Modulation of Silica Nanoparticle Uptake into Human Osteoblast Cells by Variation of the Ratio of Amino and Sulfonate Surface Groups: Effects of Serum

ACS Applied Materials and Interfaces

Volumn 7, Issue 25, 2015, Pages 13821-13833

  Shahabi, Shakiba ^a   Treccani, Laura ^a   Dringen, Ralf ^a   Rezwan, Kurosch ^a  

^a UNIVERSITY OF BREMEN   (Germany)

Author keywords

cellular uptake; functionalization; osteoblast; protein corona; silica nanoparticle; surface charge

Indexed keywords

MOBILE SECURITY; NANOPARTICLES; OSTEOBLASTS; PROTEINS; SILICA; SURFACE CHARGE; SYNTHESIS (CHEMICAL); ZETA POTENTIAL;

CELLULAR UPTAKE; FUNCTIONALIZATIONS; FUNCTIONALIZED SILICA; HUMAN OSTEOBLAST CELLS; PHYSICOCHEMICAL PROPERTY; PHYSIOLOGICAL CONDITION; PROTEIN CORONAS; SILICA NANOPARTICLES;

BODY FLUIDS;

FLUORESCENT DYE; NANOPARTICLE; SILICON DIOXIDE; SULFONIC ACID DERIVATIVE;

CELL CULTURE; CHEMISTRY; HUMAN; METABOLISM; OSTEOBLAST; SURFACE PROPERTY; TEMPERATURE;

CELLS, CULTURED; FLUORESCENT DYES; HUMANS; NANOPARTICLES; OSTEOBLASTS; SILICON DIOXIDE; SULFONIC ACIDS; SURFACE PROPERTIES; TEMPERATURE;

EID: 84934779600     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b01900     Document Type: Article

References (70)

