Biocorona‐induced modifications in engineered nanomaterial–cellular interactions impacting biomedical applications

Focus Article

Jonathan Shannahan, Lisa Kobos

Published Online: Dec 01 2019

DOI: 10.1002/wnan.1608

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

Abstract When nanoparticles (NPs) enter a physiological environment, a complex coating of biomolecules is absorbed onto their surface, known as the biocorona (BC). This coating alters nanomaterial physical properties, modulating cellular viability, internalization, and immune responses. To safely utilize NPs within medical settings, it is necessary to understand the influence of the BC on cellular responses. Due to the variety of cell types, NPs, and physiological environments, responses are variable; though trends do exist. This review article critically evaluates the currently available literature regarding the influence of the BC on NP interactions with prominent cell types that they are likely to encounter during biomedical applications. Specifically, we will examine responses related to interactions with endothelial cells, macrophages, and epithelial cells of the digestive tract and lung. Further, we will evaluate how the BC may influence interactions with bacteria and fungi, as NPs have been proposed as antimicrobial agents in medical settings. The information reviewed and discussed here may enhance the development of effective of NP‐based therapeutics and diagnostic tools. This article is categorized under: Therapeutic Approaches and Drug Discovery > Emerging Technologies Toxicology and Regulatory Issues in Nanomedicine > Toxicology of Nanomaterials Diagnostic Tools > Diagnostic Nanodevices

NPs are proposed for a number of biomedical applications which will result in their introduction into the body via intravenous injection, inhalation, or ingestion. This results in interactions with specific cell populations including endothelial cells, macrophages, gastrointestinal epithelial cells, or alveolar epithelial cells. NP, nanoparticle

[ Normal View | Magnified View ]

The BC can inhibit NP antimicrobial properties. The BC can reduce NP interactions with bacteria, reducing internalization and antibacterial activity. Antifungal activity is related to the NP's ability to associate fungal spores. The BC can inhibit these interactions, decreasing NP antifungal properties. BC, biocorona; NP, nanoparticle

[ Normal View | Magnified View ]

Biomolecules associated with the NP surface can be recognized by cell surface receptors facilitating interactions and internalization. Association with the NP surface can induce conformational alterations in biomolecule structure, allowing for receptor interactions. NP, nanoparticle

[ Normal View | Magnified View ]

