Cited by 258

The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.

Secreted Biomolecules Alter the Biological Identity and Cellular Interactions of Nanoparticles

Albanese, Alexandre, Walkey, Carl D., Olsen, Jonathan B., Guo, Hongbo, Emili, Andrew, Chan, Warren C. W.·2014·ACS Nano

Abstract

A nanoparticle’s physical and chemical properties at the time of cell contact will determine the ensuing cellular response. Aggregation and the formation of a protein corona in the extracellular environment will alter nanoparticle size, shape, and surface properties, giving it a “biological identity” that is distinct from its initial “synthetic identity”. The biological identity of a nanoparticle depends on the composition of the surrounding biological environment and determines subsequent cellular interactions. When studying nanoparticle–cell interactions, previous studies have ignored the dynamic composition of the extracellular environment as cells deplete and secrete biomolecules in a process known as “conditioning”. Here, we show that cell conditioning induces gold nanoparticle aggregation and changes the protein corona composition in a manner that depends on nanoparticle diameter, surface chemistry, and cell phenotype. The evolution of the biological identity in conditioned media enhances the cell membrane affinity, uptake, and retention of nanoparticles. These results show that dynamic extracellular environments can alter nanoparticle–cell interactions by modulating the biological identity. The effect of the dynamic nature of biological environments on the biological identity of nanoparticles must be considered to fully understand nano–bio interactions and prevent data misinterpretation.

Overview

Integrity signals

Registry

Crossref · 10.1021/nn4061012

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Research works printed but not linked: 45