1. Hornig, S.; Biskup, C.; Gräfe, A.; Wotschadlo, J.; Liebert, T.; Mohr, G.; Heinze, T. Biocompatible Fluorescent Nanoparticles for pH-Sensoring Soft Matter 2008, 4, 1169-1172
2. Latterini, L.; Amelia, M. Sensing Proteins with Luminescent Silica Nanoparticles Langmuir 2009, 25, 4767-4773
3. Liong, M.; Lu, J.; Kovochich, M.; Xia, T.; Ruehm, S.; Nel, A.; Tamanoi, F.; Zink, J. Multifunctional Inorganic Nanoparticles for Imaging, Targeting, and Drug Delivery ACS Nano 2008, 2, 889-896
4. Kumar, R.; Roy, I.; Ohulchanskyy, T.; Goswami, L.; Bonoiu, A.; Bergey, E.; Tramposch, K.; Maitra, A.; Prasad, P. Covalently Dye-Linked, Surface-Controlled, and Bioconjugated Organically Modified Silica Nanoparticles as Targeted Probes for Optical Imaging ACS Nano 2008, 2, 449-456
5. Rosenholm, J.; Sahlgren, C.; Lindén, M. Towards Multifunctional, Targeted Drug Delivery Systems Using Mesoporous Silica Nanoparticles-Opportunities & Challenges Nanoscale 2010, 2, 1870-1883
6. Febvay, S.; Marini, D.; Belcher, A.; Clapham, D. Targeted Cytosolic Delivery of Cell-Impermeable Compounds by Nanoparticle-Mediated, Light-Triggered Endosome Disruption Nano Lett. 2010, 10, 2211-2219
7. Fuller, J.; Zugates, G.; Ferreira, L.; Ow, H.; Nguyen, N.; Wiesner, U.; Langer, R. Intracellular Delivery of Coreeshell Fluorescent Silica Nanoparticles Biomaterials 2008, 29, 1526-1532
8. Xia, T.; Kovochich, M.; Liong, M.; Meng, H.; Kabehie, S.; George, S.; Zink, J.; Nel, A. Polyethyleneimine Coating Enhances the Cellular Uptake of Mesoporous Silica Nanoparticles and Allows Safe Delivery of siRNA and DNA Constructs ACS Nano 2009, 3, 3273-3286
9. Jia, T.-t.; Cai, Z.-m.; Chen, X.-m.; Lin, Z.-j.; Huang, X.-l.; Chen, X.; Chen, G.-n. Electrogenerated Chemiluminescence Ethanol Biosensor Based on Alcohol Dehydrogenase Functionalized Ru(bpy)32+ Dodoped Silica Nanoparticles Biosens. Bioelectron. 2009, 25, 263-267
10. Gao, X.; He, J.; Deng, L.; Cao, H. Synthesis and Characterization of Functionalized Rhodamine B-Doped Silica Nanoparticles Opt. Mater. 2009, 31, 1715-1719
11. Peng, J.; He, X.; Wang, K.; Tan, W.; Wang, Y.; Y, L. Noninvasive Monitoring of Intracellular pH Change Induced by Drug Stimulation Using Silica Nanoparticle Sensors Anal. Bioanal. Chem. 2007, 388, 645-654
12. Kumar, R.; Roy, I.; Ohulchanskky, T.; Vathy, L.; Bergey, E.; Sajjad, M.; Prasad, P. In Vivo Biodistribution and Clearance Studies Using Multimodal Organically Modified Silica Nanoparticles ACS Nano 2010, 4, 699-708
13. Labéguerie-Egeá, J.; McEvoy, H.; McDonagh, C. Synthesis, Characterisation and Functionalisation of Luminescent Silica Nanoparticles J. Nanopart. Res. 2011, 13, 6455-6465
14. Santra, S.; Zhang, P.; Wang, K.; Tapec, R.; Tan, W. Conjugation of Biomolecules with Luminophore-Doped Silica Nanoparticles for Photostable Biomarkers Anal. Chem. 2001, 73, 4988-4993
15. Lee, J.; Jun, Y.; Yeon, S.; Shin, J.; Cheon, J. Dual-Mode Nanoparticle Probes for High-Performance Magnetic Resonance and Fluorescence Imaging of Neuroblastoma Angew. Chem. 2006, 118, 8340-8342
16. Salvati, A.; Pitek, A.; Monopoli, M.; Prapainop, K.; Bombelli, F.; Hristov, D.; Kelly, P.; Åberg, C.; Mahon, E.; Dawson, K. Transferrin-Functionalized Nanoparticles Lose Their Targeting Capabilities When a Biomolecule Corona Adsorbs on the Surface Nat. Nanotechnol. 2013, 8, 137-143
17. Mahon, E.; Salvati, A.; Bombelli, F.; Lynch, I.; Dawson, K. Designing the Nanoparticle-Biomolecule Interface for "Targeting and Therapeutic Delivery" J. Controlled Release 2012, 161, 164-174
18. Mahmoudi, M.; Lynch, I.; Ejtehadi, M.; Monopoli, M.; Bombelli, F.; Laurent, S. Protein Nanoparticle Interactions: Opportunities and Challenges Chem. Rev. 2011, 111, 5610-5637