References

Alberts,, B., Johnson,, A., & Lewis,, J. (2002). Molecular biology of the cell (4th ed.). New York, NY: Garland Science.
Alex,, S. A., Chandrasekaran,, N., & Mukherjee,, A. (2017). Impact of gold nanorod functionalization on biocorona formation and their biological implication. Journal of Molecular Liquids, 248, 703–712. https://doi.org/10.1016/j.molliq.2017.10.119
Adamson,, S. X. F., Lin,, Z., Chen,, R., Kobos,, L., & Shannahan,, J. (2018). Experimental challenges regarding the in vitro investigation of the nanoparticle‐biocorona in disease states. Toxicology in Vitro, 51, 40–49 https://doi.org/10.1016/j.tiv.2018.05.003.
Amiri,, H., Bordonali,, L., Lascialfari,, A., Wan,, S., Monopoli,, M. P., Lynch,, I., … Mahmoudi,, M. (2013). Protein corona affects the relaxivity and MRI contrast efficiency of magnetic nanoparticles. Nanoscale, 5(18), 8656–8665 https://doi.org/10.1039/c3nr00345k.
Ashley,, C. E., Carnes,, E. C., Phillips,, G. K., Padilla,, D., Durfee,, P. N., Brown,, P. A., … Brinker,, C. J. (2011). The targeted delivery of multicomponent cargos to cancer cells by nanoporous particle‐supported lipid bilayers. Nature Materials, 10(5), 389 https://doi.org/10.1038/NMAT2992.
Bai,, W., Wu,, Z., Mitra,, S., & Brown,, J. M. (2016). Effects of multiwalled carbon nanotube surface modification and purification on bovine serum albumin binding and biological responses. Journal of Nanomaterials, 4. https://doi.org/10.1186/s40945‐017‐0033‐9.
Besnard,, M., Noel,, J. P., Appel,, M., Angelo,, J., & Couvreur,, P. (1999). Stealth® PEGylated polycyanoacrylate nanoparticles for intravenous administration and splenic targeting. Journal of Controlled Release, 60(1), 121–128.
Bisht,, S., & Maitra,, A. (2009). Dextran‐doxorubicin/chitosan nanoparticles for solid tumor therapy. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, 1(4), 415–425. https://doi.org/10.1002/wnan.043
Böhmert,, L., Girod,, M., Hansen,, U., Maul,, R., Knappe,, P., Niemann,, B., … Lampen,, A. (2014). Analytically monitored digestion of silver nanoparticles and their toxicity on human intestinal cells. Nanotoxicology, 8(6), 631–642. https://doi.org/10.3109/17435390.2013.815284
Bravo,, J., & Schnitzer,, J. E. (1993). High affinity binding, endocytosis, and degradation of conformationally modified albumins. Potential role of gp30 and gp18 as novel scavenger receptors. Journal of Biological Chemistry, 268(10), 7562–7570.
Chandran,, P., Riviere,, J. E., & Monteiro‐Riviere,, N. A. (2017). Surface chemistry of gold nanoparticles determines the biocorona composition impacting cellular uptake, toxicity and gene expression profiles in human endothelial cells. Nanotoxicology, 11(4), 507–519. https://doi.org/10.1080/17435390.2017.1314036
Cheng,, X., Tian,, X., Wu,, A., Li,, J., Tian,, J., Chong,, Y., … Ge,, C. (2015). Protein corona influences cellular uptake of gold nanoparticles by phagocytic and nonphagocytic cells in a size‐dependent manner. ACS Applied Materials %26 Interfaces, 7(37), 20568–20575. https://doi.org/10.1021/acsami.5b04290
Chakraborty,, D., Chauhan,, P., Ann,, S., Chaudhary,, S., Ethiraj,, K. R., Chandrasekaran,, N., & Mukherjee,, A. (2018). Comprehensive study on biocorona formation on functionalized selenium nanoparticle and its biological implications. Journal of Molecular Liquids, 268, 335–342. https://doi.org/10.1016/j.molliq.2018.07.070
Connor,, E. E., Mwamuka,, J., Gole,, A., Murphy,, C. J., & Wyatt,, M. D. (2005). Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small, 1(3), 325–327 https://doi.org/10.1002/smll.200400093.
Corbo,, C., & Toledano,, N. E. (2016). The impact of nanoparticle protein corona on cytotoxicity, immunotoxicity and target drug delivery. Nanomedicine, 11(1), 81–100.
Clement,, J. L., & Jarrett,, P. S. (1994). Antibacterial silver. Metal Based Drugs, 1(13), 467–482.
Daima,, H. K., Selvakannan,, P. R., Kandjani,, A. E., Shukla,, R., Bhargava,, S. K., & Bansal,, V. (2014). Synergistic influence of polyoxometalate surface corona towards enhancing the antibacterial performance of tyrosine‐capped Ag nanoparticles. Nanoscale, 6(2), 758–765. https://doi.org/10.1039/c3nr03806h
