Breus, V. V.; Heyes, C. D.; Tron, K.; Nienhaus, G. U. Zwitterionic Biocompatible Quantum Dots for Wide pH Stability and Weak Nonspecific Binding to Cells ACS Nano 2009, 3, 2573-2580
108. Fernández-Argüelles, M. T.; Yakovlev, A.; Sperling, R. A.; Luccardini, C.; Gaillard, S.; Medel, A. S.; Mallet, J.-M.; Brochon, J.-C.; Feltz, A.; Oheim, M. Synthesis and Characterization of Polymer-Coated Quantum Dots with Integrated Acceptor Dyes as FRET-Based Nanoprobes Nano Lett. 2007, 7, 2613-2617
109. Cui, M.; Liu, R.; Deng, Z.; Ge, G.; Liu, Y.; Xie, L. Quantitative Study of Protein Coronas on Gold Nanoparticles with Different Surface Modifications Nano Res. 2014, 7, 345-352
110. Schweiger, C.; Hartmann, R.; Zhang, F.; Parak, W. J.; Kissel, T.; Rivera Gil, P. Quantification of the Internalization Patterns of Superparamagnetic Iron Oxide Nanoparticles with Opposite Charge J. Nanobiotechnol. 2012, 10, 28