  1. Stark, 2011, Nanoparticles in Biological Systems, Angew. Chem., Int. Ed., 50, 1242, 10.1002/anie.200906684 · DOI
  2. Nel, 2009, Understanding Biophysicochemical Interactions at the Nano–Bio Interface, Nat. Mater., 8, 543, 10.1038/nmat2442 · DOI · Paper page
  3. Monopoli, 2012, Biomolecular Coronas Provide the Biological Identity of Nanosized Materials, Nat. Nanotechnol., 7, 779, 10.1038/nnano.2012.207 · DOI · Paper page
  4. Tenzer, 2013, Rapid Formation of Plasma Protein Corona Critically Affects Nanoparticle Pathophysiology, Nat. Nanotechnol., 8, 772, 10.1038/nnano.2013.181 · DOI · Paper page
  5. Tenzer, 2011, Nanoparticle Size Is a Critical Physicochemical Determinant of the Human Blood Plasma Corona: A Comprehensive Quantitative Proteomic Analysis, ACS Nano, 5, 7155, 10.1021/nn201950e · DOI
  6. Walkey, 2014, Protein Corona Fingerprinting Predicts the Cellular Interaction of Gold and Silver Nanoparticles, ACS Nano, 8, 2439, 10.1021/nn406018q · DOI
  7. Lundqvist, 2008, Nanoparticle Size and Surface Properties Determine the Protein Corona with Possible Implications for Biological Impacts, Proc. Natl. Acad. Sci. U. S. A., 105, 14265, 10.1073/pnas.0805135105 · DOI · Paper page
  8. Cedervall, 2007, Understanding the Nanoparticle–Protein Corona Using Methods to Quantify Exchange Rates and Affinities of Proteins for Nanoparticles, Proc. Natl. Acad. Sci. U. S. A., 104, 2050, 10.1073/pnas.0608582104 · DOI · Paper page
  9. Lynch, 2007, The Nanoparticle-Protein Complex as a Biological Entity; A Complex Fluids and Surface Science Challenge for the 21st Century, Adv. Colloid Interface Sci., 134–35, 167, 10.1016/j.cis.2007.04.021 · DOI
  10. Qiu, 2010, Surface Chemistry and Aspect Ratio Mediated Cellular Uptake of Au Nanorods, Biomaterials, 31, 7606, 10.1016/j.biomaterials.2010.06.051 · DOI
  11. Lacerda, 2009, Interaction of Gold Nanoparticles with Common Human Blood Proteins, ACS Nano, 4, 365, 10.1021/nn9011187 · DOI
  12. Rausch, 2010, Evaluation of Nanoparticle Aggregation in Human Blood Serum, Biomacromolecules, 11, 2836, 10.1021/bm100971q · DOI
  13. Maiorano, 2011, Effects of Cell Culture Media on the Dynamic Formation of Protein-Nanoparticle Complexes and Influence on the Cellular Response, ACS Nano, 4, 7481, 10.1021/nn101557e · DOI · Paper page
  14. Kim, 2005, Interaction of PLGA Nanoparticles with Human Blood Constituents, Colloids Surf., B, 40, 83, 10.1016/j.colsurfb.2004.05.007 · DOI
  15. Albanese, 2011, Effect of Gold Nanoparticle Aggregation on Cell Uptake and Toxicity, ACS Nano, 5, 5478, 10.1021/nn2007496 · DOI
  16. Yuan, 2010, Variable Nanoparticle-Cell Adhesion Strength Regulates Cellular Uptake, Phys. Rev. Lett., 105, 1381011, 10.1103/PhysRevLett.105.138101 · DOI
  17. Gao, 2005, Mechanics of Receptor-Mediated Endocytosis, Proc. Natl. Acad. Sci. U. S. A., 102, 9469, 10.1073/pnas.0503879102 · DOI
  18. Dasgupta, 2014, Shape and Orientation Matter for the Cellular Uptake of Nonspherical Particles, Nano Lett., 14, 687, 10.1021/nl403949h · DOI
  19. Lundqvist, 2011, The Evolution of the Protein Corona around Nanoparticles: A Test Study, ACS Nano, 5, 7503, 10.1021/nn202458g · DOI · Paper page
  20. Kulasingam, 2007, Proteomics Analysis of Conditioned Media from Three Breast Cancer Cell Lines: A Mine for Biomarkers and Therapeutic Targets, Mol. Cell Proteomics, 6, 1997, 10.1074/mcp.M600465-MCP200 · DOI
  21. Skalnikova, 2011, Mapping of the Secretome of Primary Isolates of Mammalian Cells, Stem Cells and Derived Cell Lines, Proteomics, 11, 691, 10.1002/pmic.201000402 · DOI
  22. Chithrani, 2006, Determining the Size and Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells, Nano Lett., 6, 662, 10.1021/nl052396o · DOI
  23. Chithrani, 2007, Elucidating the Mechanism of Cellular Uptake and Removal of Protein-Coated Gold Nanoparticles of Different Sizes and Shapes, Nano Lett., 7, 1542, 10.1021/nl070363y · DOI
  24. Clift, 2008, The Impact of Different Nanoparticle Surface Chemistry and Size on Uptake and Toxicity in a Murine Macrophage Cell Line, Toxicol. Appl. Pharmacol., 232, 418, 10.1016/j.taap.2008.06.009 · DOI