Daima,, H. K., Selvakannan,, P. R., Shukla,, R., Bhargava,, S. K., & Bansal,, V. (2013). Fine‐tuning the antimicrobial profile of biocompatible gold nanoparticles by sequential surface functionalization using polyoxometalates and lysine. PLoS ONE, 8(10), 1–14. https://doi.org/10.1371/journal.pone.0079676
Daima,, H. K., Vinay Kumar,, P., Rashmi,, S., Pandey,, S. R., Pn,, N., Mlowe,, S., & Revaprasadu,, N. (2016). Formulation, characterization and applications of titanium dioxide, polyoxometalates and silver nanocomposites. Advanced Manufacturing, Electronics and Microsystems: TechConnect Briefs, 1, 37–40.
di Silvio,, D., Rigby,, N., Bajka,, B., MacKie,, A., & Baldelli Bombelli,, F. (2016). Effect of protein corona magnetite nanoparticles derived from bread in vitro digestion on Caco‐2 cells morphology and uptake. International Journal of Biochemistry and Cell Biology, 75, 212–222. https://doi.org/10.1016/j.biocel.2015.10.019
Ding,, F., Radic,, S., Chen,, R., Chen,, P., Geitner,, N. K., Brown,, J. M., & Ke,, P. C. (2013). Direct observation of a single nanoparticle‐ubiquitin corona formation. Nanoscale, 5(19), 9162–9169. https://doi.org/10.1039/c3nr02147e
Docter,, D., Westmeier,, D., Markiewicz,, M., Stolte,, S., Knauer,, S. K., & Stauber,, R. H. (2015). The nanoparticle biomolecule corona: lessons learned—Challenge accepted? Chemical Society Reviews, 44, 6094–6121. https://doi.org/10.1039/c5cs00217f
Ehrenberg,, M. S., Friedman,, A. E., Finkelstein,, J. N., & Mcgrath,, J. L. (2009). The influence of protein adsorption on nanoparticle association with cultured endothelial cells. Biomaterials, 30(4), 603–610. https://doi.org/10.1016/j.biomaterials.2008.09.050
Ge,, C., Du,, J., Zhao,, L., Wang,, L., Liu,, Y., Li,, D., … Zhou,, R. (2011). Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proceedings of the National Academy of Sciences of the United States of America, 108(41), 16968–16973. https://doi.org/10.1073/pnas.1105270108
Gnanadhas,, D. P., Thomas,, M. B., Thomas,, R., Raichur,, A. M., & Chakravortty,, D. (2013). Interaction of silver nanoparticles with serum proteins affects their antimicrobial activity in vivo. Antimicrobial Agents and Chemotherapy, 57(10), 4945–4955. https://doi.org/10.1128/AAC.00152-13
Gordon,, T., Castelli,, W. P., Hjortland,, M. C., Kannel,, W. B., & Dawber,, T. R. (1977). Diabetes, blood lipids, and the role of obesity in coronary heart disease risk for women. The Framingham study. Annals of Internal Medicine, 87(4), 393–397. https://doi.org/10.7326/0003-4819-87-4-393
Haeri,, M., & Knox,, B. E. (2012). Endoplasmic reticulum stress and unfolded protein response pathways: Potential for treating age‐related retinal degeneration. Journal of Ophthalmic %26 Vision Research, 7(1), 45–59.
Hellstrand,, E., Lynch,, I., Andersson,, A., Drakenberg,, T., Dahlbäck,, B., Dawson,, K. A., … Cedervall,, T. (2009). Complete high‐density lipoproteins in nanoparticle corona. FEBS Journal, 276(12), 3372–3381. https://doi.org/10.1111/j.1742-4658.2009.07062
Hu,, W., Peng,, C., Lv,, M., Li,, X., Zhang,, Y., Chen,, N., … Huang,, Q. (2011). Protein corona‐mediated mitigation of cytotoxicity of graphene oxide. ACS Nano, 5(5), 3693–3700. https://doi.org/10.1021/nn200021j
Jenkins,, D. J., Wolever,, T. M., Venketeshwer Rao,, A., Hegele,, R. A., Mitchell,, S. J., Ransom,, T. P., … Wursch,, P. (1993). Effect on blood lipid of very high intakes of fiber in diets low in saturated fat and cholesterol. The New England Journal of Medicine, 329(1), 21–26.
Kanhed,, P., Birla,, S., Gaikwad,, S., Gade,, A., Seabra,, A. B., Rubilar,, O., … Rai,, M. (2014). In vitro antifungal efficacy of copper nanoparticles against selected crop pathogenic fungi. Materials Letters, 115, 13–17. https://doi.org/10.1016/j.matlet.2013.10.011
Kelly,, P. M., Åberg,, C., Polo,, E., Connell,, A. O., Cookman,, J., Fallon,, J., … Dawson,, K. A. (2015). Mapping protein binding sites on the biomolecular corona of nanoparticles. Nature Nanotechnology, 10(5), 472–479. https://doi.org/10.1038/nnano.2015.47
