The Intracellular Destiny of the Protein Corona: A Study on its Cellular Internalization and Evolution

ACS Nano

Volumn 10, Issue 11, 2016, Pages 10471-10479

  Bertoli, Filippo ^a   Garry, David ^a   Monopoli, Marco P ^a,b   Salvati, Anna ^a,c   Dawson, Kenneth A ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

biomolecular corona; degradation; lysosomes; nanoparticle cell interactions

Indexed keywords

BIOLOGY; BIOMOLECULES; CELLS; CYTOLOGY; DEGRADATION; ENZYME ACTIVITY; MOLECULAR BIOLOGY; PROTEINS;

BIO-MOLECULAR; CELL INTERACTION; CELLULAR INTERNALIZATION; EXTRACELLULAR MEDIUM; FLUORESCENCE LABELING; LYSOSOMES; MEMBRANE INTERACTIONS; NANOPARTICLE SURFACE;

NANOPARTICLES;

NANOPARTICLE; PLASMA PROTEIN; PROTEIN CORONA;

CELL ORGANELLE; CHEMISTRY; LYSOSOME;

BLOOD PROTEINS; LYSOSOMES; NANOPARTICLES; ORGANELLES; PROTEIN CORONA;

EID: 84997523874     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.6b06411     Document Type: Article

References (41)