19. Nel, A.; Mädler, L.; Velegol, D.; Xia, T.; Hoek, E.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557
20. Monopoli, M.; Åberg, C.; Salvati, A.; Dawson, K. Biomolecular Coronas Provide the Biological Identity of Nanosized Materials Nat. Nanotechnol. 2012, 7, 779-786
21. Fleischer, C.; Payne, C. Nanoparticle Surface Charge Mediates the Cellular Receptors Used by Protein-Nanoparticle Complexes J. Phys. Chem. B 2012, 116, 8901-8907
22. Casals, E.; Pfaller, T.; Duschl, A.; Oostingh, G. J.; Puntes, V. Time Evolution of the Nanoparticle Protein Corona ACS Nano 2010, 4, 3623-3632
23. Fleischer, C.; Payne, C. Nanoparticle-Cell Interactions: Molecular Structure of the Protein Corona and Cellular Outcomes Acc. Chem. Res. 2014, 47, 2651-2659
24. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T.; Dawson, K. 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
25. Kettiger, H.; Schipanski, A.; Wick, P.; Huwyler, J. Engineered Nanomaterial Uptake and Tissue Distribution: from Cell to Organism Int. J. Nanomed. 2013, 8, 3255-3269
26. Aggarwal, P.; Hall, J.; McLeland, C.; Dobrovolskaia, M.; McNeil, S. Nanoparticle Interaction with Plasma Proteins as It Relates to Particle Biodistribution, Biocompatibility and Therapeutic Efficacy Adv. Drug Delivery Rev. 2009, 61, 428-437
27. Baier, G.; Costa, C.; Zeller, A.; Baumann, D.; Sayer, C.; Araujo, P.; Mailänder, V.; Musyanovych, A.; Landfester, K. BSA Adsorption on Differently Charged Polystyrene Nanoparticles Using Isothermal Titration Calorimetry and the Influence on Cellular Uptake Macromol. Biosci. 2011, 11, 628-638
28. Kim, B.; Han, G.; Toley, B.; Kim, C.; Rotello, V.; Forbes, N. Tuning Payload Delivery in Tumour Cylindroids Using Gold Nanoparticles Nat. Nanotechnol. 2010, 5, 465-472
29. Harris, T.; Green, J.; Fung, P.; Langer, R.; Anderson, D.; Bhatia, S. Tissue-Specific Gene Delivery via Nanoparticle Coating Biomaterials 2010, 31, 998-1006
30. Schaeublin, N.; Braydich-Stolle, L.; Schrand, A.; Miller, J.; Hutchison, J.; Schlager, J.; Hussain, S. Surface Charge of Gold Nanoparticles Mediates Mechanism of Toxicity Nanoscale 2011, 3, 410-420
31. Asati, A.; Santra, S.; Kaittanis, C.; Perez, J. Surface-Charge-Dependent Cell Localization and Cytotoxicity of Cerium Oxide Nanoparticles ACS Nano 2010, 4, 5321-5331
32. Bagwe, R.; Yang, C.; Hilliard, L.; Tan, W. Optimization of Dye-Doped Silica Nanoparticles Prepared Using a Reverse Microemulsion Method Langmuir 2004, 20, 8336-8342
33. Brunauer, S.; Emmett, P.; Teller, E. Adsorption of Gases in Multimolecular Layers J. Am. Chem. Soc. 1938, 60, 309-319
34. Holthaus, M.; Stolle, J.; Treccani, L.; Rezwan, K. Orientation of Human Osteoblasts on Hydroxyapatite-Based Microchannels Acta Biomater. 2012, 8, 394-403
35. Patil, S.; Sandberg, A.; Heckert, E.; Self, W.; Seal, S. Protein Adsorption and Cellular Uptake of Cerium Oxide Nanoparticles as a Function of Zeta Potential Biomaterials 2007, 28, 4600-4607
36. Yan, Y.; Gause, K.; Kamphuis, M.; Ang, C.; O'Brien-Simpson, N.; Lenzo, J.; Reynolds, E.; Nice, E.; Caruso, F. Differential Roles of the Protein Coronain the Cellular Uptake of Nanoporous Polymer Particles by Monocyte and Macrophage Cell Lines ACS Nano 2013, 7, 10960-10970
37. Fleischer, C.; Kumar, U.; Payne, C. Cellular Binding of Anionic Nanoparticles Is Inhibited by Serum Proteins Independent of Nanoparticle Composition Biomater. Sci. 2013, 1, 975-982
38. Khalil, I.; Kogure, K.; Akita, H.; Harashima, H. Uptake Pathways and Subsequent Intracellular Trafficking in Nonviral Gene Delivery Pharmacol. Rev. 2006, 58, 32-45