Kobos,, L. M., Adamson,, S. X. F., Evans,, S., Gavin,, T. P., & Shannahan,, J. H. (2018). Altered formation of the iron oxide nanoparticle‐biocorona due to individual variability and exercise. Environmental Toxicology and Pharmacology, 62, 215–226. https://doi.org/10.1016/j.etap.2018.07.014
Kittler,, S., Greulich,, C., Diendorf,, J., Kollwe,, M., & Epple,, M. (2010). Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chemistry of Materials, 22(16), 4548–4554. https://doi.org/10.1021/cm100023p
Kuek‐Jun,, K., Sung,, W. S., Moon,, S.‐K., Choi,, J.‐S., Kim,, J. G., & Lee,, D. G. (2014). Antifungal effect of silver nanoparticles on dermatophytes. Journal of Microbiology and Biotechnology, 18(8), 1482–1484.
Landry,, M. P., Vukovic,, L., Kruss,, S., Bisker,, G., Landry,, A. M., Islam,, S., … Strano,, M. S. (2015). Comparative dynamics and sequence dependence of DNA and RNA binding to single walled carbon nanotubes. The Journal of Physical Chemistry C, 119, 10048–10058. https://doi.org/10.1021/jp511448e
Lansdown,, A. (2006). Silver in health care: Antimicrobial effects and safety in use. Biofunctional Textiles and the Skin, 33, 17–34.
Lee,, B., & Nguyen,, V. H. (2017). Protein corona: A new approach for nanomedicine design. International Journal of Nanomedicine, 12, 3137–3151.
Lee,, W., Loo,, C., Traini,, D., & Young,, P. M. (2015). Inhalation of nanoparticle‐based drug for lung cancer treatment: Advantages and challenges. Asian Journal of Pharmaceutical Sciences, 10(6), 481–489. https://doi.org/10.1016/j.ajps.2015.08.009
Lesniak,, A., Fenaroli,, F., Monopoli,, M. P., Åberg,, C., Dawson,, K. A., & Salvati,, A. (2012). Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano, 6(7), 5845–5857. https://doi.org/10.1021/nn300223w
Lesniak,, A., Salvati,, A., Santos‐Martinez,, M. J., Radomski,, M. W., Dawson,, K. A., & Aberg,, C. (2013). Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. Journal of the American Chemical Society, 135(4), 1438–1444. https://doi.org/10.1021/ja309812z
Li,, R., Chen,, R., Chen,, P., Wen,, Y., Ke,, P. C., & Cho,, S. S. (2013). Computational and experimental characterizations of silver nanoparticle—Apolipoprotein biocorona. The Journal of Physical Chemistry B, 117, 13451–13456. https://doi.org/10.1021/jp4061158
Li,, R., He,, Y., Zhang,, S., Qin,, J., & Wang,, J. (2018). Cell membrane‐based nanoparticles: A new biomimetic platform for tumor diagnosis and treatment. Acta Pharmaceutica Sinica B, 8(1), 14–22. https://doi.org/10.1016/j.apsb.2017.11.009
Li,, W., Xie,, X., & Shi,, Q. (2010). Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Applied Microbial and Cell Physiology, 85, 1115–1122. https://doi.org/10.1007/s00253-009-2159-5
Lichtenstein,, D., Ebmeyer,, J., Knappe,, P., Juling,, S., Bohmert,, L., Selve,, S., … Lampen,, A. (2015). Impact of food components during in vitro digestion of silver nanoparticles on cellular uptake and cytotoxicity in intestinal cells. Biological Chemistry, 396(11), 1255–1264.
Lin,, S., Mortimer,, M., Chen,, R., Kakinen,, A., Riviere,, J. E., Thomas,, P., … States,, U. (2018). NanoEHS beyond toxicity—Focusing on biocorona. Environmental Science: Nano, 7(4), 1433–1454. https://doi.org/10.1039/C6EN00579A.NanoEHS
Liu,, R., Jiang,, W., Walkey,, C. D., Chan,, W. C. W., & Cohen,, Y. (2015). Prediction of nanoparticles‐cell association based on corona proteins and physicochemical properties. Nanoscale, 7(21), 9664–9675. https://doi.org/10.1039/c5nr01537e
Lu,, N., Sui,, Y., Tian,, R., & Peng,, Y. Y. (2018). Adsorption of plasma proteins on single‐walled carbon nanotubes reduced cytotoxicity and modulated neutrophil activation. Chemical Research in Toxicology, 31(10), 1061–1068. https://doi.org/10.1021/acs.chemrestox.8b00141
Lundqvist,, M., Stigler,, J., Elia,, G., Lynch,, I., Cedervall,, T., & Dawson,, K. A. (2008). Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proceedings of the National Academy of Sciences of the United States of America, 105(38), 14265–14270.
Lynch, I., & Dawson, K. A. (2008). Protein‐nanoparticle interactions. Nanotoday, 3(1), 40–47.