1. 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 10.1038/nnano.2012.207
2. Wan, S.; Kelly, P. M.; Mahon, E.; Stockmann, H.; Rudd, P. M.; Caruso, F.; Dawson, K. A.; Yan, Y.; Monopoli, M. P. The "Sweet" Side of the Protein Corona: Effects of Glycosilation on Nanoparticles-Cells Interactions ACS Nano 2015, 9, 2157-2166 10.1021/nn506060q
3. Wang, F.; Yu, L.; Monopoli, M. P.; Sandin, P.; Mahon, E.; Salvati, A.; Dawson, K. A. The Biomolecular Corona Is Retained During Nanoparticle Uptake and Protects the Cells From the Damage Induced by Cationic Nanoparticles Until Degraded in the Lysosomes Nanomedicine 2013, 9, 1159-1168 10.1016/j.nano.2013.04.010
4. Doorley, G. W.; Payne, C. K. Nanoparticles Acts as Protein Carriers During Cellular Internalization Chem. Commun. (Cambridge, U. K.) 2012, 48, 2961-2963 10.1039/c2cc16937a
5. Kelly, P. M.; Aberg, C.; Polo, E.; O'Connell, A.; Cookman, J.; Fallon, J.; Krpetic, Z.; Dawson, K. A. Mapping Protein Binding Sites on the Biomolecular Corona of Nanoparticles Nat. Nanotechnol. 2015, 10, 472-479 10.1038/nnano.2015.47
6. Salvati, A.; Aberg, C.; dos Santos, T.; Varela, J.; Pinto, P.; Lynch, I.; Dawson, K. A. Experimental and Theoretical Comparison of Intracellular Import of Polymeric Nanoparticles and Small Molecules: Towards Models of Uptake Kinetics Nanomedicine 2011, 7, 818-826 10.1016/j.nano.2011.03.005
7. Gratton, S. E.; Ropp, P. A.; Pohlhaus, P. D.; Luft, J. C.; Madden, V. J.; Napier, M. E.; DeSimone, J. M. The Effects of Particle Desing on Cellular Internalizaion Pathways Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 11613-11618 10.1073/pnas.0801763105
8. Jiang, W.; Kim, B. Y.; Rutka, J. T.; Chan, W. C. Nanoparticle-Mediated Cellular Response Is Size Dependant Nat. Nanotechnol. 2008, 3, 145-150 10.1038/nnano.2008.30
9. Bexiga, M. G.; Varela, J. A.; Wang, F.; Fenaroli, F.; Salvati, A.; Lynch, I.; Simpson, J. C.; Dawson, K. A. Cationic Nanoparticles Induce Caspase 3-,7- and 9-Mediated Cytotoxicity in a Human Astrocytoma Cell Line Nanotoxicology 2011, 5, 557-567 10.3109/17435390.2010.539713
10. Kim, J. A.; Aberg, C.; Salvati, A.; Dawson, K. A. Role of Cell Cycle on the Cellular Uptake and Dilution of Nanoparticles in a Cell Population Nat. Nanotechnol. 2012, 7, 62-68 10.1038/nnano.2011.191
11. Shapero, K.; Fenaroli, F.; Lynch, I.; Cottell, D. C.; Salvati, A.; Dawson, K. A. Time and Space Resolved Uptake Study of Silica Nanoparticles by Human Cells Mol. BioSyst. 2011, 7, 371-378 10.1039/C0MB00109K
12. Wang, F.; Bexiga, M. G.; Anguissola, S.; Boya, P.; Simpson, J. C.; Salvati, A.; Dawson, K. A. Time Resolved Study of Cell Death Mechanisms Induced by Amine-Modified Polystyrene Nanoparticles Nanoscale 2013, 5, 10868-10876 10.1039/c3nr03249c
13. Frohlich, E.; Meindl, C.; Roblegg, E.; Ebner, B.; Absenger, M.; Pieber, T. R. Action of Polysterene Nanoparticles of Different Sizes on lysosomal Function and Integrity Part. Fibre Toxicol. 2012, 9, 26 10.1186/1743-8977-9-26
14. Panyam, J.; Labhasetwar, V. Dynamic of Endocytosis and Exocytosis of Poly(D,L-Lactide-Co-Glycolide) Nanoparticles in Vascular Smooth Muscle Cells Pharm. Res. 2003, 20, 212-220 10.1023/A:1022219003551
15. Lu, J.; Liong, M.; Sherman, S.; Xia, T.; Kovochich, M.; Nel, A. E.; Zink, J. I.; Tamanoi, F. Mesoporus Silica Nanoparticles for Cancer Therapy: Energy-Dependent Cellular Uptake and Delivery of Paclitaxel to Cancer Cells NanoBiotechnology 2007, 3, 89-95 10.1007/s12030-008-9003-3
16. Lesniak, A.; Fenaroli, F.; Monopoli, M. P.; Aberg, C.; Dawson, K. A.; Salvati, A. Effect of the Presence or Absence of a Protein Corona on Silica Nanoparticle Uptake and Impact on Cells ACS Nano 2012, 6, 5845-5857 10.1021/nn300223w
17. Dawson, K.A. Nanomaterials: Addressing the Challenges, Benefiting from the Opportunities. 2016, Science for Environment Policy; Science Communication Unit, University of the West of England (UWE): Bristol, U.K., 2015; pp 2, 3-5, Issue 48.
18. Maiolo, D.; Del Pino, P.; Metrangolo, P.; Parak, W. J.; Baldelli Bombelli, F. Nanomedicine Delivery: Does Protein Corona Route to the Target or off Road? Nanomedicine 2015, 10, 3231-3247 10.2217/nnm.15.163
19. Milani, S.; Bombelli, F. B.; Pitek, A. S.; Dawson, K. A.; Radler, J. Reversible Versus Irreversible Binding of Transferrin to Polystyrene Nanoparticles: Soft and Hard Corona ACS Nano 2012, 6, 2532-2541 10.1021/nn204951s