  25. Pan, 2007, Size-Dependent Cytotoxicity of Gold Nanoparticles, Small, 3, 1941, 10.1002/smll.200700378 · DOI
  26. Hauck, 2008, Assessing the Effect of Surface Chemistry on Gold Nanorod Uptake, Toxicity, and Gene Expression in Mammalian Cells, Small, 4, 153, 10.1002/smll.200700217 · DOI
  27. Perrault, 2009, Synthesis and Surface Modification of Highly Monodispersed, Spherical Gold Nanoparticles of 50–200 nm, J. Am. Chem. Soc., 131, 17042, 10.1021/ja907069u · DOI
  28. Lin, 2004, Two-Step Functionalization of Neutral and Positively Charged Thiols onto Citrate-Stabilized Au Nanoparticles, J. Phys. Chem. B, 108, 2134, 10.1021/jp036310w · DOI
  29. Guan, 2009, Cooperative Dual-Stimuli-Triggered Aggregation of Poly-L-Histidine-Functionalized Au Nanoparticles, Langmuir, 25, 2679, 10.1021/la803414c · DOI
  30. Roach, 2006, Surface Tailoring for Controlled Protein Adsorption: Effect of Topography at the Nanometer Scale and Chemistry, J. Am. Chem. Soc., 128, 3939, 10.1021/ja056278e · DOI
  31. Schaefer, 2010, Agglomeration and Filtration of Colloidal Suspensions with DVLO Interactions in Simulation and Experiment, J. Colloid Interface Sci., 349, 186, 10.1016/j.jcis.2010.05.025 · DOI
  32. Lesniak, 2010, Serum Heat Inactivation Affects Protein Corona Composition and Nanoparticle Uptake, Biomaterials, 31, 9511, 10.1016/j.biomaterials.2010.09.049 · DOI · Paper page
  33. Lesniak, 2012, Effects of the Presence or Absence of a Protein Corona on Silica Nanoparticle Uptake and Impact on Cells, ACS Nano, 6, 5845, 10.1021/nn300223w · DOI · Paper page
  34. Kneipp, 2005, Optical Probes for Biological Applications Based on Surface-Enhanced Raman Scattering from Indocyanine Green on Gold Nanoparticles, Anal. Chem., 77, 2381, 10.1021/ac050109v · DOI
  35. Levy, 2010, Gold Nanoparticles Delivery in Mammalian Live Cells: a Critical Review, Nano Rev., 1, 1, 10.3402/nano.v1i0.4889 · DOI
  36. Xu, 2012, A Physical Model for the Size-Dependent Cellular Uptake of Nanoparticles Modified with Cationic Surfactants, Int. J. Nanomedicine, 7, 3547
  37. Oh, 2010, Cellular Uptake, Cytotoxicity, and Innate Immune Response of Silica-Titania Hollow Nanoparticles Based on Size and Surface Functionality, ACS Nano, 4, 5301, 10.1021/nn100561e · DOI
  38. Jiang, 2008, Nanoparticle-Mediated Cellular Response is Size-Dependent, Nat. Nanotechnol., 3, 145, 10.1038/nnano.2008.30 · DOI
  39. Touitou, 1986, Differences Between Young and Elderly Subjects in Seasonal and Circadian Variations of Total Plasma Proteins and Blood Volume as Reflected by Hemoglobin, Hematocrit, and Erythrocyte Counts, Clin. Chem., 32, 801, 10.1093/clinchem/32.5.801 · DOI
  40. Shub, 1983, Age-Related Changes in Chemical Composition and Physical Properties of Mucus Glycoproteins from Rat Small intestine, Biochem. J., 215, 405, 10.1042/bj2150405 · DOI
  41. Dawes, 1972, Circadian Rhythms in Human Salivary Flow Rate and Composition, J. Physiol., 220, 529, 10.1113/jphysiol.1972.sp009721 · DOI
  42. Bates, 1993, Change in Macro Molecular Composition of Interstitial Fluid from Swollen Arms after Breast Cancer Treatment, and Its Implications, Clin. Sci., 85, 737, 10.1042/cs0850737 · DOI
  43. Perrault, 2009, Mediating Tumor Targeting Efficiency of Nanoparticles Through Design, Nano Lett., 9, 1909, 10.1021/nl900031y · DOI
  44. Frens, 1973, Controlled Nucleation for Regulation of Particle-Size in Monodisperse Gold Suspensions, Nature (London), Phys. Sci., 241, 20, 10.1038/physci241020a0 · DOI
  45. Albanese, 2012, Simultaneous Quantification of Cells and Nanomaterials by Inductive-Coupled Plasma Techniques, J. Lab. Autom., 18, 99, 10.1177/2211068212457039 · DOI

Cited by

Sorted by citations

See all 258

Metadata

Authors
Albanese, A., Walkey, C. D., Olsen, J. B., Guo, H., Emili, A., & Chan, W. C. W.
Venue
ACS Nano
Published
2014-05-05
Volume
8
Issue
6
Pages
5515-5526
ISSN
  • 1936-0851
  • 1936-086X
Cited by
258
References
5
Language
en
Funders
Natural Sciences and Engineering Research Council of Canada (288231, NETGP35015)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review