Mahmoudi,, M., Sheibani,, S., Milani,, A. S., Gauberti,, M., Dinarvand,, R., & Vali,, H. (2015). Crucial role of the protein corona for the specific targeting of nanoparticles. Nanomedicine, 10(2), 215–226.
Martinez‐Castanon,, G. A., Nino‐Martinez,, N., Martinez‐Gutierrez,, F., Martinez‐Mendoza,, J. R., & Ruiz,, F. (2008). Synthesis and antibacterial activity of silver nanoparticles with different sizes. Journal of Nanoparticle Research, 10, 1343–1348. https://doi.org/10.1007/s11051-008-9428-6
Miller,, M. R., Raftis,, J. B., Langrish,, J. P., McLean,, S. G., Samutrtai,, P., Connell,, S. P., … Mills,, N. L. (2017). Inhaled nanoparticles accumulate at sites of vascular disease. ACS Nano, 11(5), 4542–4552. https://doi.org/10.1021/acsnano.6b08551
Mills,, C. (2012). M1 and M2 macrophages: Oracles of health and disease. Critical Reviews in Immunology, 32(6), 463–488. https://doi.org/10.1615/CritRevImmunol.v32.i6.10
Miragoli,, M., Ceriotti,, P., Iafisco,, M., Vacchiano,, M., Salvarani,, N., Alogna,, A., … Catalucci,, D. (2018). Inhalation of peptide‐loaded nanoparticles improves heart failure. Science Translational Medicine, 10(424), 1–12.
Mirshafiee,, V., Kim,, R., Park,, S., Mahmoudi,, M., & Kraft,, M. L. (2016). Impact of protein pre‐coating on the protein corona composition and nanoparticle cellular uptake. Biomaterials, 75, 295–304. https://doi.org/10.1016/j.biomaterials.2015.10.019
Monopoli,, M. P., Åberg,, C., Salvati,, A., & Dawson,, K. A. (2012). Biomolecular coronas provide the biological identity of nanosized materials. Nature Nanotechnology, 7(12), 779–786. https://doi.org/10.1038/nnano.2012.207
Monteiro,, D. R., Gorup,, L. F., Silva,, S., Negri,, M., Camargo,, E. R. De, Oliveira,, R., … Camargo,, E. R. De. (2011). Silver colloidal nanoparticles: Antifungal effect against adhered cells and biofilms of Candida albicans and Candida glabrata. Biofouling, 27(7), 711–719. https://doi.org/10.1080/08927014.2011.599101
Moore,, K. J., & Freeman,, M. W. (2006). Scavenger receptors in atherosclerosis: Beyond lipid uptake. Arteriosclerosis, Thrombosis, and Vascular Biology, 26(8), 1702–1711. https://doi.org/10.1161/01.ATV.0000229218.97976.43
Morones,, J. R., Elechiguerra,, J. L., Camacho,, A., Holt,, K., Kouri,, J. B., Ram,, J. T., & Yacaman,, M. J. (2005). The bactericidal effect of silver nanoparticles. Nanotechnology, 16, 2346–2353. https://doi.org/10.1088/0957-4484/16/10/059
Müller,, J., Prozeller,, D., Ghazaryan,, A., Kokkinopoulou,, M., Mailänder,, V., Morsbach,, S., & Landfester,, K. (2018). Beyond the protein corona—Lipids matter for biological response of nanocarriers. Acta Biomaterialia, 71, 420–431. https://doi.org/10.1016/j.actbio.2018.02.036
Murphy,, W. G. (2014). The sex difference in haemoglobin levels in adults—Mechanisms, causes, and consequences. Blood Reviews, 28(2), 41–47. https://doi.org/10.1016/j.blre.2013.12.003
Neagu,, M., Piperigkou,, Z., Karamanou,, K., & Engin,, A. B. (2017). Protein bio‐corona: Critical issue in immune nanotoxicology. Archives of Toxicology, 91(3), 1031–1048. https://doi.org/10.1007/s00204-016-1797-5
Okabe,, Y., & Medzhitov,, R. (2016). Tissue biology perspective on macrophages. Nature Immunology, 17(1), 9–17. https://doi.org/10.1038/ni.3320
Orco,, D. D., Lundqvist,, M., Oslakovic,, C., Cedervall,, T., & Linse,, S. (2010). Modeling the time evolution of the nanoparticle‐protein corona in a body fluid. PLoS ONE, 5(6), 1–8. https://doi.org/10.1371/journal.pone.0010949
Panacek,, A., Kvitek,, L., Prucek,, R., Kolar,, M., Vecerova,, R., Pizurova,, N., … Zboril,, R. (2006). Silver colloid nanoparticles: Synthesis, characterization, and their antibacterial activity. The Journal of Physical Chemistry B, 110, 16248–16253. https://doi.org/10.1021/jp063826h
Panas,, A., Marquardt,, C., Nalcaci,, O., Bockhorn,, H., Baumann,, W., Paur,, H. R., … Weiss,, C. (2013). Screening of different metal oxide nanoparticles reveals selective toxicity and inflammatory potential of silica nanoparticles in lung epithelial cells and macrophages. Nanotoxicology, 7(3), 259–273. https://doi.org/10.3109/17435390.2011.652206