20. Rocker, C.; Potzl, 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 10.1038/nnano.2009.195
21. Barran-Berdon, A. L.; Pozzi, D.; Caracciolo, G.; Capriotti, A. L.; Caruso, G.; Cavaliere, C.; Riccioli, A.; Palchetti, S.; Lagana, A. Time Evolution of Nanoparticle Protein Corona in Human Plasma: Relevance for Targeted Drug Delivery Langmuir 2013, 29, 6485-6494 10.1021/la401192x
22. Walkey, C. D.; Olsen, J. B.; Guo, H.; Emili, A.; Chan, W. C. Nanoparticles Size and Surface Chemistry Determine Serum Adsorption and Macrophage Uptake J. Am. Chem. Soc. 2012, 134, 2139-2147 10.1021/ja2084338
23. Pelaz, B.; Del Pino, P.; Maffre, P.; Hartmann, R.; Gallego, M.; Rivera-Fernandez, S.; De la Fuente, J. M.; Nienhaus, G. U.; Parak, W. J. Surface Functionalization Of Nanoparticles With Polyethylene Glycol: Effects on Protein Adsorption and Cellular Uptake ACS Nano 2015, 9, 6996-7008 10.1021/acsnano.5b01326
24. del Pino, P.; Pelaz, B.; Zhang, Q.; Maffre, P.; Nienhaus, G. U.; Parak, W. J. Protein Corona Formation Around Nanoparticles-form the Past to the Future Mater. Horiz. 2014, 1, 301-313 10.1039/C3MH00106G
25. Schöttler, S.; Becker, G.; Winzen, S.; Steinbach, T.; Mohr, K.; Landfester, K.; Mailänder, V.; Wurm, F. R. Protein Adsorption is Required for Stealth Effect of Poly(Ethylene Glycol)- and Poly(Phosphoester)-Coated Nanocarriers Nat. Nanotechnol. 2016, 11, 372-377 10.1038/nnano.2015.330
26. Walkey, C. D.; Olsen, J. B.; Song, F.; Liu, R.; Guo, H.; Olsen, D. W.; Cohen, Y.; Emili, A.; Chan, W. C. Protein Corona Fingerprinting Predicts the Cellular Interactions of Gold and Silver Nanoparticles ACS Nano 2014, 8, 2439-2455 10.1021/nn406018q
27. Husebye, H.; Halaas, Ø Stenmark, H.; Tunheim, G.; Sandanger, Ø.; Bogen, B.; Brech, A.; Latz, E.; Espevik, T. Endocytic Pathways Regulate Toll-Like Receptor 4 Signaling and Link Innate and Adaptive Immunity EMBO J. 2006, 25, 683-692 10.1038/sj.emboj.7600991
28. Kawai, T.; Akira, S. The Role of Pattern-Recognition Receptors in Innate Immunity: Update on Toll-Like Receptors Nat. Immunol. 2010, 11, 373-384 10.1038/ni.1863
29. Butcher, N. J.; Mortimer, G. M.; Minchin, R. F. Drug Delivery: Unrevelling the Stealth Effect Nat. Nanotechnol. 2016, 11, 310-311 10.1038/nnano.2016.6
30. 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 10.1038/nnano.2010.250
31. 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 10.1021/nn202458g
32. Walkey, C. D.; Chan, W. C. W. Understanding and Controlling the Interactions of Nanomaterials With Proteins in a Physiological Environment Chem. Soc. Rev. 2012, 41, 2780-2799 10.1039/C1CS15233E
33. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T.; Dawson, K. A. Nanoparticles 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 10.1073/pnas.0805135105
34. Tenzer, S.; Docter, D.; Kuharev, J.; Musyanovych, A.; Fetz, V.; Hecht, R.; Schlenk, F.; Fischer, D.; Kiouptsi, K.; Reinhardt, C.; Landfester, K.; Schild, H.; Maskos, M.; Knauer, S. K.; Stauber, R. H. Rapid Formation of Plasma Protein Corona Critically Affects Nanoparticle Pathophysiology Nat. Nanotechnol. 2013, 8, 772-781 10.1038/nnano.2013.181
35. 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 10.1021/ja107583h
36. 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 10.1021/ja037263o
37. Bonifacino, J. S.; Rojas, R. Retrograde Transport from Endosomes to the Trans-Golgi Network Nat. Rev. Mol. Cell Biol. 2006, 7, 568-579 10.1038/nrm1985
38. Maxfield, F. R.; McGraw, T. E. Endocytic Recycling Nat. Rev. Mol. Cell Biol. 2004, 5, 121-132 10.1038/nrm1315
39. Meder, F.; Daberkow, T.; Treccani, L.; Wilhelm, M.; Schowalter, M.; Rosenauer, A.; Madler, L.; Rezwan, K. Protein Adsorption on Colloidal Aluminia Particles Functionalized with Amino, Carboxyl, Sulfonate and Phosphate Groups Acta Biomater. 2012, 8, 1221-1229 10.1016/j.actbio.2011.09.014
40. Fleischer, C. C.; Payne, C. K. Nanoparticle-Cell Interactions: Molecular Structure of the Protein Corona and Cellular Outcomes Acc. Chem. Res. 2014, 47, 2651-2659 10.1021/ar500190q
41. Yildirimer, L.; Thanh, N. T. K.; Loizidou, M.; Seifalian, A. M. Toxicology and Clinical Potential of Nanoparticles Nano Today 2011, 6, 585-607 10.1016/j.nantod.2011.10.001