39. Nooney, R.; McCahey, C.; Stranik, O.; Guevel, X.; McDonagh, C.; MacCraith, B. Experimental and Theoretical Studies of the Optimisation of Fluorescence from Near-Infrared Dye-Doped Silica Nanoparticles Anal. Bioanal. Chem. 2009, 393, 1143-1149
40. Guarnieri, D.; Malvindi, M.; Belli, V.; Pompa, P.; Netti, P. Effect of Silica Nanoparticles with Variable Size and Surface Functionalization on Human Endothelial Cell Viability and Angiogenic Activity J. Nanopart. Res. 2014, 16, 1-14
41. Lindman, S.; Lynch, I.; Thulin, E.; Nilsson, H.; Dawson, K.; Linse, S. Systematic Investigation of the Thermodynamics of HSA Adsorption to N-iso-Propylacrylamide/N-tert-Butylacrylamide Copolymer Nanoparticles. Effects of Particle Size and Hydrophobicity Nano Lett. 2007, 7, 914-920
42. Izak-Nau, E.; Voetz, M.; Eiden, S.; Duschl, A.; Puntes, V. F. Altered Characteristics of Silica Nanoparticles in Bovine and Human Serum: The Importance of Nanomaterial Characterization Prior to Its Toxicological Evaluation Part. Fibre Toxicol. 2013, 10, 1-12
43. Horie, M.; Kato, H.; Iwahashi, H. Cellular Effects of Manufactured Nanoparticles: Effect of Adsorption Ability of Nanoparticles Arch. Toxicol. 2013, 87, 771-781
44. Rezwan, K.; Meier, L.; Gauckler, L. Lysozyme and Bovine Serum Albumin Adsorption on Uncoated Silica and AlOOH-Coated Silica Particles: The Influence of Positively and Negatively Charged Oxide Surface Coatings Biomaterials 2005, 26, 4351-4357
45. Chun, K.-Y.; Stroeve, P. Protein Transport in Nanoporous Membranes Modified with Self-Assembled Monolayers of Functionalized Thiols Langmuir 2002, 18, 4653-4658
46. Robertson, B.; Zyndey, A. Protein Adsorption in Asymmetric Ultrafiltration Membranes with Highly Constricted Pores J. Colloid Interface Sci. 1990, 134, 563-575
47. Jiang, J.; Oberdörster, G.; Biswas, P. Characterization of Size, Surface Charge, and Agglomeration State of Nanoparticle Dispersions for Toxicological Studies Nanopart. Res. 2009, 11, 77-89
48. Mahl, D.; Greulich, C.; Meyer-Zaika, W.; Köller, M.; Epple, M. Gold Nanoparticles: Dispersibility in Biological Media and Cell-Biological Effect J. Mater. Chem. 2010, 20, 6176-6181
49. Graf, C.; Gao, Q.; Schütz, I.; Noufele, C.; Ruan, W.; Posselt, U.; Korotianskiy, E.; Nordmeyer, D.; Rancan, F.; Hadam, S.; Vogt, A.; Lademann, J.; Haucke, V.; Rühl, E. Surface Functionalization of Silica Nanoparticles Supports Colloidal Stability in Physiological Media and Facilitates Internalization in Cells Langmuir 2012, 28, 7598-7613
50. Keselowsky, B.; Collard, D.; García, A. Surface Chemistry Modulates Fibronectin Conformation and Directs Integrin Binding and Specificity to Control Cell Adhesion J. Biomed. Mater. Res., Part A 2003, 66A, 247-259
51. Gebauer, J.; Malissek, M.; Simon, S.; Knauer, S.; Maskos, M.; Stauber, R.; Peukert, W.; Treuel, L. Impact of the Nanoparticle-Protein Corona on Colloidal Stability and Protein Structure Langmuir 2012, 28, 9673-9679
52. Díaz, B.; Sánchez-Espinel, C.; Arruebo, M.; Faro, J.; de Miguel, E.; Magadán, S.; Yagüe, C.; Fernández-Pacheco, R.; Ibarra, M.; Santamaría, J.; González-Fernández, A. Assessing Methods for Blood Cell Cytotoxic Responses to Inorganic Nanoparticles and Nanoparticle Aggregates Small 2008, 4, 2025-2034
53. Al-Rawi, M.; Diabaté, S.; Weiss, C. Uptake and Intracellular Localization of Submicron and Nano-Sized SiO2 Particles in HeLa Cells Arch. Toxicol. 2011, 85, 813-826
54. Kittler, K.; Greulich, C.; Gebauer, J.; Diendorf, J.; Treuel, L.; Ruiz, L.; Gonzalez-Calbet, J.; Vallet-Regi, M.; Zellner, R.; Köller, M.; Epple, M. The Influence of Proteins on the Dispersability and Cell-Biological Activity of Silver Nanoparticles J. Mater. Chem. 2010, 20, 512-518