Papi,, M., Caputo,, D., Palmieri,, V., Coppola,, R., Palchetti,, S., Bugli,, F., … Caracciolo,, G. (2017). Clinically approved PEGylated nanoparticles are covered by a protein corona that boosts the uptake by cancer cells. Nanoscale, 9(29), 10327–10334. https://doi.org/10.1039/c7nr03042h
Parodi,, A., Quattrocchi,, N., van de Ven,, A. L., Chiappini,, C., Evangelopoulos,, M., Martinez,, J. O., … Tasciotti,, E. (2013). Biomimetic functionalization with leukocyte membranes imparts cell like functions to synthetic particles. Nature Nanotechnology, 8(1), 61–68. https://doi.org/10.1038/nnano.2012.212.Biomimetic
Peng,, Q., Zhang,, S., Yang,, Q., Zhang,, T., Wei,, X. Q., Jiang,, L., … Lin,, Y. F. (2013). Preformed albumin corona, a protective coating for nanoparticles based drug delivery system. Biomaterials, 34(33), 8521–8530. https://doi.org/10.1016/j.biomaterials.2013.07.102
Persaud,, I., Shannahan,, J. H., Raghavendra,, A. J., Alsaleh,, N. B., Podila,, R., & Brown,, J. M. (2019). Biocorona formation contributes to silver nanoparticle induced endoplasmic reticulum stress. Ecotoxicology and Environmental Safety, 170, 77–86. https://doi.org/10.1016/J.ECOENV.2018.11.107
Podila,, R., Vedantam,, P., Ke,, P. C., Brown,, J. M., & Rao,, A. M. (2012). Evidence for charge‐transfer‐induced conformational changes in carbon nanostructure‐protein corona. Journal of Physical Chemistry C, 116(41), 22098–22103. https://doi.org/10.1021/jp3085028
Prapainop,, K., Witter,, D. P., & Wentworth,, P. (2012). A chemical approach for cell‐specific targeting of nanomaterials: Small‐molecule‐initiated misfolding of nanoparticle corona proteins. Journal of the American Chemical Society, 134(9), 4100–4103. https://doi.org/10.1021/ja300537u
Qi,, L., Xu,, Z., Jiang,, X., Hu,, C., & Zou,, X. (2004). Preparation and antibacterial activity of chitosan nanoparticles. Carbohydrate Research, 339, 2693–2700. https://doi.org/10.1016/j.carres.2004.09.007
Raesch,, S. S., Tenzer,, S., Storck,, W., Rurainski,, A., Selzer,, D., Ruge,, C. A., … Lehr,, C. M. (2015). Proteomic and lipidomic analysis of nanoparticle corona upon contact with lung surfactant reveals differences in protein, but not lipid composition. ACS Nano, 9(12), 11872–11885. https://doi.org/10.1021/acsnano.5b04215
Raghavendra,, A. J., Fritz,, K., Fu,, S., Brown,, J. M., & Shannahan,, J. H. (2017). Variations in biocorona formation related to defects in the structure of single walled carbon nanotubes and the hyperlipidemic disease state. Scientific Reports, 7(1), 1–11. https://doi.org/10.1038/s41598-017-08896-w
Rao,, R. V., & Bredesen,, D. E. (2014). Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Current Opinion in Cell Biology, 16(6), 653–662. https://doi.org/10.1016/j.ceb.2004.09.012
Rodriguez,, P. L., Harada,, T., Christian,, D. A., Pantano,, D. A., Richard,, K., & Discher,, D. E. (2014). Minimal “self” peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science, 339, 971–975. https://doi.org/10.1126/science.1229568
Runa,, S., Hill,, A., Cochran,, V. L., Payne,, C. K., Runa,, S., Hill,, A., … Payne,, C. K. (2014). PEGylated nanoparticles: Protein corona and secondary structure. Physical Chemistry of Interfaces and Nanomaterials, XIII, 9165. https://doi.org/10.1117/12.2062767
Sahneh,, F. D., Scoglio,, C., & Riviere,, J. (2013). Dynamics of nanoparticle‐protein corona complex formation: Analytical results from population balance equations. PLoS ONE, 8(5), 1–10. https://doi.org/10.1371/journal.pone.0064690
Sahneh,, F. D., Scoglio,, C. M., Monteiro‐Riviere,, N. A., & Riviere,, J. E. (2015). Predicting the impact of biocorona formation kinetics on interspecies extrapolations of nanoparticle bio distribution modeling. Nanomedicine, 10(1), 25–33.
Salvati,, A., Pitek,, A. S., Monopoli,, M. P., Prapainop,, K., Bombelli,, F. B., Hristov,, D. R., … Dawson,, K. A. (2013). Transferrin‐functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nature Nanotechnology, 8(2), 137–143. https://doi.org/10.1038/nnano.2012.237
Sasidharan,, A., Riviere,, J. E., & Monteiro‐Riviere,, N. A. (2015). Gold and silver nanoparticle interactions with human proteins: Impact and implications in biocorona formation. Journal of Materials Chemistry B, 3(10), 2075–2082. https://doi.org/10.1039/c4tb01926a
Sasidharan,, A., Riviere,, J. E., & Monteiro‐Riviere,, N. A. (2015). Gold and silver nanoparticle interactions with human proteins: Impact and implications in biocorona formation. Journal of Materials Chemistry B, 3(10), 2075–2082. https://doi.org/10.1039/c4tb01926a
Schutz,, C. A., Juillerat‐Jeanneret,, L., Mueller,, H., Lynch,, I., & Riediker,, M. (2013). Therapeutic nanoparticles in clinics and under clinical evaluation. Nanomedicine, 8(3), 449–467.
Shannahan,, J. (2017). The biocorona: A challenge for the biomedical application of nanoparticles. Nanotechnology Reviews, 6(4), 345–353. https://doi.org/10.1515/ntrev-2016-0098
Shannahan,, J. H., Fritz,, K. S., Raghavendra,, A. J., Podila,, R., Persaud,, I., & Brown,, J. M. (2016). Disease‐induced disparities in formation of the nanoparticle‐biocorona and the toxicological consequences. Toxicological Sciences, 152(2), 406–416. https://doi.org/10.1093/toxsci/kfw097
Shannahan,, J. H., Podila,, R., Aldossari,, A. A., Emerson,, H., Powell,, B. A., Ke,, P. C., … Brown,, J. M. (2015). Formation of a protein corona on silver nanoparticles mediates cellular toxicity via scavenger receptors. Toxicological Sciences, 143(1), 136–146. https://doi.org/10.1093/toxsci/kfu217
Shannahan,, J. H., Podila,, R., & Brown,, J. M. (2015). A hyperspectral and toxicological analysis of protein corona impact on silver nanoparticle properties, intracellular modifications, and macrophage activation. International Journal of Nanomedicine, 10, 6509–6520. https://doi.org/10.2147/IJN.S92570
Siemer,, S., Westmeier,, D., Barz,, M., Eckrich,, J., Wünsch,, D., Seckert,, C., … Strieth,, S. (2019). Biomolecule‐corona formation confers resistance of bacteria to nanoparticle‐induced killing: Implications for the design of improved nanoantibiotics. Biomaterials, 192, 551–559. https://doi.org/10.1016/j.biomaterials.2018.11.028
Siemer,, S., Westmeier,, D., Vallet,, C., Becker,, S., Voskuhl,, J., Ding,, G., … Knauer,, S. K. (2018). Resistance to nano‐based antifungals is mediated by biomolecule coronas. ACS Applied Materials %26 Interfaces, 11, 104–114. https://doi.org/10.1021/acsami.8b12175
Sirelkhatim,, A., Mahmud,, S., & Seeni,, A. (2015). Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano‐Micro Letters, 7(3), 219–242. https://doi.org/10.1007/s40820-015-0040-x
Tavanti,, F., Pedone,, A., & Menziani,, M. C. (2019). Multiscale molecular dynamics simulation of multiple protein adsorption on gold nanoparticles. International Journal of Molecular Sciences, 20(14), 3539.
Tenzer,, S., Docter,, D., Rosfa,, S., Wlodarski,, A., Rekik,, A., Knauer,, S. K., … Stauber,, R. H. (2011). Nanoparticle size is a critical physico‐chemical determinant of the human blood plasma corona: A comprehensive quantitative proteomic analysis. ACS Nano, 5(9), 7155–7167. https://doi.org/10.1021/nn201950e
Tenzer,, S., Musyanovych,, A., Fetz,, V., Docter,, D., Hecht,, R., Schlenk,, F., … Schild,, H. (2013). Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nature Nanotechnology, 8(10), 772. https://doi.org/10.1038/nnano.2013.181
Tiede,, K., Hassellöv,, M., Breitbarth,, E., Chaudhry,, Q., & Boxall,, A. B. A. (2009). Considerations for environmental fate and ecotoxicity testing to support environmental risk assessments for engineered nanoparticles. Journal of Chromatography A, 1216, 503–509. https://doi.org/10.1016/j.chroma.2008.09.008
Tran,, Z. V., Weltman,, A., Glass,, G. V., & Mood,, D. P. (1983). The effects of exercise on blood lipids and lipoproteins: A meta‐analysis of studies. Medicine %26 Science in Sports %26 Exercise, 15(5), 393–402. http://europepmc.org/abstract/MED/6645868
Treuel,, L., Brandholt,, S., Maffre,, P., Wiegele,, S., Shang,, L., & Nienhaus,, U. (2014). Impact of protein modification on the protein corona on nanoparticles and nanoparticle‐cell interactions. ACS Nano, 8(1), 503–513. https://doi.org/10.1021/nn405019v