55. Panas, A.; Marquardt, C.; Nalcaci, O.; Bockhorn, H.; Baumann, W.; Paur, H.-R.; Mülhopt, S.; Diabaté, S.; Weiss, C. Screening of Different Metal Oxide Nanoparticles Reveals Selective Toxicity and Inflammatory Potential of Silica Nanoparticles in Lung Epithelial Cells and Macrophages Nanotoxicology 2012, 1-15
56. Rancan, F.; Gao, Q.; Graf, C.; Troppens, S.; Hadam, S.; Hackbarth, S.; Kembuan, C.; Blume-Peytavi, U.; Rühl, E.; Lademann, J.; Vogt, A. Skin Penetration and Cellular Uptake of Amorphous Silica Nanoparticles with Variable Size, Surface Functionalization, and Colloidal Stability ACS Nano 2012, 6, 6829-6842
57. Lesniak, A.; Fenaroli, F.; Monopoli, M.; Åberg, C.; Dawson, K.; 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
58. Kim, J.; Salvati, A.; Åberg, C.; Dawson, K. A. Suppression of Nanoparticle Cytotoxicity Approaching in Vivo Serum Concentrations: Limitations of in Vitro Testing for Nanosafety Nanoscale 2014, 6, 14180-14184
59. Wilhelm, C.; Billotey, C.; Roger, J.; Pons, J.; Bacri, J.; Gazeau, F. Intracellular Uptake of Anionic Superparamagnetic Nanoparticles as a Function of their Surface Coating Biomaterials 2003, 24, 1001-1011
60. Lorenz, M.; Holzapfel, V.; Musyanovych, A.; Nothelfer, K.; Walther, P.; Frank, H.; Landfester, K.; Schrezenmeier, H.; Mailänder, V. Uptake of Functionalized, Fluorescent-Labeled Polymeric Particles in Different Cell Lines and Stem Cells Biomaterials 2006, 27, 2820-2828
61. Mahmoudi, M.; Meng, J.; Xue, X.; Liang, C.; Rahmand, M.; Pfeiffer, C.; Hartmann, R.; Gil, P.; Pelaz, B.; Parak, W.; del Pino, P.; Carregal-Romero, S.; Kanaras, A.; Selvan, S. Interaction of Stable Colloidal Nanoparticles with Cellular Membranes Biotechnol. Adv. 2014, 1-14
62. Verma, A.; Stellacci, F. Effect of Surface Properties on Nanoparticle-Cell Interactions Small 2010, 6, 12-21
63. 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.; Stauber, R. Rapid Formation of Plasma Protein Corona Critically Affects Nanoparticle Pathophysiology Nat. Nanotechnol. 2013, 8, 772-781
64. Fröhlich, E. The Role of Surface Charge in Cellular Uptake and Cytotoxicity of Medical Nanoparticles Int. J. Nanomed. 2012, 7, 5577-5591
65. Ryman-Rasmussen, J.; Riviere, J.; Monteiro-Riviere, N. Variables Influencing Interactions of Untargeted Quantum Dot Nanoparticles with Skin Cells and Identification of Biochemical Modulators Nano Lett. 2007, 7, 1344-1348
66. Albanese, A.; Tang, P.; Chan, W. The Eeffect of Nanoparticle Size, Shape, and Surface Chemistry on Biological Systems Annu. Rev. Biomed. Eng. 2012, 14, 1-16
67. Lu, J.; Liong, M.; Sherman, S.; Xia, T.; Kovochich, M.; Nel, A.; Zink, J.; Tamanoi, F. Mesoporous Silica Nanoparticles for Cancer Therapy: Energy-Dependent Cellular Uptake and Delivery of Paclitaxel to Cancer Cells Nanobiotechnology 2007, 3, 89-95
68. Dausend, J.; Musyanovych, A.; Dass, M.; Walther, P.; Schrezenmeier, H.; Landfester, K.; Mailänder, V. Uptake Mechanism of Oppositely Charged Fluorescent Nanoparticles in HeLa Cells Macromol. Biosci. 2008, 8, 1135-1143
69. Huang, D.; Hung, Y.; Ko, B.; Hsu, S.; Chen, W.; Chien, C.; Tsai, C.; Kuo, C.; Kang, J.; Yang, C.; Mou, C.; Chen, Y. Highly Efficient Cellular Labeling of Mesoporous Nanoparticles in Human Mesenchymal Stem Cells: Implication for Stem Cell Tracking FASEB J. 2005, 19, 2014-2016
70. Chung, T.; Wu, S.; Yao, M.; Lu, C.; Lin, Y.; Hung, Y.; Mou, C.; Chen, Y.; Huang, D. The Effect of Surface Charge on the Uptake and Biological Function of Mesoporous Silica Nanoparticles in 3T3-L1 Cells and Human Mesenchymal Stem Cells Biomaterials 2007, 28, 2959-2966