Urbančič,, I., Garvas,, M., Kokot,, B., Majaron,, H., Umek,, P., Cassidy,, H., … Štrancar,, J. (2018). Nanoparticles can wrap epithelial cell membranes and relocate them across the epithelial cell layer. Nano Letters, 18(8), 5294–5305. https://doi.org/10.1021/acs.nanolett.8b02291
Varnamkhasti,, B. S., Hosseinzadeh,, H., Azhdarzadeh,, M., Vafaei,, S. Y., Atyabi,, F., & Dinarvand,, R. (2015). Protein corona hampers targeting potential of MUC1 aptamer functionalized SN‐38 core—Shell nanoparticles. International Journal of Pharmaceutics, 494(1), 430–444. https://doi.org/10.1016/j.ijpharm.2015.08.060
Vidanapathirana,, A. K., Lai,, X., Hilderbrand,, S. C., Pitzer,, J. E., Podila,, R., Sumner,, S. J., … Brown,, J. M. (2012). Multi‐walled carbon nanotube directed gene and protein expression in cultured human aortic endothelial cells is influenced by suspension medium. Toxicology, 302(2–3), 114–122. https://doi.org/10.1016/j.tox.2012.09.008
Vlasova,, M. A., Tarasova,, O. S., Riikonen,, J., Raula,, J., Lobach,, A. S., Borzykh,, A. A., … Järvinen,, K. (2014). Injected nanoparticles: The combination of experimental systems to assess cardiovascular adverse effects. European Journal of Pharmaceutics and Biopharmaceutics, 87(1), 64–72. https://doi.org/10.1016/j.ejpb.2014.02.001
Walkey,, C. D., & Chan,, W. C. W. (2012). Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chemical Society Reviews, 41(7), 2780–2799. https://doi.org/10.1039/c1cs15233e
Walkey,, C. D., Olsen,, J. B., Song,, F., Liu,, R., Guo,, H., Olsen,, D. W. H., … Chan,, W. C. W. (2014). Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS Nano, 8(3), 2439–2455. https://doi.org/10.1021/nn406018q
Wan,, S., Kelly,, P. M., Mahon,, E., Sto,, H., Rudd,, P. M., Caruso,, F., … Monopoli,, M. P. (2015). The “sweet” side of the protein corona: Effects of glycosylation on nanoparticle cell interactions. ACS Nano, 9(2), 2157–2166. https://doi.org/10.1021/nn506060q
Wang,, F., Yu,, L., Monopoli,, M. P., Sandin,, P., Mahon,, E., Salvati,, A., & Dawson,, K. A. (2013). 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: Nanotechnology, Biology, and Medicine, 9(8), 1159–1168. https://doi.org/10.1016/j.nano.2013.04.010
Westmeier,, D., Stauber,, R. H., & Docter,, D. (2016). The concept of bio‐corona in modulating the toxicity of engineered nanomaterials (ENM). Toxicology and Applied Pharmacology, 299, 53–57. https://doi.org/10.1016/j.taap.2015.11.008
Wolfram,, J., Yang,, Y., Shen,, J., Moten,, A., Chen,, C., Shen,, H., … Zhao,, Y. (2015). The nano‐plasma interface: Implications of the protein corona. Colloids and Surfaces B: Biointerfaces, 124, 17–24. https://doi.org/10.1016/j.colsurfb.2014.02.035
Yan,, Y., Gause,, K. T., Kamphuis,, M. M. J., Ang,, C., Brien‐simpson,, N. M. O., Lenzo,, J. C., … Caruso,, F. (2013). Differential roles of the protein corona in the cellular uptake of nanoporous polymer particles by monocyte and macrophage cell lines. ACS Nano, 7(12), 10960–10970. https://doi.org/10.1021/nn404481f
Yang,, W., Peters,, J. I., & Williams,, R. O. (2008). Inhaled nanoparticles—A current review. International Journal of Pharmaceutics, 356(1–2), 239–247. https://doi.org/10.1016/j.ijpharm.2008.02.011
Ye,, D., Bramini,, M., Hristov,, D. R., Wan,, S., Salvati,, A., Åberg,, C., & Dawson,, K. A. (2017). Low uptake of silica nanoparticles in Caco‐2 intestinal epithelial barriers. Beilstein Journal of Nanotechnology, 8(1), 1396–1406. https://doi.org/10.3762/bjnano.8.141
Zhou,, H., Fan,, Z., Li,, P. Y., Deng,, J., Arhontoulis,, D. C., Li,, C. Y., … Cheng,, H. (2018). Dense and dynamic polyethylene glycol shells cloak nanoparticles from uptake by liver endothelial cells for long blood circulation. ACS Nano, 12, 10130–10141. https://doi.org/10.1021/acsnano.8b04947

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

Biocorona‐induced modifications in engineered nanomaterial–cellular interactions impacting biomedical applications

Browse by Topic

Access to this WIREs title is by subscription only.

The latest WIREs articles in your inbox